peroxisome proliferator-activated receptor pathway...

Peroxisome Proliferator-Activated Receptor Pathway GenePolymorphism Associated With Extent of Coronary Artery

Disease in Patients With Type 2 Diabetes in the BypassAngioplasty Revascularization Investigation 2 Diabetes Trial

Sharon Cresci, MD; Jun Wu, MD, MS; Michael A. Province, PhD; John A. Spertus, MD, MPH;Michael Steffes, MD, PhD; Janet B. McGill, MD; Edwin L. Alderman, MD; Maria Mori Brooks, PhD;

Sheryl F. Kelsey, PhD; Robert L. Frye, MD; Richard G. Bach, MD; on behalf of the BARI 2D Study Group

Background—Coronary artery disease (CAD) is the major cause of death in patients with type 2 diabetes mellitus. Althoughdemographic and clinical factors associated with extent of CAD in patients with diabetes mellitus have been described, geneticfactors have not. We hypothesized that genetic variation in peroxisome proliferator-activated receptor (PPAR) pathway genes,important in diabetes mellitus and atherosclerosis, would be associated with extent of CAD in patients with diabetes mellitus.

Methods and Results—We genotyped 1043 patients (702 white, 175 blacks) from the Bypass Angioplasty Revascular-ization Investigation 2 Diabetes (BARI 2D) genetic cohort for 3351 variants in 223 PPAR pathway genes using a customtargeted-genotyping array. Angiographic end points were determined by a core laboratory. In whites, a single variant(rs1503298) in TLL1 was significantly (P�5.5�10�6) associated with extent of CAD, defined as number of lesions withpercent diameter stenosis �20%, after stringent Bonferroni correction for all 3351 single nucleotide polymorphisms.This association was validated in the diabetic subgroups of 2 independent cohorts, the Translational ResearchInvestigating Underlying Disparities in Acute Myocardial Infarction Patients’ Health Status (TRIUMPH) post–myocardial infarction registry and the prospective Family Heart Study (FHS) of individuals at risk for CAD.TLL1rs1503298 was also significantly associated with extent of severe CAD (�70% diameter stenosis; P�3.7�10�2)and myocardial jeopardy index (P�8.7�10�4). In general linear regression modeling, TLL1rs1503298 explained morevariance of extent of CAD than the previously determined clinical factors.

Conclusions—We identified a variant in a single PPAR pathway gene, TLL1, that is associated with the extent of CADindependently of clinical predictors, specifically in patients with type 2 diabetes mellitus and CAD.

Clinical Trial Registration—URL: http://www.clinicaltrials.gov. Unique identifier: NCT00006305.(Circulation. 2011;124:1426-1434.)

Key Words: coronary artery disease � calcium � diabetes mellitus, type 2 � genetic variation� peroxisome proliferator-activated receptors � Tolloid-like metalloproteinases

Diabetes mellitus (DM) currently affects �17 millionpeople in the United States, and �1.6 million new cases

are diagnosed each year.1 Among persons with DM, coronaryatherosclerosis is highly prevalent and accounts for themajority of deaths.1 In patients with coronary artery disease(CAD), patients with DM have lower 10-year survival thanthose without DM,2 and the extent of CAD predicts mortal-ity.3 Atherosclerosis in patients with DM has an acceleratedphenotype, with more diffuse and extensive disease that

shows more rapid progression, suggesting a distinctive patho-genesis.4 The distinct pathogenesis of the accelerated athero-sclerosis observed among patients with DM is poorly under-stood,5 and the role of genetic factors is unknown.

Clinical Perspective on p 1434Bypass Angioplasty Revascularization Investigation 2 Di-

abetes (BARI 2D) was a multicenter, randomized clinical trialthat investigated the effect of different approaches to the

Received July 2, 2010; accepted July 26, 2011.From the Washington University School of Medicine, Department of Medicine, St. Louis, MO (S.C., J.W., M.A.P., J.B.M., R.G.B.); Saint Luke’s Mid

America Heart Institute and the University of Missouri–Kansas City (J.A.S.); University of Minnesota, Minneapolis (M.S.); Stanford University, Stanford,CA (E.L.A.); University of Pittsburgh, Pittsburgh, PA (M.M.B., S.F.K.); and Mayo Clinic, Rochester, MN (R.L.F.).

A complete list of the BARI 2D Study Group is provided in the Appendix in the online-only Data Supplement.Guest Editor for this article was Kari E. North, PhD.The online-only Data Supplement is available with this article at http://circ.ahajournals.org/lookup/suppl/doi:10.1161/CIRCULATIONAHA.

111.029173/-/DC1.Correspondence to Sharon Cresci, MD, Cardiovascular Division, Washington University School of Medicine, 660 S Euclid Ave, Campus Box 8086,

St. Louis, MO 63110-1093. E-mail [email protected]© 2011 American Heart Association, Inc.

Circulation is available at http://circ.ahajournals.org DOI: 10.1161/CIRCULATIONAHA.111.029173

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treatment of both CAD and DM on long-term outcomes inpatients with type 2 DM.6,7 All patients in BARI 2D had DMand CAD suitable for, but not requiring, revascularization.Baseline extent of CAD in BARI 2D was defined angio-graphically and quantified by a core laboratory. Clinicalfactors contributing to extent of CAD among patients inBARI 2D, defined as the number of coronary lesions �20%diameter stenosis (DS), were recently reported;8 however, thetotal variance in extent of CAD explained by baseline clinicalfactors was �10%,8 providing an important rationale forexamining the putative role of genetic factors.

Peroxisome-proliferator activated receptor (PPAR) path-way genes are involved in cellular processes relevant to bothCAD and DM. Master regulators of lipid and glucose homeo-stasis, cardiac energy metabolism, vascular inflammation,and cell differentiation, PPARs have been implicated in thedevelopment and progression of both type 2 DM and athero-sclerosis in animal studies.9–12 We therefore hypothesizedthat investigating genetic variation within the PPAR genepathway would identify novel genes involved in diabeticatherosclerosis.

Using a custom PPAR pathway gene single nucleotidepolymorphism (SNP) microarray containing 3351 SNPs in223 PPAR pathway genes, we investigated genetic associa-tions of PPAR pathway genes with extent of CAD amongpatients with DM in the BARI 2D trial. We then sought tovalidate the discovered associations in 2 additional well-phe-notyped cohorts of patients with CAD and DM.

MethodsBypass Angioplasty RevascularizationInvestigation 2 Diabetes (BARI 2D) Cohort andBaseline Phenotypic DataEligibility criteria for BARI 2D have previously been described.6,7

Patients with type 2 DM having angiographically documented CADinvolving at least 1 major epicardial coronary artery (�50% DS witha positive stress test or �70% DS with classic angina) suitable fortreatment with either medical therapy or coronary revascularizationwere eligible for inclusion.6,7 Exclusion criteria included significantleft main disease (�50% DS), class III or IV congestive heart failure,and coronary revascularization within the preceding 12 months. Allpatients underwent coronary angiography, and the angiograms werereviewed by a central core laboratory (Stanford University) with astandard protocol used in previous trials and masked to patientrandomization or intended revascularization strategy.7,8 This assess-ment included quantifying the number and percent DS of each lesion,its location in the coronary tree using the BARI modification of theCoronary Artery Surgery Study map, and the lesion morphologyaccording to the American College of Cardiology/American HeartAssociation classification scheme.8 Percent DS was the ratio of theminimum diameter divided by the reference diameter (the mean ofthe proximal and distal diameter of the normal-appearing arteryadjacent to the lesion). All lesions �20% DS were counted. Inaddition to number of lesions, total myocardial jeopardy index wascalculated. The myocardial jeopardy index was calculated as thepercentage of the myocardium that was jeopardized by lesions�50% DS in any of the 3 main coronary arteries or theirbranches.8,13 In accordance with the published analysis of clinicalpredictors of extent of CAD in BARI 2D,8 number of coronarylesions �20% DS was selected to represent the overall extent ofatherosclerotic CAD; additional angiographic variables were in-cluded to represent the extent of severe atherosclerotic CAD (numberof lesions �70% DS and myocardial jeopardy index).

Bypass Angioplasty RevascularizationInvestigation 2 Diabetes (BARI 2D)Genetic CohortA total of 2368 patients were enrolled in BARI 2D from January2001 through March 2005. Of these, 1439 BARI 2D patientsconsented to genetic analysis; 1072 genomic samples (702 whites,175 blacks) were available for genotyping (353 samples from Brazilwere not available because of international restrictions on DNAshipment). To determine whether the genetic cohort was represen-tative of the entire BARI 2D cohort, clinical covariates and associ-ation with number of lesions �20% DS were determined for theentire genetic cohort (not stratified by race). Using the same clinicalcovariates and the same analytic strategy (variable entry and reten-tion criteria; entry P�0.15, retain P�0.05; age, and sex includedregardless of statistical significance) used in the entire cohort,8 wedetermined the magnitude of individual variables associated withextent of CAD (presented as semipartial correlation coefficients).

