Who puts the tubercle in tuberculosis?

Nature Reviews Microbiology

Volumn 5, Issue 1, 2007, Pages 39-47

  Russell, David G ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; GAMMA INTERFERON; LIPID; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANTIGEN DETECTION; BACTERIAL SURVIVAL; BACTERIAL TRANSMISSION; BACTERIUM CULTURE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; DISEASE COURSE; GENETIC SCREENING; HISTOPATHOLOGY; HISTORY OF MEDICINE; HUMAN; IMMUNE SYSTEM; LIPID ANALYSIS; LUNG GRANULOMA; MACROPHAGE; MORTALITY; MYCOBACTERIUM TUBERCULOSIS; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PHAGOCYTE; PREVALENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RESPIRATORY SYSTEM; REVIEW; TUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; CELL WALL; DISEASE PROGRESSION; GRANULOMA; HUMANS; LIPID METABOLISM; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

BACILLI (CLASS); BACILLUS (BACTERIUM); CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS;

EID: 33845683474     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1538     Document Type: Review

References (94)

1. Corbett, E. L. et al. The growing burden of tuberculosis: Global trends and interactions with the HIV epidemic. Arch. Intern. Med. 163, 1009-1021 (2003).
2. Frieden, T. R., Sterling, T. R., Munsiff, S. S., Watt, C. J. & Dye, C. Tuberculosis. Lancet 362, 887-899 (2003).
3. Harries, A. D. & Dye, C. Tuberculosis. Ann. Trop. Med. Parasitol. 100, 415-431 (2006).
4. Dye, C. Global epidemiology of tuberculosis. Lancet 367, 938-940 (2006).
5. Sreevatsan, S. et al. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc. Natl Acad. Sci. USA 94, 9869-9874 (1997).
6. Diamond, J. Guns, Germs and Steel, (W. W. Norton & Company, New York, 1997).
7. Casanova, J. L. & Abel, L. Genetic dissection of immunity to mycobacteria: The human model. Annu. Rev. Immunol. 20, 581-620 (2002).
8. Cooke, G. S. & Hill, A. V. Genetics of susceptibility to human infectious disease. Nature Rev. Genet. 2, 967-977 (2001).
9. Fulton, S. A. et al. Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19-kilodalton mycobacterial lipoprotein. Infect. Immun. 72, 2101-2110 (2004).
10. Baghdadi, J. E. et al. An autosomal dominant major gene confers predisposition to pulmonary tuberculosis in adults. J. Exp. Med. 203, 1679-1684 (2006).
11. Malik, S. et al. Variants of the SFTPA1 and SFTPA2 genes and susceptibility to tuberculosis in Ethiopia. Hum. Genet. 118, 752-759 (2006).
12. Bornman, L. et al. Vitamin D receptor polymorphisms and susceptibility to tuberculosis in West Africa: A case-control and family study. J. Infect. Dis. 190, 1631-1641 (2004).
13. Cervino, A. C. et al. Fine mapping of a putative tuberculosis-susceptibility locus on chromosome 15q 11-13 in African families. Hum. Mol. Genet. 11, 1599-1603 (2002).
14. Brosch, R. et al. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl Acad. Sci. USA 99, 3684-3689 (2002).
15. Gutierrez, M. C. et al. Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog. 1, e5 (2005).
16. Mostowy, S., Cousins, D., Brinkman, J., Aranaz, A. & Behr, M. A. Genomic deletions suggest a phylogeny for the Mycobacterium tuberculosis complex. J. Infect. Dis. 186, 74-80 (2002).
17. Mostowy, S. & Behr, M. A. The origin and evolution of Mycobacterium tuberculosis. Clin. Chest. Med. 26, 207-216 (2005).
18. Ulrichs, T. & Kaufmann, S. H. New insights into the function of granulomas in human tuberculosis. J. Pathol. 208, 261-269 (2006).
19. Flynn, J. L. & Chan, J. What's good for the host is good for the bug. Trends Microbiol. 13, 98-102 (2005).
20. Algood, H. M., Lin, P. L. & Flynn, J. L. Tumor necrosis factor and chemokine interactions in the formation and maintenance of granulomas in tuberculosis. Clin. Infect. Dis. 41 (Suppl. 3), 189-193 (2005).
21. Algood, H. M., Chan, J. & Flynn, J. L. Chemokines and tuberculosis. Cytokine Growth Factor Rev. 14, 467-477 (2003).
