Mycobacterium tuberculosis inhibits IFN-γ transcriptional responses without inhibiting activation of STAT1

Journal of Immunology

Volumn 163, Issue 7, 1999, Pages 3898-3906

  Ting, Li Min ^a   Kim, Anne C ^a   Cattamanchi, Ashok ^a   Ernst, Joel D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; GAMMA INTERFERON; SERINE; STAT1 PROTEIN;

ARTICLE; CELL WALL; CONTROLLED STUDY; CYTOMEGALOVIRUS; DIMERIZATION; DNA BINDING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LEISHMANIA DONOVANI; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TOXOPLASMA GONDII;

ANIMALS; ANTIBODIES, MONOCLONAL; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CELLS, CULTURED; CREB-BINDING PROTEIN; DNA-BINDING PROTEINS; HUMANS; INTERFERON TYPE II; INTERFERON-STIMULATED GENE FACTOR 3; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR PROTEINS; PHOSPHORYLATION; RECEPTORS, IGG; RNA, MESSENGER; SERINE; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; SUBCELLULAR FRACTIONS; TOXOPLASMA; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; TYROSINE;

EID: 0033214553     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Markowitz, N., N. I. Hansen, P. C. Hopewell, J. Glassroth, P. A. Kvale, B. T. Mangura, T. C. Wilcosky, J. M. Wallace, M. J. Rosen, and L. B. Reichman. 1997. Incidence of tuberculosis in the United States among HIV-infected persons; The Pulmonary Complications of HIV Infection Study Group. Ann. Intern. Med. 126:123.
2. Molloy, A., and G. Kaplan. 1996. Cell-mediated immune response [in tuberculosis]. In Tuberculosis. W. N. Rom and S. M. Garay, eds. Little, Brown, Boston, pp. 305-314.
3. Zimmerli, S., S. Edwards, and J. D. Ernst. 1996. Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages. Am. J. Respir. Cell Mol. Biol. 15:760.
4. Nathan, C. F., H. W. Murray, M. E. Wiebe, and B. Y. Rubin. 1983. Identification of interferon-γ as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158:670.
5. Nathan, C. F., T. J. Prendergast, M. E. Wiebe, E. R. Stanley, E. Platzer, H. G. Remold, K. Welte, B. Y. Rubin, and H. W. Murray. 1984. Activation of human macrophages: comparison of other cytokines with interferon-γ. J. Exp. Med. 160:600.
6. Cooper, A. M., D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme. 1993. Disseminated tuberculosis in interferon γ gene-disrupted mice. J. Exp. Med. 178:2243.
7. Flynn, J. L., J. Chan, K. J. Triebold, D. K. Dalton, T. A. Stewart, and B. R. Bloom. 1993. An essential role for interferon γ in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249.
8. Barnes, P. F., S. J. Fong, P. J. Brennan, P. E. Twomey, A. Mazumder, and R. L. Modlin. 1990. Local production of tumor necrosis factor and IFN-γ in tuberculous pleuritis. J. Immunol. 145:149.
9. Barnes, P. F., S. Lu, J. S. Abrams, E. Wang, M. Yamamura, and R. L. Modlin. 1993. Cytokine production at the site of disease in human tuberculosis. Infect. Immun. 61:3482.
10. Robinson, D. S., S. Ying, I. K. Taylor, A. Wangoo, D. M. Mitchell, A. B. Kay, Q. Hamid, and R. J. Shaw. 1994. Evidence for a Th1-like bronchoalveolar T-cell subset and predominance of interferon-γ gene activation in pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 149:989.
11. Lin, Y., M. Zhang, F. M. Hofman, J. Gong, and P. F. Barnes. 1996. Absence of a prominent Th2 cytokine response in human tuberculosis. Infect. Immun. 64: 1351.
12. Douvas, G. S., D. L. Looker, A. E. Vatter, and A. J. Crowle. 1985. γ Interferon activates human macrophages to become tumoricidal and leishmanicidal but enhances replication of macrophage-associated mycobacteria. Infect. Immun. 50:1.
