Genotypic differences in dengue virus neutralization are explained by a single amino acid mutation that modulates virus breathing

mBio

Volumn 6, Issue 6, 2015, Pages

  Dowd, Kimberly A ^a   DeMaso, Christina R ^a   Pierson, Theodore C ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; LYSINE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY E111; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; E PROTEIN TH SMAN, DENGUE VIRUS; EPITOPE; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DENGUE VIRUS; DENGUE VIRUS 1; GENETIC VARIABILITY; GENOTYPE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SENSITIVITY ANALYSIS; STRAIN DIFFERENCE; VIRAL PHENOMENA AND FUNCTIONS; VIRUS BREATHING; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS NEUTRALIZATION; VIRUS STRAIN; AMINO ACID SUBSTITUTION; CHEMISTRY; GENETICS; HUMAN; IMMUNOLOGY; MISSENSE MUTATION; MOLECULAR MODEL; PROTEIN CONFORMATION; SERODIAGNOSIS;

AMINO ACID SUBSTITUTION; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DENGUE VIRUS; EPITOPES; HUMANS; MODELS, MOLECULAR; MUTATION, MISSENSE; NEUTRALIZATION TESTS; PROTEIN CONFORMATION; VIRAL ENVELOPE PROTEINS;

EID: 84952836886     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01559-15     Document Type: Article

References (62)

