A Second RNA-Binding Site in the NS1 Protein of Influenza B Virus

Structure

Volumn 24, Issue 9, 2016, Pages 1562-1572

  Ma, Li Chung ^a   Guan, Rongjin ^a   Hamilton, Keith ^a   Aramini, James M ^a   Mao, Lei ^a   Wang, Shanshan ^b   Krug, Robert M ^b   Montelione, Gaetano T ^a,c  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 1A; NONSTRUCTURAL PROTEIN 1B; UNCLASSIFIED DRUG; INS1 PROTEIN, INFLUENZA VIRUS; PROTEIN BINDING; RECOMBINANT PROTEIN; RNA BINDING PROTEIN; VIRAL PROTEIN; VIRUS RNA;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DIMERIZATION; FLUORESCENCE POLARIZATION; INFLUENZA B VIRUS; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RNA BINDING; VIRUS REPLICATION; A-549 CELL LINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CHEMISTRY; CONSERVED SEQUENCE; ENZYME SPECIFICITY; GENE EXPRESSION; GENETICS; HUMAN; INFLUENZA A VIRUS; KINETICS; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; X RAY CRYSTALLOGRAPHY;

A549 CELLS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BINDING SITES; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GENE EXPRESSION; HUMANS; INFLUENZA A VIRUS; INFLUENZA B VIRUS; KINETICS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; RNA, VIRAL; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; SUBSTRATE SPECIFICITY; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84985945896     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2016.07.001     Document Type: Article

References (45)

