monash university · errata%...
TRANSCRIPT
Copyright Notices Notice 1 Under the Copyright Act 1968, this thesis must be used only under the normal conditions of scholarly fair dealing. In particular no results or conclusions should be extracted from it, nor should it be copied or closely paraphrased in whole or in part without the written consent of the author. Proper written acknowledgement should be made for any assistance obtained from this thesis. Notice 2 I certify that I have made all reasonable efforts to secure copyright permissions for third-party content included in this thesis and have not knowingly added copyright content to my work without the owner's permission.
ERRATA
Spine embossing: “optimization” for “optimixation”
Page VIII, reference 1, “doi: 10.1016.bip.2143, 2010” for “2010,DOI: 10.1016.bip.2143” Page VIII, Manuscript in preparation, reference 1, “J.Mol.Biol” for “Journal of Molecular Biology” Page VIII, Manuscript in preparation, reference 2, “J.Biol.Chem” for “Journal of Biological Chemistry”
Page 20, Section header “1.4.11” for “1.8.11” Page 43, Figure 2.1: “RRMKWKKK” for “RRWKMKKK” Page 89 line 8, “Vermont” for “Vermot”
Page 94 text line 7 “derivatives” for ““drivatives”
Page 95, Figure 4.3: “RRMKWKKK” for “RRWKMKKK” Page118-‐P139, chapter header, “antagonists” for “antagoists” Page 176, line 3, “processes” for “process”
Page 176, line 7, “resolution” for “resolutions”
Page 179, line 5, ”beam line.” for “beam line as described in.”
Page188, 4th text line, “Table 9.1” for “Table 11.1”
Page192, Heading at top, “Grb7” for “Gb7”
Page192, 10th last text line, “Table 9.11” for “Table 11.11” Page192, 6th last text line, “phosphotyrosine” for “phosphotyrone”
Page196, Table 9.4 Title, “comparison” for “compassion” Page 202, line 1, “especially” for “especial”
Page 202, line 5, “as well as the overall” for “as well as he overall”
Page 212, first line, “series” for “serious”
ADDENDUM
Page 27, Figure 1.7: add the following at the end of the figure caption: “The structure was solved in our laboratory and has been deposited in the pdb database pdb id: 3PQZ.” Page 43, Figure 2.1: add the following at the end of the figure caption: “Peptides G7-‐18NATE-‐alaser-‐Biotin and Penetratin-‐Biotin are the control peptides. G7-‐18NATE-‐alaser-‐Biotin is synthesized to test the impact of the “penetratin” tail on the binding of the G7-‐18NATE peptide on Grb7 SH2 domain in an SPR experiement. The Penetratin-‐Biotin is similarly synthesized to check its possible effect on Grb7 expressing cells in cell based assays. Page 44,Table 2.1: add in table footnote “The amino acids are obtained from Nova-‐Biochem of Merck Chemicals Ltd” Page 49, text line 7: add after synthesizer “(AI, Scientific; 1 Rivett Rd, 2113 North Ryde, NSW)” Page 143, paragraph 2, the statement “there has not been a single peptide that is progressed into a useful therapeutic agent”, should read as “there has not been a single Grb7 inhibitor peptide that is progressed into a useful therapeutic agent”
Page 167: Comment: The whiskers are not from a live cat but as supplied by manufacturers. Page 178, text line 11: Delete “and” Page 187: add at the end of the heading: “Grb7 SH2 domain.”
Page 186, Figure 9.5: add the following after the figure caption “The electron density is contoured at sigma level of 1.0 in the content map. The additional electron density observed (after using the Grb7-‐SH2 domain alone as a search model) was interpreted as malonic acid since 1) it possessed exactly the expected shape of malonic acid , 2) was known to be present in the crystallisation buffer and 3) was positioned to form electrostatic interactions with arginine residues in agremment with it being an dicarboxylic acid”
Page 189, Figure 9.7B: add the additional figure and figure caption.
Figure 9.7 B. – The electron density map of the bicyclic G7-‐18NATE as observed in the binding site of Grb7 SH2 domain. The electron density is shown in blue mesh surrounding the peptide atoms. Protein residues are indicated in lines(Carbon atoms in green; Oxygen atoms in red; Nitrogen atoms in blue). Water molecules are indicated by the red crosses while the phosphate ion is indicated in yellow and red lines adjacent to the phenolic moiety of the peptide’s Tyrosine residue. The map clearly shows the localization of peptide in the Grb7 SH2 domain binding site. P 196, Figure caption 9.13: delete “conservation” and replace it with “identity”
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H3COO
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O
O
HN
O PSCO
O
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HO
O
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O PSC
O
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O
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O PSCO
O
O
O
HN
O PSCO
O
+
- -
-
HN+
HN+ +
N+
O
O
H2N
O PS-CO2
Rink Amide Resin(deprotected)
piperidine
Rink Amide Resin
Fm-piperidine Adduct
PS: Polymeric Support
*
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O
O
OH
OH
O
O
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O PS
O
O
N
O
O
++
Ninhydrin Rink Amide Resin Deep Purple colored complex
Other RXNproducts
*
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!
! 90!
N N+H
O
O NH
CO-
O
S
N
NN
OC+N
N
O
O NH
CO
O
S
NN
N
C+
N
N
-O
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O
O NH
COH
O
SO
O NH
CO-
O
S
Fmoc-Cys(trt)-OH
DIPEA
PF6-
HBTUActivated Fmoc-Cys(trt) !
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O
H
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OHO
HN
O
OCH3
N
DIPEA
Fmoc-Lys(MMT)-OH
O
H
NH
OO
HN
O
OCH3
-
N
H
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Fmoc-Lys(MMT)-O-
NN
N OC N
N
PF6
HBTU
OH
HN O
O
HN
O
O CH3
C
N
N
NN
NO
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O
O
H2N
O PS
Rink Amide Resin
O
H
NH
OO
O
O
HN
O
PS
Fmoc-Lys(MMT)-Rink Amide Resin
HN
O
CH3
OC N
N
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TMU: N,N,N',N'-TetramethylureaDIPEA:N,N-diisopropyl-N-ethylamineHBTU:O-benzotriazole-1-yl-N,N,N',N'- tetramethyluroniumhexafluoro phophate !
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OH
NHO
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HS
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H
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O-
NHO
HHN
HS
O
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NHO
HHN
HS
ON
N
NN
OC+N
N
PF6-
HATU
O
NHO
H
HN
H S
O N
NN
N
C+N
N
Activated Biotin
O
Biotin
HNNH
O
NH2
PO
O
O
NH
O
H
HNH
S
O
C+N N
NH
HNO
NH
O
O
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H
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Biotin Fmoc-Lys
Rink Amide resin
Biotin-Lys-Rink amid resinFmoc-Lys-rink amide resin*
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H2N
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O
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H
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O
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HN
O
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NH
O
NH
ONH
O
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CH3
NH
O N
CO
NH
HNO
S
O
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ClCl
2-chloroacetic anhydride
HN
O
N
NH HN
O
O
O
NH
H
O
NH
O
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NH O
O
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HN
O
NH
O
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CH3
NH
O
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CO
NH
HN
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O
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H
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O
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HN
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O
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O
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NH
O
N
CO NH
NH
O
SO
O
O
O
NH
O
HNNH
O
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HN
H
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NH
O
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NH
OO
O
NH
O
HN
O
HN
O
O
NH
O
NC
O
NH
NHO
S
O
O
O
O
NN
RuCl
Cl
P
20 mol%, 48hr,RT
Hoveyda-Grubbs
2nd generation catalyst
O-allyl Serine
O-allyl Serine
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HN
O
N
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NH
O
O
O
HN
H
O
NH
O
O
HN
O
O
O
NH
O
NH
ONH
O
O
CH3
NH
O N
CO
NH
HNO
S
OCl
O
O
O
NH
O
NH
HN
NH
O
HO O
HN
H
O
NH
O
OH
HN
O
OH
O
NH
O
H2N
OHN
O
OHH3C
NH
O
N CO
HN
NH2O
HSO O
Cl
94.5%TFA/2.5%TIPS/0.5%EDT/2.5%H2O
Cl-CH2-C(O)-WFEGYDNTFPC !
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NH
O
NH
HN
NH
O
HO O
HN
H
O
NH
O
OH
HN
O
OH
O
NH
O
H2N
OHN
O
OHH3C
NH
O
N
O
HN
NH2O
HSO O
Cl
NH4HCO3
pH = 8.0, RT, 1hr
NH
O
NH
HN
NH
O
HO O
HN
H
O
NH
O
OH
HN
O
OH
O
NH
O
H2N
OHN
O
OHH3C
NH
O
N
O
HN
NH2O
O O
S-Cl
NHO
HN
NH
NHO
HO
O
HNH
ONH
O
OH
HN
O
OH
O
NH
O
NH2O
HNO
OH
CH3
HN
ONO
NH
H2NO
O
O
S
H+ + Cl-+NH4HCO3
NH4Cl + H2CHO3
H2O + CO2
side reaction removing HCl
G7-18NATE !
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Uptake of a Cell Permeable G7-18NATE Construct Into Cells and BindingWith the Grb7-SH2 Domain
Nigus D. Ambaye1, Reece C. C. Lim1, Daniel J. Clayton2, Menachem J. Gunzburg1,John T. Price1, Stephanie C. Pero3, David N. Krag3, Matthew C. J. Wilce1,Marie-Isabel Aguilar1, Patrick Perlmutter2, Jacqueline A. WilceAQ2
1
1Department of Biochemistry and Molecular Biology, Monash University, VIC 3800, Australia
2Department of Chemistry, Monash University, VIC 3800, Australia
3Department of Surgery and Vermont Cancer Center, University of Vermont, Burlington, VT
Received 14 December 2009; revised 24 January 2010; accepted 25 January 2010
Published online 00 Month 2010 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/bip.21403
This article was originally published online as an acceptedpreprint. The ‘‘Published Online’’ date corresponds to thepreprint version. You can request a copy of the preprint byemailing the Biopolymers editorial office at [email protected]
INTRODUCTION
Human growth factor receptor bound protein 7
(Grb7) is a 532-amino acid protein that was origi-
nally identified as a binding partner for activated
epidermal growth factor receptor (EGF-R).1 Grb7 is
a member of a family of proteins that includes two
other homologous proteins, Grb10 and Grb14.2,3 These pro-
teins share a conserved multidomain structure with domains
that mediate both protein–protein and protein–lipid interac-
tions. These domains include an N-terminal proline rich do-
main, a Ras-associating-like (RA) domain, a pleckstrin
homology (PH) domain, a C-terminal src-homology 2
ID: jaganm Date: 23/2/10 Time: 19:45 Path: N:/3b2/PEPS/Vol00000/100024/APPFile/C2PEPS100024
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Uptake of a Cell Permeable G7-18NATE Construct Into Cells andBinding With the Grb7-SH2 Domain
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Correspondence to: Dr. Jacqueline A. Wilce, Biochemistry and Molecular Biology,
Monash University, Wellington Road, VIC 3800, Australia;
e-mail: [email protected]
ABSTRACT:
Grb7 is an adapter protein found to be overexpressed in
several breast and other cancer cell types along with
ErbB2. Grb7 is normally an interaction partner with
focal adhesion kinase and in cancer cells also aberrantly
interacts with ErbB2. It is thus implicated in the
migratory and proliferative potential of cancer cells.
Previous studies have shown that the phage display-
derived cyclic nonphosphorylated inhibitor peptide, G7-
18NATE, when linked to Penetratin!, is able to interfere
with the interaction of Grb7 with its upstream binding
partners and to impact on both cell migration and
proliferation. Here we report the synthesis of a
biotinylated G7-18NATE covalently attached to just the
last seven residues of Penetratin! (G7-18NATE-P-
Biotin). We demonstrate that this construct is taken up
efficiently into MDA-MB-468 breast cancer cells and
colocalizes with Grb7 in the cytoplasm. We also used
isothermal titration calorimetry to determine the binding
affinity of G7-18NATE-P-Biotin to the Grb7-SH2
domain, and showed that it binds with micromolar
affinity (Kd ! 14.4 lM), similar to the affinity of G7-
18NATE (Kd ! 35.4 lM). Together this shows that this
shorter G7-18NATE-P-Biotin construct is suitable for
further studies of the antiproliferative and antimigratory
potential of this inhibitor. # 2010 Wiley Periodicals, Inc.
Biopolymers (Pept Sci) 00: 000-000, 2010.
Keywords: Grb7 adapter protein; SH2 domain; non-phospho-rylated cyclic peptide; peptide inhibitor; penetratin; cell uptake;co-localisation; breast cancer cells
Contract grant sponsors: Australian Research Council Project Grant (to J.A.W. and
D.N.K.) and Monash University Graduate Scholarship (to N.D.A.)
VVC 2010 Wiley Periodicals, Inc.
PeptideScience Volume 00 / Number 0 1
(SH2) domain, and a region between the PH and SH2
domains termed the BPS domain.3 Notably, these proteins
share a region with sequence homology to the Mig-10 C. ele-
gans gene required for migration of neuronal cells in embry-
onic development, suggesting a role for the Grb7 family in
cell migration.4AQ3Grb7-family proteins function as adaptors, coupling acti-
vated tyrosine kinase receptors to downstream signaling
pathways. Grb7 upstream binding partners include the mem-
bers of the ErbB (also known as HER) receptor family5,6 and
focal adhesion kinase (FAK)7 whose activities play a critical
role in the regulation of cell proliferation and migration,8,9
and interactions with other tyrosine kinases have also been
reported.10,11 Although a large number of binding partners
functioning upstream of Grb7 have been identified, the pre-
cise downstream events leading to cell proliferation and
migration are not yet elucidated.
