yersinia - caister academic pressyersinia systems biology and control edited by elisabeth carniel...

Caister Academic Press

YersiniaSystems Biology and Control

Edited by

Elisabeth CarnielYersinia Research UnitNational Reference Laboratory and WHO Collaborating Center for YersiniaInstitut PasteurParisFrance

and

B. Joseph HinnebuschRocky Mountain LaboratoriesNational Institute of Allergy and Infectious DiseasesNational Institutes of HealthHamilton, MTUSA

caister.com/yersinia

Copyright © 2012

Caister Academic Press Norfolk, UK

www.caister.com

British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library

ISBN: 978-1-908230-05-8

Description or mention of instrumentation, software, or other products in this book does not imply endorsement by the author or publisher. The author and publisher do not assume responsibility for the validity of any products or procedures mentioned or described in this book or for the consequences of their use.

All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior permission of the publisher. No claim to original U.S. Government works.

Cover design adapted from Figure 2.2.

Printed and bound in Great Britain


Contents

Contributors v

Preface ix

1 Transcriptional Profiling of the Yersinia pestis Life Cycle 1B. Joseph Hinnebusch, Florent Sebbane and Viveka Vadyvaloo

2 Yersinia pseudotuberculosis Gene Expression in Plasma 19Michael Marceau and Michel Simonet

3 Host Transcriptome Responses to Yersinia pestis Infection 43Zongmin Du and Ruifu Yang

4 Transcriptional Profiling of Yersinia enterocolitica–Host Cell Interactions 59Reinhard Hoffmann, Ekaterina Lenk and Jürgen Heesemann

5 Proteome Analysis of Yersinia pestis and the Mammalian Host Response to Yersinia pestis Infection 69Rembert Pieper and Scott N. Peterson

6 Yersinia pestis Metabolic Network 83Ali Navid and Eivind Almaas

7 Plague Treatment and Resistance to Antimicrobial Agents 109Marc Galimand and Patrice Courvalin

8 Enteropathogenic Yersinia: Antibiotic Resistance and Susceptibility of Yersinia enterocolitica and Yersinia pseudotuberculosis 115Jeanette N. Pham

9 Acellular Vaccines Against Plague 123E. Diane Williamson and Petra C.F. Oyston

10 Live Vaccines Against Plague and Pseudotuberculosis 143Christian E. Demeure

11 North American Plague Models of Enzootic Maintenance, Epizootic Spread, and Spatial and Temporal Distributions 169Rebecca J. Eisen and Kenneth L. Gage


Contentsiv |

12 Surveillance and Control of Plague 183Jean-Marc Duplantier

13 Tracing of Enteropathogenic Yersinia 201Maria Fredriksson-Ahomaa

14 Surveillance and Control of Enteric Yersinioses 217Truls Nesbakken

Index 239

Colour plate A1


Preface

Systems biology, made possible by advances in biotechnology and bioinformatics during the last decade, is becoming an increasingly prominent methodology in infectious disease research. Systems biology can mean different things to different people, but at its core is a com-prehensive, integrative, and quantitative analysis of all components of a biological system, such as an intact cell, organism, or community. The ambitious ultimate goal of systems biology is to understand how all the components interact to enable the system to function successfully in different conditions; for example, how a host responds to infection and how a microbe adapts to survive within its host or in an external eco-system. Deciphering these dynamic biological networks is expected to disclose new molecular targets for disease control strategies. The first part of this book reviews some of the pioneering

applications of systems biology to study host-pathogen interactions of the medically important Yersinia species. The eventual synthesis of these and future analyses should provide a more holis-tic perspective of Yersinia infection mechanisms. The epidemiology and control of plague and yersiniosis is a second focus of the book. Interest-ingly, infectious disease ecology has historically relied on systems analysis, in which the pathogen is but one component of a complex ecosystem. Discovery of the important elements of the ecosystem and characterizing the interactions that lead to disease outbreaks in a population represents another level of systems biology that is critical for effective public health surveillance and control measures. We thank Annette Griffin and Horizon Scientific Press for the opportunity to organize this volume and all of the authors for their outstanding contributions.

