Structural basis of the inhibition of STAT1 activity by Sendai virus C protein

Journal of Virology

Volumn 89, Issue 22, 2015, Pages 11487-11499

  Oda, Kosuke ^a   Matoba, Yasuyuki ^a   Irie, Takashi ^a   Kawabata, Ryoko ^a   Fukushi, Masaya ^a   Sugiyama, Masanori ^a   Sakaguchi, Takemasa ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; AMINO ACID DERIVATIVE; BETA INTERFERON; DIMER; GAMMA INTERFERON; PHOSPHATASE; PROTEIN C; STAT1 PROTEIN; TYROSINE; NONSTRUCTURAL C PROTEIN, SENDAI VIRUS; PROTEIN BINDING; STAT1 PROTEIN, HUMAN; STAT2 PROTEIN; STAT2 PROTEIN, HUMAN; VIRAL PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; MOLECULAR MODEL; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; SENDAI VIRUS; TRANSCRIPTION REGULATION; ANTAGONISTS AND INHIBITORS; BINDING SITE; CELL LINE; HEK293 CELL LINE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CELL LINE; CRYSTALLOGRAPHY, X-RAY; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HEK293 CELLS; HUMANS; INTERFERON-ALPHA; INTERFERON-BETA; INTERFERON-GAMMA; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SENDAI VIRUS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR; VIRAL PROTEINS;

EID: 84945969729     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01887-15     Document Type: Article

References (38)

