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Intracellular Niches of Microbes
A Pathogens Guide Through the Host Cell
Edited byUlrich E. Schaible and Albert Haas
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Intracellular Niches of Microbes
Edited by
Ulrich E. Schaible and Albert Haas
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Intracellular Niches of Microbes
A Pathogens Guide Through the Host Cell
Edited byUlrich E. Schaible and Albert Haas
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The Editors
Prof. Ulrich E. SchaibleResearch Center BorstelZentrum für Medizin und Biowissenschaften(FZB)Department of Molecular Infection ResearchParkallee 1 – 4023845 BorstelGermany
Prof. Albert HaasUniversity of BonnCell Biology InstituteUlrich-Haberland-Straße 61 a53121 BonnGermany
All books published by Wiley-VCH are carefullyproduced. Nevertheless, authors, editors, andpublisher do not warrant the information containedin these books, including this book, to be free oferrors. Readers are advised to keep in mind thatstatements, data, illustrations, procedural details orother items may inadvertently be inaccurate.
Library of Congress Card No.: applied for
British Library Cataloguing-in-Publication DataA catalogue record for this book is available from theBritish Library.
Bibliographic information published bythe Deutsche NationalbibliothekThe Deutsche Nationalbibliothek lists thispublication in the Deutsche Nationalbibliografie;detailed bibliographic data are available on theInternet at http://dnb.d-nb.de.
# 2009 WILEY-VCH Verlag GmbH & Co. KGaA,Weinheim
All rights reserved (including those of translation intoother languages). No part of this book may bereproduced in any form – by photoprinting,microfilm, or any other means – nor transmitted ortranslated into a machine language without writtenpermission from the publishers. Registered names,trademarks, etc. used in this book, even when notspecifically marked as such, are not to be consideredunprotected by law.
Typesetting Thomson Digital, Noida, IndiaPrinting betz-druck GmbH, DarmstadtBookbinding Litges & Dopf GmbH, HeppenheimCover Design Adam-Design, Weinheim
Printed in the Federal Republic of GermanyPrinted on acid-free paper
ISBN: 978-3-527-32207-7
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Foreword
Over the last thirty years, the combined use of bacterial genetics, molecular and cellbiology, and more recently genomics, have illuminated our understanding of thevirulence of the major human and veterinary pathogens. Among those, intracellularbacterial pathogens have played a dominant role in this endeavor because theyrecapitulate most of the existing steps of microbe-host interaction. The progressmade has been impressive, not only conceptually, but also technically. Imaging, forinstance, has often prepared and preceded the discoveries in this area where seeing isbelieving, it has also tremendously benefited from thesemodels in return. Adherenceof pathogens to cells, diversity of mechanisms of entry, a variety of mechanisms forintracellular survival and growth, from vacuolar rupture followed by escape into thecytoplasm, to remodeling of vacuoles to avoid phagolysomal fusion – a combinator-ial synthesis of these steps of interaction has led to an amazing breadth of diversifiedstrategies representing the complex solutions ‘‘developed’’ by nature for pathogensto achieve survival as species, or pathovars among these species, in the ferociousstruggle for life. These microorganisms are exposed to harsh environmental condi-tions such as fighting against protozoan predators (i.e. amoebas) for the so calledenvironmental pathogens like Legionella, or to the immune system that has appearedearly in the world of multicellular organisms.Nothing makes sense in biology if not seenunder the angle of evolution said Theodosius Dobzansky. The world of intracellularmicrobes is a perfect illustration of this statement. With the possible exception ofenvironmental pathogens, intracellular pathogens bear in their genomes the tracesof their construction under selective pressure of their host. It results in a complexmixture of gene acquisition and gene deletion that strongly differentiate them fromtheir closest commensal cousins. A permanent flux of genes, largely perpetrated bybacteriophages and plasmids permanently occurs, particularly in the gut lumen ofanimals, thereby permanently offeringmicrobes options to improve their fit with thehost. It is difficult to decipher the timing of the genetic events that have led to suchcomplex combinations. However, one would like to believe that some key steps haveoccurred at some stage, like the acquisition of a large pathogenicity island encodinginvasive capacities, thereby propelling the microorganisms in a new hostile envir-onment to which it was not prepared. Only the acquisition and/or loss of genes
