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Biological and Epidemiological Consequences of MTBC Diversity

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1019))

Abstract

Tuberculosis is caused by different groups of bacteria belonging to the Mycobacterium tuberculosis complex (MTBC). The combined action of human factors, environmental conditions and bacterial virulence determine the extent and form of human disease. MTBC virulence is a composite of different clinical phenotypes such as transmission rate and disease severity among others. Clinical phenotypes are also influenced by cellular and immunological phenotypes. MTBC phenotypes are determined by the genotype, therefore finding genotypes responsible for clinical phenotypes would allow discovering MTBC virulence factors. Different MTBC strains display different cellular and clinical phenotypes. Strains from Lineage 5 and Lineage 6 are metabolically different, grow slower, and are less virulent. Also, at least certain groups of Lineage 2 and Lineage 4 strains are more virulent in terms of disease severity and human-to-human transmission. Because phenotypic differences are ultimately caused by genotypic differences, different genomic loci have been related to various cellular and clinical phenotypes. However, defining the impact of specific bacterial genomic loci on virulence when other bacterial determinants, human and environmental factors are also impacting the phenotype would contribute to a better knowledge of tuberculosis virulence and ultimately benefit tuberculosis control.

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References

  • Agarwal N, Lamichhane G, Gupta R, Nolan S, Bishai WR (2009) Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase. Nature 460:98–102

    Article  CAS  PubMed  Google Scholar 

  • Aguilar D, Hanekom M, Mata D, Van Pittius NCG, Van Helden PD, Warren RM, Hernandez-Pando R (2010) Mycobacterium tuberculosis strains with the Beijing genotype demonstrate variability in virulence associated with transmission. Tuberculosis 90:319–325

    Article  CAS  PubMed  Google Scholar 

  • Albanna AS, Reed MB, Kotar KV, Fallow A, Mcintosh FA, Behr MA, Menzies D (2006) Reduced transmissibility of East African Indian strains of Mycobacterium tuberculosis. PLoS One 2011:e25075

    Google Scholar 

  • Alexander KA, Laver PN, Michel AL, Williams M, Van Helden PD, Warren RM, Gey Van Pittius NC (2010) Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerg Infect Dis 16:1296–1299

    Article  PubMed  PubMed Central  Google Scholar 

  • Alonso H, Aguilo JI, Samper SA, Caminero JA, Campos-Herrero MAI, Gicquel B, Brosch R, Martín C, Otal I (2011) Deciphering the role of IS6110 in a highly transmissible Mycobacterium tuberculosis Beijing strain, GC1237. Tuberculosis 91:117–126

    Article  CAS  PubMed  Google Scholar 

  • Anh DD, Borgdorff MW, Van LN, Lan NT, Van Gorkom T, Kremer K, Van Soolingen D (2000) Mycobacterium tuberculosis Beijing genotype emerging in Vietnam. Emerg Infect Dis 6:302–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astarie-Dequeker C, Nigou J, Passemar C, Guilhot C (2010) The role of mycobacterial lipids in host pathogenesis. Drug Discov Today Dis Mech 7:e33–e41

    Article  CAS  Google Scholar 

  • Baker L, Brown T, Maiden MC, Drobniewski F (2004) Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis. Emerg Infect Dis 10:1568–1577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barczak A, Domenech P, Boshoff H, Reed MB, Manca C, Kaplan G, Barry CE III (2005) In vivo phenotypic dominance in mouse mixed infections with Mycobacterium tuberculosis clinical isolates. J Infect Dis 192:600–606

    Article  PubMed  Google Scholar 

  • Basu S, Pathak SK, Banerjee A, Pathak S, Bhattacharyya A, Yang Z, Talarico S, Kundu M, Basu J (2007) Execution of macrophage apoptosis by PE_PGRS33 of Mycobacterium tuberculosis is mediated by toll-like receptor 2-dependent release of tumor necrosis factor-α. J Biol Chem 282:1039–1050

    Article  CAS  PubMed  Google Scholar 

  • Beatty WL, Rhoades ER, Ullrich HJ, Chatterjee D, Heuser JE, Russell DG (2000) Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1:235–247

    Article  CAS  PubMed  Google Scholar 

  • Behar SM, Divangahi M, Remold HG (2010) Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol 8:668–674

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bentley SD, Comas I, Bryant JM, Walker D, Smith NH, Harris SR, Thurston S, Gagneux S, Wood J, Antonio M, Quail MA, Gehre F, Adegbola RA, Parkhill J, De Jong BC (2012) The genome of Mycobacterium africanum West African 2 reveals a lineage-specific locus and genome erosion common to the M. tuberculosis complex. PLoS Negl Trop Dis 6:e1552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Betts JC, Dodson P, Quan S, Lewis AP, Thomas PJ, Duncan K, Mcadam RA (2000) Comparison of the proteome of Mycobacterium tuberculosis strain H37Rv with clinical isolate CDC 1551. Microbiology 146:3205–3216

    Article  CAS  PubMed  Google Scholar 

  • Bishai WR, Dannenberg AM Jr, Parrish N, Ruiz R, Chen P, Zook BC, Johnson W, Boles JW, Pitt ML (1999) Virulence of Mycobacterium tuberculosis CDC1551 and H37Rv in rabbits evaluated by Lurie’s pulmonary tubercle count method. Infect Immun 67:4931–4934

    CAS  PubMed  PubMed Central  Google Scholar 

  • Borgdorff MW, Van Soolingen D (2013) The re-emergence of tuberculosis: what have we learnt from molecular epidemiology? Clin Microbiol Infect 19:889–901

    Article  CAS  PubMed  Google Scholar 

  • Borgdorff MW, Van Deutekom H, De Haas PEWP, Kremer K, Van Soolingen D (2004) Mycobacterium tuberculosis, Beijing genotype strains not associated with radiological presentation of pulmonary tuberculosis. Tuberculosis 84:337–340

    Article  PubMed  Google Scholar 

  • Bos KI, Harkins KM, Herbig A, Coscolla M, Weber N, Comas I, Forrest SA, Bryant JM, Harris SR, Schuenemann VJ, Campbell TJ, Majander K, Wilbur AK, Guichon RA, Wolfe Steadman DL, Cook DC, Niemann S, Behr MA, Zumarraga M, Bastida R, Huson D, Nieselt K, Young D, Parkhill J, Buikstra JE, Gagneux S, Stone AC, Krause J (2014) Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514:494–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan PJ (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83:91–97

    Article  CAS  PubMed  Google Scholar 

  • Brookes RH, Pathan AA, Mcshane H, Hensmann M, Price DA, Hill AV (2003) CD8+ T cell-mediated suppression of intracellular Mycobacterium tuberculosis growth in activated human macrophages. Eur J Immunol 33:3293–3302

    Article  CAS  PubMed  Google Scholar 

  • Brosch R, Gordon SV, Buchrieser C, Pym AS, Garnier T, Cole ST (2000) Comparative genomics uncovers large tandem chromosomal duplications in Mycobacterium bovis BCG Pasteur. Yeast 17:111–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, Eiglmeier K, Garnier T, Gutierrez C, Hewinson G, Kremer K, Parsons LM, Pym AS, Samper S, Van Soolingen D, Cole ST (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A 99:3684–3689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brosch R, Gordon SV, Garnier T, Eiglmeier K, Frigui W, Valenti P, Dos Santos S, Duthoy SP, Lacroix C, Garcia-Pelayo C, Inwald JK, Golby P, Garcia JNÝ, Hewinson RG, Behr MA, Quail MA, Churcher C, Barrell BG, Parkhill J, Cole ST (2007) Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci 104:5596–5601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buu TN, Van Soolingen D, Huyen MNT, Lan NTN, Quy HT, Tiemersma EW, Kremer K, Borgdorff MW, Cobelens FGJ (2012) Increased transmission of Mycobacterium tuberculosis Beijing genotype strains associated with resistance to streptomycin: a population-based study. PLoS One 7:e42323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C (1999) Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34:257–267

