Immune evasion by Mycobacterium tuberculosis: Living with the enemy

Current Opinion in Immunology

Volumn 15, Issue 4, 2003, Pages 450-455

  Flynn, JoAnne L ^a   Chan, John ^b  

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

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID DERIVATIVE; CD4 ANTIGEN; COAT PROTEIN; GAMMA INTERFERON; LIPOPROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NITROGEN; TOLL LIKE RECEPTOR 2; TRYPTOPHAN DERIVATIVE;

ANTIGEN PRESENTATION; BIOGENESIS; CYTOTOXICITY; DENDRITIC CELL; IMMUNE RESPONSE; LYSOSOME; MACROPHAGE; MOLECULAR WEIGHT; MYCOBACTERIOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOSOME; PROTEIN FUNCTION; REVIEW; T LYMPHOCYTE;

EID: 0041402773     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(03)00075-X     Document Type: Review

References (57)

1. MacMicking J., Xie Q.W., Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol. 15:1997;323-350.
2. Chan J, Flynn J: Nitric oxide in Mycobacterium tuberculosis infection. In Nitric Oxide and Infection. Edited by Fang F: Plenum Publishers; 1999:281-310.
3. Chan J., Tanaka K., Carroll D., Flynn J.L., Bloom B.R. Effect of nitric oxide synthase inhibitors on murine infection with Mycobacterium tuberculosis. Infect Immun. 63:1995;736-740.
4. MacMicking J., North R.J., LaCourse R., Mudgett J.S., Shah S.K., Nathan C.F. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci USA. 94:1997;5243-5248.
5. Scanga C.A., Mohan V.P., Tanaka K., Alland D., Flynn J.L., Chan J. The NOS2 locus confers protection in mice against aerogenic challenge of both clinical and laboratory strains of Mycobacterium tuberculosis. Infect Immun. 69:2001;7711-7717.
6. Flynn J.L., Scanga C.A., Tanaka K.E., Chan J. Effects of aminoguanidine on latent murine tuberculosis. J Immunol. 160:1998;1796-1803.
7. Ehrt S., Shiloh M.U., Ruan J., Choi M., Gunzburg S., Nathan C., Xie Q., Riley L.W. A novel antioxidant gene from Mycobacterium tuberculosis. J Exp Med. 186:1997;1885-1896.
8. 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. 67:1999;3276-3283.
9. Chen L., Xie Q.W., Nathan C. Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates. Mol Cell. 1:1998;795-805.
10. Bryk R., Griffin P., Nathan C. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature. 407:2000;211-215.
11. Yu K., Mitchell C., Xing Y., Magliozzo R.S., Bloom B.R., Chan J. Toxicity of nitrogen oxides and related oxidants on mycobacteria: M. tuberculosis is resistant to peroxynitrite anion. Tuber Lung Dis. 79:1999;191-198.
12. St John G., Brot N., Ruan J., Erdjument-Bromage H., Tempst P., Weissbach H., Nathan C. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc Natl Acad Sci USA. 98:2001;9901-9906.
13. Bryk R., Lima C.D., Erdjument-Bromage H., Tempst P., Nathan C. Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science. 295:2002;1073-1077 This study provides evidence for a novel bacterial antioxidant defense mechanism that involves a nicotinamide adenine dinucleotide (reduced)-dependent peroxidase and peroynitrite reductase consisting of dihydrolipoamide dehydrogenase (Lpd), dihydrolipoamide succinyltransferase (SucB), the thioredoxin-like AhpD and peroxiredoxin alkyl hydroperoxide reductase (AhpC).
14. McKinney J.D., zu Bentrup K.H., Miczak A., Chen B., Chan W.T., Swenson D., Sacchettini J.C., Jacobs W.R. Jr., Russell D.G. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature. 406:2000;735-738.
15. Nathan C. Inducible nitric oxide synthase in the tuberculous human lung. Am J Respir Crit Care Med. 166:2002;130-131.
16. Choi H.S., Rai P.R., Chu H.W., Cool C., Chan E.D. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am J Respir Crit Care Med. 166:2002;178-186 The results of this study provide the most compelling evidence to date that reactive nitrogen intermediates are produced in human tuberculous tissues in situ.
17. Desjardins M. Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol. 5:1995;183-186.
18. Vieira O.V., Botelho R.J., Grinstein S. Phagosome maturation: aging gracefully. Biochem J. 366:2002;689-704 This is an excellent review on phagosome maturation.
19. Russell D.G. Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol. 2:2001;569-577.
20. Russell D.G., Mwandumba H.C., Rhoades E.E. Mycobacterium and the coat of many lipids. J Cell Biol. 158:2002;421-426.
21. Fratti R.A., Vergne I., Chua J., Skidmore J., Deretic V. Regulators of membrane trafficking and Mycobacterium tuberculosis phagosome maturation block. Electrophoresis. 21:2000;3378-3385.
22. Sturgill-Koszycki S., Schlesinger P.H., Chakraborty P., Haddix P.L., Collins H.L., Fok A.K., Allen R.D., Gluck S.L., Heuser J., Russell D.G. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science. 263:1994;678-681.
23. Xu S., Cooper A., Sturgill-Koszycki S., van Heyningen T., Chatterjee D., Orme I., Allen P., Russell D.G. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J Immunol. 153:1994;2568-2578.
24. Sollner T.H. Vesicle tethers promoting fusion machinery assembly. Dev Cell. 2:2002;377-378.
25. Rothman J.E. The machinery and principles of vesicle transport in the cell. Nat Med. 8:2002;1059-1062.
26. Jahn R., Sudhof T.C. Membrane fusion and exocytosis. Annu Rev Biochem. 68:1999;863-911.
