Interferon regulatory factor (IRF)-1 and IRF-2 regulate interferon γ- dependent cyclooxygenase 2 expression

Journal of Experimental Medicine

Volumn 191, Issue 12, 2000, Pages 2131-2144

  Blanco, Jorge C G ^a   Contursi, Cristina ^b   Salkowski, Cindy A ^a   DeWitt, David L ^c   Ozato, Keiko ^b   Vogel, Stefanie N ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c Michigan State University   (United States)

Author keywords

Cytokine; Inflammation; Macrophage; Prostaglandin; Septic shock

Indexed keywords

CYCLOOXYGENASE 2; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 2; INTERLEUKIN 1ALPHA; LIPOPOLYSACCHARIDE; PROSTAGLANDIN SYNTHASE;

ANIMAL CELL; ARTICLE; GENE ACTIVATION; GENE MUTATION; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; CYCLOOXYGENASE 2; DNA-BINDING PROTEINS; DRUG SYNERGISM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INTERFERON REGULATORY FACTOR-1; INTERFERON REGULATORY FACTOR-2; INTERFERON TYPE II; INTERLEUKIN-1; ISOENZYMES; LIPOPOLYSACCHARIDES; LIVER; MICE; MICE, MUTANT STRAINS; PHOSPHOPROTEINS; PROMOTER REGIONS (GENETICS); PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PROTEIN BINDING; REPRESSOR PROTEINS; RESPONSE ELEMENTS; SHOCK, SEPTIC; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0034686471     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.12.2131     Document Type: Article

References (80)

