Structural Basis for a Novel Interaction between the NS1 Protein Derived from the 1918 Influenza Virus and RIG-I

Structure

Volumn 23, Issue 11, 2015, Pages 2001-2010

  Jureka, Alexander S ^a   Kleinpeter, Alex B ^a   Cornilescu, Gabriel ^b   Cornilescu, Claudia C ^b   Petit, Chad M ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; HOMODIMER; NONSTRUCTURAL PROTEIN 1; RETINOIC ACID INDUCIBLE PROTEIN I; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; INS1 PROTEIN, INFLUENZA VIRUS; PROTEIN BINDING; VIRAL PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; ENZYME ACTIVATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; INFLUENZA VIRUS; INNATE IMMUNITY; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; RNA BINDING; SEQUENCE ALIGNMENT; SPANISH INFLUENZA; VIRUS VIRULENCE; AMINO ACID SEQUENCE; BINDING SITE; CHEMISTRY; HUMAN; INFLUENZA A VIRUS (H1N1); METABOLISM; MOLECULAR DOCKING; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; BINDING SITES; DEAD BOX PROTEIN 58; DEAD-BOX RNA HELICASES; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA PANDEMIC, 1918-1919; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84946499454     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.08.007     Document Type: Article

References (50)

1. J. Ayllon, and A. Garcia-Sastre The NS1 protein: a multitasking virulence factor Curr. Top. Microbiol. Immunol. 386 2014 73 107
2. J. Ayllon, P. Domingues, R. Rajsbaum, L. Miorin, M. Schmolke, B.G. Hale, and A. Garcia-Sastre A single amino acid substitution in the novel H7N9 Influenza A Virus NS1 protein increases CPSF30 binding and virulence J. Virol. 88 2014 12146 12151
3. K. Briknarova, C.J. Thomas, J. York, and J.H. Nunberg Structure of a zinc-binding domain in the Junin virus envelope glycoprotein J. Biol. Chem. 286 2011 1528 1536
4. C.Y. Chien, R. Tejero, Y. Huang, D.E. Zimmerman, C.B. Rios, R.M. Krug, and G.T. Montelione A novel RNA-binding motif in influenza A virus non-structural protein 1 Nat. Struct. Biol. 4 1997 891 895
5. C.Y. Chien, Y. Xu, R. Xiao, J.M. Aramini, P.V. Sahasrabudhe, R.M. Krug, and G.T. Montelione Biophysical characterization of the complex between double-stranded RNA and the N-terminal domain of the NS1 protein from influenza A virus: evidence for a novel RNA-binding mode Biochemistry 43 2004 1950 1962
6. G.E. Crooks, G. Hon, J.M. Chandonia, and S.E. Brenner WebLogo: a sequence logo generator Genome Res. 14 2004 1188 1190
7. S.K. Dankar, E. Miranda, N.E. Forbes, M. Pelchat, A. Tavassoli, M. Selman, J. Ping, J. Jia, and E.G. Brown Influenza A/Hong Kong/156/1997(H5N1) virus NS1 gene mutations F103L and M106I both increase IFN antagonism, virulence and cytoplasmic localization but differ in binding to RIG-I and CPSF30 Virol. J. 10 2013 243
8. K. Das, L.C. Ma, R. Xiao, B. Radvansky, J. Aramini, L. Zhao, J. Marklund, R.L. Kuo, K.Y. Twu, E. Arnold, and et al. Structural basis for suppression of a host antiviral response by influenza A virus Proc. Natl. Acad. Sci. USA 105 2008 13093 13098
9. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax Nmrpipe - a multidimensional spectral processing system based on Unix pipes J. Biomol. NMR 6 1995 277 293
10. N.C. Fitzkee, and A. Bax Facile measurement of (1)H-(1)(5)N residual dipolar couplings in larger perdeuterated proteins J. Biomol. NMR 48 2010 65 70
11. M.P. Foster, D.S. Wuttke, K.R. Clemens, W. Jahnke, I. Radhakrishnan, L. Tennant, M. Reymond, J. Chung, and P.E. Wright Chemical shift as a probe of molecular interfaces: NMR studies of DNA binding by the three amino-terminal zinc finger domains from transcription factor IIIA J. Biomol. NMR 12 1998 51 71
