The non-human primate model of tuberculosis

Journal of Medical Primatology

Volumn 41, Issue 3, 2012, Pages 191-201

  Kaushal, D ^a,b   Mehra, S ^a   Didier, P J ^a   Lackner, A A ^a,b  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Latent; Mycobacterium tuberculosis; Non human primate; Reactivation; TB AIDS coinfection

Indexed keywords

BACTERIAL STRAIN; EXPERIMENTAL MODEL; GENETIC ASSOCIATION; GENOME; HISTOPATHOLOGY; HUMAN; HYPOXIA; IMMUNE SYSTEM; INFECTION; INFECTION SENSITIVITY; MACACA; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TUBERCULOSIS;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MACACA; MONKEY DISEASES; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

MACACA; MYCOBACTERIUM TUBERCULOSIS; PRIMATES;

EID: 84861483812     PISSN: 00472565     EISSN: 16000684     Source Type: Journal    
DOI: 10.1111/j.1600-0684.2012.00536.x     Document Type: Review

References (83)

1. Dye C, Scheele C, Dolin P, Pathania V, Raviglione MC: Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. JAMA 1999; 282:677-86.
2. Shah NS, Wright A, Bai GH, Barrera L, Boulahbal F, Martín-Casabona N, Drobniewski F, Drobniewski F, Gilpin C, Havelková M, Lepe R, Lumb R, Metchock B, Portaels F, Rodrigues MF, Rüsch-Gerdes S, Van Deun A, Vincent V, Laserson K, Wells C, Cegielski JP: Worldwide emergence of extensively drug-resistant tuberculosis. Emerg Infect Dis 2007; 13:380-7.
3. Fletcher HA: Correlates of immune protection from tuberculosis. Curr Mol Med 2007; 7:319-25.
4. Harrington M: From HIV to tuberculosis and back again: a tale of activism in 2 pandemics. Clin Infect Dis 2010; 50:S260-6.
5. von Reyn CF, Kimambo S, Mtei L, Arbeit RD, Maro I, Bakari M, Matee M, Lahey T, Adams LV, Black W, Mackenzie T, Lyimo J, Tvaroha S, Waddell R, Kreiswirth B, Horsburgh CR, Pallangyo K: Disseminated tuberculosis in human immunodeficiency virus infection: ineffective immunity, polyclonal disease and high mortality. Int J Tuberc Lung Dis 2011; 15:1087-92.
6. Koch R: Classics in infectious diseases. The etiology of tuberculosis: Robert Koch. Berlin, Germany. Rev Infect Dis 1982; 4:1270-4.
7. Padilla-Carlin DJ, McMurray DN, Hickey AJ: The guinea pig as a model of infectious diseases. Comp Med 2008; 58:324-40.
8. Nedeltchev GG, Raghunand TR, Jassal MS, Lun S, Cheng QJ, Bishai WR: Extrapulmonary dissemination of Mycobacterium bovis but not Mycobacterium tuberculosis in a bronchoscopic rabbit model of cavitary tuberculosis. Infect Immun 2009; 77:598-603.
9. Beamer GL, Turner J: Murine models of susceptibility to tuberculosis. Arch Immunol Ther Exp 2005; 53:469-83.
10. Flynn JL: Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect 2006; 8:1179-88.
11. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L: Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010; 327:466-9.
12. Davis JM, Clay H, Lewis JL, Ghori N, Herbomel P, Ramakrishnan L: Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 2002; 17:693.
13. Hirsch VM, Lifson JD: Simian immunodeficiency virus infection of monkeys as a model system for the study of AIDS pathogenesis, treatment, and prevention. Adv Pharmacol 2000; 49:437-77.
14. Lackner AA, Veazey RS: Current concepts in AIDS pathogenesis: insights from the SIV/macaque model. Annu Rev Med 2007; 58:461-76.
15. Deere JD, Schinazi RF, North TW: Simian immunodeficiency virus macaque models of HIV latency. Curr Opin HIV AIDS 2011; 6:57-61.
16. Staprans SI, Feinberg MB, Shiver JW, Casimiro DR: Role of nonhuman primates in the evaluation of candidate AIDS vaccines: an industry perspective. Curr Opin HIV AIDS 2010; 5:377-85.
