Shake, rattle, and roll: Impact of the dynamics of flavivirus particles on their interactions with the host

Virology

Volumn 479-480, Issue , 2015, Pages 508-517

  Kuhn, Richard J ^a   Dowd, Kimberly A ^b   Beth Post, Carol ^c   Pierson, Theodore C ^b  

^a PURDUE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Antibody mediated neutralization; Dengue virus; Flavivirus; Structural dynamics; Viral breathing; West nile virus

Indexed keywords

VIRUS ANTIGEN; VIRUS PROTEIN;

CHEMISTRY; FLAVIVIRUS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION;

ANTIGENS, VIRAL; FLAVIVIRUS; HOST-PATHOGEN INTERACTIONS; PROTEIN CONFORMATION; VIRAL PROTEINS;

EID: 84937511919     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.03.025     Document Type: Review

References (125)

1. Ansarah-Sobrinho C., Nelson S., Jost C.A., Whitehead S.S., Pierson T.C. Temperature-dependent production of pseudoinfectious dengue reporter virus particles by complementation. Virology 2008, 381:67-74.
2. Austin S.K., Dowd K.A., Shrestha B., Nelson C.A., Edeling M.A., Johnson S., Pierson T.C., Diamond M.S., Fremont D.H. Structural basis of differential neutralization of DENV-1 genotypes by an antibody that recognizes a cryptic epitope. PLoS Pathog. 2012, 8:e1002930.
3. Bachi T., Gerhard W., Yewdell J.W. Monoclonal antibodies detect different forms of influenza virus hemagglutinin during viral penetration and biosynthesis. J. Virol. 1985, 55:307-313.
4. Bai Y., Sosnick T.R., Mayne L., Englander S.W. Protein folding intermediates: native-state hydrogen exchange. Science 1995, 269:192-197.
5. Beasley D.W., Barrett A.D. Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein. J. Virol. 2002, 76:13097-13100.
6. Belnap D.M., Filman D.J., Trus B.L., Cheng N., Booy F.P., Conway J.F., Curry S., Hiremath C.N., Tsang S.K., Steven A.C., Hogle J.M. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 2000, 74:1342-1354.
7. Beltramello M., Williams K.L., Simmons C.P., Macagno A., Simonelli L., Quyen N.T., Sukupolvi-Petty S., Navarro-Sanchez E., Young P.R., de Silva A.M., Rey F.A., Varani L., Whitehead S.S., Diamond M.S., Harris E., Lanzavecchia A., Sallusto F. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 2010, 8:271-283.
8. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., Drake J.M., Brownstein J.S., Hoen A.G., Sankoh O., Myers M.F., George D.B., Jaenisch T., Wint G.R., Simmons C.P., Scott T.W., Farrar J.J., Hay S.I. The global distribution and burden of dengue. Nature 2013, 496:504-507.
9. Borbat P.P., Costa-Filho A.J., Earle K.A., Moscicki J.K., Freed J.H. Electron spin resonance in studies of membranes and proteins. Science 2001, 291:266-269.
10. Bothner B., Dong X.F., Bibbs L., Johnson J.E., Siuzdak G. Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J. Biol. Chem. 1998, 273:673-676.
11. Bressanelli S., Stiasny K., Allison S.L., Stura E.A., Duquerroy S., Lescar J., Heinz F.X., Rey F.A. Structure of a flavivirus envelope glycoprotein in its low-pH-induced membrane fusion conformation. EMBO J. 2004, 23:728-738.
12. Carson S.D. Kinetic models for receptor-catalyzed conversion of coxsackievirus B3 to A-particles. J. Virol. 2014, 88:11568-11575.
13. Chen Y., Maguire T., Hileman R.E., Fromm J.R., Esko J.D., Linhardt R.J., Marks R.M. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 1997, 3:866-871.
14. Cherrier M.V., Kaufmann B., Nybakken G.E., Lok S.M., Warren J.T., Chen B.R., Nelson C.A., Kostyuchenko V.A., Holdaway H.A., Chipman P.R., Kuhn R.J., Diamond M.S., Rossmann M.G., Fremont D.H. Structural basis for the preferential recognition of immature flaviviruses by a fusion-loop antibody. EMBO J. 2009, 28:3269-3276.