22. Ulrichs, T et al. Differential organization of the local immune response in patients with active cavitary tuberculosis or with nonprogressive tuberculoma. J. Infect. Dis. 192, 89-97 (2005).
23. Fenhalls, G. et al. Distribution of IFN-γ, IL-4 and TNF-α protein and CD8 T cells producing IL-12p40 mRNA in human lung tuberculous granulomas. Immunology 105, 325-335 (2002).
24. Tully, G. et al. Highly focused T cell responses in latent human pulmonary Mycobacterium tuberculosis infection. J. Immunol. 174, 2174-2184 (2005).
25. Kaplan, G. et al. Mycobacterium tuberculosis growth at the cavity surface: A microenvironment with failed immunity. Infect. Immun. 71, 7099-7108 (2003).
26. Dheda, K. et al. Lung remodeling in pulmonary tuberculosis. J. Infect. Dis. 192, 1201-1209 (2005).
27. Lin, P. L. et al. Early events in Mycobacterium tuberculosis infection in cynomolgus macaques. Infect. Immun. 74, 3790-3803 (2006).
28. Alatas, F. et al. Vascular endothelial growth factor levels in active pulmonary tuberculosis. Chest 125, 2156-2159 (2004).
29. Ragno, S. et al. Changes in gene expression in macrophages infected with Mycobacterium tuberculosis: A combined transcriptomic and proteomic approach. Immunology 104, 99-108 (2001).
30. Tsai, M. C. et al. Characterization of the tuberculous granuloma in murine and human lungs: Cellular composition and relative tissue oxygen tension. Cell. Microbiol. 8, 218-232 (2006).
31. 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).
32. 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).
33. Deretic, V. et al. Mycobacterium tuberculosis inhibition of phagolysosome biogenesis and autophagy as a host defence mechanism. Cell. Microbiol. 8, 719-727 (2006).
34. Russell, D. G. Mycobacterium tuberculosis: Here today, and here tomorrow. Nature Rev. Mol. Cell Biol. 2, 569-577 (2001).
35. Russell, D. G., Purdy, G. E., Owens, R. M., Rohde, K. & Yates, R. M. Mycobacterium tuberculosis and the concept of the '4 minute' phagosome. ASM News 71, 459-463 (2005).
36. Sturgill-Koszycki, S., Schaible, U. E. & Russell, D. G. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J. 15, 6960-6968 (1996).
37. Russell, D. G., 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. 156, 4764-4773 (1996).
38. Mwandumba, H. C. et al. Mycobacterium tuberculosis resides in nonacidified vacuoles in endocytically competent alveolar macrophages from patients with tuberculosis and HIV infection. J. Immunol. 172, 4592-4598 (2004).
39. Pethe, K. et al. Isolation of Mycobacterium tuberculosis mutants defective in the arrest of phagosome maturation. Proc. Natl Acad. Sci. USA 101, 13642-13647 (2004).
40. MacMicking, J. D., Taylor, G. A. & McKinney, J. D. Immune control of tuberculosis by IFN-γ-inducible LRG-47. Science 302, 654-659 (2003 ).
41. 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).
42. Via, L. E. et al. Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897-905 (1998).
43. Munoz-Elias, E. J. et al. Replication dynamics of Mycobacterium tuberculosis in chronically infected mice. Infect. Immun. 73, 546-551 (2005).
44. Rees, R. J. & Hart, P. D. Analysis of the host-parasite equilibrium in chronic murine tuberculosis by total and viable bacillary counts. Br. J. Exp. Pathol. 42, 83-88 (1961).
45. Ribi, E. et al. Induction of resistance to tuberculosis in mice with defined components of mycobacteria and with some unrelated materials. Immunology 46, 297-305 (1982).
46. Hamamoto, Y., Kobara, Y., Kojima, A., Kumazawa, Y. & Yasuhira, K. Experimental production of pulmonary granulomas. I. Immune granulomas induced by chemically modified cell walls and their constituents. Br. J. Exp. Pathol. 62, 259-269 (1981).
47. McLaughlin, C. A., Parker, R., Hadlow, W. J., Toubiana, R. & Ribi, E. Moieties of mycobacterial mycolates required for inducing granulomatous reactions. Cell. Immunol. 38, 14-24 (1978).