17. Veazey RS, Ketas TJ, Dufour J, Moroney-Rasmussen T, Green LC, Klasse PJ, Moore JP: Protection of rhesus macaques from vaginal infection by vaginally delivered maraviroc, an inhibitor of HIV-1 entry via the CCR5 co-receptor. J Infect Dis 2010; 202:739-44.
18. Pichyangkul S, Kum-Arb U, Yongvanitchit K, Limsalakpetch A, Gettayacamin M, Lanar DE, Ware LA, Stewart VA, Heppner DG, Mettens P, Cohen JD, Ballou WR, Fukuda MM: Preclinical evaluation of the safety and immunogenicity of a vaccine consisting of Plasmodium falciparum liver-stage antigen 1 with adjuvant AS01B administered alone or concurrently with the RTS, S/AS01B vaccine in rhesus primates. Infect Immun 2008; 76:229-38.
19. Purcell RH, Emerson SU: Animal models of hepatitis A and E. ILAR J 2001; 42:161-77.
20. Johnson RF, Yellayi S, Cann JA, Johnson A, Smith AL, Paragas J, Jahrling PB, Blaney JE: Cowpox virus infection of cynomolgus macaques as a model of hemorrhagic smallpox. Virology 2011; 418:102-12.
21. Reed DS, Lackemeyer MG, Garza NL, Sullivan LJ, Nichols DK: Aerosol exposure to Zaire ebolavirus in three nonhuman primate species: differences in disease course and clinical pathology. Microbes Infect 2011; 13:930-6.
22. Dupuy LC, Richards MJ, Reed DS, Schmaljohn CS: Immunogenicity and protective efficacy of a DNA vaccine against Venezuelan equine encephalitis virus aerosol challenge in nonhuman primates. Vaccine 2010; 28:7345-50.
23. Geisbert TW, Daddario-DiCaprio KM, Hickey AC, Smith MA, Chan YP, Wang LF, Mattapallil JJ, Geisbert JB, Bossart KN, Broder CC: Development of an acute and highly pathogenic nonhuman primate model of Nipah virus infection. PLoS ONE 2010; 5:e10690.
24. Swenson DL, Warfield KL, Larsen T, Alves DA, Coberley SS, Bavari S: Monovalent virus-like particle vaccine protects guinea pigs and nonhuman primates against infection with multiple Marburg viruses. Expert Rev Vaccines 2008; 7:417-29.
25. Lawler JV, Endy TP, Hensley LE, Garrison A, Fritz EA, Lesar M, Baric RS, Kulesh DA, Norwood DA, Wasieloski LP, Ulrich MP, Slezak TR, Vitalis E, Huggins JW, Jahrling PB, Paragas J: Cynomolgus macaque as an animal model for severe acute respiratory syndrome. PLoS Med 2006; 3:e149.
26. Durbin AP, Elkins WR, Murphy BR: African green monkeys provide a useful nonhuman primate model for the study of human parainfluenza virus types-1, -2, and -3 infection. Vaccine 2000; 18:2462-9.
27. Shipley TW, Kling HM, Morris A, Patil S, Kristoff J, Guyach SE, Murphy JE, Shao X, Sciurba FC, Rogers RM, Richards T, Thompson P, Montelaro RC, Coxson HO, Hogg JC, Norris KA: Persistent pneumocystis colonization leads to the development of chronic obstructive pulmonary disease in a nonhuman primate model of AIDS. J Infect Dis 2010; 202:302-12.
28. Twenhafel NA: Pathology of inhalational anthrax animal models. Vet Pathol 2010; 47:819-30.
29. Zhang W, Ahmad G, Torben W, Noor Z, Le L, Damian RT, Wolf RF, White GL, Chavez-Suarez M, Podesta RB, Kennedy RC, Siddiqui AA: Sm-p80-based DNA vaccine provides baboons with levels of protection against Schistosoma mansoni infection comparable to those achieved by the irradiated cercarial vaccine. J Infect Dis 2010; 201:1105-12.
30. Kari L, Whitmire WM, Crane DD, Reveneau N, Carlson JH, Goheen MM, Peterson EM, Pal S, de la Maza LM, Caldwell HD: Chlamydia trachomatis native major outer membrane protein induces partial protection in nonhuman primates: implication for a trachoma transmission-blocking vaccine. J Immunol 2009; 182:8063-70.