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allowing the pathogen to cope with these new conditions was able to secure itssurvival. It is not the strongest of the species that survives. . .nor the most intelligent thatsurvives. It is the one that is the most adaptable to change said Darwin inOn the origin ofspecies by way of natural selection. It is interesting to consider that our ‘‘contemporary’’pathogens still have a large capacity to evolve, but that only the stochastic acquisitionof new genes by horizontal transfer can achieve the quantum leap changes thatmovethe evolutionary process. It is also interesting to observe that several genomes ofintracellular pathogens, particularly those that have become obligate intracellularparasites (i.e. Rickettsia spp., Chlamydia spp.,Mycobacterium leprae) show highly deg-raded genomes, with massive amount of gene loss. Whether this is a true reflectionof the need for compensatory gene deletion to the acquisition of new intracellularpathogenic properties, or simply the loss in absence of selective pressure of genes(i.e. metabolic pathways) that are no longer useful to the pathogen since it benefitsfrom the cell nutrients, is still an open and debated question. In any event, theprogression towards complete intracellular parasitism that is often accompanied byrestriction in species specificity is a dominant feature of intracellular microorgan-isms that certainly needs further investigation.Last but not least, it seems that the ultimate option for these microorganisms is to
become true symbionts. Indeed, some molecular systems such as secretory appa-ratus that are essential to deliver virulence effectors are conserved in true symbionts,probably with the aim to deliver symbiotic effectors. The ultimate example is theabsolute harnessing by eukaryotic cells of Rickettsia spp. to generate mitochondria asO2 appeared on earth. No need to reach this extreme, however, Wolbachia spp. doparasitize insects in a very ‘‘stealthy’’manner, and only recently was it observed thatthis symbiosis, beside its well known effect on fecundity, was stimulating a back-ground level of innate immunity allowing these insects to resist viral infection.The world of intracellular pathogens, and symbionts that should now be part of
this global concept, appears as a gold mine of strategies whose purpose often stillneeds to be understood.In an amazing series of contributions by renowned world experts, this volume
provides the first integrated, coherent and exhaustive review of the biology ofintracellular pathogens and symbionts. It offers a fascinating vision of the evolu-tionary logics that have led microorganisms to venture into cells and to adapt to theenvironment of this niche in a way that led to genomic modifications which madethem for ever different and highly adapted to this particular life style. For some ofthem it evolved to the ultimate point of becoming obligate intracellular pathogens, oreven symbionts.Ulrich Schaible and Albert Haas should be congratulated for their exceptional
vision of the field, contagious enthusiasm that helped assemble this key stonevolume, and, last but not least, exceptional service to our community.
Philippe J. SansonettiProfesseur au Collège de FranceProfesseur à lInstitut Pasteur
VI Foreword
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Contents
Foreword VList of Contributors XVII
Part I General Aspects 1
1 Introduction: The Evolution of Intracellular Life Formsand their Niches 3Ulrich E. Schaible and Albert Haas
1.1 A Short History of Theories and Discoveries 31.2 A Look Through the Microscope of Evolution 51.3 Continuous Exchange of Information 91.4 Evolution of Intracellular Parasitism 101.5 Intracellular Symbionts: Tamed or Acclimatized Parasites? 131.6 An Ecological View of Intracellular Life 141.7 The Immunologists View 161.8 The Public Health View 171.9 The Book 18
References 18
2 Limited Genomes and Gene Transfer in the Evolutionof Intracellular Parasitism and Symbiosis 21Naraporn Somboonna and Deborah Dean
2.1 Introduction to Gene Transfer and Evolution 212.2 Gene Transfer in Intracellular Bacterial Parasites 232.3 Gene Transfer in Intracellular Symbionts 272.4 Gene Transfer in Intracellular Parasites and Fungi 292.5 Summary and Outlook 30
References 32
3 Phagocytosis: Early Events in Particle Recognition and Uptake 37Gabriela Cosío and Sergio Grinstein
3.1 Phagocytosis: An Overview 37