13. Byrd, T. F., and M. A. Horwitz. 1989. Interferon γ-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J. Clin. Invest. 83: 1457.
14. Murray, H. W., A. M. Granger, and R. F. Teitelbaum. 1991. γ Interferon-activated human macrophages and Toxoplasma gondii, Chlamydia psittaci, and Leishmania donovani: antimicrobial role of limiting intracellular iron. Infect. Immun. 59:4684.
15. Rook, G. A. W., J. Steele, M. Ainsworth, and B. R. Champion. 1986. Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant γ-interferon on human monocytes and murine peritoneal macrophages. Immunology 59:333.
16. Darnell, J. E., Jr., I. M. Kerr, and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415.
17. Ihle, J. N. 1995. Cytokine receptor signalling. Nature 377:591.
18. Ihle, J. N. 1996. STATs: signal transducers and activators of transcription. Cell 84:331.
19. Sekimoto, T., K. Nakajima, T. Tachibana, T. Hirano, and Y. Yoneda. 1996. Interferon-γ-dependent nuclear import of Stal1 is mediated by the GTPase activity of Ran/TC4. J. Biol. Chem. 271:31017.
20. Wen, Z., Z. Zhong, and J. E. Darnell, Jr. 1995. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82:241.
21. Zhang, J. J., U. Vinkemeier, W. Gu, D. Chakravarti, C. M. Horvath, and J. E. Darnell, Jr. 1996. Two contact regions between Stat1 and CBP/p300 in interferon γ signaling. Proc. Natl. Acad. Sci. USA 93:15092.
22. Haspel, R. L., M. Salditt-Georgieff, and J. E. Darnell, Jr. 1996. The rapid inactivation of nuclear tyrosine phosphorylated Stat1 depends upon a protein tyrosine phosphatase. EMBO J. 15:6262.
23. Kim, T. K., and T. Maniatis. 1996. Regulation of interferon-γ-activated STAT1 by the ubiquitin-proteasome pathway. Science 273:1717.
24. Zimmerli, S., M. Majeed, M. Gustavsson, O. Stendahl, D. A. Sanan, and J. D. Ernst. 1996. Phagosome-lysosome fusion is a calcium-independent event in macrophages. J. Cell Biol. 132:49.
25. Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248.
26. Frank, D. A., S. Mahajan, and J. Ritz. 1997. B lymphocytes from patients with chronic lymphocytic leukemia contain signal transducer and activator of transcription (STAT) 1 and STAT3 constitutively phosphorylated on serine residues. J. Clin. Invest. 100:3140.
27. 2+ and phospholipid binding domains. Biochem. Biophys. Res. Commun. 200:867.
28. Gaffen, S. L., S. Y. Lai, W. Xu, F. Gouilleux, B. Groner, M. A. Goldsmith, and W. C. Greene. 1995. Signaling through the interleukin 2 receptor β chain activates a STAT-5-like DNA-binding activity. Proc. Natl. Acad. Sci. USA 92:7192.
29. Nandan, D., and N. E. Reiner. 1997. TGF-β attenuates the class II transactivator and reveals an accessory pathway of IFN-γ action. J. Immunol. 158:1095.
30. Pearse, R. N., R. Feinman, K. Shuai, J. E. J. Darnell, and J. V. Ravetch. 1993. Interferon γ-induced transcription of the high-affinity Fc receptor for IgG requires assembly of a complex that includes the 91-kDa subunit of transcription factor ISGF3. Proc. Natl. Acad. Sci. USA 90:4314.
31. Chon, S. Y., H. H. Hassanain, and S. L. Gupta. 1996. Cooperative role of interferon regulatory factor 1 and p91 (STAT1) response elements in interferon-γ-inducible expression of human indoleamine 2,3-dioxygenase gene. J. Biol. Chem. 271:17247.
32. Decker, T., D. J. Lew, Y. S. Cheng, D. E. Levy, and J. E. Darnell, Jr. 1989. Interactions of α-and γ-interferon in the transcriptional regulation of the gene encoding a guanylate-binding protein. EMBO J. 8:2009.
33. Horvath, C. M., and J. E. Darnell, Jr. 1996. The antiviral state induced by α interferon and γ interferon requires transcriptionally active Stat1 protein. J. Virol. 70:647.
