Latent tuberculosis: Mechanisms of host and bacillus that contribute to persistent infection

Lancet Infectious Diseases

Volumn 3, Issue 9, 2003, Pages 578-590

  Tufariello, JoAnn M ^a   Chan, John ^a   Flynn, JoAnne L ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10;

BACTERIAL REACTIVATION; BACTERIAL VIRULENCE; CYTOKINE PRODUCTION; HOST PATHOGEN INTERACTION; HOST RANGE; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; LATENT PERIOD; LATENT TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TUBERCULOSIS;

EID: 0042863345     PISSN: 14733099     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1473-3099(03)00741-2     Document Type: Review

References (176)

1. The World Health Report 1999: making a difference. Geneva: WHO, 1999: 116.
2. Daniel TM, Bates JH, Downes KA. History of tuberculosis. In: Bloom BR, ed. Tuberculosis: pathogenesis, protection and control. Washington DC: ASM Press, 1994: 13-24.
3. Tuberculosis. WHO fact sheet no 104. Geneva: WHO, 2002.
4. Dolin PJ, Raviglione MC, Kochi A. Global tuberculosis incidence and mortality during 1990-2000. Bull World Health Organ 1994; 72: 213-20.
5. De Cock KM, Chaisson RE. Will DOTS do it? A reappraisal of tuberculosis control in countries with high rates of HIV infection. Int J Tuberc Lung Dis 1999; 3: 457-65.
6. Pablos-Mendez A, Raviglione MC, Laszlo A, et al. Global surveillance for antituberculosis-drug resistance, 1994-1997. World Health Organization-International Union against Tuberculosis and Lung Disease Working Group on Anti-Tuberculosis Drug Resistance Surveillance. [erratum appears in N Engl J Med 1998; 339: 139]. N Engl J Med 1998; 338: 1641-49.
7. Snider DE Jr, Castro KG. The global threat of drug-resistant tuberculosis. N Engl J Med 1998; 338: 1689-90.
8. Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. JAMA 1999; 282: 677-86.
9. Styblo K. Recent advances in epidemiological research in tuberculosis. Adv Tuberc Res 1980; 20: 1-63.
10. Flynn JL, Chan J. Immunology of tuberculosis. Annu Rev Immunol 2001; 19: 93-129.
11. Gedde-Dahl T. Tuberculous infection in the light of tuberculin matriculation. Am J Hyg 1952; 56: 139-214.
12. Selwyn PA, Hartel D, Lewis VA, et al. A prospective study of the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. N Engl J Med 1989; 320: 545-50.
13. Stead WW. Pathogenesis of a first episode of chronic pulmonary tuberculosis in man: recrudescence of residuals of the primary infection or exogenous reinfection? Am Rev Respir Dis 1967; 95: 729-45.
14. Stead WW. Pathogenesis of the sporadic case of tuberculosis. N Engl J Med 1967; 277: 1008-12.
15. Opie E, Aronson J. Tubercule bacilli in latent tuberculosis lesions and in lung tissue without tuberculosis lesions. Arch Pathol 1927; 4: 1-21.
16. Means TK, Wang S, Lien E, Yoshimura A, Golenbock DT, Fenton MJ. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J Immunol 1999; 163: 3920-27.
17. Hertz CJ, Kiertscher SM, Godowski PJ, et al. Microbial lipopeptides stimulate dendritic cell maturation via Toll-like receptor 2. J Immunol 2001; 166: 2444-50.
18. Bodnar KA, Serbina NV, Flynn JL. Interaction of Mycobacterium tuberculosis with murine dendritic cells. Infect Immun 2001; 69: 800-09.
19. Henderson RA, Watkins SC, Flynn JL. Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J Immunol 1994; 159: 635-43.
20. Gonzalez-Juarrero M, Turner OC, Turner J, Marietta P, Brooks JV, Orme IM. Temporal and spatial arrangement of lymphocytes within lung granulomas induced by aerosol infection with Mycobacterium tuberculosis. Infect Immun 2001; 69: 1722-28.