1. Lamb RA, Parks GD. 2013. Paramyxoviridae: the viruses and their replication, p 957-995. In Knipe DM, Howley PM (ed), Fields virology, 6th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Nagai Y, Takakura A, Irie T, Yonemitsu Y, Gotoh B. 2011. Sendai virus: evolution from mouse pathogen to a state-of-the-art tool in virus research and biotechnology, p 115-173. In Samal SK (ed), The biology of paramyxoviruses. Caister Academic Press, Norfolk, United Kingdom.
3. Irie T, Nagata N, Igarashi T, Okamoto I, Sakaguchi T. 2010. Conserved charged amino acids within Sendai virus C protein play multiple roles in the evasion of innate immune responses. PLoS One 5:e10719. http://dx.doi.org/10.1371/journal.pone.0010719.
4. Komatsu T, Takeuchi K, Yokoo J, Gotoh B. 2004. C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-beta production. Virology 325:137-148. http://dx.doi.org/10.1016/j.virol.2004.04.025.
5. Takeuchi K, Komatsu T, Kitagawa Y, Sada K, Gotoh B. 2008. Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J Virol 82:10102-10110. http://dx.doi.org/10.1128/JVI.00599-08.
6. Irie T, Nagata N, Yoshida T, Sakaguchi T. 2008. Paramyxovirus Sendai virus C proteins are essential for maintenance of negative-sense RNA genome in virus particles. Virology 374:495-505. http://dx.doi.org/10.1016/j.virol.2008.01.004.
7. Irie T, Okamoto I, Yoshida A, Nagai Y, Sakaguchi T. 2014. Sendai virus C proteins regulate viral genome and antigenome synthesis to dictate the negative genome polarity. J Virol 88:690-698. http://dx.doi.org/10.1128/JVI.02798-13.
8. Hasan MK, Kato A, Muranaka M, Yamaguchi R, Sakai Y, Hatano I, Tashiro M, Nagai Y. 2000. Versatility of the accessory C proteins of Sendai virus: contribution to virus assembly as an additional role. J Virol 74:5619-5628. http://dx.doi.org/10.1128/JVI.74.12.5619-5628.2000.
9. Kurotani A, Kiyotani K, Kato A, Shioda T, Sakai Y, Mizumoto K, Yoshida T, Nagai Y. 1998. Sendai virus C proteins are categorically nonessential gene products but silencing their expression severely impairs viral replication and pathogenesis. Genes Cells 3:111-124. http://dx.doi.org/10.1046/j.1365-2443.1998.00170.x.
10. Garcin D, Latorre P, Kolakofsky D. 1999. Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J Virol 73: 6559-6565.
11. Gotoh B, Takeuchi K, Komatsu T, Yokoo J, Kimura Y, Kurotani A, Kato A, Nagai Y. 1999. Knockout of the Sendai virus C gene eliminates the viral ability to prevent the interferon-alpha/beta-mediated responses. FEBS Lett 459:205-210. http://dx.doi.org/10.1016/S0014-5793(99)01241-7.
12. Takeuchi K, Komatsu T, Yokoo J, Kato A, Shioda T, Nagai Y, Gotoh B. 2001. Sendai virus C protein physically associates with Stat1. Genes Cells 6:545-557. http://dx.doi.org/10.1046/j.1365-2443.2001.00442.x.
13. Kato A, Ohnishi Y, Kohase M, Saito S, Tashiro M, Nagai Y. 2001. Y2, the smallest of the Sendai virus C proteins, is fully capable of both counteracting the antiviral action of interferons and inhibiting viral RNA synthesis. J Virol 75:3802-3810. http://dx.doi.org/10.1128/JVI.75.8.3802-3810.2001.
14. Young DF, Didcock L, Goodbourn S, Randall RE. 2000. Paramyxoviridae use distinct virus-specific mechanisms to circumvent the interferon response. Virology 269:383-390. http://dx.doi.org/10.1006/viro.2000.0240.
15. Gotoh B, Komatsu T, Takeuchi K, Yokoo J. 2003. The C-terminal half-fragment of the Sendai virus C protein prevents the gamma-activated factor from binding to a gamma-activated sequence site. Virology 316:29-40. http://dx.doi.org/10.1016/S0042-6822(03)00590-7.
16. Gotoh B, Takeuchi K, Komatsu T, Yokoo J. 2003. The STAT2 activation process is a crucial target of Sendai virus C protein for the blockade of alpha interferon signaling. J Virol 77:3360-3370. http://dx.doi.org/10.1128/JVI.77.6.3360-3370.2003.
17. Mao X, Ren Z, Parker GN, Sondermann H, Pastorello MA, Wang W, McMurray JS, Demeler B, Darnell JE, Jr, Chen X. 2005. Structural bases of unphosphorylated STAT1 association and receptor binding. Mol Cell 17:761-771. http://dx.doi.org/10.1016/j.molcel.2005.02.021.
18. Reich NC. 2013. STATs get their move on. JAKSTAT 2:e27080. http://dx.doi.org/10.4161/jkst.27080.
19. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108:193-199. http://dx.doi.org/10.1016/0378-1119(91)90434-D.
20. Sugahara F, Uchiyama T, Watanabe H, Shimazu Y, Kuwayama M, Fujii Y, Kiyotani K, Adachi A, Kohno N, Yoshida T, Sakaguchi T. 2004. Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology 325:1-10. http://dx.doi.org/10.1016/j.virol.2004.04.019.
21. Irie T, Yoshida A, Sakaguchi T. 2013. Clustered basic amino acids of the small Sendai virus C protein Y1 are critical to its Ran GTPase-mediated nuclear localization. PLoS One 8:e73740. http://dx.doi.org/10.1371/journal.pone.0073740.
22. Sakaguchi T, Irie T, Kawabata R, Yoshida A, Maruyama H, Kawakami H. 2011. Optineurin with amyotrophic lateral sclerosis-related mutations abrogates inhibition of interferon regulatory factor-3 activation. Neurosci Lett 505:279-281. http://dx.doi.org/10.1016/j.neulet.2011.10.040.
23. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326. http://dx.doi.org/10.1016/S0076-6879(97)76066-X.
24. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763. http://dx.doi.org/10.1107/S0907444994003112.
25. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54:905-921.
26. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158.
27. Brunger AT. 1992. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355:472-475. http://dx.doi.org/10.1038/355472a0.
28. Bromberg J, Chen X. 2001. STAT proteins: signal tranducers and activators of transcription. Methods Enzymol 333:138-151. http://dx.doi.org/10.1016/S0076-6879(01)33052-5.
29. ten Hoeve J, de Jesus Ibarra-Sanchez M, Fu Y, Zhu W, Tremblay M, David M, Shuai K. 2002. Identification of a nuclear Stat1 protein tyrosine phosphatase. Mol Cell Biol 22:5662-5668. http://dx.doi.org/10.1128/MCB.22.16.5662-5668.2002.
30. Kato A, Ohnishi Y, Hishiyama M, Kohase M, Saito S, Tashiro M, Nagai Y. 2002. The amino-terminal half of Sendai virus C protein is not responsible for either counteracting the antiviral action of interferons or downregulating viralRNAsynthesis. J Virol 76:7114-7124. http://dx.doi.org/10.1128/JVI.76.14.7114-7124.2002.
31. Gotoh B, Takeuchi K, Komatsu T. 2004. Inhibition of the gamma interferon response by a Sendai virus C protein mutant with no STAT1-binding ability. FEBS Lett 567:291-296. http://dx.doi.org/10.1016/j.febslet.2004.05.001.
32. Schaap M, Hancock R, Wilderspin A, Wells G. 2013. Development of a steady-state FRET-based assay to identify inhibitors of the Keap1-Nrf2protein-protein interaction. Protein Sci 22:1812-1819. http://dx.doi.org/10.1002/pro.2384.
33. Zhong M, Henriksen MA, Takeuchi K, Schaefer O, Liu B, ten Hoeve J, Ren Z, Mao X, Chen X, Shuai K, Darnell JE, Jr. 2005. Implications of an antiparallel dimeric structure of nonphosphorylated STAT1 for the activation-inactivation cycle. Proc Natl Acad Sci U S A 102:3966-3971. http://dx.doi.org/10.1073/pnas.0501063102.
34. Mertens C, Zhong M, Krishnaraj R, Zou W, Chen X, Darnell JE, Jr. 2006. Dephosphorylation of phosphotyrosine on STAT1 dimers requires extensive spatial reorientation of the monomers facilitated by the N-terminal domain. Genes Dev 20:3372-3381. http://dx.doi.org/10.1101/gad.1485406.
35. Komatsu T, Takeuchi K, Yokoo J, Gotoh B. 2002. Sendai virus C protein impairs both phosphorylation and dephosphorylation processes of Stat1. FEBS Lett 511:139-144. http://dx.doi.org/10.1016/S0014-5793(01)03301-4.
36. Wenta N, Strauss H, Meyer S, Vinkemeier U. 2008. Tyrosine phosphorylation regulates the partitioning of STAT1 between different dimer conformations. Proc Natl Acad Sci U S A 105:9238-9243. http://dx.doi.org/10.1073/pnas.0802130105.
37. Garcin D, Marq JB, Strahle L, le Mercier P, Kolakofsky D. 2002. All four Sendai virusCproteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295:256-265. http://dx.doi.org/10.1006/viro.2001.1342.
38. DeLano WL. 2002. The PyMOL molecular graphics system. DeLano Scientific, San Carlos, CA.