Elisabeth Carniel and B. Joseph Hinnebusch


Index

Aαβ1 integrin 64Abattoir 212, 223–225, 227, 232ABC transporter 22–26, 73, 74, 78, 85, 129, 153Abundance 19, 46, 54, 69–71, 73, 75–80, 150, 174, 179,

183, 184, 187–192, 196Acetate 28, 34, 35, 42, 79, 94, 95, 97, 103Adenovirus 149, 157, 158, 162, 163, 165, 167Adjuvant 126, 131, 133, 147, 150, 157, 158, 160. See also

VaccineAerosol 113, 128, 129, 132, 134, 144, 145, 149AFLP 207Ail 10, 12, 15–17, 40, 69, 73, 75, 76, 78, 81, 202, 205, 214Alexandre Yersin 144Alpha-ketoglutarate dehydrogenase 35Alum 126, 160Amikacin 113, 115. See also AntibioticAminoglycosides 110, 111, 113–115, 119. See also

AntibioticAmoxicillin-clavulanate 116–118. See also AntibioticAmoxi-clav see amoxicillin-clavunalateAmpicillin 110, 111, 115–121. See also AntibioticAnimal 2, 19, 26, 43–47, 53, 54, 110, 123, 125–127,

131–135, 138, 140, 142, 143, 145, 146, 148, 149, 155, 156, 158, 159, 161, 165, 171, 173, 174, 176, 178, 180, 181, 186–190, 198, 201, 202, 204, 208–212, 214, 217, 219, 222–224, 226, 227, 230–234. See also Wild animals

Analysis of variance 21, 23, 29, 36, 39, 41ANOVA see Analysis of varianceAnti F1 antibodies 161, 190. See also F1 antigenAntiapoptotic genes 64Anti-bactericidal peptides 150. See also Bacteriocin

pesticinAntibiotic 85, 90, 110–115, 117, 119–121, 143–145, 157,

158, 161, 173, 183, 184Antibiotic-resistant strain 143. See also AntibioticAnticoagulants 192, 193, 197Anti-inflammatory cytokine IL-10 see IL-10Antimicrobial susceptibility 121. See also AntibioticAnti-phagocytic 44, 150Antiqua 86, 87, 103, 184. See also BiovarsApoptosis 45–47, 49, 52, 56, 62, 128, 133, 144, 152, 164

Apoptosis inhibitors 46araC 87, 88ARE motif 61

AroaroA 7, 124, 137, 138, 140, 142, 147, 149, 156,

162–164, 166, 167aroC 149, 156, 167aroD 156, 163, 167

Aspartase 6, 16, 18, 86, 89, 93, 97, 102, 103, 107aspA 6, 89, 91–93, 95, 97, 98

Attenuated vaccine strains 124. See also VaccineAustralia 117, 126, 143, 195, 197, 219, 231Auxotrophy 147Azithromycin 115. See also Antibiotic

Bβ-barrel 69, 73, 76, 78β-lactamase see Beta-lactamaseBacteriocin pesticin 144Bacterioferritin 26, 27, 40Bait boxes 183, 192, 193BALB/c mice see MouseB-cell lymphoma protein 2 (Bcl-2) 46Beta-lactamase 115, 116, 118–121. See also AntibioticBiofilm 2–4, 9–12, 16–18, 69, 75, 78, 100–103, 105, 106,

127, 170Biotinylation 76Bioserotype 115, 116, 120, 202, 203, 206, 207, 209,

212–214, 217–2202/O:5,27 119, 202, 203, 209, 218, 2202/O:9 116, 117, 202, 203, 209, 215, 217–2204/O:3 116–120, 202–204, 208, 209, 212, 214, 217–

221, 223, 226, 228, 229, 233Bioterrorist weapon 143, 144Biotypes 103, 117, 118, 121, 184, 201, 202, 207, 213,

217–221biotype 1A 202, 205, 207, 214, 218, 219

Biovars 51, 70, 84, 86, 87, 93, 107, 144Blood stream 144Bone marrow derived macrophages (BMDB) see

MacrophageBronchoalveolar lavage fluids 44Bubonic plague see PlagueBurrow 180, 183, 184, 189, 191–195, 198

CC57BL/6 mice see MouseC5AR see Complement


Index240 |

Calcium 37, 40, 49, 77, 78, 81, 91, 94, 102–104, 106, 141Canada 117, 176, 203, 218–220, 236Carbapenem 119, 120. See also AntibioticCarnivore 189, 190, 195. See also AnimalsCase–control studies 208, 218Caspase 46, 133, 142, 167CCP see Critical control pointCD14 47, 48, 53, 61, 63Cefotaxime 116, 117, 119–121. See also AntibioticCeftriaxone 119, 120. See also AntibioticCephalosporinase 115. See also AntibioticCephalosporins 110, 111, 115, 116, 119, 120. See also

AntibioticChemokines 44–46, 48, 51, 53, 60, 61Chloramphenicol 106, 109–111, 115, 119. See also

AntibioticChromatography 70, 74

two-dimensional liquid chromatography 70immunochromatography 187

CIN 190, 204Ciprofloxacin 110, 113–115, 117, 119, 120. See also

AntibioticCitrobacter freundii 116Class A β-lactamase 115, 116, 118. See also AntibioticClass C 115, 116. See also AntibioticClavulanate 117–119. See also AntibioticClinical trials 123, 125, 131, 156, 163Comparative transcriptomics 5Complement

component 48component 5 receptor (C5AR) 46

Conjugative plasmid see PlasmidControl 16, 17, 21, 28, 37, 41, 45, 47, 50, 55, 56, 59, 62,