21. Grzybowski S, Allen EA. The challenge of tuberculosis in decline. Am Rev Respir Dis 1964; 90: 707-20.
22. Stead WW. Tuberculosis among elderly persons: an outbreak in a nursing home. Ann Intern Med 1981; 94: 606-10.
23. Stead WW, Lofgren JP, Warren E, Thomas C. Tuberculosis as an endemic and nosocomial infection among the elderly in nursing homes. N Engl J Med 1985; 312: 1483-87.
24. Rees RJW, Hart D'A. Analysis of the host-parasite equilibrium in chronic murine tuberculosis by total and viable bacillary counts. Br J Exp Pathol 1961; 42: 83-88.
25. McCune RM, Feldmann FM, Lambert HP, McDermott W. Microbial persistence I: the capacity of tubercle bacilli to survive sterilization in mouse tissues. J Exp Med 1966; 123: 445-68.
26. McCune RM, Feldman FM, McDermott W. Microbial persistence II: characteristics of the sterile state of tubercle bacilli. J Exp Med 1966; 123: 469-86.
27. Scanga CA, Mohan VP, Joseph H, Yu K, Chan J, Flynn JL. Reactivation of latent tuberculosis: variations on the Cornell murine model. Infect Immun 1999; 67: 4531-38.
28. van Pinxteren LAH, Cassidy JP, Smedegaard BHC, Agger EM, Andersen P. Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur J Immunol 2000; 30: 3689-98.
29. Lowrie DB, Tascon RE, Bonato VLD, et al. Therapy of tuberculosis in mice by DNA vaccination. Nature 1999; 400: 269-71.
30. Flynn JL, Chan J. Animal models of tuberculosis. In: Rom SMG, ed. Tuberculosis, 2nd edn. Philadelphia: Lippincott, Williams and Wilkins, 2003: 237-50.
31. Lurie M. Studies on the mechanism of immunity in tuberculosis: the fate of tubercle bacilli ingested by mononuclear phagocytes derived from normal and immunized animals. J Exp Med 1942; 75: 247.
32. Lurie MB. Resistance to tuberculosis: experimental studies in native and acquired defense mechanisms. Cambridge, MA: Harvard University Press, 1964.
33. Walsh GP, Tan EV, de la Cruz EC, et al. The Philippine cynomolgus monkey (Macaca fascularis) provides a new nonhuman primate model of tuberculosis that resembles human disease. Nat Med 1996; 2: 430-36.
34. Langermans JAM, Andersen P, van Soolingen D, et al. Divergent effect of bacillus Calmette-Guerin (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.
35. Shen Y, Zhou D, Qiu L, et al. Adaptive immune response of Vγ2Vδ2+T cells during mycobacterial infections. Science 2002; 295: 2255-58.
36. Capuano SVI, Croix DA, Pawar S, et al. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M tuberculosis infection. Infect Immun (in press).
37. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR. An essential role for interferon-γ in resistance to Mycobacterium tuberculosis infection. J Exp Med 1993; 178: 2249-54.
38. Cooper AM, Dalton DK, Stewart TA, Griffen JP, Russell DG, Orme IM Disseminated tuberculosis in IFN-γ gene-disrupted mice. J Exp Med 1993; 178: 2243-48.
39. MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, Nathan CF. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci USA 1997; 94: 5243-48.
40. Scanga CA, Mohan VP, Tanaka K, Alland D, Flynn JL. The NOS2 locus confers protection in mice against aerogenic challenge of both clinical and laboratory strains of Mycobacterium tuberculosis. Infect Immun 2001; 69: 7711-17.
41. Cooper AM, Pearl JE, Brooks JV, Ehlers IMO. Expression of the nitric oxide synthase 2 gene is not essential for early control of Mycobacterium tuberculosis in the murine lung. Infect Immun 2000; 68:6879-82.
42. Caruso AM, Serbina N, Klein E, Triebold K, Bloom BR, Flynn JL. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-γ, yet succumb to tuberculosis. J Immunol 1999; 162: 5407-16.
