STAT activation and differential complex formation dictate selectivity of interferon responses

Acta Biochimica Polonica

Volumn 54, Issue 1, 2007, Pages 27-38

  Wesoly, Joanna ^a   Szweykowska Kulinska, Zofia ^a   Bluyssen, Hans A R ^a  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Gene regulation; IFNs; IRFs; JAK STAT pathway; Transcription factor complexes

Indexed keywords

EID: 33947583705     PISSN: 0001527X     EISSN: 1734154X     Source Type: Journal    
DOI: 10.18388/abp.2007_3266     Document Type: Review

References (87)

1. Barnes B, Lubyova B, Pitha PM (2002) On the role of IRF in host defense. J Interferon Cytokine Res 22: 59-71.
2. Bluyssen HA, Levy DE (1997) Stat2 is a transcriptional activator that requires sequence-specific contacts provided by stat1 and p48 for stable interaction with DNA. J Biol Chem 272: 4600-4605.
3. Bluyssen HA, Muzaffar R, Vlieststra RJ, van der Made AC, Leung S, Stark GR, Kerr IM, Trapman J, Levy DE (1995) Combinatorial association and abundance of components of interferon-stimulated gene factor 3 dictate the selectivity of interferon responses. Proc Natl Acad Sci USA 92: 5645-5649.
4. Bluyssen AR, Durbin JE, Levy DE (1996) ISGF3 gamma p48, a specificity switch for interferon activated transcription factors. Cytokine Growth Factor Rev 7: 11-17.
5. Brierley MM, Fish EN (2005) Functional relevance of the conserved DNA-binding domain of STAT2. J Biol Chem 280: 13029-13036.
6. Brierley MM, Marchington KL, Jurisica I, Fish EN (2006) Identification of GAS-dependent interferon-sensitive target genes whose transcription is STAT2-dependent but ISGF3-independent. FEBS J 273: 1569-1581.
7. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA (1993) Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259: 1739-1742.
8. Darnell JE Jr, Kerr IM, Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421.
9. Decker T, Lew DJ, Cheng YS, Levy DE, Darnell JE Jr (1989) Interactions of alpha- and gamma-interferon in the transcriptional regulation of the gene encoding a guanylate-binding protein. EMBO J 8: 2009-2014.
10. Decker T, Lew DJ, Mirkovitch J, Darnell JE, Jr. (1991) Cytoplasmic activation of GAF, an IFN-gamma-regulated DNA-binding factor. EMBO J 10: 927-932.
11. Decker T, Kovarik P, Meinke A (1997) GAS elements: a few nucleotides with a major impact on cytokine-induced gene expression. J Interferon Cytokine Res 17: 121-134.
12. Decker T, Muller M, Stockinger S (2005) The yin and yang of type I interferon activity in bacterial infection. Nat Rev Immunol 5: 675-687.
13. Durbin JE, Hackenmiller R, Simon MC, Levy DE (1996) Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84: 443-450.
14. Friedman RL, Manly SP, McMahon M, Kerr IM, Stark GR (1984) Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell 38: 745-755.
15. Fu XY, Kessler DS, Veals SA, Levy DE, Darnell JE Jr (1990) ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc Natl Acad Sci USA 87: 8555-8559.
16. Fu XY, Schindler C, Improta T, Aebersold R, Darnell JE Jr (1992) The proteins of ISGF-3, the interferon alpha-induced transcriptional activator, define a gene family involved in signal transduction. Proc Natl Acad Sci USA 89: 7840-7843.
17. Ghislain JJ, Fish EN (1996) Application of genomic DNA affinity chromatography identifies multiple interferon-alpha-regulated Stat2 complexes. J Biol Chem 271: 12408-12413.
18. Ghislain JJ, Wong T, Nguyen M, Fish EN (2001) The interferon-inducible Stat2:Stat1 heterodimer preferentially binds in vitro to a consensus element found in the promoters of a subset of interferon-stimulated genes. J Interferon Cytokine Res 21: 379-388.
