Functional Genetic Diversity among Complex Clinical Isolates: Delineation of Conserved Core and Lineage-Specific Transcriptomes during Intracellular Survival

1. HershbergR

LipatovM

SmallPM

ShefferH

NiemannS

2008 High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6 e311

2. WirthT

HildebrandF

Allix-BeguecC

WolbelingF

KubicaT

2008 Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog 4 e1000160

3. SousaAO

SalemJI

LeeFK

VerçosaMC

CruaudP

1997 An epidemic of tuberculosis with a high rate of tuberculin anergy among a population previously unexposed to tuberculosis, the Yanomami Indians of the Brazilian Amazon. Proceedings of the National Academy of Sciences of the United States of America 94 13227 13232

4. AchtmanM

2008 Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62 53 70

5. AllandD

WhittamTS

MurrayMB

CaveMD

HazbonMH

2003 Modeling bacterial evolution with comparative-genome-based marker systems: application to Mycobacterium tuberculosis evolution and pathogenesis. J Bacteriol 185 3392 3399

6. FirmaniMA

RileyLW

2002 Mycobacterium tuberculosis CDC1551 is resistant to reactive nitrogen and oxygen intermediates in vitro. Infect Immun 70 3965 3968

7. O'BrienL

CarmichaelJ

LowrieDB

AndrewPW

1994 Strains of Mycobacterium tuberculosis differ in susceptibility to reactive nitrogen intermediates in vitro. Infect Immun 62 5187 5190

8. RhoadesER

OrmeIM

1997 Susceptibility of a panel of virulent strains of Mycobacterium tuberculosis to reactive nitrogen intermediates. Infect Immun 65 1189 1195

9. BarczakAK

DomenechP

BoshoffHI

ReedMB

MancaC

2005 In vivo phenotypic dominance in mouse mixed infections with Mycobacterium tuberculosis clinical isolates. J Infect Dis 192 600 606

10. ManabeYC

DannenbergAMJr

TyagiSK

HatemCL

YoderM

2003 Different strains of Mycobacterium tuberculosis cause various spectrums of disease in the rabbit model of tuberculosis. Infect Immun 71 6004 6011

11. Marquina-CastilloB

Garcia-GarciaL

Ponce-de-LeonA

Jimenez-CoronaME

Bobadilla-Del ValleM

2008 Virulence, immunopathology and transmissibility of selected strains of Mycobacterium tuberculosis in a murine model. Immunology

12. PalanisamyGS

DuteauN

EisenachKD

CaveDM

TheusSA

2009 Clinical strains of Mycobacterium tuberculosis display a wide range of virulence in guinea pigs. Tuberculosis (Edinb)

13. TsenovaL

EllisonE

HarbacheuskiR

MoreiraAL

KurepinaN

2005 Virulence of selected Mycobacterium tuberculosis clinical isolates in the rabbit model of meningitis is dependent on phenolic glycolipid produced by the bacilli. J Infect Dis 192 98 106

14. van der SpuyGD

KremerK

NdabambiSL

BeyersN

DunbarR

2009 Changing Mycobacterium tuberculosis population highlights clade-specific pathogenic characteristics. Tuberculosis (Edinb) 89 120 125

15. MalikAN

Godfrey-FaussettP

2005 Effects of genetic variability of Mycobacterium tuberculosis strains on the presentation of disease. Lancet Infect Dis 5 174 183

16. NicolMP

WilkinsonRJ

2008 The clinical consequences of strain diversity in Mycobacterium tuberculosis. Trans R Soc Trop Med Hyg 102 955 965

17. ReedMB

DomenechP

MancaC

SuH

BarczakAK

2004 A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431 84 87

18. SinsimerD

HuetG

MancaC

TsenovaL

KooMS

2008 The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 76 3027 3036

19. KeatingLA

WheelerPR

MansoorH

InwaldJK

DaleJ

2005 The pyruvate requirement of some members of the Mycobacterium tuberculosis complex is due to an inactive pyruvate kinase: implications for in vivo growth. Mol Microbiol 56 163 174

20. ReedMB

GagneuxS

DeriemerK

SmallPM

BarryCE3rd

2007 The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J Bacteriol 189 2583 2589

21. GaoQ

KripkeKE

SaldanhaAJ

YanW

HolmesS

2005 Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 151 5 14

22. RohdeKH

AbramovitchRB

RussellDG

2007 Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2 352 364

23. SchnappingerD

EhrtS

VoskuilMI

LiuY

ManganJA

2003 Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages: Insights into the Phagosomal Environment. J Exp Med 198 693 704