43. Saunders BM, Frank AA, Orme IM, Cooper AM CD4 is required for the development of a protective granulomatous response to pulmonary tuberculosis. Cell Immunol 2002; 216: 65-72.
44. Ottenhof TH, Kumararatne D, Casanova JL. Novel human immunodeficiencies reveal the essential role of type-1 cytokines in immunity to intracellular bacteria. Immunol Today 1998; 19: 491-94.
45. Tascon RE, Stavropoulos E, Lukacs KV, Colston MJ. Protection against Mycobacterium tuberculosis infection by CD8 T cells requires production of gamma interferon. Infect Immun 1998; 66: 830-34.
46. Serbina NV, Flynn JL. Early emergence of CD8+ T cells primed for production of type 1 cytokines in the lungs of Mycobacterium tuberculosis-infected mice. Infect Immun 1999; 67: 3980-88.
47. Feng CG, Bean AGD, Hooi H, Briscoe H, Britton WJ. Increase in gamma interferon-secreting CD8+, as well as CD4+ T cells in lungs following aerosol infection with Mycobacterium tuberculosis. Infect Immun 1999; 67: 3242-47.
48. Scanga CA, Mohan VP, Yu K, Joseph H, Tanaka K, Chan J, Flynn JL. Depletion of CD4+ T cells causes reactivation of murine persistent tuberculosis despite continued expression of IFN-γ and NOS2. J Exp Med 2000; 192: 347-58.
49. Oddo M, Renno T, Attinger A, Bakker T, MacDonald HR, Meylan PRA. Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J Immunol 1998; 160: 5448-54.
50. Keane J, Remold HG, Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol 2000; 164: 2016-20.
51. Molloy A, Laochumroonvorapong P, Kaplan G. Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J Exp Med 1994; 180: 1499-509.
52. Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A, Alber G. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 1996; 184: 747-52.
53. Kennedy MK, Park LS. Characterization of interleukin-15 (IL-15) and the IL-15 receptor complex. J Clin Immunol 1996; 16: 134-43.
54. Noelle RJ. CD40 and its ligand in host defense. Immunity 1996; 4: 415-19.
55. Campbell KA, Ovendale PJ, Kennedy MK, Fanslow SG, Reed SG, Maliszewski CR. CD40 ligand is required for protective cell-mediated immunity to Leishmania major. Immunity 1996; 4: 283-89.
56. Matloubian M, Concepcion R, Ahmed R. CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J Virol 1994; 68: 8056-63.
57. Borrow P, Tough DF, Eto D, et al. CD40 Ligand-mediated interactions are involved in the generation of memory CD8+ cytotoxic T lymphocytes (CTL) but are not required for the maintenance of CTL memory following infections. J Virol 1998; 72: 7440-49.
58. Kirberg D, Bruno L, von Boehmer H. CD4+8- help prevents rapid deletion of CD8+ cells after a transient response to antigen. Eur J Immunol 1993; 23: 1963-67.
59. Clarke SRM The critical role of CD40/CD40L in the CD4-dependent generation of CD8+ T cell immunity. J Leukoc Biol 2000; 67: 607-14.
60. Serbina NV, Lazarevic V, Flynn JL. CD4+ T cells are required for the development of cytotoxic CD8+ T cells during Mycobacterium tuberculosis infection. J Immunol 2001; 167: 6991-7000.
61. Khan IA, Kaspar LH. IL-15 augments CD8 T cell-mediated immunity against Toxoplasma gondii infection in mice. J Immunol 1996; 157: 2103-08.
62. Khan IA, Casciotti L. IL-15 prolongs the duration of CD8 T cell-mediated immunity in mice infected with a vaccine strain of Toxoplasma gondii. J Immunol 1999; 163: 4503-09.
63. Zhang X, Sun S, Hwang I, Tough DF, Sprent J. Potent and selective stimulation of memory phenotype CD8+ T cells in vivo by IL-15. Immunity 1998; 8: 591.
64. Stenger S, Hanson DA, Teitelbaum R, et al. An antimicrobial activity of cytotoxic T cells mediated by granulysin. Science 1998; 282: 121-25.