Studies have shown that Grb7 is involved in cancer cell
progression. Although Grb7 normally binds to the cytoplas-
mic domain of the ErbB3 receptor, in cancer cells it has
been found in tight association with the ErbB2 receptor
that plays a major role in cancer cell proliferation.6 Grb7 is
tightly coamplified with ErbB2 in breast cancer cell lines,
and there is also a strong correlation between ErbB2 and
Grb7 overexpression in oesophageal and gastric carci-
noma.12,13 A role for Grb7 in the transition from low-grade
to high-grade tumor has also been reported. Coamplifica-
tion and coexpression of Grb7 and ErbB2 is found in high-
grade invasive Barrett’s carcinoma, but not in less aggressive
tumors.14 Similarly, Grb7 expression is increased markedly
in high-grade but not in low-grade chronic lymphocytic
leukemia.15 There is also compelling evidence that impli-
cates Grb7 in cancer cell migration. Grb7 is found in focal
adhesions in association with FAK16 and plays a key role in
integrin-mediated signal transduction in cell migration.17
Overexpression of Grb7 has been shown to enhance cell
migration, whereas inhibition of the Grb7 resulted in the
inhibition of cell migration.7 Taken together, these studies
have made the Grb7 an attractive target in the development
of anticancer therapeutics.
The interaction between Grb7 and its partners is mediated
by the SH2 domain (residues 416-532) of Grb7.6 This do-
main therefore constitutes a good target for the inhibition of
Grb7 with its upstream binding partners. To this end, a non-
phosphorylated peptide inhibitor was developed using a
phage-displayed peptide library method.18 This peptide con-
tains 10 amino acids flanked by two terminal cysteines (seq:
CWFEGYDNTFPC) to create a cyclic peptide through disul-
fide linkage. The peptide was then synthesized as a redox-sta-
ble thioether bridged analog, referred to as G7-18NATE. The
cyclic nature of the peptide was found to be necessary for
binding to Grb7-SH2 domain, as also seen for Grb2-SH2 do-
main interaction with its YXN motif peptide targets. The G7-
18NATE peptide, however, binds with high specificity (does
not bind to the Grb2 or the closely related Grb14) and has
been shown to specifically inhibit the association of Grb7
with ErbB2.
Cellular studies with the G7-18NATE peptide have shown
that it is able to interfere with both cell proliferation and cell
migration.19,20 Since peptides of the size and composition of
G7-18NATE are generally impermeable to the cell mem-
brane, cell permeable forms of the peptide were constructed
by the covalent attachment of carrier peptides Penetratin"C
or Tat. Cell permeable G7-18NATE was shown to inhibit pro-
liferation in several breast cancer cell lines that overexpress
Grb7 and not nonmalignant breast cells.19 It was shown that
cotreatment of cell permeable forms of G7-18NATE with Dox-
orubicin or Trastuzumab (Herceptin) results in enhanced
antiproliferation of breast cancer cells. Furthermore, in a
recent breakthrough study, a cell permeable form of the
G7-18NATE peptide was shown to successfully block the
Grb7 interaction with FAK and inhibit cell migration of a
pancreatic cancer cell line.20 Such a peptide, which binds
Grb7 without the need for phosphotyrosine, represents a
particularly attractive starting point for targeting Grb7
because phosphate groups are intrinsically unstable chemical
moieties and reduce cell wall permeability.
Cellular studies of the effects of G7-18NATE on cell prolif-
eration showed that Penetratin"C effected the uptake of G7-
18NATE into cells more efficiently than Tat.19 Penetratin"C is
a 17-amino acid residue sequence derived from the third do-
main of the antennapedia homeodomain.21 Fischer et al.
have previously shown that the last seven residues of Pene-
tratin"C are sufficient to confer cell permeability to a cargo,
though uptake is reduced compared with full length Pene-
tratin"C .22 In this study, we have sought to determine
whether this shorter region of Penetratin"C would be suffi-
cient to effect cellular uptake of G7-18NATE, and also
whether the presence of this cell permeabilization sequence
impacts on the binding of the peptide to its target. We thus
report the synthetic strategy utilized for the preparation of
G7-18NATE synthesized with a short Penetratin"C sequence
and a biotin label for cellular uptake studies (G7-18NATE-P-
Biotin). We show that this cell permeabilization sequence
does not interfere with the interaction of G7-18NATE with
the Grb7-SH2 domain target and that the construct is effi-
ciently taken up into cells. Together this shows that this
shorter G7-18NATE-P-Biotin construct is suitable for further
studies of the antiproliferative and antimigratory potential of
this inhibitor.
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2 Ambaye et al.
Biopolymers (Peptide Science)
EXPERIMENTAL PROCEDURES
Preparation of G7-18NATE and G7-18NATE-P-BiotinPeptidesG7-18NATE (cyclo-(CH2CO-WFEGYDNTFPC)-amide) and
G7-18NATE-P-Biotin (cyclo-(CH2CO-WFEGYDNTFPCRR
MKWKKK(Biotin))-amide) were synthesized as peptide am-
ide using the Fmoc based solid phase peptide synthesis strat-
egy on a Rink amide resin (1.0 mmol/g).23 The resin swelling
was conducted as pre-treatment for 30 minutes in dimethyl
formamide (DMF) in three times the resin volume followed
by treatment with 30% v/v piperidine in DMF for 30 minutes
at room temperature (RT) to effect removal of the 9-floure-
nylmethoxycarbonyl (Fmoc) group from the Rink amide
resin. The successful removal of Fmoc was checked with a
ninhydrin based Kaiser’s test.24 All amino acids were coupled
as their Fmoc-derivatives. The first residue was preactivated
using O-benzotriazol-1-yl-N,N,N0,N0-tetramethyluronium
hexafluorophosphate (HBTU) and di-isopropyl ethylamine
(DIPEA) and then loaded manually to the deprotected resin
and coupled at RT for 30 minutes. A CEM Liberty automated
synthesizer (Ai Scientific, Australia) was then used to incor-
porate the remaining residues. The system uses microwave
energy to drive coupling and deprotection reactions to com-
pletion. The coupling agent was HBTU containing hydroxy-
benztriazole (HoBt) and the activator base employed was di-
isopropylethylamine (DIEPA) in N-methyl pyrollidone
(NMP). Double couplings were carried out for Met, Lys, Arg,
Phe, Trp, Thr, and Asn residues.
In the case of the G7-18NATE-P-Biotin peptide, the
C-terminal Lys side chain was protected with the monome-
thoxytrityl (Mmt), which could be selectively removed with
a cocktail of 10% acetic acid, 20% trifluoro-ethanol, and
70% dichloromethane. Biotin was then coupled at sixfold
molar excess using 2-(7-aza-1H-benzotriazole-1-yl)-1,1,3,
3-tetramethyluronium hexafluorophosphate (HATU) as a
coupling agent in anhydrous dimethylsulphoxide (DMSO)
while DIEPA was used as activating agent. The biotinylation
reaction was carried out for 60 minutes at room tempera-
ture. The success of the biotin coupling was checked using
Kaiser’s test.24
Following incorporation of the residues using the micro-
wave synthesizer, chloroacetylation was carried out manually
as at room temperature. Briefly, chloroacetic acid anhydride
was used to cap the N-terminal amino moiety manually at
room temperature and the reaction was effected for about 30
minutes. The peptide was then fully cleaved from the resin
and fully deprotected using a 94.5% trifluoroaceticacid
(TFA)/2.5% triisopropylsilane (TIPS)/2.5%H2O/0.5% etha-
nedithiothreitol (EDT) cleavage cocktail with a 20-fold excess
volume over dry weight of resin-peptide for 3 hours at room
temperature. The TFA was evaporated under a stream of
nitrogen gas and the resin dried at room temperature. This
was followed by precipitation of peptide in cold diethylether.
Finally, the peptide was dissolved and extracted with succes-
sive small volumes of 50%ACN/H2O and lyophilized over-
night. Thioether formation was effected by dissolving the ly-
ophilized peptide at 2 mg/ml in 50 mM NH4HCO3 in
50%ACN/H2O of pH 8.0. The cyclized peptide was freeze-
dried and purified using preparative RP HPLC and finally
homogeneity and identity of the prepared peptide was con-
firmed by analytical reverse phase HPLC and electron-spray
mass spectroscopy as presented below.
Peptide Purification by Reverse Phase HPLCPeptide purification was conducted using HPLC (Agilent,
Australia) on a C18 reverse phase preparative columns (2.2
cm 3 25 cm, Vydac 28TP1022). The mobile phase A con-
tained 0.1%TFA/water while mobile phase B comprised
0.1%TFA 80% acetonitrile in water. All buffers were filtered
using 0.45 lM filter. The lyophilized peptides were dissolved
in 1.5 equivalents of MQ H2O/0.1%TFA/20%ACN and 2M
urea as needed to aid in solubility. A linear gradient was
developed and purification on 20% to 80% acetonitrile/0.1%
TFA over 60 minutes on an equilibrated HPLC column with
a flow rate of 6 ml/min. Detection was performed at 214 and
280 nm and fractions were collected by hand. Experiments
were carried out at a flow rate of 6 ml/min, at ambient tem-
perature. The appropriate fractions were pooled and lyophi-
lized. Fractions collected were confirmed by electrospray
mass spectrometry and analytical reverse phase HPLC.
Structure Confirmation by Mass SpectrometryThe progress and success of capping and folding reaction and
also the final identity of preparative HPLC collected fraction
and the final peptide purity was conformed with electrospray
mass spectrometry (Agilent, Australia) in conjuction with
reverse phase analytical HPLC. Negative ion mode of ion
generation was employed for G7-18NATE and a positive ion
mode was pursued for G7-18NATE-P-Biotin. For the nega-
tive ion mode, an amount of peptide enough to form a 0.5
mg/ml solution was dissolved in 10 mM NH4OOCH3/
50%ACN solution while for a positive ion mode the solvent
used was 0.1%TFA 50% ACN/H2O. (G7-18NATE: [M-H]#
m/z ! 1417.6 (calculated), 1417.1 (observed); G7-18NATE-
P-Biotin: [M+H]+ m/z ! 2787.2 (calculated), 2786.5
(observed)).
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Synthetic Strategy Utilized for the Preparation of G7-18NATE AQ13
Biopolymers (Peptide Science)
Preparation of Grb7-SH2 DomainThe pGex2T plasmid containing the Grb7-SH2 insert
(encoding residues 415–532 of human Grb7) was obtained
from Dr. Roger Daly.25 Grb7-SH2 was expressed as a GST
fusion protein in Escherichia coli strain BL21(DE3).pLysS as
previously described.26 The cells were resuspended in phos-
phate buffer saline (PBS) with 2 mM EDTA and 0.5% Triton-
X 100 and lysed by sonication. GST-Grb7-SH2 was purified
by glutathione affinity chromatography, using a GSTrap FF
column (GE) and eluted with PBS containing 0.5% Triton-
X100, 10 mM glutathione, and 1 mM DTT. The Grb7-SH2
fusion protein was cleaved with thrombin liberating free
Grb7-SH2, which was purified by cation exchange chroma-
tography using a HiTrap SH HP column (GE), after dialysis
into 20 mM HEPES pH 7.4, 20% glycerol, and 1 mM DTT,
and eluted with a gradient from 0 to 0.5M NaCl. Peak frac-
tions were dialyzed into 50 mM MES pH 6.6, 100 mM NaCl
and 1 mM DTT and further purified by size exclusion chro-
matography using a sephadex 75 XK 16/60 column (GE).
Grb7-SH2 domain was concentrated and stored at 48C. Thefinal concentration was determined spectrophotometrically
at A280 using an extinction coefficient of 8480 M#1.27
Isothermal Titration Calorimetry (ITC)ITC binding experiments were performed on a VP-ITC
microcalorimeter (Microcal, Northampton, MA) at
258C.28,29 Grb7-SH2 domain was dialyzed extensively against
50 mM NaOOCCH3 (pH 6.6), 100 mM NaCl, and 1 mM
DTTat 48C overnight. Lyophilized G7-18NATE was dissolved
in appropriate volume of filtered dialysate buffer. The con-
centration of Grb7-SH2 was determined by recording its ab-
sorbance at 280 nm whereas that of the peptides was deter-
mined from their mass obtained with an analytical balance
and dissolution in the required volume. The peptide and
protein solutions were degassed and thermostated at 208Cfor 5 minutes using the ThermoVac of the VP-ITC microca-
lorimeter. The reference power of the experiment was set to
20 lCal/sec and the cell contents were stirred continuously at
307 rpm throughout the titrations. The feedback mode gain
was set to high with fast and autoequilibrations options
applied. The reference cell was filled with Milli-Q water. The
peptides of 0.70 to 1.3 mM concentrations were titrated into
Grb7-SH2 solutions of 50 to 70 lM concentrations in 10 llinjections with a 3-minute delay between each injection. A
binding isotherm was generated by plotting the heat change
evolved per injection against the molar ratio of peptides to
Grb7-SH2 domain receptor. A blank determination in which
the peptides were titrated against the buffer was carried out
to account for heats of dilution and mixing which was then
subtracted from the binding data. The corrected data was
then employed to fit to a single binding site model using a
nonlinear least squares with the Origin (Microcal Software,
Northampton, MA). All of the ITC fitting parameters were
kept floating.