    Article  CAS  PubMed  Google Scholar 

  • Cambier CJ, Takaki KK, Larson RP, Hernandez RE, Tobin DM, Urdahl KB, Cosma CL, Ramakrishnan L (2014) Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 505:218–222

    Article  CAS  PubMed  Google Scholar 

  • Canetti G (1970) Infection caused by atypical mycobacteria and antituberculous immunity. Lille Med 15:280–282

    CAS  PubMed  Google Scholar 

  • Carmona J, Cruz A, Moreira-Teixeira L, Sousa C, Sousa J, Osorio NS, Saraiva AL, Svenson S, Kallenius G, Pedrosa J, Rodrigues F, Castro AG, Saraiva M (2013) Mycobacterium tuberculosis strains are differentially recognized by TLRs with an impact on the immune response. PLoS ONE 8:e67277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casanova JL, Abel L (2002) Genetic dissection of immunity to mycobacteria: the human model. Annu Rev Immunol 20:581–620

    Article  CAS  PubMed  Google Scholar 

  • Caws M, Thwaites G, Dunstan S, Hawn TR, Thi Ngoc Lan N, Thuong NTT, Stepniewska K, Huyen MNT, Bang ND, Huu Loc T, Gagneux S, Van Soolingen D, Kremer K, Van Der Sande M, Small P, Thi Hoang Anh P, Chinh NT, Thi Quy H, Thi Hong Duyen N, Quang Tho D, Hieu NT, Torok E, Hien TT, Dung NH, Thi Quynh Nhu N, Duy PM, Vinh Chau N, Farrar J (2008) The influence of host and bacterial genotype on the development of disseminated disease with Mycobacterium tuberculosis. PLoS Pathog 4:e1000034

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chacon-Salinas R, Serafin-Lopez J, Ramos-Payan R, Mendez-AragoN P, Hernndez-Pando R, Van Soolingen D, Flores-Romo L, Estrada-Parra S, Estrada-Garcia I (2005) Differential pattern of cytokine expression by macrophages infected in vitro with different Mycobacterium tuberculosis genotypes. Clin Exp Immunol 140:443–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chavadi S, Wooff E, Coldham NG, Sritharan M, Hewinson RG, Gordon SV, Wheeler PR (2009) Global effects of inactivation of the pyruvate kinase gene in the Mycobacterium tuberculosis complex. J Bacteriol 191:7545–7553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Gan H, Remold HG (2006) A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J Immunol 176:3707–3716

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Divangahi M, Gan H, Shin DS, Hong S, Lee DM, Serhan CN, Behar SM, Remold HG (2008) Lipid mediators in innate immunity against tuberculosis: opposing roles of PGE2 and LXA4 in the induction of macrophage death. J Exp Med 205:2791–2801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YY, Chang JR, Huang WF, Hsu SC, Kuo SC, Sun JR, Dou HY (2014) The pattern of cytokine production in vitro induced by ancient and modern Beijing Mycobacterium tuberculosis strains. PLoS One 9:e94296

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chesne-Seck ML, Barilone N, Boudou F, Asensio JG, Kolattukudy PE, Martin C, Cole ST, Gicquel B, Gopaul DN, Jackson M (2008) A point mutation in the two-component regulator PhoP-PhoR accounts for the absence of polyketide-derived acyltrehaloses but not that of phthiocerol dimycocerosates in Mycobacterium tuberculosis H37Ra. J Bacteriol 190:1329–1334

    Article  CAS  PubMed  Google Scholar 

  • Clark M, Riben P, Nowgesic E (2002) The association of housing density, isolation and tuberculosis in Canadian First Nations communities. Int J Epidemiol 31:940–945

    Article  PubMed  Google Scholar 

  • Click ES, Moonan PK, Winston CA, Cowan LS, Oeltmann JE (2012) Relationship between Mycobacterium tuberculosis phylogenetic lineage and clinical site of tuberculosis. Clin Infect Dis 54:211–219

    Article  PubMed  Google Scholar 

  • Colijn C, Brandes A, Zucker J, Lun DS, Weiner B, Farhat MR, Cheng TY, Moody DB, Murray M, Galagan JE (2009) Interpreting expression data with metabolic flux models: predicting Mycobacterium tuberculosis mycolic acid production. PLoS Comput Biol 5:e1000489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Collins FM, Smith MM (1969) Comparative study of virulence of Mycobacterium tuberculosis measured in mice and guinea pigs. Am Rev Respir Dis 100:631

    CAS  PubMed  Google Scholar 

  • Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, Parkhill J, Malla B, Berg S, Thwaites G, Yeboah-Manu D, Bothamley G, Mei J, Wei LH, Bentley S, Harris SR, Niemann S, Diel R, Aseffa A, Gao Q, Young D, Gagneux S (2013) Out-of-Africa migration and neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45:1176–U311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Constant P, Perez E, Malaga W, Laneelle MA, Saurel O, Daffe M, Guilhot C (2002) Role of the pks15/1 gene in the biosynthesis of phenolglycolipids in the Mycobacterium tuberculosis complex. J Biol Chem 277:38148–38158

    Article  CAS  PubMed  Google Scholar 

  • Converse SE, Mougous JD, Leavell MD, Leary JA, Bertozzi CR, Cox JS (2003) MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence. Proc Natl Acad Sci U S A 100:6121–6126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Copin R, Coscolla M, Seiffert SN, Bothamley G, Sutherland J, Mbayo G, Gagneux S, Ernst JD (2014) Sequence diversity in the pe_pgrs genes of Mycobacterium tuberculosis is independent of human T cell recognition. mBio 5:e00960

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coscolla M, Gagneux S (2014) Consequences of genomic diversity in Mycobacterium tuberculosis. Semin Immunol 26:431–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coscolla M, Lewin A, Metzger S, Maetz-Rennsing K, Calvignac-Spencer S, Nitsche A, Dabrowski PW, Radonic A, Niemann S, Parkhill J, Couacy-Hymann E, Feldman J, Comas I, Boesch C, Gagneux S, Leendertz FH (2013) Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee. Emerg Infect Dis 19:969–976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cousins DV, Peet RL, Gaynor WT, Williams SN, Gow BL (1994) Tuberculosis in imported hyrax (Procavia capensis) caused by an ususual variant belonging to the Mycobacterium tuberculosis complex. Vet Microbiol 42:135–145

    Article  CAS  PubMed  Google Scholar 

  • Cowley D, Govender D, February B, Wolfe M, Steyn L, Evans J, Wilkinson R-J, Nicol M-P (2008) Recent and rapid emergence of W-Beijing strains of Mycobacterium tuberculosis in Cape Town, South Africa. Clin Infect Dis 47:1252–1259

    Article  PubMed  Google Scholar 

  • Cox JS, Chen B, Mcneil M, Jacobs WR Jr (1999) Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402:79–83