65. Flynn JL, Goldstein MM, Triebold KJ, Koller B, Bloom BR. Major histocompatibility complex class I-restricted T cells are required for resistance to Mycobacterium tuberculosis infection. Proc Natl Acad Sci USA 1992; 89: 12013-17.
66. Rolph MS, Raupach B, Kobernick HH, et al. MHC class Ia-restricted T cells partially account for beta2-microglobulin-dependent resistance to Mycobacterium tuberculosis. Eur J Immunol 2001; 31: 1944-49.
67. Behar SM, Dascher CC, Grusby MJ, Wang CR, Brenner MB. Susceptibility of mice deficient in CDID or TAP1 to infection with Mycobacterium tuberculosis. J Exp Med 1999; 189: 1973-80.
68. Turner J, D'Souza CD, Pearl JE, et al. CD8- and CD95/95L-dependent mechanisms of resistance in mice with chronic pulmonary tuberculosis. Am J Respir Cell Mol Biol 2001; 24: 203-09.
69. Mogues T, Goodrich ME, Ryan L, LaCourse R, North RJ. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J Exp Med 2001; 193: 271-80.
70. Lazarevic V, Flynn J. CD8(+) T cells in tuberculosis. Am J Respir Crit Care Med 2002; 166: 1116-21.
71. Laochumroonvorapong P, Wang J, Hu CC, et al. Perforin, a cytotoxic molecule which mediates cell necrosis, is not required for the early control of mycobacterial infection in mice. Infect Immun 1997; 65: 127-32.
72. Cooper AM, D'Souza C, Frank AA, Orme IM. The course of Mycobacterium tuberculosis infection in the lungs of mice lacking expression of either perforinor granzyme-mediated cytolytic mechanisms. Infect Immun 1997; 65: 1317-20.
73. Lewinsohn DM, Zhu L, Madison VJ, et al. Classically restricted human CD8+ T lymphocytes derived from Mycobacterium tuberculosis-infected cells: definition of antigen specificity. J Immunol 2001; 166: 439-46.
74. Lalvani A, Brookes R, Wilkinson R, et al. Human cytolytic and interferon gamma-secreting CD8+ T lymphocytes specific for Mycobacterium tuberculosis. Proc Natl Acad Sci USA 1998; 95: 270-75.
75. Chan J, Fan XD, Hunter SW, Brennan PJ, Bloom BR. Lipoarabinomannan, a possible virulence factor involved in persistence of Mycobacterium tuberculosis within macrophages. Infect Immun 1991; 59: 1755-61.
76. Gercken J, Pryjma J, Ernst M, Flad HD. Defective antigen presentation by Mycobacterium tuberculosis-infected monocytes. Infect Immun 1994; 62: 3472-78.
77. Wadee AA, Kuschke RH, Dooms TG. The inhibitory effects of Mycobacterium tuberculosis on MHC class II expression by monocytes activated with riminophenazines and phagocyte stimulants. Clin Exp Immunol 1995; 100: 434-39.
78. Hmama Z, Gabathuler R, Jefferies WA, Dejong G, Reiner NE. Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J Immunol 1998; 161: 4882-93.
79. Wojciechowski W, DeSanctis J, Skamene E, Radzioch D. Attenuation of MHC class II expression in macrophages infected with Mycobacterium bovis bacillus Calmette-Guerin involves class II transactivator and depends on the Nramp1 gene. J Immunol 1999; 163: 2688-96.
80. Noss EH, Pai RK, Sellati TJ, et al. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol 2001; 167: 910-18.
81. Ramachandra L, Noss E, Boom WH, Harding CV. Processing of Mycobacterium tuberculosis antigen 85B involves intraphagosomal formation of peptide-major histocompatibility complex II complexes and is inhibited by live bacilli that decrease phagosome maturation. J Exp Med 2001; 194: 1421-32.
82. Ting LM, Kim AC, Cattamanchi A, Ernst JD. Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J Immunol 1999; 163: 3898-906.
83. Pancholi P, Mirza A, Schauf V, Steinman RM, Bhardwaj N. Presentation of mycobacterial antigens by human dendritic cells: lack of transfer from infected macrophages. Infect Immun 1993; 61: 5326-32.
