The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through toll-like receptor-2

Journal of Immunology

Volumn 170, Issue 5, 2003, Pages 2409-2416

  López, Martín ^a   Sly, Laura M ^a   Luu, Yvonne ^a   Young, Douglas ^b   Cooper, Howard ^b   Reiner, Neil E ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 8; CASPASE 9; GLYCOPROTEIN; LIPOCORTIN 5; MONOCLONAL ANTIBODY; PHOSPHATIDYLSERINE; PROTEIN P19; TOLL LIKE RECEPTOR 2; VIRULENCE FACTOR;

ACYLATION; APOPTOSIS; ARTICLE; BACTERIAL VIRULENCE; CELL VIABILITY; CHO CELL; HUMAN; HUMAN CELL; MACROPHAGE; MONOCYTE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

EID: 0344643405     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.5.2409     Document Type: Article

References (47)

1. Kaufmann, S. H., and J. D. van Embden. 1993. Tuberculosis: a neglected disease strikes back. Trends Microbiol. 1:2.
2. Day, M. 1998. Fighting talk: WHO gets tough on TB after criticism from scientists. New Sci. 2127:21 (Abstr.).
3. Armstrong, J. A., and P. D. Hart. 1975. 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. 142:1.
4. Hingley-Wilson, S. M., L. M. Sly, N. E. Reiner, and W. R. McMaster. 2000. The immunobiology of the mycobacterial infected macrophage. Mod. Aspects Immunobiology 1:96.
5. Fenton, M. J., and M. W. Vermeulen. 1996. Immunopathology of tuberculosis: roles of macrophages and monocytes. Infect. Immun. 64:683.
6. Sly, L. M., M. Lopez, W. M. Nauseef, and N. E. Reiner. 2001. 1α,25-Dihydroxyvitamin D3-induced monocyte antimycobacterial activity is regulated by phosphatidylinositol 3-kinase and mediated by the NADPH-dependent phagocyte oxidase. J. Biol. Chem. 276:35482.
7. Clemens, D. L., and M. A. Horwitz. 1995. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181:257.
8. Sturgill-Koszycki, S., P. H. Schlesinger, P. Chakraborty, P. L. Haddix, H. L. Collins, A. K. Fok, R. D. Allen, S. L. Gluck, J. Heuser, and D. G. Russell. 1994. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678.
9. Cohen, G. B., R. Ren, and D. Baltimore. 1995. Modular binding domains in signal transduction proteins. Cell 80:237.
10. Mazzaccaro, R. J., M. Gedde, E. R. Jensen, H. M. Van Santen, H. L. Ploegh, K. L. Rock, and B. R. Bloom. 1996. Major histocompatibility class I presentation of soluble antigen facilitated by Mycobacterium tuberculosis infection. Proc. Natl. Acad. Sci. USA 93:11786.
11. Reiner, N. E. 1994. Altered cell signaling and mononuclear phagocyte deactivation during intracellular infection. Immunol. Today 15:374.
12. Knutson, K. L., Z. Hmama, P. Herrera-Velit, R. Rochford, and N. E. Reiner. 1998. Lipoarabinomannan of Mycobacterium tuberculosis promotes protein tyrosine dephosphorylation and inhibition of mitogen-activated protein kinase in human mononuclear phagocytes. J. Biol. Chem. 273:645.
13. Rojas, M., M. Olivier, P. Gros, L. F. Barrera, and L. F. Garcia. 1999. TNF-α and IL-10 modulate the induction of apoptosis by virulent Mycobacterium tuberculosis in murine macrophages. J. Immunol. 162:6122.
14. Santucci, M. B., M. Amicosante, R. Cicconi, C. Montesano, M. Casarini, S. Giosue, A. Bisetti, V. Colizzi, and M. Fraziano. 2000. Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages: early membrane modifications and intracellular mycobacterial viability. J. Infect. Dis. 181:1506.
