Modulation of gamma interferon receptor 1 by Mycobacterium tuberculosis: A potential immune response evasive mechanism

Infection and Immunity

Volumn 75, Issue 5, 2007, Pages 2500-2510

  Singhal, Amit ^a   Jaiswal, Anand ^b   Arora, Virendra K ^b   Prasad, Hanumanthappa K ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^b LRS Hospital of Tuberculosis and Allied Disease   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; GAMMA INTERFERON RECEPTOR; PHORBOL 13 ACETATE 12 MYRISTATE; PHORBOL ESTER DERIVATIVE; TUBERCULOSTATIC AGENT;

ARTICLE; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; GENE CONSTRUCT; GENE DELETION; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOBLOTTING; IMMUNOMODULATION; LUNG TUBERCULOSIS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; STATISTICAL SIGNIFICANCE;

ANTIGENS, CD14; CELL LINE; CELLS, CULTURED; DOWN-REGULATION; HUMANS; LEUKOCYTES, MONONUCLEAR; MYCOBACTERIUM TUBERCULOSIS; RECEPTORS, INTERFERON; TUBERCULOSIS, PULMONARY;

EID: 34248395113     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01743-06     Document Type: Article

References (65)

1. Aaronson, D. S., and C. M. Horvath. 2002. A road map for those who don't know JAK-STAT. Science 296:1653-1655.
2. Abou-Zeid, C., T. L. Ratliff, H. G. Wiker, M. Harboe, J. Bennedsen, and G. A. Rook. 1988. Characterization of fibronectin-binding antigens released by Mycobacterium tuberculosis and Mycobacterium bovis BCG. Infect. Immun. 56:3046-3051.
3. Anderson, G. M., and S. O. Freytag. 1991. Synergistic activation of a human promoter in vivo by transcription factor Sp1. Mol. Cell. Biol. 11:1935-1943.
4. Ansari, N. A., V. Ramesh, and P. Salotra. 2006. Interferon (IFN)-γ, tumor necrosis factor-α, interleukin-6, and IFN-γ receptor 1 are the major immunological determinants associated with post-kala azar dermal leishmaniasis. J. Infect. Dis. 194:958-965.
5. Aoki, K., S. Matsumoto, Y. Hirayama, T. Wada, Y. Ozeki, M. Niki, P. Domenech, K. Umemori, S. Yamamoto, A. Mineda, M. Matsumoto, and K. Kobayashi. 2004. Extracellular mycobacterial DNA-binding protein 1 participates in mycobacterium-lung epithelial cell interaction through hyaluronic acid. J. Biol. Chem. 279:39798-39806.
6. Bach, E. A., M. Auget, and R. D. Schreiber. 1997. The IFN-γ receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15:563-591.
7. 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. 61:3482-3489.
8. Bhattacharyya, S., R. Singla, A. B. Dey, and H. K. Prasad. 1999. Dichotomy of cytokine profiles in patients and high-risk healthy subjects exposed to tuberculosis. Infect. Immun. 67:5597-5603.
9. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Chatterji, U., J. E. Riby, T. Taniguchi, E. L. Bjeldanes, L. F. Bjeldanes, and G. L. Firestone. 2004. Indole-3-carbinol stimulates transcription of the interferon gamma receptor 1 gene and augments interferon responsiveness in human breast cancer cells. Carcinogenesis 25:1119-1128.
11. Chen, G. H., R. A. McDonald, J. C. Wells, G. B. Huffnagle, N. W. Lukacs, and G. B. Toews. 2005. The gamma interferon receptor is required for the protective pulmonary inflammatory response to Cryptococcus neoformans. Infect. Immun. 73:1788-1796.
12. Coccia, E. M., N. D. Russo, E. Stellacci, U. Testa, G. Marziali, and A. Battistini. 1999. STAT1 activation during monocyte to macrophage maturation: role of adhesion molecules. Int. Immunol. 11:1075-1083.
13. 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. 178:2243-2247.
14. Cox, R. A. 2004. Quantitative relationships for specific growth rates and macromolecular compositions of Mycobacterium tuberculosis, Streptomyces coelicolor A3(2) and Escherichia coli B/r: an integrative theoretical approach. Microbiology 150:1413-1426.