    Article  CAS  PubMed  Google Scholar 

  • De Jong BC, Hill PC, Brookes RH, Gagneux S, Jeffries DJ, Otu JK, Donkor SA, Fox A, Mcadam KP, Small PM, Adegbola RA (2006) Mycobacterium africanum elicits an attenuated T cell response to early secreted antigenic target, 6 kDa, in patients with tuberculosis and their household contacts. J Infect Dis 193:1279–1286

    Article  PubMed  Google Scholar 

  • De Jong B-C, Hill P-C, Aiken A, Awine T, Antonio M, Adetifa I-M, Jacksonâ-Sillah D-J, Fox A, Deriemer K, Gagneux S, Borgdorff M-W, Mcadam K-P, Corrah T, Small P-M, Adegbola R-A (2008) Progression to active tuberculosis, but not transmission, varies by Mycobacterium tuberculosis lineage in the Gambia. J Infect Dis 198:1037–1043

    Article  PubMed  PubMed Central  Google Scholar 

  • Dheenadhayalan V, Delogu G, Brennan MJ (2004) Expression of the PE_PGRS 33 protein in Mycobacterium smegmatis triggers necrosis in macrophages and enhanced mycobacterial survival. Microbes Infect

    Google Scholar 

  • Dheenadhayalan V, Delogu G, Brennan MJ. Expression of the PE_PGRS 33 protein in Mycobacterium smegmatis triggers necrosis in macrophages and enhanced mycobacterial survival. Microbes and Infection. 2006;8(1):262–72.

    Google Scholar 

  • Divangahi M, Chen M, Gan H, Desjardins D, Hickman TT, Lee DM, Fortune S, Behar SM, Remold HG (2009) Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol 10:899–906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domenech P, Reed MB (2009) Rapid and spontaneous loss of phthiocerol dimycocerosate (PDIM) from Mycobacterium tuberculosis grown in vitro: implications for virulence studies. Microbiology 155:3532–3543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domenech P, Reed MB, Dowd CS, Manca C, Kaplan G, Barry CE 3rd (2004) The role of MmpL8 in sulfatide biogenesis and virulence of Mycobacterium tuberculosis. J Biol Chem 279:21257–21265

    Article  CAS  PubMed  Google Scholar 

  • Domenech P, Reed MB, Barry CE 3rd (2005) Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance. Infect Immun 73:3492–3501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Domenech P, Kolly GS, Leon-Solis L, Fallow A, Reed MB (2010) Massive gene duplication event among clinical isolates of the Mycobacterium tuberculosis W/Beijing family. J Bacteriol 192:4562–4570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan L, Gan H, Arm J, Remold HG (2001) Cytosolic phospholipase A2 participates with TNF-alpha in the induction of apoptosis of human macrophages infected with Mycobacterium tuberculosis H37Ra. J Immunol 166:7469–7476

    Article  CAS  PubMed  Google Scholar 

  • Dubnau E, Chan J, Raynaud C, Mohan VP, Laneelle MA, Yu K, Quemard A, Smith I, Daffe M (2000) Oxygenated mycolic acids are necessary for virulence of Mycobacterium tuberculosis in mice. Mol Microbiol 36:630–637

    Article  CAS  PubMed  Google Scholar 

  • Ernst JD (2012) The immunological life cycle of tuberculosis. Nat Rev Immunol 12:581–591

    Article  CAS  PubMed  Google Scholar 

  • European Concerted Action on New Genetic, M, Techniques for The, E, Control Of, T (2006) Beijing/W genotype Mycobacterium tuberculosis and drug resistance. Emerg Infect Dis 12:736–743

    Article  Google Scholar 

  • Fenner L, Egger M, Bodmer T, Furrer H, Ballif M, Battegay M, Helbling P, Fehr J, Gsponer T, Rieder HL, Zwahlen M, Hoffmann M, Bernasconi E, Cavassini M, Calmy A, Dolina M, Frei R, Janssens JP, Borrell S, Stucki D, Schrenzel J, Bçôttger EC, Gagneux S, For the Swiss, H. I. V. C. & Molecular Epidemiology of Tuberculosis Study, G (2013) HIV infection disrupts the sympatric host-pathogen relationship in human tuberculosis. PLoS Genet 9:e1003318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filliol I, Motiwala AS, Cavatore M, Qi W, Hernando Hazbon M, Bobadilla Del Valle M, Fyfe J, Garcia-Garcia L, Rastogi N, Sola C, Zozio T, Guerrero MI, Leon CI, Crabtree J, Angiuoli S, Eisenach KD, Durmaz R, Joloba ML, Rendon A, Sifuentes-Osornio J, Ponce De Leon A, Cave MD, Fleischmann R, Whittam TS, Alland D (2006) Global phylogeny of Mycobacterium tuberculosis based on Single Nucleotide Polymorphism (SNP) analysis: insights into tuberculosis evolution, phylogenetic accuracy of other DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol 188:759–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Firdessa R, Berg S, Hailu E, Schelling E, Gumi B, Erenso G, Gadisa E, Kiros T, Habtamu M, Hussein J, Zinsstag J, Robertson BD, Ameni G, Lohan AJ, Loftus B, Comas I, Gagneux S, Tschopp R, Yamuah L, Hewinson G, Gordon SV, Young DB, Aseffa A (2013) Mycobacterial lineages causing pulmonary and extrapulmonary tuberculosis, Ethiopia. Emerg Infect Dis 19:460–463

    Article  PubMed  PubMed Central  Google Scholar 

  • Firmani MA, Riley LW (2002) Mycobacterium tuberculosis CDC1551 is resistant to reactive nitrogen and oxygen intermediates in vitro. Infect Immun 70:3965–3968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forrellad MA, Klepp LI, Gioffré A, Sabio Y, García J, Morbidoni HR, Santangelo MDLP, Cataldi AA, Bigi F (2013) Virulence factors of the Mycobacterium tuberculosis complex. Virulence 4:3–66

    Article  PubMed  PubMed Central  Google Scholar 

  • Fratti RA, Chua J, Vergne I, Deretic V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proceedings of the National Academy of Sciences. 2003;100(9):5437–42.

    Google Scholar 

  • Gagneux S, Deriemer K, Van T, Kato-Maeda M, De Jong BC, Narayanan S, Nicol M, Niemann S, Kremer K, Gutierrez MC, Hilty M, Hopewell PC, Small PM (2006a) Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci 103:2869–2873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gagneux S, Long CD, Small PM, Van T, Schoolnik GK, Bohannan BJM (2006b) The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 312:1944–1946

    Article  CAS  PubMed  Google Scholar 

  • Gan H, Lee J, Ren F, Chen M, Kornfeld H, Remold HG (2008) Mycobacterium tuberculosis blocks crosslinking of annexin-1 and apoptotic envelope formation on infected macrophages to maintain virulence. Nat Immunol 9:1189–1197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gangadharam PR, Cohn ML, Middlebrook G (1963) Infectivity, pathogenicity and sulpholipid fraction of some Indians and British strains of tubercle bacilli. Tubercle 44:452–455

    Article  CAS  PubMed  Google Scholar 

  • Gey Van Pittius N, Sampson S, Lee H, Kim Y, Van Helden P, Warren R (2006) Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol Biol 6:95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Glickman MS, Cox JS, Jacobs WR Jr (2000) A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol Cell 5:717–727

    Article  CAS  PubMed  Google Scholar 

  • Godreuil S, Torrea G, Terru D, Chevenet F, Diagbouga S, Supply P, Van De Perre P, Carriere C, Bañuls AL (2007) First molecular epidemiology study of Mycobacterium tuberculosis in Burkina Faso. J Clin Microbiol 45:921–927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golby P, Hatch KA, Bacon J, Cooney R, Riley P, Allnutt J, Hinds J, Nunez J, Marsh PD, Hewinson RG, Gordon SV (2007) Comparative transcriptomics reveals key gene expression differences between the human and bovine pathogens of the Mycobacterium tuberculosis complex. Microbiology 153:3323–3336

