Structural basis of STAT2 recognition by IRF9 reveals molecular insights into ISGF3 function

Proceedings of the National Academy of Sciences of the United States of America

Volumn 115, Issue 4, 2018, Pages E601-E609

  Rengachari, Srinivasan ^a   Groiss, Silvia ^a   Devos, Juliette M ^a   Caron, Elise ^b   Grandvaux, Nathalie ^b,c   Panne, Daniel ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Crystal structure; Innate immunity; IRF transcription factor; JAK STAT signaling; STAT2

Indexed keywords

INTERFERON REGULATORY FACTOR 9; INTERFERON STIMULATED GENE FACTOR 3; STAT1 PROTEIN; STAT2 PROTEIN; IRF9 PROTEIN, HUMAN; IRF9 PROTEIN, MOUSE; JANUS KINASE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; GENE; GENE EXPRESSION REGULATION; HUMAN; IFIT1 GENE; INTRACELLULAR SIGNALING; JAK-STAT SIGNALING; MOLECULAR RECOGNITION; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; ANIMAL; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; JANUS KINASES; MICE; POINT MUTATION; PROTEIN DOMAINS; SIGNAL TRANSDUCTION; STAT2 TRANSCRIPTION FACTOR;

EID: 85040862710     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1718426115     Document Type: Article

References (56)