31. Smith MA, Takeuchi K, Anderson G, Ware GO, McClure HM, Raybourne RB, Mytle N, Doyle MP: Dose-response model for Listeria monocytogenes-induced stillbirths in nonhuman primates. Infect Immun 2008; 76:726-31.
32. Virtaneva K, Graham MR, Porcella SF, Hoe NP, Su H, Graviss EA, Gardner TJ, Allison JE, Lemon WJ, Bailey JR, Parnell MJ, Musser JM: Group A Streptococcus gene expression in humans and cynomolgus macaques with acute pharyngitis. Infect Immun 2003; 71:2199-207.
33. Campos-Neto A, Porrozzi R, Greeson K, Coler RN, Webb JR, Seiky YA, Reed SG, Grimaldi G Jr: Protection against cutaneous leishmaniasis induced by recombinant antigens in murine and nonhuman primate models of the human disease. Infect Immun 2001; 69:4103-8.
34. Waag DM, Byrne WR, Estep J, Gibbs P, Pitt ML, Banfield CM: Evaluation of cynomolgus (Macaca fascicularis) and rhesus (Macaca mulatta) monkeys as experimental models of acute Q fever after aerosol exposure to phase-I Coxiella burnetii. Lab Anim Sci 1999; 49:634-8.
35. Barclay WR, Anacker RL, Brehmer W, Leif W, Ribi E: Aerosol induced tuberculosis in subhuman primates and the course of the disease after intravenous BCG vaccination. Infect Immun 1970; 2:574-82.
36. Chaparas SD, Good RC, Janicki BW: Tuberculin-induced lymphocyte transformation and skin reactivity in monkeys vaccinated or not vaccinated with Bacille Calmette-Guerin, then challenged with virulent Mycobacterium tuberculosis. Am Rev Respir Dis 1975; 112:43-7.
37. Walsh GP, Tan EV, dela Cruz EC, Abalos RM, Villahermosa LG, Young LJ, Cellona RV, Nazareno JB, Horwitz MA: The Philippine cynomolgus monkey (Macaca fasicularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med 1996; 2:430-6.
38. Capuano SV 3rd, Croix DA, Pawar S, Zinovik A, Myers A, Lin PL, Bissel S, Fuhrman C, Klein E, Flynn JL: Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect Immun 2003; 71:5831-44.
39. Langermans JA, Doherty TM, Vervenne RA, van der Laan T, Lyashchenko K, Greenwald R, Agger EM, Aagaard C, Weiler H, van Soolingen D, Dalemans W, Thomas AW, Andersen P: Protection of macaques against Mycobacterium tuberculosis infection by a subunit vaccine based on a fusion protein of antigen 85B and ESAT-6. Vaccine 2005; 23:2740-50.
40. Lin PL, Pawar S, Myers A, Pegu A, Fuhrman C, Reinhart TA, Capuano SV, Klein E, Flynn JL: Early events in Mycobacterium tuberculosis infection in cynomolgus macaques. Infect Immun 2006; 74:3790-803.
41. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS, Eum SY, Taylor K, Klein E, Manjunatha U, Gonzales J, Lee EG, Park SK, Raleigh JA, Cho SN, McMurray DN, Flynn JL, Barry CE 3rd: Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 2008; 76:2333-40.
42. Lin PL, Rodgers M, Smith L, Bigbee M, Myers A, Bigbee C, Chiosea I, Capuano SV, Fuhrman C, Klein E, Flynn JL: Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect Immun 2009; 77:4631-42.
43. Reed SG, Coler RN, Dalemans W, Tan EV, DeLa Cruz EC, Basaraba RJ, Orme IM, Skeiky YA, Alderson MR, Cowgill KD, Prieels JP, Abalos RM, Dubois MC, Cohen J, Mettens P, Lobet Y: Defined tuberculosis vaccine, Mtb72F/AS02A, evidence of protection in cynomolgus monkeys. Proc Natl Acad Sci USA 2009; 106:2301-6.
44. Larsen MH, Biermann K, Chen B, Hsu T, Sambandamurthy VK, Lackner AA, Aye PP, Didier P, Huang D, Shao L, Wei H, Letvin NL, Frothingham R, Haynes BF, Chen ZW, Jacobs WR Jr: Efficacy and safety of live attenuated persistent and rapidly cleared Mycobacterium tuberculosis vaccine candidates in non-human primates. Vaccine 2009; 27:4709-17.