1. Smith, W.L. 1992. Prostanoid biosynthesis and mechanisms of action. Am. J. Physiol. 263:F181-F191.
2. Smith, W.L., and D.L. DeWitt. 1995. Biochemistry of prostaglandin endoperoxide H synthase-1 and synthase-2 and their differential susceptibility to nonsteroidal anti-inflammatory drugs. Semin. Nephrol. 15:179-194.
3. Smith, W.L., R.M. Garavito, and D.L. DeWitt. 1996. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J. Biol. Chem. 271:33157-33160.
4. Boehm, U., T. Klamp, M. Groot, and J.C. Howard. 1997. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15:749-795.
5. Mamane, Y., C. Heylbroeck, P. Genin, M. Algarte, M.J. Servant, C. LePage, C. DeLuca, H. Kwon, R. Lin, and J. Hiscott. 1999. Interferon regulatory factors: the next generation. Gene. 237:1-14.
6. Taniguchi, T., M.S. Lamphier, and N. Tanaka. 1997. IRF-1: the transcription factor linking the interferon response and oncogenesis. Biochim. Biophys. Acta. 1333:M9-M17.
7. Harada, H., K. Willison, J. Sakakibara, M. Miyamoto, T. Fujita, and T. Taniguchi. 1990. Absence of the type 1 IFN system in EC cells: transcriptional activator (IRF-1) and repressor (IRF-2) genes are developmentally regulated. Cell. 63: 303-312.
8. Yamamoto, H., M.S. Lamphier, T. Fujita, T. Taniguchi, and H. Harada. 1994. The oncogenic transcription factor IRF-2 possesses a transcriptional repression and a latent activation domain. Oncogene. 9:1423-1428.
9. Levy, D.E. 1998. Analysis of interferon-regulated proteins binding the interferon-alpha-stimulated response element. Methods. 15:167-174.
10. Tanaka, N., T. Kawakami, and T. Taniguchi. 1993. Recognition DNA sequences of interferon regulatory factor 1 (IRF-1) and IRF-2, regulators of cell growth and the interferon system. Mol. Cell. Biol. 13:4531-4538.
11. Kimura, T., K. Nakayama, J. Penninger, M. Kitagawa, H. Harada, T. Matsuyama, N. Tanaka, R. Kamijo, J. Vilcek, T.W. Mak, et al. 1994. Involvement of the IRF-1 transcription factor in antiviral responses to interferons. Science. 264: 1921-1924.
12. Kamijo, R., H. Harada, T. Matsuyama, M. Bosland, J. Gerecitano, D. Shapiro, J. Le, S.I. Koh, T. Kimura, S.J. Green, et al. 1994. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science. 263:1612-1615.
13. Salkowski, C.A., K. Kopydlowski, J. Blanco, M.J. Cody, R. McNally, and S.N. Vogel. 1999. IL-12 is dysregulated in macrophages from IRF-1 and IRF-2 knockout mice. J. Immunol. 163:1529-1536.
14. Salkowski, C.A., S.A. Barber, G.R. Detore, and S.N. Vogel. 1996. Differential dysregulation of nitric oxide production in macrophages with targeted disruptions in IFN regulatory factor-1 and -2 genes. J. Immunol. 156:3107-3110.
15. McIntire, F.C., H.W. Sievert, G.H. Barlow, R.A. Finley, and A. Y. Lee. 1967. Chemical, physical, biological properties of a lipopolysaccharide from Escherichia coli K-235. Biochemistry. 6:2363-2372.
16. Nelson, N., Y. Kanno, C. Hong, C. Contursi, T. Fujita, B.J. Fowlkes, E. O'Connell, J. Hu-Li, W.E. Paul, D. Jankovic, et al. 1996. Expression of IFN regulatory factor family proteins in lymphocytes. Induction of Stat-1 and IFN consensus sequence binding protein expression by T cell activation. J. Immunol. 156:3711-3720.
17. Politis, A.D., K. Ozato, J.E. Coligan, and S.N. Vogel. 1994. Regulation of IFN-gamma-induced nuclear expression of IFN consensus sequence binding protein in murine peritoneal macrophages. J. Immunol. 152:2270-2278.
18. Nogawa, S., C. Forster, F. Zhang, M. Nagayama, M.E. Ross, and C. Iadecola. 1998. Interaction between inducible nitric oxide synthase and cyclooxygenase-2 after cerebral ischemia. Proc. Natl. Acad. Sci. USA. 95:10966-10971.
19. Konecki, D.S., J. Brennand, J.C. Fuscoe, C.T. Caskey, and A.C. Chinault. 1982. Hypoxanthine-guanine phosphoribosyltransferase genes of mouse and Chinese hamster: construction and sequence analysis of cDNA recombinants. Nucleic Acids Res. 10:6763-6775.
20. Kraemer, S.A., K.A. Arthur, M.S. Denison, W.L. Smith, and D.L. De Witt. 1996. Regulation of prostaglandin endoperoxide H synthase-2 expression by 2,3,7,8,-tetrachlorodibenzo-p-dioxin. Arch. Biochem. Biophys. 330:319-328.
21. Medvedev, A.E., J.C. Blanco, N. Qureshi, and S.N. Vogel. 1999. Limited role of ceramide in lipopolysaccharide-mediated mitogen-activated protein kinase activation, transcription factor induction, and cytokine release. J. Biol. Chem. 274: 9342-9350.