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3.2 Recognition of Target Particles 383.3 Signaling Events Upon Ligand Recognition 423.4 Membrane Dynamics During Phagocytosis 463.5 Phagosome Maturation 483.6 Inflammatory Signals Linked to Phagocytosis 503.7 Concluding Remarks 52
References 52
4 Cellular Model Systems Used to Study Phagosome Biogenesis 65Michael Steinert
4.1 From Grazing to Host Defense 654.2 Dictyostelium, a Professional Phagocyte at the Border
of Multicellularity 664.3 Dictyostelium, a Surrogate Host for Legionella, Mycobacterium
and Other Pathogens 674.4 Legionella-directed Phagosome Biogenesis 704.5 The Whole Animal Model Drosophila melanogaster 724.6 Infection of Drosophila Phagocytes 734.7 Conclusions 74
References 75
5 Methods Used to Study Phagosome Biogenesis 77Albert Haas
5.1 Describing the World Within – Whole-Cell Assaysfor Phagosome Contents 77
5.2 Biochemical Analysis and Assays with Purified Phagosomes 875.3 Use of Fluorescence-Activated Cell Sorting (FACS)
in Phagosome Research 885.4 Knockdown, Knockout and Phagosome Research 895.5 Transcriptomics as a Phagosome Environmental Sensor 90
References 91
6 In Vitro Fusion Assays with Phagosomes 95Ulrike Becken and Albert Haas
6.1 Introduction 956.2 A Variety of Assays 966.3 Studying Normal Maturation . . . 1016.4 . . . and the Pathogenic Case 103
References 105
7 Phagosome Proteomes Unite! A Virtual Model of Maturationas a Tool to Study Pathogen-Induced Changes 107Régis Dieckmann and Thierry Soldati
7.1 Background 1077.2 A Methods Guide to Phagosome Proteomics 108
VIII Contents
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7.3 Particle-Induced Impact on Phagosome Isolation 1127.4 Comparative Proteomics of Microbe-Containing Vacuoles 1137.5 Conclusions 121
References 122
8 Phagosome–Cytoskeleton Interactions 125Maximiliano G. Gutierrez and Gareth Griffiths
8.1 Introduction 1258.2 The Actin Cytoskeleton. General Background 1268.3 The Microtubule Cytoskeleton – General Background 1368.4 Concluding Remarks 140
References 140
9 Intracellular Microbe Whole-Genome Expression Profiling:Methodological Considerations and Biological Inferences 145Simon J. Waddell and Philip D. Butcher
9.1 Introduction 1459.2 Methodological Considerations 1469.3 Biological Inferences from Expression Profiling 1499.4 Concluding Remarks 155
References 156
10 Everybody Has A Home of Their Own – The Phagosome Zoo 159Albert Haas
10.1 Come On In, Get Killed! Death in the Shredder 15910.2 Professionals and Laypersons 16310.3 Come On In, Have Fun! Life in a Golden Cage 16510.4 Immune Activation and the Loss of Home 18410.5 Why Not Pathogens in Peroxisomal Vacuoles? 18510.6 Looking for a New Home 18610.7 Summary 186
References 187
11 Consequences of Pathogen Compartmentationfor Therapeutic Intervention 191Albert Haas and Ulrich Schaible
11.1 The Problem 19111.2 Consequences of Intracellular Localization for Treatment
with Antibiotics 19111.3 Many Roads Lead Into the Host Cell 19511.4 And Off You Go . . . 19711.5 Small Molecules Pave the Road to the Future 19711.6 How Do You Come Up With A Successful Small Molecule? 19811.7 A Few More, Maybe Even Practicable, Ideas For the Future . . . 199
References 200
Contents IX
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12 The Immune Response to Intracellular Pathogens 203Daniel S. Korbel and Ulrich E. Schaible
12.1 General Introduction 20312.2 Innate Immunity 20612.3 Adaptive Immunity 21712.4 Conclusion 23012.5 Excursus – Immunity in Plants 230
References 232
Part II Selected Pathogens 235
IIA Vacuolar Bacteria 235
13 Afipia felis 237Bianca E. Schneider and Albert Haas
13.1 Introduction of Afipia felis and its Role in Cat Scratch Disease 23713.2 Uptake and Intracellular Compartmentation of Afipia felis
in Murine Macrophages 24013.3 The Port of Entry Paves the Way for Non-Endocytic
Compartmentation 24213.4 Host and Pathogen Determinants Involved in Diverted
Phagosome Biogenesis 25013.5 Immunology of the Afipia-Containing Phagosome 25113.6 Summary and Outlook 252
References 253
14 Brucella 255Monika Kalde, Edgardo Moreno, and Jean-Pierre Gorvel
14.1 Introduction 25514.2 Characterization of Intra-Host Cell Compartmentation of Brucella
and its Relationship to Virulence 25814.3 Factors Involved in Diverted Phagosome Maturation and
Compartment Maintenance 26214.4 Immunology of Phagosomes Containing Brucella 26614.5 Conclusions 269
References 270
15 Chlamydiae 273Ted Hackstadt
15.1 Diseases 27315.2 Characterization of the Chlamydial Inclusion and its Relationship
to Virulence 27315.3 Genes Involved in Chlamydial Inclusion Maturation 27515.4 Immunology of the Chlamydial Inclusion 28115.5 Summary and Outlook 283
References 283
X Contents
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16 Coxiella burnetii 287Stacey D. Gilk, Daniel E. Voth, and Robert A. Heinzen