24. ChangJC

MinerMD

PandeyAK

GillWP

HarikNS

2009 igr Genes and Mycobacterium tuberculosis cholesterol metabolism. J Bacteriol 191 5232 5239

25. MusserJM

KapurV

WilliamsDL

KreiswirthBN

van SoolingenD

1996 Characterization of the catalase-peroxidase gene (katG) and inhA locus in isoniazid-resistant and -susceptible strains of Mycobacterium tuberculosis by automated DNA sequencing: restricted array of mutations associated with drug resistance. J Infect Dis 173 196 202

26. TheusS

EisenachK

FomukongN

SilverRF

CaveMD

2007 Beijing family Mycobacterium tuberculosis strains differ in their intracellular growth in THP-1 macrophages. Int J Tuberc Lung Dis 11 1087 1093

27. LiQ

WhalenCC

AlbertJM

LarkinR

ZukowskiL

2002 Differences in rate and variability of intracellular growth of a panel of Mycobacterium tuberculosis clinical isolates within a human monocyte model. Infect Immun 70 6489 6493

28. ZhangM

GongJ

YangZ

SamtenB

CaveMD

1999 Enhanced capacity of a widespread strain of Mycobacterium tuberculosis to grow in human macrophages. J Infect Dis 179 1213 1217

29. MohnWW

van der GeizeR

StewartGR

OkamotoS

LiuJ

2008 The actinobacterial mce4 locus encodes a steroid transporter. J Biol Chem 283 35368 35374

30. PandeyAK

SassettiCM

2008 Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci U S A 105 4376 4380

31. SchaibleUE

Sturgill-KoszyckiS

SchlesingerPH

RussellDG

1998 Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J Immunol 160 1290 1296

32. Sturgill-KoszyckiS

SchaibleUE

RussellDG

1996 Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. Embo J 15 6960 6968

33. BhattK

GurchaSS

BhattA

BesraGS

JacobsWRJr

2007 Two polyketide-synthase-associated acyltransferases are required for sulfolipid biosynthesis in Mycobacterium tuberculosis. Microbiology 153 513 520

34. HatziosSK

SchelleMW

HolsclawCM

BehrensCR

BotyanszkiZ

2009 PapA3 is an acyltransferase required for polyacyltrehalose biosynthesis in Mycobacterium tuberculosis. J Biol Chem 284 12745 12751

35. SirakovaTD

ThirumalaAK

DubeyVS

SprecherH

KolattukudyPE

2001 The Mycobacterium tuberculosis pks2 gene encodes the synthase for the hepta- and octamethyl-branched fatty acids required for sulfolipid synthesis. J Biol Chem 276 16833 16839

36. ConversePJ

KarakousisPC

KlinkenbergLG

KesavanAK

LyLH

2009 Role of the dosR-dosS two-component regulatory system in Mycobacterium tuberculosis virulence in three animal models. Infect Immun 77 1230 1237

37. NiemannS

KoserCU

GagneuxS

PlinkeC

HomolkaS

2009 Genomic diversity among drug sensitive and multidrug resistant isolates of Mycobacterium tuberculosis with identical DNA fingerprints. PLoS One 4 e7407

38. FirmaniMA

RileyLW

2002 Reactive nitrogen intermediates have a bacteriostatic effect on Mycobacterium tuberculosis in vitro. J Clin Microbiol 40 3162 3166

39. Chacon-SalinasR

Serafin-LopezJ

Ramos-PayanR

Mendez-AragonP

Hernandez-PandoR

2005 Differential pattern of cytokine expression by macrophages infected in vitro with different Mycobacterium tuberculosis genotypes. Clin Exp Immunol 140 443 449

40. ParkJS

TamayoMH

Gonzalez-JuarreroM

OrmeIM

OrdwayDJ

2006 Virulent clinical isolates of Mycobacterium tuberculosis grow rapidly and induce cellular necrosis but minimal apoptosis in murine macrophages. J Leukoc Biol 79 80 86

41. TorrellesJB

KnaupR

KolarethA

SlepushkinaT

KaufmanTM

2008 Identification of Mycobacterium tuberculosis clinical isolates with altered phagocytosis by human macrophages due to a truncated lipoarabinomannan. J Biol Chem 283 31417 31428