15. Curry, H., G. R. Alvarez, B. S. Zwilling, and W. P. Lafuse. 2004. Toll-like receptor 2 stimulation decreases IFN-gamma receptor expression in mouse RAW264.7 macrophages. J. Interferon Cytokine Res. 24:699-710.
16. Dasgupta, B., K. Roychoudhury, S. Ganguly, P. K. Sinha, S. Vimal, P. Das, and S. Roy. 2003. Antileishmanial drugs cause up-regulation of interferon-gamma receptor 1, not only in the monocytes of visceral leishmaniasis cases but also in cultured THP-1 cells. Ann. Trop. Med. Parasitol. 97:245-257.
17. Dorman, S. E., C. Picard, D. Lammas, K. Heyne, J. T. van Dissel, R. Baretto, S. D. Rosenzweig, M. Newport, M. Levin, J. Roesler, D. Kumararatne, J. L. Casanova, and S. M. Holland. 2004. Clinical features of dominant and recessive IFN-γ receptor 1 deficiencies. Lancet 364:2113-2121.
18. Flynn, J. L., and J. Chan. 2003. Immune evasion by Mycobacterium tuberculosis: living with the enemy. Curr. Opin. Immunol. 15:450-455.
19. 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. 178:2249-2254.
20. Foster, N., S. D. Hulme, and P. A. Barrow. 2003. Induction of antimicrobial pathways during early-phase immune response to Salmonella spp. in murine macrophages: gamma interferon (IFN-γ) and upregulation of IFN-γ receptor alpha expression are required for NADPH phagocytic oxidase gp91-stimulated oxidative burst and control of virulent Salmonella spp. Infect. Immun. 71:4733-4741.
21. Hmama, Z., R. Gabathuler, W. A. Jefferies, G. D. Jong, and N. E. Reiner. 1998. Attenuation of HLADR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J. Immunol. 161:4882-4893.
22. Hussain, S., B. S. Zwilling, and W. P. Lafuse. 1999. Mycobacterium avium infection of mouse macrophages inhibits IFN-γ Janus kinase-STAT signaling and gene induction by down regulation of IFN-γ receptor. J. Immunol. 163:2041-2048.
23. Kierszenbaum, F., H. M. Lopez, M. K. Tanner, and M. B. Sztein. 1995. Trypanosoma cruzi-induced decrease in the level of interferon-γ receptor expression by resting and activated blood lymphocytes. Parasite Immunol. 17:207-214.
24. Kincaid, E. Z., and J. D. Ernst. 2003. Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-gamma without inhibiting STAT1 function. J. Immunol. 171:2042- 2049.
25. Kinhikar, A. G., D. Varagas, H. Li, S. B. Mahaffey, L. Hinds, J. T. Belisle, and S. Laal. 2006. Mycobacterium tuberculosis malate synthase is a laminin-binding adhesin. Mol. Microbiol. 60:999-1013.
26. Krakauer, T., and J. J. Oppenheim. 1993. IL-1 and tumor necrosis factor-alpha each up-regulate both the expression of IFN-gamma receptors and enhance IFN-gamma-induced HLA-DR expression on human monocytes and a human monocytic cell line (THP-1). J. Immunol. 150:1205-1211.
27. Langmann, T., C. Buechler, S. Ries, A. Schaeffler, C. Aslanidis, M. Schuierer, M. Weiler, K. Sandhoff, P. J. de Jong, and G. Schmitz. 1999. Transcription factors Sp1 and AP-2 mediate induction of acid sphingomyelinase during monocytic differentiation. J. Lipid Res. 40:870-880.
28. 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 98:3203-3207.
29. Liu, S., R. A. Shapiro, S. Nie, D. Zhu, Y. Vodovotz, and T. R. Billiar. 2000. Characterization of rat CD14 promoter and its regulation by transcription factors AP1 and Sp family proteins in hepatocytes. Gene 250:137-147.
30. López, M., L. M. Sly, Y. Luu, D. Young, H. Cooper, and N. E. Reiner. 2003. The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J. Immunol. 170:2409-2416.
31. Matsuura, K., T. Ishida, M. Setoguchi, Y. Higuchi, S. Akizuki, and S. Yamamoto. 1992. Identification of a tissue-specific regulatory element within the murine CD14 gene. J. Biol. Chem. 267:21787-21794.