1. Abendroth, J., Gardberg, A.S., Robinson, J.I., Christensen, J.S., Staker, B.L., Myler, P.J., Stewart, L.J., Edwards, T.E., SAD phasing using iodide ions in a high-throughput structural genomics environment. J. Stuct. Funct. Genomics 12 (2011), 83–95.
2. Acton, T.B., Gunsalus, K.C., Xiao, R., Ma, L.C., Aramini, J., Baran, M.C., Chiang, Y.-W., Climent, T., Cooper, B., Denissova, N.G., et al. Robotic cloning and protein production platform of the Northeast Structural Genomics Consortium. Methods Enzymol. 394 (2005), 210–243.
3. Acton, T.B., Xiao, R., Anderson, S., Aramini, J., Buchwald, W.A., Ciccosanti, C., Conover, K., Everett, J., Hamilton, K., Huang, Y.J., et al. Preparation of protein samples for NMR structure, function, and small-molecule screening studies. Methods Enzymol. 493 (2011), 21–60.
4. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Echols, N., Headd, J.J., Hung, L.W., Jain, S., Kapral, G.J., Grosse Kunstleve, R.W., et al. The Phenix software for automated determination of macromolecular structures. Methods 55 (2011), 94–106.
5. Aramini, J.M., Ma, L.C., Zhou, L., Schauder, C.M., Hamilton, K., Amer, B.R., Mack, T.R., Lee, H.W., Ciccosanti, C.T., Zhao, L., et al. Dimer interface of the effector domain of non-structural protein 1 from influenza A virus: an interface with multiple functions. J. Biol. Chem. 286 (2011), 26050–26060.
6. Aramini, J.M., Hamilton, K., Ma, L.C., Swapna, G.V., Leonard, P.G., Ladbury, J.E., Krug, R.M., Montelione, G.T., (19)F NMR reveals multiple conformations at the dimer interface of the nonstructural protein 1 effector domain from influenza A virus. Structure 22 (2014), 515–525.
7. Ayllon, J., Russell, R.J., Garcia-Sastre, A., Hale, B.G., Contribution of NS1 effector domain dimerization to influenza A virus replication and virulence. J. Virol. 86 (2012), 13095–13098.
8. Baker, N.A., Sept, D., Joseph, S., Holst, M.J., McCammon, J.A., Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98 (2001), 10037–10041.
9. Bhattacharya, A., Tejero, R., Montelione, G.T., Evaluating protein structures determined by structural genomics consortia. Proteins 66 (2007), 778–795.
10. Bornholdt, Z.A., Prasad, B.V., X-ray structure of influenza virus NS1 effector domain. Nat. Struct. Mol. Biol. 13 (2006), 559–560.
11. Bornholdt, Z.A., Prasad, B.V., X-ray structure of NS1 from a highly pathogenic H5N1 influenza virus. Nature 456 (2008), 985–988.
12. Chen, Z., Li, Y., Krug, R.M., Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3’-end processing machinery. EMBO J. 18 (1999), 2273–2283.
13. Chien, C.Y., Tejero, R., Huang, Y., Zimmerman, D.E., Rios, C.B., Krug, R.M., Montelione, G.T., A novel RNA-binding motif in influenza A virus non-structural protein 1. Nat. Struct. Biol. 4 (1997), 891–895.
14. Das, K., Ma, L.C., Xiao, R., Radvansky, B., Aramini, J., Zhao, L., Marklund, J., Kuo, R.L., Twu, K.Y., Arnold, E., et al. Structural basis for suppression of a host antiviral response by influenza A virus. Proc. Natl. Acad. Sci. USA 105 (2008), 13093–13098.
15. Dauber, B., Schneider, J., Wolff, T., Double-stranded RNA binding of influenza B virus nonstructural NS1 protein inhibits protein kinase R but is not essential to antagonize production of alpha/beta interferon. J. Virol. 80 (2006), 11667–11677.
16. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. 3rd, Snoeyink, J., Richardson, J.S., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007), W375–W383.
17. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., Bax, A., NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995), 277–293.
18. DeLano, W.L., The PyMOL Molecular Graphics System, Version 1.5.0.4. 2002, Schrödinger, LLC.
19. Donelan, N.R., Dauber, B., Wang, X., Basler, C.F., Wolff, T., Garcia-Sastre, A., The N- and C-terminal domains of the NS1 protein of influenza B virus can independently inhibit IRF-3 and beta interferon promoter activation. J. Virol. 78 (2004), 11574–11582.
20. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Cryst. D Biol. Crystallogr. 60 (2004), 2126–2132.
21. Farmer, B.T. 2nd, Constantine, K.L., Goldfarb, V., Friedrichs, M.S., Wittekind, M., Yanchunas, J. Jr., Robertson, J.G., Mueller, L., Localizing the NADP+ binding site on the MurB enzyme by NMR. Nat. Struct. Biol. 3 (1996), 995–997.
22. Fushman, D., Weisemann, R., Thuring, H., Ruterjans, H., Backbone dynamics of ribonuclease T1 and its complex with 2’GMP studied by two-dimensional heteronuclear NMR spectroscopy. J. Biomol. NMR 4 (1994), 61–78.