16.1 Coxiella burnetii and Q Fever 28716.2 Characterization of the Intrahost Compartment of Coxiella
and its Relationship to Virulence 28816.3 Genes Involved in Diverted Phagosome Maturation/
Compartment Maintenance 29516.4 Immunology of the Coxiella Parasitophorous Vacuole 29716.5 Summary and Outlook 297
References 298
17 Ehrlichia and Anaplasma 301Yasuko Rikihisa
17.1 Ehrlichia andAnaplasma and the Illnesses They Cause inHumans 30117.2 Characterization of Host Cell Compartmentalization
of E. chaffeensis and A. phagocytophilum 30217.3 Microbe Genes Involved in Subverting Phagosome
Maturation/Compartment Maintenance 31017.4 Immunology of Phagosomes Containing E. chaffeensis
and A. phagocytophilum 31117.5 Summary and Outlook 312
References 312
18 Legionella pneumophila 315Alyssa Ingmundson and Craig R. Roy
18.1 Legionella pneumophila Biology 31518.2 The Intracellular Compartment of L. pneumophila 31518.3 Requirements for Intracellular Replication 31618.4 The Immune Response to L. pneumophila Infection 32018.5 Summary and Outlook 322
References 323
19 Mycobacterium tuberculosis and His Comrades 327Ulrich E. Schaible
19.1 Pathogenic Mycobacteria 32719.2 Intracellular Compartment and Virulence Properties
of Mycobacteria 33219.3 Host Response and Transmission 34619.4 Outlook 348
References 349
20 Rhodococcus equi and Nocardia asteroides 355Kristine von Bargen and Albert Haas
20.1 Rhodococcus and Nocardia and Illnesses Caused by them 35520.2 Characterization of Intra-Host Cell Compartmentation and
its Relationship to Virulence 357
Contents XI
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20.3 Genes Involved in Diverted Phagosome Maturation orCompartmentation and its Maintenance 361
20.4 Immunology of Phagosomes Containing R. equi orN. asteroides 364
20.5 Summary and Outlook 367References 368
21 Salmonella 373Olivia Steele-Mortimer
21.1 Introduction 37321.2 Characterization of the SCV and its Role in
Virulence 37621.3 Factors Affecting SCV Biogenesis 37821.4 Immunology of the SCV 38321.5 Summary 384
References 384
IIB Intracytosolic Bacteria 391
22 Burkholderia pseudomallei 393Joanne M. Stevens and Mark P. Stevens
22.1 Burkholderia pseudomallei and Melioidosis 39322.2 An Overview of the Intracellular Life of B. pseudomallei 39422.3 Genome Structure and Diversity of B. pseudomallei 39522.4 Cell Contact and Adherence 39622.5 Invasion 39822.6 Endosome Escape 40022.7 Actin-Based Motility 40122.8 Cell Fusion 40422.9 Intracellular Replication 40522.10 Immunology of B. pseudomallei-Host Cell Interactions 40622.11 Concluding Remarks 407
References 408
23 Francisella tularensis 415Lee-Ann H. Allen and Grant S. Schulert
23.1 Francisella tularensis and Tularemia 41523.2 F. tularensis Inhibits Phagosome Maturation Prior to Egress
and Replication in the Cytosol 41623.3 F. tularensis Virulence Factors that Disrupt Phagocyte
Function 42223.4 Immunology of Phagosome and Host Defense 42423.5 Summary and Outlook 424
References 425
XII Contents
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24 Listeria monocytogenes 431Damien Balestrino and Pascale Cossart
24.1 Listeria and Listeriosis 43124.2 The Intracellular Lifestyle of Listeria and its Relationship
to Virulence 43524.3 Bacterial Factors Involved in Escape From the
Vacuole 44124.4 Survey Inside the Phagosome and Phagosome
Maturation 44624.5 Summary and Outlook 451
References 452
25 Mycobacterium marinum 455Monica Hagedorn and Thierry Soldati
25.1 An Introduction to Mycobacterium marinum and theIllness Caused by it 455
25.2 Characterization of Intra-Host Cell Compartmentationof M. marinum and its Relationship to Virulence 458
25.3 Genes Involved in Diverting Phagosome Maturationand in Compartment Maintenance 461
25.4 Immunological Aspects of M. marinum Infection 46325.5 Whats Next? (Outlook and Summary) 464
References 465
26 Rickettsia 469Sanjeev K. Sahni, Elena Rydkina, and David J. Silverman
26.1 Introduction to Rickettsiae and Rickettsial Diseases 46926.2 Intracytoplasmic Behavior of Rickettsiae 47226.3 Host Cell Interactions with Pathogenic Rickettsia
Species 47726.4 Animal Models and Immunology of Rickettsioses 47926.5 Genomics and Proteomics of Rickettsia Species 48026.6 Summary and Outlook 482
References 483
27 Shigella 485Guy Tran Van Nhieu and Philippe Sansonetti
27.1 Introduction 48527.2 Escape into the Cytoplasm and Intracytoplasmic
Replication 48827.3 Genes Involved in Phagosome Escape and Intracytoplasmic
Life 49327.4 Host Defense Against Cytoplasmic Shigella 49627.5 Summary and Outlook 499
References 499
Contents XIII
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IIC Intracellular Symbionts 505
28 Bacterial Symbionts of Plants 507Kumiko Kambara, William J. Broughton, and William J. Deakin