32. Menozzi, F. D., J. H. Rouse, M. Alavi, M. Laude-Sharp, J. Muller, R. Bischoff, M. J. Brennan, and C. Locht. 1996. Identification of a heparin-binding hemagglutinin present in mycobacteria. J. Exp. Med. 184:993-1001.
33. Mitani, Y., A. Takakoa, S. H. Kim, Y. Kato, T. Yokochi, N. Tanaka, and T. Taniguchi. 2001. Cross talk of the interferon-α/β signaling complex with gp130 for effective interleukin-6 signaling. Genes Cells 6:631-640.
34. Nagabhushanam, V., A. Solache, L. M. Ting, C. J. Escaron, J. Y. Zhang, and J. D. Ernst. 2003. Innate inhibition of adaptive immunity: Mycobacterium tuberculosis-induced IL-6 inhibits macrophage responses to IFN-gamma. J. Immunol. 171:4750-4757.
35. Nagao, M., Y. Nakajima, H. Kanehiro, M. Hisanaga, Y. Aomatsu, S. Ko, Y. Tatekawa, N. Ikeda, H. Kanokogi, Y. Urizono, T. Kobayashi, T. Shibaji, T. Kanamura, S. Ogawa, and H. Nakano. 2000. The impact of interferon gamma receptor expression on the mechanism of escape from host immune surveillance in hepatocellular carcinoma. Hepatology 32:491-500.
36. Nathan, C. F., T. J. Prendergast, M. E. Wiebe, E. R. Stanely, E. Platzer, H. G. Renold, K. Welte, B. Y. Rubin, and H. W. Murray. 1984. Activation of human macrophages: comparison of other cytokines with interferon-γ. J. Exp. Med. 160:600-605.
37. Pestka, S., S. V. Kotenko, G. Muthukumaran, L. S. Izotova, J. R. Cook, and G. Garotta. 1997. The interferon gamma (IFN-γ) receptor: a paradigm for the multichain cytokine receptor. Cytokine Growth Factor Rev. 8:189-206.
38. Pfizenmaier, K., K. Wiegmann, P. Scheurich, S. Hemmi, H. Blucthmann, R. Kamije, J. Vileck, R. M. Zinkerngel, and M. Aguet. 1988. High affinity human IFN-gamma-binding capacity is encoded by a single receptor gene located in proximity to c-ras on human chromosome region 6q16 to 6q22. J. Immunol. 141:856-860.
39. Philipsen, S., and G. Suske. 1999. A tale of three fingers: the family of mammalian Sp/XKLF transcription factors. Nucleic Acids Res. 27:2991-3000.
40. Ramana, C. V., M. Chatterjee-Kishore, H. Nguyen, and G. R. Stark. 2000. Complex roles of Stat1 in regulating gene expression. Oncogene 19:2619-2627.
41. Ramana, C. V., M. P. Gil, R. D. Schreiber, and G. R. Stark. 2002. Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling. Trends Immunol. 23:96-101.
42. Raval, P., S. Obici, S. A. Russel, and W. J. Murphy. 1995. Characterization of the 5′ flanking region and gene encoding the mouse interferon-gamma receptor. Gene 154:219-223.
43. Ray, M., A. A. Gam, R. A. Boukins, and R. T. Kenny. 2000. Inhibition of interferon-γ signaling by Leishmania donovani. J. Infect. Dis. 181:1121-1128.
44. Rivera-Marrero, C. A., W. Schuyler, S. Roser, J. D. Ritzenthaler, S. A. Newburn, and J. Roman. 2002. M. tuberculosis induction of matrix metalloproteinase-9: the role of mannose and receptor-mediated mechanisms. Am. J. Physiol. Lung Cell. Mol. Physiol. 282:L546-L555.
45. Roder, K., S. S. Wolf, K. F. Beck, S. Sickinger, and M. Schweizer. 1997. NF-Y binds to the inverted CCAAT box, an essential element for cAMP-dependent regulation of the rat fatty acid synthase (FAS) gene. Gene (Amsterdam) 184:21-26.
46. Rugeles, M. T., B. Rincon, C. Rugeles, C. J. Montoya, M. Hernandez, C. Estrada, M. M. Olivares, and P. J. Patino. 2004. Normal expression of IFN-γR in four patients with uncommon mycobacterial infection phenotypes. Braz. J. Med. Biol. Res. 37:1353-1363.
47. Saidi, R. F., F. Williams, J. Ng, G. Danquah, V. K. Mittal, S. G. ReMine, and M. J. Jacobs. 2006. Interferon receptors and the caspase cascade regulate the antitumor effects of interferons on human pancreatic cancer cell lines. Am. J. Surg. 191:358-363.