    Article  CAS  PubMed  Google Scholar 

  • Gonzalo-Asensio J, Malaga W, Pawlik A, Astarie-Dequeker C, Passemar C, Moreau F, Laval FO, Daffe M, Martin C, Brosch R, Guilhot C (2014) Evolutionary history of tuberculosis shaped by conserved mutations in the PhoPR virulence regulator. Proc Natl Acad Sci 111:11491–11496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goren MB, Brokl O, Schaefer WB (1974a) Lipids of putative relevance to virulence in Mycobacterium tuberculosis: correlation of virulence with elaboration of sulfatides and strongly acidic lipids. Infect Immun 9:142–149

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goren MB, Brokl O, Schaefer WB (1974b) Lipids of putative relevance to virulence in Mycobacterium tuberculosis: phthiocerol dimycocerosate and the attenuation indicator lipid. Infect Immun 9:150–158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goren MB, Grange JM, Aber VR, Allen BW, Mitchison DA (1982) Role of lipid content and hydrogen peroxide susceptibility in determining the guinea-pig virulence of Mycobacterium tuberculosis. Br J Exp Pathol 63:693–700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grange JM, Aber VR, Allen BW, Mitchison DA, Mikhail JR, Mcswiggan DA, Collins CH (1977) Comparison of strains of Mycobacterium tuberculosis from british, ugandan and asian immigrant patients: a study in bacteriophage typing, susceptibility to hydrogen peroxide and sensitivity to thiophen-2-carbonic acid hydrazide. Tubercle 58:207–215

    Article  CAS  PubMed  Google Scholar 

  • Grange JM, Aber VR, Allen BW, Mitchison DA, Goren MB (1978) The correlation of bacteriophage types of Mycobacterium tuberculosis with guinea-pig virulence and in vitro-indicators of virulence. J Gen Microbiol 108:1–7

    Article  CAS  PubMed  Google Scholar 

  • Groenheit R, Ghebremichael S, Svensson J, Rabna P, Colombatti R, Riccardi F, Couvin D, Hill VÇ, Rastogi N, Koivula T, Kçïllenius G (2011) The guinea-bissau family of Mycobacterium tuberculosis complex revisited. PLoS One 6:e18601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanekom M, Van Der Spuy GD, Streicher E, Ndabambi SL, Mcevoy CRE, Kidd M, Beyers N, Victor TC, Van Helden PD, Warren RM (2007) A recently evolved sublineage of the Mycobacterium tuberculosis Beijing strain family was associated with an increased ability to spread and cause disease. J Clin Microbiol JCM 45:1483–1490

    Article  CAS  Google Scholar 

  • He XY, Zhuang YH, Zhang XG, Li GL (2003) Comparative proteome analysis of culture supernatant proteins of Mycobacterium tuberculosis H37Rv and H37Ra. Microbes Infect 5:851–856

    Article  CAS  PubMed  Google Scholar 

  • Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S, Homolka S, Roach JC, Kremer K, Petrov DA, Feldman MW, Gagneux S (2008) High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6:e311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hett EC, Rubin EJ (2008) Bacterial growth and cell division: a mycobacterial perspective. Microbiol Mol Biol Rev 72:126–156. table of contents

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hinchey J, Lee S, Jeon BY, Basaraba RJ, Venkataswamy MM, Chen B, Chan J, Braunstein M, Orme IM, Derrick SC, Morris SL, Jacobs WR Jr, Porcelli SA (2007) Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J Clin Invest 117:2279–2288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirsh AE, Tsolaki AG, Deriemer K, Feldman MW, Small PM (2004) Stable association between strains of Mycobacterium tuberculosis and their human host populations. Proc Natl Acad Sci U S A 101:4871–4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homolka S, Niemann S, Russell DG, Rohde KH (2010) Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog 6:e1000988

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huet G, Constant P, Malaga W, Laneelle MA, Kremer K, Van Soolingen D, Daffe M, Guilhot C (2009) A lipid profile typifies the Beijing strains of Mycobacterium tuberculosis: identification of a mutation responsible for a modification of the structures of phthiocerol dimycocerosates and phenolic glycolipids. J Biol Chem 284:27101–27113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackett PS, Aber VR, Lowrie DB (1978) Virulence and resistance to superoxide, low pH and hydrogen peroxide among strains of Mycobacterium tuberculosis. J Gen Microbiol 104:37–45

    Article  CAS  PubMed  Google Scholar 

  • Jhingan GD, Kumari S, Jamwal SV, Kalam H, Arora D, Jain N, Krishnakumaar L, Samal A, Rao KVS, Kumar D, Nandicoori VK (2016) Comparative proteomic analyses of avirulent, virulent and clinical strains of Mycobacterium tuberculosis identifies strain-specific patterns. J Biol Chem 291: 14257–14273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jungblut PR, Schaible UE, Mollenkopf HJ, Zimny-Arndt U, Raupach B, Mattow J, Halada P, Lamer S, Hagens K, Kaufmann SH (1999) Comparative proteome analysis of Mycobacterium tuberculosis and Mycobacterium bovis BCG strains: towards functional genomics of microbial pathogens. Mol Microbiol 33:1103–1117

    Article  CAS  PubMed  Google Scholar 

  • Kato-Maeda M, Kim EY, Flores L, Jarlsberg LG, Osmond D, Hopewell PC (2010) Differences among sublineages of the East-Asian lineage of Mycobacterium tuberculosis in genotypic clustering. Int J Tuberc Lung Dis 14:538–544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kato-Maeda M, Shanley CA, Ackart D, Jarlsberg LG, Shang S, Obregon-Henao A, Harton M, Basaraba RJ, Henao-Tamayo M, Barrozo JC, Rose J, Kawamura LM, Coscolla M, Fofanov VY, Koshinsky H, Gagneux S, Hopewell PC, Ordway DJ, Orme IM (2012) Beijing sublineages of Mycobacterium tuberculosis differ in pathogenicity in the guinea pig. Clin Vaccine Immunol 19:1227–1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch A, Mizrahi V, Warner DF (2014) The impact of drug resistance on Mycobacterium tuberculosis physiology: what can we learn from rifampicin? Emerg Microbes Infect 3:e17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong Y, Cave MD, Yang D, Zhang L, Marrs CF, Foxman B, Bates JH, Wilson F, Mukasa LN, Yang ZH (2005) Distribution of insertion- and deletion-associated genetic polymorphisms among four Mycobacterium tuberculosis phospholipase C genes and associations with extrathoracic tuberculosis: a population-based study. J Clin Microbiol 43:6048–6053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong Y, Cave MD, Zhang L, Foxman B, Marrs CF, Bates JH, Yang ZH (2006) Population-based study of deletions in five different genomic regions of Mycobacterium tuberculosis and possible clinical relevance of the deletions. J Clin Microbiol 44:3940–3946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong Y, Cave MD, Zhang L, Foxman B, Marrs CF, Bates JH, Yang ZH (2007) Association between Mycobacterium tuberculosis Beijing/W lineage strain infection and extrathoracic tuberculosis: insights from epidemiologic and clinical characterization of the three principal genetic groups of M. tuberculosis clinical isolates. J Clin Microbiol 45:409–414