79, 103, 123, 133, 134, 136, 139, 147, 159, 160, 164–166, 169, 173, 178–181, 183–186, 188, 189, 192–199, 208, 210, 212, 215, 217, 218, 220–223, 225, 227, 229, 230, 232, 233, 235, 236

Correlatesof immunity 161. See also Vaccineof protection 132, 135, 140. See also Vaccine

Cortisone 152, 166Co-trimoxazole 119, 120. See also AntibioticCrabtree effect 28Critical control point 208, 218, 222, 227Cross-reacting immunological material 98Cryosection 60CryptFind 85, 88–90, 96Cryptic genes 85, 88, 89, 90, 96, 104Cystathionine gamma-lyase 98

Ddam see DNA adenine methylaseDamage-associated molecular pattern (DAMP) 60Decontamination 222, 227Dendritic cells 61, 63, 65, 152, 163, 164, 166, 167,Detection 20, 38, 54, 70, 77, 113, 116, 121, 127, 141, 161,

187, 196, 197, 201, 204–206, 209, 211–216, 218, 228, 234, 235, 237

Devignat 86, 87, 103, 154, 184, 196Diagnosis 109, 186, 187, 195, 216Discriminatory power 206, 207, 211

Diversity 85, 105, 161, 162, 174, 193, 195, 198, 206, 208, 214, 215, 234, 235

DNA adenine methylase (dam) 147, 164DNA microarray see MicroarrayDraining lymph node see Lymph nodeDual specificity phosphatase 1 47, 48Dynamics 50, 52, 103, 169, 172, 180–182, 189, 197

EEfflux

systems 8, 9protein 23, 25, 39

Enterobacter cloacae 116Enteropathogenic 43, 54, 80, 115, 119, 121, 143, 151,

154–156, 201–209, 211–214, 216, 217, 230, 233Enterotoxin 205Environment 1, 3, 4, 6, 10, 11, 15, 19, 20, 22, 35, 37, 38,

40, 41, 44, 60, 69–73, 77, 80–92, 94, 95, 97–99, 101, 103, 104, 106, 109, 112, 145, 176, 187, 189, 191, 193, 194, 201, 204, 205, 210–212, 215, 220, 224, 231, 233–235

Enzootic 123, 169–173, 175, 176, 178, 185Enzyme

A 115–118, 121. See also AntibioticB 115–120. See also Antibiotic

Epidemic 102, 125, 154, 169, 173, 174, 180, 184, 185, 186, 192–195, 198, 211, 219, 231, 232. See also Pandemics

Epidemiology 113, 120, 141, 166, 170, 196–198, 211–213, 216, 232–234

Epizootic 16, 103, 123, 169–176, 178–180, 182, 184, 194, 198, 230. See also Animals

erpA 28, 33EV

NIIEG 146, 148EV76 80, 141, 145, 146, 148, 150, 152–154, 160,

161, 166exb 8, 22, 26Experimental design 20

FF1 antigen 17, 69, 72, 80, 125–127, 130, 137, 138, 140–

142, 150, 151, 157, 158, 165–167, 187, 195Farm 210, 211, 214, 221, 223, 230, 232FBA see Flux balance analysisFerritin 26, 27, 40, 43, 44,Flagellin 131, 132, 140, 160Flea 1–13, 15–17, 20, 35, 40, 69, 72, 77, 78, 79, 82, 86,

88, 91, 94, 97, 100–104, 106, 109, 112, 113, 123, 126, 127, 141, 143–145, 167, 169–174, 176, 179–185, 187, 189–198

flea-borne transmission 16, 81, 170–172, 179, 181, 182

vector 1, 9, 16–18, 42, 69, 70, 72, 77, 78, 81, 85, 91, 100, 103, 104, 105, 107, 112, 142, 177, 180, 181, 195–197

Fluoroquinolones 110, 113–115, 119. See also AntibioticFlux balance analysis 87–90Focus 44, 66, 84, 113, 123, 176, 178, 183–188, 190,

192–194, 198, 221, 224, 237Food 1, 3, 6, 19, 83, 103, 112, 144, 174, 189, 193, 201,

202–206, 208, 209, 211–215Fresh produce 201, 211, 231. See also Food


Index | 241

GGene expression microarray see TranscriptomeGenome 1, 4, 10, 16, 17, 19–21, 28, 40, 47, 55–56, 69–71,

81, 82, 84, 85, 87–90, 93, 98–100, 102–107, 127, 137, 138, 140, 146, 154, 163, 168, 206, 208, 212