Validation Cohorts

Translational Research Investigating UnderlyingDisparities in Acute Myocardial Infarction Patients’Health Status StudyTranslational Research Investigating Underlying Disparities inAcute Myocardial Infarction Patients’ Health Status (TRIUMPH)was a large, prospective, observational cohort study of consecutivepatients with acute myocardial infarction presenting to 24 UShospitals from April 2005 to December 2008.14 Myocardial infarc-tion was diagnosed with contemporary definitions,15 and all patientshad an elevated troponin blood test. Thirty-one percent of TRIUMPHpatients had DM on enrollment. Extent of CAD was determined byangiography and defined as the number of vessels with �20% DS.We genotyped 386 whites using the PPAR pathway custom arrayconstituting the genetic cohort for the present analysis. The studywas approved by the Institutional Review boards of all participatinginstitutions, and written informed consent was provided by eachparticipant. A separate consent form for the acquisition of blood forgenetic analysis was signed by each participant.

Family Heart StudyThe Family Heart Study (FHS) has been described in detail.16,17

Briefly, adults (45 to 69 years of age) were recruited from 1 of 3studies: the Framingham study, the Utah study, and 2 AtherosclerosisRisk in Communities sites. Subjects and their family members wereeither randomly selected or selected because they had a high relativerisk of coronary heart disease.17 Of these, 14% had DM. The cardiaccomputed tomography subset of FHS (the FHS Subclinical Athero-sclerosis Network) recruited patients and their family memberspreviously enrolled in FHS who had been genotyped by genome-wide association study to undergo cardiac computed tomography todetermine the extent of coronary artery and aortic calcification.16,17

Coronary artery calcification was determined by a core laboratory(Wake Forest University Health Sciences, Winston Salem, NC) aspreviously described.16,17 In brief, 2 sequential scans were performed1 minute apart; the amount of calcium was quantified by theAgatston scoring method adjusted for slice thickness; and the totalcoronary artery calcification score was calculated as the sum of theAgatston scores from each scan and then averaged. We genotyped974 whites with the Illumina 550K SNP array.

Genotyping and Custom ArrayDNA was isolated and extracted with the Puregene genomic DNApurification kit (Gentra, Minneapolis, MN). DNA (4 �g) wasgenotyped using a custom-designed PPAR pathway–targeted geno-typing 3K array containing 3351 SNPs in 223 genes within the PPARpathway and 100 SNPs, allowing identification of ethnic origin bymapping by admixture linkage disequilibrium (Affymetrix, SantaClara, CA; Table I in the online-only Data Supplement).18

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Method of Selection of Genes on Custom ArrayThe PPAR pathway genes were selected if they met 1 of 2 criteria:were identified as a PPAR pathway gene in the published literatureor showed �2-fold upregulation or downregulation in in vitro geneexpression profiling experiments performed with mouse heartsoverexpressing PPAR� compared with nontransgenic littermates(data graciously provided by Dr Daniel P. Kelly, Burnham Institutefor Medical Research, Orlando, FL).

Method of Selection of Single NucleotidePolymorphisms on Custom ArrayThe SNPs were chosen from HapMap data. The projected popula-tions selected for tagging were Africans and whites, with a biastoward white coverage. A tagging SNP approach (from 5 kbupstream of the gene to 5 kb downstream of the gene; minor allelefrequency of �10% in white and black populations; the method ofCarlson et al19 was used to select tagging SNPs; r2 �0.8 required)was used. If a tagging SNP was in a large bin (containing �5 SNPswith r2 �0.8), we included 2 tagging SNPs on the array to ensuremaximal data acquisition (although genotyping only 1 tagging SNPis highly efficient, if it fails to genotype, a large amount of data couldpotentially be lost). In addition to the tagging SNPs, the array alsoincludes all nonsynonymous coding SNPs in each gene (regardless ofminor allele frequency). The SNP coverage provided by the finalpanel was 8500/�10 000 whites and 7000/�11 000 Yorubans.

Genotyping Quality Control DataData completeness was 99.64% and repeatability was 100%. Toensure high-quality data and to minimize false-positive results,filtering criteria were set as follows: genotype call rate �0.80 perSNP, minor allele frequency �0.01, and P value for Hardy-Weinberg equilibrium test �0.0001. Using the PLINK analysisprogram (version 1.06), we identified 5 white subjects whosereported sex did not match the sex estimated from the X chromosomedata. These 5 samples were excluded from further analysis. Clusteranalysis implemented in PLINK was used for screening any evidenceof subtle population stratifications based on pairwise identity-by-state sharing distance among all possible pairs of the SNPs. Acrossthe samples of the BARI 2D genetic cohort, 4 well-separatedsubgroups correlated with self-reported ethnic groups, and the 2major groups of blacks and whites were clearly distinguished. Inblacks, no further population stratification was detected according tomultidimensional scaling plots (Figure I in the online-only DataSupplement). In whites, subtle clustering was noted; we thereforeestimated 10 principal components using Eigenstrat.

Statistical Methods

Clinical CovariatesThe primary end point for our analysis was number of lesions �20%DS documented on the coronary angiogram. Myocardial jeopardyindex and number of lesions �70% DS were also determined forvariant(s) achieving significance in replication cohorts. Number oflesions and myocardial jeopardy index were evaluated as continuousvariables, with kernel density estimators used to plot their overalldistributions. Continuous variables were compared by Student t testsor Wilcoxon tests (depending on distributional properties); categor-ical variables were compared by �2 tests. Stepwise linear regressionwas used to identify baseline factors associated with number oflesions (log transformed) and myocardial jeopardy index.

Single Nucleotide Polymorphism AssociationTo prevent confounding from racial admixture, we performed ouranalyses separately in our 2 largest racial groups (whites, n�702;blacks, n�175). Single SNP associations for the number of lesions�20% DS were tested in general linear regression analyses using anadditive genetic model. Age, sex, body mass index, and priorrevascularization were included in the model as covariates. Signifi-cance level was 1.5�10�5 using stringent Bonferroni correction forall 3351 SNPs.

ValidationWe validated putative statistically significant associations in the 2separate cohorts of patients systematically assessed for extent ofCAD described above, TRIUMPH and FHS. Because the significantassociation was observed in white BARI 2D subjects, white TRIUMPHand FHS subjects were used for validation. None of the subjects wererelated in TRIUMPH. Because FHS had related subjects, we usedmixed models to take family structure into account. Values ofP�0.05 were considered statistically significant for validation anal-yses. Statistical analyses were performed with SAS 9.1 (SASInstitute Inc, Cary, NC), and plots were generated by R 2.3.1(CRAN, the comprehensive R archive network).

ResultsThe Bypass Angioplasty RevascularizationInvestigation 2 Diabetes (BARI 2D)Genetics CohortThe baseline characteristics of the patients making up thegenetic cohort of BARI 2D were similar to those of the entiregroup (Table). The primary end point representing the extentof CAD (number of coronary lesions �20% DS) was thesame in the BARI 2D genetic cohort (mean number ofcoronary lesions �20% DS � 4.6�2.2) and in the entireBARI 2D cohort (mean number of coronary lesions �20%DS � 4.6�2.3). To further confirm that the extent of CAD inthe genetics subgroup was representative of the entire cohort,the magnitude of association between clinical covariates andnumber of coronary lesions �20% DS was compared be-tween the 2 groups. As shown in Figure 1, individual clinicalcovariates in the BARI 2D genetic cohort showed correla-tions with the extent of CAD similar to those of the entireBARI 2D cohort. Similar to the entire BARI 2D cohort,female sex, black race, higher body mass index, and higher30-second pulse were associated with less extensive CAD,whereas older age, longer duration of DM, hypertension, andhigher tissue-type plasminogen activator antigen levels wereassociated with more extensive CAD.