1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GRW, Simmons CP, Scott TW, Farrar JJ, Hay SI. 2013. The global distribution and burden of dengue. Nature 496:504-507. http://dx.doi.org/10.1038/nature12060.
2. Kaufmann B, Rossmann MG. 2011. Molecular mechanisms involved in the early steps of flavivirus cell entry. Microbes Infect 13:1-9. http:// dx.doi.org/10.1016/j.micinf.2010.09.005.
3. Holmes EC, Twiddy SS. 2003. The origin, emergence and evolutionary genetics of dengue virus. Infect Genet Evol 3:19-28. http://dx.doi.org/ 10.1016/S1567-1348(03)00004-2.
4. Rico-Hesse R. 1990. Molecular evolution and distribution of dengue viruses type 1 and 2 in nature. Virology 174:479-493. http://dx.doi.org/ 10.1016/0042-6822(90)90102-W.
5. Goncalvez AP, Escalante AA, Pujol FH, Ludert JE, Tovar D, Salas RA, Liprandi F. 2002. Diversity and evolution of the envelope gene of dengue virus type 1. Virology 303:110-119. http://dx.doi.org/10.1006/ viro.2002.1686.
6. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, Lenches E, Jones CT, Mukhopadhyay S, Chipman PR, Strauss EG, Baker TS, Strauss JH. 2002. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717-725. http:// dx.doi.org/10.1016/S0092-8674(02)00660-8.
7. Zhang X, Ge P, Yu X, Brannan JM, Bi G, Zhang Q, Schein S, Zhou ZH. 2013. Cryo-EM structure of the mature dengue virus at 3.5-A resolution. Nat Struct Mol Biol 20:105-110. http://dx.doi.org/10.1038/nsmb.2463.
8. Pierson TC, Fremont DH, Kuhn RJ, Diamond MS. 2008. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 4:229-238. http://dx.doi.org/10.1016/j.chom.2008.08.004.
9. Stiasny K, Kiermayr S, Holzmann H, Heinz FX. 2006. Cryptic properties of a cluster of dominant flavivirus cross-reactive antigenic sites. J Virol 80:9557-9568. http://dx.doi.org/10.1128/JVI.00080-06.
10. Crill WD, Roehrig JT. 2001. 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 75:7769-7773. http://dx.doi.org/10.1128/ JVI.75.16.7769-7773.2001.
11. Kuhn RJ, Dowd KA, Beth Post C, Pierson TC. 2015. Shake, rattle, and roll: impact of the dynamics of flavivirus particles on their interactions with the host. Virology 479-480:508-517. http://dx.doi.org/10.1016/ j.virol.2015.03.025.
12. Li Q, Yafal AG, Lee YM, Hogle J, Chow M. 1994. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J Virol 68:3965-3970.
13. Yewdell JW, Taylor A, Yellen A, Caton A, Gerhard W, Bachi T. 1993. Mutations in or near the fusion peptide of the influenza virus hemagglutinin affect an antigenic site in the globular region. J Virol 67:933-942.
14. Dowd KA, Jost CA, Durbin AP, Whitehead SS, Pierson TC. 2011. A dynamic landscape for antibody binding modulates antibody-mediated neutralization of West Nile virus. PLoS Pathog 7:e1002111. http:// dx.doi.org/10.1371/journal.ppat.1002111.
15. Dowd KA, Mukherjee S, Kuhn RJ, Pierson TC. 2014. Combined effects of the structural heterogeneity and dynamics of flaviviruses on antibody recognition. J Virol 88:11726-11737. http://dx.doi.org/10.1128/ JVI.01140-14.
16. Sabo MC, Luca VC, Ray SC, Bukh J, Fremont DH, Diamond MS. 2012. Hepatitis C virus epitope exposure and neutralization by antibodies is affected by time and temperature. Virology 422:174-184. http:// dx.doi.org/10.1016/j.virol.2011.10.023.
17. Lewis JK, Bothner B, Smith TJ, Siuzdak G. 1998. Antiviral agent blocks breathing of the common cold virus. Proc Natl Acad Sci U S A 95: 6774-6778. http://dx.doi.org/10.1073/pnas.95.12.6774.
18. Roy A, Post CB. 2012. Long-distance correlations of rhinovirus capsid dynamics contribute to uncoating and antiviral activity. Proc Natl Acad Sci U S A 109:5271-5276. http://dx.doi.org/10.1073/pnas.1119174109.
19. Fibriansah G, Ng TS, Kostyuchenko VA, Lee J, Lee S, Wang J, Lok SM. 2013. Structural changes in dengue virus when exposed to a temperature of 37°C. J Virol 87:7585-7592. http://dx.doi.org/10.1128/JVI.00757-13.
20. Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS, Rossmann MG. 2013. Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci U S A 110:6795-6799. http://dx.doi.org/ 10.1073/pnas.1304300110.
21. Kostyuchenko VA, Chew PL, Ng TS, Lok SM. 2014. Near-atomic resolution cryo-electron microscopic structure of dengue serotype 4 virus. J Virol 88:477-482. http://dx.doi.org/10.1128/JVI.02641-13.
22. Whitehead SS, Blaney JE, Durbin AP, Murphy BR. 2007. Prospects for a dengue virus vaccine. Nat Rev Microbiol 5:518-528. http://dx.doi.org/ 10.1038/nrmicro1690.
23. Austin SK, Dowd KA, Shrestha B, Nelson CA, Edeling MA, Johnson S, Pierson TC, Diamond MS, Fremont DH. 2012. Structural basis of differential neutralization of DENV-1 genotypes by an antibody that recognizes a cryptic epitope. PLoS Pathog 8:e1002930. http://dx.doi.org/ 10.1371/journal.ppat.1002930.