84. Thoma-Uszynski S, Stenger S, Takeuchi O, et al. Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 2001; 291: 1544-47.
85. Underhill DM, Ozinsky A, Hajjar AM, et al. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature. 1999; 401: 811-15.
86. Chan J, Xing Y, Magliozzo R, Bloom BR. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J Exp Med 1992; 175: 1111-22.
87. Denis M. Interferon-gamma-treated murine macrophages inhibit growth of tubercule bacilli via the generation of reactive nitrogen intermediates. Cell Immunol 1991; 132: 150-57.
88. Chan J, Tanaka K, Carroll D, Flynn JL, Bloom BR. Effect of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect Immun 1995; 63: 736-40.
89. Flynn JL, Scanga CA, Tanaka KE, Chan J. Effects of aminoguanidine on latent murine tuberculosis. J Immunol 1998; 160: 1796-803.
90. Nathan C. Inducible nitric oxide synthase in the tuberculous human lung. Am J Respir Crit Care Med 2002; 166: 130-31.
91. Rockett KA, Brookes R, Udalova I, Vidal V, Hill AV, Kwiatkowski D. 1,25-dihydroxyvitamin D3 induces nitric oxide synthase and suppresses growth of Mycobacterium tuberculosis in a human macrophage-like cell line. Infect Immun 1998; 66: 5314-21.
92. Bellamy R, Ruwende C, Corrah T, et al. Tuberculosis and chronic hepatitis B virus infection in Africans and variation in the vitamin D receptor gene. J Infect Dis 1999; 179: 721-24.
93. Rich EA, Torres M, Sada E, Finegan CK, Hamilton BD, Toossi Z. Mycobacterium tuberculosis (MTB)-stimulated production of nitric oxide by human alveolar macrophages and relationship of nitric oxide production to growth inhibition of MTB. Tubercle Lung Dis 1997; 78: 247-55.
94. Nozaki Y, Hasegawa Y, Ichiyama S, Nakashima I, Shimokata K. Mechanism of nitric oxide-dependent killing of Mycobacterium bovis BCG in human alveolar macrophages. Infect Immun 1997; 65: 3644-47.
95. Nicholson S, Bonecini-Almeida Mda G, Lapa e Silva JR, et al. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J Exp Med 1996; 183: 2293-302.
96. Wang CH, Liu CY, Lin HC, Yu CT, Chung KF, Kuo HP. Increased exhaled nitric oxide in active pulmonary tuberculosis due to inducible NO synthase upregulation in alveolar macrophages. Eur Respir J 1998; 11: 809-15.
97. Choi HS, Rai PR, Chu HW, Cool C, Chan ED. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis, [comment]. Am J Respir Crit Care Med 2002; 166: 178-86.
98. Ehrt S, Shiloh MU, Ruan J, et al. A novel antioxidant gene from Mycobacterium tuberculosis. J Exp Med 1997; 186: 1885-96.
99. Ruan J, St John G, Ehrt S, Riley L, Nathan C. noxR3, a novel gene from Mycobacterium tuberculosis, protects Salmonella typhimurium from nitrosative and oxidative stress. Infect Immun 1999; 67: 3276-83.
100. Cole ST, Brosch R, Parkhill J, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998; 393: 537-44.
101. Chen L, Xie QW, Nathan C. Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates. Mol Cell 1998; 1: 795-805.
102. Jacobson FS, Morgan RW, Christman MF, Ames BN. An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage: purification and properties. J Biol Chem 1989; 264: 1488-96.
103. Storz G, Christman MF, Sies H, Ames BN. Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc Natl Acad Sci USA 1987; 84: 8917-21.
104. Tartaglia LA, Storz G, Brodsky MH, Lai A, Ames BN. Alkyl hydroperoxide reductase from Salmonella typhimurium: sequence and homology to thioredoxin reductase and other flavoprotein disulfide oxidoreductases. J Biol Chem 1990; 265: 10535-40.
