Tuberculosis: A problem with persistence

Nature Reviews Microbiology

Volumn 1, Issue 2, 2003, Pages 97-105

  Stewart, Graham R ^a   Robertson, Brian D ^a   Young, Douglas B ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; C57BL MOUSE; DISEASE MODEL; GUINEA PIG; HUMAN; IMMUNOLOGY; LUNG; LUNG TUBERCULOSIS; LYMPH NODE; MICROBIOLOGY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; PHYSIOLOGY; REVIEW; TIME;

ANIMALS; DISEASE MODELS, ANIMAL; GUINEA PIGS; HUMANS; LUNG; LYMPH NODES; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; TIME FACTORS; TUBERCULOSIS, PULMONARY;

EID: 1842561506     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro749     Document Type: Article

References (105)

1. Dye, C., Scheele, S., Dolin, P., Pathania, V & Raviglione, M. C. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 282, 677-686 (1999).
2. Bloom, B. R. & Murray, C. J. Tuberculosis: commentary on a reemergent killer. Science 257, 1055-1064 (1992).
3. Selwyn, P. A. et al. A prospective study of the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. N. Engl. J. Med. 320, 545-550 (1989).
4. Russell, D. G. Mycobacterium tuberculosis: here today, and here tomorrow. Nature Rev. Mol. Cell Biol. 2, 569-577 (2001).
5. Via, L. E. et al. Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897-905 (1998).
6. Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P H. & Russell, D. G. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160, 1290-1296 (1998).
7. Kaufmann, S. H. How can immunology contribute to the control of tuberculosis? Nature Rev. Immunol. 1, 20-30 (2001).
8. Ewer, K. et al. Comparison of T-cell-based assay with tuberculin skin test for diagnosis of Mycobacterium tuberculosis infection in a school tuberculosis outbreak. Lancet 361, 1168-1173 (2003).
9. Mazurek, G. H. et al. Comparison of a whole-blood interferon y assay with tuberculin skin testing for detecting latent Mycobacterium tuberculosis infection. JAMA 286, 1740-1747 (2001).
10. Stead, W. W. 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. 95, 729-745 (1967).
11. Powell, K. E. & Farer, L. S. The rising age of the tuberculosis patient: a sign of success and failure. J. Infect Dis. 142, 946-948 (1980).
12. Comstock, G. W., Baum, C. & Snider, D. E. Jr. Isoniazid prophylaxis among Alaskan Eskimos: a final report of the bethel isoniazid studies. Am. Rev. Respir. Dis. 119, 827-830 (1979).
13. Lillebaek, T. et al. Molecular evidence of endogenous reactivation of Mycobacterium tuberculosis after 33 years of latent infection. J. Infect. Dis. 185, 401-404 (2002).
14. Small, P M. et al. The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N. Engl. J. Med. 330, 1703-1709 (1994).
15. Maguire, H. et al. Molecular epidemiology of tuberculosis in London 1995-7 showing low rate of active transmission. Thorax 57, 617-622 (2002).
16. Opie, E. L. & Aronson, J. D. Tubercle bacilli in latent tuberculous lesions and in lung tissue without tuberculous lesions. Arch. Pathol. 4, 1-21 (1927).
17. Griffith, A. S. Types of tubercle bacilli in human tuberculosis. J. Pathol. Bacterid. 32, 813-840 (1929).
18. Feldman, W. H. & Bagenstoss, A. H. The residual infectivity of the primary complex of tuberculosis. Am. J. Pathol. 14, 473-490 (1938).
19. Robertson, H. E. The persistence of tuberculous infections. Am. J. Pathol. 9, S711-S719 (1933).
20. Vandiviere, H. M., Loring, W. E., Melvin, I. & Willis, S. The treated pulmonary lesion and its tubercle bacillus. II. The death and resurrection. Am. J. Med. Sci. 232, 30-37 (1956).
21. Loomis, H. P. Some facts in the etiology of tuberculosis. evidenced by thirty autopsies and experiments upon animals. Medical Record 38, 689-698 (1890).
22. Pizzini, D. L. Tuberkelbacillen in den Lymphdrusen Nichttuberkuloser. Ztschr. f. Klin. Med. 21, 329-343 (1892).
23. Kalble, J. Untersuchungen uber den Keimgehalt normaler Bronchiallymphdrusen. Munchen med. Wchnschr. 46, 622-625 (1899).
24. Balasubramanian, V, Wiegeshaus, E. H., Taylor, B. T. & Smith, D. W. Pathogenesis of tuberculosis: pathway to apical localization. Tuber. Lung Dis. 75, 168-178 (1994).