24. Lok SM, Kostyuchenko V, Nybakken GE, Holdaway HA, Battisti AJ, Sukupolvi-Petty S, Sedlak D, Fremont DH, Chipman PR, Roehrig JT, Diamond MS, Kuhn RJ, Rossmann MG. 2008. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat Struct Mol Biol 15:312-317. http://dx.doi.org/10.1038/nsmb.1382.
25. Nybakken GE, Oliphant T, Johnson S, Burke S, Diamond MS, Fremont DH. 2005. Structural basis of West Nile virus neutralization by a therapeutic antibody. Nature 437:764-769. http://dx.doi.org/10.1038/ nature03956.
26. Oliphant T, Engle M, Nybakken GE, Doane C, Johnson S, Huang L, Gorlatov S, Mehlhop E, Marri A, Chung KM, Ebel GD, Kramer LD, Fremont DH, Diamond MS. 2005. Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus. Nat Med 11:522-530. http://dx.doi.org/10.1038/nm1240.
27. Oliphant T, Nybakken GE, Engle M, Xu Q, Nelson CA, Sukupolvi-Petty S, Marri A, Lachmi BE, Olshevsky U, Fremont DH, Pierson TC, Diamond MS. 2006. Antibody recognition and neutralization determinants on domains I and II of West Nile virus envelope protein. J Virol 80:12149-12159. http://dx.doi.org/10.1128/JVI.01732-06.
28. Shrestha B, Brien JD, Sukupolvi-Petty S, Austin SK, Edeling MA, Kim T, O'Brien KM, Nelson CA, Johnson S, Fremont DH, Diamond MS. 2010. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog 6:e1000823. http://dx.doi.org/10.1371/journal.ppat.1000823.
29. Ansarah-Sobrinho C, Nelson S, Jost CA, Whitehead SS, Pierson TC. 2008. Temperature-dependent production of pseudoinfectious dengue reporter virus particles by complementation. Virology 381:67-74. http:// dx.doi.org/10.1016/j.virol.2008.08.021.
30. Belmusto-Worn VE, Sanchez JL, McCarthy K, Nichols R, Bautista CT, Magill AJ, Pastor-Cauna G, Echevarria C, Laguna-Torres VA, Samame BK, Baldeon ME, Burans JP, Olson JG, Bedford P, Kitchener S, Monath TP. 2005. Randomized, double-blind, phase III, pivotal field trial of the comparative immunogenicity, safety, and tolerability of two yellow fever 17D vaccines (Arilvax and YF-VAX) in healthy infants and children in Peru. Am J Trop Med Hyg 72:189-197.
31. Heinz FX, Holzmann H, Essl A, Kundi M. 2007. Field effectiveness of vaccination against tick-borne encephalitis. Vaccine 25:7559-7567. http://dx.doi.org/10.1016/j.vaccine.2007.08.024.
32. Mason RA, Tauraso NM, Spertzel RO, Ginn RK. 1973. Yellow fever vaccine: direct challenge of monkeys given graded doses of 17D vaccine. Appl Microbiol 25:539-544.
33. Monath TP, Nichols R, Archambault WT, Moore L, Marchesani R, Tian J, Shope RE, Thomas N, Schrader R, Furby D, Bedford P. 2002. Comparative safety and immunogenicity of two yellow fever 17D vaccines (ARILVAX and YF-VAX) in a phase III multicenter, double-blind clinical trial. Am J Trop Med Hyg 66:533-541.
34. Capeding MR, Tran NH, Hadinegoro SR, Ismail HI, Chotpitayasunondh T, Chua MN, Luong CQ, Rusmil K, Wirawan DN, Nallusamy R, Pitisuttithum P, Thisyakorn U, Yoon IK, van der Vliet D, Langevin E, Laot T, Hutagalung Y, Frago C, Boaz M, Wartel TA, Tornieporth NG, Saville M, Bouckenooghe A, CYD14 Study Group. 2014. Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial. Lancet 384:1358-1365. http://dx.doi.org/10.1016/S0140-6736(14)61060-6.
35. Villar L, Dayan GH, Arredondo-Garcia JL, Rivera DM, Cunha R, Deseda C, Reynales H, Costa MS, Morales-Ramirez JO, Carrasquilla G, Rey LC, Dietze R, Luz K, Rivas E, Miranda Montoya MC, Cortes Supelano M, Zambrano B, Langevin E, Boaz M, Tornieporth N, Saville M, Noriega F, CYD14 Study Group. 2015. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med 372:113-123. http://dx.doi.org/10.1056/NEJMoa1411037.
36. Diamond MS, Pierson TC, Fremont DH. 2008. The structural immunology of antibody protection against West Nile virus. Immunol Rev 225: 212-225. http://dx.doi.org/10.1111/j.1600-065X.2008.00676.x.
37. Brien JD, Austin SK, Sukupolvi-Petty S, O'Brien KM, Johnson S, Fremont DH, Diamond MS. 2010. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J Virol 84: 10630-10643. http://dx.doi.org/10.1128/JVI.01190-10.
38. Lanciotti RS, Gubler DJ, Trent DW. 1997. Molecular evolution and phylogeny of dengue-4 viruses. J Gen Virol 78:2279-2284. http:// dx.doi.org/10.1099/0022-1317-78-9-2279.
39. Sukupolvi-Petty S, Austin SK, Engle M, Brien JD, Dowd KA, Williams KL, Johnson S, Rico-Hesse R, Harris E, Pierson TC, Fremont DH, DiamondMS. 2010. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J Virol 84:9227-9239. http:// dx.doi.org/10.1128/JVI.01087-10.