105. Storz G, Jacobson FS, Tartaglia LA, Morgan RW, Silveira LA, Ames BN. An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: genetic characterization and cloning of ahp. J Bacteriol 1989; 171: 2049-55.
106. Bryk R, Griffin P, Nathan C. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 2000; 407: 211-15.
107. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996; 271: C1424-37.
108. Yu K, Mitchell C, Xing Y, Magliozzo RS, Bloom BR, Chan J. Toxicity of nitrogen oxides and related oxidants on mycobacteria: M tuberculosis is resistant to peroxynitrite anion. Tuberc Lung Dis 1999; 79: 191-98.
109. St John G, Brot N, Ruan J, et al. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc Natl Acad Sci USA 2001; 98: 9901-06.
110. Moskovitz J, Berlett BS, Poston JM, Stadtman ER. The yeast peptide-methionine sulfoxide reductase functions as an antioxidant in vivo. Proc Natl Acad Sci USA 1997; 94: 9585-99.
111. Moskovitz J, Rahman MA, Strassman J, et al. Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage. J Bacteriol 1995; 177: 502-07.
112. Ouellet H, Ouellet Y, Richard C, et al. Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proc Natl Acad Sci USA 2002; 99: 5902-07.
113. Master SS, Springer B, Sander P, Boettger EC, Deretic V, Timmins GS. Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. Microbiology. 2002; 148: 3139-44.
114. Springer B, Master S, Sander P, et al. Silencing of oxidative stress response in Mycobacterium tuberculosis: expression patterns of ahpC in virulent and avirulent strains and effect of ahpC inactivation. Infect Immun 2001; 69: 5967-73.
115. Desjardins M Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol 1995; 5: 183-86.
116. Desjardins M, Huber LA, Parton RG, Griffiths G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 1994; 124: 677-88.
117. Vieira OV, Botelho RJ, Grinstein S. Phagosome maturation: aging gracefully. Biochem J 2002; 366: 689-704.
118. Armstrong J, D'Arcy Hart P. Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes. J Exp Med 1971; 134: 713-40.
119. Hart PD, Armstrong JA, Brown CA, Draper P. Ultrastructural study of the behavior of macrophages toward parasitic mycobacteria. Infect Immun 1972; 5: 803-07.
120. Crowle AJ, Dahl R, Ross E, May MH. Evidence that vesicles containing living, virulent Mycobacterium tuberculosis or Mycobacterium avium in cultured human macrophages are not acidic. Infect Immun 1991; 59: 1823-31.
121. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, et al. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase.[erratum appears in Science 1994; 263: 1359]. Science 1994; 263: 678-81.
122. Sturgill-Koszycki S, Schaible UE, Russell DG. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 1996; 15: 6960-68.
123. Russell DG, Dant J, Sturgill-Koszycki S. Mycobacterium avium- and Mycobacterium tuberculosis-containing vacuoles are dynamic, fusion-competent vesicles that are accessible to glycosphingolipids from the host cell plasmalemma. J Immunol 1996; 156: 4764-73.
124. de Chastellier C, Lang T, Thilo L. Phagocytic processing of the macrophage endoparasite, Mycobacterium avium, in comparison to phagosomes which contain Bacillus subtilis or latex beads. Eur J Cell Biol 1995; 68: 167-82.
125. Clemens DL, Horwitz MA. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 1996; 184: 1349-55.
126. Waters MG, Pfeffer SR. Membrane tethering in intracellular transport. Curr Opin Cell Biol 1999; 11: 453-39.
127. Pelham HR. SNAREs and the specificity of membrane fusion. Trends Cell Biol 2001; 11: 99-101.
128. Hay JC. SNARE complex structure and function. Exp Cell Res 2001; 271: 10-21.
129. Via LE, Deretic D, Ulmer RJ, Hibler NS, Huber LA, Deretic V. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 1997; 272: 13326-31.
130. Clemens DL, Lee BY, Horwitz MA. Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal late. Infect Immun 2000; 68: 2671-84.
131. Clemens DL, Lee BY, Horwitz MA. Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect Immun 2000; 68: 5154-66.
132. Fratti RA, Backer JM, Gruenberg J, Corvera S, Deretic V. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 2001; 154: 631-44.