15. Crill W.D., Roehrig J.T. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J. Virol. 2001, 75:7769-7773.
16. Crowell R.L., Philipson L. Specific alterations of coxsackievirus B3 eluted from HeLa cells. J. Virol. 1971, 8:509-515.
17. Curry S., Chow M., Hogle J.M. The poliovirus 135S particle is infectious. J. Virol. 1996, 70:7125-7131.
18. de Alwis R., Smith S.A., Olivarez N.P., Messer W.B., Huynh J.P., Wahala W.M., White L.J., Diamond M.S., Baric R.S., Crowe J.E., de Silva A.M. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc. Natl. Acad. Sci. USA 2012, 109:7439-7444.
19. Dejnirattisai W., Wongwiwat W., Supasa S., Zhang X., Dai X., Rouvinsky A., Jumnainsong A., Edwards C., Quyen N.T., Duangchinda T., Grimes J.M., Tsai W.Y., Lai C.Y., Wang W.K., Malasit P., Farrar J., Simmons C.P., Zhou Z.H., Rey F.A., Mongkolsapaya J., Screaton G.R. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat. Immunol. 2015, 16:170-177.
20. Diamond M.S., Pierson T.C., Fremont D.H. The structural immunology of antibody protection against West Nile virus. Immunol. Rev. 2008, 225:212-225.
21. Dodson G.G., Lane D.P., Verma C.S. Molecular simulations of protein dynamics: new windows on mechanisms in biology. EMBO Rep. 2008, 9:144-150.
22. Dowd K.A., Jost C.A., Durbin A.P., Whitehead S.S., Pierson T.C. A dynamic landscape for antibody binding modulates antibody-mediated neutralization of West Nile virus. PLoS Pathog. 2011, 7:e1002111.
23. Dowd K.A., Mukherjee S., Kuhn R.J., Pierson T.C. Combined effects of the structural heterogeneity and dynamics of flaviviruses on antibody recognition. J. Virol. 2014, 88:11726-11737.
24. Dowd K.A., Pierson T.C. Antibody-mediated neutralization of flaviviruses: a reductionist view. Virology 2011, 411:306-315.
25. Elshuber S., Allison S.L., Heinz F.X., Mandl C.W. Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J. Gen. Virol. 2003, 84:183-191.
26. Fibriansah G., Ng T.S., Kostyuchenko V.A., Lee J., Lee S., Wang J., Lok S.M. Structural changes in dengue virus when exposed to a temperature of 37°C. J. Virol. 2013, 87:7585-7592.
27. Fibriansah G., Tan J.L., Smith S.A., de Alwis A.R., Ng T.S., Kostyuchenko V.A., Ibarra K.D., Wang J., Harris E., de Silva A., Crowe J.E., Lok S.M. A potent anti-dengue human antibody preferentially recognizes the conformation of E protein monomers assembled on the virus surface. EMBO Mol. Med. 2014, 6:358-371.
28. Fibriansah G., Tan J.L., Smith S.A., de Alwis R., Ng T.S., Kostyuchenko V.A., Jadi R.S., Kukkaro P., de Silva A.M., Crowe J.E., Lok S.M. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat. Commun. 2015, 6:6341.
29. Fricks C.E., Hogle J.M. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 1990, 64:1934-1945.
30. Gromowski G.D., Barrett A.D. Characterization of an antigenic site that contains a dominant, type-specific neutralization determinant on the envelope protein domain III (ED3) of dengue 2 virus. Virology 2007, 366:349-360.
31. Gruenberger M., Pevear D., Diana G.D., Kuechler E., Blaas D. Stabilization of human rhinovirus serotype 2 against pH-induced conformational change by antiviral compounds. J. Gen. Virol. 1991, 72(Pt 2):431-433.
32. Guirakhoo F., Heinz F.X., Mandl C.W., Holzmann H., Kunz C. Fusion activity of flaviviruses: comparison of mature and immature (prM-containing) tick-borne encephalitis virions. J. Gen. Virol. 1991, 72(Pt 6):1323-1329.
33. Hadfield A.T., Lee W., Zhao R., Oliveira M.A., Minor I., Rueckert R.R., Rossmann M.G. The refined structure of human rhinovirus 16 at 2.15A resolution: implications for the viral life cycle. Structure 1997, 5:427-441.