27. Waters M.G., Pfeffer S.R. Membrane tethering in intracellular transport. Curr Opin Cell Biol. 11:1999;453-459.
28. Zerial M., McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2:2001;107-117.
29. Fratti R.A., Backer J.M., 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. 154:2001;631-644.
30. Clemens D.L., Lee B.Y., Horwitz M.A. Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect Immun. 68:2000;2671-2684.
31. Via L., Deretic D., Ulmer R.J., Hibler N.S., Huber L.A., 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. 272:1997;13326-13331.
32. Clemens D.L., Lee B.Y., Horwitz M.A. Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect Immun. 68:2000;5154-5166.
33. Fratti R.A., Chua J., Deretic V. Cellubrevin alterations and Mycobacterium tuberculosis phagosome maturation arrest. J Biol Chem. 277:2002;17320-17326.
34. Ferrari G., Langen H., Naito M., Pieters J.A. Coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell. 97:1999;435-447.
35. 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. 3:2001;785-793.
36. Noss E.H., Harding C.V., Boom W.H. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol. 201:2000;63-74.
37. Hmama Z., Gabathuler R., Jefferies W.A., Dejong 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. 161:1998;4882-4893.
38. Wojciechowski W., DeSanctis J., Skamene E., Radzioch D. Attenuation of MHC Class II expression in macrophages infected with Mycobacterium bovis BCG involves Class II transactivator and depends on the Nramp1 gene. J Immunol. 163:1999;2688-2696.
39. Ting L.M., Kim A.C., Cattamanchi A., Ernst J.D. Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J Immunol. 163:1999;3898-3906.
40. Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT, Boom WH, Harding CV: 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, 167:910-918.
41. Means T.K., Wang S., Lien E., Yoshimura A., Golenbock D.T., Fenton M.J. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J Immunol. 163:1999;3920-3927.
42. Underhill D.M., Ozinsky A., Hajjar A.M., Stevens A., Wilson C.B., Bassetti M., Aderem A. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature. 401:1999;811-815.
43. Henderson R.A., Watkins S.C., Flynn J.L. Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J Immunol. 159:1997;635-643.
44. Bodnar K.A., Serbina N.V., Flynn J.L. Interaction of Mycobacterium tuberculosis with murine dendritic cells. Infect Immun. 69:2001;800-809.
45. Hertz C.J., Kiertscher S.M., Godowski P.J., Bouis D.A., Norgard M.V., Roth M.D., Modlin R.L. Microbial lipopeptides stimulate dendritic cell maturation via Toll-like receptor 2. J Immunol. 166:2001;2444-2450.
46. + T cells during Mycobacterium tuberculosis infection. J Immunol. 167:2001;6991-7000.
47. Jiao X., Lo-Man R., Guermonprez P., Fiette L., Deriaud E., Burgaud S., Gicquel B., Winter N., Leclerc C. Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity. J Immunol. 168:2002;1294-1301 The authors of this paper present evidence that dendritic cells can harbor mycobacteria in vivo, and confirm in vitro evidence that dendritic cells are impaired in their ability to kill intracellular M. tuberculosis.
48. Brightbill H.D., Libraty D.H., Krutzik S.R., Yang R.B., Belisle J.T., Bleharski J.R., Maitland M., Norgard M.V., Plevy S.E., Smale S.T.et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science. 285:1999;732-736.
49. Yeremeev V.V., Lyadova I.V., Nikonenko B.V., Apt A.S., Abou-Zeid C., Inwald J., Young D.B. The 19-kD antigen and protective immunity in a murine model of tuberculosis. Clin Exp Immunol. 120:2000;274-279.
50. Post F.A., Manca C., Neyrolles O., Ryffel B., Young D.B., Kaplan G. Mycobacterium tuberculosis 19-kilodalton lipoprotein inhibits Mycobacterium smegmatis-induced cytokine production by human macrophages in vitro. Infect Immun. 69:2001;1433-1439.
51. Abou-Zeid C., Gares M.P., Inwald J., Janssen R., Zhang Y., Young D.B., Hetzel C., Lamb J.R., Baldwin S.L., Orme I.M.et al. Induction of a type 1 immune response to a recombinant antigen from Mycobacterium tuberculosis expressed in Mycobacterium vaccae. Infect Immun. 65:1997;1856-1862.
52. Yeremeev V.V., Stewart G.R., Neyrolles O., Skrabal K., Avdienko V.G., Apt A.S., Young D.B. Deletion of the 19. kDa antigen does not alter the protective efficacy of BCG Tuber Lung Dis. 80:2000;243-247.
53. Lopez M., Sly L.M., Luu Y., Young D., Cooper H., Reiner N.E. The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J Immunol. 170:2003;2409-2416 Another demonstration that the 19 kDa lipoprotein interacts with TLR2, but with a different outcome - apoptosis.
54. Keane J., Remold H.G., Kornfeld H. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J Immunol. 164:2000;2016-2020.
55. Ramachandra L., Noss E., Boom W.H., Harding C.V. 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. 194:2001;1421-1432.
56. Fratti R.A., Chua J., Vergne I., Deretic V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA. 100:2003;5432-5437.
57. Pai RK, Convery M, Hamilton TA, Boom WH, Harding CV: Inhibition of IFN-γ-induced class II transactivator expression by 19 kDa lipoprotein from Mycobacterium tuberculosis: A potential mechanism for immune evasion. J Immunol 2003, 171:in press.