Genotypic 206Gentamicin 109, 110, 113–115, 117, 119, 120. See also

AntibioticGerbil 184, 189, 192. See also AnimalsGILZ 65Girard and Robic 125, 144, 145, 164glpD see GlucoseGlucose 7, 15, 28, 34, 35, 39, 92–95, 103, 104, 106

glpD 87, 105glucose 6-phosphate dehydrogenase 6, 14, 17, 86, 90,

93, 105glucose overflow 28, 35, 42

Glutamate dehydrogenase 95, 98Glycerol-3-phosphate dehydrogenase 29, 87, 105Glyoxylate

cycle 34shunt 94, 95

gmhA 12, 16, 101GmhA 101, 103Growth factor-β (TGF-β) 45, 49, 53Guinea pig 99, 124–126, 131, 133, 134, 139–141, 145,

146, 148, 155, 164–166

HHACCP see Hazard analysis critical control pointHaffkine 144, 145. See also VaccineHazard analysis critical control point 222, 224, 230HeLa cells 42, 64Hemin storage 16, 17, 23, 104, 106

Hms 8–12, 16, 17, 22, 23, 41, 75, 78, 101, 104–106, 145, 152

High-pathogenicity island 22, 40, 75, 100, 137, 144, 145, 148, 152–155, 163, 202, 212, 213

yersiniabactin 4, 8, 14, 22, 25, 26, 41, 69, 72, 73, 75, 88, 100, 102, 105, 106, 145, 153

High-pathogenic 202Hms see Hemin storageHmu 8, 14, 22, 23, 78, 100, 104, 163Horizontal gene transfer 112Host cell transcriptome see TranscriptomeHPI see High-pathogenicity islandHtrA 8, 80, 149, 156, 163, 167Hypothetical protein 13–15, 20, 25, 39, 78, 80

IIdentification 11, 16, 42, 69–71, 73, 74, 77, 78, 80, 81IFNγ 46, 51, 62–64, 134, 159–161IHR see International Health RegulationImmunoglobulin

IgA 156, 158IgG 80, 133, 142, 156, 158

InterleukinIL-4 46, 51, 134, 138, 160, 164IL-6 45IL-10 44, 56, 61, 63, 129, 134, 141, 151, 160, 167IL-17 51, 160, 165

IL-18 47, 63IlvN 96Imipenem 116–121. See also AntibioticIn vivo expression technology (IVET) 19Inc

A/C see PlasmidP see Plasmid

Induction 1, 4, 9, 22, 38, 46, 51, 56, 61, 63, 65, 77, 94, 102, 110, 116, 117, 119, 121, 129, 133, 134, 141, 151, 158, 162, 166, 167

Inflammasome 147, 163Inflammatory response 44–46, 54, 55, 63, 66Injectisome see pYVInner membrane 35, 73

protein 13, 25Insecticide 145, 183, 191–193, 195, 197,198International Health Regulation 183, 185, 186, 199Invasin 35, 37, 41, 137, 202

inv gene 35, 37, 41, 86, 205Inv protein 64, 66, 202

Iron 22, 24, 27, 28–33, 35, 69, 70, 78–80, 100, 145, 152,homeostasis 71, 78, 79regulation 37, 38siderophore 8, 15, 24–27, 75, 78, 100, 145, 153starvation 8–10, 19, 27, 35, 38, 69, 78, 79–81, 100,

145storage 79, 100sulfur (Fe–S) cluster 27–33, 40transporter 8, 23, 24, 39, 78, 79, 100uptake 4, 12, 14, 15, 22, 23, 26, 27, 38, 72, 73, 78, 81,

100, 124, 144, 152, 153, 202Isolation 4, 5, 71, 72, 103, 109, 110, 130, 136, 181, 204,

210, 212, 214, 217, 218, 233, 235, 236ITC 204

JJ774A.1 46

KKat

katA 8, 27katG 29, 101

Killed whole-cell vaccine see VaccineKlebsiella

oxytoca 115pneumoniae 115

KLF2 65, 66Knockouts 90, 134

LLactococcus lactis 155, 158, 163LCR see Low-calcium responseLcrV see pYVLegislation 194Leucine-rich repeat protein 72Liver 4, 19, 44, 47, 51, 53, 63, 144, 156, 209, 230Lipopolysaccharide 10, 11, 44, 46, 60, 144, 150, 160Low-calcium response see pYVLPS see LipopolysaccharideLpxL/LpxM acyl-transferases 150Lymph node 2, 4, 44, 45, 54, 144


Index242 |

MMacroarray 20, 21. See also MicroarrayMacrolides 115. See also AntibioticMacrophage 4, 13, 17, 44–46, 50, 55–57, 60, 61, 63–67,

72, 81, 82, 104, 106, 127, 139, 142, 147, 151–153, 156, 159–161, 168

bone marrow derived macrophages (BMDB) 46, 64macrophage inflammatory protein-1α 45