Peroxisome Proliferator-Activated ReceptorPathway Single Nucleotide PolymorphismAssociations With Extent of CoronaryArtery DiseaseTo prevent confounding from racial admixture, we performedour analyses separately in our 2 largest racial groups (whites,n�702; blacks, n�175). In white BARI 2D subjects, singleSNP analysis identified 1 SNP (rs1503298) that was highlysignificantly associated (P�5.5�10�6) with number of cor-onary lesions �20% DS (Figure 2), even after stringentBonferroni correction for all 3351 SNPs. This SNP is locatedin intron 12 of the gene that encodes Tolloid-like 1 (TLL1), ametalloproteinase that regulates bone morphogeneticprotein-2 (BMP-2) and transforming growth factor-�. Thisassociation remained significant after inclusion of all baselineclinical covariates and principal components in the model.The mean�SE residual of number of lesions �20% by TLL1rs1503298 genotype after adjustment for age, sex, and bodymass index in white BARI 2D subjects is shown in Figure 3A.To put these data into a clinically relevant context, an averageBARI 2D subject (a 63-year-old man with a body mass indexof 30 kg/m2) with the TT genotype would have 4.43 coronarylesions �20% DS; with the CT genotype, 5.02 coronary lesions

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Table. Baseline Characteristics of the Entire Bypass Angioplasty Revascularization Investigation 2 Diabetes (BARI 2D) Cohort, theBARI 2D Genetic Cohort, and the White Subgroups of BARI 2D, Translational Research Investigating Underlying Disparities in AcuteMyocardial Infarction Patients’ Health Status (TRIUMPH), and Family Heart Study (FHS)

All Patients(n�2368)

Genetics Cohort(n�1072)

Genetics CohortWhites (n�702)

FHS DM Whites(n�139)

TRIUMPH DMWhites (n�100)

Age, mean (SD), y 62.4 (8.9) 63.1 (9.2) 64.3 (8.8) 63.6 (11.3) 58.8 (11.5)

Male, % 70.4 69.4 75.2 42.4 67.0

Race, %

White 70.4 66.6 100.0 100.0 100.0

Black 17 17.1 0 0 0

Asian 4.2 5.5 0 0 0

Indian/Native American 4.3 0.1 0 0 0

Other 4.1 5.9 0 0 0

Hispanic ethnicity 12.5 14.0 5.1

Region of world, %

United States 63.3 76.1 75.5 100.0 100.0

Canada 14.9 15.3 17.2 0 0

Mexico 3.6 4.0 0 0 0

Czechoslovakia 3.2 4.6 7.3 0 0

BMI categories, %

Normal or underweight, �25 kg/m2 9.7 7.9 5.1 23.0 11.1

Overweight, 25–�30 kg/m2 34 30.9 28.8 41.7 26.3

Class 1 obese, 30–�35 kg/m2 32.1 31.8 35.3 24.5 35.4

Class 2 obese, 35–�40 kg/m2 15.3 17.1 19.4 7.9 11.1

Class 3 obese, �40 kg/m2 9 12.2 11.6 2.9 16.2

Blood pressure �130/80 mm Hg,% 52.4 48.8 45.1 47.5 79.0

History of hypertension, % 82.5 81.9 81.6 53.2 77.0

History of myocardial infarction, % 32 29.5 30.0 12.6 24.0

History of congestive heart failure, % 6.6 8.4 8.9 0.7 13.0

Anginal status, %

None 17.9 21.1 22.7 87.8 27.0

Anginal equivalents only 21.4 25.2 26.4

Stable CCS1 14.3 14.4 14.7

Stable CCS2 28.8 24.5 23.5

Stable CCS3 7.5 5.2 5.3

Stable CCS4 1.2 0.7 0.7

Unstable angina 9.5 8.9 6.8

Duration of DM, %

�5 y 33.3 32.1 32.1

5–�10 y 23.5 23.1 22.9

10–�20 y 29.2 30.4 30.1

�20 y 14.1 14.3 14.6

History of insulin use, % 29.3 29.0 27.4

Glycemia measurements, %

HbA1c �7.0% 41.7 45.5 48.0 47.4

7.0%�HbA1c�8.0% 25.3 27.9 23.6 12.6

HbA1c �8.0% 33 26.6 28.5 40.0

Total cholesterol �200 mg/dL, % 19.0 18.5 16.6 29.6 34.0

Triglycerides �200 mg/dL, % 31.0 32.3 34.8 27.4 41.0

HDL �40 mg/dL for men or �50 mg/dL for women, % 72.4 74.4 78.8 44.4 68.0

LDL �100 mg/dL, % 40.5 40.4 36.0 55.0 33.0

DM indicates diabetes mellitus; BMI, body mass index; CCS, Canadian Cardiovascular Society; HbA1c, hemoglobin A1c; HDL, high-density lipoprotein; and LDL,low-density lipoprotein.




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�20% DS; and with the CC genotype, 5.46 coronary lesions�20% DS (Figure 3B). Of note, in general linear regressionmodeling, this SNP explained more variance of the phenotype(number of coronary lesions �20% DS) than the previouslydetermined clinical factors. TLL1 rs1503298 explained 2.75%of the variance compared with sex (1.61%), age (0.12%), andbody mass index (0.01%). Subjects with the TLL1 rs1503298CT genotype had 22% more coronary lesions �20% DScompared with those with the TT genotype, and those withthe CC genotype had 37% more coronary lesions �20% DS.

In the smaller subgroup of black BARI 2D subjects(n�175), no SNP was found to be significantly associatedwith number of coronary lesions �20% DS after stringentBonferroni correction for all 3351 SNPs. This included TLL1rs1503298 (P�0.25).

ValidationFor validation, the genetic association observed in BARI 2Dwas tested in both the overall group and the diabetic sub-groups of 2 independent cohorts of patients with CAD,TRIUMPH and FHS. These validation cohorts were chosenbecause both TRIUMPH and FHS were independent popula-tions with detailed information on extent of CAD by quanti-

tative imaging studies, both had detailed information onsubjects with and without carefully defined DM, both hadextensive phenotypic data to allow consistent adjustment forcovariates, and both were genotyped for relevant poly-morphisms. Validation analyses were performed on (white)subjects with and without DM within these same cohorts toobtain insight into whether the association was specific toindividuals with DM.

When the same model was applied in TRIUMPH with theidentical SNPs used in BARI 2D, a significant associationwith extent of CAD was selectively demonstrated for TLL1rs1503298 among patients with DM (n�98; P�3.3�10�2)but not in the overall cohort (n�386; P�1.8�10�1). Acongruent trend was found in FHS with the use of a lesssensitive measure of CAD extent. The association betweenrs1503298 and extent of CAD defined by coronary calciumscore was demonstrated selectively in FHS individuals withDM (n�139; P�8.5�10�2) but did not replicate in the largerFHS cohort (n�974; P�5.7�10�1).

Associations With Severe Coronary Artery DiseaseWe also investigated whether the TLL1rs1503298 variant wasassociated with the extent of severe CAD and myocardial

Figure 1. Comparison of clinical covariates associated with number of lesions �20% in the Bypass Angioplasty RevascularizationInvestigation 2 Diabetes (BARI 2D) genetic cohort (right) compared with the entire BARI 2D cohort (left). DM indicates diabetes mellitus;ABI, ankle-brachial index; and t-PA, tissue-type plasminogen activator.

Figure 2. Results of tests for a trend inthe association between number oflesions �20% and each single nucleo-tide polymorphism on a custom chip inwhites in Bypass Angioplasty Revascu-larization Investigation 2 Diabetes (BARI2D). Red line depicts the threshold forstatistical significance after Bonferronicorrection for multiple comparisons.




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jeopardy index in BARI 2D, variables previously associatedwith mortality in other studies.3,13 TLL1 rs1503298 wassignificantly associated with both number of coronary lesions�70% DS (P�3.7�10�2) and myocardial jeopardy index(P�8.7�10�4; Figure 4).

DiscussionUsing a gene pathway microarray approach, we have identi-fied a novel PPAR pathway genetic polymorphism that issignificantly associated with extent of CAD in patients withDM. The TLL1 rs1503298 variant, located in intron 12 ofTLL1, showed associations with rigorous and objectivelyderived measures of atherosclerotic coronary disease in BARI2D and explained more variance of the phenotype than thepreviously determined clinical factors. The association ofextent of CAD observed with TLL1 rs1503298 in BARI 2Dwas validated by replication in the diabetic patients in 2independent populations, TRIUMPH and FHS.