34. Halstead S.B. Neutralization and antibody-dependent enhancement of dengue viruses. Adv. Virus Res. 2003, 60:421-467.
35. Haqqani A.A., Tilton J.C. Entry inhibitors and their use in the treatment of HIV-1 infection. Antivir. Res. 2013, 98:158-170.
36. Harrison S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:690-698.
37. Heinz B.A., Rueckert R.R., Shepard D.A., Dutko F.J., McKinlay M.A., Fancher M., Rossmann M.G., Badger J., Smith T.J. Genetic and molecular analyses of spontaneous mutants of human rhinovirus 14 that are resistant to an antiviral compound. J. Virol. 1989, 63:2476-2485.
38. Hewat E.A., Neumann E., Conway J.F., Moser R., Ronacher B., Marlovits T.C., Blaas D. The cellular receptor to human rhinovirus 2 binds around the 5-fold axis and not in the canyon: a structural view. EMBO J. 2000, 19:6317-6325.
39. Hogle J.M., Chow M., Filman D.J. Three-dimensional structure of poliovirus at 2.9A resolution. Science 1985, 229:1358-1365.
40. Jarmer J., Zlatkovic J., Tsouchnikas G., Vratskikh O., Strauss J., Aberle J.H., Chmelik V., Kundi M., Stiasny K., Heinz F.X. Variation of the specificity of the human antibody responses after tick-borne encephalitis virus infection and vaccination. J. Virol. 2014, 88:13845-13857.
41. Jimenez-Clavero M.A., Douglas A., Lavery T., Garcia-Ranea J.A., Ley V. Immune recognition of swine vesicular disease virus structural proteins: novel antigenic regions that are not exposed in the capsid. Virology 2000, 270:76-83.
42. Junjhon J., Edwards T.J., Utaipat U., Bowman V.D., Holdaway H.A., Zhang W., Keelapang P., Puttikhunt C., Perera R., Chipman P.R., Kasinrerk W., Malasit P., Kuhn R.J., Sittisombut N. Influence of pr-M cleavage on the heterogeneity of extracellular dengue virus particles. J. Virol. 2010, 84:8353-8358.
43. Kanai R., Kar K., Anthony K., Gould L.H., Ledizet M., Fikrig E., Marasco W.A., Koski R.A., Modis Y. Crystal structure of west nile virus envelope glycoprotein reveals viral surface epitopes. J. Virol. 2006, 80:11000-11008.
44. Karplus M., Kuriyan J. Molecular dynamics and protein function. Proc. Natl. Acad. Sci. USA 2005, 102:6679-6685.
45. Kaufmann B., Nybakken G.E., Chipman P.R., Zhang W., Diamond M.S., Fremont D.H., Kuhn R.J., Rossmann M.G. West Nile virus in complex with the Fab fragment of a neutralizing monoclonal antibody. Proc. Natl. Acad. Sci. USA 2006, 103:12400-12404.
46. Kaufmann B., Vogt M.R., Goudsmit J., Holdaway H.A., Aksyuk A.A., Chipman P.R., Kuhn R.J., Diamond M.S., Rossmann M.G. Neutralization of West Nile virus by cross-linking of its surface proteins with Fab fragments of the human monoclonal antibody CR4354. Proc. Natl. Acad. Sci. USA 2010, 107:18950-18955.
47. Kiermayr S., Stiasny K., Heinz F.X. Impact of quaternary organization on the antigenic structure of the tick-borne encephalitis virus envelope glycoprotein E. J. Virol. 2009, 83:8482-8491.
48. Kliks S.C., Nimmanitya S., Nisalak A., Burke D.S. Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants. Am. J. Trop. Med. Hyg. 1988, 38:411-419.
49. Kneller G.R. Quasielastic neutron scattering and relaxation processes in proteins: analytical and simulation-based models. Phys. Chem. Chem. Phys.: PCCP 2005, 7:2641-2655.
50. Kolatkar P.R., Bella J., Olson N.H., Bator C.M., Baker T.S., Rossmann M.G. Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J. 1999, 18:6249-6259.
51. Konishi E., Mason P.W. Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the premembrane protein. J. Virol. 1993, 67:1672-1675.
52. Kostyuchenko V.A., Chew P.L., Ng T.S., Lok S.M. Near-atomic resolution cryo-electron microscopic structure of dengue serotype 4 virus. J. Virol. 2014, 88:477-482.