25. Feldman, W. H. & Bagenstoss, A. H. The occurrence of virulent tubercle bacteria in presumably non-tuberculous lung tissue. Am. J. Pathol. 5, 501-515 (1939).
26. Hernandez-Pando, R. et al. Persistence of DNA from Mycobacterium tuberculosis in superficially normal lung tissue during latent infection. Lancet 356, 2133-2138 (2000).
27. Rhoades, E. R., Frank, A. A. & Orme, I. M. Progression of chronic pulmonary tuberculosis in mice aerogenically infected with virulent Mycobacterium tuberculosis. Tuber. Lung Dis. 78, 57-66 (1997).
28. McCune, R. M., Feldman, F. M., Lambert, H. P & McDermott, W. Microbial persistence. I. The capacity of tubercle bacilli to survive sterilization in mouse tissues. J. Exp. Med. 123, 445-468 (1966).
29. Mitchison, D. A. Treatment of tuberculosis. The Mitchell lecture 1979. J. R. Coll. Physicians Lond. 14, 98-99 (1980).
30. McMurray, D. N. Disease model: pulmonary tuberculosis. Trends Mol. Med. 7, 135-137 (2001).
31. Ho, R. S., Fok, J. S., Harding, G. E. & Smith, D. W Host-parasite relationships in experimental airborne tuberculosis. VII. Fate of Mycobacterium tuberculosis in primary lung lesions and in primary lesion-free lung tissue infected as a result of bacillemia. J. Infect Dis. 138, 237-241 (1978).
32. Smith, D. W., Balasubramanian, V & Wiegeshaus, E. A guinea pig model of experimental airborne tuberculosis for evaluation of the response to chemotherapy: the effect on bacilli in the initial phase of treatment. Tubercle 72, 223-231 (1991).
33. Dannenberg, A. M. J. in Tuberculosis: Pathogenesis, Protection and Control (ed. Bloom, B. R.) 149-156 (American Society for Microbiology, Washington DC, 1994).
34. Walsh, G. P. et al. The Philippine cynomolgus monkey (Macaca fasicularis) provides a new non-human primate model of tuberculosis that resembles human disease. Nature Med. 2, 430-436 (1996).
35. Flynn, J. L. et al. Non-human primates: a model for tuberculosis research. Tuberculosis 83, 116-118 (2003).
36. Much, H. Uber die granulare, nach Ziel nicht darstellbare Form des Tuberkulosevirus. Beitrage Klinische Tuberkulose 8, 85 (1907).
37. Much, H. Die nach Ziehl nicht darstellbaren Formen des Tuberkelbacillus. Berl. Klin. Wochenschr. 45. 691-694 (1908).
38. Calmette, A. & Valtis, J. Virulent filterable elements of the tubercle bacillus. Ann. Med. 19, 553-560 (1926).
39. Khomenko, A. G. The variability of Mycobacterium tuberculosis in patients with cavitary pulmonary tuberculosis in the course of chemotherapy. Tubercle68, 243-253 (1987).
40. Cole, S. T et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544 (1998).
41. Rees, R. J. W. & D'Arcy Hart, P. Analysis of the host-parasite equilibrium in chronic murine tuberculosis by total and viable bacillary counts. Br. J. Exp. Pathol. 42, 83-88 (1960).
42. Wallace, J. G. The heat resistance of tubercle bacilli in the lungs of infected mice. Am. Rev. Respir. Dis. 83, 866-871 (1961).
43. Wayne, L. G. & Sohaskey, C. D. Nonreplicating persistence of Mycobacterium tuberculosis. Annu. Rev. Microbiol. 55, 139-163 (2001).
44. Wayne, L. G. & Lin, K. Y Glyoxylate metabolism and adaptation of Mycobacterium tuberculosis to survival under anaerobic conditions. Infect. Immun. 37, 1042-1049 (1982).
45. McKinney, J. D. et al. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406, 735-738 (2000).
46. Sherman, D. R. etal. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding a-crystallin. Proc. Natl Acad. Sci. USA 98, 7534-7539 (2001).
47. Park, H. D. et al. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol. Microbiol. 48, 833-843 (2003).
48. Yuan, Y, Crane, D. D. & Barry, C. E. III. Stationary phase- associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial α-crystallin homologue. J. Bacteriol 178, 4484-4492 (1996).
49. Shi, L., Jung, Y. J., Tyagi, S., Gennaro, M. L. & North, R. J. Expression of Th1-mediated immunity in mouse lungs induces a Mycobacterium tuberculosis transcription pattern characteristic of nonreplicating persistence. Proc. Natl Acad. Sci. USA 100, 241-246 (2003).
50. Voskuil, M. I. et al. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198, 705-713 (2003).