Cell Uptake and Visualization ExperimentsMDA-MB-468 breast cancer cells were seeded on sterilized
glass coverslips (13 mm diameter) in 24-well plate and grown
in DMEM with 10% FBS to 60% to 70% confluence. G7-
18NATE-P-Biotin (1 mg/ml in MilliQ water) was diluted in
culture medium and applied to the cells at a final concentra-
tion of 10 lM. After 30 minutes of incubation with the pep-
tide at 378C, cells were washed with medium (500 ll perwell) twice and continued to incubate for an additional 30
minutes, after which the cells were washed twice (500 ll/well,13 PBS: 140 mM NaCl, 10 mM Na2HPO4, 2.7 mM KCl, 1.8
mM KH2PO4, 1 mM CaCl2, and 0.5 mM MgCl2) and fixed
(4% paraformaldehyde in 13 PBS, 300 ll per well, 20
minutes). Cells were then permeabilized (0.5% Tween-20 in
13 PBS, 500 ll per well, 20 minutes), blocked (3% bovine
serum albumin, BSA, in 13 PBS, 500 ll per well, 30
minutes), and treated with Streptavidin, Alexa Fluor1 594
conjugate (Molecular Probe, 10 lg/ml in 0.1% BSA, 30 llper coverslip) for 1 hour at room temperature in the dark
and then washed twice with 13 PBS. For detection of Grb7,
fixed cells were treated with rabbit polyclonal anti-Grb7 (H-
70) (Santa Cruz sc-13954, 1:1000 in 0.1% BSA, 30 ll per cov-erslip) in humid chamber overnight at 48C and then washed
three times with 13 PBS before treated with goat antirabbit
IgG-FITC (Molecular Probe, 1:50 in 0.1% BSA, 30 ll percoverslip) for 1 hour at room temperature. Cells were washed
three times with 13 PBS. For double immunostaining, both
Streptavidin, Alexa Fluor1 594 conjugate and goat anti-rab-
bit IgG-FITC were treated together on Grb7 immunolabeled
cells. After mounting on glycerol-based mounting medium,
slides were stored with minimal light exposure before view-
ing by confocal microscopy (Olympus FV1000), using a
1003 oil-objective lens.
RESULTS
Synthesis of G7-18NATE and G7-18NATE-Penetratin-BiotinThe sequences of G7-18NATE and G7-18NATE-P-Biotin are
displayed in Figure F11. The prototype peptide G7-18NATE,
which was identified using the phage display technique by
Pero et al.18 is interesting for its selective antagonist potential
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4 Ambaye et al.
Biopolymers (Peptide Science)
for Grb7, having minimal or no activity against the closely
related adaptor proteins such as Grb2, Grb10, and Grb14.
The synthesis of both peptides was effected utilizing a stand-
ard solid phase peptide synthesis based on Fmoc chemistry.
Specifically, amino acids were all preactivated using the
HBTU/DIPEA reagents before coupling. In both cases, the
first residue was coupled manually at room temperature and
chloroacetylation was conducted at the final residue. The
selective deprotection of the C-terminal lysine side chain
facilitated its biotinylation at the start of the G7-18NATE-P-
Biotin synthesis. Thioether formation between the cysteine
side chain and the N-terminus of both peptides was achieved
in aqueous solution subsequent to their cleavage from the
resin. The thiolate anion of the cysteine forms at pH 8 and
acts as a nucleophile to displace the chloride ion from the N-
terminal chloroacetyl group to form the thioether ring. A
yield of about 15.5% for G7-18NATE and about 2.5% for
G7-18NATE-P-Biotin was achieved. The lower yield obtained
for G7-18NATE-P-Biotin likely reflects the number of extra
coupling and deprotection steps and, most importantly, the
poor coupling efficiencies of sequential Lys and Arg residues
in the Penetratin"C -derived sequence despite the use of dou-
ble couplings.
ITC Binding for G7-18NATE and G7-18NATE-P-Biotin Binding to Grb7-SH2In order to check whether the presence of the Penetratin-
derived sequence would interfere, or otherwise, with the G7-
18NATE/Grb7-SH2 domain interaction, their in vitro associ-
ation was analyzed using ITC. The determination of the ther-
modynamic parameters for the formation of ligand-receptor
complexes offers a helpful description of such associations.29
The ITC enthalpic readout gives a direct measure of the
binding contribution from the formation or breakage of
noncovalent bonds in the system while the entropic data
gives quantitative value for the change in order of the system
as a result of confomational and/or solvation changes. The
precise determination of both these terms along with the
number of binding sites (N) and binding constant (Kb) from
the experiment makes ITC an invaluable tool for a clearer
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FIGURE 1 Peptides synthesized for the current study. One lettercode for amino acids are shown in bold.
FIGURE 2 ITC Thermograms obtained from the isothermal titration of (A) G7-18NATE and (B)G7-18NATE-P-Biotin peptides against the Grb7-SH2 domain. The upper panel show raw dataobtained from 10 ll injections of peptides at 258C. The lower panels in both figures display plots ofintegrated total energy exchanged (as kcal/mol of injected peptides) as a function of molar ratio ofthe peptide to the Grb7-SH2 domain.
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Synthetic Strategy Utilized for the Preparation of G7-18NATE AQ15
Biopolymers (Peptide Science)
understanding of important attributes of ligand-receptor
associations. FigureF2 2 displays the thermograms of the G7-
18NATE and its cell penetrable variant, G7-18NATE-P-Bio-
tin, titrated against the SH2 domain of Growth factor recep-
tor bound protein 7 (Grb7). TableT1 I shows the in vitro bind-
ing thermodynamics data analysis.
The ITC experiments show that every titration injection
for both peptides is associated with a release of heat and
hence the binding phenomenon is exothermic. Moreover, the
binding in both cases can be explained as enthalpically
driven, whereas the contribution of entropy to the over all
binding is minimal (G7-18NATE-P-Biotin) or even negative
(G7-18NATE). From these data, the G7-18NATE-P-Biotin
binds with slightly higher affinity (Kd ! 14.4 lM) than G7-
18NATE (Kd ! 35.4 lM). Though the enthalpic component
of binding for G7-18NATE-Penetratin-Biotin is about half
that of G7-18NATE, its entropic contribution is more than
10 times higher resulting in its relatively higher affinity.
Uptake of G7-18NATE-P-Biotin and ColocalizationWith Grb7To demonstrate whether G7-18NATE-P-Biotin is spontane-
ously taken up into cultured cells, subcellular localization of
the peptide was examined in our cell line of interest, human
breast cancer cells MDA-MB-468. The cells were treated with
G7-18NATE-P-Biotin at 10 lM or untreated. After 30-mi-
nute incubation with the peptide, the cells were examined for
their uptake of the biotinylated peptide using a fluorescently-
labeled streptavidin that binds biotin. After 30 minutes, cells
showed incorporation of the G7-18NATE-P-Biotin through-
out the cytoplasm of the cells as well as fainter nuclear local-
ization (FigureF3 3C). Cells with no treatment do not show de-
tectable fluorescence (Figure 3A). This indicates that the pep-
tide had indeed spontaneously traversed the cell membrane
from the culture medium into the cells.
As G7-18NATE is able to bind to the SH2 domain of Grb7
as shown previously, colocalization of the peptide with Grb7
was examined. The cells, treated with G7-18NATE-P-Biotin
or untreated, were double stained for Grb7 and biotin. Grb7
was found to be distributed throughout the cytoplasm and
to be excluded from the nucleus of the cells (Figure 3B).
Thus, Grb7 and G7-18NATE-P-Biotin both appear to be
present throughout the cytoplasm, providing the opportu-
nity for these molecules to interact (Figure 3D).
DISCUSSIONThe G7-18NATE peptide is an important lead for the study of
the effect of Grb7 inhibition in cells and for the potential devel-
opment of inhibitors of Grb7 where it is aberrantly overex-
pressed in cancer. The peptide provides the specificity required
for Grb7 inhibition, an attribute that is unlikely to be mim-
icked by a small molecule antagonist. It suffers, however, as do
most peptides, in its requirement for both aqueous solubility
and sufficient lipid solubility. Aqueous solubility is required
for easy transport across biological fluids, whereas sufficient
lipid solubility is mandatory for molecules to cross themyriads
of membrane layers before they reach the target site. Inability
to strike a balanced aqueous and lipid solubility can be linked
to problems ranging from safety, efficacy, and manufacturabil-
ity to difficulty of discovering a new chemotypes. The mem-
brane permeability issue is particularly demanding for the ex-
ploitation of intracellular targets. The requirement is especially
pronounced for charged and polar molecules such as peptides.
Cell permeablizing cargoes such as Penetratin"C therefore rep-
resent attractive vehicles for the transport of otherwise cell-
impermeable candidates and exploration of the potential of
novel intracellular molecules as drug targets.
The G7-18NATE peptide has previously been transported
into cells by the use of the full Penetratin"C sequence to dem-
onstrate biological activity in cells.19,20 Here, we sought to
determine the utility of a shortened version of Penetration"C
because the last seven residues have been shown to be suffi-
cient for effective uptake of peptides into cells.22 We were
interested to check that the G7-18NATE peptide interaction
with the Grb7-SH2 domain was not detrimentally affected by
the presence of the short Penetratin"C -derived sequence, and
that uptake into the cell for interaction with the Grb7 mole-
cule in vivo was effected. To these ends we prepared G7-
18NATE (as previously reported30) and G7-18NATE with the
seven Penetratin"C -derived residues synthesized as a C-ter-
minal extension and an extra C-terminal biotinylated lysine
to facilitate intracellular detection (G7-18NATE-P-Biotin).
Both peptides were successfully synthesized and cyclized for
the current studies.
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Table 1 Thermodynamic Binding Parameters of the G7-18NATE Peptides
Binding Parameter Kb(M#1) DH (Cal/mol) DS (Cal/mol/8K) DG (Cal/mol) N Kd (lM)
G7-18NATE 2.89E46 0.44E4 #64046 889 #1.05 #6090 1.05 6 0.11 35.4 6 5G7-18NATE-P-Biotin 7.27E46 1.49E4 #3583 6222 10.2 #6627.7 1.10 6 0.04 14.4 6 3
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6 Ambaye et al.
Biopolymers (Peptide Science)
A comparison of the peptide interactions with the Grb7-
SH2 domain was undertaken using ITC. The affinity of G7-
18NATE-P-Biotin (14.4 lM) and that of G7-18NATE (35.4
lM) for the Grb7-SH2 domain were found to be of the same
order of magnitude. The affinity of G7-18NATE is comparable
to previously reported values of 35.7 lM and 13.2 lM30,31
where the differences are likely to reflect differences in the ex-
perimental conditions such as buffer type and composition,
peptide and protein concentrations. Interestingly, the slightly
higher affinity estimated for the G7-18NATE-P-Biotin peptide
is a reflection not of an increased enthalpic contribution to
binding, but rather appears to be due to a larger increase in
entropy of the system. Considering the structures of the pep-
tides, the structure of G7-18NATE-P-Biotin would be
expected to display greater flexibility, and to display a more
enthropically unfavorable binding than the seemingly more
rigid G7-18NATE. However, entropy is a combined effect of
both conformational and solvation/desolvation phenomena.
In the present case, given the highly charged nature of the Pen-
etratin"C -derived tail, it is likely to be highly solvated and thus
produce a compensatory favorable entropy via desolvation
during the binding event. The two peptides exhibit a similar
stoichiometry of 1:1 for their binding to the Grb7-SH2 do-
main. Overall, this study shows that the impact of the Pene-
tratin"C -derived sequence on the binding of G7-18NATE to
Grb7-SH2 domain is minimal and, most importantly, that the
Penetratin"C -derived sequence does not interfere or nega-
tively impact the binding of G7-18NATE to its target.
The G7-18NATE-P-Biotin peptide was found to be readily
taken up by cells in culture, similar to other peptides cova-
ID: jaganm Date: 23/2/10 Time: 19:45 Path: N:/3b2/PEPS/Vol00000/100024/APPFile/C2PEPS100024
FIGURE 3 Localization of G7-18NATE-P-Biotin in MDA-MB-468 breast cancer cells. The cellswere exposed to 10 lM G7-18NATE-P-Biotin for 30 minutes before being fixed and permeabilized.(A) The no peptide control shows no staining by the Streptavidin, Alexa Fluor1 594 conjugate. (B)Grb7 was localized using anti-Grb7 and anti-rabbit-FITC. (C) The biotinylated peptide was local-ized using Streptavidin, Alexa Fluor1 594 conjugate and (D) shows the merged images.
J_ID: Z8J Customer A_ID: 2009-00109.R1 Cadmus Art: PEPS21403 Date: 23-FEBRUARY-10 Stage: I Page: 7
COLOR
Synthetic Strategy Utilized for the Preparation of G7-18NATE AQ17
Biopolymers (Peptide Science)
lently attached to the full-length Penetratin"C construct.32,33
This was as expected from studies of the cellular permeability
of different sequences derived from Penetratin"C ,22 but
has not been previously demonstrated for the G7-18NATE
peptide nor shown, to the best of our knowledge, using con-
focal microscopy for this sequence. Furthermore, the G7-
18NATE was found to be mainly localized in the cytoplasm
that is also where Grb7 was shown to reside in the human
MDA-MB-468 breast cancer cells. Whilst the cell rupture and
fixation processes required for the detection of biotin with
streptavidin and the detection of Grb7 with antibodies may
impact on the fine detail of molecular localization in the cell,
their colocalization in the cytoplasm suggests that this con-
struct is suitable for studies of the effect of G7-18NATE/Grb7
interactions in cells.