48. Yamamoto, K. & Karinuma, M. Genetic control of granuloma response to oil-associated BCG cell wall vaccine in mice. Microbiol. Immunol. 22, 335-348 (1978).
49. Granger, D. L., Yamamoto, K. I. & Ribi, E. Delayed hypersensitivity and granulomatous response after immunization with protein antigens associated with a mycobacterial glycolipid and oil droplets. J. Immunol. 116, 482-488 (1976).
50. Meyer, T J., Ribi, E. & Azuma, I. Biologically active components from mycobacterial cell walls. V. Granuloma formation in mouse lungs and guinea pig skin. Cell. Immunol. 16, 11-24 (1975).
51. Moore, V. L., Myrvik, Q. N. & Kato, M. Role of cord factor (trehalose-6, 6′-dimycolate) in allergic granuloma formation in rabbits. Infect. Immun. 6, 5-8 (1972).
52. Bekierkunst, A. et al. Granuloma formation induced in mice by chemically defined mycobacterial fractions. J. Bacteriol. 100, 95-102 (1969).
53. Bekierkunst, A. Acute granulomatous response produced in mice by trehalose-6, 6-dimycolate. J. Bacteriol. 96, 958-961 (1968).
54. White, R. G., Jolles, P., Samour, D. & Lederer, E. Correlation of adjuvant activity and chemical structure of wax D fractions of Mycobacteria. Immunology 7, 158-171 (1964).
55. Xu, S. et al. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 153, 2568-2578 (1994).
56. Beatty, W. L. et al. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1, 235-247 (2000).
57. Beatty, W. L., Ullrich, H. J. & Russell, D. G. Mycobacterial surface moieties are released from infected macrophages by a constitutive exocytic event. Eur. J. Cell Biol. 80, 31-40 (2001).
58. Schaible, U. E. et al. Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD 1 in tuberculosis. Nature Med. 9, 1039-1046 (2003).
59. Winau, F., Kaufmann, S. H. & Schaible, U. E. Apoptosis paves the detour path for CD 8 T cell activation against intracellular bacteria. Cell. Microbiol. 6, 599-607 (2004).
60. van den Elzen, P. et al. Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 437, 906-910 (2005).
61. Rhoades, E. et al. Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG. Mol. Microbiol. 48, 875-888 (2003).
62. Beatty, W. L. & Russell, D. G. Identification of mycobacterial surface proteins released into subcellular compartments of infected macrophages. Infect. Immun. 68, 6997-7002 (2000).
63. Ullrich, H. J., Beatty, W. L. & Russell, D. G. Interaction of Mycobacterium avium-containing phagosomes with the antigen presentation pathway. J. Immunol. 165, 6073-6080 (2000).
64. Arend, S. M. et al. Detection of active tuberculosis infection by T cell responses to early-secreted antigenic target 6-kDa protein and culture filtrate protein 10. J. Infect. Dis. 181, 1850-1854 (2000).
65. Fortune, S. M. et al. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc. Natl Acad. Sci. USA 102, 10676-10681 (2005).
66. Weldingh, K. et al. Two-dimensional electrophoresis for analysis of Mycobacterium tuberculosis culture filtrate and purification and characterization of six novel proteins. Infect. Immun. 66, 3492-3500 (1998).
67. Moody, D. B. et al. T-cell activation by lipopeptide antigens. Science 303, 527-531 (2004).
68. Ulrichs, T., Moody, D. B., Grant, E., Kaufmann, S. H. & Porcelli, S. A. T-cell responses to CD 1-presented lipid antigens in humans with Mycobacterium tuberculosis infection. Infect. Immun. 71, 3076-3087 (2003).
69. Dascher, C. C. & Brenner, M. B. CD 1 antigen presentation and infectious disease. Contrib. Microbiol. 10, 164-182 (2003).
70. Puissegur, M. P. et al. An in vitro dual model of mycobacterial granulomas to investigate the molecular interactions between mycobacteria and human host cells. Cell Microbiol. 6, 423-33 (2004).
71. Syed, S. S. & Hunter, R. L. Jr. Studies on the toxic effects of quartz and a mycobacterial glycolipid, trehalose 6, 6′-dimycolate. Ann. Clin. Lab. Sci. 27, 375-383 (1997).
72. + mice. J. Interferon. Cytokine Res. 21, 1089-1096 (2001).