MAPK see Mitogen activated protein kinaseMass spectrometry 69–71, 77

LC-MS/MS 70, 80LC-ESI-MS/MS 70, 73, 77MALDI-MS 70MALDI-TOF-MS 80MALDI-TOFTOF 70, 73peptide mass fingerprinting 70

Mediaevalis 70, 86, 87. See also BiovarsMeat. See also Food

chain 217, 221, 222, 227, 235inspection 224, 227, 235

Meiotrophy 88Meropenem 120. See also AntibioticMetabolism 7, 20, 27, 28, 41, 42, 53, 69, 79, 83–85,

87–100, 102, 103, 105, 106, 144, 233Microarray 1, 4, 5, 15, 17, 20, 21, 41, 45–47, 51, 53–55, 59,

64–66, 69, 70, 80, 81, 85, 89, 92, 94, 95, 97–99, 101, 104, 106, 146, 165, 168, 205, 215, 216. See also Macroarray

Microtus 51, 84, 86, 87, 107, 128, 190. See also BiovarsMini-ferritin 27Mini-pYV see pYVMIP-1α see Macrophage inflammatory protein-1αMitogen activated protein kinase 49, 64, 67MLVA 197, 199, 207, 208. See also TypingModel 2, 4, 5, 17, 18, 19, 22, 35, 43–47, 50, 51, 53–56, 59,

64, 66, 67, 69, 72, 82, 84, 85, 87–90, 103, 106, 107, 110, 113, 123, 126, 129, 131–135, 138–142, 151, 164–166, 168–181, 184, 188–190, 194, 196–198, 229, 232, 233

Modelling 85, 87, 96, 105, 107, 169, 170, 172, 173, 176, 178–181, 183, 194, 196, 234

climate 173–175, 178, 179, 231metapopulation 172, 194susceptible-infectious-recovered (SIR) 171–173vector efficiency 171, 172vectorial capacity 172, 173weather see climate

Monitoring 1, 145, 161, 183, 184, 190, 198, 212, 214, 221, 233

MouseBALB/c mice 46, 47, 56, 63, 128, 135, 141, 142, 167C57BL/6 mice 63, 127, 135protection assay (MPI) 159SCID/Beige mice 134–136, 138, 159, 164specific pathogen free 223spleen 60

Moxifloxacin 115. See also AntibioticMultidrug resistance 112–114, 196. See also AntibioticMultilocus sequence typing (MLST) 207, 208. See also

Typing

NNapA 8, 31, 86

Neutrophil 43–45, 51, 52, 56, 59, 60, 63, 67, 133, 139, 152, 159

New Zealand 117, 219, 231, 232, 234NFκB signalling 64Nitrate reductase 31, 87, 94Nitric oxide synthase (NOS) 56, 140, 159, 166NK cell 46, 47, 64Non-human primate 131, 132, 141, 162. See also AnimalsNon-pathogenic 60, 201, 202, 204, 205, 210, 215, 219,

220, 227Normalization 21

OO-antigen 144, 155. See also LPSOmp

OmpA 10, 37, 73, 75, 76, 80ompC 10, 37, 42, 73, 75, 78ompC2 37

Opsonization 151, 159, 161Orientalis 22, 51, 86, 87, 184. See also BiovarsOtten 125, 140, 144, 145Outbreak 123, 125, 132, 137, 143–146, 173, 181–183,

195, 198, 201–203, 206–208, 210, 211, 213, 215, 217–219, 229, 231–236. See also Epidemic

Outer membrane 72outer surface proteins 9, 10proteins 10, 14, 21, 23, 24, 37, 69, 71, 74–76, 129proteome 78

Oxaloacetate 34, 91–93, 95, 97–99OxyR 8, 79, 80, 101

PPAGE 76

BN-PAGE 76PAMPs see Pathogen-associated molecular patternsPandemics 43, 104, 123, 143, 144, 184, 196Pathogen-associated molecular patterns 60, 63Pattern recognition receptors 60, 61, 67pCDI see pYVPCR 21, 105, 181, 187, 191, 196, 197, 201, 205–208, 210,

213, 214–216, 218, 223, 225, 230, 234Pectinesterase 72Pentose phosphate pathway 6, 8, 14, 90, 92–94, 98Peptidoglycan 73, 75, 160Peripheral myelin protein 22 (PMP22) 46Periplasm 71, 72, 76, 78

periplasmic protein 14, 15, 23–26, 31, 72, 73, 79, 82, 87, 129

Pesticide 179, 192, 194, 199. See also RodenticidePesticin see Bacteriocin pesticinPestoides 16, 87, 89, 93, 102, 151, 167. See also BiovarsPets 209, 210, 212, 219, 223, 230, 233Peyer’s patches 19, 66, 156PFGE see Pulsed-field gel electrophoresispFra 3, 126, 144