Together these studies have demonstrated the suitability
of the Penetratin"C -derived sequence for the delivery of G7-
18NATE to cells for interaction with Grb7. These studies
have confirmed that the interaction of the G7-18NATE with
the Grb7 SH2 domain occurs with micromolar affinity, and
that this is not detrimentally impacted on by the addition
of the Penetratin"C -derived cell penetrating sequence.
Future derivatives of the G7-18NATE peptide, which are
currently sought with improved affinity for Grb7, are also
likely to be assisted in their delivery into cells using this
strategy.
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ID: jaganm Date: 23/2/10 Time: 19:45 Path: N:/3b2/PEPS/Vol00000/100024/APPFile/C2PEPS100024
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8 Ambaye et al.
Biopolymers (Peptide Science)
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Declaration for Thesis Chapter [5-6-71
Deciaration by candidate
In the case of Chapter [5],[6] and [7] the nature and extent of my contribution to the work was
as follows:
Nature of contribution
Co;a;;t.a uitt"ir screening, ThermoFluot u"a rtd
binding experiment, prepared the receptor protein and
contributed towards manuscript preparation
Contribution (%) Signature
90% ., .- .
Signature
,ti:.::.i. r...:-,
The following co-authors contributed to the work. Co-authors who are students at Monash
Universitv must also indicate the extent of their contribution in percentage terms:
Name
Reeie C lit"'
rohn r Fiicel
racquetlne A wil..'
Nature of contribution
conauftea trie ieri uat;d ;;;;t
fvieniChem J Gunzburg I P articipated in protein expre ssion/purifi cation
Mutttr.* ci wiiiei ico"ttiU"i"o to auta i"i"tpt"iitio"
Contributed to data interpretation
Planned and supervised the overall experiments !,i :' *'';E'- r: !--i--.
'- -
and oversaw the reporting of the results , ,!
tl"pa.t-e"i of biochemlitry and Molecular Bioiogy, Monash University, VIC 3800, Australia;
Declaration by co-authors
I hereby certi$'that:
(1) the above declaration correctly reflects the nature and extent of the candidate's
contribution to this work, and the nature of the contribution of each of the co-authors.
(2) they meet the criteria for authorship in that they have participated in the conception,
execution, or interpretation, of at least that part of the publication in their field of expertise;
(3) they take pubiic responsibility for their part of the publication, except for the responsible
author who accepts overall responsibility for the publication;
(4) there are no other authors of the publication according to these criteria;
iSj potential conflicts of interest have been disclosed to (a) granting bodies, (b) the editor or
publisher ofjournals or other publications, and (c) the head of the responsible academic unit;
and(6) the original data are stored at the above location(s) and will be held for at least five years
from the date indicated below:
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Benzopyrazine derivatives: A novel class of growth factor receptor boundprotein 7 antagonists
Nigus D. Ambaye, Menachem J. Gunzburg, Reece C. C. Lim, John T. Price, Matthew C. J. Wilce !,Jacqueline A. Wilce !,!
Department of Biochemistry and Molecular Biology, Monash University, Wellington Road, Victoria 3800, Australia
a r t i c l e i n f o
Article history:Received 30 July 2010Revised 8 October 2010Accepted 12 October 2010Available online xxxx
Keywords:Grb7Adapter proteinSH2 domainBenzopyrazinesCancer cellsSimilarity searchVirtual screeningITCThermofluorMelting point shift assayCellular growth assay
a b s t r a c t
Growth factor receptor bound protein 7 (Grb7) is an adapter protein that functions as a downstreameffector of growth factor mediated signal transduction. Over-expression of Grb7 has been implicated ina variety of cancers such as breast, blood, pancreatic, esophageal, and gastric carcinomas. Inhibition ofGrb7 has been shown to reduce the migratory and proliferative potential of these cancers, making itan attractive therapeutic target. Starting with a known peptide antagonist, the present work reportsthe application of a succession of computational ligand design tools comprising a ligand shape based sim-ilarity search, molecular docking and a 2D-similarity search to identify small molecular antagonists of theGrb7-SH2 domain from the NCI chemical database. Binding to the Grb7-SH2 domain was then experi-mentally tested using melting point shift assays and isothermal titration calorimetry. Overall, a total of11 benzopyrazine based small molecular antagonists were identified with affinity for the Grb7-SH2domain. Representative compounds tested using ITC were revealed to possess moderate binding affinityin the lowmicromolar range. Finally, the lead compound (NSC642056) was found to reduce the growth ofa Grb7-expressing breast cancer cell line with an IC50 of 86 lM. It is expected that the identified antag-onists will be useful additions to further explore the function of Grb7 and for the development of inhib-itors with therapeutic potential.
! 2010 Published by Elsevier Ltd.
1. Introduction
Growth factor Receptor Bound protein 7 (Grb7) is an adapterprotein that mediates signals from tyrosine kinases to effect down-stream events.1 Grb7 is of great interest as a therapeutic target incancers in which it is aberrantly overexpressed with HER2 and im-pacts on cell proliferation and migration.2 Grb7 co-overexpressionhas been implicated in a variety of human cancers such as breast,3
blood,4 pancreatic,5 esophageal6 and gastric carcinomas.7 More-over, the level of Grb7 over-expression is shown to correlate withseverity of Barrett’s carcinoma8 and lymphocytic leukemia.4 Inaddition to growth factor dependent signaling, Grb7 is also knownto associate with focal adhesion kinase9 and to be a component ofintegrin-mediated signal transduction which is an important path-way in cancer cell migration.10 The importance of Grb7 in cancerhas been established by a comparative analysis of the characteris-tics of Grb7 over-expressing and Grb7 knockout cancer cells.11,12
Finally, Grb7 has been demonstrated to be a targetable protein thatcan be blocked by synthetic agents resulting in a significant reduc-tion of cancer cell viability.5 Put together, these investigations
make Grb7 a highly attractive target for the design of anti-canceragents.
Grb7 is amulti-domain protein composed of a proline rich N-ter-minal domain, a Ras-associating domain, a plekstrin homology (PH)domain, a C-terminal Src homology 2 (SH2) domain and a BPS do-main (between the PH and SH2 domains).13,14 Each domain servesa distinct role that contributes to the overall signaling function ofGrb7.15 The physical association of Grb7with its activated upstreambinding partners is predominantly mediated by the C-terminal SH2domain of Grb7. The SH2 domain bears a cationic pocket that is thebinding site of phosphorylated tyrosines. Specific phosphotyrosinesare recognized based upon the sequence surrounding the phospho-tyrosine residue.15 The SH2 domain is also found in a number ofGrb7-related and other adaptor proteins guiding their specific inter-actions with upstream binding partners.16–18 This step is the mostcritical event in growth factor dependent Grb7 mediated signaltransduction. As such, the SH2 domain forms an essential modulefor Grb7mediated oncogenic signaling. Since the Grb7-SH2 domainis readily produced and its crystal structure is available, it provides aclear opportunity for inhibitor development via computational andbiochemical studies.19
Virtual screening has been developed as a powerful tool for theacceleration of drug discovery, specifically in the early part of leadcompound design.20,21 Ligand based virtual screening, a broad sub-
0968-0896/$ - see front matter ! 2010 Published by Elsevier Ltd.doi:10.1016/j.bmc.2010.10.030
! Corresponding author. Tel.: + 61 3 9902 9226; fax: +61 3 9902 9500.E-mail address: [email protected] (J.A. Wilce).
! Co-senior authors.
Bioorganic & Medicinal Chemistry xxx (2010) xxx–xxx
Contents lists available at ScienceDirect
Bioorganic & Medicinal Chemistry
journal homepage: www.elsevier .com/locate /bmc
Please cite this article in press as: Ambaye, N. D.; et al. Bioorg. Med. Chem. (2010), doi:10.1016/j.bmc.2010.10.030
category of virtual screening, is based on the principle that similarstructures produce similar effects.22 Depending on the representa-tion and description of lead structures, several approaches exist thattransform such information into a model that can be used to scancompound repositories.22,23 Most commonly, chemical similaritymeasures based on twoor three-dimensional structure ormolecularshape are employed in ligand based virtual screening efforts24,25
as well as in optimization tools such as quantitative structure–activity relationship,26,27 molecular docking28 and pharmacophoremapping.29,30
There have been numerous reports of the design and optimiza-tion of peptide-derived agents geared towards inhibition of thebroad class of growth factor receptor bound adaptor proteins, viatheir SH2 domains.31,32 A variety of tactics ranging from phosphor-ylation33 macrocyclization34 conformational restriction35 and useof amino acid surrogates36 have been exploited to optimize thebinding affinity of the lead peptides. Indeed, this has remarkablyresulted in the development of effective inhibitors37 and contrib-uted to a better understanding of the structural and functionalinvestigations of the SH2 domains. More specifically, Pero et al.have utilized a phage display techniques to discover an 11-residuenon-phosphorylated polypeptide (termed G7-18NATE) antagonistof Grb7.5,38 This peptide does not possess a rigid structure in solu-tion but interacts with the Grb7-SH2 domain with micromolaraffinity in a predicted turn-structure at the phosphotyrosine bind-ing site.19,39 Cell-permeable forms of this peptide have been shownto maintain their binding to Grb7-SH2 and to have anti-prolifera-tive and anti-migratory activity in cancer cell lines.5,40,41 Togetherthis demonstrates the potential for non-phosphorylated com-pounds to bind to the Grb7-SH2 domain and to possess anti-canceractivity. Experiments conducted in vitro on G7-18NATE and otherphosphorylated peptides demonstrate the potential for peptides tobe modified to enhance their affinity for Grb7-SH2.42,43 However,almost all the identified antagonists to date belong to a singlechemical class, that is, peptides, and thus are subject to issuesinherent to peptidic structures such as bioavailability, permeabilityand stability that remain a stumbling block for the application ofthese molecules in vivo. Most presumably due to these bottlenecks,to date there has not been a single peptide that has progressed tothe development of a useful therapeutic agent targeting Grb7 andrelated growth factor binding proteins, despite extensive efforts.31
With this in mind, the present work was initiated as a first step inthe development of a potent, selective and stable small molecularantagonist of the Grb7 oncoprotein. To the authors’ knowledge thisis the first time a small molecular antagonist is reported to bind tothe Grb7-SH2 domain. This work reports a shape based virtualscreening, molecular docking, 2D-similarity search, melting pointshift assay and isothermal titration calorimetric study carried outto identify a novel structural class of Grb7 antagonist. We finallyreport a preliminary functional study carried out with the leadcompound that demonstrates its growth inhibitory effects in abreast cancer cell line.
2. Results
2.1. Shape based query using known antagonist of the Grb7-SH2domain
Given the limited number and lack of structural diversity in theso far reported antagonists of Grb7, a shape based virtual screeningwas undertaken as a starting point to identify a novel lead. Struc-tural studies of SH2 domains in complex with peptide-based li-gands and numerous binding studies of modified peptide ligandshave revealed the common features of their interactions.18 Thus,as a starting point to the filtering of compounds, a shape based
query was generated using a tripeptide (m-aminobenzoyl-pY(a-Me)pYN-NH2) shown previously to be the most potent antagonistof growth factor bound adaptor 2 (Grb2) and Grb7 proteins andalso the smallest and simplest of the known antagonists.44 As theexperimental conformation of the tripeptide in complex with theGrb7-SH2 domain was not available, a conformational searchstrategy was pursued to establish possible bioactive conforma-tions. To this end, the MacroModel45 conformation search46 enginein Schrodinger47 was employed to generate stable conformers forinterrogation.
In order to select the conformer thatmay represent the optimumshape for the shaped-based query, a test database of known antago-nists of Grb7-SH2with determined comparative experimental affin-ities43 was prepared using the Maestro interface of Schrodinger.47
Since the lowest energy conformer is not necessarily the bioactiveconformer,46 all of the top five conformers of the query tripeptidewere evaluated for their suitability as a shape based query modelby considering their ability to rank-order the known antagonists.This assumes that all the known antagonists bind at the same siteon the same receptor as the query tripeptide. The program PHASE48
was employed to carry out a shape based virtual screeningexperiment.
Table 1 indicates the shape similarity coefficient obtained usingthe top five stable conformers of the tripeptide as shape based que-ries against the mini-database of known Grb7 antagonists. The cor-relation coefficient obtained between the shape based similarityindices of the antagonists and their pIC50 values depict the strengthof the relationship. The best correlation obtained is 0.93, corre-sponding to conformer 5. Thus, although the differences in the pep-tide affinities for their target do not span a wide range, whichlimits the significance of the correlation, conformer 5 was selectedas the basis for the shape based query in the subsequent lead iden-tification procedure.
2.2. Virtual screening of the NCI chemical database
A schematic representation of the virtual screening flowchartused is displayed in Figure 1. The tripeptide conformer 5 was usedas a shape based query to screen the National Cancer Institute(NCI) database (which contained 250, 251 structures at the timeof this work) [http://dtp.nci.nih.gov/]. This returned a total of63,300 hits when the similarity score cut-off was set at 0.41. Thetop hits from the shape based search were further screened usingthe Glide based molecular docking protocol.49,50 The top 5000 fromthe search were docked using Glide’s high-throughput virtualscreening (Glide HTVS) docking routine. This initial crude dockingprotocol resulted in 1886 successfully docked hits. All of the 1886hits were subsequently re-docked using the more accurate Glidestandard precision (Glide SP) docking procedure. Inspection ofthe failed structures revealed that the rejects were either simpleor polycyclic hydrocarbons that met the shape based criteria. TheGlide SP docking experiment resulted in 1854 of the 1886 hitsbeing successfully re-docked. The top 200 from the Glide SP dock-ing were finally docked with the extra precision Glide (Glide XP)docking routine. The molecular docking protocol was the samethroughout the computational experiment. Of the 200 hits identi-fied, 15 potential candidates with favorable Glide SP or Glide XPdocking scores, and with good predicted surface complementarityand interactions at the target Grb7-SH2 domain surface uponexamination, were selected. The compounds identified and theirdocking scores are shown in Table 2.
