Inhibition of IFN-γ-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: A potential mechanism for immune evasion

Journal of Immunology

Volumn 171, Issue 1, 2003, Pages 175-184

  Pai, Rish K ^a   Convery, Marilyn ^a   Hamilton, Thomas A ^b   Henry Boom, W ^b   Harding, Clifford V ^a,c  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASS II TRANSACTIVATOR; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 4; LIPOPROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; PROTEIN; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION; BACTERIAL PROTEINS; CARRIER PROTEINS; CELL LINE; CELL NUCLEUS; DNA-BINDING PROTEINS; GENES, REPORTER; GENETIC VECTORS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INTERFERON TYPE II; INTERLEUKIN-4; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPROTEINS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; MYELOID DIFFERENTIATION FACTOR 88; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC; REPRESSOR PROTEINS; RNA, MESSENGER; STAT1 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 0037530648     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Caruso, A. M., N. Serbina, E. Klein, K. Triebold, B. R. Bloom, and J. L. Flynn. 1999. Mice deficient in CD4 T cells have only transiently diminished levels of IFN-γ, yet succumb to tuberculosis. J. Immunol. 162:5407.
2. 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.
3. 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.
4. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science 259:1739.
5. Ottenhoff, T. H., D. Kumararatne, and J. L. Casanova. 1998. Novel human immunodeficiencies reveal the essential role of type-I cytokines in immunity to intracellular bacteria. Immunol. Today 19:491.
6. Noss, E. H., C. V. Harding, and W. H. Boom. 2000. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell. Immunol. 201:63.
7. Noss, E. H., R. K. Pai, T. J. Sellati, J. D. Radolf, J. Belisle, D. T. Golenbock, W. H. Boom, and C. V. Harding. 2001. 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.
8. Stenger, S., and R. L. Modlin. 2002. Control of Mycobacterium tuberculosis through mammalian Toll-like receptors. Curr. Opin. Immunol. 14:452.
9. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry III, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537.
10. Brightbill, H. D., D. H. Library, 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.
11. Chu, R. S., D. Askew, E. H. Noss, A. Tobian, A. M. Krieg, and C. V. Harding. 1999. CpG oligodeoxynucleotides down-regulate macrophage class II MHC antigen processing. J. Immunol. 163:1188.
12. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11:443.
13. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9:143.
14. Sklar, M. D., A. Tereba, B. D. Chen, and W. S. Walker. 1985. Transformation of mouse bone marrow cells by transfection with a human oncogene related to c-myc is associated with the endogenous production of macrophage colony stimulating factor 1. J. Cell. Physiol. 125:403.
15. Harding, C. V., D. S. Collins, O. Kanagawa, and E. R. Unanue. 1991. Liposome-encapsulated antigens engender lysosomal processing for class II MHC presentation and cytosolic processing for class I presentation. J. Immunol. 147:2860.
16. Havlir, D. V., R. S. Wallis, W. H. Boom, T. M. Daniel, K. Chervenak, and J. J. Ellner. 1991. Human immune responses to Mycobacterium tuberculosis antigens. Infect. Immun. 59:665.
17. Simpson, D. A., S. Feeney, C. Boyle, and A. W. Stitt. 2000. Retinal VEGF mRNA measured by SYBR green 1 fluorescence: a versatile approach to quantitative PCR. Mol. Vis. 6:178.
18. Nikcevich, K. M., J. F. Piskurich, R. P. Hellendall, Y. Wang, and J. P. Ting. 1999. Differential selectivity of CIITA promoter activation by IFN-γ and IRF-1 in astrocytes and macrophages: CIITA promoter activation is not affected by TNF-α. J. Neuroimmunol. 99:195.
19. Piskurich, J. F., M. W. Linhoff, Y. Wang, and J. P. Ting. 1999. Two distinct γ-interferon-inducible promoters of the major histocompatibility complex class II transactivator gene are differentially regulated by STAT1, interferon regulatory factor 1, and transforming growth factor-β. Mol. Cell. Biol. 19:431.
20. Ohmori, Y., and T. A. Hamilton. 2000. Interleukin-4/STAT6 represses STAT1 and NF-κB-dependent transcription through distinct mechanisms. J. Biol. Chem. 275:38095.
21. Cao, H., R. G. Wolff, M. S. Meltzer, and R. M. Crawford. 1989. Differential regulation of class II MHC determinants on macrophages by IFN-γ and IL-4. J. Immunol. 143:3524.
22. Stuart, P. M., A. Zlotnik, and J. G. Woodward. 1988. Induction of class I and class II MHC antigen expression on murine bone marrow-derived macrophages by IL-4 (B cell stimulatory factor 1). J. Immunol. 140:1542.