28.1 Introduction to Rhizobia and Symbioses 50728.2 Invasion of Plant Cells by Rhizobia and Arbuscular Mycorrhizae 50828.3 Plant Genes Involved in Symbiosis Initiation 51028.4 Symbiotic Signals Produced by Rhizobia 51428.5 Summary and Outlook 521
References 521
29 Cyanobacterial and Algal Symbioses 527Goran Kovacevic, Jürgen M. Steiner, and Wolfgang Löffelhardt
29.1 Introduction 52729.2 Intracellular Cyanobacteria 52729.3 Intracellular Algae 536
References 543
30 Insect Symbionts 547Heike Feldhaar and Roy Gross
30.1 Introduction 54730.2 Mutualistic Primary Endosymbionts with a Function in
Nutritional Upgrading 55030.3 Endosymbionts that Interfere with Reproduction 55430.4 Endosymbiont Communities 55830.5 Conclusion and Future Directions 559
References 560
IID Parasites and Fungi 565
31 Histoplasma capsulatum 567S. L. Newman
31.1 Histoplasma capsulatum and Histoplasmosis 56731.2 Characterization of the Macrophage Phagosomes Containing
H. capsulatum Yeasts 56931.3 Genes Involved in the IntracellularSurvival ofH.capsulatumYeasts 57331.4 Immunology of Phagosomes Containing H. capsulatum Yeasts 57931.5 Summary and Outlook 579
References 580
32 Leishmania: L. mexicana vs. donovani vs. major;Amastigotes vs. Promastigotes 583Christine Matte, Julia Mallégol, and Albert Descoteaux
32.1 Leishmania and Leishmaniases 583
XIV Contents
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32.2 Characterization of Intra-Host Cell Compartmentation ofLeishmania and its Relationships to Virulence 584
32.3 Leishmania Molecules Involved in Diverted PhagosomeMaturation/Compartment Maintenance 586
32.4 Immunology of Phagosomes ContainingLeishmania 592
32.5 Summary and Outlook 593References 593
33 Plasmodium and Babesia 597Markus Winterberg, Jude M. Przyborski, and Klaus Lingelbach
33.1 Introduction 59733.2 Illness 59933.3 Characterization of Intra-Host Compartmentation and its
Relationship to Virulence 60033.4 From Parasite Cell Biology and Genomics to Drug Targets 60733.5 Summary and Outlook 609
References 609
34 Theileria 613Dirk Dobbelaere and Martin Baumgartner
34.1 Introduction to Theileria and the Disease 61334.2 Characterization of the Intra-Host Cell Compartment . . .
Which Compartment? 61534.3 Genes Involved in Host–Parasite Interaction 62334.4 Immune Responses Directed Against the Schizont 62534.5 Summary and Outlook 626
References 628
35 Toxoplasma gondii 633L. David Sibley
35.1 Introduction of Toxoplasma gondii and Toxoplasmosis 63335.2 Characterization of the Intracellular Compartment Occupied
by T. gondii 63535.3 Parasite Factors Involved in Maturation and Maintenance
of the Parasite-Containing Vacuole 63835.4 Immunology of the Intracellular Compartment Occupied
by T. gondii 64135.5 Summary and Outlook 646
References 647
36 Trypanosoma cruzi 655Martin C. Taylor
36.1 Introduction: The Parasite and its Disease 65536.2 Intracellular Compartmentation of T. cruzi 657
Contents XV
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36.3 Maintenance of the Infected Cell 66336.4 Immunology of T. cruzi Infection 66436.5 Summary and Outlook 666
References 667
37 Trichinella and the Nurse Cell 669David B. Guiliano and Yelena Oksov
37.1 Introduction to Trichinella and Trichinellosis 66937.2 Remodeling of the Host Cell Compartment by Trichinella 67137.3 Parasite Molecules Involved in the Remodeling and Maintenance
of the Nurse Cell Complex 67937.4 The Immunology of the Nurse Cell 68437.5 Future Work and Outlook 686
References 686
Index 689
XVI Contents
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List of Contributors
XVII
Lee-Ann H. AllenDepartments of Microbiology andInternal MedicineThe Inflammation Program and theVA Medical CenterIowa City, IA 52242USA
Damien BalestrinoInstitut PasteurUnité des Interactions BactériesCellules75015 ParisFranceandINSERMU60475015 ParisFranceandINRAUSC202075015 ParisFrance
Kristine von BargenCell Biology InstituteUniversity of BonnUlrich-Haberland-Str. 61a53121 BonnGermany
Martin BaumgartnerDivision of Molecular PathobiologyDCR-VPHVetsuisse Faculty BernUniversity of BernLänggassstr. 1223012 BernSwitzerland
Ulrike BeckenCell Biology InstituteUniversity of BonnUlrich-Haberland-Str. 61a53121 BonnGermany
William J. BroughtonLBMPSSciences IIIUniversité de Genève30 Quai Ernest-Ansermet1211 Geneva 4Switzerland
Philip D. ButcherMedical MicrobiologyCentre for InfectionDivision of Cellular & MolecularMedicineSt. Georges University of LondonCranmer Terrace, TootingLondon SW17 0REUK
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Gabriela CosíoProgram in Cell BiologyHospital for Sick Children555 University AvenueToronto, Ontario M5G 1X8Canada