22. Wang, I.M., J.C. Blanco, S.Y. Tsai, M.J. Tsai, and K. Ozato. 1996. Interferon regulatory factors and TFIIB cooperatively regulate interferon-responsive promoter activity in vivo and in vitro. Mol. Cell. Biol. 16:6313-6324.
23. Masumi, A., I.M. Wang, B. Lefebvre, X.J. Yang, Y. Nakatani, and K. Ozato. 1999. The histone acetylase PCAF is a phorbol-ester-inducible coactivator of the IRF family that confers enhanced interferon responsiveness. Mol. Cell. Biol. 19:1810-1820.
24. Dignam, J.D., R.M. Lebovitz, and R.G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
25. Bovolenta, C., P.H. Driggers, M.S. Marks, J.A. Medin, A.D. Politis, S.N. Vogel, D.E. Levy, K. Sakaguchi, E. Appella, J.E. Coligan, and K. Ozato. 1994. Molecular interactions between interferon consensus sequence binding protein and members of the interferon regulatory factor family. Proc. Natl. Acad. Sci. USA. 91:5046-5050.
26. Matsuura, H., M. Sakaue, K. Subbaramaiah, H. Kamitani, T.E. Eling, A.J. Dannenberg, T. Tanabe, H. Inoue, J. Arata, and A.M. Jetten. 1999. Regulation of cyclooxygenase-2 by interferon gamma and transforming growth factor alpha in normal human epidermal keratinocytes and squamous carcinoma cells. Role of mitogen-activated protein kinases. J. Biol. Chem. 274:29138-29148.
27. Lakics, V., and S.N. Vogel. 1998. Lipopolysaccharide and ceramide use divergent signaling pathways to induce cell death in murine macrophages. J. Immunol. 161:2490-2500.
28. Barrios-Rodiles, M., G. Tiraloche, and K. Chadee. 1999. Lipopolysaccharide modulates cyclooxygenase-2 transcriptionally and posttranscriptionally in human macrophages independently from endogenous IL-1 beta and TNF-alpha. J. Immunol. 163:963-969.
29. Lee, S.H., E. Soyoola, P. Chanmugam, S. Hart, W. Sun, H. Zhong, S. Liou, D. Simmons, and D. Hwang. 1992. Selective expression of mitogen-inducible cyclooxygenase in macrophages stimulated with lipopolysaccharide. J. Biol. Chem. 267: 25934-25938.
30. Yang, T., D. Sun, Y.G. Huang, A. Smart, J.P. Briggs, and J.B. Schnermann. 1999. Differential regulation of COX-2 expression in the kidney by lipopolysaccharide: role of CD14. Am. J. Physiol. 277:F10-F16.
31. Endo, T., F. Ogushi, and S. Sone. 1996. LPS-dependent cyclooxygenase-2 induction in human monocytes is down-regulated by IL-13, but not by IFN-gamma. J. Immunol. 156: 2240-2246.
32. Inoue, H., and T. Tanabe. 1998. Transcriptional role of the nuclear factor kappa B site in the induction by lipopolysaccharide and suppression by dexamethasone of cyclooxygenase-2 in U937 cells. Biochem. Biophys. Res. Commun. 244: 143-148.
33. O'Banion, M.K., V.D. Winn, and D.A. Young. 1992. cDNA cloning and functional activity of a glucocorticoid-regulated inflammatory cyclooxygenase. Proc. Natl. Acad. Sci. USA. 89: 4888-4892.
34. Ristimaki, A., S. Garfinkel, J. Wessendorf, T. Maciag, and T. Hla. 1994. Induction of cyclooxygenase-2 by interleukin-1 alpha. Evidence for post-transcriptional regulation. J. Biol. Chem. 269:11769-11775.
35. Martin, E., C. Nathan, and Q.W. Xie. 1994. Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J. Exp. Med. 180:977-984.
36. Xie, Q.W., R. Whisnant, and C. Nathan. 1993. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 177:1779-1784.
37. Scharton-Kersten, T., C. Contursi, A. Masumi, A. Sher, and K. Ozato. 1997. Interferon consensus sequence binding protein-deficient mice display impaired resistance to intracellular infection due to a primary detect in interleukin 12 p40 induction J. Exp. Med. 186:1523-1534.
38. Sims, S.H., Y. Cha, M.F. Romine, P.Q. Gao, K. Gottlieb, and A.B. Deisseroth. 1993. A novel interferon-inducible domain: structural and functional analysis of the human interferon regulatory factor 1 gene promoter. Mol. Cell. Biol. 13: 690-702.
39. Coccia, E.M., G. Marziali, E. Stellacci, E. Perrotti, K. Ilari, R. Orsatti, and A. Battistini. 1995. Cells resistant to interferon-beta respond to interferon-gamma via the Stat1-IRF-1 pathway. Virology. 211:113-122.
40. Harada, H., T. Fujita, M. Miyamoto, Y. Kimura, M. Maruyama, A. Furia, T. Miyata, and T. Taniguchi. 1989. Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell. 58:729-739.
41. Quandt, K., K. Frech, H. Karas, E. Wingender, and T. Werner. 1995. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res. 23:4878-4884.