48. Sakamoto, S., J. Nie, and T. Taniguchi. 1999. Cutting edge: phorbol ester induction of IFN-γ receptors leads to enhanced DRα gene expression. J. Immunol. 162:4381-4384.
49. Sakamoto, S., and T. Taniguchi. 2001. Identification of a phorbol ester responsive element in the interferon-γ receptor 1 chain gene. J. Biol. Chem. 276:37327-37341.
50. 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. 181:1506-1509.
51. Schaber, J. D., H. Fang, J. Xu, P. M. Grimley, and H. Pwi. 1998. Prolactin activates STAT1 but does not antagonize STAT1 activation and growth inhibition by type I interferons in human breast cancer cells. Cancer Res. 58:1914-1919.
52. Schorey, J. S., M. A. Holsti, T. L. Ratliff, P. M. Allen, and E. J. Brown. 1996. Characterization of the fibronectin-attachment protein of Mycobacterium avium reveals a fibronectin-binding motif conserved among mycobacteria. Mol. Microbiol. 21:321-329.
53. Shimoji, Y., V. Ng, K. Matsumura, V. A. Fischetti, and A. Rambukkana. 1999. A 21-kDa surface protein of Mycobacterium leprae binds peripheral nerve laminin-2 and mediates Schwann cell invasion. Proc. Natl. Acad. Sci. USA 96:9857-9862.
54. Shirey, K. A., J. Y. Jung, G. S. Maeder, and J. M. Carlin. 2006. Upregulation of IFN-gamma receptor expression by proinflammatory cytokines influences IDO activation in epithelial cells. J. Interferon Cytokine Res. 26:53-62.
55. Shirey, K. A., J. Y. Jung, and J. M. Carlin. 2006. Up-regulation of gamma interferon receptor expression due to Toll-like receptor interaction does not enhance signaling of signal transducer and activator of transcription 1. Infect. Immun. 74:6877-6884.
56. Sibley, L. D., L. B. Adams, and J. L. Krahenbhul. 1990. Inhibition of interferon-γ-mediated activation in mouse macrophages treated with lipoarabinomannan. Clin. Exp. Immunol. 80:141-148.
57. Spanopoulou, E., V. Giguere, and F. Grosveld. 1991. The functional domain of the murine Thy-1 gene promoter. Mol. Cell. Biol. 11:2216-2228.
58. Ström, A. C., M. Forsberg, P. Lillhager, and G. Westin. 1996. The transcription factors Sp1 and Oct-1 interact physically to regulate human U2 snRNA gene expression. Nucleic Acids Res. 24:1981-1986.
59. Takaoka, A., Y. Mitani, H. Suemori, M. Sato, T. Yokochi, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Cross talk between interferon-γ and -α/β signaling components in caveolar membrane domains. Science 288:2357-2360.
60. Tassiulas, I., X. Hu, H. Ho, Y. Kashyap, P. Paik, Y. Hu, C. L. Lowell, and L. B. Ivashkiv. 2004. Amplification of IFN-α-induced STAT1 activation and inflammatory function by Syk and ITAM-containing adaptors. Nat. Immunol. 5:1181-1189.
61. Ting, L. M., A. C. Kim, A. Chattamanchi, and J. D. Ernst. 1999. Mycobacterium tuberculosis inhibits IFN-γ transcriptional responses without inhibiting activation of STAT-1. J. Immunol. 163:3898-3906.
62. Valente, G., L. Ozmen, F. Novelli, M. Genuna, G. Palestro, G. Formi, and G. Garetta. 1992. Distribution of IFN-γ receptor in human tissues. Eur. J. Immunol. 22:2403-2412.
63. Wang, Y., H. M. Curry, B. S. Zwilling, and W. P. Lafuse. 2005. Mycobacteria inhibition of IFN-γ induced HLADR gene expression by up-regulating histone deacetylation at the promoter region in human THP-1 monocytic cells. J. Immunol. 174:5687-5694.
64. Zhang, D. E., C. J. Hetherington, S. Tan, S. E. Dziemis, D. A. Gonzalez, H. Chen, and D. G. Tenen. 1994. Sp1 is a critical factor for the monocytic specific expression of human CD14. J. Biol. Chem. 269:11425- 11434.
65. Zhang, Y., M. Broser, and W. N. Rom. 1994. Activation of the interleukin 6 gene by Mycobacterium tuberculosis or lipopolysaccharide is mediated by nuclear factors NF-IL6 and NF-κB. Proc. Natl. Acad. Sci. USA 91:2225-2229.