34. Horvai, A. E., L. Xu, E. Korzus, G. Brard, D. Kalafus, T. M. Mullen, D. W. Rose, M. G. Rosenfeld, and C. K. Glass. 1997. Nuclear integration of JAK/STAT and Ras/AP-1 signaling by CBP and p300. Proc. Natl. Acad. Sci. USA 94:1074.
35. Panek, R. B., Y. J. Lee, and E. N. Benveniste. 1995. TGF-β suppression of IFN-γ-induced class II MHC gene expression does not involve inhibition of phosphorylation of JAK1, JAK2, or signal transducers and activators of transcription, or modification of IFN-γ enhanced factor X expression. J. Immunol. 154:610.
36. Lee, Y. J., Y. Han, H. T. Lu, V. Nguyen, H. Qin, P. H. Howe, B. A. Hocevar, J. M. Boss, R. M. Ransohoff, and E. N. Benveniste. 1997. TGF-β suppresses IFN-γ induction of class II MHC gene expression by inhibiting class II transactivator messenger RNA expression. J. Immunol. 158:2065.
37. Hirsch, C. S., T. Yoneda, L. Averill, J. J. Elmer, and Z. Toossi. 1994. Enhancement of intracellular growth of Mycobacterium tuberculosis in human monocytes by transforming growth factor-β1. J. Infect. Dis. 170:1229.
38. Nandan, D., and N. E. Reiner. 1995. Attenuation of γ interferon-induced tyrosine phosphorylation in mononuclear phagocytes infected with Leishmania donovani: selective inhibition of signaling through Janus kinases and Stat1. Infect. Immun. 63:4495.
39. Miller, D. M., B. M. Rahill, J. M. Boss, M. D. Lairmore, J. E. Durbin, W. J. Waldman, and D. D. Sedmak. 1998. Human cytomegalovirus inhibits MHC class II expression by disruption of the JAK/STAT pathway. J. Exp. Med. 187: 675.
40. Hottiger, M. O., L. K. Felzien, and G. J. Nabel. 1998. Modulation of cytokine-induced HIV gene expression by competitive binding of transcription factors to the coactivator p300. EMBO J. 17:3124.
41. Eckner, R., M. E. Ewen, D. Newsome, M. Gerdes, J. A. DeCaprio, J. B. Lawrence, and D. M. Livingston. 1994. Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev. 8:869.
42. Arany, Z., D. Newsome, E. Oldread, D. M. Livingston, and R. Eckner. 1995. A family of transcriptional adaptor proteins targeted by the E1A oncoprotein. Nature 374:81.
43. Look, D. C., W. T. Roswit, A. G. Frick, Y. Gris-Alevy, D. M. Dickhaus, M. J. Walter, and M. J. Holtzman. 1998. Direct suppression of Stat1 function during adenoviral infection. Immunity 9:871.
44. Zhu, M., S. John, M. Berg, and W. J. Leonard. 1999. Functional association of Nmi with Stat5 and Stat1 in IL-2-and IFNγ-mediated signaling. Cell 96:121.
45. Chawla, S., G. E. Hardingham, D. R. Quinn, and H. Bading. 1998. CBP: a signal-regulated transcriptional coactivator controlled by nuclear calcium and CaM kinase IV. Science 281:1505.
46. 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: role of the Src homology 2 containing tyrosine phosphatase 1. J. Biol. Chem. 273:645.
47. Sibley, L. D., and J. L. Krahenbuhl. 1987. Mycobacterium leprae-burdened macrophages arc refractory to activation by γ interferon. Infect. Immun. 55:446.
48. Sibley, L. D., and J. L. Krahenbuhl. 1988. Induction of unresponsiveness to γ interferon in macrophages infected with Mycobacterium leprae. Infect. Immun. 56:1912.
49. Sibley, L. D., S. W. Hunter, P. J. Brennan, and J. L. Krahenbuhl. 1988. Mycobacterial lipoarabinomannan inhibits γ interferon-mediated activation of macrophages. Infect. Immun. 56:1232.
50. Chan, J., X. Fan, S. W. Hunter, P. J. Brennan, and B. R. Bloom. 1991. Lipoarabinomannan, a possible virulence factor involved in persistence of Mycobacterium tuberculosis within macrophages. Infect. Immun. 59:1755.
51. De Kimpe, S. J., M. Kengatharan, C. Thiemermann, and J. R. Vane. 1995. The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. Proc. Natl. Acad. Sci. USA 92:10359.