23. Goddard, T.D., Kneller, D.G., Sparky 3. 2000, University of California.
24. Guan, R., Ma, L.C., Leonard, P.G., Amer, B.R., Sridharan, H., Zhao, C., Krug, R.M., Montelione, G.T., Structural basis for the sequence-specific recognition of human ISG15 by the NS1 protein of influenza B virus. Proc. Natl. Acad. Sci. USA 108 (2011), 13468–13473.
25. Hale, B.G., Jackson, D., Chen, Y.H., Lamb, R.A., Randall, R.E., Influenza A virus NS1 protein binds p85beta and activates phosphatidylinositol-3-kinase signaling. Proc. Natl. Acad. Sci. USA 103 (2006), 14194–14199.
26. Hoffmann, E., Mahmood, K., Yang, C.F., Webster, R.G., Greenberg, H.B., Kemble, G., Rescue of influenza B virus from eight plasmids. Proc. Natl. Acad. Sci. USA 99 (2002), 11411–11416.
27. Huang, Y.J., Acton, T.B., Montelione, G.T., DisMeta: a meta server for construct design and optimization. Methods Mol. Biol. 1091 (2014), 3–16.
28. Kay, L.E., Torchia, D.A., Bax, A., Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28 (1989), 8972–8979.
29. Kerry, P.S., Turkington, H.L., Ackermann, K., Jameison, S.A., Bode, B.E., Analysis of influenza A virus NS1 dimer interfaces in solution by pulse EPR distance measurements. J. Phys. Chem. B 118 (2014), 10882–10888.
30. Krug, R.M., Fodor, E., The virus genome and its replication. Webster, R.G., Braciale, T.J., Lamb, R.A., (eds.) Influenza Textbook, Second Edition, 2013, Wiley-Blackwell, 57–66.
31. Krug, R.M., Garcia-Sastre, A., The NS1 protein: a master regulator of host and viral functions. Webster, R.G., Monto, A.S., Braciale, T.J., Lamb, eds, R.A., (eds.) Textbook of Influenza, Second Edition, 2013, Wiley-Blackwell, 114–132.
32. Kuo, R.L., Zhao, C., Malur, M., Krug, R.M., 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.
33. Li, S., Min, J.Y., Krug, R.M., Sen, G.C., Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349 (2006), 13–21.
34. Liu, J., Lynch, P.A., Chien, C.Y., Montelione, G.T., Krug, R.M., Berman, H.M., Crystal structure of the unique RNA-binding domain of the influenza virus NS1 protein. Nat. Struct. Biol. 4 (1997), 896–899.
35. Luft, J.R., Collins, R.J., Fehrman, N.A., Lauricella, A.M., Veatch, C.K., DeTitta, G.T., A deliberate approach to screening for initial crystallization conditions of biological macromolecules. J. Struct. Biol. 142 (2003), 170–179.
36. Mäkelä, S.M., Österlund, P., Westenius, V., Latvala, S., Diamond, M.S., Gale, M. Jr., Julkunen, I., RIG-I signaling is essential for influenza B virus-induced rapid interferon gene expression. J. Virol. 89 (2015), 12014–12025.
37. Nemeroff, M.E., Barabino, S.M., Li, Y., Keller, W., Krug, R.M., 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.
38. Panavas, T., Sanders, C., Butt, T.R., SUMO fusion technology for enhanced protein production in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 497 (2009), 303–317.
39. Qian, X.Y., Chien, C.Y., Lu, Y., Montelione, G.T., Krug, R.M., An amino-terminal polypeptide fragment of the influenza virus NS1 protein possesses specific RNA-binding activity and largely helical backbone structure. RNA 1 (1995), 948–956.
40. Sharma, S., Zheng, H., Huang, Y.J., Ertekin, A., Hamuro, Y., Rossi, P., Tejero, R., Acton, T.B., Xiao, R., Jiang, M., et al. Construct optimization for protein NMR structure analysis using amide hydrogen/deuterium exchange mass spectrometry. Proteins 76 (2009), 882–894.
41. Terwilliger, T.C., Adams, P.D., Read, R.J., McCoy, A.J., Moriarty, N.W., Grosse-Kunstleve, R.W., Afonine, P.V., Zwart, P.H., Hung, L.W., Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Cryst. D Biol. Crystallogr. 65 (2009), 582–601.
42. Vranken, W.F., Boucher, W., Stevens, T.J., Fogh, R.H., Pajon, A., Llinas, M., Ulrich, E.L., Markley, J.L., Ionides, J., Laue, E.D., The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59 (2005), 687–696.
43. Xia, S., Robertus, J.D., X-ray structures of NS1 effector domain mutants. Arch. Biochem. Biophys. 494 (2010), 198–204.
44. Xiao, R., Anderson, S., Aramini, J., Belote, R., Buchwald, W.A., Ciccosanti, C., Conover, K., Everett, J.K., Hamilton, K., Huang, Y.J., et al. The high-throughput protein sample production platform of the Northeast Structural Genomics Consortium. J. Struct. Biol. 172 (2010), 21–33.
45. Yin, C., Khan, J.A., Swapna, G.V., Ertekin, A., Krug, R.M., Tong, L., Montelione, G.T., Conserved surface features form the double-stranded RNA binding site of non-structural protein 1 (NS1) from influenza A and B viruses. J. Biol. Chem. 282 (2007), 20584–20592.