Yersinia murine toxin 3, 12, 69, 72, 79, 137Pgm locus 70, 71, 145, 146, 150, 152, 153pH6 antigen 12, 14, 37, 72, 75, 150, 153Phagocytosis 44, 50, 55, 103, 126, 128, 142, 144, 151,

153, 159, 161–163Phenotypic 3, 81, 83–85, 104, 206, 213–215, 234PhoP/PhoQ 9, 11, 12, 156, 164


Index | 243

Phosphoenolpyruvatecarboxykinase 97carboxylase 91, 92, 97

Phosphoheptose isomerase 101, 102Phosphotransferase

systems 6, 7, 13, 14, 35, 41aminoglycoside 111

Pig 99, 124–126, 131, 133, 134, 139–141, 145, 146, 148, 155, 164–166, 201, 204, 208–210, 212, 214–228, 230–236. See also Pork

Placental growth factor (PLGF1) 45Plague

bubonic 1, 2, 4, 5, 9, 11, 16, 17, 41–46, 50, 51,55, 56, 72, 83, 102, 104, 110, 123, 126, 132, 134–139, 141, 143–150, 152, 154, 156, 162–165, 167, 168, 180, 181, 185, 195, 197

pneumonic 43, 44, 46, 51, 54, 110, 123, 125, 126, 128, 130, 131, 133, 135, 143–154, 156–161, 173

Plasma 13, 16, 19–29, 34–40, 42, 61, 72, 81, 103Plasmid

conjugative plasmid 111, 113, 114, 144IncA/C 109, 111–114. See also AntibioticIncP 111, 114. See also AntibioticpCD1 see pYVpFra see pFrapIP1202 111, 112. See also AntibioticpIP1203 109, 112. See also AntibioticpMT1 see pFrapPCP1 see pPlapYV see pYVR751 111, 114RSF1010 111, 114

Plasminogen activator see pPlapMT1 see pFraPneumonic plague see PlaguePolyamine biosynthesis 101Polysaccharide 78, 101

exopolysaccharide 101, 152Population 19, 86, 103, 123, 132, 133, 145, 161, 169,

171–176, 178–181, 184–187, 189, 190, 193, 194, 217, 221, 224

Pork 201, 203, 208–215, 217–220, 224, 227–229, 231–236. See also Pig

Post-mortem inspection 222, 227pPCP1 see pPlapPla 127, 144

Plasminogen activator Pla 4, 12, 105, 139, 144, 153Prairie dogs 43, 159, 165, 166, 169, 173, 175, 176, 180,

182, 191, 192, 198. See also AnimalsPredictive 28, 59, 89, 171, 184, 188, 190, 196Preventative 192–194, 217, 221, 224, 232Proinflammatory 44, 55, 60, 62, 64, 66

cytokine 43, 45, 47, 61Prophylaxis 109–111, 114, 123, 135, 144Proteomics 69, 70, 81, 84

proteome 15, 27, 37, 38, 69–73, 77, 78, 80–82PRRs see Pattern recognition receptorsPsaA see pH6 antigenPTS see Phosphotransferase systemsPulsed-field gel electrophoresis 201, 206–211. See also

TypingPutrescine 7, 101, 107

Pyruvate oxidase 80pYV 37, 45, 51, 54, 62, 65, 70, 71, 77, 78, 128, 140, 144,

145, 147, 152injectisome 72, 124, 128, 129, 137, 140, 144, 151,

152LcrV 16, 56, 69, 72, 76–78, 80, 81, 130–132, 136–

141, 149–152, 155, 163, 166–168low-calcium response 77, 91, 94, 95, 97–99mini-pYV 64, 65V antigen 16, 44, 76, 124–126, 128–131, 133–142,

145, 147, 150–154, 156–158, 162–168virF 205, 215yadA 36, 37, 40–42, 65, 86, 156, 205yop see YopYsc 36, 40, 65, 72, 75, 77, 78, 80, 81, 128, 129, 139,

144, 152, 165

RR751 see PlasmidRabies 159, 166RAPD 207, 208, 215Rat 1, 5, 6, 13, 16, 43, 47, 50, 51, 54, 56, 102, 109, 111,

112, 126, 130, 136, 141, 171, 172, 180, 185, 189–198. See also Animals

Rattus 188, 190, 195, 198REAP 206, 207, 209–211. See also TypingRe-emerging disease 43, 143Reservoir 85, 88, 102, 109, 143, 158, 159, 162, 171, 172,

180, 181, 183–186, 188, 192–194, 196–198, 201, 210, 211, 217, 219, 220, 230, 231. See also Animals

Resistance 9, 12, 13, 15, 18, 37, 40–42, 46, 55, 64, 66, 78, 81, 102, 103, 107, 109–115, 117, 119, 121, 140, 142, 144, 157, 161, 161, 165, 166, 183, 188, 191, 192, 194–198, 202, 214, 230, 233