2.3. Predicted binding mode of hit NSC642056
An example of a compound selected by the above criterion, abenzopyrazine numbered NSC642056, is shown in its docked
2 N. D. Ambaye et al. / Bioorg. Med. Chem. xxx (2010) xxx–xxx
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geometry in Figure 2. NSC642056 is predicted to form a number ofspecific binding interactions with the binding site of the Grb7-SH2domain. The phenyl ring of the benzoyl moiety is appropriatelypositioned to make favorable hydrophobic/van der Waals interac-tions with the side chains of Leu481 and Tyr480 within the bindingsite. A potential hydrophobic/van der Waals bond with the sidechains of Val468 and His479 is also apparent with the aromaticsystem of the hit. In addition, the hit also forms multiple hydrogen
bonding interactions with the Grb7-SH2 domain binding site. Thecarbonyl adjacent to the ester moiety is observed to make twohydrogen bonding interactions with the guanidine group ofArg458. Moreover two other hydrogen bonding contact pairs occurbetween each of the di-oxo moieties on the anilinobenzene carbox-amide with the backbone NHs of Arg462 and Asn461 residues. Fi-nally the carboxamide amino moiety is involved in a hydrogenbonding interactions with the Gln463 of Grb7-SH2 binding site.
2.4. Experimental pre-screening with melting point shift assay
Out of the top 15 potential hits, five were available at the timeof this work and kindly provided by the NCI Developmental andTherapeutic program unit of the USA (Drug synthesis and Chemis-try branch, http://dtp.nci.nih.gov/) (indicated in Table 2). Thesewere subjected to in vitro binding studies, as supplied by the NCIwithout further characterization. Experimental pre-screening ofthese compounds was carried out using a Thermofluor based ther-mal shift assay.52,53 This assay is based upon the increased meltingtemperature of a protein induced by ligand binding. The com-pounds were dissolved in 1% DMSO/buffer solution and their effecton the melting temperature of the Grb7-SH2 domain was deter-mined. One of out of the five tested compounds, NSC642056, pro-duced a positive melting point shift (Table 3). Interestingly, thefinding that hit NSC642056 interacts with the Grb7-SH2 domaincorrelates with its better shape based similarity coefficient andglide docking score relative to those of the four structures thatturned out to be false hits. Indeed, NSC642056 occurs in the top5 of the priority list while the negative hits were in the bottom 5of the 15 hits suggested from the combined virtual screeningexperiment. The change in melting point produced by the hit
Table 1Shape similarity index of known Grb7 antagonists using the top five conformers of the m-aminobenzoyl-pY(a-Me)pYN-NH2 tripeptide as a query
S. No Known antagonist pIC50a Shape similarity indexb
Conf. 1 Conf. 2 Conf. 3 Conf. 4 Conf. 5
1 PEpYVNQ-NH2 5.96 0.54 0.50 0.48 0.39 0.472 Ac-pYVNQ-NH2 5.47 0.51 0.46 0.39 0.43 0.353 EpYVNQ-NH2 5.815 0.51 0.48 0.43 0.45 0.454 pYVNQ-NH2 5.45 0.45 0.48 0.43 0.41 0.38Correlation coefficientc 0.58 0.62 0.63 0.04 0.93
a The pIC50 values were obtained from the reported IC50 value43 using the equation pIC50 = !logIC50.b Conf. 1–5 represent the top five conformers of the query tripeptide used in the virtual screening experiment.c The correlation coefficient indicates the correlation between the pIC50 value and the shape similarity value for each conformer.
Figure 1. Schematic representation of the virtual screening experiment conductedbased on m-aminobenzoyl (a-Me)pY-NH2 tripeptide as shape based query.
Table 2Final hits identified based on the tripeptide based shape search
Rank Hit ID. Shape similarity index Glide SP docking Glide XP docking
Glide score Emodel Glide score Emodel
1 NSC677186 0.433 !6.348 !79.584 !5.130 !95.5862 NSC677177 0.463 !6.337 !84.217 !4.790 !62.8363 NSC677184 0.429 !5.883 !73.463 !4.190 !89.9244 NSC633047 0.480 !5.792 !68.058 !3.420 !79.2005 NSC642056* 0.457 !5.749 !71.077 !4.900 !81.6126 NSC677147 0.437 !5.716 !69.901 !3.200 !77.7137 NSC677176 0.427 !5.484 !72.001 !3.310 !80.7908 NSC713163 0.413 !5.368 !44.324 !3.760 !45.1989 NSC677174 0.427 !5.318 !63.131 !3.560 !74.519
10 NSC100787 0.428 !5.277 !63.580 !4.550 !84.74011 NSC129843* 0.435 !5.264 !75.089 !3.780 !83.88912 NSC642057* 0.436 !5.256 !67.214 !3.540 !76.78913 NSC344032 0.441 !5.252 !64.706 !3.220 !77.36514 NSC687783* 0.426 !5.241 !65.861 !3.750 !68.42215 NSC657678* 0.458 !5.223 !61.619 !3.870 !74.176
* Indicates hits that are tested experimentally.
N. D. Ambaye et al. / Bioorg. Med. Chem. xxx (2010) xxx–xxx 3
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was 0.6 "C at 100 lM and 1.1 "C at 200 lM which were slightlylower than that produced by a peptide-based (G7-18NATE)38
Grb7-SH2 inhibitor control (1.35 "C at 100 lM and 1.85 "C at200 lM). Thus, hit NSC642056 was able to effect stabilization com-parable to the known G7-18NATE-based polypeptide inhibitorwhich suggests that the compound may have potential as anantagonist of Grb7.
2.5. Lead discovery using 2D-similarity searches and bindingstudies
In an effort to discover further compounds with affinity forGrb7-SH2, structures related to NSC642056 were sought. To thisend, analogues of the hit were screened using a two-dimensional(2D) structure based similarity search.23 The 2D-search was under-taken against the same NCI database using the SMILES54 descrip-tion of the lead structure as an input. The use of the leadNSC642056 as a 2D-query returned 22 benzopyrazine hits of which15 were available at the time of this work from the NCI develop-mental and Therapeutic program. The 15 compounds were then as-sessed using the melting point shift assay as described above. Theresult, shown in Table 3, revealed that out of the 15 structural ana-logues tested 10 were able to produce a positive melting pointshift. The change in melting point induced by the analogues was
found to be comparable to that of the lead NSC642056 compound(Fig. 3). The structures of the 10 leads identified in addition to thestarting structure are shown in Figure 4. The 10 identified com-pounds were sub-classified into di-substituted benzopyrazines(NSC644743, NSC646820, NSC646823, and NSC648589), tri-substi-tuted benzopyrazines with benzoyl substituent (NSC642040,NSC648607, and NSC648605) and tri-substituted benzopyrazineswith a nitro substituent (NSC644750, NSC644770, and NSC644745).Though these are analogues of NSC642056, the virtual screeningcriteria adopted in the initial shape based search might have pre-vented these structures from showing up within the top 15 ofthe shape based hits.
2.6. Confirmation of binding by ITC
Further characterization of these interactions was undertakenusing isothermal titration calorimetry (ITC).55 ITC measures theamount of heat absorbed or released as one interacting species is ti-trated into the other. From this, the equilibrium dissociation con-stant, free energy, enthalpy, entropy and stoichiometry of binding
Figure 2. Binding mode of lead NSC642056. (A) The specific interaction between the ligand and Grb7-SH2 domain. The ligand is displayed in ball and stick format whilebinding site residues are shown in line format. The yellow dotted lines represent hydrogen bonds between the hit and Grb7 binding site; the figure was produced in Maestroof Schrodinger suite. (B) The overall fold of Grb7-SH2 domain depicting its surface, secondary structural elements and the relative positioning of the lead compound. Thefigure was produced by virtual molecular dynamics (VMD) visualization program.51
Table 3Tanimotto similarity coefficient and melting point shift data for benzopyrazinederivatives
S. No. Hit code Tanimotto similaritycoefficient (%)
DTma ("C)
100 lM 200 lM
1 NSC642040 97 0.45 0.952 NSC648605 98 0.05 0.553 NSC644743 92 0.95 0.954 NSC648607 97 0.45 1.455 NSC644745 90 1.30 1.306 NSC644750 94 0.45 0.857 NSC644770 94 0.45 0.558 NSC646820 90 1.20 0.959 NSC646823 95 1.00 0.70
10 NSC648589 92 0.90 0.60A NSC642056 100 0.60 1.10B G7-18NATE Not applicable 1.35 1.85
a The change in melting point (DTm) are obtained from duplicate experimentsafter the melting point of Grb7-SH2 apo (Tm = 49 "C) was subtracted from that of thehit bound form. NSC642056 was the lead compound while G7-18NATE is the ref-erence polypeptide concurrently run in the melting shift assay.
1.2
2.2
3.2
4.2
5.2
37 42 47 52Temperature (ºC)
Fluo
rese
nce
Inte
nsity
Grb7 SH2 apo
Grb7 SH2-NSC642056
(Tm = 49.00C)
(Tm = 49.60C)
Figure 3. Unfolding curve of Grb7-SH2 domain obtained from thermal meltingexperiment. The filled square curve corresponds to the apo form of Grb7(Tm = 49.0 "C) while the open square curve represents that of Grb7–NSC642056complex (Tm = 49.6 "C).
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can be determined.56 The binding of NSC642056 as well as 5 repre-sentative compounds from three classes of substituted benzopyra-zines, identified by the Grb7-SH2 domain melting point assay,were determined by ITC. As shown in Table 4, the equilibriumdisso-ciation constant for hit NSC642056 was found to be 17.15 lM. Thisnot only confirms the binding but demonstrates that it occurs witha moderate affinity. The binding data shows that the compoundsinteract with favorable enthalpy and unfavorable entropy with a1:1 binding stoichiometry. In a similar vein, the analogue structures(representative structures from each subclass—NSC642040,NSC644745, NSC644743, NSC646823, and NSC648607)—were sub-jected to the ITC binding assay. Figure 5 shows the ITC binding iso-therm for one of the analogues tested.
Each of the compounds characteristically bound with evolutionof heat, that is, through exothermic binding similar to the leadNSC642056 (Table 4). The experimental affinities were found tobe of moderate values ranging from Kd = 3.06 lM for NSC646807to Kd = 17.15 lM for NSC642056 lead. Though the free energy ofbinding is in a very close range (ca. !7 kcal/mol), deconvolutioninto its constituents reveals subtle differences in the entropic andenthalpic contributions to binding. In the case of NSC648607 andNSC644743, the enthalpic contribution to binding is greater thanthe entropic part. However, for leads NSC644745 and NSC646823the enthalpic/entropic ratio is reversed. The fact that the grossbinding affinities remained virtually unaffected despite the differ-ences in the relative contribution of the constituent parts suggests
N
N
O
O
O
O
O
ONH
OH
ONH2
N
N
O
O
O
O
O
ONH
OH
NSC642056 NSC642040
N
N
O
O
O
O
O
ONH
OH
NSC648605
O
N
NO
O O
O
ONH
OH
NSC648607
A
B
N
N
O
O
O
O
ONH
OH
NSC644743
N
N
O
O
O
O
ONH
OH
N
N
O
O
O
O
O
NH
OH
O
NSC646823 NSC648589
NN
OO
O
OO
HN
OHC
NO2
CN
O2N
NSC644745
N
NOO
O
OO
HN
OH
NO2
NC
NN
OO
O
OO
HN
OH
O2N
N
N
O
O
O
O
ONH
OH
O2N
NSC646820
NH2
O
NSC644750
O
NSC644770
O
Figure 4. Chemical structures of the benzopyrazine derivatives. (A) Tri-substituted benzopyrazines with benzoyl substituent. (B) Di-substituted benzopyrazine derivatives.(C) Tri-substituted benzopyrazines with a nitro substituent.