19. Grandvaux N, Servant MJ, tenOever B, Sen GC, Balachandran S, Barber GN, Lin R, Hiscott J (2002) Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J Virol 76: 5532-5539.
20. Gupta S, Jiang M, Pernis AB (1999) IFN-alpha activates Stat6 and leads to the formation of Stat2:Stat6 complexes in B cells. J Immunol 163: 3834-3841.
21. Hardy MP, Owczarek CM, Trajanovska S, Liu X, Kola I, Hertzog PJ (2001) The soluble murine type I interferon receptor Ifnar-2 is present in serum, is independently regulated, and has both agonistic and antagonistic properties. Blood 97: 473-482.
22. Honda K, Taniguchi T (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 6: 644-658.
23. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N, Taniguchi T (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777.
24. Horvath CM, Wen Z, Darnell JE Jr (1995) A STAT protein domain that determines DNA sequence recognition suggests a novel DNA-binding domain. Genes Dev 9: 984-994.
25. Horvath CM, Stark GR, Kerr IM, Darnell JE Jr (1996) Interactions between STAT and non-STAT proteins in the interferon-stimulated gene factor 3 transcription complex. Mol Cell Biol 16: 6957-6964.
26. Huang S, Hendriks W, Althage A, Hemmi S, Bluethmann H, Kamijo R, Vilcek J, Zinkernagel RM, Aguet M (1993) Immune response in mice that lack the interferon-gamma receptor. Science 259: 1742-1745.
27. Hwang SY, Hertzog PJ, Holland KA, Sumarsono SH, Tymms MJ, Hamilton JA, Whitty G, Bertoncello I, Kola I (1995) A null mutation in the gene encoding a type I interferon receptor component eliminates antiproliferative and antiviral responses to interferons alpha and beta and alters macrophage responses. Proc Natl Acad Sci USA 92: 11284-11288.
28. Igarashi K, David M, Larner AC, Finbloom DS (1993) In vitro activation of a transcription factor by gamma interferon requires a membrane-associated tyrosine kinase and is mimicked by vanadate. Mol Cell Biol 13: 3984-3989.
29. Isaacs A, Lindenmann J (1957) Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 147: 258-267.
30. Kessler DS, Veals SA, Fu XY, Levy DE (1990) Interferon-alpha regulates nuclear translocation and DNA-binding affinity of ISGF3, a multimeric transcriptional activator. Genes Dev 4: 1753-1765.
31. Khan KD, Shuai K, Lindwall G, Maher SE, Darnell JE Jr, Bothwell AL (1993) Induction of the Ly-6A/E gene by interferon alpha/beta and gamma requires a DNA element to which a tyrosine-phosphorylated 91-kDa protein binds. Proc Natl Acad Sci USA 90: 6806-6810.
32. Kimura T, Kadokawa Y, Harada H, Matsumoto M, Sato M, Kashiwazaki Y, Tarutani M, Tan RS, Takasugi T, Matsuyama T, Mak TW, Noguchi S, Taniguchi T (1996) Essential and non-redundant roles of p48 (ISGF3 gamma) and IRF-1 in both type I and type II interferon responses, as revealed by gene targeting studies. Genes Cells 1: 115-124.
33. Kisseleva T, Bhattacharya S, Braunstein J, Schindler CW (2002) Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene 285: 1-24.
34. Kumatori A, Yang D, Suzuki S, Nakamura M (2002) Cooperation of STAT-1 and IRF-1 in interferon-gamma-induced transcription of the gp91(phox) gene. J Biol Chem 277: 9103-9111.
35. Larner AC, Jonak G, Cheng YS, Korant B, Knight E, Darnell JE Jr (1984) Transcriptional induction of two genes in human cells by beta interferon. Proc Natl Acad Sci USA 81: 6733-6737.
36. Le Bon A, Schiavoni G, D'Agostino G, Gresser I, Belardelli F, Tough DF (2001) Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 14: 461-470.