Rho family 65RhoB 65

Ribonucleotide reductase (RNR) 27Ribotyping 104, 206, 207, 209, 210, 214RNA-seq 15, 18, 54, 56, 57Rodent 1, 3, 19, 43, 44, 87, 112, 123, 143, 145, 158,

169, 171, 172, 174–176, 178–181, 183, 184, 187–198, 209–211, 219, 222, 230, 231. See also Animals

Rodenticide 145, 183, 189, 192–195, 197, 198. See also Pesticide

RovA 9, 12, 16, 37, 38, 41, 163RSF1010 see Plasmid

SSalmonella 60, 130, 137, 139, 141–143, 147, 153, 156,

157, 162–168, 213, 227, 229, 233, 235, 236enterica 72, 109, 112, 114, 138, 140, 156, 163–167

SCID/Beige mice see MouseSecretome 9–11, 71, 72Septicemia 120Serine hydroxylmethyl transferase 96Serotype 40, 41, 64, 112, 117, 119, 121, 141, 144, 149,

151, 155–157, 202, 203, 206, 208–211, 213, 215, 217, 218, 220, 231, 233, 234, 236

Shrew 188, 189, 211. See also AnimalsSialoglycoprotein endopeptidase 72Sibling species 188, 195. See also AnimalsSiderophore see Iron


Index244 |

Signature tagged mutagenesis 19, 39, 41, 164SLAP see Src-like adapterSlaughter hygiene 217, 224, 225, 227Sod

sodA 8, 27, 156sodB 27, 31, 79

Spermidine 7, 101Specific pathogen free see MouseSPF see Specific pathogen freeSpleen 4, 39, 44–48, 50, 51, 53, 56, 59, 60, 63, 67, 120,

142, 144, 156, 190, 230. See also MouseSplenocytes 63, 135Sporadic 202, 203, 210, 212, 213, 215, 220, 231, 233, 236

cases 211, 215, 217–220Src-like adapter (SLAP) 47STM see Signature tagged mutagenesisStress responses 6Subcellular fractions 70, 71, 77, 80Subunit vaccine see VaccineSuccinate dehydrogenase 6, 13, 30, 35sufABCD 28, 33Sulfite

dehydrogenase 98oxidase 98

Sulfonamides 115. See also AntibioticSurveillance 50, 112, 114, 165, 169, 174, 176, 178–180,

183–186, 188–192, 194–198, 202, 217, 219–221, 224, 225, 231–233, 235

Survey 16, 45, 70–72, 78, 80, 119, 165, 180, 181, 186, 188, 190, 233

Synthetic lethal mutations 90System-level analyses 83, 87

TT cell receptor (TCR)–CD3 complex 47TCA cycle 6, 8, 13, 28, 34, 35, 92, 94, 95, 97, 102Temperature 3, 4, 11, 17, 20, 21, 35–38, 40, 41, 44, 55,

70, 73, 76–78, 81, 82, 85, 91, 92, 97, 101, 102, 104, 105, 125–127, 130, 171, 173–176, 178–181, 203, 204, 207, 217, 222, 226–230, 232–234, 236

Tetracycline 109–111, 113, 115. See also AntibioticT helper

Th1 50, 51, 133, 134, 158, 160Th2 51, 133, 134, 158, 160Th17 51, 160, 165

Tjiwidej 93, 125, 145, 147, 152Toll-like receptor 44, 48, 56, 59, 141, 160, 162, 163, 166,

167TLR2 44, 61, 128, 141, 151TLR4 44, 61, 150, 166TLR6 61, 151,TLR8 47, 63

TMH 90Tn21-like elements 111TNFα 45, 134, 159TLR see Toll-like receptorTonB 8, 14, 22, 23, 25, 26, 42, 72, 75, 78Toolbox system 59Transcription

factor KLF2 (gene klf2) 65, 66factors 45, 60, 62, 64, 80

Transcriptional profiles See TranscriptomeTranscriptional responses 22, 43, 45, 46, 51, 52, 55, 56,

59, 60, 63, 66, 67Transcriptome 4, 5, 6, 13, 19–21, 26, 28, 34, 38, 45, 46,

54–56, 62–64, 66, 101, 102, 104analysis 16, 19, 40, 59, 66, 81, 103gene expression microarray 41, 92, 99host cell transcriptome 62, 64profiling 45

Transgenic plants 158Transglycosylase 78Translocator pore 72, 76Transmission 1, 4, 9, 11, 12, 43, 70, 77, 78, 83, 94, 100,

131, 159, 169, 170–174, 176, 179, 180, 183, 185, 190, 191, 194, 209, 210, 230, 231

blocked flea 2, 4, 11, 12, 170, 172, 179cycle 1, 169, 173, 175,early phase 2–4, 172, 173factors 1, 11, 12, 100flea-borne 1, 2, 4, 20, 43, 44, 77, 86, 126, 170–172,

