Structure and sequence based functional annotation of Zika virus NS2b protein: Computational insights

Biochemical and Biophysical Research Communications

Volumn 492, Issue 4, 2017, Pages 659-667

  Aguilera Pesantes, Daniel ^a   Méndez, Miguel A ^a  

^a UNIVERSIDAD SAN FRANCISCO DE QUITO   (Ecuador)

Author keywords

Computational alanine scanning mutagenesis; Flavivirus; NS2b; NS3; Protein disorder; Transmembrane domains; Zika virus

Indexed keywords

ALANINE; ASPARTIC ACID; GLYCINE; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 2B; NONSTRUCTURAL PROTEIN 3; PROTEINASE; UNCLASSIFIED DRUG; NS2B PROTEIN, FLAVIVIRUS; VIRAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SUBSTRATE; LIFE CYCLE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; WEST NILE VIRUS; ZIKA VIRUS; CHEMICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; ENZYMOLOGY; MOLECULAR MODEL; PROTEIN CONFORMATION; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; COMPUTER SIMULATION; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN DOMAINS; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL NONSTRUCTURAL PROTEINS; ZIKA VIRUS;

EID: 85012912360     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2017.02.035     Document Type: Article

References (82)

1. Lanciotti, R.S., Kosoy, O.L., Laven, J.J., Velez, J.O., Lambert, A.J., Johnson, A.J., Stanfield, S.M., Duffy, M.R., Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia. Emerg. Infect. Dis. 14:2007 (2008), 1232–1239.
2. Kostyuchenko, V.A., Lim, E.X., Zhang, S., Fibriansah, G., Ng, T.-S., Ooi, J.S., Shi, J., Lok, S.-M., Structure of the thermally stable Zika virus. Nature 533 (2016), 425–428.
3. Tian, Hongliang, et al. The crystal structure of Zika virus helicase: basis for antiviral drug design. Protein & cell 7 (2016), 450–454.
4. Lei, J., Hansen, G., Nitsche, C., Klein, C.D., Zhang, L., Hilgenfeld, R., Crystal structure of Zika virus NS2B-NS3 protease in complex with a boronate inhibitor. Science 353 (2016), 503–505.
5. Xu, X., Song, H., Qi, J., Liu, Y., Wang, H., Su, C., Shi, Y., Gao, G.F., Contribution of intertwined loop to membrane association revealed by Zika virus full- length NS1 structure. EMBO J. 35 (2016), 2170–2178.
6. Coloma, J., Jain, R., Rajashankar, K.R., García-Sastre, A., Aggarwal, A.K., Structures of NS5 methyltransferase from Zika virus. Cell Rep. 16 (2016), 3097–3102.
7. Geser, A., Henderson, B.E., Christensen, S., A multipurpose serological survey in Kenya: 2. Results of arbovirus serological tests. Bull. World Health Organ., 43, 1970, 539.
8. World Health Organization, Zika virus outbreaks in the Americas. Wkly. Epidemiol. Rec. 90 (2015), 609–610.
9. Li, M.I., Wong, P.S.J., Ng, L.C., Tan, C.H., Oral susceptibility of Singapore Aedes (stegomyia) aegypti (linnaeus) to Zika virus. PLoS Negl. Trop. Dis., 6, 2012, e1792.
10. Kaddumukasa, M., Mutebi, J.-P., Lutwama, J., Masembe, C., Akol, A., Mosquitoes of Zika Forest, Uganda: species composition and relative abundance. J. Med. entomol. 51:2012 (2014), 104–113.
11. Foy, B.D., Kobylinski, K.C., Chilson Foy, J.L., Blitvich, B.J., Travassos da Rosa, A., Haddow, A.D., Lanciotti, R.S., Tesh, R.B., Probable non-vector-borne transmission of Zika virus, Colorado. USA. Emerg. Infect. Dis. 17 (2011), 880–882.