37. Levy DE, Darnell JE Jr (2002) Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3: 651-662.
38. Levy DE, Lee CK (2002) What does Stat3 do? J Clin Invest 109: 1143-1148.
39. Levy DE, Kessler DS, Pine R, Darnell JE Jr (1989) Cytoplasmic activation of ISGF3, the positive regulator of interferon-alpha-stimulated transcription, reconstituted in vitro. Genes Dev 3: 1362-1371.
40. Levy DE, Lew DJ, Decker T, Kessler DS, Darnell JE Jr (1990) Synergistic interaction between interferon-alpha and interferon-gamma through induced synthesis of one subunit of the transcription factor ISGF3. EMBO J 9: 1105-1111.
41. Lew DJ, Decker T, Darnell JE Jr (1989) Alpha interferon and gamma interferon stimulate transcription of a single gene through different signal transduction pathways. Mol Cell Biol 9: 5404-5411.
42. Lew DJ, Decker T, Strehlow I, Darnell JE (1991) Overlapping elements in the guanylate-binding protein gene promoter mediate transcriptional induction by alpha and gamma interferons. Mol Cell Biol 11: 182-191.
43. Li X, Leung S, Qureshi S, Darnell JE Jr, Stark GR (1996) Formation of STAT1-STAT2 heterodimers and their role in the activation of IRF-1 gene transcription by interferon-alpha. J Biol Chem 271: 5790-5794.
44. Lu B, Ebensperger C, Dembic Z, Wang Y, Kvatyuk M, Lu T, Coffman RL, Pestka S, Rothman PB (1998) Targeted disruption of the interferon-gamma receptor 2 gene results in severe immune defects in mice. Proc Natl Acad Sci USA 95: 8233-8238.
45. Majumder S, Zhou LZ, Chaturvedi P, Babcock G, Aras S, Ransohoff RM (1998) p48/STAT-1alpha-containing complexes play a predominant role in induction of IFN-gamma-inducible protein, 10 kDa (IP-10) by IFN-gamma alone or in synergy with TNF-alpha. J Immunol 161: 4736-4744.
46. Martinez-Moczygemba M, Gutch MJ, French DL, Reich NC (1997) Distinct STAT structure promotes interaction of STAT2 with the p48 subunit of the interferon-alpha-stimulated transcription factor ISGF3. J Biol Chem 272: 20070-20076.
47. Matsumoto M, Tanaka N, Harada H, Kimura T, Yokochi T, Kitagawa M, Schindler C, Taniguchi T (1999) Activation of the transcription factor ISGF3 by interferon-gamma. Biol Chem 380: 699-703.
48. Meraro D, Gleit-Kielmanowicz M, Hauser H, Levi BZ (2002) IFN-stimulated gene 15 is synergistically activated through interactions between the myelocyte/lymphocyte-specific transcription factors, PU.1, IFN regulatory factor-8/IFN consensus sequence binding protein, and IFN regulatory factor-4: characterization of a new subtype of IFN-stimulated response element. J Immunol 168: 6224-6231.
49. Meraz MA, White JM, Sheehan KC, Bach EA, Rodig SJ, Dighe AS, Kaplan DH, Riley JK, Greenlund AC, Campbell D, Carver-Moore K, DuBois RN, Clark R, Aguet M, Schreiber RD (1996) Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84: 431-442.
50. Muller M, Laxton C, Briscoe J, Schindler C, Improta T, Darnell JE Jr, Stark GR, Kerr IM (1993) Complementation of a mutant cell line: central role of the 91 kDa polypeptide of ISGF3 in the interferon-alpha and - gamma signal transduction pathways. EMBO J 12: 4221-4228.
51. Nakaya T, Sato M, Hata N, Asagiri M, Suemori H, Noguchi S, Tanaka N, Taniguchi T (2001) Gene induction pathways mediated by distinct IRFs during viral infection. Biochem Biophys Res Commun 283: 1150-1156.