179human-to-human 110mechanical 170, 171mechanism 4, 170, 173oral 86, 89routes 1, 43, 201, 206, 208, 211, 230

Trap 70, 189, 190, 194Tristetraprolin 61, 67TTP see TristetraprolinTTSS see Type III secretion systemTwo-dimensional gel electrophoresis 70Type III secretion system 17, 37, 38, 44, 55, 76, 106, 124,

128, 130, 137, 138, 140, 144, 145, 147, 151, 152, 154, 155, 161, 163

Type three secretion system see Type III secretion systemType VI secretion 76, 78, 82Typing 201, 206–209, 211–214, 216, 234

UUrease 15, 86, 88, 89, 106

ureD 86, 88, 89, 106

VV antigen see pYVVaccine 71, 80, 81, 83, 123–127, 129–147, 150–168, 198

killed whole cell vaccine 145, 146subunit vaccine 73, 80, 81, 123, 124, 126, 131, 132,

135, 138, 139, 142, 143, 145, 147, 158, 161, 162, 164vaccinia virus 158, 159, 162, 164

Valine–pyruvate aminotransferase 96Vector 1, 4, 9, 16–18, 42, 69, 70, 72, 77, 78, 81, 85, 91,

100–105, 107, 109, 112, 140, 142, 143, 148, 156–160, 163, 165, 166, 169, 171–174, 176–186, 188–192, 195–197, 199, 211

Vegetables 203, 208, 211, 217, 219, 220, 230, 232. See also Food

Vesicular stomatitis virus 149, 157, 166VirF see pYVVirulence 1, 4, 5, 6, 11, 12, 15–17, 19, 20, 22, 27, 35–43,

45, 51, 54–57, 59, 62, 64, 70–73, 77, 78, 80, 81, 83, 86, 87, 91, 93, 94, 99, 100–107, 114, 124, 126–128 , 135,


Index | 245

137–142, 144–147, 150–153, 155–157, 160–167, 182–184, 201, 202, 205, 212–214, 216, 219, 230, 233

factors 3, 4, 5, 9, 11, 12, 15, 17, 19, 20, 27, 35, 38, 40, 41, 44, 51, 62, 69, 70, 84, 88, 91, 100, 112, 124, 126, 127, 138, 144, 147, 150, 152, 154, 165, 167, 202

VNTR 207, 208. See also Typing and MLVAVSV see Vesicular stomatitis virus

WWater 1, 43, 178, 201, 203, 205, 208, 210–213, 215, 217,

219, 220, 222, 223, 226, 227, 230–236Wild animals 211, 223, 231. See also Animals

XXenopsylla cheopis see Flea

YYadA see pYVYbt see YersiniabactinYersinia murine toxin see pFraYersiniabactin see High-pathogenicity island and Iron

yfeABCD-yfeE locus 22, 24. See also IronYmoA 9, 17, 37, 38, 40Ymt see Yersinia murine toxinYop

effector proteins 4, 37YopB 36, 72, 76, 128, 140, 147YopBDE translocon 152YopD 36, 69, 72, 76, 80, 81, 128, 147YopH 36, 44, 46, 50, 55, 65, 125, 128, 137, 147, 148,

152, 163YopK 36, 147, 148, 154, 164YopP/J 46, 59, 61, 64–66, 147, 148, 152, 212

YPM 10, 14, 202Ysc see pYVyst see Enterotoxin

ZZoonosis 143, 158, 169, 181, 197Zoonotic 43, 182, 201, 208, 212, 213, 217, 233, 234Zwf 6, 8, 14, 93, 94


Colour plate | A1

Figure 3.1 Y. pestis–host interaction revealed by the transcriptional responses after exposure to Y. pestis. The dynamics of bacterial load (red line) and PMNs numbers in lung tissue (blue line) are shown at different time points post infection. The clustered gene expression data of Y. pestis and of lung tissue of infected mice

are shown in the solid line frame and the dotted line frame, respectively. Red represents the up-regulation

and green represents the down-regulation of specific genes. This figure is drawn according to the results of Liu et al. (2009).


Colour plateA2 |

Figure 4.1 Serial cryosections of mouse spleen collected three days after intraperitoneal infection with

Y. enterocolitica O:8 (from C57BL/6 mouse carrying the CX3CR1-EGFP reporter gene expressed by a

subpopulation of DCs and macrophages). Five abscess-like lesions/Y. enterocolitica microcolonies are

shown. Left: Y. enterocolitica patches: pink; neutrophils (Ly6G+): red; CX3CR1-positive cells: green. Right: Y. enterocolitica patches: pink; B lymphocytes (white pulp): red; CX3CR1-positive cells: green (Lenk, 2011).


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