45. Diedrich CR, Mattila JT, Klein E, Janssen C, Phuah J, Sturgeon TJ, Montelaro RC, Lin PL, Flynn JL: Reactivation of latent tuberculosis in cynomolgus macaques infected with SIV is associated with early peripheral T cell depletion and not virus load. PLoS ONE 2010; 5:e9611.
46. Lin PL, Myers A, Smith L, Bigbee C, Bigbee M, Fuhrman C, Grieser H, Chiosea I, Voitenek NN, Capuano SV, Klein E, Flynn JL: Tumor necrosis factor neutralization results in disseminated disease in acute and latent Mycobacterium tuberculosis infection with normal granuloma structure in a cynomolgus macaque model. Arthritis Rheum 2010; 62:340-50.
47. Green AM, Mattila JT, Bigbee CL, Bongers KS, Lin PL, Flynn JL: CD4(+) regulatory T cells in a cynomolgus macaque model of Mycobacterium tuberculosis infection. J Infect Dis 2010; 202:533-41.
48. Mattila JT, Diedrich CR, Lin PL, Phuah J, Flynn JL: Simian immunodeficiency virus-induced changes in T cell cytokine responses in cynomolgus macaques with latent Mycobacterium tuberculosis infection are associated with timing of reactivation. J Immunol 2011; 186:3527-37.
49. Ford CB, Lin PL, Chase MR, Shah RR, Iartchouk O, Galagan J, Mohaideen N, Ioerger TR, Sacchettini JC, Lipsitch M, Flynn JL, Fortune SM: Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 2011; 43:482-6.
50. Lin PL, Dietrich J, Tan E, Abalos RM, Burgos J, Bigbee C, Bigbee M, Milk L, Gideon HP, Rodgers M, Cochran C, Guinn KM, Sherman DR, Klein E, Janssen C, Flynn JL, Andersen P: The multistage vaccine H56 boosts the effects of BCG to protect cynomolgus macaques against active tuberculosis and reactivation of latent Mycobacterium tuberculosis infection. J Clin Invest 2012; 122:303-14.
51. Croix DA, Capuano S 3rd, Simpson L, Fallert BA, Fuller CL, Klein EC, Reinhart TA, Murphey-Corb M, Flynn JL: Effect of mycobacterial infection on virus loads and disease progression in simian immunodeficiency virus-infected rhesus monkeys. AIDS Res Hum Retroviruses 2000; 16:1895-908.
52. Shen Y, Shen L, Sehgal P, Zhou D, Simon M, Miller M, Enimi EA, Henckler B, Chalifoux L, Sehgal N, Gastron M, Letvin NL, Chen ZW: Antiretroviral agents restore Mycobacterium-specific T-cell immune responses and facilitate controlling a fatal tuberculosis-like disease in Macaques coinfected with simian immunodeficiency virus and Mycobacterium bovis BCG. J Virol 2001; 75:8690-6.
53. Shen Y, Zhou D, Chalifoux L, Shen L, Simon M, Zeng X, Lai X, Li Y, Sehgal P, Letvin NL, Chen ZW: Induction of an AIDS virus-related tuberculosis-like disease in macaques: a model of simian immunodeficiency virus- mycobacterium coinfection. Infect Immun 2002; 70:869-77.
54. Shen Y, Zhou D, Qiu L, Lai X, Simon M, Shen L, Kou Z, Wang Q, Jiang L, Estep J, Hunt R, Clagett M, Sehgal PK, Li Y, Zeng X, Morita CT, Brenner MB, Letvin NL, Chen ZW: Adaptive immune response of Vgamma2Vdelta2+ T cells during mycobacterial infections. Science 2002; 295:2255-8.
55. Safi H, Gormus BJ, Didier PJ, Blanchard JL, Lakey DL, Martin LN, Murphey-Corb M, Vankayalapati R, Barnes PF: Spectrum of manifestations of Mycobacterium tuberculosis infection in primates infected with SIV. AIDS Res Hum Retroviruses 2003; 19:585-95.
56. Gormus BJ, Blanchard JL, Alvarez XH, Didier PJ: Evidence for a rhesus monkey model of asymptomatic tuberculosis. J Med Primatol 2004; 33:134-45.