12. M.U. Gack, R.A. Albrecht, T. Urano, K.S. Inn, I.C. Huang, E. Carnero, M. Farzan, S. Inoue, J.U. Jung, and A. Garcia-Sastre Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I Cell Host Microbe 5 2009 439 449
13. J.E. Garrus, U.K. von Schwedler, O.W. Pornillos, S.G. Morham, K.H. Zavitz, H.E. Wang, D.A. Wettstein, K.M. Stray, M. Cote, R.L. Rich, and et al. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding Cell 107 2001 55 65
14. K.M. Graef, F.T. Vreede, Y.F. Lau, A.W. McCall, S.M. Carr, K. Subbarao, and E. Fodor The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon J. Virol. 84 2010 8433 8445
15. Z. Guo, L.M. Chen, H. Zeng, J.A. Gomez, J. Plowden, T. Fujita, J.M. Katz, R.O. Donis, and S. Sambhara NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I Am. J. Respir. Cell Mol. Biol. 36 2007 263 269
16. B.G. Hale, J. Steel, R.A. Medina, B. Manicassamy, J. Ye, D. Hickman, R. Hai, M. Schmolke, A.C. Lowen, D.R. Perez, and et al. Inefficient control of host gene expression by the 2009 pandemic H1N1 influenza A virus NS1 protein J. Virol. 84 2010 6909 6922
17. N.S. Heaton, D. Sachs, C.J. Chen, R. Hai, and P. Palese Genome-wide mutagenesis of influenza virus reveals unique plasticity of the hemagglutinin and NS1 proteins Proc. Natl. Acad. Sci. USA 110 2013 20248 20253
18. D. Jackson, M.J. Hossain, D. Hickman, D.R. Perez, and R.A. Lamb A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity Proc. Natl. Acad. Sci. USA 105 2008 4381 4386
19. F. Jiang, A. Ramanathan, M.T. Miller, G.Q. Tang, M. Gale Jr., S.S. Patel, and J. Marcotrigiano Structural basis of RNA recognition and activation by innate immune receptor RIG-I Nature 479 2011 423 427
20. B.A. Johnson, and R.A. Blevins NMR view: a computer program for the visualization and analysis of NMR data J. Biomol. NMR 4 1994 603 614
21. H. Kato, O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K.J. Ishii, and et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature 441 2006 101 105
22. G. Kochs, A. Garcia-Sastre, and L. Martinez-Sobrido Multiple anti-interferon actions of the influenza A virus NS1 protein J. Virol. 81 2007 7011 7021
23. E. Kowalinski, T. Lunardi, A.A. McCarthy, J. Louber, J. Brunel, B. Grigorov, D. Gerlier, and S. Cusack Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA Cell 147 2011 423 435
24. R.L. Kuo, C. Zhao, M. Malur, and R.M. Krug Influenza A virus strains that circulate in humans differ in the ability of their NS1 proteins to block the activation of IRF3 and interferon-beta transcription Virology 408 2010 146 158
25. Y. Li, Z.Y. Chen, W. Wang, C.C. Baker, and R.M. Krug The 3′-end-processing factor CPSF is required for the splicing of single-intron pre-mRNAs in vivo RNA 7 2001 920 931
26. S.M. Liao, Q.S. Du, J.Z. Meng, Z.W. Pang, and R.B. Huang The multiple roles of histidine in protein interactions Chem. Cent. J. 7 2013 44
27. M. Mibayashi, L. Martinez-Sobrido, Y.M. Loo, W.B. Cardenas, M. Gale Jr., and A. Garcia-Sastre Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus J. Virol. 81 2007 514 524
28. N.A. Molinari, I.R. Ortega-Sanchez, M.L. Messonnier, W.W. Thompson, P.M. Wortley, E. Weintraub, and C.B. Bridges The annual impact of seasonal influenza in the US: measuring disease burden and costs Vaccine 25 2007 5086 5096