Pascale CossartInstitut PasteurUnité des Interactions BactériesCellules75015 ParisFranceandINSERMU60475015 ParisFranceandINRAUSC202075015 ParisFrance
Deborah DeanCenter for Immunobiology andVaccine DevelopmentChildrens Hospital Oakland ResearchInstituteOakland, CAUSAandUCB and UCSF Joint Graduate Groupin BioengineeringUniversity of California at BerkeleyBerkeley, CAUSAandUniversity of California at San FranciscoSan Francisco, CAUSA
andDepartment of MedicineUniversity of California at San FranciscoSan Francisco, CAUSA
William J. DeakinLBMPSSciences IIIUniversité de Genève30 Quai Ernest Ansermet1211 Geneva 4Switzerland
Albert DescoteauxINRS-Institut Armand-FrappierUniversité du QuébecLaval, Quebec H7V 1B7Canada
Régis DieckmannDépartement de BiochimieFaculté des SciencesUniversité de GenèveSciences II30 quai Ernest Ansermet1211 Geneva 4Switzerland
Dirk DobbelaereDivision of Molecular PathobiologyDCR-VPHVetsuisse Faculty BernUniversity of BernLänggassstr. 1223012 BernSwitzerland
Heike FeldhaarLehrstuhl für VerhaltensbiologieUniversität OsnabrückBarbarastr. 1149076 OsnabrückGermany
XVIII List of Contributors
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Stacey D. GilkCoxiella Pathogenesis SectionLaboratory of Intracellular ParasitesRocky Mountain LaboratoriesNational Institute of Allergy andInfectious DiseasesNational Institutes of HealthHamilton, MT 59840USA
Jean-Pierre GorvelCentre dImmunologie deMarseille-Luminycase 90613288 Marseille Cedex 9France
David B. GuilianoInfectious and Tropical DiseasesDivision of Infection and ImmunityWindeyer Building46 Cleveland StreetLondon W1T 4JFUK
Gareth GriffithsElectronmicroscopical Unitfor Biological SciencesUniversity of OsloP.O. Box 1062, Blindern0316 OsloNorway
Sergio GrinsteinProgram in Cell BiologyHospital for Sick Children555 University AvenueToronto, Ontario M5G 1X8Canada
Roy GrossLehrstuhl für MikrobiologieBiozentrumUniversität WürzburgAm Hubland97074 WürzburgGermany
Maximiliano G. GutierrezHelmholtz-Zentrum fürInfektionsforschung GmbHInhoffenstr. 738124 BraunschweigGermany
Albert HaasCell Biology InstituteUniversity of BonnUlrich-Haberland-Str. 61a53121 BonnGermany
Ted HackstadtHost–Parasite Interactions SectionLaboratory of Intracellular ParasitesRocky Mountain LaboratoriesNational Institute of Allergy andInfectious DiseasesNational Institutes of HealthHamilton, MT 59840USA
Robert A. HeinzenCoxiella Pathogenesis SectionLaboratory of Intracellular ParasitesRocky Mountain LaboratoriesNational Institute of Allergy andInfectious DiseasesNational Institutes of HealthHamilton, MT 59840USA
List of Contributors XIX
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Monica HagedornDépartement de BiochimieFaculté des SciencesUniversité de GenèveSciences II30 quai Ernest Ansermet1211 Geneva 4Switzerland
Alyssa IngmundsonSection of Microbial PathogenesisYale University School of MedicineBoyer Center for Molecular Medicine295 Congress AvenueNew Haven, CT 06536USA
Monika KaldeCentre dImmunologie deMarseille-Luminycase 90613288 Marseille Cedex 9France
Kumiko KambaraLBMPSSciences IIIUniversité de Genève30 Quai Ernest Ansermet1211 Geneva 4Switzerland
Daniel S. KorbelCentre for Digestive DiseasesThe Blizard InstituteBarts and The London School ofMedicine and DentistryQueen Mary, University of London4 Network StreetLondon E1 2ATUK
andLondon School of Hygiene andTropical MedicineDepartment of Infectious andTropical DiseasesImmunology UnitKeppel StreetLondon WC1 7HTUK
Goran KovacevicFaculty of ScienceUniversity of ZagrebRooseveltov trg 610000 ZagrebCroatia
Wolfgang LöffelhardtMax F. Perutz LaboratoriesUniversity of ViennaDepartment of BiochemistryDr. Bohrgasse 91030 ViennaAustria
Klaus LingelbachFB BiologyDepartment of ParasitologyPhilipps-University MarburgKarl-von-Frisch-Str. 835043 MarburgGermany
Julia MallégolINRS-Institut Armand-FrappierUniversité du QuébecLaval, Quebec H7V 1B7Canada
Christine MatteINRS-Institut Armand-FrappierUniversité du QuébecLaval, Quebec H7V 1B7Canada
XX List of Contributors
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Edgardo MorenoPrograma de Investigaciónen Enfermedades TropicalesEscuela de Medicina Veterinaria304–3000 HerediaCosta Rica
Simon L. NewmanDivision of Infectious DiseasesUniversity of Cincinatti Col. Med.P.O. Box 670560Cincinatti, OH 45267-0560USA
Yelena OksovLaboratory of Electron MicroscopyLindsey F. Kimball Research InstituteNew York Blood CenterNew York, NY 10021USA
Jude M. PrzyborskiFB BiologyDepartment of ParasitologyPhilipps-University MarburgKarl-von-Frisch-Str. 835043 MarburgGermany
Elena RydkinaDepartments of Microbiology/Immunology and MedicineUniversity of Rochester Medical Schoolof Medicine and Dentistry601 Elmwood AvenueRochester, NY 14642USA