42. Boschi-MullerS

AzzaS

BranlantG

2001 E. coli methionine sulfoxide reductase with a truncated N terminus or C terminus, or both, retains the ability to reduce methionine sulfoxide. Protein Sci 10 2272 2279

43. LopezB

AguilarD

OrozcoH

BurgerM

EspitiaC

2003 A marked difference in pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes. Clin Exp Immunol 133 30 37

44. MancaC

TsenovaL

BergtoldA

FreemanS

ToveyM

2001 Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha/beta. Proc Natl Acad Sci U S A 98 5752 5757

45. GagneuxS

SmallPM

2007 Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 7 328 337

46. GutierrezMC

BrisseS

BroschR

FabreM

OmaisB

2005 Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog 1 e5

47. JoshiSM

PandeyAK

CapiteN

FortuneSM

RubinEJ

2006 Characterization of mycobacterial virulence genes through genetic interaction mapping. Proc Natl Acad Sci U S A 103 11760 11765

48. KendallSL

WithersM

SoffairCN

MorelandNJ

GurchaS

2007 A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis. Mol Microbiol 65 684 699

49. SenaratneRH

SiddersB

SequeiraP

SaundersG

DunphyK

2008 Mycobacterium tuberculosis strains disrupted in mce3 and mce4 operons are attenuated in mice. J Med Microbiol 57 164 170

50. Van der GeizeR

YamK

HeuserT

WilbrinkMH

HaraH

2007 A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc Natl Acad Sci U S A 104 1947 1952

51. GuptaS

JainS

TyagiAK

1999 Analysis, expression and prevalence of the Mycobacterium tuberculosis homolog of bacterial virulence regulating proteins. FEMS Microbiol Lett 172 137 143

52. SinghA

GuptaR

VishwakarmaRA

NarayananPR

ParamasivanCN

2005 Requirement of the mymA operon for appropriate cell wall ultrastructure and persistence of Mycobacterium tuberculosis in the spleens of guinea pigs. J Bacteriol 187 4173 4186

53. SinghA

JainS

GuptaS

DasT

TyagiAK

2003 mymA operon of Mycobacterium tuberculosis: its regulation and importance in the cell envelope. FEMS Microbiol Lett 227 53 63

54. CoxJS

ChenB

McNeilM

JacobsWRJr

1999 Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402 79 83

55. DomenechP

ReedMB

DowdCS

MancaC

KaplanG

2004 The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis. J Biol Chem 279 21257 21265

56. MurryJP

PandeyAK

SassettiCM

RubinEJ

2009 Phthiocerol dimycocerosate transport is required for resisting interferon-gamma-independent immunity. J Infect Dis 200 774 782

57. CamachoLR

ConstantP

RaynaudC

LaneelleMA

TriccasJA

2001 Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J Biol Chem 276 19845 19854

58. JainM

PetzoldCJ

SchelleMW

LeavellMD

MougousJD

2007 Lipidomics reveals control of Mycobacterium tuberculosis virulence lipids via metabolic coupling. Proc Natl Acad Sci U S A 104 5133 5138

59. SinghA

CrossmanDK

MaiD

GuidryL

VoskuilMI

2009 Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog 5 e1000545

60. GohKS

RastogiN

BerchelM

HuardRC

SolaC

2005 Molecular evolutionary history of tubercle bacilli assessed by study of the polymorphic nucleotide within the nitrate reductase (narGHJI) operon promoter. J Clin Microbiol 43 4010 4014

61. StermannM

SedlacekL

MaassS

BangeFC

2004 A promoter mutation causes differential nitrate reductase activity of Mycobacterium tuberculosis and Mycobacterium bovis. J Bacteriol 186 2856 2861

62. WayneLG

HayesLG

1998 Nitrate reduction as a marker for hypoxic shiftdown of Mycobacterium tuberculosis. Tuber Lung Dis 79 127 132

63. ChauhanS

SinghA

TyagiJS

2010 A single-nucleotide mutation in the -10 promoter region inactivates the narK2X promoter in Mycobacterium bovis and Mycobacterium bovis BCG and has an application in diagnosis. FEMS Microbiol Lett 303 190 196

64. StermannM

BohrssenA

DiephausC

MaassS

BangeFC

2003 Polymorphic nucleotide within the promoter of nitrate reductase (NarGHJI) is specific for Mycobacterium tuberculosis. J Clin Microbiol 41 3252 3259