53. Kuhn R.J., Zhang W., Rossmann M.G., Pletnev S.V., Corver J., Lenches E., Jones C.T., Mukhopadhyay S., Chipman P.R., Strauss E.G., Baker T.S., Strauss J.H. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 2002, 108:717-725.
54. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 1998, 393:648-659.
55. Lewis J.K., Bothner B., Smith T.J., Siuzdak G. Antiviral agent blocks breathing of the common cold virus. Proc. Natl. Acad. Sci. USA 1998, 95:6774-6778.
56. Li Q., Yafal A.G., Lee Y.M., Hogle J., Chow M. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J. Virol. 1994, 68:3965-3970.
57. Lok S.M., Kostyuchenko V., Nybakken G.E., Holdaway H.A., Battisti A.J., Sukupolvi-Petty S., Sedlak D., Fremont D.H., Chipman P.R., Roehrig J.T., Diamond M.S., Kuhn R.J., Rossmann M.G. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 2008, 15:312-317.
58. Lorenz I.C., Allison S.L., Heinz F.X., Helenius A. Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J. Virol. 2002, 76:5480-5491.
59. Luca V.C., AbiMansour J., Nelson C.A., Fremont D.H. Crystal structure of the Japanese encephalitis virus envelope protein. J. Virol. 2012, 86:2337-2346.
60. Ma L., Jones C.T., Groesch T.D., Kuhn R.J., Post C.B. Solution structure of dengue virus capsid protein reveals another fold. Proc. Natl. Acad. Sci. USA 2004, 101:3414-3419.
61. Marsh J.A., Teichmann S.A., Forman-Kay J.D. Probing the diverse landscape of protein flexibility and binding. Curr. Opin. Struct. Biol. 2012, 22:643-650.
62. Mateu M.G. Assembly, stability and dynamics of virus capsids. Arch. Biochem. Biophys. 2013, 531:65-79.
63. McDermott B.M., Rux A.H., Eisenberg R.J., Cohen G.H., Racaniello V.R. Two distinct binding affinities of poliovirus for its cellular receptor. J. Biol. Chem. 2000, 275:23089-23096.
64. McSharry J.J., Caliguiri L.A., Eggers H.J. Inhibition of uncoating of poliovirus by arildone, a new antiviral drug. Virology 1979, 97:307-315.
65. Modis Y., Ogata S., Clements D., Harrison S.C. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 2003, 100:6986-6991.
66. Modis Y., Ogata S., Clements D., Harrison S.C. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004, 427:313-319.
67. Mukhopadhyay S., Kim B.S., Chipman P.R., Rossmann M.G., Kuhn R.J. Structure of West Nile virus. Science 2003, 302:248.
68. Mukhopadhyay S., Kuhn R.J., Rossmann M.G. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 2005, 3:13-22.
69. Munro J.B., Gorman J., Ma X., Zhou Z., Arthos J., Burton D.R., Koff W.C., Courter J.R., Smith A.B., Kwong P.D., Blanchard S.C., Mothes W. Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 2014, 346:759-763.
70. Munro J.B., Mothes W. The HIV-1 Env trimer in HD. Structure 2014, 22:935-936.
71. Nelson S., Jost C.A., Xu Q., Ess J., Martin J.E., Oliphant T., Whitehead S.S., Durbin A.P., Graham B.S., Diamond M.S., Pierson T.C. Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLoS Pathog. 2008, 4:e1000060.
72. Nybakken G.E., Oliphant T., Johnson S., Burke S., Diamond M.S., Fremont D.H. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 2005, 437:764-769.
73. Oliphant T., Engle M., Nybakken G.E., Doane C., Johnson S., Huang L., Gorlatov S., Mehlhop E., Marri A., Chung K.M., Ebel G.D., Kramer L.D., Fremont D.H., Diamond M.S. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat. Med. 2005, 11:522-530.
74. Oliphant T., Nybakken G.E., Austin S.K., Xu Q., Bramson J., Loeb M., Throsby M., Fremont D.H., Pierson T.C., Diamond M.S. Induction of epitope-specific neutralizing antibodies against West Nile virus. J. Virol. 2007, 81:11828-11839.