    Article  CAS  PubMed  Google Scholar 

  • Krishnan N, Malaga W, Constant P, Caws M, Thi Hoang Chau T, Salmons J, Thi Ngoc Lan N, Bang ND, Daffç M, Young DB, Robertson BD, Guilhot C, Thwaites GE (2011) Mycobacterium tuberculosis lineage influences innate immune response and virulence and is associated with distinct cell envelope lipid profiles. PLoS One 6:e23870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kubica T, Rusch-Gerdes S, Niemann S (2004) The Beijing genotype is emerging among multidrug-resistant Mycobacterium tuberculosis strains from Germany. Int J Tuberc Lung Dis 8:1107–1113

    CAS  PubMed  Google Scholar 

  • Kwan CK, Ernst JD (2011) HIV and tuberculosis: a deadly human syndemic. Clin Microbiol Rev 24:351–376

    Article  PubMed  PubMed Central  Google Scholar 

  • Langlois-Klassen D, Senthilselvan A, Chui L, Kunimoto D, Saunders LD, Menzies D, Long R (2013) Transmission of Mycobacterium tuberculosis Beijing strains, Alberta, Canada, 1991–2007. Emerg Infect Dis 19: 701–711

    Article  PubMed  PubMed Central  Google Scholar 

  • Laochumroonvorapong P, Paul S, Manca C, Freedman VH, Kaplan G (1997) Mycobacterial growth and sensitivity to H2O2 killing in human monocytes in vitro. Infect Immun 65:4850–4857

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Remold HG, Ieong MH, Kornfeld H (2006) Macrophage apoptosis in response to high intracellular burden of Mycobacterium tuberculosis is mediated by a novel caspase-independent pathway. J Immunol 176:4267–4274

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Whalen CC, Albert JM, Larkin R, Zukowski L, Cave MD, Silver RF (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lillebaek T, Andersen AB, Dirksen A, Glynn JR, Kremer K (2003) Mycobacterium tuberculosis Beijing genotype. Emerg Infect Dis 9:1553–1557

    Article  PubMed  PubMed Central  Google Scholar 

  • Lygizos M, Shenoi S, Brooks R, Bhushan A, Brust J, Zelterman D, Deng Y, Northrup V, Moll A, Friedland G (2013) Natural ventilation reduces high TB transmission risk in traditional homes in rural KwaZulu-Natal, South Africa. BMC Infect Dis 13:300

    Article  PubMed  PubMed Central  Google Scholar 

  • Målen H, De Souza GA, Pathak S, Søfteland T, Wiker HG (2011) Comparison of membrane proteins of Mycobacterium tuberculosis H37Rv and H37Ra strains. BMC Microbiol 11:1–10

    Article  CAS  Google Scholar 

  • Manca C, Paul S, Barry CE III, Freedman VH, Kaplan G (1999) Mycobacterium tuberculosis catalase and peroxidase activities and resistance to oxidative killing in human monocytes in vitro. Infect Immun 67:74–79

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manca C, Tsenova L, Bergtold A, Freeman S, Tovey M, Musser JM, Barry CE, Freedman VH, Kaplan G (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 g. Proc Natl Acad Sci U S A 98:5752–5757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manca C, Reed MB, Freeman S, Mathema B, Kreiswirth B, Barry CE III, Kaplan G (2004) Differential monocyte activation underlies strain-specific Mycobacterium tuberculosis pathogenesis. Infect Immun:5511–5514

    Google Scholar 

  • Manca C, Tsenova L, Freeman S, Barczak AK, Tovey M, Murray PJ, Barry C, Kaplan G (2005) Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J Interf Cytokine Res 25:694–701

    Article  CAS  Google Scholar 

  • Marais BJ, Hesseling AC, Schaaf HS, Gie RP, Van Helden PD, Warren RM (2009) Mycobacterium tuberculosis transmission is not related to household genotype in a setting of high endemicity. J Clin Microbiol 47: 1338–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mcdonough KA, Kress Y, Bloom BR (1993) Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 61:2763–2773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Melnyk AH, Wong A, Kassen R (2015) The fitness costs of antibiotic resistance mutations. Evolutionary applications. 8(3):273–283

    Google Scholar 

  • Mihret A, Bekele Y, Loxton AG, Aseffa A, Howe R, Walzl G (2012) Plasma level of IL-4 differs in patients infected with different modern lineages of M. tuberculosis. J Trop Med 2012:518564

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller BH, Shinnick TM (2000) Evaluation of Mycobacterium tuberculosis genes involved in resistance to killing by human macrophages. Infect Immun 68: 387–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mostowy S, Cleto C, Sherman DR, Behr MA (2004) The Mycobacterium tuberculosis complex transcriptome of attenuation. Tuberculosis (Edinb) 84:197–204

    Article  Google Scholar 

  • Nahid P, Bliven EE, Kim EY, Mac Kenzie WR, Stout JE, Diem L, Johnson JL, Gagneux S, Hopewell PC, Kato-Maeda M, The Tuberculosis Trials, C (2010) Influence of M. tuberculosis lineage variability within a clinical trial for pulmonary tuberculosis. PLoS One 5:e10753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Newton SM, Smith RJ, Wilkinson KA, Nicol MP, Garton NJ, Staples KJ, Stewart GR, Wain JR, Martineau AR, Fandrich S, Smallie T, Foxwell B, Al Obaidi A, Shafi J, Rajakumar K, Kampmann B, Andrew PW, Ziegler-Heitbrock L, Barer MR, Wilkinson RJ (2006) A deletion defining a common Asian lineage of Mycobacterium tuberculosis associates with immune subversion. Proc Natl Acad Sci 103:15594–15598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicol MP, Sola C, February B, Rastogi N, Steyn L, Wilkinson RJ (2005) Distribution of strain families of Mycobacterium tuberculosis causing pulmonary and extrapulmonary disease in hospitalized children in Cape Town, South Africa. J Clin Microbiol 43: 5779–5781

    Article  PubMed  PubMed Central  Google Scholar 

  • Niobe-Eyangoh SN, Kuaban C, Sorlin P, Cunin P, Thonnon J, Sola C, Rastogi N, Vincent V, Gutierrez MC (2003) Genetic biodiversity of Mycobacterium tuberculosis complex strains from patients with pulmonary tuberculosis in Cameroon. J Clin Microbiol 41: 2547–2553

    Article  PubMed  PubMed Central  Google Scholar 

  • North RJ, Ryan L, Lacource R, Mogues T, Goodrich ME (1999) Growth rate of Mycobacteria in mice as an unreliable indicator of Mycobacterial virulence. Infect Immun 67:5483–5485

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Brien L, Carmichael J, Lowrie DB, Andrew PW (1994) Strains of Mycobacterium tuberculosis differ in susceptibility to reactive nitrogen intermediates in vitro. Infect Immun 62:5187–5190

    PubMed  PubMed Central  Google Scholar 

  • O’Garra A, Redford PS, Mcnab FW, Bloom CI, Wilkinson RJ, Berry MPR (2013) The immune response in tuberculosis. Annu Rev Immunol 31:475–527

    Article  PubMed  CAS  Google Scholar 

  • Oddo M, Renno T, Attinger A, Bakker T, Macdonald HR, Meylan PR (1998) Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol 160:5448–5454

    CAS  PubMed  Google Scholar 

  • Ogarkov O, Mokrousov I, Sinkov V, Zhdanova S, Antipina S, Savilov E (2012) Lethal combination of Mycobacterium tuberculosis Beijing genotype and human CD209 -336G allele in Russian male population. Infect Genet Evol 12:732–736