1. Stark GR, Darnell JE, Jr (2012) The JAK-STAT pathway at twenty. Immunity 36: 503–514.
2. Levy DE, Darnell JE, Jr (2002) Stats: Transcriptional control and biological impact. Nat Rev Mol Cell Biol 3:651–662.
3. Paul WE, Seder RA (1994) Lymphocyte responses and cytokines. Cell 76:241–251.
4. Kishimoto T, Taga T, Akira S (1994) Cytokine signal transduction. Cell 76:253–262.
5. Schindler C, Shuai K, Prezioso VR, Darnell JE, Jr (1992) Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257:809–813.
6. Levy DE, Kessler DS, Pine R, Reich N, Darnell JE, Jr (1988) Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev 2:383–393.
7. 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.
8. 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.
9. Escalante CR, Yie J, Thanos D, Aggarwal AK (1998) Structure of IRF-1 with bound DNA reveals determinants of interferon regulation. Nature 391:103–106.
10. Furui J, et al. (1998) Solution structure of the IRF-2 DNA-binding domain: A novel subgroup of the winged helix-turn-helix family. Structure 6:491–500.
11. Takahasi K, et al. (2003) X-ray crystal structure of IRF-3 and its functional implications. Nat Struct Biol 10:922–927.
12. Panne D, Maniatis T, Harrison SC (2007) An atomic model of the interferon-beta enhanceosome. Cell 129:1111–1123.
13. Yanai H, Negishi H, Taniguchi T (2012) The IRF family of transcription factors: Inception, impact and implications in oncogenesis. OncoImmunology 1:1376–1386.
14. Reich N, et al. (1987) Interferon-induced transcription of a gene encoding a 15-kDa protein depends on an upstream enhancer element. Proc Natl Acad Sci USA 84: 6394–6398.
15. Qin BY, et al. (2003) Crystal structure of IRF-3 reveals mechanism of autoinhibition and virus-induced phosphoactivation. Nat Struct Biol 10:913–921.
16. Hiscott J, Lin R (2005) IRF-3 releases its inhibitions. Structure 13:1235–1236.
17. Chen W, et al. (2008) Insights into interferon regulatory factor activation from the crystal structure of dimeric IRF5. Nat Struct Mol Biol 15:1213–1220.
18. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140: 805–820.
19. Ablasser A, et al. (2013) cGAS produces a 2?-5?-linked cyclic dinucleotide second messenger that activates STING. Nature 498:380–384.
20. Kato H, Takahasi K, Fujita T (2011) RIG-I-like receptors: Cytoplasmic sensors for non-self RNA. Immunol Rev 243:91–98.
21. Zhao B, et al. (2016) Structural basis for concerted recruitment and activation of IRF-3 by innate immune adaptor proteins. Proc Natl Acad Sci USA 113:E3403–E3412.
22. Banninger G, Reich NC (2004) STAT2 nuclear trafficking. J Biol Chem 279:39199–39206.
23. 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.
24. Kraus TA, Lau JF, Parisien JP, Horvath CM (2003) A hybrid IRF9-STAT2 protein recapitulates interferon-stimulated gene expression and antiviral response. J Biol Chem 278:13033–13038.
25. Lau JF, Parisien JP, Horvath CM (2000) Interferon regulatory factor subcellular localization is determined by a bipartite nuclear localization signal in the DNA-binding domain and interaction with cytoplasmic retention factors. Proc Natl Acad Sci USA 97: 7278–7283.
26. Improta T, et al. (1994) Transcription factor ISGF-3 formation requires phosphorylated Stat91 protein, but Stat113 protein is phosphorylated independently of Stat91 protein. Proc Natl Acad Sci USA 91:4776–4780.
27. 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.
28. 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.
29. Remesh SG, Santosh V, Escalante CR (2015) Structural studies of IRF4 reveal a flexible autoinhibitory region and a compact linker domain. J Biol Chem 290:27779–27790.
30. Panne D, McWhirter SM, Maniatis T, Harrison SC (2007) Interferon regulatory factor 3 is regulated by a dual phosphorylation-dependent switch. J Biol Chem 282: 22816–22822.
31. Bluyssen HA, et al. (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.
32. Chowdhury FZ, Farrar JD (2013) STAT2: A shape-shifting anti-viral super STAT. JAK-STAT 2:e23633.
33. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD (1998) How cells respond to interferons. Annu Rev Biochem 67:227–264.
34. Panne D, Maniatis T, Harrison SC (2004) Crystal structure of ATF-2/c-Jun and IRF-3 bound to the interferon-beta enhancer. EMBO J 23:4384–4393.
35. Fujii Y, et al. (1999) Crystal structure of an IRF-DNA complex reveals novel DNA recognition and cooperative binding to a tandem repeat of core sequences. EMBO J 18: 5028–5041.
36. 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.
37. Liongue C, O’Sullivan LA, Trengove MC, Ward AC (2012) Evolution of JAK-STAT pathway components: Mechanisms and role in immune system development. PLoS One 7:e32777.
38. Randall RE, Goodbourn S (2008) Interferons and viruses: An interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89: 1–47.
39. Mao X, et al. (2005) Structural bases of unphosphorylated STAT1 association and receptor binding. Mol Cell 17:761–771.
40. Neculai D, et al. (2005) Structure of the unphosphorylated STAT5a dimer. J Biol Chem 280:40782–40787.
41. Majumder S, et al. (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.
42. Rauch I, et al. (2015) Noncanonical effects of IRF9 in intestinal inflammation: More than type I and type III interferons. Mol Cell Biol 35:2332–2343.
43. Svensson O, Malbet-Monaco S, Popov A, Nurizzo D, Bowler MW (2015) Fully automatic characterization and data collection from crystals of biological macromolecules. Acta Crystallogr D Biol Crystallogr 71:1757–1767.
44. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66:125–132.
45. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658–674.
46. Winn MD, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67:235–242.
47. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126–2132.
48. Adams PD, et al. (2011) The Phenix software for automated determination of macromolecular structures. Methods 55:94–106.
49. Chen VB, et al. (2010) MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12–21.
50. DeLano WL (2002) The PyMOL Molecular Graphics System (DeLano Scientific, San Carlos, CA).
51. Petoukhov MV, et al. (2012) New developments in the ATSAS program package for small-angle scattering data analysis. J Appl Crystallogr 45:342–350.
52. Herzog F, et al. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 337:1348–1352.
53. Kosinski J, et al. (2015) Xlink analyzer: Software for analysis and visualization of cross-linking data in the context of three-dimensional structures. J Struct Biol 189:177–183.
54. Grandvaux N, et al. (2002) Transcriptional profiling of interferon regulatory factor 3 target genes: Direct involvement in the regulation of interferon-stimulated genes. J Virol 76:5532–5539.
55. Becker S, Corthals GL, Aebersold R, Groner B, Müller CW (1998) Expression of a tyrosine phosphorylated, DNA binding Stat3beta dimer in bacteria. FEBS Lett 441: 141–147.
56. Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320–W324.