The association of TLL1 rs1503298 with extent of CADwas observed among white patients with type 2 DM in theBARI 2D trial, in whom clinically stable CAD was definedand quantified by core laboratory interpretation of coronaryangiograms. This association was validated by replication inthe white diabetic subgroups of 2 independent populationswith CAD: the TRIUMPH cohort, in whom CAD in patientswith acute myocardial infarction was defined angiographi-cally, and the FHS cohort, in whom individuals at high risk ofCAD had their extent of coronary artery calcification deter-

mined by computed tomography scanning. The observationthat this variant was reproducibly associated with extent ofdisease quantified by disparate methods among individualswith disparate clinical manifestations supports a potential rolefor this genetic polymorphism in the pathogenesis of diabeticatherosclerosis. Further reinforcing the clinical relevance ofthe association between this SNP and CAD in patients withDM, the TLL1 rs1503298 polymorphism showed strongassociations not only with the primary end point of number oflesions �20% DS but also with number of angiographicallysevere (�70% DS) lesions and with myocardial jeopardyindex, a semiquantitative method used to estimate the amountof potential myocardial ischemia attributable to the locationand severity of coronary lesions in an individual; thesemeasures of extent of severe CAD have previously beenshown to correlate with prognosis in patients with CAD.3,13

To the best of our knowledge, this is the first demonstrationof a significant association of genetic variation specificallywith extent of the atherosclerotic disease that develops amongpatients with DM, in which atherosclerosis has been known todisplay a distinctively aggressive phenotype.20–22

The observation of an association between extent of CADin patients with DM and this particular gene in the PPARpathway–regulated processes is noteworthy. TLL1 encodes aprotein, Tolloid-like 1 (TLL1), that has been identified withinthe cascade of cellular processes related to vascular inflam-mation and calcification. Because vascular calcification is aprominent feature of the phenotype of diabetic atherosclerosis,23

genetic variability in TLL1 may have strong biologicalplausibility as a contributor to its pathogenesis.23 TLLI is ametalloproteinase that cleaves the BMP-2 antagonists Chor-

Figure 3. A, Mean (�SE) residual of number of lesions �20%by TLL1 rs1503298 genotype after adjustment for age, sex, andbody mass index (BMI) in white Bypass Angioplasty Revascular-ization Investigation 2 Diabetes (BARI 2D) subjects. B, Numberof lesions �20% by genotype for the average BARI 2D subject(a 63-year-old man with a BMI of 30 kg/m2).

Figure 4. Mean (�SE) residual of number of lesions �70% (A)and myocardial jeopardy index (MJI; B) by TLL1 rs1503298 ge-notype after adjustment for age, sex, and body mass index inwhite Bypass Angioplasty Revascularization Investigation 2 Dia-betes (BARI 2D) subjects.




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din and gremlin, thereby upregulating BMP-2/4 pathwaygenes that promote inflammation and extracellular matrixneogenesis.24,25 BMP-2 itself is an important mediator oftissue calcification, and endothelial BMP-2 expression can beupregulated by vascular oxidative stress, intravascular pres-sure, and elevated glucose.26–29 BMP-2 appears to play acritical role in programming the phenotype of the calcifyingvascular cell, the mural cell type that directs osteogenicmineralization in the vessel wall.24,25,27,30–32 Moreover, TLL1is also a member of the BMP-1–related activators of theprocollagen C-proteinase enhancer.33,34 Because TLL1 isat the intersection of the BMP-2/4 and frizzled-relatedprotein-2 signals that drive collagen deposition, TLL1 isalso likely to be a critical regulator of collagenous matrixdeposition, a hallmark of robust calcification processes incardiovascular tissues and in bone.33,34 BMP-2 is upregu-lated in human atherosclerotic plaques26,35 and has beenidentified as a key multifunctional regulator of vascularcalcium accrual in atherosclerosis and diabetic arterioscle-rosis.36,37 Thus, TLL1 has a direct link to fundamentalcellular processes involved in vascular calcification, awidely recognized feature of atherosclerosis that is char-acteristically increased in patients with DM compared withthose without DM.4,20 –22

Previous genetic association studies have observed associ-ations between polymorphisms of PPAR pathway genes andthe risk of developing type 2 DM, obesity, insulin resistance,abnormal lipid profiles, and cardiovascular disease in Euro-pean and American populations (reviewed elsewhere9,38). Inseparate candidate gene studies, an SNP in intron 7 of thePPAR� gene (PPARA IVS7 2498)39 and 2 SNPs in PPARG(the gene encoding PPAR�) were associated with increasedrisk of myocardial infarction in patients with type 2 DM.40

Also using a candidate gene approach, Regieli et al41 reportedan association between the Pro12Ala variant (rs1801282) ofPPARG and both angiographic extent of CAD and 10-yearrisk of ischemic events, including death, among 679 partici-pants in the Regression Growth Evaluation Statin Study(REGRESS) without differentiation of result by diabeticstatus. This association was not confirmed in other studies.42

Of note, in the present analysis, the IVS7 2498 SNP inPPARA and the Pro12Ala polymorphism in PPARG (bothpresent on the PPAR pathway array used) were not identifiedas variants with a significant association with extent of CADin the BARI 2D cohort.

Our findings should be considered in the context ofseveral potential limitations. First, to prevent confounding fromracial admixture, we performed analyses in the largest racialgroups (whites and black) separately. The association betweenTLL1rs1503298 and extent of CAD was observed among whitepatients with DM. Similar analyses did not confirm an associa-tion between TLL1 and extent of CAD among black participantsin BARI 2D, although the smaller sample size may have limitedthe power to detect a significant relationship if present, or theremay be different patterns of linkage disequilibrium betweenTLL1 rs1503298 and the causal variant in different ethnicgroups. Our findings therefore cannot be extrapolated to otherracial groups and should be examined independently in ade-quately powered, racially characterized cohorts, particularly

given the burden of DM and CAD in black and Hispanicpatients. In addition, this study used the genetic cohort of BARI2D, and although the genetic cohort had baseline characteristicssimilar to those of the overall BARI 2D cohort, selection bias ispossible. However, because patients (and their treating physi-cians) were unaware of their genetic code, it is unlikely that therewas a direct association between genotype and participation inthe genetic cohort of BARI 2D to make selection bias signifi-cantly problematic. Furthermore, it should be noted that diabeticpatients with the most extensive, or unstable, CAD for whomimmediate revascularization was considered clinically indicatedwere excluded from BARI 2D by design. Therefore, the ob-served association has not been tested in this potentially impor-tant subgroup of patients with DM and CAD. Finally, it shouldbe noted that the mechanisms of action of TLL1 could poten-tially be via a pathway other than PPAR. Without furtherconfirmation, caution is warranted in attributing the observedassociation to a direct or indirect effect of PPAR activation.

ConclusionsUsing a gene pathway microarray approach, we identified andvalidated a novel PPAR pathway gene variant, TLL1 rs1503298,that is significantly associated with extent of CAD specifically inwhite patients with DM. The reproducibility of the observedassociation across populations, despite varied clinical manifes-tations of CAD and varied methods of quantifying the extent ofatherosclerosis, underscores its potential importance and rele-vance to the fundamental pathophysiology of diabetic athero-sclerosis. Moreover, the physiological pathways affected by thisgenetic variant may provide novel targets for further investiga-tion and therapeutic intervention to address the accelerated rateof progression and the high risk of adverse events associatedwith CAD in patients with DM.

AcknowledgmentsWe would like to thank Dr Dwight A. Towler for critical review ofthis manuscript.

Sources of FundingBARI 2D is funded by the National Heart, Lung, and Blood Instituteand the National Institute of Diabetes and Digestive and KidneyDiseases (U01 HL061744, U01 HL061746, U01 HL061748, andU01 HL063804). Significant supplemental funding is provided byGlaxoSmithKline, Collegeville, PA; Bristol-Myers Squibb MedicalImaging, Inc, North Billerica, MA; Astellas Pharma US, Inc,Deerfield, IL; Merck & Co, Inc, Whitehouse Station, NJ; AbbottLaboratories, Inc, Abbott Park, IL; and Pfizer, Inc, New York, NY.Generous support is given by Abbott Laboratories Ltd, MediSenseProducts, Mississauga, ON, Canada; Bayer Diagnostics, Tarrytown,NY; Becton, Dickinson and Co, Franklin Lakes, NJ; J.R. CarlsonLabs, Arlington Heights, IL; Centocor, Inc, Malvern, PA; Eli Lillyand Co, Indianapolis, IN; LipoScience, Inc, Raleigh, NC; MerckSante, Lyon, France; Novartis Pharmaceuticals Corp, East Hanover,NJ; and Novo Nordisk, Inc, Princeton, NJ. Dr Cresci is funded byNational Institutes of Health (NIH) R21HL089681; NIH SpecializedCenter for Clinically-Oriented Research in Cardiac Dysfunction andDisease P50 HL077113, P60 DK20579; and The Longer LifeFoundation. The content is solely the responsibility of the authorsand does not necessarily represent the official views of the NationalHeart, Lung, and Blood Institute, the National Institute of Diabetesand Digestive and Kidney Diseases, or the NIH.




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DisclosuresNone.