15. Klingler, K., K. M. Tchou-Wong, O. Brandli, C. Aston, R. Kim, C. Chi, and W. N. Rom. 1997. Effects of mycobacteria on regulation of apoptosis in mononuclear phagocytes. Infect. Immun. 65:5272.
16. Fratazzi, C., R. D. Arbeit, C. Carini, and H. G. Remold. 1997. Programmed cell death of Mycobacterium avium serovar 4-infected human macrophages prevents the mycobacteria from spreading and induces mycobacterial growth inhibition by freshly added, uninfected macrophages. J. Immunol. 158:4320.
17. Rojas, M., L. F. Barrera, G. Puzo, and L. F. Garcia. 1997. Differential induction of apoptosis by virulent Mycobacterium tuberculosis in resistant and susceptible murine macrophages: role of nitric oxide and mycobacterial products. J. Immunol. 159:1352.
18. Placido, R., G. Mancino, A. Amendola, F. Mariani, S. Vendetti, M. Piacentini, A. Sanduzzi, M. L. Bocchino, M. Zembala, and V. Colizzi. 1997. Apoptosis of human monocytes/macrophages in Mycobacterium tuberculosis infection. J. Pathol. 181:31.
19. Keane, J., M. K. Balcewicz-Sablinska, H. G. Remold, G. L. Chupp, B. B. Meek, M. J. Fenton, and H. Kornfeld. 1997. Infection by Mycobacterium tuberculosis promotes human alveolar macrophage apoptosis. Infect. Immun. 65:298.
20. Keane. J., H. G. Remold, and H. Kornfeld. 2000. Virulent Mycobacterium tuberculosis strains evade apoptosis of infected alveolar macrophages. J. Immunol. 164:2016.
21. Durrbaum-Landmann, I., J. Gercken, H. D. Flad, and M. Ernst. 1996. Effect of in vitro infection of human monocytes with low numbers of Mycobacterium tuberculosis bacteria on monocyte apoptosis. Infect. Immun. 64:5384.
22. Balcewicz-Sablinska, M. K., J. Keane, H. Kornfeld, and H. G. Remold. 1998. Pathogenic Mycobacterium tuberculosis evades apoptosis of host macrophages by release of TNF-R2, resulting in inactivation of TNF-α. J. Immunol. 161:2636.
23. Brightbill, H. D., D. H. Libraty, S. R. Krutzik, R. B. Yang, J. T. Belisle, J. R. Bleharski, M. Maitland, M. V. Norgard, S. E. Plevy, S. T. Smale, et al. 1999. Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science 285:732.
24. Imler, J. L., and J. A. Hoffmann. 2001. Toll receptors in innate immunity. Trends Cell Biol. 11:304.
25. Kopp, E. B., and R. Medzhitov. 1999. The Toll-receptor family and control of innate immunity. Curr. Opin. Immunol. 11:13.
26. Lien, E., T. J. Sellati, A. Yoshimura, T. H. Flo, G. Rawadi, R. W. Finberg, J. D. Carroll, T. Espevik, R. R. Ingalls, J. D. Radolf, and D. T. Golenbock. 1999. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem. 274:33419.
27. Means, T. K., E. Lien, A. Yoshimura, S. Wang, D. T. Golenbock. and M. J. Fenton. 1999. The CD14 ligands lipoarabinomannan and lipopolysaccharide differ in their requirement for Toll-like receptors. J. Immunol. 163:6748.
28. Hayashi, F., K. D. Smith, A. Ozinsky, T. R. Hawn, E. C. Yi, D. R. Goodlett, J. K. Eng, S. Akira, D. M. Underhill, and A. Aderem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099.
29. Bauer, S., C. J. Kirschning, H. Hacker, V. Redecke, S. Hausmann, S. Akira, H. Wagner, and G. B. Lipford. 2001. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. USA 98:9237.