52. Novick D, Cohen B, Rubinstein M (1994) The human interferon alpha/beta receptor: characterization and molecular cloning. Cell 77: 391-400.
53. Ohmori Y, Hamilton TA (1993) Cooperative interaction between interferon (IFN) stimulus response element and kappa B sequence motifs controls IFN gamma- and lipopolysaccharide-stimulated transcription from the murine IP-10 promoter. J Biol Chem 268: 6677-6688.
54. Ousman SS, Wang J, Campbell IL (2005) Differential regulation of interferon regulatory factor (IRF)-7 and IRF-9 gene expression in the central nervous system during viral infection. J Virol 79: 7514-7527.
55. Park C, Li S, Cha E, Schindler C (2000) Immune response in Stat2 knockout mice. Immunity 13: 795-804.
56. Pearse RN, Feinman R, Ravetch JV (1991) Characterization of the promoter of the human gene encoding the high-affinity IgG receptor: transcriptional induction by gamma-interferon is mediated through common DNA response elements. Proc Natl Acad Sci USA 88: 11305-11309.
57. Pearse RN, Feinman R, Shuai K, Darnell JE Jr, Ravetch JV (1993) Interferon gamma-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: 4314-4318.
58. Pellegrini S, Schindler C (1993) Early events in signalling by interferons. Trends Biochem Sci 18: 338-342.
59. Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202: 8-32.
60. Peters KL, Smith HL, Stark GR, Sen GC (2002) IRF-3-dependent, NFkappa B- and JNK-independent activation of the 561 and IFN-beta genes in response to double-stranded RNA. Proc Natl Acad Sci USA 99: 6322-6327.
61. Platanias LC (2005) Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 5: 375-386.
62. Qing Y, Stark GR (2004) Alternative activation of STAT1 and STAT3 in response to interferon-gamma. J Biol Chem 279: 41679-41685.
63. Qureshi SA, Salditt-Georgieff M, Darnell JE Jr (1995) Tyrosine-phosphorylated Stat1 and Stat2 plus a 48-kDa protein all contact DNA in forming interferon-stimulated-gene factor 3. Proc Natl Acad Sci USA 92: 3829-3833.
64. Ramana CV, Kumar A, Enelow R (2005) Stat1-independent induction of SOCS-3 by interferon-gamma is mediated by sustained activation of Stat3 in mouse embryonic fibroblasts. Biochem Biophys Res Commun 327: 727-733.
65. Reid LE, Brasnett AH, Gilbert CS, Porter AC, Gewert DR, Stark GR, Kerr IM (1989) A single DNA response element can confer inducibility by both alpha- and gamma-interferons. Proc Natl Acad Sci USA 86: 840-844.
66. Sarkis PT, Ying S, Xu R, Yu XF (2006) STAT1-independent cell type-specific regulation of antiviral APOBEC3G by IFN-alpha. J Immunol 177: 4530-4540.
67. Schindler C, Fu XY, Improta T, Aebersold R, Darnell JE Jr (1992a) Proteins of transcription factor ISGF-3: one gene encodes the 91- and 84-kDa ISGF-3 proteins that are activated by interferon alpha. Proc Natl Acad Sci USA 89: 7836-7839.
68. Schindler C, Shuai K, Prezioso VR, Darnell JE Jr (1992b) Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257: 809-813.
69. Sehgal PB (2003) Plasma membrane rafts and chaperones in cytokine/STAT signaling. Acta Biochim Polon 50: 583-594.
70. Seidel HM, Milocco LH, Lamb P, Darnell JE Jr, Stein RB, Rosen J (1995) Spacing of palindromic half sites as a determinant of selective STAT (signal transducers and activators of transcription) DNA binding and transcriptional activity. Proc Natl Acad Sci USA 92: 3041-3045.