133. Christoforidis S, Miaczynska M, Ashman K, et al. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1999; 1: 249-52.
134. Fratti RA, Chua J, Vergne I, Deretic V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA 2003 (in press).
135. Beatty WL, Rhoades ER, Ullrich HJ, Chatterjee D, Heuser JE, Russell DG. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 2000; 1: 235-47.
136. Frehel C, de Chastellier C, Lang T, Rastogi N. Evidence for inhibition of fusion of lysosomal and prelysosomal compartments with phagosomes in macrophages infected with pathogenic Mycobacterium avium. Infect Immun 1986; 52: 252-62.
137. Schaible U, Sturgill-Koszycki S, Schlesinger PH, Russell DG. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J Immunol 1998; 160: 1290-96.
138. Armstrong J, D'Arcy Hart P. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli: reversal of the usual nonfusion pattern and observations on bacterial survival. J Exp Med 1975; 142: 1-16.
139. Ferrari G, Langen H, Naito M, Pieters JA. Coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 1999; 97: 435-47.
140. de Hostos EL. The coronin family of actin-associated proteins. Trends Cell Biol 1999; 9: 345-50.
141. Schuller S, Neefjes J, Ottenhoff T, Thole J, Young D. Coronin is involved in uptake of Mycobacterium bovis BCG in human macrophages but not in phagosome maintenance. Cell Microbiol 2001; 3: 785-93.
142. Hoal-van Helden EG, Hon D, Lewis LA, Beyers N, van Helden PD. Mycobacterial growth in human macrophages: variation according to donor, inoculum and bacterial strain. Cell Biol Int 2001; 25: 71-81.
143. Solomon JM, Leung GS, Isberg RR. Intracellular replication of Mycobacterium marinum within Dictyostelium discoideum: efficient replication in the absence of host coronin. Infect Immun 2003; 71: 3578-86.
144. Ramakrishnan L, Valdivia RH, McKerrow JH, Falkow S. Mycobacterium marinum causes both long-term subclinical infection and acute disease in the leopard frog (Rana pipiens). Infect Immun 1997; 65: 767-73.
145. Maniak M, Rauchenberger R, Albrecht R, Murphy J, Gerisch G. Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell 1995; 83: 915-24.
146. Bean AGD, Roach DR, Briscoe H, et al. Structural deficiencies in granuloma formation in TNF gene-targeted mice underlie the heightened susceptibility to aerosol Mycobacterium tuberculosis infection, which is not compensated for by lymphotoxin. J Immunol 1999; 162: 3504-11.
147. Mohan VP, Scanga CA, Yu K, et al. Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect Immun 2001; 69: 1847-55.
148. Flynn JL, Goldstein MM, Chan J, et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 1995; 2: 561-72.
149. Adams LB, Mason CM, Kolls JK, Scollard D, Krahenbuhl JL, Nelson S. Exacerbation of acute and chronic murine tuberculosis by administration of a tumor necrosis factor receptor-expressing adenovirus. J Infect Dis 1995; 171: 400-05.
150. Tramontana JM, Utaipat U, Molloy A, et al. Thalidomide treatment reduces tumor necrosis factor alpha production and enhances weight gain in patients with pulmonary tuberculosis. Mol Med 1995; 1: 384-97.
151. Rook GA. Mycobacteria, cytokines and antibiotics. Pathol Biol 1990; 38: 276-80.
152. Moreira AL, Tsenova-Berkova L, Wang J, et al. Effect of cytokine modulation by thalidomide on the granulomatous response in murine tuberculosis. Tuberc Lung Dis 1997; 78: 47-55.
153. Bekker LG, Moreira AL, Bergtold A, Freeman S, Ryffel B, Kaplan G. Immunopathologic effects of tumor necrosis factor alpha in murine mycobacterial infection are dose dependent. Infect Immun 2000; 68: 6954-61.
154. Beutler B, Cerami A. Tumor necrosis, cachexia, shock, and inflammation: a common mediator. Annu Rev Biochem 1988; 57: 505-18.