75. Oliphant T., Nybakken G.E., Engle M., Xu Q., Nelson C.A., Sukupolvi-Petty S., Marri A., Lachmi B.E., Olshevsky U., Fremont D.H., Pierson T.C., Diamond M.S. Antibody recognition and neutralization determinants on domains I and II of West Nile Virus envelope protein. J. Virol. 2006, 80:12149-12159.
76. Olson N.H., Kolatkar P.R., Oliveira M.A., Cheng R.H., Greve J.M., McClelland A., Baker T.S., Rossmann M.G. Structure of a human rhinovirus complexed with its receptor molecule. Proc. Natl. Acad. Sci. USA 1993, 90:507-511.
77. Organtini L.J., Makhov A.M., Conway J.F., Hafenstein S., Carson S.D. Kinetic and structural analysis of coxsackievirus B3 receptor interactions and formation of the A-particle. J. Virol. 2014, 88:5755-5765.
78. Osawa M., Takeuchi K., Ueda T., Nishida N., Shimada I. Functional dynamics of proteins revealed by solution NMR. Curr. Opin. Struct. Biol. 2012, 22:660-669.
79. Otto M.J., Fox M.P., Fancher M.J., Kuhrt M.F., Diana G.D., McKinlay M.A. In vitro activity of WIN 51711, a new broad-spectrum antipicornavirus drug. Antimicrob. Agents Chemother. 1985, 27:883-886.
80. Pancera M., Zhou T., Druz A., Georgiev I.S., Soto C., Gorman J., Huang J., Acharya P., Chuang G.Y., Ofek G., Stewart-Jones G.B., Stuckey J., Bailer R.T., Joyce M.G., Louder M.K., Tumba N., Yang Y., Zhang B., Cohen M.S., Haynes B.F., Mascola J.R., Morris L., Munro J.B., Blanchard S.C., Mothes W., Connors M., Kwong P.D. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 2014, 514:455-461.
81. Park C., Marqusee S. Probing the high energy states in proteins by proteolysis. J. Mol. Biol. 2004, 343:1467-1476.
82. Pevear D.C., Fancher M.J., Felock P.J., Rossmann M.G., Miller M.S., Diana G., Treasurywala A.M., McKinlay M.A., Dutko F.J. Conformational change in the floor of the human rhinovirus canyon blocks adsorption to HeLa cell receptors. J. Virol. 1989, 63:2002-2007.
83. Pevear D.C., Tull T.M., Seipel M.E., Groarke J.M. Activity of pleconaril against enteroviruses. Antimicrob. Agents Chemother. 1999, 43:2109-2115.
84. Phelps D.K., Post C.B. A novel basis of capsid stabilization by antiviral compounds. J. Mol. Biol. 1995, 254:544-551.
85. Pierson T.C., Diamond M.S. Degrees of maturity: the complex structure and biology of flaviviruses. Curr. Opin. Virol. 2012, 2:168-175.
86. Pierson T.C., Kielian M. Flaviviruses: braking the entering. Curr. Opin. Virol. 2013, 3:3-12.
87. Pierson T.C., Xu Q., Nelson S., Oliphant T., Nybakken G.E., Fremont D.H., Diamond M.S. The stoichiometry of antibody-mediated neutralization and enhancement of West Nile virus infection. Cell Host Microbe 2007, 1:135-145.
88. Plevka P., Battisti A.J., Junjhon J., Winkler D.C., Holdaway H.A., Keelapang P., Sittisombut N., Kuhn R.J., Steven A.C., Rossmann M.G. Maturation of flaviviruses starts from one or more icosahedrally independent nucleation centres. EMBO Rep. 2011, 12:602-606.
89. Racaniello V.R. Picornaviridae: the viruses and their replication. Fields virology 2007, Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia. 5th ed. B.N. Fields, D.M. Knipe, P.M. Howley (Eds.).
90. Rayaprolu V., Kruse S., Kant R., Venkatakrishnan B., Movahed N., Brooke D., Lins B., Bennett A., Potter T., McKenna R., Agbandje-McKenna M., Bothner B. Comparative analysis of adeno-associated virus capsid stability and dynamics. J. Virol. 2013, 87:13150-13160.
91. Reisdorph N., Thomas J.J., Katpally U., Chase E., Harris K., Siuzdak G., Smith T.J. Human rhinovirus capsid dynamics is controlled by canyon flexibility. Virology 2003, 314:34-44.