Yasuko RikihisaDepartment of Veterinary BiosciencesCollege of Veterinary MedicineThe Ohio State University1925 Coffey RoadColumbus, OH 43210USA
Craig R. RoySection of Microbial PathogenesisYale University School of MedicineBoyer Center for Molecular Medicine295 Congress AvenueNew Haven, CT 06536USA
Sanjeev K. SahniDepartments of Microbiology/Immunology and MedicineUniversity of Rochester Medical Schoolof Medicine and Dentistry601 Elmwood, AvenueRochester NY 14642USA
Philippe SansonettiUnité de Pathogénie MicrobienneMoléculaireInstitut PasteurParisFranceandUnité 786Institut National de la Santé etde la Recherche MédicaleInserm U786ParisFrance
Ulrich E. SchaibleResearch Center BorstelLeibniz-Zentrum für Medizin undBiowissenschaftenDepartment of Molecular InfectionResearchParkallee 1-4023845 BorstelGermany
List of Contributors XXI
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andLondon School of Hygiene andTropical MedicineDepartment of Infectious andTropical DiseasesImmunology UnitKeppel StreetLondon WC1 7HTUK
Bianca E. SchneiderInfectious and Tropical DiseasesImmunology UnitLondon School of Hygiene andTropical MedicineKeppel StreetLondon WC1 7HTUK
Grant S. SchulertDepartments of Microbiology andInternal MedicineThe Inflammation Program and theVA Medical CenterIowa City, IA 52242USA
L. David SibleyDepartment of Molecular MicrobiologyWashington University School ofMedicineSt. Louis, MO 63110USA
David J. SilvermanDepartment of Microbiology andImmunologyUniversity of Maryland School ofMedicineBaltimore, MDUSA
Thierry SoldatiDépartement de BiochimieFaculté des SciencesUniversité de GenèveSciences II30 quai Ernest Ansermet1211 Geneva 4Switzerland
Naraporn SomboonnaCenter for Immunobiology andVaccine DevelopmentChildrens Hospital Oakland ResearchInstituteOakland, CAUSAandUCB and UCSF Joint Graduate Groupin BioengineeringUniversity of California at BerkeleyBerkeley, CAUSAandUniversity of California at San FranciscoSan Francisco, CAUSAandNational Center for GeneticEngineering and BiotechnologyNational Science and TechnologyDevelopment AgencyPathumthani 12120Thailand
Olivia Steele-MortimerLaboratory of Intracellular ParasitesNational Institutes of Allergy andInfectious DiseasesNational Institutes of HealthRocky Mountain LaboratoriesHamilton, MT 59840USA
XXII List of Contributors
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Jürgen M. SteinerMax F. Perutz LaboratoriesUniversity of ViennaDepartment of BiochemistryDr. Bohrgasse 91030 ViennaAustria
Guy Tran Van NhieuInserm U 971Unité de CommunicationsIntercellulaires et InfectionsMicrobiennosCollège de France11, Place Marcelin Berthelot75005 Paris CedexFrance
Michael SteinertInstitut für MikrobiologieTechnische Universität BraunschweigSpielmannstr. 738106 BraunschweigGermany
Joanne M. StevensDivision of MicrobiologyInstitute for Animal HealthComptonBerkshire RG20 7NNUK
Mark P. StevensDivision of MicrobiologyInstitute for Animal HealthComptonBerkshire RG20 7NNUK
Martin C. TaylorLondon School of Hygiene andTropical MedicineKeppel StreetLondon WC1 7HTUK
Daniel E. VothCoxiella Pathogenesis SectionLaboratory of Intracellular ParasitesRocky Mountain LaboratoriesNational Institute of Allergy andInfectious DiseasesNational Institutes of HealthHamilton, MT 59840USA
Simon J. WaddellMedical MicrobiologyCentre for InfectionDivision of Cellular & MolecularMedicineSt. Georges University of LondonCranmer Terrace, TootingLondon SW17 0REUK
Markus WinterbergFB BiologyDepartment of ParasitologyPhilipps-University MarburgKarl-von-Frisch-Str. 835043 MarburgGermany
List of Contributors XXIII
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Part IGeneral Aspects
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1Introduction: The Evolution of Intracellular Life Formsand their NichesUlrich E. Schaible and Albert Haas
As species are produced and exterminated by slowly acting andstill existing causes, and not by miraculous acts of creation and bycatastrophes; and as the most important of all causes of organicchange is one which is almost independent of altered and perhapssuddenly altered physical conditions, namely, the mutual relation oforganism to organism, – the improvement of one being entailing theimprovement or extermination of others. Charles Darwin
1.1A Short History of Theories and Discoveries