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CLINICAL PERSPECTIVEIn patients with diabetes mellitus, atherosclerosis is more extensive and rapidly progressive. The reasons for this are notknown but may relate in part to genetic variation that influences vascular disease severity. Using microarray technologyto interrogate �3000 tagged single nucleotide polymorphism markers of peroxisome proliferator-activated receptorpathway genes, we have discovered a polymorphism in the TLL1 gene that is significantly associated with angiographicextent of coronary artery disease among patients with type 2 diabetes mellitus. This genetic polymorphism explains morevariance of the phenotype than previously determined clinical factors. This association was initially observed in whitepatients with type 2 diabetes mellitus in the Bypass Angioplasty Revascularization Investigation 2 Diabetes (BARI 2D)trial and then validated specifically in the diabetic subgroups of 2 other independent white patient cohorts withquantitatively coronary imaging. TLL1 encodes a metalloproteinase that regulates procollagen processing and themetabolism of inhibitors of bone morphogenetic proteins involved with atherosclerotic calcification. These observationsidentify a novel putative genetic contributor to the biology of diabetic coronary atherosclerosis and suggest that targetingthe TLL1/bone morphogenetic proteins pathway may afford specific therapeutic intervention for diabetic vascular disease.




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G. BachMcGill, Edwin L. Alderman, Maria Mori Brooks, Sheryl F. Kelsey, Robert L. Frye and Richard

Sharon Cresci, Jun Wu, Michael A. Province, John A. Spertus, Michael Steffes, Janet B.Angioplasty Revascularization Investigation 2 Diabetes Trial

With Extent of Coronary Artery Disease in Patients With Type 2 Diabetes in the Bypass Peroxisome Proliferator-Activated Receptor Pathway Gene Polymorphism Associated

Print ISSN: 0009-7322. Online ISSN: 1524-4539 Copyright © 2011 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Circulation doi: 10.1161/CIRCULATIONAHA.111.029173

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SUPPLEMENTAL MATERIAL

Appendix A. List of BARI 2D investigators

Supplemental Tables:

Table S1. SNPs on custom microarray.

External Id Chromosome Position

(bp)

rs10001430 4 149661719

rs1000251 10 70832692

rs10004472 4 149456789

rs10008978 4 158122734

rs10011050 4 167358281

rs10015602 4 167213076

rs10018177 4 167377929

rs10020847 4 54994062

rs1002424 5 40803154

rs10025830 4 167184975

rs10029166 4 177996946

rs10032020 4 149375634

rs10034661 4 120601688

rs1003483 11 2124119

rs10041520 5 142756877

rs10044342 5 88214439

rs10046869 9 74430685

rs10047514 12 61824389

rs10049682 4 167302186

rs10051894 5 149140178

rs10052957 5 142766894

rs10053664 5 40821568

rs10058792 5 92953474

rs1007542 15 56629956

rs1007543 15 56627742

rs10080122 5 149099034

rs10083386 14 74417338

rs10083847 17 10178510

rs1008673 22 24318567

rs10099756 8 82562557

rs10100904 8 19871222

rs10109480 8 82552799

rs1011024 7 98842052

rs10113 19 51804488

rs1011300 12 109807050

rs10116811 9 74449856

rs1012543 5 149157138

rs10127480 1 213232818

rs1013078 9 74482835

rs10131667 14 75984250

rs10134248 14 76018615

rs10137185 14 63845529

rs10137295 14 75998525

rs10137303 14 95797755

rs10142318 14 63674034

rs10147171 14 95797627

rs10152719 15 58901949

rs10156070 7 45701808

rs10158279 1 65745717

rs10162630 15 58872020

rs10170546 2 178074297

rs1017713 11 75177100

rs1018139 4 167205606

rs10181778 2 227439742

rs10196915 2 178013810

rs1019974 15 98037650

rs1020285 4 158197382

rs10205923 2 227440062

rs1020730 15 58835870

rs10212213 3 24256457

rs10239118 7 128962563

rs10249970 7 94873563

rs10254081 7 20216

rs1025649 1 213541497

rs1025650 1 213541407

rs1027478 2 47301677

rs10283151 8 19866974

rs1028584 20 42484395

rs1030847 1 213429112

rs1030854 1 213512626

rs1035550 16 85160208

rs1038071 5 149103348

rs10408374 19 7078294

rs10408844 19 7195884

rs10409959 19 17468175

rs10411667 19 7124992

rs10416429 19 7181438

rs10417922 19 17476609

rs10420008 19 7185575

rs1042311 22 44948299

rs10423221 19 17453844

rs10424224 19 7191481

rs10425868 19 7186947

rs10426094 19 7156240

rs10426384 19 55489869

rs1042713 5 148186633

rs1042714 5 148186666

rs1042718 5 148187110

rs1042838 11 100438622

rs10429164 7 79885213

rs10431795 15 58634475

rs10432782 21 31958262

rs10434100 4 149645412

rs10437675 11 103303351

rs10442683 1 213116428

rs1044471 12 1767217

rs1046088 22 39898883

rs10462335 5 88123960

rs1046248 14 95773237

rs10463410 5 148193103

rs10465543 1 22879524

rs10476930 5 149519518

rs10482633 5 142730726

rs10482672 5 142672726

rs10484922 6 152224431

rs10492952 1 213398496

rs10492957 1 213513126

rs10493380 1 65758138

rs10494337 1 156963203

rs10495038 1 213555987

rs10495750 2 24906096

rs10496195 2 74986587

rs10496196 2 75032180

rs10496197 2 75032368

rs1050111 16 15824698

rs1050113 16 15746535

rs1050163 16 15718524

rs10502024 11 103396408

rs10502028 11 103512209

rs1050483 19 19164802

rs1050807 - 0

rs10510411 3 12321849

rs10510412 3 12321962

rs10510418 3 12363563

rs10510420 3 12408298

rs10510565 3 25363894

rs10510568 3 25577736

rs1051429 6 118988515

rs10514302 5 88062973

rs10514303 5 88080785

rs10517654 4 158138367

rs10517658 4 158145795

rs10518674 15 50105438

rs10519068 15 58855996

rs10519107 15 59114168

rs10519111 15 59169989

rs10519114 15 59255637

rs10519116 15 59282352

rs10519942 4 149456164

rs10519952 4 149559019

rs10521 9 136673544

rs1054156 15 58718763

rs1054203 10 70824818

rs1054789 15 58988635

rs1055659 22 44958817

rs1056471 2 26424608

rs1056505 17 40287192

rs1056632 2 26424384

rs1056896 4 186052512

rs1057744 14 104688087

rs1058322 12 1707240

rs1059611 8 19868843

rs1060619 12 6515042

rs1061430 8 145510987

rs1063539 3 188058094

rs1063831 12 93921472

rs1063926 17 10243665

rs1063955 3 121008821

rs1065782 7 45704798

rs10732705 9 74383554

rs10735003 12 1750646

rs10735380 12 101346703

rs10735491 1 213501673

rs10735810 12 46559162

rs10740051 10 51240158

rs10744960 15 59284879

rs1075846 5 149484351

rs10761576 10 51236885

rs10762275 10 70710625

rs10773986 12 1711585

rs10775167 15 56600674

rs10779271 1 213221384

rs10779274 1 213231885

rs10779276 1 213245782

rs10779279 1 213314367

rs10779286 1 213484675

rs10779935 2 47296662

rs1078000 19 17482508

rs10783215 12 46518165

rs10783219 12 46581755

rs10789038 1 56829138

rs10789184 1 65748983

rs10789186 1 65762498

rs10791999 11 68327414

rs10799760 1 22800352

rs10800775 1 198068043

rs10800776 1 198070210

rs10800777 1 198131745

rs10808240 7 128860710

rs10823350 10 70782400

rs10848557 12 1698071

rs10848568 12 1720645

rs10852375 16 15779398

rs10854011 19 19151441

rs10857561 10 49278644

rs10860603 12 99446416

rs10860861 12 101288036

rs10860865 12 101334189

rs10860869 12 101367519

rs10863249 1 213094852

rs10863250 1 213104156

rs10863252 1 213117829

rs10863259 1 213175564

rs10863262 1 213214375

rs10863268 1 213271282

rs10865803 3 25197055

rs10865971 3 52456446

rs10869410 9 74359398

rs10869417 9 74384005

rs10869423 9 74414220

rs10869430 9 74465817

rs10869433 9 74498220

rs10869436 9 74509489

rs10875549 5 149146245

rs10877969 12 61833506

rs10889563 1 65761188

rs10891314 11 111421857

rs10891338 11 111570644

rs10891342 11 111582408

rs10895065 11 100484937

rs10895559 11 103376724

rs10895570 11 103451058

rs10895572 11 103486066

rs10895575 11 103488072

rs10895586 11 103520887

rs10895587 11 103521917

rs10895593 11 103525964

rs10896370 11 68353269

rs10899084 11 74686218

rs10899119 11 75162879

rs10899121 11 75169851

rs10908764 1 156942067

rs10918169 1 162102133

rs10920181 1 198061786

rs10920182 1 198065730

rs10924074 1 116633061

rs10930781 2 177940139

rs10930783 2 178003868

rs10932201 2 208251763

rs10953286 7 98532453

rs1096389 8 76573223

rs10994675 10 51233999

rs10998702 10 70726938

rs10998730 10 70770788

rs10998742 10 70790328

rs11039149 11 47233251

rs11039159 11 47250597

rs1105297 1 43080689

rs11061974 12 1737278

rs11065766 12 109812569

rs1106964 4 167221986

rs11070877 15 50130394

rs11070879 15 50138955

rs11071386 15 56602612

rs11071557 15 58856246

rs11071563 15 58942966

rs11071564 15 58972901

rs11071576 15 59057915

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Supplemental Figures and Figure Legend

Figure S1. Multidimensional scaling, performed separately in the Caucasian and African

American races (our two largest racial sub-groups).