Table 4Thermodynamic binding parameters for the benzopyrazine derivatives
Lead NSC642040 NSC644745 NSC646823 NSC644743 NSC6468607 NSC642056
Stoichiometry 1.11 ± 0.03 1.14 ± 0.03 1.04 ± 0.11 1.06 ± 0.03 1.04 ± 0.02 1.09 ± 0.04Kb (105 M!1) 2.06 ± 0.42 1.58 ± 0.35 1.41 ± 0.10 1.85 ± 0.46 3.48 ± 0.87 0.60 ± 0.10DH (Kcal/mol) !2.94 ± 0.11 !1.33 ± 0.05 !0.74 ± 0.09 !6.11 ± 0.32 !5.54 ± 0.19 !10.23 ± 0.51DS (cal/mol/K) 14.35 19.3 21.1 3.61 6.89 !12.5TDS (Kcal/mol) 4.28 5.75 6.29 1.08 2.05 !3.73DG (Kcal/mol) !7.21 ± 0.11 !7.08 ± 0.05 !7.03 ± 0.09 !!7.19 ± 0.32 !7.56 ± 0.19 !6.50 ± 0.51Kd (lM) 5.06 ± 1.03 6.57 ± 1.20 7.12 ± 0.50 5.76 ± 1.40 3.06 ± 0.77 17.15 ± 2.97
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that entropy–enthalpy compensation phenomenon taking place.This is commonly observed in ligand–receptor binding studies.57
2.7. Cellular growth inhibitory assay
Finally, a cellular growth assay was conducted using theMDA-MB-468 breast cancer cell line to determine whether the leadcompound would display activity in an in vivo system. To this ef-fect, the impact of compound NSC642056 on these Grb7-express-ing cancer cells was investigated. The result, as shown in Figure6, shows that the lead compound impacts on the growth of thecells in a concentration dependent manner. The in vivo IC50 deter-mined for the cell growth inhibition is found to be 86.0 lM. This iscompared to the in vitro Kd of 17.3 lM, and thus suggests a corre-lation between the inhibitor binding affinity for the Grb7 targetand the concentration required for cell growth inhibition. Futureinvestigations, using both cells in which Grb7 is knocked out usingRNAi and knocked back in, will allow us to identify the extent towhich the inhibitor action is indeed occurring through bindingand inhibition of Grb7.
3. Discussion
Few antagonists of Grb7 have previously been identified. Thosereported include the polypeptide G7-18NATE5,38,39 identifiedthrough phage display and found to be selective for Grb7 with min-imal activity against related proteins. Other short peptides are alsoreported to bind to the Grb7-SH2 domain in vitro.43 Being peptidicin nature, however, the potential for their in vivo use is restricteduntil major issues such as the limited bioavailability, in vivo insta-
bility, cell impermeability and high synthetic costs of peptides areresolved.58 Here we identify compounds of the benzopyrazine classthat have an equivalent affinity for the Grb7-SH2 domain as thepreviously reported peptides (i.e., moderate to low micromolarbinding affinity), and suggest that these may offer an alternativescaffold for the development of potent inhibitors of Grb7. Similarlyto the in vivo activity of the peptide-based Grb7 inhibitor,G7-18NATE, inhibition of the growth of cancer cells is observed.40
Future experiments will be required to demonstrate whether themode of action is specifically via Grb7 inhibition, or also/alterna-tively through other pathways. The current studies do not establishwhether these compounds possess intrinsic specificity for theGrb7-SH2 domain. Being predicted to bind to the peptide recogni-tion surface of the Grb7-SH2 domain, however, we propose thatthey would be amenable to modification to improve their affinity,pharmacological properties and potentially to confer specificity forGrb7. The compounds would not be the target of proteases, whichis a major obstacle for the use of peptides as drugs, and their rela-tively smaller size is predicted to improve their bioavailability totheir intracellular target.
Benzopyrazines from the NCI database were identified in thecurrent study owing to their ability to adopt a structurally similarshape to a known peptide-based inhibitor of the Grb7-SH2 domain.The present work effectively exploited the molecular similarityprinciple that shape based similarity can reflect similarity in po-tential binding interactions.59,60 The shape based virtual screeningexperiment was able to identify moderate affinity lead candidates,as confirmed by a Thermofluor binding assay. The identification ofa substituted benzopyrazine (NSC642056) prompted a 2D-similar-ity search, resulting in the identification of further benzopyrazineswith potential for binding to the Grb7-SH2 domain. Binding to thetarget was confirmed experimentally using both melting point as-says and ITC. Overall, the computational experiments attest to theusefulness of the application of a succession of virtual screeningtools in lead compound identification.
The Thermofluor binding assay proved an effective experimen-tal method to confirm ligand binding. It is a rapid and inexpensiveassay that does not utilize very much material. Thermofluor ex-ploits the concept of protein stabilization upon ligand binding.Only a one degree change in the melting temperature of the pro-tein was observed upon interaction with the lead compounds. Thisrelatively low value is typical for ligands binding with micromolaraffinity and may represent the limit of detection of the meth-od.54,55,61 Similar thermal shift values were measured for a knownpeptide inhibitor of the Grb7-SH2 domain that binds with micro-molar affinity. ITC was used to confirm the interactions, measurethe affinity and also provided insight into the entropic versusenthalpic contributions to binding. Though the identified benzo-
0.0 0.5 1.0 1.5 2.0-4
-2
0
-1.0
-0.8
-0.6
-0.4
-0.2
0.0
0 50 100 150 200
Time (min)
!cal
/sec
Molar Ratio
kcal
/mol
e of
inje
ctan
t
Figure 5. ITC thermogram of a benzopyrazine derivative, NSC642040. The upperpanel show raw data obtained from 10 ll injections of compound at 25 "C. Thelower panel display plots of integrated total energy exchanged (as kcal/mol ofinjected compound) as a function of molar ratio of the compound to the Grb7-SH2domain (squares). Solid lines indicate the fit to a single-site saturation model.
IC50 of 642056 in MDA-MB-468
0 1 2 3 4 5 6405060708090
100110
log [lead NSC 642056]
% c
ell v
iabi
lity
Figure 6. Cellular growth inhibition curve obtained for MDA-MB-468 breast cancercells treated with the lead NSC642056. The IC50 was found to be 86 lM.
6 N. D. Ambaye et al. / Bioorg. Med. Chem. xxx (2010) xxx–xxx
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pyrazines bound with only micromolar binding these smallmolecule antagonists could be useful for the experimental andclinical investigations of Grb7 and related proteins.
In conclusion, starting with a known peptide antagonist, thepresent work reported the successful application of a successionof computational ligand design tools comprising ligand shapebased similarity search, molecular docking and 2D-similaritysearch to identify a novel class of small molecular antagonists ofGrb7. Experimental binding studies with a melting point shift as-say and ITC confirmed the interactions and shed some light onthe thermodynamic aspects of the binding interactions. That thelead NSC642056 antagonist reduced the growth of breast cancercells was confirmed in the MDA-MB-435 cell line. Further workwill be required to determine whether the mode of action is, in-deed, via Grb7 inhibition. It is expected that the newly identifiedbenzopyrazine scaffolds will be useful additional agents to furtherexplore and accelerate functional studies of Grb7 and potentiallylead to the development of novel therapeutics.
4. Experimental section
4.1. Generation of the shape based query
MacroModel’s45 conformation search46 engine in Schrodinger47
was employed to generate stable conformers of the m-amin-obenzoyl-pY(a-Me)pYN-NH2 peptide, previously shown to be a po-tent inhibitor of the Grb7-SH2 domain.43 The optimal potential forliquid simulation force field with a distance dependent dielectricconstant was used during the conformation search. Partial chargeswere computed using the force field. Geometry optimizationwas ef-fected with maximum iteration of 5000 and a gradient convergentcriterion was applied with a threshold of 0.05. The systematic tor-sional sampling option was employed to generate representativeconformations of the tripeptide reference query. Unless specificallymentioned, all other conformation search parameters were kept attheir default value.
4.2. Shape based similarity virtual screening
The program PHASE48 was employed to carry out shape basedvirtual screening experiments. The atom type used for volumescoring was set to none so as not to bias the search towards a par-ticular hit class particularly for the subsequent database screening.The conformer that produced the best correlation between theshape based similarity index and the biological activities of thepeptides in the mini-database was then employed to serve as aquery to search the enhanced National Cancer Institute (NCI) data-base. The average similarity index of the known antagonist wasthen used as a cut-off during the NCI screening.
4.3. Molecular docking
The program Glide was used to perform Grb7-SH2 domaindocking studies for top hits from the shape based search. Glidecomprises three docking routines that are designed to suit differentstages of chemical database screening.49,50 The PDB file for theGrb7-SH2 domain was read into Maestro in Schrodinger and theprotein preparation wizard used to set up the protein includingaddition of hydrogen atoms and deletion of water molecules be-yond 5 Å from protein atoms. Hydrogen bond assignment was ef-fected with the exhaustive sampling option and the system wassubsequently relaxed with geometry minimization. A grid of size12 " 12 " 12 Å was defined using the peptide binding surfaceabout the phosphotyrosine pocket to define the binding site. Allthe other docking parameters were kept at their default values.
4.4. Expression and purification of Grb7-SH2 domain
The SH2 domain of Grb7 was used as a receptor for the thermalshift and ITC binding experiments. The pGex2T plasmid containingthe Grb7-SH2 insert encoding residues 415–532 of human Grb7protein was expressed in Escherichia coli expression system as aGST fusion protein in BL21(DE3)pLysS host strains.62,63 Cell induc-tion was achieved with 400 lM isopropyl b-D-1-thiogalactopyra-noside. Cell resuspension was carried out in ice-cold phosphatebuffer saline with 2 mM EDTA, 0.5% Triton-X 100 and lysis by son-ication. The fusion protein was purified by glutathione affinitychromatography (GE Healthcare) and cleaved with thrombin. Puri-fication using cation exchange chromatography was then effectedusing a HiTrap SP column (GE) after an overnight dialysis into20 mM HEPES pH 7.4, 20% glycerol, and 1 mM DTT at 4 "C. Thiswas followed by dialysis into 50 mM MES pH 6.6, 100 mM NaCl,and 1 mM DTT and final purification by size exclusion chromatog-raphy using a Sephadex 75 XK 16/60 column (GE). Grb7-SH2 do-main was concentrated and stored at 4 "C. Its purity was verifiedusing SDS–PAGE. The final concentration was determined withUV–vis spectroscopy.64
4.5. Thermofluor based melting point shift assay
The thermofluor based melting point shift assay relies on an in-crease inmelting point of the target protein as an indication of com-pound binding.52,53 The dye Sypro Orange is used to detect themelting transitions through its binding to exposed hydrophobic re-gions of the unfolding protein. The melting point of the Grb7-SH2domain was determined with the use of Quiagen’s quantitativeRT-PCR instrument (www.qiagen.com). The wavelength of excita-tion/emission was set to 470/555 and 470/610 nm. A heating rateof at 1 "C per min was programmed over a 30–80 "C temperaturerange with a holding time of 60 s. The buffer used was 50 mMMES, 100 mM NaCl, pH 6.6, 1 mM dithiothreitol (DTT). The purifiedGrb7-SH2 domainwas added to each tube to yield a final concentra-tion of 20 lM. The protein concentrationwas established using UV–vis spectrophotometer at 280 nm and amolar extinction coefficientof 8480 M!1 cm!1. All the compounds were dissolved in 1% DMSO/buffer solution and a final concentration of 100 lM and 200 lMwas added to the protein. Aftermixing, 25 ll of the protein/hit solu-tion was transferred to the PCR tubes for the melting experiment. Aknownpeptide inhibitor38was also tested as a positive control. Eachdenaturation experiment was conducted in duplicate and in eachcase the average melting temperature was taken for analysis. TheRotor-Gene 3000 software was used to set up the experiment andanalyze the results.
4.6. Isothermal titration calorimetry
ITC binding experimentswere performed on a VP-ITCMicrocalo-rimeter (Microcal, Northampton, MA, USA) at 25 "C.55,56 TheGrb7-SH2 domain was dialyzed against 2 L of 50 mM NaOOCCH3
(pH 6.6), 100 mM NaCl, and 1 mM DTT. The concentration of Grb7-SH2 and hits was determined as described in the melting experi-ment. The hit and protein solutions were degassed and thermo-stated at 20 "C for 5 min using the ThermoVac of the VP-ITCMicrocalorimeter. The reference power of the experiment was setto 20 lCal/s and the cell contents were stirred continuously at307 rpm throughout the titrations. The feedback mode gain wasset to highwith fast and auto equilibrations options applied. The ref-erence cell was filled with MQ water. The hits at concentrations inthe range of 500–950 lM were titrated into Grb7-SH2 solutions of50–85 lM concentrations in 7–10 ll injections with a 3–6 min de-lay between each injection. A binding isotherm was generated byplotting the heat change evolved per injection against the molar
N. D. Ambaye et al. / Bioorg. Med. Chem. xxx (2010) xxx–xxx 7
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ratio of the leads to Grb7-SH2 domain receptor. A blank determina-tion in which the compounds were titrated against the buffer wascarried out to account for heats of dilution and mixing which wasthen subtracted from the binding data. The corrected data was thenfitted by a single binding sitemodel using a non-linear least squareswith the Origin (Microcal Software, Northampton, MA, USA).
4.7. Lead optimization by 2D-similarity search
Two-dimensional structure based similarity22,23 searches of theNational Cancer Institute database (http://dtp.nci.nih.gov/) wereconducted using the SMILES53 description of chemical structureusing the lead NSC642056 as input. The SMILES string was gener-ated using the enhanced NCI database browser platform. The max-imum number of hits was set to 1000. Hits with Tanimottosimilarity coefficients above 90% were obtained for further subse-quent experimental investigation.
