Nonconventional initiation complex assembly by STAT and NF-κB transcription factors regulates nitric oxide synthase expression

Immunity

Volumn 33, Issue 1, 2010, Pages 25-34

  Farlik, Matthias ^a   Reutterer, Benjamin ^a   Schindler, Christian ^b   Greten, Florian ^c   Vogl, Claus ^d   Müller, Mathias ^d   Decker, Thomas ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Molimmuno; RNA; Signaling

Indexed keywords

CYCLIN DEPENDENT KINASE 7; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 9; INTERFERON STIMULATED GENE FACTOR 3; RNA POLYMERASE II; STAT PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; TRANSCRIPTION FACTOR IIH;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION;

ANIMALS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INTERFERON TYPE I; INTERFERON-STIMULATED GENE FACTOR 3; LISTERIA INFECTIONS; LISTERIA MONOCYTOGENES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; PROTEIN BINDING; RNA POLYMERASE II; STAT TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR TFIIH;

EID: 77954917130     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.07.001     Document Type: Article

References (53)

1. Adelman K., Kennedy M.A., Nechaev S., Gilchrist D.A., Muse G.W., Chinenov Y., Rogatsky I. Immediate mediators of the inflammatory response are poised for gene activation through RNA polymerase II stalling. Proc. Natl. Acad. Sci. USA 2009, 106:18207-18212.
2. Baccarini M., Bistoni F., Lohmann Matthes M.L. In vitro natural cell-mediated cytotoxicity against Candida albicans: Macrophage precursors as effector cells. J. Immunol. 1985, 134:2658-2665.
3. Barbalat R., Lau L., Locksley R.M., Barton G.M. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 2009, 10:1200-1207.
4. Bogdan C. Nitric oxide and the immune response. Nat. Immunol. 2001, 2:907-916.
5. Chapman R.D., Heidemann M., Hintermair C., Eick D. Molecular evolution of the RNA polymerase II CTD. Trends Genet. 2008, 24:289-296.
6. Chen L.F., Greene W.C. Shaping the nuclear action of NF-kappaB. Nat. Rev. Mol. Cell Biol. 2004, 5:392-401.
7. Darnell J.E. STATs and gene regulation. Science 1997, 277:1630-1635.
8. Dempsey P.W., Doyle S.E., He J.Q., Cheng G. The signaling adaptors and pathways activated by TNF superfamily. Cytokine Growth Factor Rev. 2003, 14:193-209.
9. Doyle S., Vaidya S., O'Connell R., Dadgostar H., Dempsey P., Wu T., Rao G., Sun R., Haberland M., Modlin R., Cheng G. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 2002, 17:251-263.
10. Durbin J.E., Hackenmiller R., Simon M.C., Levy D.E. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 1996, 84:443-450.
11. Edelson B.T., Unanue E.R. MyD88-dependent but Toll-like Receptor 2-independent innate immunity to Listeria: No role for either in macrophage listericidal activity. J. Immunol. 2002, 169:3869-3875.
12. Egly J.M. The 14th Datta Lecture. TFIIH: From transcription to clinic. FEBS Lett. 2001, 498:124-128.
13. Gao J.J., Filla M.B., Fultz M.J., Vogel S.N., Russell S.W., Murphy W.J. Autocrine/paracrine IFN-alphabeta mediates the lipopolysaccharide-induced activation of transcription factor Stat1alpha in mouse macrophages: pivotal role of Stat1alpha in induction of the inducible nitric oxide synthase gene. J. Immunol. 1998, 161:4803-4810.
14. Greten F.R., Arkan M.C., Bollrath J., Hsu L.C., Goode J., Miething C., Goktuna S.I., Neuenhahn M., Fierer J., Paxian S., et al. NF-kappaB is a negative regulator of IL-1beta secretion as revealed by genetic and pharmacological inhibition of IKKbeta. Cell 2007, 130:918-931.