The complex mutual relationship between intracellular microbes and their hostcells is a challenging field of research and requires the perspective of evolutionbiology. The individual host–microbe interactions covered in this book all raise thefollowing questions: how domicrobes enter, survive and proliferate in, and how dothey exit host cells? And how can intracellular niches be characterized and what arethe benefits of intracellular life for the microbes and its consequences for the hostcell? The question, however, is how and under what selective pressure did theseinteractions evolve? The year 2009 marks the 200th birthday of Charles Darwin(1809–1882; 12th February 1809), and, more importantly, the 150th anniversary ofthe publication of his most important book The Origin of Species by Means of NaturalSelection (24th November 1859) [1]. In this eminent and highly disputed andprovocatively revolutionary work, Darwin outlined the concept of evolution bynatural selection in the struggle of life. The concept of interspecies competition asthe driving force for the evolution of all bacterial, animal and plant species laid thebasis for modern day biology.Louis Pasteur (1822–1895) and others proved that microbial life did not arise
spontaneously andmiraculously, but rather due to the omnipresence of microorgan-isms, an important fact for food preservation and the consequential establishment ofsterilization techniques. The seminalwork of the nineteenth-centurymicrobiologists
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set the path to study the novel complexity of interspecies interactions in naturalscience and medical research. Although infectious diseases were an importantdeterminant for human history, causingmigration, settlement and conflict behavior,it was not until the nineteenth century that infectious agents were identified ascausative agents for certain diseases rather than the diseases being of mysteriousorigins. The time between the end of the nineteenth and the beginning of thetwentieth century was the high season of bacteriology, during which a huge numberofmicrobial species were identified using newly developed culture techniques.Manyof these microbes were associated with humans, animals or plants, and they wereeither pathogens, beneficial symbionts or commensals. A number of thosemicrobeshad chosen other unicellular or multicellular organisms as their ecological niches.Finally, infectious diseases were recognized as the driving force for the evolution ofthe innate and, in vertebrates, the acquired immune systems (Chapter 12).Robert Koch (1843–1910) and his colleagues identified the first intracellular
pathogenic bacterium, the tubercle bacillus (Mycobacterium tuberculosis). In thelate nineteenth century tuberculosis was the prime cause of death in the metro-politan areas of Europe and North America, stirring up intensive medical andscientific interest. At around the same time, an important virulence trait of thetubercle bacillus, that is, living in macrophages, was described by Elie Metchnikoff(1845–1916), the founder of phagocyte biology. This is still a prime topic intuberculosis research today (see Chapter 19). Metchnikoff was the first to observethe phagocytosis of bacteria by phagocytes in 1883 during his time at the VienneseInstitute of Zoology and he also pointed out the importance of these cells in hostresponse and inflammation [2, 3]. The termmacrophage was attributed to him andmade him the founder of innate immunity. In 1908, he received the Nobel Prizefor his achievements. Metchnikoff was also the first to observe tubercle bacillithriving intracellularly in macrophages (Figure 1.1) [4]. However, it was not untilthe last quarter of the twentieth century that scientists started to study thevirulence factors of pathogens, and that intracellular pathogens (and symbionts)were highlighted for their unique capabilities to survive within and manipulatetheir host cells.The identification of intracellular survival mechanisms was made possible
by novel techniques in cell biology and the arrival of modern molecular genetics.J. A. Armstrong and Philip DArcy Hart [5, 6] were the first to show inhibition ofphagolysosome fusion by the tubercle bacillus. Similar peculiarities of Toxoplasmagondii- and Chlamydia psittaci-containing vacuoles were published in 1979 and1981, respectively [7, 8]. In the last decade of the twentieth century, many virulencetraits of intracellular microbes were elucidated. Genome analyses and moleculartechniques, paired with novel model systems such as yeast two-hybrid screeningtechnology, uncovered pathogenicity islands and plasmids, virulence factors, aswell as host cell target structures. It was discovered that throughout evolution theremust have been a tremendous horizontal gene transfer between differentmicrobesas well as between bacteria and eukaryotes (Chapter 2). Many of those pathogensand their virulence traits will be covered in this book. Some important intracellularmicrobes, such as M. leprae, Chlamydia and Rickettsia, are not yet accessible to
4j 1 Introduction: The Evolution of Intracellular Life Forms and their Niches