12. Besnard, M., Lastère, S., Teissier, A., Cao-Lormeau, V., Musso, D., Evidence of perinatal transmission of Zika virus, French Polynesia, december 2013 and february 2014. Euro Surveill., 19, 2014, 20751.
13. Musso, D., Nhan, T., Robin, E., Roche, C., Bierlaire, D., Zisou, K., Shan Yan, A., Cao- Lormeau, V., Broult, J., Potential for Zika virus transmission through blood transfusion demonstrated during an outbreak in French Polynesia, November 2013 to February 2014. Euro Surveill. 19 (2014), 1–3.
14. Duffy, M.R., et al. Zika virus outbreak on yap island, Federated States OF Micronesia. N. Engl. J. Med. 360 (2009), 2536–2543.
15. Villamil-Gómez, W.E., González-Camargo, O., Rodriguez-Ayubi, J., Zapata-Serpa, D., Rodriguez-Morales, A.J., Dengue, chikungunya and Zika co-infection in a patient from Colombia. J. Infect. public health 9 (2016), 684–686.
16. Chang, C., Ortiz, K., Ansari, A., Gershwin, M.E., The Zika outbreak of the 21st century. J. Autoimmun. 68 (2016), 1–13.
17. Schuck-Paim, C., López, D., Simonsen, L., Alonso, W., Unintended pregnancies in Brazil–A challenge for the recommendation to delay pregnancy due to Zika. PLoS Curr. Outbreaks, first ed., 2016 Mar 16.
18. Dick, G., Kitchen, S., Haddow, A., Zika virus (I). Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg. 46 (1952), 509–520.
19. Dick, G., Paper: epidemiological notes on some viruses isolated in Uganda (yel- low fever, rift valley fever, bwamba fever, West Nile, mengo, semliki forest, bunyamw- era, ntaya, Uganda S and Zika viruses). Trans. R. Soc. Trop. Med. Hyg. 47 (1953), 13–48.
20. Marano, G., Pupella, S., Vaglio, S., Liumbruno, G.M., Grazzini, G., Zika virus and the never-ending story of emerging pathogens and transfusion medicine. Blood Transfus., 14–2, 2016, 95.
21. Weissenböck, H., Hubálek, Z., Bakonyi, T., Nowotny, N., Zoonotic mosquito- borne flaviviruses: worldwide presence of agents with proven pathogenicity and potential candidates of future emerging diseases. Veterinary Microbiol. 140 (2010), 271–280.
22. Kuno, G., Chang, G.-J., Full-length sequencing and genomic characterization of Bagaza, Kedougou, and Zika viruses. Arch. virol. 152 (2007), 687–696.
23. Nitsche, C., Holloway, S., Schirmeister, T., Klein, C.D., Biochemistry and medicinal chemistry of the dengue virus protease. Chem. Rev. 114 (2014), 11348–11381.
24. Bessaud, M., Pastorino, B.A., Peyrefitte, C.N., Rolland, D., Grandadam, M., Tolou, H.J., Functional characterization of the NS2B/NS3 protease complex from seven viruses belonging to different groups inside the genus Flavivirus. Virus Res. 120 (2006), 79–90.
25. others, et al. Complete genome sequence of Zika virus from the first imported case in Mainland China. Genome Announc., 4, 2016 e00291–16.
26. Enfissi, A., Codrington, J., Roosblad, J., Kazanji, M., Rousset, D., Zika virus genome from the Americas. Lancet 387 (2016), 227–228.
27. Piorkowski, G., Richard, P., Baronti, C., Gallian, P., Charrel, R., Leparc-Goffart, I., de Lamballerie, X., Complete coding sequence of Zika virus from Martinique outbreak in 2015. New Microbes New Infect. 11 (2016), 52–53.
28. Baronti, C., Piorkowski, G., Charrel, R.N., Boubis, L., Leparc-Goffart, I., de Lam- ballerie, X., Complete coding sequence of Zika virus from a French Polynesia outbreak in 2013. Genome Announc., 2, 2014 e00500–14.
29. Brinkworth, R.I., Fairlie, D.P., Leung, D., Young, P.R., Homology model of the dengue 2 virus NS3 protease: putative interactions with both substrate and NS2B cofactor. J. general virol. 80 (1999), 1167–1177.