92. Ren J., Wang X., Hu Z., Gao Q., Sun Y., Li X., Porta C., Walter T.S., Gilbert R.J., Zhao Y., Axford D., Williams M., McAuley K., Rowlands D.J., Yin W., Wang J., Stuart D.I., Rao Z., Fry E.E. Picornavirus uncoating intermediate captured in atomic detail. Nat. Commun. 2013, 4:1929.
93. Roivainen M., Piirainen L., Rysa T., Narvanen A., Hovi T. An immunodominant N-terminal region of VP1 protein of poliovirion that is buried in crystal structure can be exposed in solution. Virology 1993, 195:762-765.
94. Rossmann M.G., Arnold E., Erickson J.W., Frankenberger E.A., Griffith J.P., Hecht H.J., Johnson J.E., Kamer G., Luo M., Mosser A.G., et al. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 1985, 317:145-153.
95. Rossmann M.G., Palmenberg A.C. Conservation of the putative receptor attachment site in picornaviruses. Virology 1988, 164:373-382.
96. Rouvinski A., Guardado-Calvo P., Barba-Spaeth G., Duquerroy S., Vaney M.C., Kikuti C.M., Navarro Sanchez M.E., Dejnirattisai W., Wongwiwat W., Haouz A., Girard-Blanc C., Petres S., Shepard W.E., Despres P., Arenzana-Seisdedos F., Dussart P., Mongkolsapaya J., Screaton G.R., Rey F.A. Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature 2015.
97. Roy A., Post C.B. Long-distance correlations of rhinovirus capsid dynamics contribute to uncoating and antiviral activity. Proc. Natl. Acad. Sci. USA 2012, 109:5271-5276.
98. Sabo M.C., Luca V.C., Ray S.C., Bukh J., Fremont D.H., Diamond M.S. Hepatitis C virus epitope exposure and neutralization by antibodies is affected by time and temperature. Virology 2012, 422:174-184.
99. Sanchez M.D., Pierson T.C., McAllister D., Hanna S.L., Puffer B.A., Valentine L.E., Murtadha M.M., Hoxie J.A., Doms R.W. Characterization of neutralizing antibodies to West Nile virus. Virology 2005, 336:70-82.
100. Sauter P., Chehadeh W., Lobert P.E., Lazrek M., Goffard A., Soumillon M., Caloone D., Vantyghem M.C., Weill J., Fajardy I., Alm G., Lucas B., Hober D. A part of the VP4 capsid protein exhibited by coxsackievirus B4 E2 is the target of antibodies contained in plasma from patients with type 1 diabetes. J. Med. Virol. 2008, 80:866-878.
101. Shrestha B., Brien J.D., Sukupolvi-Petty S., Austin S.K., Edeling M.A., Kim T., O'Brien K.M., Nelson C.A., Johnson S., Fremont D.H., Diamond M.S. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog. 2010, 6:e1000823.
102. Smith T.J., Chase E.S., Schmidt T.J., Olson N.H., Baker T.S. Neutralizing antibody to human rhinovirus 14 penetrates the receptor-binding canyon. Nature 1996, 383:350-354.
103. Stiasny K., Kiermayr S., Holzmann H., Heinz F.X. Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J. Virol. 2006, 80:9557-9568.
104. Strauss M., Levy H.C., Bostina M., Filman D.J., Hogle J.M. RNA transfer from poliovirus 135S particles across membranes is mediated by long umbilical connectors. J. Virol. 2013, 87:3903-3914.
105. Sukupolvi-Petty S., Austin S.K., Engle M., Brien J.D., Dowd K.A., Williams K.L., Johnson S., Rico-Hesse R., Harris E., Pierson T.C., Fremont D.H., Diamond M.S. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J. Virol. 2010, 84:9227-9239.
106. Sukupolvi-Petty S., Brien J.D., Austin S.K., Shrestha B., Swayne S., Kahle K., Doranz B.J., Johnson S., Pierson T.C., Fremont D.H., Diamond M.S. Functional analysis of antibodies against dengue virus type 4 reveals strain-dependent epitope exposure that impacts neutralization and protection. J. Virol. 2013, 87:8826-8842.