    Article  PubMed  Google Scholar 

  • Olsen I, Balasingham SV, Davidsen T, Debebe E, Rodland EA, Van Soolingen D, Kremer K, Alseth I, Tønjum T (2009) Characterization of the major formamidopyrimidine-DNA glycosylase homolog in Mycobacterium tuberculosis and its linkage to variable tandem repeats. FEMS Immunol Med Microbiol 56:151–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ordway DJ, Sonnenberg MG, Donahue SA, Belisle JT, Orme IM (1995) Drug-resistant strains of Mycobacterium tuberculosis exhibit a range of virulence for mice. Infect Immun 63:741–743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ordway D, Henao-Tamayo M, Harton M, Palanisamy G, Troudt J, Shanley C, Basaraba RJ, Orme IM (2007) The hypervirulent Mycobacterium tuberculosis strain HN878 induces a potent TH1 response followed by rapid down-regulation. J Immunol 179:522–531

    Article  CAS  PubMed  Google Scholar 

  • Pareek M, Evans J, Innes J, Smith G, Hingley-Wilson S, Lougheed KE, Sridhar S, Dedicoat M, Hawkey P, Lalvani A (2013) Ethnicity and mycobacterial lineage as determinants of tuberculosis disease phenotype. Thorax 68:221–229

    Article  PubMed  Google Scholar 

  • Parsons SDC, Drewe JA, Van Pittius NCG, Warren RM, Van Heiden PD (2013) Novel cause of tuberculosis in meerkats, South Africa. Emerg Infect Dis 19: 2004–2007

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul S, Laochumroonvorapong P, Kaplan G (1996) Comparable growth of virulent and avirulent Mycobacterium tuberculosis in human macrophages in vitro. J Infect Dis 174:105–112

    Article  CAS  PubMed  Google Scholar 

  • Perez-Lago L, Navarro Y, Herranz M, Bouza E, Garcia-De-Viedma D (2013) Differences in gene expression between clonal variants of Mycobacterium tuberculosis emerging as a result of microevolution. Int J Med Microbiol 303:674–677

    Article  CAS  PubMed  Google Scholar 

  • Phares C, Wangroongsarb P, Chantra S, Paveenkitiporn W, Tondella ML, Benson R, Thacker WL, Fields B, Moore M, Fischer J, Dowell S, Olsen S (2007) Epidemiology of severe pneumonia caused by Legionella longbeachae, Mycoplasma pneumoniae, and Chlamydia pneumoniae: 1 year, population based surveillance for severe pneumonia in Thailand. Clin Infect Dis 45:e147–e155

    Article  PubMed  Google Scholar 

  • Pheiffer C, Betts JC, Flynn HR, Lukey PT, Van Helden P (2005) Protein expression by a Beijing strain differs from that of another clinical isolate and Mycobacterium tuberculosis H37Rv. Microbiology 151:1139–1150

    Article  CAS  PubMed  Google Scholar 

  • Portevin D, Gagneux S, Comas I, Young D (2011) Human macrophage responses to clinical isolates from the Mycobacterium tuberculosis complex discriminate between ancient and modern lineages. PLoS Pathog 7:e1001307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Portevin D, Sukumar S, Coscolla M, Shui G, Li B, Guan XL, Bendt AK, Young D, Gagneux S, Wenk MR (2014) Lipidomics and genomics of Mycobacterium tuberculosis reveal lineage-specific trends in mycolic acid biosynthesis. Microbiol Open 3:823–835

    Article  CAS  Google Scholar 

  • Rakotosamimanana N, Raharimanga V, Andriamandimby SF, Soares JL, Doherty TM, Ratsitorahina M, Ramarokoto H, Zumla A, Huggett J, Rook G, Richard V, Gicquel B, Rasolofo-Razanamparany V, The VVSG (2010) Variation in IFN-{gamma} responses to different infecting strains of Mycobacterium tuberculosis in AFB smear positive patients and household contacts in Antananarivo, Madagascar. Clin Vaccine Immunol CVI

    Google Scholar 

  • Reed MB, Domenech P, Manca C, Su H, Barczak AK, Kreiswirth BN, Kaplan G, Barry CE (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431:84–87

    Article  CAS  PubMed  Google Scholar 

  • Reed MB, Pichler VK, Mcintosh F, Mattia A, Fallow A, Masala S, Domenech P, Zwerling A, Thibert L, Menzies D, Schwartzman K, Behr MA (2009) Major Mycobacterium tuberculosis lineages associate with patient country of Origin. J Clin Microbiol 47:1119–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiling N, Homolka S, Walter K, Brandenburg J, Niwinski L, Ernst M, Herzmann C, Lange C, Diel R, Ehlers S, Niemann S (2013) Clade-specific virulence patterns of Mycobacterium tuberculosis complex strains in human primary macrophages and aerogenically infected mice. mBio 4

    Google Scholar 

  • Rhoades ER, Orme IM (1997) Susceptibility of a panel of virulent strains of Mycobacterium tuberculosis to reactive nitrogen intermediates. Infect Immun 65:1189–1195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha-Ramirez LM, Estrada-Garcia I, Lopez-Marin LM, Segura-Salinas E, Mendez-Aragon P, Van Soolingen D, Torres-Gonzalez R, Chacon-Salinas R, Estrada-Parra S, Maldonado-Bernal C, Lopez-Macias C, Isibasi A (2008) Mycobacterium tuberculosis lipids regulate cytokines, TLR-2/4 and MHC class II expression in human macrophages. Tuberculosis 88:212–220

    Article  CAS  PubMed  Google Scholar 

  • Rose G, Cortes T, Comas I, Coscolla M, Gagneux S, Young DB (2013) Mapping of genotype-phenotype diversity among clinical isolates of Mycobacterium tuberculosis by sequence-based transcriptional profiling. Genome Biol Evol 5:1849–1862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouse DA, Morris SL (1995) Molecular mechanisms of isoniazid resistance in Mycobacterium tuberculosis and Mycobacterium bovis. Infect Immun 63:1427–1433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rousseau C, Sirakova TD, Dubey VS, Bordat Y, Kolattukudy PE, Gicquel B, Jackson M (2003) Virulence attenuation of two Mas-like polyketide synthase mutants of Mycobacterium tuberculosis. Microbiology 149:1837–1847

    Article  CAS  PubMed  Google Scholar 

  • Rousseau C, Winter N, Pivert E, Bordat Y, Neyrolles O, Ave P, Huerre M, Gicquel B, Jackson M (2004) Production of phthiocerol dimycocerosates protects Mycobacterium tuberculosis from the cidal activity of reactive nitrogen intermediates produced by macrophages and modulates the early immune response to infection. Cell Microbiol 6:277–287

    Article  CAS  PubMed  Google Scholar 

  • Ruckdeschel K, Roggenkamp A, Lafont V, Mangeat P, Heesemann J, Rouot B (1997) Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect Immun 65:4813–4821

    CAS  PubMed  PubMed Central  Google Scholar 

  • Safi H, Barnes PF, Lakey DL, Shams H, Samten B, Vankayalapati R, Howard ST (2004) IS6110 functions as a mobile, monocyte-activated promoter in Mycobacterium tuberculosis. Mol Microbiol 52:999–1012