Figure S1.

The BARI 2D Study Group:

University of Pittsburgh, Pittsburgh, PA (Coordinating Center): (Principal

Investigator) Katherine M. Detre, MD, DrPH†, Sheryl F. Kelsey, PhD (Co-Principal

Investigator) Maria Mori Brooks, PhD (Co-Investigators) Trevor J. Orchard, MBBCh,

MMedSci, Stephen B. Thomas, PhD, Kim Sutton Tyrrell, RN, DrPH, Jamal S. Rana, MD,

PhD (Coordinator) Frani Averbach, MPH, RD (Administrative Coordinators) Joan M.

MacGregor, MS, Scott M. O’Neal, MA, Kathleen Pitluga, BA, Veronica Sansing, PhD,

Mary Tranchine, BS, Sharon W. Crow, MEd (Statisticians) Marianne (Marnie) Bertolet,

PhD, Regina Hardison, MS, Kevin Kip, PhD, Manuel Lombardero, MS, Jiang Lu, MS

(Data Managers) Sue Janiszewski, MSIS, Darina Protivnak, MSIS, Sarah Reiser, BS

(System Programmers) Stephen Barton, ASB, Ping Guo, BS, Yulia Kushner, BS, BA

(System Support) Jeffrey P. Martin, MBA, Christopher Kania, BS, Michael Kania, BS,

Jeffrey O’Donnell, BS (Consultant) Rae Ann Maxwell, RPh, PhD, Mayo Clinic

Foundation, Rochester, MN: (Study Chair) Robert L. Frye, MD National Heart, Lung

and Blood Institute, Bethesda, MD, National Institutes of Health, Bethesda, MD

(Program Office): (Project Officer) Suzanne Goldberg, RN, MSN (Deputy Project

Officer) Yves Rosenberg, MD, MPH (NHLBI Officers) Patrice Desvigne-Nickens, MD,

Abby Ershow, ScD, David Gordon, MD, PhD, Dina Paltoo, PhD, MPH National Institute

of Diabetes and Digestive and Kidney Diseases, National Institutes of Health,

Bethesda, MD (Co-Funding): (Program Director for Diabetes Complications) Teresa L.

Z. Jones, MD University of São Paulo Heart Institute, São Paulo, Brazil (Clinical

Site): (Principal Investigators) Cardiology: Whady Hueb, MD, José Ramires, MD, Neuza

Lopes, MD; Diabetology: Bernardo Léo Wajchenberg, MD (Investigators) Eulogio E.

Martinez, MD, Sergio A. Oliveira, MD, Expedito E. Ribeiro, MD, Marcos Perin, MD

(Coordinator) Roberto Betti, MD Toronto General Hospital/University Health

Network, Toronto, Canada (Clinical Site): (Principal Investigators) Cardiology:

Leonard Schwartz, MD; Diabetology: George Steiner, MD (Investigators) Alan Barolet,

MD, Yolanda Groenewoud, MD (Coordinators) Lisa Mighton, RN, CDE, Kathy Camelon,

RD, CDE Texas Health Science at San Antonio/South Texas Veterans Health Care

System, San Antonio, TX (Clinical Site): (Principal Investigators) Cardiology: Robert

O’Rourke, MD†; Diabetology: Janet Blodgett, MD (Investigators) Edward Sako, MD, PhD

(Coordinators) Judith Nicastro, RN, Robin Prescott, MSN Mayo Clinic-Rochester

Rochester, MN (Clinical Site, Vanguard Site): (Principal Investigators) Cardiology:

Charanjit Rihal, MD; Diabetology: Frank Kennedy, MD (Investigators) Gregory Barsness,

MD, Amanda Basu, MD, Alfredo Clavell, MD, Robert Frye, MD, David R. Holmes Jr.,

MD, Amir Lerman, MD, Charles Mullaney, MD, Guy Reeder, MD, Robert Rizza, MD,

Hartzell Schaff, MD, Steven Smith, MD, Virend Somers, MD, Thoralf Sundt, MD, Henry

Ting, MD, R Scott Wright, MD (Coordinators) Pam Helgemoe, RN, Diane Lesmeister,

Deborah Rolbiecki, LPN Mexican Institute of the Social Security, México City, D.F.,

México (Clinical Site): (Principal Investigators) Cardiology: Luis Lepe-Montoya, MD;

Diabetology, Jorge Escobedo, MD, FACP (Investigators) Rafael Barraza, MD, Rubén

Baleón, MD, Arturo Campos MD, Paula García, MD, Carlos Lezama, MD, Carlos

Miramontes, MD, Salvador Ocampo, MD, Joaquín V. Peñafiel, MD, Aquiles Valdespino,

MD, Raúl Verdín, MD, Héctor Albarrán, MD, Fernando Ayala, MD, Eduardo Chávez,

MD, Héctor Murillo, MD (Coordinators) Luisa Virginia Buitrón, MD, Beatriz Rico-Verdin,

MD, PhD, Fabiola Angulo, CCT University Hospitals of Cleveland/CASE Medical

School Cleveland, OH (Clinical Site, Vanguard Site): (Principal Investigators)

Cardiology: Dale Adler, MD, Austin Arthur Halle, MD; Diabetology: Faramarz Ismail-

Beigi, MD, PhD (Investigators) Suvinay Paranjape, MD (Coordinators) Stacey Mazzurco,

RN, Karen Ridley, RN, BSN Memphis VA Medical Center/University of Tennessee,

Memphis, TN (Clinical Site): (Principal Investigators) Cardiology: Kodangudi

Ramanathan, MD; Diabetology: Solomon Solomon, MD, Nephrology: Barry Wall, MD

(Investigators) Darryl Weinman, MD (Coordinators) Tammy Touchstone, RN, BSN, Lillie

Douglas, RN Montréal Heart Institute/Hôtel-Dieu-CHUM Montréal, Canada (Clinical

Site, Vanguard Site): (Principal Investigators) Cardiology: Martial Bourassa, MD, Jean-

Claude Tardif, MD; Diabetology: Jean-Louis Chiasson, MD, Marc Andre Lavoie, MD,

Rémi Rabasa-Lhoret, MD, PhD (Coordinators) Hélène Langelier, BSC, RD, Suzy

Foucher, RN, BA, Johanne Trudel, RN, BSc Albert Einstein College of

Medicine/Montefiore, Bronx, NY (Clinical Site): (Principal Investigators) Cardiology:

Scott Monrad, MD, Vankeepuram Srinivas, MD; Diabetology: Joel Zonszein, MD

(Investigators) Jill Crandall, MD (Coordinators) Helena Duffy, ANP, CDE, Eugen

Vartolomei, MD Fuqua Heart Center/Piedmont Hospital, Atlanta, GA (Clinical Site):

(Principal Investigators) Cardiology: Spencer King III, MD, Carl Jacobs, MD;

Diabetology: David Robertson, MD (Coordinators) Marty Porter, PhD, Melanie Eley, RN,

CCRC, Emmalee Nichols, BS, CRC, Jennifer LaCorte, RN, BSN, CCRN, Melinda Mock,

RN, BSN, MA University of Alabama at Birmingham, Birmingham, AL (Clinical Site,

Vanguard Site): (Principal Investigators) Cardiology: William Rogers, MD; Diabetology:

Fernando Ovalle, MD, David Bell, MBBCh (Investigators) Vijay K. Misra, MD, William B.