15. Harada H., Matsumoto M., Sato M., Kashiwazaki Y., Kimura T., Kitagawa M., Yokochi T., Tan R.S., Takasugi T., Kadokawa Y., et al. Regulation of IFN-alpha/beta genes: evidence for a dual function of the transcription factor complex ISGF3 in the production and action of IFN-alpha/beta. Genes Cells 1996, 1:995-1005.
16. Herskovits A.A., Auerbuch V., Portnoy D.A. Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system. PLoS Pathog. 2007, 3:e51.
17. Hirose Y., Ohkuma Y. Phosphorylation of the C-terminal domain of RNA polymerase II plays central roles in the integrated events of eucaryotic gene expression. J. Biochem. 2007, 141:601-608.
18. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., Taniguchi T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777.
19. Kagan J.C., Su T., Horng T., Chow A., Akira S., Medzhitov R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat. Immunol. 2008, 9:361-368.
20. Kamijo R., Harada H., Matsuyama T., Bosland M., Gerecitano J., Shapiro D., Le J., Koh S.I., Kimura T., Green S.J., et al. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 1994, 263:1612-1615.
21. Kim Y.K., Bourgeois C.F., Pearson R., Tyagi M., West M.J., Wong J., Wu S.Y., Chiang C.M., Karn J. Recruitment of TFIIH to the HIV LTR is a rate-limiting step in the emergence of HIV from latency. EMBO J. 2006, 25:3596-3604.
22. Kleinert H., Schwarz P.M., Forstermann U. Regulation of the expression of inducible nitric oxide synthase. Biol. Chem. 2003, 384:1343-1364.
23. Koch F., Jourquin F., Ferrier P., Andrau J.C. Genome-wide RNA polymerase II: Not genes only!. Trends Biochem. Sci. 2008, 33:265-273.
24. Kovarik P., Stoiber D., Novy M., Decker T. Stat1 combines signals derived from IFN-gamma and LPS receptors during macrophage activation. EMBO J. 1998, 17:3660-3668.
25. Lau J.F., Nusinzon I., Burakov D., Freedman L.P., Horvath C.M. Role of metazoan mediator proteins in interferon-responsive transcription. Mol. Cell. Biol. 2003, 23:620-628.
26. Lowenstein C.J., Alley E.W., Raval P., Snowman A.M., Snyder S.H., Russell S.W., Murphy W.J. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 1993, 90:9730-9734.
27. Margaritis T., Holstege F.C. Poised RNA polymerase II gives pause for thought. Cell 2008, 133:581-584.
28. Meraz M.A., White J.M., Sheehan K.C., Bach E.A., Rodig S.J., Dighe A.S., Kaplan D.H., Riley J.K., Greenlund A.C., Campbell D., et al. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 1996, 84:431-442.
29. Muller U., Steinhoff U., Reis L.F., Hemmi S., Pavlovic J., Zinkernagel R.M., Aguet M. Functional role of type I and type II interferons in antiviral defense. Science 1994, 264:1918-1921.
30. Nissen R.M., Yamamoto K.R. The glucocorticoid receptor inhibits NFkappaB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 2000, 14:2314-2329.
31. Nusinzon I., Horvath C.M. Histone deacetylases as transcriptional activators? Role reversal in inducible gene regulation. Sci. STKE 2005, 2005:re11.
32. Pandey A.K., Yang Y., Jiang Z., Fortune S.M., Coulombe F., Behr M.A., Fitzgerald K.A., Sassetti C.M., Kelliher M.A. NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog. 2009, 5:e1000500.
33. Parekh B.S., Maniatis T. Virus infection leads to localized hyperacetylation of histones H3 and H4 at the IFN-beta promoter. Mol. Cell 1999, 3:125-129.
34. Park C., Li S., Cha E., Schindler C. Immune response in Stat2 knockout mice. Immunity 2000, 13:795-804.
35. Paulson M., Press C., Smith E., Tanese N., Levy D.E. IFN-Stimulated transcription through a TBP-free acetyltransferase complex escapes viral shutoff. Nat. Cell Biol. 2002, 4:140-147.