23. Harton, J. A., and J. P. Ting. 2000. Class II transactivator: mastering the art of major histocompatibility complex expression. Mol. Cell. Biol. 20:6185.
24. Reith, W., and B. Mach. 2001. The bare lymphocyte syndrome and the regulation of MHC expression. Annu. Rev. Immunol. 19:331.
25. Chang, C.-H., G. Guerder, S.-C. Hong, W. van Ewijk, and R. A. Flavell. 1996. Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression. Immunity 4:167.
26. Itoh-Lindstrom, Y., J. F. Piskurich, N. J. Felix, Y. Wang, W. J. Brickey, J. L. Platt, B. H. Koller, and J. P. Ting. 1999. Reduced IL-4-, lipopolysaccharide-, and IFN-γ-induced MHC class II expression in mice lacking class II transacfivator due to targeted deletion of the GTP-binding domain. J. Immunol. 163:2425.
27. Wright, K. L., K. C. Chin, M. Linhoff, C. Skinner, J. A. Brown. J. M. Boss, G. R. Stark, and J. P. Ting. 1998. CIITA stimulation of transcription factor binding to major histocompatibility complex class II and associated promoters in vivo. Proc. Natl. Acad. Sci. USA 95:6267.
28. DeSandro, A. M., U. M. Nagarajan, and J. M. Boss. 2000. Associations and interactions between bare lymphocyte syndrome factors. Mol. Cell. Biol. 20:6587.
29. Hake, S. B., K. Masternak, C. Kammerbauer, C. Janzen, W. Reith, and V. Steimle. 2000. CIITA leucine-rich repeats control nuclear localization, in vivo recruitment to the major histocompatibility complex (MHC) class II enhanceosome, and MHC class II gene transactivation. Mol. Cell. Biol. 20:7716.
30. Masternak, K., A. Muhlethaler-Mottet, J. Villard, M. Zufferey, V. Steimle, and W. Reith. 2000. CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex. Genes Dev. 14:1156.
31. Zhu, X. S., M. W. Linhoff, G. Li, K. C. Chin, S. N. Maity, and J. P. Ting. 2000. Transcriptional scaffold: CIITA interacts with NF-Y, RFX, and CREB to cause stereospecific regulation of the class II major histocompatibility complex promoter. Mol. Cell. Biol. 20:6051.
32. Muhlethaler-Mottet, A., L. A. Otten, V. Steimle, and B. Mach. 1997. Expression of MHC class II molecules in different cellular and functional compartments is controlled by differential usage of multiple promoters of the transactivator CIITA. EMBO J. 16:2851.
33. Waldburger, J. M., T. Suter, A. Fontana, H. Acha-Orbea, and W. Reith. 2001. Selective abrogation of major histocompatibility complex class II expression on extrahematopoietic cells in mice lacking promoter IV of the class II transactivator gene. J. Exp. Med. 194:393.
34. Pai, R. K., D. Askew, W. H. Boom, and C. V. Harding. 2002. Regulation of class II MHC expression in APCs: roles of types I, III, and IV class II transactivator. J. Immunol. 169:1326.
35. Hussain, S., B. S. Zwilling, and W. P. Lafuse. 1999. Mycobacterium avium infecfion of mouse macrophages inhibits IFN-γ Janus kinase-STAT signaling and gene induction by down-regulation of the IFN-γ receptor. J. Immunol. 163:2041.
36. Boehm, U., T. Klamp, M. Groot, and J. C. Howard. 1997. Cellular responses to interferon-γ. Annu. Rev. Immunol. 15:749.
37. Starr, R., T. A. Willson, E. M. Viney, L. J. Murray, J. R. Rayner, B. J. Jenkins, T. J. Gonda, W. S. Alexander, D. Metcalf, N. A. Nicola, and D. J. Hilton. 1997. A family of cytokine-inducible inhibitors of signalling. Nature 387:917.
38. Yasukawa, H., A. Sasaki, and A. Yoshimura. 2000. Negative regulation of cytokine signaling pathways. Annu. Rev. Immunol. 18:143.
39. Alexander, W. S. 2002. Suppressors of cytokine signalling (SOCS) in the immune system. Nat. Rev. Immunol. 2:410.
40. Alexander, W. S., R. Starr, J. E. Fenner, C. L. Scott, E. Handman, N. S. Sprigg, J. E. Corbin, A. L. Cornish, R. Darwiche, C. M. Owczarek, et al. 1999. SOCS1 is a critical inhibitor of interferon-γ signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98:597.
41. Marine, J. C., D. J. Topham, C. McKay, D. Wang, E. Parganas, D. Stravopodis, A. Yoshimura, and J. N. Ihle. 1999. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell 98:609.