4.8. Cellular growth inhibitory studies
To determine the effects of the compounds on cellular growth,MDA-MB-468 breast cancer cells were resuspended at5 " 104 cells/mL and 100 lL of this cell suspension was plated in96 well plates (BD Biosciences, California, USA). The following daycells were treated with a range of concentration of the compounds,each concentration with triplicates wells. Cells were incubated un-der standard growth conditions with 10% fetal bovine serum overa 4-day period (0–4 days). Adherent cell cultures were fixed in situafter 4 days by the addition of 25 ll of cold 50% trichloroacetic acidsolution (Sigma–Aldrich,Missouri, USA) and incubated for 60 min at4 "C. The supernatant was then discarded and the plate was washedfive timeswith running distilledwater before being dried overnight.Fixed cells were stained by the addition of 100 ll of sulforhodamineB (SRB) sodium salt solution (0.4% (w/v) in 1% acetic acid; Sigma–Al-drich,Missouri, USA) and incubated for10 minat roomtemperature.Unbound SRB solution was removed by washing five times with 1%acetic acid after which the plates were air-dried overnight. The fol-lowing day, the bound stain was solubilized with 100 ll of 10 mMTris buffer (pH 10.5) and the absorbance of the eluted dye was readon the spectrophotometric BMG PolarStar Optima plate reader(BMGLabtech,Offenburg,Germany) at 540 nm. SRB is a total proteinstain, which directly correlates with cell number and is used rou-tinely tomeasure cell growth rate. TheNonlinear regression analysisof the concentration–response plot was conducted using GraphPadPrism software.
Acknowledgments
This work was funded by an Australian Research Council ProjectGrant awarded to J.A.W. and D.N.K. and a Monash UniversityGraduate Scholarship awarded to N.D.A. M.C.J.W. and J.T.P. arethe recipients of a Senior Research Fellowship and a R.D. WrightFellowship respectively from the National Health and MedicalResearch Council of Australia. We thank the Drug Synthesis andChemistry Branch of National Cancer Institute of the USA forproviding the compounds used in the screening and testing. TheVictorian partnership for advanced computing (VPAC) is acknowl-edged for granting us access to the computational facilityemployed in the study.
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laration for Thesis Chapter [8-9]
Declaration by candidate
In the case of Chapter [8] and [9], the nature and extent of my contribution to the work was as.S :
l{ature of contributionProtein expression/purifi cation, set up crystailization
trials, data collection and structure determination.manuscript preparation
The following co-authors contributed to the work. Co-authors who are students at MonashUniversity must also indicate the extent of their contribution in percentage terms:
Contribution(o/o) Signature
80% ' ' . , - . . - ' , , , - .
l[ame
Daouda Troarel
Nature of contribution
Assisted in data cotiection anA struiture solutionJ Gunzburg
I Participated i n protein expressi on/puri fi cation
'ico1e R Contributed in data collectionrk deltthew
ick Permutter2
solution, data intelpretation
Contributed to peptide synthesis
Contributed to peptide synthesis and Datainterpretation
ibel l Anguilarr
R Wiicel Planned and supervised the overall experiments ./... . .. .,
and oversaw the renorfins of fhe reqrrlfq , i' -
and oversaw the reporting of the resu-lis ,,:.f" '' 1 - i ?1 i
rDepartment of siochemisiry ana Moiecutii nioiogy, Monaitr universiry, VIC 3800, Australia; 2 Deparrmenr ofChemistry, Monash University, VIC 3800, Australia;
Declaration by co-authors
I hereby certift that:
(l) the above declaration correctly reflects the nature and extent of the candidate,scontribution to this work, and the nature of the contribution of each of the co-authors.(2) they meet the criteria for authorship in that they have participated in the conception,!xecution, or interpretation, of at least that part of the publication in their field of expertise;(3) they take public responsibility for their part of the publication, except for the ..rponribl.author who accepts overall responsibility for the publication;(4) there are no other authors of the publication according to these criteria;(5) potential conflicts of interest have been disclosed to (a) granting bodies, (b) the editor orpublisher ofjournals or other publications, and (c) the head of the responsible academic unit;and
(6) the original data are stored at the above location(s) and will be held for at least five vearsfrom the date indicated below:
1
Borgo' Assisted in peptide synthesis : '': ..r
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(*-7&-$! &-.%2#,.&*-/! 6&.=! T=#&-! U! &-,):7%! 7&2%,.! &-.%2#,.&*-/! 6&.=! 42$IGP?!
O*2%*9%2\! &-7&2%,.!=F72*$%-!(*-7&-$! &-.%2#,.&*-/!6&.=!H&/ICS!*,,:2! 9&#!(2&7$&-$!
6#.%2!>PMS?!4-*.=%2!6#.%2R(2&7$%7!=F72*$%-!(*-7&-$!&-.%2#,.&*-!&/!*(/%29%7!6&.=!
;F/ICN! 9&#! (2&7$&-$!6#.%2/! #.! >SAI\! >PCW\! #-7! >PC>?! 477&.&*-#)! =F72*$%-! (*-7/!
%K&/.!6&.=!.=%!(#,5(*-%!QH!*+!H&/ICS!9&#!(2&7$&-$!6#.%2/!>SAI!#-7!>PIA?!V-!T=#&-!
U\! .=%! 8*/.! &8D*2.#-.! 2%/&7:%/! #2%e! LIGP! _U@4! fGA?GGsA`! #-7! HICS! _U@4!
&'()*+,!=-!J46'!,+1CA3*4CD!/.2:,.:2%/!*+!B2(C!@HA!7*8#&-!
! %<0!
f>I?SGsA`?!'=&/!,)%#2)F!%/.#()&/=%/!.=%!8*/.!&8D*2.#-.!(&-7&-$!/&.%!2%/&7:%/!*+!B2(C!
@HA!7*8#&-\!/%%!X&$?!S?N!+*2!,*8D#2&/*-/?!
0
5
10
15
20
25
30
R462 R438 R458 S460 Q461 V468 L481
Binding site residues
Bu
rrie
d s
urf
ace a
rea
!
X&$:2%! S?NE! L%/&7:%! ,*-.2&(:.&*-! .*! &-.%2#,.&*-!6&.=!8#)*-&,! #,&7! =&$=)&$=.&-$! .=%!8*/.!&8D*2.#-.! 2%/&7:%/! *+! .=%! B2(C! @HA! 7*8#&-! *+! ,=#&-! 4! (&-7&-$! /&.%?! '=%! =&/.*$2#8!&-7&,#.%/!2%/&7:%/!LINA\!;IP>!#-7!oIN>!#/!.=%!.=2%%!8*/.!&8D*2.#-.!(&-7&-$!D#2.-%2/!*+!8#)*-&,!#,&7!&-!.=%!B2(C!@HA!(&-7&-$!/&.%?!
!
<='*#0(',80=*%3*1+:%,"$*+$"-*",0'(+$0"%,#*?"0=*
O#)*-&,! #,&7! /%%8/! .*! +*28! #! -:8(%2! *+! =F72*$%-! (*-7&-$! &-.%2#,.&*-/!6&.=! .=%!
#D*! /.2:,.:2%\! #-7! &.! &/!6%))! D)#,%7! &-! .=%! D=*/D=*.F2*/&-%! 2%,*$-&.&*-! D*,5%.! *+!
B2(C!@HA!7*8#&-?!0-.%2%/.&-$)F\!8#)*-&,!#,&7!&/!#)/*!+*:-7!#/!#!/.2:,.:2#)!+%#.:2%!*+!
/%9%2#)! B2(A! #-.#$*-&/./! #/! D#2.! *+! D=*/D=*.F2*/&-%!8&8%.&,/?! J9%-!8*2%\! &.! =#/!
(%,*8%!,)%#2!.=#.!6=%-!.=%!#,.&9&.&%/!*+!.=*/%!B2(A!#-.#$*-&/./!#2%!,*8D#2%7\!&.!&/!
+*:-7! .=#.!8#)*-&,! #,&7! ,*-.#&-&-$! #-.#$*-&/./! D*//%/! *-%! *+! .=%! =&$=%/.! (&-7&-$!
#++&-&.F?IW\I>! B&9%-! &./! D2*9%-! 2*)%! &-! %-=#-,&-$! .=%! (&-7&-$! #++&-&.F! *+! B2(A!
#-.#$*-&/./!#-7!.=%!*(/%29#.&*-!.=#.!&.!+*28%7!#!-:8(%2!*+!,)*/%!.*!&7%#)!=F72*$%-!
(*-7&-$! &-.%2#,.&*-/!6&.=! .=%! D2%/%-.! B2(C! @HA! 7*8#&-! /.2:,.:2%\! #! a:#-.&.#.&9%!
%/.&8#.&*-!*+! &./! (&-7&-$! #++&-&.F!6#/! /*:$=.?! '*! .=#.! %++%,.\! #!'=%28*X):*2!(#/%7!
8%).&-$! D*&-.! /=&+.! #//#F! 6#/! %8D)*F%7?! '=%! /F/.%8! 7%.%,./! ,=#-$%/! &-! 8%).&-$!
D*&-./!(%.6%%-!#D*!#-7!=*)*!+*28/!*+!D2*.%&-/?!4!D*/&.&9%!8%).&-$!D*&-.!/=&+.!*+!.=%!
=&.^B2(C! @HA! 7*8#&-! ,*8D)%K! &/! .#5%-! #/! #-! &-7&,#.*2! *+! (&-7&-$! D=%-*8%-*-?!
X2*8! .=&/! %KD%2&8%-.! &.! &/! +*:-7! .=#.! 8#)*-&,! #,&7! (&-7/! 6&.=! &-,2%7&()F! =&$=!
#++&-&.F!.*!.=%!B2(C!@HA!7*8#&-!#/!&-7&,#.%7!(F!.=%!=&$=!8%).&-$!D*&-.!/=&+.!+*2!.=%!
#//*,&#.&*-!%9%-.\!&?%?\!,)*/%!.*!>W!WT!#/!/=*6-!&-!'#()%!S?A?!'=&/!&/!%/D%,&#))F!6=%-!
&'()*+,!=-!J46'!,+1CA3*4CD!/.2:,.:2%/!*+!B2(C!@HA!7*8#&-!
! %<<!
,*8D#2%7! .*! .=#.! *+! #! 5-*6-! D*)FD%D.&7%! #-.#$*-&/.! *+! B2(C! @HA! 7*8#&-RBCR
>PQ4'J!_%'8!f!>?G!WT`?!
!*<+5:'*^BFS*<='(1+:*#0+5":"0)*-+0+*
T*8D*:-7! T*-,%-.2#.&*-!_wO`! '8_WT`! í'8_WT`!@*7&:8!O#)*-#.%^B2(C! >WW! NA?>! S?MG!! AWW! N>?MC! S?W!! MWW! NA?GG! S?CN!B2(C!@HA!7*8#&-! AW! MA?MC! RRRRRR!
*
*
FB*!"#$B+3634+3$9:;<=>.!?I95B:$0&H$'()*+,$3()@4#J$7A5C3AC5#*
*<='*.&'(+::*C0(;$0;('*
'=%!,2F/.#)!/.2:,.:2%!*+!(&,F,)&,!BCR>PQ4'J^B2(C!@HA!7*8#&-!,*8D)%K!6#/!/*)9%7!
.*! ! >?C! s! 2%/*):.&*-?! '=%! /.#.&/.&,#)! D#2#8%.%2/! #//*,&#.%7! 6&.=! .=%! /.2:,.:2%!
/*):.&*-!D2*,%//!#2%!/=*6-! &-!'#()%!>>?>\!#)*-$!6&.=! .=#.!*+! .=%!#D*!/.2:,.:2%?!4/!
/=*6-! &-! .=%! .#()%\! .=%! +&-#)! /.2:,.:2%! 6#/! ,*8D2&/%7! *+! >NAN! -*-R=F72*$%-!
D2*.%&-/! #.*8/\! >WN! 6#.%2! 8*)%,:)%/! #-7! AWW! #.*8/! +2*8! .=%! D%D.&7%! #-7!
D=*/D=#.%!D&,5%7!+2*8!.=%!D%D.&7%!/*):.&*-!7:2&-$!.=%!,2F/.#))&[#.&*-?!'=%!/.2:,.:2%!
6#/!/*)9%7! .*!#! +&-#)! +2%%RL! +#,.*2!*+!AI?CCl!#-7!LR+#,.*2!*+!>P?CGl?!'=%!D2*.%&-!
6#/! +*:-7! .*! ,2F/.#))&[%! &-! #! 8*-*,)&-&,! ,2F/.#)! /F/.%8! D*//%//&-$! #! "A>! /D#,%!
$2*:D?!'=&/! &/! &-!,*-.2#/.! .*! .=%!#D*!/.2:,.:2%! .=#.!6#/! +*:-7! &-!#! .2&$*-#)!,2F/.#)!
/F/.%8!6&.=!"NG!/D#,%!$2*:D?!0.!#)/*!7&++%2/!+2*8!.=%!D2%9&*:/!/.2:,.:2%!*+!.=%!B2(C!
@HA!7*8#&-\!6=&,=!6#/!/*)9%7!&-!#!/D#,%!$2*:D!*+!"AA>?AM!V9%2#))\!.=%!%-.&2%!/F/.%8!
6#/!2%+&-%7!.*!28/7!&-!(*-7!)%-$.=!*+!W?W>S!s!#-7!.*!A?WNS!&-!(*-7!#-$)%?!
'=%! #/F88%.2&,! :-&.! *+! .=%! B2(C! @HA^U&,F,)&,! BCR>PQ4'J! ,*R,2F/.#)! /.2:,.:2%!
,*8D2&/%/! #! .*.#)! *+! .6*!B2(C!@HA!7*8#&-/!#-7! .6*!D%D.&7%/?!'=%! /.2:,.:2%/!#2%!
#22#-$%7!#/!7&8%2/!6&.=!%#,=!8*-*8%2!,*8D2&/&-$!#!D%D.&7%!*-!%#,=!,=#&-!*+!.=%!
B2(C!@HA!7*8#&-?! 0-.%2%/.&-$)F\! .=&/! &/! &-!,*-.2#/.! .*!.=%!,2F/.#)!/.2:,.:2%!*+!B2(C!