36. Plumlee C.R., Lee C., Beg A.A., Decker T., Shuman H.A., Schindler C. Interferons direct an effective innate response to Legionella pneumophila infection. J. Biol. Chem. 2009, 284:30058-30066.
37. Ramsauer K., Farlik M., Zupkovitz G., Seiser C., Kroger A., Hauser H., Decker T. Distinct modes of action applied by transcription factors STAT1 and IRF1 to initiate transcription of the IFN-gamma-inducible gbp2 gene. Proc. Natl. Acad. Sci. USA 2007, 104:2849-2854.
38. Reis L.F., Ruffner H., Stark G., Aguet M., Weissmann C. Mice devoid of interferon regulatory factor 1 (IRF-1) show normal expression of type I interferon genes. EMBO J. 1994, 13:4798-4806.
39. Roeder R.G. The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem. Sci. 1996, 21:327-335.
40. Sato M., Suemori H., Hata N., Asagiri M., Ogasawara K., Nakao K., Nakaya T., Katsuki M., Noguchi S., Tanaka N., Taniguchi T. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000, 13:539-548.
41. Schindler C., Levy D.E., Decker T. JAK-STAT signaling: From interferons to cytokines. J. Biol. Chem. 2007, 282:20059-20063.
42. Spilianakis C., Kretsovali A., Agalioti T., Makatounakis T., Thanos D., Papamatheakis J. CIITA regulates transcription onset via Ser5-phosphorylation of RNA Pol II. EMBO J. 2003, 22:5125-5136.
43. Spink J., Evans T. Binding of the transcription factor interferon regulatory factor 1 to the inducible nitric oxide synthase promoter. J. Biol. Chem. 1997, 272:24417-24425.
44. Stetson D.B., Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 2006, 24:93-103.
45. Stockinger S., Materna T., Stoiber D., Bayr L., Steinborn R., Kolbe T., Unger H., Chakraborty T., Levy D.E., Muller M., Decker T. Production of type I IFN sensitizes macrophages to cell death induced by Listeria monocytogenes. J. Immunol. 2002, 169:6522-6529.
46. Stockinger S., Reutterer B., Schaljo B., Schellack C., Brunner S., Materna T., Yamamoto M., Akira S., Taniguchi T., Murray P.J., et al. IFN regulatory factor 3-dependent induction of type I IFNs by intracellular bacteria is mediated by a TLR- and Nod2-independent mechanism. J. Immunol. 2004, 173:7416-7425.
47. Stockinger S., Kastner R., Kernbauer E., Pilz A., Westermayer S., Reutterer B., Soulat D., Stengl G., Vogl C., Frenz T., et al. Characterization of the interferon-producing cell in mice infected with Listeria monocytogenes. PLoS Pathog. 2009, 5:e1000355.
48. Toshchakov V., Jones B.W., Perera P.Y., Thomas K., Cody M.J., Zhang S., Williams B.R., Major J., Hamilton T.A., Fenton M.J., Vogel S.N. TLR4, but not TLR2, mediates IFN-beta-induced STAT1alpha/beta-dependent gene expression in macrophages. Nat. Immunol. 2002, 3:392-398.
49. Varinou L., Ramsauer K., Karaghiosoff M., Kolbe T., Pfeffer K., Muller M., Decker T. Phosphorylation of the Stat1 transactivation domain is required for full-fledged IFN-gamma-dependent innate immunity. Immunity 2003, 19:793-802.
50. Xie Q.W., Whisnant R., Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J. Exp. Med. 1993, 177:1779-1784.
51. Xie Q.W., Kashiwabara Y., Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J. Biol. Chem. 1994, 269:4705-4708.
52. Zhong H., May M.J., Jimi E., Ghosh S. The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol. Cell 2002, 9:625-636.
53. Zwaferink H., Stockinger S., Reipert S., Decker T. Stimulation of inducible nitric oxide synthase expression by beta interferon increases necrotic death of macrophages upon Listeria monocytogenes infection. Infect. Immun. 2008, 76:1649-1656.