Threonine 80 phosphorylation of non-structural protein 1 regulates the replication of influenza A virus by reducing the binding affinity with RIG-I

Cellular Microbiology

Volumn 19, Issue 2, 2017, Pages

  Zheng, Weinan ^a   Cao, Shuaishuai ^a   Chen, Can ^a,b   Li, Jing ^a   Zhang, Shuang ^a   Jiang, Jingwen ^a,c   Niu, Yange ^a,b   Fan, Wenhui ^a   Li, Yun ^a   Bi, Yuhai ^a   Gao, George F ^a,b,d,e   Sun, Lei ^a   Liu, Wenjun ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^e CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; MUTANT PROTEIN; NONSTRUCTURAL PROTEIN 1; RETINOIC ACID INDUCIBLE PROTEIN I; THREONINE; VIRUS NUCLEOPROTEIN; CORE PROTEIN; DDX58 PROTEIN, HUMAN; INS1 PROTEIN, INFLUENZA VIRUS; NP PROTEIN, INFLUENZA A VIRUS; PROTEIN BINDING; RNA BINDING PROTEIN; VIRAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FEMALE; INFLUENZA A VIRUS; INNATE IMMUNITY; INTERFERON PRODUCTION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TRANSCRIPTION; AMINO ACID SUBSTITUTION; ANIMAL; CHEMISTRY; DISEASE MODEL; DNA MUTATIONAL ANALYSIS; GENETICS; HOST PATHOGEN INTERACTION; IMMUNE EVASION; INFLUENZA A VIRUS (H1N1); METABOLISM; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; VIROLOGY; VIRULENCE;

AMINO ACID SUBSTITUTION; ANIMALS; DEAD BOX PROTEIN 58; DISEASE MODELS, ANIMAL; DNA MUTATIONAL ANALYSIS; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; INFLUENZA A VIRUS, H1N1 SUBTYPE; MASS SPECTROMETRY; MICE; ORTHOMYXOVIRIDAE INFECTIONS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA-BINDING PROTEINS; THREONINE; VIRAL CORE PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

EID: 84980351226     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12643     Document Type: Article

References (47)

1. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124: 783–801.
2. Bui, M., Myers, J.E., and Whittaker, G.R. (2002) Nucleo-cytoplasmic localization of influenza virus nucleoprotein depends on cell density and phosphorylation. Virus Res 84: 37–44.
3. Carrillo, B., Choi, J.M., Bornholdt, Z.A., Sankaran, B., Rice, A.P., and Prasad, B.V. (2014) The influenza A virus protein NS1 displays structural polymorphism. J Virol 88: 4113–4122.
4. Chenavas, S., Estrozi, L.F., Slama-Schwok, A., Delmas, B., Di Primo, C., Baudin, F., et al. (2013) Monomeric nucleoprotein of influenza A virus. PLoS Pathog 9: e1003275.
5. Cheng, A., Wong, S.M., and Yuan, Y.A. (2009) Structural basis for dsRNA recognition by NS1 protein of influenza A virus. Cell Res 19: 187–195.
6. Cohen, P. (2000a) The regulation of protein function by multisite phosphorylation--a 25 year update. Trends Biochem Sci 25: 596–601.
7. Cohen, P. (2000b) The regulation of protein function by multisite phosphorylation--a 25 year update. Trends Biochem Sci 25: 596–610.
8. Das, K., Ma, L.C., Xiao, R., Radvansky, B., Aramini, J., Zhao, L., et al. (2008) Structural basis for suppression of a host antiviral response by influenza A virus. Proc Natl Acad Sci U S A 105: 13093–13098.
9. Greenspan, D., Palese, P., and Krystal, M. (1988) Two nuclear location signals in the influenza virus NS1 nonstructural protein. J Virol 62: 3020–3026.
10. Gregoriades, A., Christie, T., and Markarian, K. (1984) The membrane (M1) protein of influenza virus occurs in two forms and is a phosphoprotein. J Virol 49: 229–235.
11. Hale, B.G. (2014) Conformational plasticity of the influenza A virus NS1 protein. J Gen Virol 95: 2099–2105.
12. Hale, B.G., Knebel, A., Botting, C.H., Galloway, C.S., Precious, B.L., Jackson, D., et al. (2009) CDK/ERK-mediated phosphorylation of the human influenza A virus NS1 protein at threonine-215. Virology 383: 6–11.
13. Hale, B.G., Randall, R.E., Ortin, J., and Jackson, D. (2008) The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89: 2359–2376.
14. Hsiang, T.Y., Zhou, L., and Krug, R.M. (2012) Roles of the phosphorylation of specific serines and threonines in the NS1 protein of human influenza A viruses. J Virol 86: 10370–10376.
15. Hutchinson, E.C., Denham, E.M., Thomas, B., Trudgian, D.C., Hester, S.S., Ridlova, G., et al. (2012) Mapping the phosphoproteome of influenza A and B viruses by mass spectrometry. PLoS Pathog 8: e1002993.
16. Jagger, B.W., Wise, H.M., Kash, J.C., Walters, K.A., Wills, N.M., Xiao, Y.L., et al. (2012) An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337: 199–204.
17. Jia, D., Rahbar, R., Chan, R.W., Lee, S.M., Chan, M.C., Wang, B.X., et al. (2010) Influenza virus non-structural protein 1 (NS1) disrupts interferon signaling. PLoS One 5: e13927.
18. Kathum, O.A., Schrader, T., Anhlan, D., Nordhoff, C., Liedmann, S., Pande, A., et al. (2015) Phosphorylation of Influenza A virus NS1 protein at threonine 49 suppresses its interferon antagonistic activity. Cell Microbiol.
19. Keller, A., Nesvizhskii, A.I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383–5392.
20. Kinoshita-Kikuta, E., Aoki, Y., Kinoshita, E., and Koike, T. (2007) Label-free kinase profiling using phosphate affinity polyacrylamide gel electrophoresis. Mol Cell Proteomics 6: 356–366.
21. Kinoshita, E., Kinoshita-Kikuta, E., and Koike, T. (2009) Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat Protoc 4: 1513–1521.
22. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K., and Koike, T. (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics 5: 749–757.
23. Kochs, G., Garcia-Sastre, A., and Martinez-Sobrido, L. (2007) Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 81: 7011–7021.
24. Krug, R.M., Yuan, W., Noah, D.L., and Latham, A.G. (2003) Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309: 181–189.
25. Li, Y., Yamakita, Y., and Krug, R.M. (1998) Regulation of a nuclear export signal by an adjacent inhibitory sequence: the effector domain of the influenza virus NS1 protein. Proc Natl Acad Sci U S A 95: 4864–4869.
26. Liu, X., Sun, L., Yu, M., Wang, Z., Xu, C., Xue, Q., et al. (2009) Cyclophilin A interacts with influenza A virus M1 protein and impairs the early stage of the viral replication. Cell Microbiol 11: 730–741.
27. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408.
28. Long, J.X., Peng, D.X., Liu, Y.L., Wu, Y.T., and Liu, X.F. (2008) Virulence of H5N1 avian influenza virus enhanced by a 15-nucleotide deletion in the viral nonstructural gene. Virus Genes 36: 471–478.
29. Loo, Y.M., Fornek, J., Crochet, N., Bajwa, G., Perwitasari, O., Martinez-Sobrido, L., et al. (2008) Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82: 335–345.
30. Melen, K., Kinnunen, L., Fagerlund, R., Ikonen, N., Twu, K.Y., Krug, R.M., and Julkunen, I. (2007) Nuclear and nucleolar targeting of influenza A virus NS1 protein: striking differences between different virus subtypes. J Virol 81: 5995–6006.
31. Mibayashi, M., Martinez-Sobrido, L., Loo, Y.M., Cardenas, W.B., Gale, M., Jr., and Garcia-Sastre, A. (2007) Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 81: 514–524.
32. Mondal, A., Potts, G.K., Dawson, A.R., Coon, J.J., and Mehle, A. (2015) Phosphorylation at the homotypic interface regulates nucleoprotein oligomerization and assembly of the influenza virus replication machinery. PLoS Pathog 11: e1004826.
33. Muramoto, Y., Noda, T., Kawakami, E., Akkina, R., and Kawaoka, Y. (2013) Identification of novel influenza A virus proteins translated from PA mRNA. J Virol 87: 2455–2462.
34. Nesvizhskii, A.I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646–4658.
35. Neumann, G., Watanabe, T., Ito, H., Watanabe, S., Goto, H., Gao, P., et al. (1999) Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96: 9345–9350.
36. Pearlman, S.M., Serber, Z., and Ferrell, J.E., Jr. (2011) A mechanism for the evolution of phosphorylation sites. Cell 147: 934–946.
37. Privalsky, M.L., and Penhoel, E.E. (1981) The structural and synthesis of influenza virus phosphoproteins. J Biol Chem 256: 5368–5376.
38. Privalsky, M.L., and Penhoet, E.E. (1978) Influenza virus proteins: identity, synthesis, and modification analyzed by two-dimensional gel electrophoresis. Proc Natl Acad Sci U S A 75: 3625–3629.
39. Robb, N.C., Chase, G., Bier, K., Vreede, F.T., Shaw, P.C., Naffakh, N., et al. (2011) The influenza A virus NS1 protein interacts with the nucleoprotein of viral ribonucleoprotein complexes. J Virol 85: 5228–5231.
40. Samji, T. (2009) Influenza A: understanding the viral life cycle. Yale J Biol Med 82: 153–159.
41. Trapp, S., Soubieux, D., Marty, H., Esnault, E., Hoffmann, T.W., Chandenier, M., et al. (2014) Shortening the unstructured, interdomain region of the non-structural protein NS1 of an avian H1N1 influenza virus increases its replication and pathogenicity in chickens. J Gen Virol 95: 1233–1243.
42. Turrell, L., Hutchinson, E.C., Vreede, F.T., and Fodor, E. (2014) Regulation of Influenza A Virus Nucleoprotein Oligomerisation by Phosphorylation. J Virol.
43. Wang, S., Zhao, Z., Bi, Y., Sun, L., Liu, X., and Liu, W. (2013) Tyrosine 132 phosphorylation of influenza A virus M1 protein is crucial for virus replication by controlling the nuclear import of M1. J Virol 87: 6182–6191.
44. Wang, Z., Liu, X., Zhao, Z., Xu, C., Zhang, K., Chen, C., et al. (2011) Cyclophilin E functions as a negative regulator to influenza virus replication by impairing the formation of the viral ribonucleoprotein complex. PLoS One 6: e22625.
45. Wise, H.M., Hutchinson, E.C., Jagger, B.W., Stuart, A.D., Kang, Z.H., Robb, N., et al. (2012) Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain. PLoS Pathog 8: e1002998.
46. Zhang, K., Wang, Z., Liu, X., Yin, C., Basit, Z., Xia, B., and Liu, W. (2012) Dissection of influenza A virus M1 protein: pH-dependent oligomerization of N-terminal domain and dimerization of C-terminal domain. PLoS One 7: e37786.
47. Zheng, W., Li, J., Wang, S., Cao, S., Jiang, J., Chen, C., et al. (2015) Phosphorylation controls the nuclear-cytoplasmic shuttling of influenza A virus nucleoprotein. J Virol 89: 5822–5834.