155. Tracey KJ, Cerami A. Tumor necrosis factor in the malnutrition (cachexia) of infection and cancer. Am J Trop Med Hyg 1992; 47: 2-7.
156. Feldmann M, Maini RN. Anti-TNF therapy of rheumatoid arthritis: what have we learned? Annu Rev Immunol 2001; 19: 163-96.
157. Shanahan JC, St Clair W. Tumor necrosis factor-alpha blockade: a novel therapy for rheumatic disease. Clin Immunol 2002; 103: 231-42.
158. Gardam MA, Keystone EC, Menzies R, et al. Antitumour necrosis factor agents and tuberculosis risk: mechanisms of action and clinical management. Lancet Infect Dis 2003; 3: 148-55.
159. Long R, Gardam M Tumour necrosis factor-alpha inhibitors and the reactivation oflatent tuberculosis infection. CMAJ Can Med Assoc J 2003; 168: 1153-56.
160. Keane J, Gershon SK. Tuberculosis and treatment with infliximab. N Engl J Med 2002; 346: 625-26.
161. Diagnostic Standards and Classification of Tuberculosis in Adults and Children. Am J Respir Crit Care Med 2000; 161: 1376-95.
162. Keane J, Gershon S, Wise RP, et al. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 2001; 345: 1098-104.
163. Smith S, Liggitt D, Jeromsky E, Tan X, Skerrett SJ, Wilson CB. Local role for tumor necrosis factor alpha in the pulmonary inflammatory response to Mycobacterium tuberculosis infection. Infect Immun 2002; 70: 2082-89.
164. Lugering A, Schmidt M, Lugering N, Pauels HG, Domschke W, Kucharzik T. Infliximab induces apoptosis in monocytes from patients with chronic active Crohn's disease by using a caspase-dependent pathway. Gastroenterology 2001; 121: 1145-57.
165. ten Hove T, van Montfrans C, Peppelenbosch MP, van Deventer SJ. Infliximab treatment induces apoptosis of lamina propria T lymphocytes in Crohn's disease. Gut 2002; 50: 206-11.
166. Agnholt J, Kaltoft K. Infliximab downregulates interferon-gamma production in activated gut T-lymphocytes from patients with Crohn's disease. Cytokine 2001; 15: 212-22.
167. Keane J, Balcewicz-Sablinska MK, Remold HG, et al. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect Immun 1997; 65: 298-304.
168. Sedgwick JD, Riminton DS, Cyster JG, Korner H. Tumor necrosis factor: a master-regulator of leukocyte movement. Immunol Today 2000; 21: 110-13.
169. Murray PJ, Yang L, Onufryk C, Tepper RI, Young RA. T cell-derived IL-10 antagonizes macrophage function in mycobacteria infection. J Immunol 1997; 158: 315-21.
170. North RJ. Mice incapable of making IL-4 and IL-10 display normal resistance in infection with Mycobacterium tuberculosis. Clin Exp Immunol 1998; 113: 55-58.
171. Roach DR, Martin E, Bean AGD, Rennick DM, Briscoe H, Britton WJ. Endogenous inhbition of antimycobacterial immunity by IL-10 varies between mycobacterial species. Scand J Immunol 2001; 54: 163-70.
172. Turner J, Gonzalez-Juarrero M, Ellis DL, et al. In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. J Immunol 2002; 169: 6343-51.
173. Turner J, Gonzalez-Juarrero M, Saunders BM, et al. Immunological basis for reactivation of tuberculosis in mice. Infect Immun 2001; 69: 3264-70.
174. Demangel C, Bertolino P, Britton WJ. Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur J Immunol 2002; 32: 994-1002.
175. D'Amico G, Frascaroli G, Bianchi G, et al. Uncoupling of inflammatory chemokine receptors by IL-10: generation of functional decoys. Nat Immunol 2000; 1: 387-91.
176. Hickman SP, Chan J, Salgame P. Mycobacterium tuberculosis induces differential cytokine production from dendritic cells and macrophages with divergent effects on naive T cell polarization. J Immunol 2002; 168: 4636-42.