42. Dalpke, A. H., S. Opper, S. Zimmermann, and K. Heeg. 2001. Suppressors of cytokine signaling (SOCS)-1 and SOCS-3 are induced by CpG-DNA and modulate cytokine responses in APCs. J. Immunol. 166:7082.
43. Stoiber, D., P. Kovarik, S. Cohney, J. A. Johnston, P. Steinlein, and T. Decker. 1999. Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-γ. J. Immunol. 163:2640.
44. Brysha, M., J. G. Zhang, P. Bertolino, J. E. Corbin, W. S. Alexander, N. A. Nicola, D. J. Hilton, and R. Starr. 2001. Suppressor of cytokine signaling-1 attenuates the duration of interferon-γ signal transduction in vitro and in vivo. J. Biol. Chem. 276:22086.
45. Starr, R., D. Metcalf, A. G. Elefanty, M. Brysha, T. A. Willson, N. A. Nicola, D. J. Hilton, and W. S. Alexander. 1998. Liver degeneration and lymphoid deficiencies in mice lacking suppressor of cytokine signaling-1. Proc. Natl. Acad. Sci. USA 95:14395.
46. Rozell, B., J. A. Barcena, E. Martinez-Galisteo, C. A. Padilla, and A. Holmgren. 1993. Immunochemical characterization and tissue distribution of glutaredoxin (thioltransferase) from calf. Eur. J. Cell Biol. 62:314.
47. Muhlethaler-Mottet, A., W. Di Berardino, L. A. Otten, and B. Mach. 1998. Acfivation of the MHC class II transactivator CIITA by interferon-γ requires cooperative interaction between Stat1 and USF-1. Immunity 8:157.
48. Ting, L. M., A. C. Kim, A. Cattamanchi, and J. D. Ernst. 1999. Mycobacterium tuberculosis inhibits IFN-γ transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163:3898.
49. Young, D. B., and T. R. Garbe. 1991. Lipoprotein antigens of Mycobacterium tuberculosis. Res. Microbiol. 142:55.
50. Neyrolles, O., K. Gould, M. P. Gares, S. Brett, R. Janssen, P. O'Gaora, J. L. Herrmann, M. C. Prevost, E. Perret, J. E. Thole, and D. Young. 2001. Lipoprotein access to MHC class I presentation during infection of murine macrophages with live mycobacteria. J. Immunol. 166:447.
51. Takeuchi, O., S. Sato, T. Horiuchi, K. Hoshino, K. Takeda, Z. Dong, R. L. Modlin, and S. Akira. 2002. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J. Immunol. 169:10.
52. Ozinsky, A., D. M. Underhill, I. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA 97:13766.
53. Siewert, E., W. Muller-Esteri, R. Starr, P. C. Heinrich, and F. Schaper. 1999. Different protein turnover of interleukin-6-type cytokine signalling components. Eur. J. Biochem. 264:251.
54. Liu, B., J. Liao, X. Rao, S. A. Kushner, C. D. Chung, D. D. Chang, and K. Shuai. 1998. Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. USA 95:10626.
55. Liu, B., M. Gross, J. ten Hoeve, and K. Shuai. 2001. A transcriptional corepressor of Stat1 with an essential LXXLL signature motif. Proc. Natl. Acad. Sci. USA 98:3203.
56. Morris, A. C., W. E. Spangler, and J. M. Boss. 2000. Methylation of class II trans-activator promoter IV: a novel mechanism of MHC class II gene control. J. Immunol. 164:4143.
57. Morris, A. C., G. W. Beresford, M. R. Mooney, and J. M. Boss. 2002. Kinetics of a γ-interferon response: expression and assembly of CIITA promoter IV and inhibition by methylation. Mol. Cell. Biol. 22:4781.
58. Pattenden, S. G., R. Klose, E. Karaskov, and R. Bremner. 2002. Interferon-γ-induced chromatin remodeling at the CIITA locus is BRG1 dependent. EMBO J. 21:1978.
59. Landmann, S., A. Muhlethaler-Mottet, L. Bemasconi, T. Suter, J. M. Waldburger, K. Mastemak, J. F. Arrighi, C. Hauser, A. Fontana, and W. Reith. 2001. Maturation of dendritic cells is accompanied by rapid transcriptional silencing of class II transactivator (CIITA) expression. J. Exp. Med. 194:379.
60. Blobel, G. A. 2002. CBP and p300: versatile coregulators with important roles in hematopoietic gene expression. J. Leukocyte Biol. 71:545.
61. Beresford, G. W., and J. M. Boss. 2001. CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter. Nat. Immunol. 2:652.
62. 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.
63. 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.
64. Gehring, A. J., R. E. Rojas, D. H. Canaday, D. L. Lakey, C. V. Harding, and W. H. Boom. 2003. The Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-γ regulated HLA-DR and FcγR1 on human macrophages through TLR-2. Infect. Immun. In press.