30. Narayanan, R., Zeka virus therapeutics: drug targets and repurposing medicine from the human genome. MOJ Proteom. Bioinform., 3, 2016, 00084.
31. Kuno, G., Chang, G.-J., J. Biol. Transm. arboviruses reexamination new insights into compon., Mech. unique traits as well as their Evol. trends. Clin. Microbiol. Rev. 18 (2005), 608–637.
32. Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N., Sternberg, M.J., The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10 (2015), 845–858.
33. Nugent, T., Jones, D.T., Transmembrane protein topology prediction using support vector machines. BMC Bioinforma., 10, 2009, 1.
34. Käll, L., Krogh, A., Sonnhammer, E.L., A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 338 (2004), 1027–1036.
35. Kyte, J., Doolittle, R.F., A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 (1982), pp.105–132.
36. Release, S., 2: Prime, Version 3.3. Schrödinger. 2014, LLC, New York, NY.
37. Madhavi Sastry, G., Adzhigirey, M., Day, T., Annabhimoju, R., Sherman, W., Protein and ligand preparation: parameters, protocols, and influence on virtual screening enrichments. J. Computer-Aided Mol. Des. 27 (2013), 221–234.
38. Du, J., Sun, H., Xi, L., Li, J., Yang, Y., Liu, H., Yao, X., Molecular modeling study of checkpoint kinase 1 inhibitors by multiple docking strategies and prime/MM– GBSA calculation. J. Comput. Chem. 32 (2011), 2800–2809.
39. Srivastava, M., Singh, H., Naik, P.K., Molecular modeling evaluation of the antimalarial activity of artemisinin analogues: molecular docking and rescoring using Prime/MM-GBSA Approach. Curr. Res. J. Biol. Sci. 2 (2010), 83–102.
40. Gesto, D., Cerqueira, N., Ramos, M., Fernandes, P., Discovery of new drug- gable sites in the anti-cholesterol target HMG-CoA reductase by computational alanine scanning mutagenesis. J. Mol. Model. 20 (2014), 1–13.
41. Noble, C.G., Seh, C.C., Chao, A.T., Shi, P.Y., Ligand-bound structures of the dengue virus protease reveal the active conformation. J. virol. 86 (2012), 438–446.
42. Erbel, P., Schiering, N., D'Arcy, A., Renatus, M., Kroemer, M., Lim, S.P., Yin, Z., Keller, T.H., Vasudevan, S.G., Hommel, U., Structural basis for the activa- tion of flaviviral NS3 proteases from dengue and West Nile virus. Nat. Struct. Mol. Biol. 13 (2006), 372–373.
43. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E.U.C.S.F., Chimera visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612.
44. Needleman, S.B., Wunsch, C.D., A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48 (1970), 443–453.
45. Meng, E.C., Pettersen, E.F., Couch, G.S., Huang, C.C., Ferrin, T.E., Tools for integrated sequence-structure analysis with UCSF Chimera. BMC Bioinforma., 7, 2006, p1.
46. Sievers, Fabian, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7, 2011, p.539.
47. Ward, J.J., Sodhi, J.S., McGuffin, L.J., Buxton, B.F., Jones, D.T., Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337 (2004), 635–645.
48. Capra, J.A., Singh, M., Predicting functionally important residues from sequence conservation. Bioinformatics 23 (2007), 1875–1882.
49. Edwards, Y.J., Cottage, A., Bioinformatics methods to predict protein struc- ture and function. Mol. Biotechnol. 23 (2003), 139–166.