40. Sukupolvi-Petty S, Brien JD, Austin SK, Shrestha B, Swayne S, Kahle K, Doranz BJ, Johnson S, Pierson TC, Fremont DH, Diamond MS. 2013. Functional analysis of antibodies against dengue virus type 4 reveals strain-dependent epitope exposure that impacts neutralization and protection. J Virol 87:8826-8842. http://dx.doi.org/10.1128/JVI.01314-13.
41. Wahala WMPB, Donaldson EF, de Alwis R, Accavitti-Loper MA, Baric RS, de Silva AM. 2010. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog 6:e1000821. http:// dx.doi.org/10.1371/journal.ppat.1000821.
42. Mukhopadhyay S, Kim BS, Chipman PR, Rossmann MG, Kuhn RJ. 2003. Structure of West Nile virus. Science 302:248. http://dx.doi.org/ 10.1126/science.1089316.
43. Pierson TC, Diamond MS. 2012. Degrees of maturity: the complex structure and biology of flaviviruses. Curr Opin Virol 2:168-175. http:// dx.doi.org/10.1016/j.coviro.2012.02.011.
44. Plevka P, Battisti AJ, Junjhon J, Winkler DC, Holdaway HA, Keelapang P, Sittisombut N, Kuhn RJ, Steven AC, Rossmann MG. 2011. Maturation of flaviviruses starts from one or more icosahedrally independent nucleation centres. EMBO Rep 12:602-606. http://dx.doi.org/10.1038/ embor.2011.75.
45. Nelson S, Jost CA, Xu Q, Ess J, Martin JE, Oliphant T, Whitehead SS, Durbin AP, Graham BS, Diamond MS, Pierson TC. 2008. Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLoS Pathog 4:e1000060. http://dx.doi.org/10.1371/ journal.ppat.1000060.
46. Chow M, Yabrov R, Bittle J, Hogle J, Baltimore D. 1985. Synthetic peptides from four separate regions of the poliovirus type 1 capsid protein VP1 induce neutralizing antibodies. Proc Natl Acad SciUSA82:910-914. http://dx.doi.org/10.1073/pnas.82.3.910.
47. Emini EA, Jameson BA, Wimmer E. 1983. Priming for and induction of anti-poliovirus neutralizing antibodies by synthetic peptides. Nature 304: 699-703. http://dx.doi.org/10.1038/304699a0.
48. Hogle JM, Chow M, Filman DJ. 1985. Three-dimensional structure of poliovirus at 2.9-A resolution. Science 229:1358-1365. http://dx.doi.org/ 10.1126/science.2994218.
49. Katpally U, Fu TM, Freed DC, Casimiro DR, Smith TJ. 2009. Antibodies to the buried N terminus of rhinovirus VP4 exhibit cross-serotypic neutralization. J Virol 83:7040-7048. http://dx.doi.org/10.1128/JVI.00557-09.
50. Pulli T, Lankinen H, Roivainen M, Hyypiä T. 1998. Antigenic sites of coxsackievirus A9. Virology 240:202-212. http://dx.doi.org/10.1006/ viro.1997.8908.
51. Munro JB, Gorman J, Ma X, Zhou Z, Arthos J, Burton DR, Koff WC, Courter JR, Smith AB, III, Kwong PD, Blanchard SC, Mothes W. 2014. Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 346:759-763. http://dx.doi.org/10.1126/ science.1254426.
52. Cockburn JJ, Navarro Sanchez ME, Goncalvez AP, Zaitseva E, Stura EA, Kikuti CM, Duquerroy S, Dussart P, Chernomordik LV, Lai CJ, Rey FA. 2012. Structural insights into the neutralization mechanism of a higher primate antibody against dengue virus. EMBO J 31:767-779. http://dx.doi.org/10.1038/emboj.2011.439.
53. Pierson TC, Kuhn RJ. 2012. Capturing a virus while it catches its breath. Structure 20:200-202. http://dx.doi.org/10.1016/j.str.2012.01.014.
54. Crowell RL, Philipson L. 1971. Specific alterations of coxsackievirus B3 eluted from HeLa cells. J Virol 8:509-515.
55. Fricks CE, Hogle JM. 1990. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J Virol 64:1934-1945.
56. Carson SD. 2014. Kinetic models for receptor-catalyzed conversion of coxsackievirus B3 to A-particles. J Virol 88:11568-11575. http:// dx.doi.org/10.1128/JVI.01790-14.
57. Organtini LJ, Makhov AM, Conway JF, Hafenstein S, Carson SD. 2014. Kinetic and structural analysis of coxsackievirus B3 receptor interactions and formation of the A-particle. J Virol 88:5755-5765. http://dx.doi.org/ 10.1128/JVI.00299-14.
58. Curry S, Chow M, Hogle JM. 1996. The poliovirus 135S particle is infectious. J Virol 70:7125-7131.
59. Butan C, Filman DJ, Hogle JM. 2014. Cryo-electron microscopy reconstruction shows poliovirus 135S particles poised for membrane interaction and RNA release. J Virol 88:1758-1770. http://dx.doi.org/10.1128/ JVI.01949-13.
60. Luca VC, AbiMansour J, Nelson CA, Fremont DH. 2012. Crystal structure of the Japanese encephalitis virus envelope protein. J Virol 86: 2337-2346. http://dx.doi.org/10.1128/JVI.06072-11.
61. Pierson TC, Sánchez MD, Puffer BA, Ahmed AA, Geiss BJ, Valentine LE, Altamura LA, Diamond MS, Doms RW. 2006. A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus infection. Virology 346:53-65. http://dx.doi.org/10.1016/ j.virol.2005.10.030.
62. Mukherjee S, Lin TY, Dowd KA, Manhart CJ, Pierson TC. 2011. The infectivity of prM-containing partially mature West Nile virus does not require the activity of cellular furin-like proteases. J Virol 85: 12067-12072. http://dx.doi.org/10.1128/JVI.05559-11.