30. Means, T. K., S. Wang, E. Lien, A. Yoshimura, D. T. Golenbock, and M. J. Fenton. 1999. Human Toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 163:3920.
31. Underhill, D. M., A. Ozinsky, K. D. Smith, and A. Aderem. 1999. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 96:14459.
32. Means, T. K., B. W. Jones, A. B. Schromm, B. A. Shurtleff, J. A. Smith, J. Keane, D. T. Golenbock, S. N. Vogel, and M. J. Fenton. 2001. Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J. Immunol. 166:4074.
33. Aliprantis, A. O., R. B. Yang, D. S. Weiss, P. Godowski, and A. Zychlinsky. 2000. The apoptotic signaling pathway activated by Toll-like receptor-2. EMBO J. 19:3325.
34. Herrmann, J. L., P. O'Gaora, A. Gallagher, J. E. Thole, and D. B. Young. 1996. Bacterial glycoproteins: a link between glycosylation and proteolytic cleavage of a 19 kDa antigen from Mycobacterium tuberculosis. EMBO J. 15:3547.
35. Young, D. B., and T. R. Garbe. 1991. Lipoprotein antigens of Mycobacterium tuberculosis. Res. Microbiol. 142:55.
36. Thoma-Uszynski, S., S. Stenger, O. Takeuchi, M. T. Ochoa, M. Engele, P. A. Sieling, P. F. Barnes, M. Rollinghoff, P. L. Bolcskei, M. Wagner, et al. 2001. Induction of direct antimicrobial activity through mammalian Toll-like receptors. Science 291:1544.
37. Hmama, Z., D. Nandan, L. Sly, K. L. Knutson, P. Herrera-Velit, and N. E. Reiner. 1999. 1α.25-dihydroxyvitamin D(3)-induced myeloid cell differentiation is regulated by a vitamin D receptor-phosphatidylinositol 3-kinase signaling complex. J. Exp. Med. 190:1583.
38. Abou-Zeid, C., M. P. Gares, J. Inwald, R. Janssen, Y. Zhang, D. B. Young, C. Hetzel, J. R. Lamb, S. L. Baldwin, I. M. Orme, et al. 1997. Induction of a type 1 immune response to a recombinant antigen from Mycobacterium tuberculosis expressed in Mycobacterium vaccae. Infect. Immun. 65:1856.
39. Kaufmann, S. H., and M. O. Hengartner. 2001. Programmed cell death: alive and well in the new millennium. Trends Cell Biol. 11:526.
40. +2-dependent cell signaling. J. Infect. Dis. 182:240.
41. Monack, D. M., B. Raupach, A. E. Hromockyj, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93:9833.
42. Monack, D. M., J. Mecsas, N. Ghori, and S. Falkow. 1997. Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl. Acad. Sci. USA 94:10385.
43. Zychlinsky, A., M. C. Prevost. and P. J. Sansonetti. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167.
44. Zychlinsky, A., B. Kenny, R. Menard, M. C. Prevost, I. B. Holland, and P. J. Sansonetti. 1994. IpaB mediates macrophage apoptosis induced by Shigella flexneri. Mol. Microbiol. 11:619.
45. Aliprantis, A. O., R. B. Yang, M. R. Mark, S. Suggett, B. Devaux, J. D. Radolf, G. R. Klimpel, P. Godowski, and A. Zychlinsky. 1999. Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science 285:736.
46. Ciaramella, A., A. Martino, R. Cicconi, V. Colizzi, and M. Fraziano. 2000. Mycobacterial 19-kDa lipoprotein mediates Mycobacterium tuberculosis-induced apoptosis in monocytes/macrophages at early stages of infection. Cell Death Differ. 7:1270.
47. Oddo, M., T. Renno, A. Attinger, T. Bakker, H. R. MacDonald, and P. R. A. Meylan. 1998. Fas ligand-induced apoptosis of infected human macrophages reduces the viability of intracellular Mycobacterium tuberculosis. J. Immunol. 160:5448.