50. Mueller, N.H., Yon, C., Ganesh, V.K., Padmanabhan, R., Characterization of the West Nile virus protease substrate specificity and inhibitors. Int. J. Biochem. cell Biol. 39 (2007), 606–614.
51. Falgout, B., Miller, R., Lai, C., Deletion analysis of dengue virus type 4 nonstructural protein NS2B: identification of a domain required for NS2B-NS3 protease activity. J. Virol. 67 (1993), 2034–2042.
52. Chernov, A.V., Shiryaev, S.A., Aleshin, A.E., Ratnikov, B.I., Smith, J.W., Lid- dington, R.C., Strongin, A.Y., The two-component NS2B-NS3 proteinase represses DNA unwinding activity of the West Nile virus NS3 helicase. J. Biol. Chem. 283 (2008), 17270–17278.
53. Condotta, S.A., Martin, M.M., Boutin, M., Jean, F., Detection and in-cell selectivity profiling of the full-length West Nile virus NS2B/NS3 serine protease using membrane-anchored fluorescent substrates. Biol. Chem. 391 (2010), 549–559.
54. Lin, C., Amberg, S.M., Chambers, T.J., Rice, C.M., Cleavage at a novel site in the NS4A region by the yellow fever virus NS2B-3 proteinase is a prerequisite for processing at the downstream 4A/4B signalase site. J. virol. 67 (1993), 2327–2335.
55. others„, et al. Enhancement of hepatitis C virus NS3 proteinase activity by as- sociation with NS4A-specific synthetic peptides: identification of sequence and critical residues of NS4A for the cofactor activity. Virology 225 (1996), 328–338.
56. Urbanowski, M.D., Hobman, T.C., The West Nile virus capsid protein blocks apoptosis through a phosphatidylinositol 3-kinase-dependent mechanism. J. virol. 87 (2013), 872–881.
57. Youn, S., Cho, H., Fremont, D.H., Diamond, M.S., A short N-terminal peptide motif on flavivirus nonstructural protein NS1 modulates cellular targeting and immune recognition. J. virol. 84 (2010), 9516–9532.
58. Quinan, B.R., Flesch, I.E., Pinho, T.M., Coelho, F.M., Tscharke, D.C., da Fonseca, F.G., An intact signal peptide on dengue virus E protein enhances immunogenicity for CD8+ T cells and antibody when expressed from modified vaccinia Ankara. Vaccine 32 (2014), pp.2972–2979.
59. Blobel, G., Dobberstein, B., Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67 (1975), 835–851.
60. Stocks, C., Lobigs, M., Signal peptidase cleavage at the flavivirus C-prM junction: dependence on the viral NS2B-3 protease for efficient processing requires de- terminants in C, the signal peptide, and prM. J. virol. 72 (1998), 2141–2149.
61. Markoff, L., In vitro processing of dengue virus structural proteins: cleavage of the pre-membrane protein. J. virol. 63 (1989), 3345–3352.
62. Su, X.-C., Ozawa, K., Qi, R., Vasudevan, S.G., Lim, S.P., Otting, G., NMR analysis of the dynamic exchange of the NS2B cofactor between open and closed conformations of the West Nile virus NS2B-NS3 protease. PLoS Negl. Trop. Dis., 3, 2009, e561.
63. Yusof, R., Clum, S., Wetzel, M., Murthy, H.K., Padmanabhan, R., Purified NS2B/NS3 serine protease of dengue virus type 2 exhibits cofactor NS2B dependence for cleavage of substrates with dibasic amino acids in vitro. J. Biol. Chem. 275 (2000), 9963–9969.
64. Zuo, Z., Liew, O.W., Chen, G., Chong, P.C.J., Lee, S.H., Chen, K., Jiang, H., Puah, C.M., Zhu, W., Mechanism of NS2B-mediated activation of NS3pro in dengue virus: molecular dynamics simulations and bioassays. J. virol. 83 (2009), 1060–1070.
65. Falgout, B., Pethel, M., Zhang, Y., Lai, C., Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of dengue virus nonstructural proteins. J. virol. 65 (1991), 2467–2475.