57. Qiu L, Huang D, Chen CY, Wang R, Shen L, Shen Y, Hunt R, Estep J, Haynes BF, Jacobs WR Jr, Letvin N, Du G, Chen ZW: Severe tuberculosis induces unbalanced up-regulation of gene networks and overexpression of IL-22, MIP-1alpha, CCL27, IP-10, CCR4, CCR5, CXCR3, PD1, PDL2, IL-3, IFN-beta, TIM1, and TLR2 but low antigen-specific cellular responses. J Infect Dis 2008; 198:1514-9.
58. Shen L, Shen Y, Huang D, Qiu L, Sehgal P, Du GZ, Miller MD, Letvin NL, Chen ZW: Development of Vgamma2Vdelta2+ T cell responses during active mycobacterial coinfection of simian immunodeficiency virus-infected macaques requires control of viral infection and immune competence of CD4+ T cells. J Infect Dis 2004; 19:1438-47.
59. Verreck FA, Vervenne RA, Kondova I, van Kralingen KW, Remarque EJ, Braskamp G, van der Werff NM, Kersbergen A, Ottenhoff TH, Heidt PJ, Gilbert SC, Gicquel B, Hill AV, Martin C, McShane H, Thomas AW: MVA.85A boosting of BCG and an attenuated, phoP deficient M. tuberculosis vaccine both show protective efficacy against tuberculosis in rhesus macaques. PLoS ONE 2009; 4:e5264.
60. Chen CY, Huang D, Wang RC, Shen L, Zeng G, Yao S, Shen Y, Halliday L, Fortman J, McAllister M, Estep J, Hunt R, Vasconcelos D, Du G, Porcelli SA, Larsen MH, Jacobs WR Jr, Haynes BF, Letvin NL, Chen ZW: A critical role for CD8 T cells in a nonhuman primate model of tuberculosis. PLoS Pathog 2009; 5:e1000392.
61. Sugawara I, Sun L, Mizuno S, Taniyama T: Protective efficacy of recombinant BCG Tokyo (Ag85A) in rhesus monkeys (Macaca mulatta) infected intratracheally with H37Rv Mycobacterium tuberculosis. Tuberculosis 2009; 89:62-7.
62. Dutta NK, Mehra S, Didier PJ, Roy CJ, Doyle LA, Alvarez X, Ratterree M, Be NA, Lamichhane G, Jain SK, Lacey MR, Lackner AA, Kaushal D: Genetic requirements for the survival of tubercle bacilli in primates. J Infect Dis 2010; 201:1743-52.
63. Sharpe SA, McShane H, Dennis MJ, Basaraba RJ, Gleeson F, Hall G, McIntyre A, Gooch K, Clark S, Beveridge NE, Nuth E, White A, Marriott A, Dowall S, Hill AV, Williams A, Marsh PD: Establishment of an aerosol challenge model of tuberculosis in rhesus macaques and an evaluation of endpoints for vaccine testing. Clin Vaccine Immunol 2010; 17:1170-82.
64. Mehra S, Pahar B, Dutta NK, Conerly CN, Philippi-Falkenstein K, Alvarez X, Kaushal D: Transcriptional reprogramming in nonhuman primate (rhesus macaque) tuberculosis granulomas. PLoS ONE 2010; 5:e12266.
65. Yao S, Huang D, Chen CY, Halliday L, Zeng G, Wang RC, Chen ZW: Differentiation, distribution and gammadelta T cell-driven regulation of IL-22-producing T cells in tuberculosis. PLoS Pathog 2010; 6:e1000789.
66. Mehra S, Golden NA, Stuckey KJ, Didier PJ, Doyle LA, Russell-Lodrigue KE, Sugimoto C, Hasegawa A, Sivasubramani SK, Kuroda MJ, Blanchard JL, Lackner AA, Kaushal D: The Mycobacterium tuberculosis SigH is required for bacterial burden as well as immunopathology in primates. J Infect Dis 2012; 205.
67. Luciw PA, Oslund KL, Yang XW, Adamson L, Ravindran R, Canfield DR, Tarara R, Hirst L, Christensen M, Lerche NW, Offenstein H, Lewinsohn D, Ventimiglia F, Brignolo L, Wisner ER, Hyde DM: Stereological analysis of bacterial load and lung lesions in nonhuman primates (rhesus macaques) experimentally infected with Mycobacterium tuberculosis. Am J Physiol Lung Cell Mol Physiol 2011; 301:L731-8.