51. Cramer, T & Johnson, R. S. A novel role for the hypoxia inducible transcription factor HIF-1 a: critical regulation of inflammatory cell function. Cell Cycle 2, 192-193 (2003).
52. Mukamolova, G. V, Kaprelyants, A. S., Young, D. I., Young, M. & Kell, D. B. A bacterial cytokine. Proc. Natl Acad. Sci. USA 95, 8916-8921 (1998).
53. Steyn, A. J. et al. Mycobacterium tuberculosis WhiB3 interacts with RpoV to affect host survival but is dispensable for in vivo growth. Proc. Natl Acad. Sci. USA 99, 3147-3152 (2002).
54. Zahrt, T. C. & Deretic, V. Mycobacterium tuberculosis signal transduction system required for persistent infections. Proc. Natl Acad. Sci. USA 98, 12706-12711 (2001).
55. Glickman, M. S., Cox, J. S. & Jacobs, W. R. Jr. A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol. Cell 5, 717-727 (2000).
56. Ramakrishnan, L., Federspiel, N. A. & Falkow, S. Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288, 1436-1439 (2000).
57. Stewart, G. R. et al. Overexpression of heat-shock proteins reduces survival of Mycobacterium tuberculosis in the chronic phase of infection. Nature Med. 7, 732-737 (2001).
58. Kaushal, D. et al. Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proc. Natl Acad. Sci. USA 99, 8330-8335 (2002).
59. Parish, T. et al. Deletion of two-component regulatory systems increases the virulence of Mycobacterium tuberculosis. Infect. Immun. 71, 1134-1140 (2003).
60. Flynn, J. L. & Chan, J. Immunology of tuberculosis. Annu. Rev. Immunol. 19, 93-129 (2001).
61. Casanova, J. L. & Abel, L. Genetic dissection of immunity to mycobacteria: the human model. Annu. Rev. Immunol. 20, 581-620 (2002).
62. Ting, L. M., Kim, A. C., Cattamanchi, A. & Ernst, J. D. Mycobacterium tuberculosis inhibits IFN-y transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163, 3898-3906 (1999).
63. + regulatory T cells control Leishmania major persistence and immunity. Nature 420, 502-507 (2002).
64. Sakaguchi, S. Regulatory T cells: mediating compromises between host and parasite. Nature Immunol. 4, 10-11 (2003).
65. Caruso, A. M. et al. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-y, yet succumb to tuberculosis. J. Immunol. 162, 5407-5416 (1999).
66. van Pinxteren, L. A., Cassidy, J. P., Smedegaard, B. H., Agger, E. M. & Andersen, P. Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur. J. Immunol. 30, 3689-3698 (2000).
67. + T cells causes reactivation of murine persistent tuberculosis despite continued expression of interferon y and nitric oxide synthase 2. J. Exp. Med. 192, 347-358 (2000).
68. Wong, P. & Pamer, E. G. CD8 T cell responses to infectious pathogens. Annu. Rev. Immunol. 21, 29-70 (2003).
69. + CTL from lungs of Mycobacterium tuberculosis- infected mice express perforin in vivo and lyse infected macrophages. J. Immunol. 165, 353-363 (2000).
70. Stenger, S. et al. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 282, 121-125 (1998).
71. Turner, J. et al. CD8- and CD95/95L-dependent mechanisms of resistance in mice with chronic pulmonary tuberculosis. Am. J. Respir. Cell Mol. Biol. 24, 203-209 (2001).
72. Turner, J. et al. In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. J. Immunol. 169, 6343-6351 (2002).
73. Mohan, V. P. et al. Effects of tumor necrosis factor aon host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect. Immun. 69, 1847-1855 (2001).
74. Keane, J. et al. Tuberculosis associated with infliximab, a tumor necrosis factor a-neutralizing agent. N. Engl. J. Med. 345, 1098-1104 (2001).
75. Winslow, G. M., Roberts, A. D., Blackman, M. A. & Woodland, D. L. Persistence and turnover of antigen- specific CD4 T cells during chronic tuberculosis infection in the mouse. J. Immunol. 170, 2046-2052 (2003).
76. Comstock, G. W., Livesay, V. T. & Woolpert, S. F. The prognosis of a positive tuberculin reaction in childhood and adolescence. Am. J. Epidemiol. 99, 131-138 (1974).
77. Underhill, D. M., Ozinsky, A., Smith, K D. & Aderem, A. Tolllike receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl Acad. Sci. USA 96, 14459-14463 (1999).