42. Giese, N.A., L. Gabriele, T.M. Doherty, D.M. Klinman, L. Tadesse-Heath, C. Contursi, S.L. Epstein, and H.C. Morse III. 1997. Interferon (IFN) consensus sequence-binding protein, a transcription factor of the IFN regulatory factor family, regulates immune responses in vivo through control of interleukin 12 expression. J. Exp. Med. 186:1535-1546.
43. Gri, G., D. Savio, G. Trinchieri, and X. Ma. 1998. Synergistic regulation of the human interleukin-12 p40 promoter by NFkappaB and Ets transcription factors in Epstein-Barr virus-transformed B cells and macrophages. J. Biol. Chem. 273: 6431-6438.
44. Asano, K., H. Nakamura, C.M. Lilly, M. Klagsbrun, and J.M. Drazen. 1997. Interferon gamma induces prostaglandin G/H synthase-2 through an autocrine loop via the epidermal growth factor receptor in human bronchial epithelial cells. J. Clin. Invest. 99:1057-1063.
45. Riese, J., T. Hoff, A. Nordhoff, D.L. DeWitt, K. Resch, and V. Kaever. 1994. Transient expression of prostaglandin endoperoxide synthase-2 during mouse macrophage activation. J. Leukoc. Biol. 55:476-482.
46. Harada, H., M. Kitagawa, N. Tanaka, H. Yamamoto, K. Harada, M. Ishihara, and T. Taniguchi. 1993. Anti-oncogenic and oncogenic potentials of interferon regulatory factors-1 and -2. Science. 259:971-974.
47. Kargman, S., S. Charleson, M. Cartwright, J. Frank, D. Riendeau, J. Mancini, J. Evans, and G. O'Neill. 1996. Characterization of Prostaglandin G/H Synthase 1 and 2 in rat, dog, monkey, and human gastrointestinal tracts. Gastroenterology. 111:445-454.
48. Eberhart, C.E., R.J. Coffey, A. Radhika, F.M. Giardiello, S. Ferrenbach, and R.N. DuBois. 1994. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology. 107:1183-1188.
49. Kargman, S.L., G.P. O'Neill, P.J. Vickers, J.F. Evans, J.A. Mancini, and S. Jothy. 1995. Expression of prostaglandin G/H synthase-1 and -2 protein in human colon cancer. Cancer Res. 55:2556-2559.
50. Sano, H., Y. Kawahito, R.L. Wilder, A. Hashiramoto, S. Mukai, K. Asai, S. Kimura, H. Kato, M. Kondo, and T. Hla. 1995. Expression of cyclooxygenase-1 and -2 in human colorectal cancer. Cancer Res. 55:3785-3789.
51. Tsujii, M., S. Kawano, and R.N. DuBois. 1997. Cyclooxygenase-2 expression in human colon cancer cells increases metastatic potential. Proc. Natl. Acad. Sci. USA. 94:3336-3340.
52. Tanaka, N., and T. Taniguchi. 1992. Cytokine gene regulation: regulatory cis-elements and DNA binding factors involved in the interferon system. Adv. Immunol. 52:263-281.
53. Lew, D.J., T. Decker, I. Strehlow, and J.E. Darnell. 1991. Overlapping elements in the guanylate-binding protein gene promoter mediate transcriptional induction by alpha and gamma interferons. Mol. Cell. Biol. 11:182-191.
54. Lowenstein, C.J., E.W. Alley, P. Raval, A.M. Snowman, S.H. Snyder, S.W. Russell, and W.J. Murphy. 1993. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. USA. 90:9730-9734.
55. Wadleigh, D.J., S.T. Reddy, E. Kopp, S. Ghosh, and H.R. Herschman. 2000. Transcriptional activation of the cyclooxygenase-2 gene in endotoxin-treated RAW 264.7 macrophages. J. Biol. Chem. 275:6259-6266.
56. D'Acquisto, F., T. Iuvoue, L. Rombola, L. Sautebin, M. Di Rosa, and R. Carnuccio. 1997. Involvement of NF-kappaB in the regulation of cyclooxygenase-2 protein expression in LPS-stimulated J774 macrophages. FEBS Lett. 418:175-178.
57. Browning, J.L., and A. Ribolini. 1987. Interferon blocks interleukin 1-induced prostaglandin release from human peripheral monocytes. J. Immunol. 138:2857-2863.
58. Barrios-Rodiles, M., and K. Chadee. 1998. Novel regulation of cyclooxygenase-2 expression and prostaglandin E2 production by IFN-gamma in human macrophages. J. Immunol. 161: 2441-2448.
59. Kim, Y., and S.M. Fischer. 1998. Transcriptional regulation of cyclooxygenase-2 in mouse skin carcinoma cells. Regulatory role of CCAAT/enhancer-binding proteins in the differential expression of cyclooxygenase-2 in normal and neoplastic tissues. J. Biol. Chem. 273:27686-27694.
60. Xie, W., B.S. Fletcher, R.D. Andersen, and H.R. Herschman. 1994. v-src induction of the Tis10/Pgs2 prostaglandin synthase gene is mediated by an Atf/Cre transcription response element. Mol. Cell. Biol. 14:6531-6539.
61. Xie, W., and H.R. Herschman. 1995. v-src induces prostaglandin synthase 2 gene expression by activation of the c-Jun N-terminal kinase and the c-Jun transcription factor. J. Biol. Chem. 270:27622-27628.