@HA^BCR>PQ4'J!/.2:,.:2%!&-!6=&,=!*-)F!*-%!D%D.&7%!6#/!(*:-7!.*!%#,=!B2(C!@HA!
7&8%2!7:%!.*!,2F/.#)!D#,5&-$!2%/.2#&#-./?!X&$?!S?C!7&/D)#F/!.=%!*9%2#))!#22#-$%8%-.!
*(/%29%7! D&,.*2&#))F?! '=#.! .=%! D2*.%&-! #//%8()%/! &-! 7&8%2&,! +*28! &/! #)/*! 6=#.! &/!
*(/%29%7! +*2! .=%! #D*! +*28! *+! B2(C! @HA! 7*8#&-! _>`! /:$$%/.&-$! .=#.! .=%! *9%2#))!
&'()*+,!=-!J46'!,+1CA3*4CD!/.2:,.:2%/!*+!B2(C!@HA!7*8#&-!
! %<=!
#22#-$%8%-.!*+!.=%!#D*!#-7!=*)*!+*28/!#2%!/&8&)#2?!0-!,*88*-!6&.=!.=%!/.2:,.:2%!*+!
.=%!#D*!+*28!#-7!.*!.=#.!*+!*.=%2!@HA!7*8#&-/\N!.=%!,*R,2F/.#)!/.2:,.:2%!%K=&(&.%7!
.=%! .FD&,#)! +*)7!6&.=!%#,=!8*-*8%2!,*8D2&/&-$!#!D#&2!*+!"R=%)&,%/! +)#-5&-$!%&.=%2!
/&7%!*+!#-.&RD#2#))%)!!R/=%%./?! ! 0-!,*88*-!.*!.=%!#D*!/.2:,.:2%!.=%!.6*!,=#&-/\!#2%!
8#7%!*+!.6*!"R=%)&,%/!_"4!#-7!"U`!#-7!+&9%!!R/.2#-7/\! )#(%)%7!!U\!!T\!!1\!!1p!#-7!
!J?! _/%%! X&$?S?A! +*2! 7%/&$-#.&*-/`! #-7! #! -:8(%2! *+! )**D! /.2:,.:2%/?! 4! ,%-.2%! *+!
&-9%2/&*-!2%)#.%/!.=%!.6*!,=#&-/?!!
!!!!!!!!!!!!!!!!!!!
!
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dOV;!!
!
!
&'()*+,!=-!J46'!,+1CA3*4CD!/.2:,.:2%/!*+!B2(C!@HA!7*8#&-!
! %=>!
<='*-"1'("2+0"%,*",0'(3+$'*
'=%!&-.%2+#,%!(%.6%%-!.=%!.6*!,=#&-/!&/!8#7%!(F!.=%!.6*!TR.%28&-#)!#)D=#!=%)&,%/!
_"!`!*+!.=%!.6*!,=#&-/\!/%%!X&$?S?P\!&-!#!/&7%!6#F/!#22#-$%8%-.!#/!*DD*/%7!.*!9&#!&./!
D%D.&7%R(&-7&-$! /&.%! &-! .=%! #D*! /.2:,.:2%?! '=%! &-.%2+#,%! &/! =%)7! .*$%.=%2!
D2%7*8&-#-.)F! (F! =F72*D=*(&,! &-.%2#,.&*-! 6=%2%(F! +*:2! D=%-F)#)#-&-%/!
_,*8D2&/&-$! .6*!"=%M>>! +2*8! .=%! #)D=#! =%)&,%/! #-7! .6*! "=%MWA! +2*8! .=%! )**D/`!
#-7! 0)%M>I! *-! (*.=! %-7/! *+! .=%! "4! =%)&K! +*28! .=%! ,*2%! *+! .=%! =F72*D=*(&,!
&-.%2#,.&*-?! V+! .=%/%! "=%M>>! &-! (*.=! ,=#&-/! &/! +*:-7! .*! (%! .=%! ,%-.2#)! &-.%2#,.&-$!
2%/&7:%!#))!.=%!*.=%2!.=2%%!D=%-F)#)#-&-%!#-7!&/*)%:,&-%!2%/&7:%/?!O*2%*9%2\!.=%!.6*!
"=%M>>! 2%/&7:%/! #2%! /%%-! .*! 8#5%! .6*! =F72*$%-! (*-7/! 6&.=! 4/-M>M! 9&#! .=%&2!
(#,5(*-%!,#2(*-F)!,#2(*-?!!
!!X&$:2%!S?PE!'=%!7&8%2&[#.&*-!&-.%2+#,%!+*28%7!(F!.=%!.6*!,=#&-/!*+!.=%!B2(C!@HA!7*8#&-?!'=%!+*:2!"=%!2%/&7:%/!*-!(*.=!,=#&-/_XM>>!*-!.=%!=%)&K!#-7!XMWA!*-!.=%!)**D`!#2%!/=*6-!.*!+*28!#!D2%7*8&-#-.)F!=F72*D=*(&,!7&8%2!&-.%2+#,%?!4)/*!/=*6-!#2%!.=%!+*:2!=F72*$%-!(*-7/!!
&'()*+,!=-!J46'!,+1CA3*4CD!/.2:,.:2%/!*+!B2(C!@HA!7*8#&-!
! %=%!
'=&/! /:$$%/./! .=#.! .=%! .6*! 2%/&7:%/! #! 5%F! 2*)%! &-! .=%! 7&8%2&[#.&*-! *+! B2(C! @HA!
7*8#&-?! 0-7%%7\! .=&/! =#/! (%%-! +*:-7! .=%! ,#/%! D2%9&*:/)FAM\IA! 6=%2%! B2(C! @HA!
7*8#&-! )#,5&-$! .=%/%! 2%/&7:%/! 6#/! +*:-7! .*! (%! 7%9*&7! *+! .=%&2! 7&8%2&[#.&*-!
D2*D%2.FR&?%?\!%K&/.!&-!8*-*8%2&,!+*28/?!477&.&*-#))F!#!D#&2!*+!=F72*$%-!(*-7/!%K&/.!
(%.6%%-! .=%! (#,5(*-%! ,#2(*-F)! *+! 42$MW>! *-! (*.=! ,=#&-/! #-7! .=%! /&7%! ,=#&-! *+!
4/-M>M?! ;#/.)F\! D*.%-.&#)! %)%,.2*/.#.&,! &-.%2#,.&*-! D#&2! %K&/./! (%.6%%-!
42$MW>^42$M>N!*-!(*.=!%-7/!*+! .=%!7&8%2?! b:7$&-$!(F! 2%/&7:%!(:2&%7! /:2+#,%!#2%!
+*2!7&8%2!+*28#.&*-\!.=%!+&9%!8*/.!&8D*2.#-.!2%/&7:%/!+*2!7&8%2&[#.&*-!#2%!;%:M>I!
_U@4E!T=#&-!4!f!S>?M>\!T=#&-!U!f>>A?M>`\!"=%M>>!_U@4\!T=#&-!4!f!NI?PA\!T=#&-!U!f!
NN?>G`\!B)-MWC!_T=#&-!4!fNN?A>\!T=#&-!U!f!NI?MI`\!42$MW>!_T=#&-!4!f!M>?>>\!T=#&-!U!
f!MW?MC`!#-7!4/-M>M!_T=#&-!4!f!IS?PG\!T=#&-!U!f!IS?AP`?!'=%!)#/.!.6*!2%/&7:%/!#2%!
#)/*! -*.&,%7! .*! D#2.&,&D#.%! .=%! 7&2%,.&*-#)! =F72*$%-! (*-7&-$! &-.%2#,.&*-?! X&$?S?S!
/=*6/! .=%!=&/.*$2#8/!*+! &-.%2+#,%! 2%/&7:%/!#,,*27&-$! .*! .=%&2!(:2&%7! /:2+#,%!#2%#!
7:2&-$!7&8%2!+*28#.&*-?!4/!.=%!=&/.*$2#8!/=*6/\!.=%!.6*!,=#&-/!#2%!/%%-!.*!8#5%!
.=%!7&8%2!6&.=!&7%-.&,#)!2%/&7:%/!#-7!.=%!2%/&7:%/!#2%!/=*6-!.*!8#5%!#!8*2%!*2!)%//!
&7%-.&,#)!,*-.2&(:.&*-\!&?%?\!.=%F!#2%!/F88%.2&,#)!7&8%2/?!
0
20
40
60
80
100
120
R4
90
L4
91
Y4
92
Q4
99
T5
00
R5
01
F5
02
T5
03
Q5
07
E5
10
F5
11
Q5
13
L5
14
N5
15
Residues on the dimer Interface
Bu
rrie
d S
urf
ac
e A
rea Chain A Chain B
!
X&$:2%!S?SE!!0-.%2+#,%!2%/&7:%/!*+!,=#&-!4!#-7!,=#&-!U!(F!.=%&2!(:2&%7!/:2+#,%!#2%#!&-!7&8%2!+*28#.&*-?!'=%!7&8%2!&/!/%%-!.*!(%!+*28%7!(F!&7%-.&,#)!2%/&7:%/!*-!.=%!.6*!,=#&-/!#-7!.=%!&7%-.&,#)! 2%/&7:%/! #2%! /%%-! .*!8#5%! #!8*2%! *2! )%//! &7%-.&,#)! ,*-.2&(:.&*-! #/! #//%//%7! (F!.=%&2!(:2&%7!/:2+#,%!#2%#?!
!
!
!
&'()*+,!=-!J46'!,+1CA3*4CD!/.2:,.:2%/!*+!B2(C!@HA!7*8#&-!
! %=7!
<='*5",-",8*",0'(+$0"%,*%3*0='*/'/0"-'*?"0=*456*CKF*-%1+",*
4/! /=*6-! &-! X&$?S?>W\! .=%! (&,F,)&,! D%D.&7%! &/! /%%-! .*!8#5%! #! -:8(%2! *+! =F72*$%-!
(*-7&-$! #-7! D*.%-.&#)! =F72*D=*(&,! &-.%2#,.&*-/?! '=%! &-.%2#,.&-$! 2%/&7:%/! *-! .=%!
D2*.%&-!#2%!)*,#.%7!*-!"4\!!1\!!1p\!4U!)**D/?!@D%,&+&,#))F!42$IGP!*-!"4!=%)&K!&/!/%%-!
.*!8#5%!.6*!=F72*$%-/!(*-7/!6&.=!&./!$:#-&7&-%!$2*:D!6&.=!.=%!(#,5(*-%!,#2(*-F)!
*+!B)FI!*+! .=%!(&,F,)&,!BCR>PQ4'J!D%D.&7%?!1N!*+! .=%!D%D.&7%! &/!#)/*!/%%-!.*!8#5%!
.=2%%!=F72*$%-!(*-7/E!9&#!&./!/&7%!,=#&-!TVVH!6&.=!.=%!(#,5(*-%/!#8&7%!*+!H&/ICS!
#-7!*-%!9&#!&./!(#,5(*-%!QH!6&.=!.=%!(#,5(*-%!TV!*+!'F2IPW?!QC!*+!.=%!D%D.&7%!&/!
#)/*! -*.&,%7! .*!8#5%! .=2%%! =F72*$%-! (*-7/! 9&#! &./! /&7%! ,=#&-! ,#2(*K#8&7%! $2*:D!
6&.=!(#,5(*-%!TV!*+!O%.ISM!#-7!TV!*+!0)%IPA?!JG!*+!.=%!D%D.&7%!&/!#)/*!-*.&,%7!.*!
+*28! .6*! =F72*$%-R(*-7&-$! &-.%2#,.&*-/!6&.=! .=%! 42$INA! (*.=! 9&#! &./! /&7%! ,=#&-!
#-7!(#,5(*-%!,#2(*-F)!$2*:D?!XA!*+!.=%!D%D.&7%!&/!/%%-!%-$:)+%7!(F!#!=F72*D=*(&,!
2%$&*-! 7%+&-%7! (F! 2%/&7:%/! ;%:IPG! #-7! ;%:IP>! &-7&,#.&-$! D*.%-.&#)! =F72*D=*(&,!
&-.%2#,.&*-/?!!
'=%!.6*!,=#&-/!*+!.=%!B2(C!@HA!7*8#&-!#2%!-*.&,%7!.*!&-.%2#,.!#)8*/.!&7%-.&,#))F!.*!
.=%&2!2%/D%,.&9%!D%D.&7%/?!0-!D#2.&,:)#2\!.=%!"0@4!#-#)F/&/!*+!(&-7&-$!/&.%!2%/&7:%/!&-!
.%28/! *+! .=%&2! (:2&%7! /:2+#,%! #2%#! :D*-! &-.%2#,.&*-! 6&.=! .=%! D%D.&7%/! /=*6/!
&7%-.&,#)! #8&-*! #,&7/! *-! (*.=! ,=#&-/! #2%! &-.%2#,.&-$! &-! &7%-.&,#)! +#/=&*-\! .=&/! &/!
(%,#:/%! &.! &/! #! /F88%.2&,#)! 7&8%2?! 4/! D%2! .=%! 2%/&7:%/!U@4! _&-!sA`\! .=%! +&9%!8*/.!
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0
10
20
30
40
50
60
70
80
R4
38
S4
60
R4
62
N4
63
V4
68
V4
77
K4
78
H4
79
Y4
80
L4
81
L4
83
S4
94
M4
95
D4
96
D4
97
I51
8
Binding site residues
Bu
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d s
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ac
e a
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Chain A Chain B
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