71. Servant MJ, Tenoever B, Lin R (2002) Overlapping and distinct mechanisms regulating IRF-3 and IRF-7 function. J Interferon Cytokine Res 22: 49-58.
72. Shuai K, Schindler C, Prezioso VR, Darnell JE Jr (1992) Activation of transcription by IFN-gamma: tyrosine phosphorylation of a 91-kD DNA binding protein. Science 258: 1808-1812.
73. Shuai K, Stark GR, Kerr IM, Darnell JE Jr (1993) A single phosphotyrosine residue of Stat91 required for gene activation by interferon-gamma. Science 261: 1744-1746.
74. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD (1998) How cells respond to interferons. Annu Rev Biochem 67: 227-264.
75. Strehlow I, Seegert D, Frick C, Bange FC, Schindler C, Bottger EC, Decker T (1993) The gene encoding IFP 53/tryptophanyl-tRNA synthetase is regulated by the gamma-interferon activation factor. J Biol Chem 268: 16590-16595.
76. Takaoka A, Yanai H (2006) Interferon signalling network in innate defence. Cell Microbiol 8: 907-922.
77. Takaoka A, Yanai H, Kondo S, Duncan G, Negishi H, Mizutani T, Kano S, Honda K, Ohba Y, Mak TW, Taniguchi T (2005) Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434: 243-249.
78. Taniguchi T, Ogasawara K, Takaoka A, Tanaka N (2001) IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 19: 623-655.
79. Veals SA, Schindler C, Leonard D, Fu XY, Aebersold R, Darnell JE Jr, Levy DE (1992) Subunit of an alpha-interferon-responsive transcription factor is related to interferon regulatory factor and Myb families of DNA-binding proteins. Mol Cell Biol 12: 3315-3324.
80. Veals SA, Santa Maria T, Levy DE (1993) Two domains of ISGF3 gamma that mediate protein-DNA and protein-protein interactions during transcription factor assembly contribute to DNA-binding specificity. Mol Cell Biol 13: 196-206.
81. Vinkemeier U, Cohen SL, Moarefi I, Chait BT, Kuriyan J, Darnell JE Jr (1996) DNA binding of in vitro activated Stat1 alpha, Stat1 beta and truncated Stat1: interaction between NH2-terminal domains stabilizes binding of two dimers to tandem DNA sites. EMBO J 15: 5616-5626.
82. Wagner TC, Velichko S, Vogel D, Rani MR, Leung S, Ransohoff RM, Stark GR, Perez HD, Croze E (2002) Interferon signaling is dependent on specific tyrosines located within the intracellular domain of IFNAR2c. Expression of IFNAR2c tyrosine mutants in U5A cells. J Biol Chem 277: 1493-1499.
83. Xie R, van Wijnen AJ, van Der Meijden C, Luong MX, Stein JL, Stein GS (2001) The cell cycle control element of histone H4 gene transcription is maximally responsive to interferon regulatory factor pairs IRF-1/IRF-3 and IRF-1/IRF-7. J Biol Chem 276: 18624-18632.
84. Xiong H, Zhu C, Li H, Chen F, Mayer L, Ozato K, Unkeless JC, Plevy SE (2003) Complex formation of the interferon (IFN) consensus sequence-binding protein with IRF-1 is essential for murine macrophage IFN-gamma-induced iNOS gene expression. J Biol Chem 278: 2271-2277.
85. Xu X, Sun YL, Hoey T (1996) Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain. Science 273: 794-797.
86. Yang H, Lin CH, Ma G, Baffi MO, Wathelet MG (2003) Interferon regulatory factor-7 synergizes with other transcription factors through multiple interactions with p300/CBP coactivators. J Biol Chem 278: 15495-15504.
87. Zimmermann A, Trilling M, Wagner M, Wilborn M, Bubic I, Jonjic S, Koszinowski U, Hengel H (2005) A cytomegaloviral protein reveals a dual role for STAT2 in IFN-{gamma} signaling and antiviral responses. J Exp med 201: 1543-1553.