73. Behling, C. A., Perez, R. L., Kidd, M. R., Staton, G. W., Jr & Hunter, R. L. Induction of pulmonary granulomas, macrophage procoagulant activity, and tumor necrosis factor-α by trehalose glycolipids. Ann. Clin. Lab. Sci. 23, 256-266 (1993).
74. Bentley, A. G. et al. In vitro delayed hypersensitivity granuloma formation: Development of an antigen-coated bead model. J. Immunol. 134, 4163-4169 (1985).
75. Lima, V. M. et al. Role of trehalose dimycolate in recruitment of cells and modulation of production of cytokines and NO in tuberculosis. Infect. Immun. 69, 5305-5312 (2001).
76. Sakaguchi, I. et al. Trehalose 6, 6′-dimycolate (Cord factor) enhances neovascularization through vascular endothelial growth factor production by neutrophils and macrophages. Infect. Immun. 68, 2043-2052 (2000).
77. Yamagami, H. et al. Trehalose 6, 6′-dimycolate (cord factor) of Mycobacterium tuberculosis induces foreign-body- and hypersensitivity-type granulomas in mice. Infect. Immun. 69, 810-815 (2001).
78. Geisel, R. E., Sakamoto, K., Russell, D. G. & Rhoades, E. R. In vivo activity of released cell wall lipids of Mycobacterium bovis bacillus Calmette-Guerin is due principally to trehalose mycolates. J. Immunol. 174, 5007-5015 (2005).
79. Rhoades, E. R., Geisel, R. E., Butcher, B. A., McDonough, S. & Russell, D. G. Cell wall lipids from Mycobacterium bovis BCG are inflammatory when inoculated within a gel matrix: Characterization of a new model of the granulomatous response to mycobacterial components. Tuberculosis (Edinb) 85, 159-176 (2005).
80. Hunter, R. L., Olsen, M., Jagannath, C. & Actor, J. K. Trehalose 6, 6′-dimycolate and lipid in the pathogenesis of caseating granulomas of tuberculosis in mice. Am. J. Pathol. 168, 1249-1261 (2006).
81. Ryll, R., Kumazawa, Y. & Yano, I. Immunological properties of trehalose dimycolate (cord factor) and other mycolic acid-containing glycolipids-a review. Microbiol. Immunol. 45, 801-811 (2001).
82. Hamasaki, N. et al. In vivo administration of mycobacterial cord factor (Trehalose 6, 6′-dimycolate) can induce lung and liver granulomas and thymic atrophy in rabbits. Infect. Immun. 68, 3704-3709 (2000).
83. Bekierkunst, A. & Yarkoni, E. Granulomatous hypersensitivity to trehalose-6, 6′-dimycolate (cord factor) in mice infected with BCG. Infect. Immun. 7, 631-638 (1973).
84. 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).
85. Rao, V., Fujiwara, N., Porcelli, S. A. & Glickman, M. S. Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J. Exp. Med. 201, 535-543 (2005).
86. Rao, V., Gao, F., Chen, B., Jacobs, W. R. Jr & Glickman, M. S. Trans-cyclopropanation of mycolic acids on trehalose dimycolate suppresses Mycobacterium tuberculosis-induced inflammation and virulence. J. Clin. Invest. 116, 1660-1667 (2006).
87. Camacho, L. R. et al. Analysis of the phthiocerol dimycocerosate locus of Mycobacterium tuberculosis. Evidence that this lipid is involved in the cell wall permeability barrier. J. Biol. Chem. 276, 19845-19854 (2001).
88. Camacho, L. R., Ensergueix, D., Perez, E., Gicquel, B. & Guilhot, C. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol. Microbiol. 34, 257-267 (1999).
89. Cox, J. S., Chen, B., McNeil, M. & Jacobs, W. R. Jr. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402, 79-83 (1999).
90. Reed, M. B. et al. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431, 84-87 (2004).
91. Tsenova, L. et al. 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 (2005).
92. Fuller, C. L., Flynn, J. L. & Reinhart, T. A. In situ study of abundant expression of proinflammatory chemokines and cytokines in pulmonary granulomas that develop in cynomolgus macaques experimentally infected with Mycobacterium tuberculosis. Infect. Immun. 71, 7023-7034 (2003).
93. Rhoades, E. R., Cooper, A. M. & Orme, I. M. Chemokine response in mice infected with Mycobacterium tuberculosis. Infect. Immun. 63, 3871-3877 (1995).
94. Cooper, A. M. et al. Disseminated tuberculosis in interferon γ gene-disrupted mice. J. Exp. Med. 178, 2243-2247 (1993).