29. S. Myong, S. Cui, P.V. Cornish, A. Kirchhofer, M.U. Gack, J.U. Jung, K.P. Hopfner, and T. Ha Cytosolic viral sensor RIG-I is a 5′-triphosphate-dependent translocase on double-stranded RNA Science 323 2009 1070 1074
30. M.E. Nemeroff, S.M. Barabino, Y. Li, W. Keller, and R.M. Krug Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3′ end formation of cellular pre-mRNAs Mol. Cell 1 1998 991 1000
31. G. Neumann, and Y. Kawaoka Transmission of influenza A viruses Virology 479-480 2015 234 246
32. B. Opitz, A. Rejaibi, B. Dauber, J. Eckhard, M. Vinzing, B. Schmeck, S. Hippenstiel, N. Suttorp, and T. Wolff IFNbeta induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein Cell. Microbiol. 9 2007 930 938
33. H. Oshiumi, M. Matsumoto, S. Hatakeyama, and T. Seya Riplet/RNF135, a RING finger protein, ubiquitinates RIG-I to promote interferon-beta induction during the early phase of viral infection J. Biol. Chem. 284 2009 807 817
34. A. Pichlmair, O. Schulz, C.P. Tan, T.I. Naslund, P. Liljestrom, F. Weber, and C. Reis e Sousa RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates Science 314 2006 997 1001
35. M. Ruckert, and G. Otting Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments J. Am. Chem. Soc. 122 2000 7793 7797
36. M. Schlee, and G. Hartmann The chase for the RIG-I ligand - recent advances Mol. Ther. 18 2010 1254 1262
37. F.H. Schumann, H. Riepl, T. Maurer, W. Gronwald, K.P. Neidig, and H.R. Kalbitzer Combined chemical shift changes and amino acid specific chemical shift mapping of protein-protein interactions J. Biomol. NMR 39 2007 275 289
38. C.D. Schwieters, and G.M. Clore The VMD-XPLOR visualization package for NMR structure refinement J. Magn. Reson. 149 2001 239 244
39. C.D. Schwieters, J.J. Kuszewski, N. Tjandra, and G.M. Clore The XPLOR-NIH NMR molecular structure determination package J. Magn. Reson. 160 2003 65 73
40. A. Spesock, M. Malur, M.J. Hossain, L.M. Chen, B.L. Njaa, C.T. Davis, A.S. Lipatov, I.A. York, R.M. Krug, and R.O. Donis The virulence of 1997 H5N1 influenza viruses in the mouse model is increased by correcting a defect in their NS1 proteins J. Virol. 85 2011 7048 7058
41. J.K. Taubenberger, and D.M. Morens 1918 Influenza: the mother of all pandemics Emerg. Infect. Dis. 12 2006 15 22
42. W.W. Thompson, L. Comanor, and D.K. Shay Epidemiology of seasonal influenza: use of surveillance data and statistical models to estimate the burden of disease J. Infect. Dis. 194 Suppl 2 2006 S82 S91
43. Y. Tian, C.D. Schwieters, S.J. Opella, and F.M. Marassi A practical implicit solvent potential for NMR structure calculation J. Magn. Reson. 243 2014 54 64
44. K.Y. Twu, R.L. Kuo, J. Marklund, and R.M. Krug The H5N1 influenza virus NS genes selected after 1998 enhance virus replication in mammalian cells J. Virol. 81 2007 8112 8121
45. T.S. Ulmer, B.E. Ramirez, F. Delaglio, and A. Bax Evaluation of backbone proton positions and dynamics in a small protein by liquid crystal NMR spectroscopy J. Am. Chem. Soc. 125 2003 9179 9191
46. W. Wang, K. Riedel, P. Lynch, C.Y. Chien, G.T. Montelione, and R.M. Krug RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids RNA 5 1999 195 205
47. 13C chemical-shift data J. Biomol. NMR 4 1994 171 180
48. K. Wüthrich NMR of Proteins and Nucleic Acids 1986 Wiley Interscience
49. M. Yoneyama, M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nat. Immunol. 5 2004 730 737
50. S. Yoo, D.G. Myszka, C. Yeh, M. McMurray, C.P. Hill, and W.I. Sundquist Molecular recognition in the HIV-1 capsid/cyclophilin A complex J. Mol. Biol. 269 1997 780 795