62. Inoue, H., T. Nanayama, S. Hara, C. Yokoyama, and T. Tanabe. 1994. The cyclic AMP response element plays an essential role in the expression of the human prostaglandin-endoperoxide synthase 2 gene in differentiated U937 monocytic cells. FEBS Lett. 350:51-54.
63. Sorli, C.H., H.J. Zhang, M.B. Armstrong, R.V. Rajotte, J. Maclouf, and R.P. Robertson. 1998. Basal expression of cyclooxygenase-2 and nuclear factor-interlenkin 6 are dominant and coordinately regulated by interleukin 1 in the pancreatic islet. Proc. Natl. Acad. Sci. USA. 95:1788-1793.
64. Yamamoto, K., T. Arakawa, N. Ueda, and S. Yamamoto. 1995. Transcriptional roles of nuclear factor kappa B and nuclear factor-interleukin-6 in the tumor necrosis factor alpha-dependent induction of cyclooxygenase-2 in MC3T3-E1 cells. J. Biol. Chem. 270:31315-31320.
65. Struhl, K. 1999. Fundamentally different logic of gene regulation in eukaryotes and prokaryotes. Cell. 98:1-4.
66. Fujita, T., L.F. Reis, N. Watanabe, Y. Kimura, T. Taniguchi, and J. Vilcek. 1989. Induction of the transcription factor IRF-1 and interferon-beta mRNAs by cytokines and activators of second-messenger pathways. Proc. Natl. Acad. Sci. USA. 86: 9936-9940.
67. Watanabe, N., J. Sakakibara, A.G. Hovanessian, T. Taniguchi, and T. Fujita. 1991. Activation of IFN-beta element by IRF-1 requires a posttranslational event in addition to IRF-1 synthesis. Nucleic Acids Res. 19:4421-4428.
68. Coccia, E.M., N. Passini, A. Battistini, C. Pini, F. Sinigaglia, and L. Rogge. 1999. Interleukin-12 induces expression of interferon regulatory factor-1 via signal transducer and activator of transcription-4 in human T helper type 1 cells. J. Biol. Chem. 274:6698-6703.
69. Galon, J., C. Sudarshan, S. Ito, D. Finbloom, and J.J. O'Shea. 1999. IL-12 induces IFN regulating factor-1 (IRF-1) gene expression in human NK and T cells. J. Immunol. 162:7256-7262.
70. Barber, S.A., M.J. Fultz, C.A. Salkowski, and S.N. Vogel. 1995. Differential expression of interferon regulatory factor 1 (IRF-1), IRF-2, and interferon consensus sequence binding protein genes in lipopolysaccharide (LPS)-responsive and LPS-hyporesponsive macrophages. Infect. Immun. 63:601-608.
71. Xie, Q.W., Y. Kashiwabara, and C. Nathan. 1994. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269:4705-4708.
72. Vodovotz, Y., C. Bogdan, J. Paik, Q.W. Xie, and C. Nathan. 1993. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor beta. J. Exp. Med. 178: 605-613.
73. Vodovotz, Y., N.S. Kwon, M. Pospischil, J. Manning, J. Paik, and C. Nathan. 1994. Inactivation of nitric oxide synthase after prolonged incubation of mouse macrophages with IFN-gamma and bacterial lipopolysaccharide. J. Immunol. 152: 4110-4118.
74. Ding, A.H., C.F. Nathan, and D.J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141:2407-2412.
75. Contursi, C., I.M. Wang, L. Gabriele, M. Gadina, J. O'Shea, H.C. Morse III, and K. Ozato. 2000. IFN consensus sequence binding protein potentiates STAT1-dependent activation of IFNgamma-responsive promoters in macrophages. Proc. Natl. Acad. Sci. USA. 97:91-96.
76. Iadecola, C., C. Forster, S. Nogawa, H.B. Clark, and M.E. Ross. 1999. Cyclooxygenase-2 immunoreactivity in the human brain following cerebral ischemia. Acta Neuropathol. 98: 9-14.
77. Miettinen, S., F.R. Fusco, J. Yrjanheikki, R. Keinanen, T. Hirvonen, R. Roivainen, M. Narhi, T. Hokfelt, and J. Koistinaho. 1997. Spreading depression and focal brain ischemia induce cyclooxygenase-2 in cortical neurons through N-methyl-D-aspartic acid-receptors and phospholipase A2. Proc. Natl. Acad. Sci. USA. 94:6500-6505.
78. Nogawa, S., F. Zhang, M.E. Ross, and C. Iadecola. 1997. Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J. Neurosci. 17:2746-2755.
79. Iadecola, C., C.A. Salkowski, F. Zhang, T. Aber, M. Nagayama, S.N. Vogel, and M.E. Ross. 1999. The transcription factor interferon regulatory factor 1 is expressed after cerebral ischemia and contributes to ischemic brain injury. J. Exp. Med. 189:719-727.
80. Senaldi, G., C.L. Shaklee, J. Guo, L. Martin, T. Boone, T.W. Mak, and T.R. Ulich. 1999. Protection against the mortality associated with disease models mediated by TNF and IFN-gamma in mice lacking IFN regulatory factor-1. J. Immunol. 163:6820-6826.