66. Cahour, A., Falgout, B., Lai, C., Cleavage of the dengue virus polyprotein at the NS3/NS4A and NS4B/NS5 junctions is mediated by viral protease NS2B-NS3, whereas NS4A/NS4B may be processed by a cellular protease. J. virol. 66 (1992), 1535–1542.
67. Nall, T.A., Chappell, K.J., Stoermer, M.J., Fang, N.-X., Tyndall, J.D., Young, P.R., Fairlie, D.P., Enzymatic characterization and homology model of a catalytically active recombinant West Nile virus NS3 protease. J. Biol. Chem. 279 (2004), 48535–48542.
68. Love, R.A., Parge, H.E., Wickersham, J.A., Hostomsky, Z., Habuka, N., Moomaw, E.W., Adachi, T., Hostomska, Z., The crystal structure of hepatitis C virus NS3 proteinase reveals a trypsin-like fold and a structural zinc binding site. Cell 87 (1996), 331–342.
69. others, et al. Crystal structure of the hepatitis C virus NS3 protease domain complexed with a synthetic NS4A cofactor peptide. Cell 87 (1996), 343–355.
70. Zhang, L., Mohan, P.M., Padmanabhan, R., Processing and localization of Dengue virus type 2 polyprotein precursor NS3-NS4A-NS4B-NS5. J. virol. 66 (1992), 7549–7554.
71. Aleshin, A.E., Shiryaev, S.A., Strongin, A.Y., Liddington, R.C., Structural evidence for regulation and specificity of flaviviral proteases and evolution of the Flaviviridae fold. Protein Sci. 16 (2007), 795–806.
72. Robin, G., Chappell, K., Stoermer, M.J., Hu, S.-H., Young, P.R., Fairlie, D.P., Martin, J.L., Structure of West Nile virus NS3 protease: ligand stabilization of the catalytic conformation. J. Mol. Biol. 385 (2009), 1568–1577.
73. Chen, W.-N., Loscha, K.V., Nitsche, C., Graham, B., Otting, G., The dengue virus NS2B–NS3 protease retains the closed conformation in the complex with BPTI. FEBS Lett. 588 (2014), 2206–2211.
74. Dunker, A.K., Brown, C.J., Lawson, J.D., Iakoucheva, L.M., Obradovic, Z., Intrinsic disorder and protein function. Biochemistry 41 (2002), 6573–6582.
75. Ortiz, J.F., MacDonald, M.L., Masterson, P., Uversky, V.N., Siltberg-Liberles, J., Rapid evolutionary dynamics of structural disorder as a potential driving force for biological divergence in flaviviruses. Genome Biol. Evol. 5 (2013), 504–513.
76. De Almeida, H., Bastos, I.M., Ribeiro, B.M., Maigret, B., Santana, J.M., New binding site conformations of the dengue virus NS3 protease accessed by molecular dynamics simulation. PloS one, 8, 2013, e72402.
77. Schüller, A., Yin, Z., Chia, C.B., Doan, D.N., Kim, H.-K., Shang, L., Loh, T.P., Hill, J., Vasudevan, S.G., Tripeptide inhibitors of dengue and West Nile virus NS2B–NS3 protease. Antivir. Res. 92 (2011), 96–101.
78. Khan, Asif, et al. Conservation and variability of dengue virus proteins: implications for vaccine design. PLoS Negl. Trop. Dis., 2, 2008, e272.
79. Panchenko, A.R., Kondrashov, F., Bryant, S., Prediction of functional sites by analysis of sequence and structure conservation. Protein Sci. 13 (2004), 884–892.
80. Wang, K., Samudrala, R., Incorporating background frequency improves entropy-based residue conservation measures. BMC Bioinforma., 7, 2006, 385.
81. Chothia, C., Janin, J., Principles of protein-protein recognition. Nature 256 (1975), 705–708.
82. Caffery, D.R., Somaroo, S., Hughes, J.D., Mintseris, J., Huang, E.S., Are protein-protein interfaces more conserved in sequence than the rest of the protein surface?. Protein Sci. 13 (2004), 190–202.