    Article  CAS  PubMed  Google Scholar 

  • Sarkar R, Lenders L, Wilkinson KA, Wilkinson RJ, Nicol MP (2012) Modern lineages of Mycobacterium tuberculosis exhibit lineage-specific patterns of growth and cytokine induction in human monocyte-derived macrophages. PLoS One 7:e43170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shell SS, Prestwich EG, Baek SH, Shah RR, Sassetti CM, Dedon PC, Fortune SM (2013) DNA methylation impacts gene expression and ensures hypoxic survival of Mycobacterium tuberculosis. PLoS Pathog 9:e1003419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK (2001) Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding α-crystallin. Proc Natl Acad Sci 98:7534–7539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinsimer D, Huet G, Manca C, Tsenova L, Koo MS, Kurepina N, Kana B, Mathema B, Marras SAE, Kreiswirth BN, Guilhot C, Kaplan G (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirakova TD, Thirumala AK, Dubey VS, Sprecher H, Kolattukudy PE (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

    Article  CAS  PubMed  Google Scholar 

  • Sirakova TD, Dubey VS, Cynamon MH, Kolattukudy PE (2003a) Attenuation of Mycobacterium tuberculosis by disruption of a mas-like gene or a chalcone synthase-like gene, which causes deficiency in dimycocerosyl phthiocerol synthesis. J Bacteriol 185:2999–3008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirakova TD, Dubey VS, Kim HJ, Cynamon MH, Kolattukudy PE (2003b) The largest open reading frame (pks12) in the Mycobacterium tuberculosis genome is involved in pathogenesis and dimycocerosyl phthiocerol synthesis. Infect Immun 71:3794–3801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith NH, Kremer K, Inwald J, Dale J, Driscoll JR, Gordon SV, Van Soolingen D, Glyn Hewinson R, Maynard Smith J (2006) Ecotypes of the Mycobacterium tuberculosis complex. J Theor Biol 239:220–225

    Article  PubMed  Google Scholar 

  • Soto CY, Menendez MC, Perez E, Samper S, Gomez AB, Garcia MJ, Martin C (2004) IS6110 mediates increased transcription of the phoP virulence gene in a multidrug-resistant clinical isolate responsible for tuberculosis outbreaks. J Clin Microbiol 42:212–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stavrum R, Praygod G, Range N, Faurholt-Jepsen D, Jeremiah K, Faurholt-Jepsen M, Krarup H, Aabye M, Changalucha J, Friis H, Andersen A, Grewal H (2014) Increased level of acute phase reactants in patients infected with modern Mycobacterium tuberculosis genotypes in Mwanza, Tanzania. BMC Infect Dis 14:309

    Article  PubMed  PubMed Central  Google Scholar 

  • Subbaiah TV, Ramachandran K (1961) The consistency of the susceptibility to hydrogen peroxide of tubercle bacilli isolated from South Indian patients before treatment. Tubercle 42:322–324

    Article  Google Scholar 

  • Subbaiah TV, Mitchison DA, Selkon JB (1960) The susceptibility to hydrogen peroxide of Indian and British isoniazid-sensitive and isoniazid-resistant tubercle bacilli. Tubercle 41:323–333

    Article  Google Scholar 

  • Subbian S, Bandyopadhyay N, Tsenova L, O’Brien P, Khetani V, Kushner N, Peixoto B, Soteropoulos P, Bader J, Karakousis P, Fallows D, Kaplan G (2013) Early innate immunity determines outcome of Mycobacterium tuberculosis pulmonary infection in rabbits. Cell Commun Signal 11:60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Supply P, Marceau M, Mangenot S, Roche D, Rouanet C, Khanna V, Majlessi L, Criscuolo A, Tap J, Pawlik A, Fiette L, Orgeur M, Fabre M, Parmentier C, Frigui W, Simeone R, Boritsch EC, Debrie AS, Willery E, Walker D, Quail MA, Ma L, Bouchier C, Salvignol G, Sayes F, Cascioferro A, Seemann T, Barbe V, Locht C, Gutierrez MC, Leclerc C, Bentley SD, Stinear TP, Brisse S, Medigue C, Parkhill J, Cruveiller S, Brosch R (2013) Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis. Nat Genet 45:172–179

    Article  CAS  PubMed  Google Scholar 

  • Tantivitayakul P, Panapruksachat S, Billamas P, Palittapongarnpim P (2010) Variable number of tandem repeat sequences act as regulatory elements in Mycobacterium tuberculosis. Tuberculosis 90:311–318

    Article  CAS  PubMed  Google Scholar 

  • Tanveer M, Hasan Z, Kanji A, Hussain R, Hasan R (2009) Reduced TNF-[alpha] and IFN-[gamma] responses to Central Asian strain 1 and Beijing isolates of Mycobacterium tuberculosis in comparison with H37Rv strain. Trans R Soc Trop Med Hyg 103:581–587

    Article  CAS  PubMed  Google Scholar 

  • Theus S-A, Cave MD, Eisenach K-D (2005) Intracellular macrophage growth rates and cytokine profiles of Mycobacterium tuberculosis strains with different transmission dynamics. J Infect Dis 191:453–460

    Article  CAS  PubMed  Google Scholar 

  • Theus SA, Cave MD, Eisenach K, Walrath J, Lee H, Mackay W, Whalen C, Silver RF (2006) Differences in the growth of paired Ugandan Isolates of Mycobacterium tuberculosis within human mononuclear phagocytes correlate with epidemiological evidence of strain virulence. Infect Immun 74:6865–6876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tientcheu LD, Sutherland JS, De Jong BC, Kampmann B, Jafali J, Adetifa IM, Antonio M, Dockrell HM, Ota MO (2014) Differences in T-cell responses between Mycobacterium tuberculosis and Mycobacterium africanum-infected patients. Eur J Immunol 44:1387–1398

    Article  CAS  PubMed  Google Scholar 

  • Torrelles JB, Schlesinger LS (2010) Diversity in Mycobacterium tuberculosis mannosylated cell wall determinants impacts adaptation to the host. Tuberculosis 90:84–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torrelles JB, Knaup R, Kolareth A, Slepushkina T, Kaufman TM, Kang P, Hill PJ, Brennan PJ, Chatterjee D, Belisle JT, Musser JM, Schlesinger LS (2008) Identification of Mycobacterium tuberculosis clinical isolates with altered phagocytosis by human macrophages due to a truncated lipoarabinomannan. J Biol Chem 283:31417–31428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsenova L, Ellison E, Harbacheuski R, Moreira A-L, Kurepina N, Reed M-B, Mathema B, Barry C-E III, Kaplan G (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

    Article  PubMed  Google Scholar 

  • Tsolaki AG, Hirsh AE, Deriemer K, Enciso JA, Wong MZ, Hannan M, De La Salmoniere Y-O, Aman K, Kato-Maeda M, Small PM (2004) Functional and evolutionary genomics of Mycobacterium tuberculosis : Insights from genomic deletions in 100 strains. Proc Natl Acad Sci U S A 101:4865–4870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuite AR, Guthrie JL, Alexander DC, Whelan MS, Lee B, Lam K, Ma J, Fisman DN, Jamieson FB (2013) Epidemiological evaluation of spatiotemporal and genotypic clustering of Mycobacterium tuberculosis in Ontario, Canada. Int J Tuberc Lung Dis 17:1322–1327

    Article  CAS  PubMed  Google Scholar 

  • Valway SE, Sanchez MP, Shinnick TF, Orme I, Agerton T, Hoy D, Jones JS, Westmoreland H, Onorato IM (1998) An outbreak involving extensive transmission of a virulent strain of Mycobacterium tuberculosis. N Engl J Med 338:633–639