68. Mehra S, Golden NA, Dutta NK, Midkiff CC, Alvarez X, Doyle LA, Asher M, Russell-Lodrigue K, Monjure C, Roy CJ, Blanchard JL, Didier PJ, Veazey RS, Lackner AA, Kaushal D: Reactivation of latent tuberculosis in rhesus macaques by coinfection with simian immunodeficiency virus. J Med Primatol 2011; 40:233-43.
69. Sampson SL, Mansfield KG, Carville A, Magee DM, Quitugua T, Howerth EW, Bloom BR, Hondalus MK: Extended safety and efficacy studies of a live attenuated double leucine and pantothenate auxotroph of Mycobacterium tuberculosis as a vaccine candidate. Vaccine 2011; 29:4839-47.
70. Zeng G, Chen CY, Huang D, Yao S, Wang RC, Chen ZW: Membrane-bound IL-22 after de novo production in tuberculosis and anti-Mycobacterium tuberculosis effector function of IL-22+ CD4+ T cells. J Immunol 2011; 187:190-9.
71. Sharpe SA, Eschelbach E, Basaraba RJ, Gleeson F, Hall GA, McIntyre A, Williams A, Kraft SL, Clark S, Gooch K, Hatch G, Orme IM, Marsh PD, Dennis MJ: Determination of lesion volume by MRI and stereology in a macaque model of tuberculosis. Tuberculosis 2009; 89:405-16.
72. Langermans JA, Andersen P, van Soolingen D, Vervenne RA, Frost PA, van der Laan T, van Pinxteren LA, van den Hombergh J, Kroon S, Peekel I, Florquin S, Thomas AW: Divergent effect of bacillus Calmette-Guérin (BCG) vaccination on Mycobacterium tuberculosis infection in highly related macaque species: implications for primate models in tuberculosis vaccine research. Proc Natl Acad Sci USA 2001; 98:11497-502.
73. Lewinsohn DM, Tydeman IS, Frieder M, Grotzke JE, Lines RA, Ahmed S, Prongay KD, Primack SL, Colgin LMA, Lewis AD, Lewinsohn DA: High resolution radiographic and fine immunologic definition of TB disease progression in the rhesus macaque. Microbes Infect 2006; 8:2587-98.
74. Sassetti CM, Boyd DH, Rubin EJ: Comprehensive identification of conditionally essential genes in mycobacteria. Proc Natl Acad Sci USA 2001; 98:12712-7.
75. Rengarajan J, Bloom BR, Rubin EJ: Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci USA 2005; 102:8327-32.
76. Griffin JE, Gawronski JD, DeJesus MA, Loerger TR, Akerley BA, Sassetti CM: High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 2011; 7:e1002251.
77. Kurthkoti K, Varshney U: Distinct mechanisms of DNA repair in mycobacteria and their implications in attenuation of the pathogen growth. Mech Ageing Dev 2011; in press.
78. Williams MJ, Kana BD, Mizrahi V: Functional analysis of molybdopterin biosynthesis in mycobacteria identifies a fused molybdopterin synthase in Mycobacterium tuberculosis. J Bacteriol 2011; 193:98-106.
79. Russell DG: Who puts the tubercle in tuberculosis? Nat Rev Microbiol 2007; 5:39-47.
80. Kaufmann SH, Cole ST, Mizrahi V, Rubin E, Nathan C: Mycobacterium tuberculosis and the host response. J Exp Med 2005; 201:1693-7.
81. Park HD, Guinn KM, Harrell MI, Liao R, Voskuil MI, Tompa M, Schoolnik GK, Sherman DR: Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 2003; 48:833-43.
82. Roberts DM, Liao RP, Wisedchaisri G, Hol WG, Sherman DR: Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J Biol Chem 2004; 279:23082-7.
83. Zinman G, Brower-Sinning R, Emeche CH, Ernst J, Huang GT, Mahony S, Myers AJ, O'Dee DM, Flynn JL, Nau GJ, Ross TM, Salter RD, Benos PV, Bar Joseph Z, Morel PA: Large scale comparison of innate responses to viral and bacterial pathogens in mouse and macaque. PLoS ONE 2011; 6:e22401.