65. FritzC

MaassS

KreftA

BangeFC

2002 Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue specific. Infect Immun 70 286 291

66. SohaskeyCD

WayneLG

2003 Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 185 7247 7256

67. ParwatiI

van CrevelR

van SoolingenD

2010 Possible underlying mechanisms for successful emergence of the Mycobacterium tuberculosis Beijing genotype strains. Lancet Infect Dis 10 103 111

68. FallowA

DomenechP

ReedMB

2010 Strains of the East Asian (W/Beijing) lineage of Mycobacterium tuberculosis are DosS/DosT-DosR two-component regulatory system natural mutants. J Bacteriol 192 2228 2238

69. HonakerRW

LeistikowRL

BartekIL

VoskuilMI

2009 Unique roles of DosT and DosS in DosR regulon induction and Mycobacterium tuberculosis dormancy. Infect Immun 77 3258 3263

70. KumarA

ToledoJC

PatelRP

LancasterJRJr

SteynAJ

2007 Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc Natl Acad Sci U S A 104 11568 11573

71. CheepsattayakornA

CheepsattayakornR

2009 Human genetic influence on susceptibility of tuberculosis: from infection to disease. J Med Assoc Thai 92 136 141

72. HirshAE

TsolakiAG

DeRiemerK

FeldmanMW

SmallPM

2004 Stable association between strains of Mycobacterium tuberculosis and their human host populations. Proc Natl Acad Sci U S A 101 4871 4876

73. ReedMB

PichlerVK

McIntoshF

MattiaA

FallowA

2009 Major Mycobacterium tuberculosis lineages associate with patient country of origin. J Clin Microbiol 47 1119 1128

74. CohenT

ColijnC

MurrayM

2008 Modeling the effects of strain diversity and mechanisms of strain competition on the potential performance of new tuberculosis vaccines. Proc Natl Acad Sci U S A 105 16302 16307

75. ButcherPD

ManganJA

MonahanIM

1998 Intracellular gene expression. Analysis of RNA from mycobacteria in macrophages using RT-PCR. Methods Mol Biol 101 285 306

76. ManganJA

MonahanIM

ButcherPD

2002 Gene Expression during host-pathogen interactions: approaches to bacterial mRNA extraction and labeling for microarray analysis.

WrenBW

DorrellN

Methods in Microbiology London Academic Press 137 151

77. EdgarR

DomrachevM

LashAE

2002 Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30 207 210

78. ReddyTB

RileyR

WymoreF

MontgomeryP

DeCaprioD

2009 TB database: an integrated platform for tuberculosis research. Nucleic Acids Res 37 D499 508

79. LivakKJ

SchmittgenTD

2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 402 408

80. KendallSL

MovahedzadehF

RisonSC

WernischL

ParishT

2004 The Mycobacterium tuberculosis dosRS two-component system is induced by multiple stresses. Tuberculosis (Edinb) 84 247 255

81. KumarA

DeshaneJS

CrossmanDK

BolisettyS

YanBS

2008 Heme oxygenase-1-derived carbon monoxide induces the Mycobacterium tuberculosis dormancy regulon. J Biol Chem 283 18032 18039

82. ParkHD

GuinnKM

HarrellMI

LiaoR

VoskuilMI

2003 Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 48 833 843

83. VoskuilMI

SchnappingerD

ViscontiKC

HarrellMI

DolganovGM

2003 Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198 705 713

84. KhanA

SarkarD

2006 Identification of a respiratory-type nitrate reductase and its role for survival of Mycobacterium smegmatis in Wayne model. Microb Pathog 41 90 95

85. WeberI

FritzC

RuttkowskiS

KreftA

BangeFC

2000 Anaerobic nitrate reductase (narGHJI) activity of Mycobacterium bovis BCG in vitro and its contribution to virulence in immunodeficient mice. Mol Microbiol 35 1017 1025

86. GagneuxS

DeRiemerK

VanT

Kato-MaedaM

de JongBC

2006 Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 103 2869 2873

87. BroschR

GordonSV

MarmiesseM

BrodinP

BuchrieserC

2002 A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A 99 3684 3689

88. MarmiesseM

BrodinP

BuchrieserC

GutierrezC

SimoesN

2004 Macro-array and bioinformatic analyses reveal mycobacterial ‘core’ genes, variation in the ESAT-6 gene family and new phylogenetic markers for the Mycobacterium tuberculosis complex. Microbiology 150 483 496