107. Teoh E.P., Kukkaro P., Teo E.W., Lim A.P., Tan T.T., Yip A., Schul W., Aung M., Kostyuchenko V.A., Leo Y.S., Chan S.H., Smith K.G., Chan A.H., Zou G., Ooi E.E., Kemeny D.M., Tan G.K., Ng J.K., Ng M.L., Alonso S., Fisher D., Shi P.Y., Hanson B.J., Lok S.M., MacAry P.A. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci. Transl. Med. 2012, 4. (139ra183).
108. Thomsen N.K., Poulsen F.M. Low energy of activation for amide hydrogen exchange reactions in proteins supports a local unfolding model. J. Mol. Biol. 1993, 234:234-241.
109. Throsby M., Geuijen C., Goudsmit J., Bakker A.Q., Korimbocus J., Kramer R.A., Clijsters-van der Horst M., de Jong M., Jongeneelen M., Thijsse S., Smit R., Visser T.J., Bijl N., Marissen W.E., Loeb M., Kelvin D.J., Preiser W., ter Meulen J., de Kruif J. Isolation and characterization of human monoclonal antibodies from individuals infected with West Nile Virus. J. Virol. 2006, 80:6982-6992.
110. Tsang S.K., Danthi P., Chow M., Hogle J.M. Stabilization of poliovirus by capsid-binding antiviral drugs is due to entropic effects. J. Mol. Biol. 2000, 296:335-340.
111. Turner R.B., Dutko F.J., Goldstein N.H., Lockwood G., Hayden F.G. Efficacy of oral WIN 54954 for prophylaxis of experimental rhinovirus infection. Antimicrob. Agents Chemother. 1993, 37:297-300.
112. Wahala W.M., Huang C., Butrapet S., White L.J., de Silva A.M. Recombinant dengue type 2 viruses with altered e protein domain III epitopes are efficiently neutralized by human immune sera. J. Virol. 2012, 86:4019-4023.
113. Wahala W.M., Kraus A.A., Haymore L.B., Accavitti-Loper M.A., de Silva A.M. Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology 2009, 392:103-113.
114. Wiggan O., Livengood J.A., Silengo S.J., Kinney R.M., Osorio J.E., Huang C.Y., Stinchcomb D.T. Novel formulations enhance the thermal stability of live-attenuated flavivirus vaccines. Vaccine 2011, 29:7456-7462.
115. Wilen C.B., Tilton J.C., Doms R.W. Molecular mechanisms of HIV entry. Adv. Exp. Med. Biol. 2012, 726:223-242.
116. Williams K.L., Wahala W.M., Orozco S., de Silva A.M., Harris E. Antibodies targeting dengue virus envelope domain III are not required for serotype-specific protection or prevention of enhancement in vivo. Virology 2012, 429:12-20.
117. Witz J., Brown F. Structural dynamics, an intrinsic property of viral capsids. Arch. Virol. 2001, 146:2263-2274.
118. Wu Z., Asokan A., Samulski R.J. Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol. Ther.: J. Am. Soc. Gene Ther. 2006, 14:316-327.
119. Wyatt R., Moore J., Accola M., Desjardin E., Robinson J., Sodroski J. Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J. Virol. 1995, 69:5723-5733.
120. Wyatt R., Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 1998, 280:1884-1888.
121. Yu I.M., Holdaway H.A., Chipman P.R., Kuhn R.J., Rossmann M.G., Chen J. Association of the pr peptides with dengue virus at acidic pH blocks membrane fusion. J. Virol. 2009, 83:12101-12107.
122. Yu I.M., Zhang W., Holdaway H.A., Li L., Kostyuchenko V.A., Chipman P.R., Kuhn R.J., Rossmann M.G., Chen J. Structure of the immature dengue virus at low pH primes proteolytic maturation. Science 2008, 319:1834-1837.
123. Zhang X., Sheng J., Plevka P., Kuhn R.J., Diamond M.S., Rossmann M.G. Dengue structure differs at the temperatures of its human and mosquito hosts. Proc. Natl. Acad. Sci. USA 2013, 110:6795-6799.
124. Zhang Y., Kaufmann B., Chipman P.R., Kuhn R.J., Rossmann M.G. Structure of immature West Nile virus. J. Virol. 2007, 81:6141-6145.
125. Zhang Y., Zhang W., Ogata S., Clements D., Strauss J.H., Baker T.S., Kuhn R.J., Rossmann M.G. Conformational changes of the flavivirus E glycoprotein. Structure 2004, 12:1607-1618.