    Article  CAS  PubMed  Google Scholar 

  • Van Crevel R, Nelwan RHH, De Lenne W, Veeraragu Y, Van Der Zanden AG, Amin Z, Van Der Meer JWM, Van Soolingen D (2001) Mycobacterium tuberculosis Beijing genotype strains associated with febrile response to treatment. Emerg Infect Dis 7:880–883

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Der Spuy GD, Warren RM, Richardson M, Beyers N, Behr MA, Van Helden PD (2003) Use of genetic distance as a measure of ongoing transmission of Mycobacterium tuberculosis. J Clin Microbiol 41:5640–5644

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Der Spuy GD, Kremer K, Ndabambi SL, Beyers N, Dunbar R, Marais BJ, Van Helden PD, Warren RM (2009) Changing Mycobacterium tuberculosis population highlights clade-specific pathogenic characteristics. Tuberculosis 89:120–125

    Article  PubMed  Google Scholar 

  • Van Laarhoven A, Mandemakers JJ, Kleinnijenhuis J, Enaimi M, Lachmandas E, Joosten LAB, Ottenhoff THM, Netea MG, Van Soolingen D, Van Crevel R (2013) Low induction of proinflammatory cytokines parallels evolutionary success of modern strains within the Mycobacterium tuberculosis Beijing genotype. Infect Immun 81:3750–3756

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Soolingen D, Hoogenboezem T, De Haas PEW, Hermans PWM, Koedam MA, Teppema KS, Brennan PJ, Besra GS, Portaels F, Top J, Schouls LM, Van Embden JDA (1997) A novel pathogenic taxon of the Mycobacterium tuberculosis complex, Canetti: characterization of an exceptional isolate from Africa. Int J Syst Bacteriol 47:1236–1245

    Article  PubMed  Google Scholar 

  • Vander Beken S, Al Dulayymi JR, Naessens T, Koza G, Maza-Iglesias M, Rowles R, Theunissen C, De Medts J, Lanckacker E, Baird MS, Grooten J (2011) Molecular structure of the Mycobacterium tuberculosis virulence factor, mycolic acid, determines the elicited inflammatory pattern. Eur J Immunol 41:450–460

    Article  CAS  PubMed  Google Scholar 

  • Velmurugan K, Chen B, Miller JL, Azogue S, Gurses S, Hsu T, Glickman M, Jacobs WR Jr, Porcelli SA, Briken V (2007) Mycobacterium tuberculosis nuoG is a virulence gene that inhibits apoptosis of infected host cells. PLoS Pathog 3:e110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vergne I, Fratti RA, Hill PJ, Chua J, Belisle J, Deretic V. Mycobacterium tuberculosis Phagosome Maturation Arrest: Mycobacterial Phosphatidylinositol Analog Phosphatidylinositol Mannoside Stimulates Early Endosomal Fusion. Molecular Biology of the Cell. 2004;15(2):751–60.

    Google Scholar 

  • Vergne I, Fratti RA, Hill PJ, Chua J, Belisle J, Deretic V. Mycobacterium tuberculosis Phagosome Maturation Arrest: Mycobacterial Phosphatidylinositol Analog Phosphatidylinositol Mannoside Stimulates Early Endosomal Fusion. Molecular Biology of the Cell. 2004;15(2):751–60.

    Google Scholar 

  • Via LE, Weiner DM, Schimel D, Lin PL, Dayao E, Tankersley SL, Cai Y, Coleman MT, Tomko J, Paripati P, Orandle M, Kastenmayer RJ, Tartakovsky M, Rosenthal A, Portevin D, Eum SY, Lahouar S, Gagneux S, Young DB, Flynn JL, Barry CE (2013) Differential virulence and disease progression following Mycobacterium tuberculosis complex infection of the common marmoset (Callithrix jacchus). Infect Immun 81:2909–2919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, Sherman DR, Schoolnik GK (2003) Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198:705–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wampande E, Mupere E, Debanne S, Asiimwe B, Nsereko M, Mayanja H, Eisenach K, Kaplan G, Boom H, Gagneux S, Joloba M (2013) Long-term dominance of Mycobacterium tuberculosis Uganda family in peri-urban Kampala-Uganda is not associated with cavitary disease. BMC Infect Dis 13:484

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang C, Peyron P, Mestre O, Kaplan G, Van Soolingen D, Gao Q, Gicquel B, Neyrolles O (2010) Innate immune response to Mycobacterium tuberculosis Beijing and other genotypes. PLoS One 5:e13594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weiner B, Gomez J, Victor TC, Warren RM, Sloutsky A, Plikaytis BB, Posey JE, Van Helden PD, Gey Van Pittius NC, Koehrsen M, Sisk P, Stolte C, White J, Gagneux S, Birren B, Hung D, Murray M, Galagan J (2012) Independent large scale duplications in multiple M. tuberculosis lineages overlapping the same genomic region. PLoS One 7:e26038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wickstrum JR, Bokhari SM, Fischer JL, Pinson DM, Yeh HW, Horvat RT, Parmely MJ (2009) Francisella tularensis induces extensive caspase-3 activation and apoptotic cell death in the tissues of infected mice. Infect Immun 77:4827–4836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wirth T, Hildebrand F, Allix-Beguec C, Wölbeling F, Kubica T, Kremer K, Van Soolingen D, Rüsch-Gerdes S, Locht C, Brisse S, Meyer A, Supply P, Niemann S (2008) Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog 4:e1000160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang Z, Yang D, Kong Y, Zhang L, Marrs CF, Foxman B, Bates JH, Wilson F, Cave MD (2005) Clinical relevance of Mycobacterium tuberculosis plcD gene mutations. Am J Respir Crit Care Med 171:1436–1442

    Article  PubMed  PubMed Central  Google Scholar 

  • Yindeeyoungyeon W, Likitvivatanavong S, Palittapongarnpim P (2009) Characterization of alpha-isopropylmalate synthases containing different copy numbers of tandem repeats in Mycobacterium tuberculosis. BMC Microbiol 9:122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu G, Fu X, Jin K, Zhang L, Wu W, Cui Z, Hu Z, Li Y (2011) Integrative analysis of transcriptome and genome indicates two potential genomic islands are associated with pathogenesis of Mycobacterium tuberculosis. Gene 489:21–29

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Gong J, Yang Z, Samten B, Cave MD, Barnes P-F (1999) Enhanced capacity of a widespread strain of Mycobacterium tuberculosis to grow in human macrophages. J Infect Dis 179:1213–1217

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Mantis N, Zhang X-R, Potoka DA, Watkins SC, Ford HR (2000) Salmonella typhimurium induces apoptosis in human monocyte-derived macrophages. Microbiol Immunol 44:987–995

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Zhong J, Jia X, Liu G, Kang Y, Dong M, et al. (2016) Precision methylome characterization of Mycobacterium tuberculosis complex (MTBC) using PacBio single-molecule real-time (SMRT) technology. Nucleic Acids Res. 44(2):730–43.

    Google Scholar 

  • Zumla A, Raviglione M, Hafner R, Fordham Von Reyn C (2013) Tuberculosis. N Engl J Med 368: 745–755

    Article  CAS  PubMed  Google Scholar 

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Coscolla, M. (2017). Biological and Epidemiological Consequences of MTBC Diversity. In: Gagneux, S. (eds) Strain Variation in the Mycobacterium tuberculosis Complex: Its Role in Biology, Epidemiology and Control. Advances in Experimental Medicine and Biology, vol 1019. Springer, Cham. https://doi.org/10.1007/978-3-319-64371-7_5

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