Hillegass, MD, Raed Aqel, MD (Coordinators) Penny Pierce, RN, BSN, Melanie Smith,

RN, BSN, Leah Saag, RN, Ashley Vaughn, RN, Dwight Smith, RN, Tiffany Grimes, RN,

Susan Rolli, RN, Roberta Hill, RN, Beth Dean Barrett, RN, Clarinda Morehead, LPN,

Ken Doss Northwestern University Medical School, Chicago, IL (Clinical Site):

(Principal Investigators) Cardiology: Charles J. Davidson, MD; Diabetology: Mark

Molitch, MD (Investigators) Nirat Beohar, MD (Coordinators) Elaine Massaro, MS, RN,

CDE, Lynne Goodreau, RN, Fabiola Arroyo, CCT Na Homolce Hospital, Prague,

Czech Republic, (Clinical Site): (Principal Investigators) Cardiology: Petr Neužil, MD,

PhD, Lenka Pavlíĉková, MD; Diabetology: Štĕpánka Stehlíková, MD (Investigators)

Jaroslav Benedik, MD (Coordinator) Liz Coling University of Ottawa Heart

Institute/Ottawa Hospital-Riverside Campus, Ottawa, Canada, (Clinical Site):

(Principal Investigators) Cardiology: Richard Davies, MD, Christopher Glover, MD,

Michel LeMay, MD, Thierry Mesana, MD; Diabetology: Teik Chye Ooi, MD, Mark

Silverman, MD, Alexander Sorisky, MD (Coordinators) Colette Favreau, RN, Susan

McClinton, BScN New York Medical College/Westchester Medical Center, Valhalla,

NY (Clinical Site): (Principal Investigators) Cardiology: Melvin Weiss, MD; Diabetology:

Irene Weiss, MD (Investigators) Leo Saulle, MD, Harichandra Kannam, MD

(Coordinators) Joanne C. Kurylas, RN, CDE, Lorraine Vasi, RN University, Atlanta, GA

(Clinical Site): (Principal Investigators) Cardiology: John Douglas Jr., MD, Ziyad

Ghazzal, MD, Laurence Sperling, MD, Spencer King, III, MD, Diabetology: Priya

Dayamani, MD, Suzanne Gebhart, MD (Investigators) Sabreena Basu, MD, Tarek

Helmy, MD, Vin Tangpricha, MD, PhD (Coordinators) Pamela Hyde, RN, Margaret

Jenkins, RN, CDE, CCRC, Barbara P. Grant, CVT Washington Hospital

Center/Georgetown University Medical Center, Washington, DC (Clinical Site):

(Principal Investigators) Cardiology: Kenneth Kent, MD, William Suddath, MD;

Diabetology: Michelle Magee, MD (Coordinators) Patricia Julien-Williams, CNP, Vida

Reed, RN, CDE Carine Nassar, RD, MS, CDE Québec Heart Institute/Laval Hôpital,

Sainte-Foy, Canada (Clinical Site): (Principal Investigators) Cardiology: Gilles

Dagenais, MD; Diabetology: Claude Garceau, MD (Coordinator) Dominique Auger, RN

University of British Columbia/Vancouver Hospital, British Columbia, Canada

(Clinical Site): (Principal Investigators) Cardiology: Christopher Buller, MD; Diabetology:

Tom Elliott, MBBS, (Investigators) Krishnan Ramanathan MBChB, Donald Ricci, MD

(Coordinators) Rebecca Fox, PA, MSc, Daniela Kolesniak, MD NYU School of

Medicine, New York, NY (Clinical Site): (Principal Investigators) Cardiology: Michael

Attubato, MD, Frederick Feit, MD; Diabetology: Stephen Richardson, MD (Investigators)

Ivan Pena Sing, MD, James Slater, MD (Coordinators) Angela Amendola, MS, PA-C,

RD, CDE ,Bernardo Vargas, BS Lahey Clinic Medical Center, Burlington, MA,

(Clinical Site, Vanguard Site): (Principal Investigators) Cardiology: Nicholas

Tsapatsaris, MD, Bartholomew Woods, MD; Diabetology: Gary Cushing, MD

(Investigators) Martin K. Rutter, MD, Premranjan Singh, MD (Coordinators) Gail

DesRochers, RN, Gail Woodhead, RN, Deborah Gannon, MS, Nancy Shinopulos

Campbell, RN University of Virginia, Charlottesville, VA (Clinical Site): (Principal

Investigators) Cardiology: Michael Ragosta, MD, Ian Sarembock, MD, Eric Powers, MD;

Diabetology: Eugene Barrett, MD (Coordinators) Linda Jahn, RN, MEd, Karen Murie, RN

University of Minnesota/Minnesota Veterans Research Institute, Minneapolis, MN

(Clinical Site): (Principal Investigators) Cardiology: Gladwin Das, MB, BS, MD, Gardar

Sigurdsson, MD, Carl White, MD; Diabetology: John Bantle, MD (Investigator) J. Bruce

Redmon, MD (Coordinator) Christine Kwong, MPH, RD, CDE St. Luke's/Roosevelt

Hospital Center, New York, NY (Clinical Site): (Principal Investigators)

Cardiology: Jacqueline Tamis-Holland, MD; Diabetology: Jeanine Albu, MD

(Investigators) Judith S. Hochman, MD, James Slater, MD, James Wilentz, MD

(Coordinators) Sylvaine Frances, PA, Deborah Tormey, RN University of Florida,

Gainesville, FL (Clinical Site): (Principal Investigators) Cardiology: Carl Pepine, MD,

Karen Smith, MD; Endocrinology: Laurence Kennedy, MDFRCP (Coordinators) Karen

Brezner, CCRC, Tempa Curry, RN Saint Louis University, St. Louis, MO (Clinical

Site): (Principal Investigators) Cardiology: Frank Bleyer, MD; Diabetology: Stewart

Albert, MD (Investigator) Arshag Mooradian, MD, (Coordinator) Sharon Plummer, NP

University of Texas at Houston, Houston, TX (Clinical Site): (Principal Investigators)

Cardiology: Francisco Fuentes, MD, Roberto Robles, MD; Diabetology: Victor Lavis, MD

(Investigators) Jaime Gomez, MD, Cesar Iliescu, MD (Coordinators) Carol Underwood,

BSN, RN, CCRC, Maria Selin Fulton, RN, CDE, Julie Gomez Ramirez, BSN, RN,

Jennifer Merta, MA, Glenna Scott, RN Kaiser-Permanente Medical Center, San Jose,

CA (Clinical Site): (Principal Investigators) Cardiology: Ashok Krishnaswami, MD;

Diabetology: Lynn Dowdell, MD (Coordinator) Sarah Berkheimer, RN Henry Ford Heart

& Vascular Institute, Detroit, MI (Clinical Site): (Principal Investigators)

Cardiology: Adam Greenbaum, MD; Diabetology: Fred Whitehouse, MD (Coordinators)

Raquel Pangilinan, BSN, RN, Kelly Mann, RN, BSN, CDE Boston Medical Center,

Boston, MA (Clinical Site): (Principal Investigators) Cardiology: Alice K. Jacobs, MD;

Diabetology: Elliot Sternthal, MD (Investigators) Susana Ebner, MD, Zoran Nedeljkovic,

MD (Coordinator) Paula Beardsley, LPN Fletcher Allen Health Care (Vanguard Site),

Burlington, VT (Clinical Site): (Principal Investigators) Cardiology: David Schneider,

MD; Diabetology: Richard Pratley, MD, William Cefalu, MD, Joel Schnure, MD

(Coordinators) Michaelanne Rowen, RN, CCRC, Linda Tilton, MS, RD, DE Jim Moran

Heart & Vascular Institute, Fort Lauderdale, FL (Clinical Site): (Principal

Investigators) Cardiology: Alan Niederman, MD; Diabetology: Cristina Mata, MD

(Coordinator) Terri Kellerman, RN Baylor College of Medicine, Houston, TX (Clinical

Site: (Principal Investigators) Cardiology: John Farmer, MD; Diabetology: Alan J.