78. Thoma-Uszynski, S. et al. Induction of direct antimicrobial activity through mammalian Toll-like receptors. Science 291, 1544-1547 (2001).
79. Noss, E. H. 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. 167, 910-918 (2001).
80. Lopez, M. et al. The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J. Immunol. 170, 2409-2416 (2003).
81. Geijtenbeek, T. B. et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17 (2003).
82. Tailleux, L. et al. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197, 121-127 (2003).
83. Manca, C. et al. 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-a/p. Proc. Natl Acad. Sci. USA 98, 5752-5757 (2001).
84. Dye, C., Watt, C. J. & Bleed, D. Low access to a highly effective therapy: a challenge for international tuberculosis control. Bull. World Health Organ. 80, 437-444 (2002).
85. Stewart, G. R. & Young, D. B. Tuberculosis vaccines. Brit. Med. Bull. 62, 73-86 (2002).
86. Lalvani, A. et al. Enhanced contact tracing and spatial tracking of Mycobacterium tuberculosis infection by enumeration of antigen-specific T cells. Lancet357, 2017-2021 (2001).
87. American-Thoracic Society. Targeted tuberculin testing and treatment of latent tuberculosis infection. Am. J. Respir. Crit. Care Med. 161, S221-S247 (2000).
88. Hmama, Z., Gabathuler, R., Jefferies, W. A., de Jong, G. & Reiner, N. E. Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J. Immunol. 161, 4882-4893 (1998).
89. Noss, E. H., Harding, C. V. & Boom, W. H. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell. Immunol. 201, 63-74 (2000).
90. Global Alliance Tuberculosis. Scientific blueprint for tuberculosis drug development. Tuberculosis 81, 1-52 (2001).
91. Lowrie, D. B. et al. Therapy of tuberculosis in mice by DNA vaccination. Nature 400, 269-271 (1999).
92. Bonato, V L., Lima, V. M., Tascon, R. E., Lowrie, D. B. & Silva, C. L. Identification and characterization of protective T cells in hsp65 DNA-vaccinated and Mycobacterium tuberculosis-infected mice. Infect. Immun. 66, 169-175 (1998).
93. Turner, O. C. et al. Lack of protection in mice and necrotizing bronchointerstitial pneumonia with bronchiolitis in guinea pigs immunized with vaccines directed against the hsp60 molecule of Mycobacterium tuberculosis. Infect. Immun. 68, 3674-3679 (2000).
94. Taylor, J. L. et al. Pulmonary necrosis resulting from DNA vaccination against tuberculosis. Infect. Immun. 71, 2192-2198 (2003).
95. Li, Z., Kelley, C., Collins, F., Rouse, D. & Morris, S. Expression of katG in Mycobacterium tuberculosis is associated with its growth and persistence in mice and guinea pigs. J. infect. Dis. 177, 1030-1035 (1998).
96. Fritz, C., Maass, S., Kreft, A. & Bange, F. C. Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue specific. Infect. Immun. 70, 286-291 (2002).
97. Murphy, H. N. et al. Trehalose metabolism in mycobacteria. Keystone Symposium, Taos (2003).
98. Chen, P, Ruiz, R. E., Li, Q., Silver, R. F & Bishai, W. R. Construction and characterization of a Mycobacterium tuberculosis mutant lacking the alternate sigma factor gene, sigF. Infect. Immun. 68, 5575-5580 (2000).
99. Barry, C. E. III. Mycobacterial lipids and lipid metabolism. Keystone Symposium, Taos (2003).
100. Kaplan, G. The role of Mycobacterium tuberculosis lipids in immunity and virulence of clinical isolates. Keystone Symposium, Taos (2003).
101. Primm, T P. et al. The stringent response of Mycobacterium tuberculosis is required for long-term survival. J. Bacteriol. 182, 4889-4898 (2000).
102. Hutter, B. & Dick, T Up-regulation of narX, encoding a putative 'fused nitrate reductase' in anaerobic dormant Mycobacterium bovis BCG. FEMS Microbiol. Lett. 178, 63-69 (1999).
103. Fenhalls, G. et al. In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infect. Immun. 70, 6330-6338 (2002).
104. Hutter, B. & Dick, T. Analysis of the dormancy-inducible narK2 promoter in Mycobacterium bovis BCG. FEMS Microbiol. Lett. 188, 141-146 (2000).
105. Chan, K. et al. Complex pattern of Mycobacterium marinum gene expression during long-term granulomatous infection. Proc. Natl Acad. Sci. USA 99, 3920-3925 (2002).