Garber, MD, PhD (Investigators) Neal Kleiman, MD (Coordinators) Nancy Howard, RN,

BSN, Debra Nichols, RN, Madonna Pool, RN, MSN Duke University, Durham, NC

(Clinical Site): (Principal Investigators) Cardiology: Christopher Granger, MD;

Diabetology: Mark Feinglos, MD (Investigators) George Adams, MD, Jennifer Green, MD

(Coordinators) Bernadette Druken, RN, CCRP, Dani Underwood, MSN, ANP University

of Maryland Hospital, Baltimore, MD (Clinical Site): (Principal Investigators)

Cardiology: J. Lawrence Stafford, MD; Diabetology: Thomas Donner, MD (Investigator)

Warren Laskey, MD (Coordinator) Dana Beach, RN University of Chicago Medical

Center, Chicago, IL (Clinical Site): (Principal Investigators) Cardiology: John Lopez,

MD; Diabetology: Andrew Davis, MD (Investigators) David Faxon, MD, Sirimon

Reutrakul, MD (Coordinator) Emily Bayer, RN, BSN University of Pittsburgh Medical

Center, Pittsburgh, PA (Clinical Site, Vanguard Site): (Principal Investigators)

Cardiology: Oscar Marroquin, MD, Howard Cohen, MD; Diabetology: Mary Korytkowski,

MD (Coordinators) Glory Koerbel, MSN, CDE, Lisa Baxendell, RN, Debbie Rosenfelder,

BSN, CCRC, Louise DeRiso, MSN, Carole Farrell, BSN, Tina Vita, RN Washington

University/Barnes Jewish Hospital, St. Louis, MO (Clinical Site): (Principal

Investigators) Diabetology: Janet McGill, MD; Cardiology: Ronald Krone, MD, Richard

Bach, MD (Coordinators) Carol Recklein, RN, MHS, CDE, Kristin M. Luepke, RN, MSN,

Mary Jane Clifton Mount Sinai Medical Center, New York, NY (Clinical Site):

(Principal Investigators) Cardiology: Michael E. Farkouh, MD, MSc, Michael C. Kim,

MD, FACC; Diabetology: Donald A. Smith, MD, MPH (Coordinators) Ida Guzman, RN,

ANP, Arlene Travis, RN, MSN, Mid America Heart Institute, Kansas City, MO

(Clinical Site): (Principal Investigators) Cardiology: James O’Keefe, MD; Diabetology:

Alan Forker, MD, William Isley, MD† (Investigator) Richard Moe, MD, PhD (Coordinators)

Paul Kennedy, RN, Margaret Rosson, LPN, Aimee Long, RN University of Michigan,

Ann Arbor, MI (Clinical Site): (Principal Investigators) Cardiology: Eric Bates, MD;

Diabetology: William Herman, MD, MPH, Rodica Pop-Busui, MD, PhD (Investigators)

Claire Duvernoy, MD, Martin Stevens, MBBCh (Coordinators) Ann Luciano, RN, Cheryl

Majors, BSN Johns Hopkins Bayview Medical Center, Baltimore, MD (Clinical Site):

(Principal Investigators) Cardiology: Sheldon H. Gottlieb, MD; Diabetology: Annabelle

Rodriguez, MD (Coordinator) Melanie Herr, RN Brown University/Rhode Island

Hospital, Providence, RI (Clinical Site): (Principal Investigators) Cardiology: David

Williams, MD; Diabetology: Robert J. Smith, MD (Investigators), J. Dawn Abbott, MD,

Marc J. Laufgraben, MD (Coordinators) Mary Grogan, RN, Janice Muratori, RNP

Houston VA Medical Center, Houston, TX (Clinical Site): (Principal Investigators)

Cardiology: Gabriel Habib, MD, MS; Diabetology: Marco Marcelli, MD (Investigators)

Issam Mikati, MD (Coordinators) Emilia Cordero, NP, Gina Caldwell, LVN New York

Hospital Queens /Lang Research Center, Queens, NY (Clinical Site): (Principal

Investigators) Cardiology: David Schechter, MD; Diabetology: Daniel Lorber, MD;

Nephrology: Phyllis August, MD, MPH (Coordinators) Maisie Brown, RN, MSN, Patricia

Depree, PhD, ANP, CDE Wilhelminen Hospital, Vienna, Austria (Clinical Site):

(Principal Investigators) Cardiology: Kurt Huber, MD; Diabetology: Ursula Hanusch-

Enserer, MD (Investigators) Nelly Jordanova, MD (Coordinators) Dilek Cilesiz, MD, Birgit

Vogel, MD St. Joseph Mercy Hospital/Michigan Heart and Vascular Institute and

the Ann Arbor Endocrinology and Diabetes, P.C., Ann Arbor, MI (Clinical Site):

(Principal Investigators) Cardiology: Ben McCallister Jr., MD; Diabetology: Michael

Kleerekoper, MD, Kelly Mandagere, MD, Robert Urbanic, MD (Investigators)

James Bengston, MD, MPH, Bobby K. Kong, MD, Andrew Pruitt, MD, Jeffrey Sanfield,

MD (Coordinators) Carol Carulli, RN, Ruth Churley-Strom, MSN The Ohio State

University Medical Center, Columbus, OH (Clinical Site): (Principal Investigators)

Cardiology: Raymond Magorien, MD; Diabetology: Kwame Osei, MD (Coordinators)

Cecilia Casey Boyer, RN, MS, CDE Mayo Clinic-Scottsdale, Scottsdale, AZ (Clinical

Site): (Principal Investigators) Cardiology: Richard Lee, MD; Diabetology: Pasquale

Palumbo, MD (Coordinator) Joyce Wisbey, RN Angiographic Core Laboratory,

Stanford University, Stanford, CA: (Principal Investigator) Edwin Alderman, MD (Staff)

Fumiaki Ikeno, MD, Anne Schwarzkopf† Biochemistry Core Laboratory, University of

Minnesota, Minneapolis, MN: (Principal Investigator) Michael Steffes, MD, PhD (Staff)

Maren Nowicki, CLS, Jean Bucksa, CLS ECG Core Laboratory, Saint Louis

University, St. Louis, MO (U01 HL061746): (Principal Investigator) Bernard Chaitman,

MD (Staff) Jane Eckstein, RN, Karen Stocke, BS, MBA Economics Core Laboratory,

Stanford University, Stanford, CA (U01 HL061748): (Principal Investigator) Mark A.

Hlatky, MD (Staff) Derek B. Boothroyd, PhD, Kathryn A. Melsop, MS Fibrinolysis Core

Laboratory, University of Vermont, Burlington, VT (U01 HL063804): (Principal

Investigator) Burton E. Sobel, MD (Staff) Michaelanne Rowen, RN, CCRC, Dagnija

Neimane, BS Nuclear Cardiology Core Laboratory, University of Alabama at

Birmingham, Birmingham, AL (Astellas Pharma US, Inc.): (Principal Investigator)

Ami E. Iskandrian, MD (Staff) Mary Beth Schaaf, RN, BSN Diabetes Management

Center, Case Western Reserve University, Cleveland, OH: (Director) Saul Genuth,

MD (Staff) Theresa Bongarno, BS, Hypertension Management Center, Lahey Clinic

Medical Center, Burlington, MA: (Co-Director) Richard Nesto, MD Hypertension

Management Center, New York Hospital Queens, Queens, NY: (Co-Director) Phyllis

August, MD, MPH (Staff) Karen Hultberg, MS Lifestyle Intervention Management

Center, Johns Hopkins Bayview Medical Center, Baltimore, MD: (Co-Director)

Sheldon H. Gottlieb, MD Lifestyle Intervention Management Center, St.

Luke’s/Roosevelt Hospital Center, New York, NY: (Co-Director) Jeanine Albu, MD

(Staff) Helene Rosenhouse-Romeo, RD, CDE Lipid Management Center, University

of Pittsburgh, Pittsburgh, PA: (Director) Trevor J. Orchard, MBBCh, MMedSci (Staff)

Georgia Pambianco, MPH, Manuel Lombardero, MS Safety Officer, North Canton,

OH: Michael Mock, MD† Operations Committee: (Chair) Robert L. Frye, MD(Members)

Maria Mori Brooks, PhD, Patrice Desvigne-Nickens, MD, Abby Ershow, ScD, Saul

Genuth, MD, Suzanne Goldberg, RN, MSN, David Gordon, MD, PhD, Regina Hardison,

MS, Teresa L. Z. Jones, MD, Sheryl Kelsey, PhD, Richard Nesto, MD, Trevor Orchard,

MBBCh, MMedSci, Dina Paltoo, PhD, MPH, Yves Rosenberg, MD, MPH Morbidity and

Mortality Classification Committee (MMCC): (Chair) Thomas Ryan, MD (Co-Chair)

Harold Lebovitz, MD (Members) Robert Brown, MD, Gottlieb Friesinger, MD, Edward

Horton, MD, Jay Mason, MD, Renu Virmani, MD, Lawrence Wechsler, MD Data and

Safety Monitoring Board (DSMB): (Chair) C. Noel Bairey-Merz, MD (former Chair) J.

Ward Kennedy, MD† (Executive Secretary) David Gordon, MD, PhD (Members) Elliott

Antman, MD, John Colwell, MD, PhD, Sarah Fowler, PhD, Curt Furberg, MD, PhD, Lee

Goldman, MD, Bruce Jennings, MA, Scott Rankin, MD.

†Deceased

peroxisome proliferator-activated receptor pathway...

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