A new quaternary structure epitope on dengue virus serotype 2 is the target of durable type-specific neutralizing antibodies

mBio

Volumn 6, Issue 5, 2015, Pages

  Gallichotte, E N ^a   Widman, D G ^b   Yount, B L ^b   Wahala, W M ^a   Durbin, A ^c   Whitehead, S ^d   Sariol, C A ^e,f   Crowe, J E ^g   De Silva, A M ^a   Barica, R S ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b IL   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

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

^e UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^f UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

^g UNIVERSITY OF PUERTO RICO MEDICAL SCIENCES CAMPUS   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; INTERCELLULAR ADHESION MOLECULE 3; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN; E-GLYCOPROTEIN, DENGUE VIRUS TYPE 2; VIRUS ANTIBODY;

ADULT; AEDES ALBOPICTUS; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; CROSS REACTION; DENGUE VIRUS 2; DENGUE VIRUS 4; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN QUATERNARY STRUCTURE; VIRUS NEUTRALIZATION; VIRUS TITRATION; BLOOD; DENGUE VIRUS; IMMUNOLOGY;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DENGUE VIRUS; EPITOPES, B-LYMPHOCYTE; HUMANS; VIRAL ENVELOPE PROTEINS;

EID: 84946594505     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01461-15     Document Type: Article

References (31)

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 GR, 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. Schmitz J, Roehrig J, Barrett A, Hombach J. 2011. Next generation dengue vaccines: a review of candidates in preclinical development. Vaccine 29:7276-7284. http://dx.doi.org/10.1016/j.vaccine.2011.07.017.
3. Wan SW, Lin CF, Wang S, Chen YH, Yeh TM, Liu HS, Anderson R, Lin YS. 2013. Current progress in dengue vaccines. J Biomed Sci 20:37. http://dx.doi.org/10.1186/1423-0127-20-37.
4. 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.
5. 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. 2014. Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlledtrial. Lancet 384:1358-1365. http://dx.doi.org/10.1016/S0140-6736(14)61060-6.
6. Villar L, Dayan GH, Arredondo-García JL, Rivera DM, Cunha R, Deseda C, Reynales H, Costa MS, Morales-Ramírez JO, Carrasquilla G, Rey LC, Dietze R, Luz K, Rivas E, Miranda Montoya MC, Cortés Supelano M, Zambrano B, Langevin E, Boaz M, Tornieporth N. 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.
7. Hadinegoro SR, Arredondo-García JL, Capeding MR, Deseda C, Chotpitayasunondh T, Dietze R, Ismail HI, Reynales H, Limkittikul K, Rivera-Medina DM, Tran HN, Bouckenooghe A, Chansinghakul D, Cortés M, Fanouillere K, Forrat R, Frago C, Gailhardou S, Jackson N, Noriega F, Plennevaux E, Wartel TA, Zambrano B, Saville M, CYDTDV Dengue Vaccine Working Group. 27 July 2015. Efficacy and longterm safety of a dengue vaccine in regions of endemic disease. N Engl J Med. http://dx.doi.org/10.1056/NEJMoa1506223.
8. Roehrig JT. 2003. Antigenic structure of flavivirus proteins. Adv Virus Res 59:141-175. http://dx.doi.org/10.1016/S0065-3527(03)59005-4.
9. 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.
10. de Alwis R, Smith SA, Olivarez NP, Messer WB, Huynh JP, Wahala WM, White LJ, Diamond MS, Baric RS, Crowe JE, de Silva AM. 2012. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc Natl Acad Sci U S A 109:7439-7444. http://dx.doi.org/10.1073/pnas.1200566109.
11. Dejnirattisai W, Wongwiwat W, Supasa S, Zhang X, Dai X, Rouvinski A, Rouvinsky A, Jumnainsong A, Edwards C, Quyen NT, Duangchinda T, Grimes JM, Tsai WY, Lai CY, Wang WK, Malasit P, Farrar J, Simmons CP, Zhou ZH, Rey FA. 2015. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol 16:170-177. http://dx.doi.org/10.1038/ni.3058.
12. Fibriansah G, Tan JL, Smith SA, de Alwis AR, Ng TS, Kostyuchenko VA, Ibarra KD, Wang J, Harris E, de Silva A, Crowe JE, Lok SM. 2014. A potent anti-dengue human antibody preferentially recognizes the conformation of E protein monomers assembled on the virus surface. EMBO Mol Med 6:358-371. http://dx.doi.org/10.1002/emmm.201303404.
13. Rouvinski A, Guardado-Calvo P, Barba-Spaeth G, Duquerroy S, Vaney MC, Kikuti CM, Navarro Sanchez ME, Dejnirattisai W, Wongwiwat W, Haouz A, Girard-Blanc C, Petres S, Shepard WE, Desprès P, Arenzana-Seisdedos F, Dussart P, Mongkolsapaya J, Screaton GR, Rey FA. 2015. Recognition determinants of broadly neutralizing human antibodies against dengue viruses. Nature 520:-109-U260. http://dx.doi.org/10.1038/nature14130.
14. Teoh EP, Kukkaro P, Teo EW, Lim AP, Tan TT, Yip A, Schul W, Aung M, Kostyuchenko VA, Leo YS, Chan SH, Smith KG, Chan AH, Zou G, Ooi EE, Kemeny DM, Tan GK, Ng JK, Ng ML, Alonso S. 2012. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci Transl Med 4:139ra83. http://dx.doi.org/10.1126/scitranslmed.3003888.
15. Fibriansah G, Ibarra KD, Ng TS, Smith SA, Tan JL, Lim XN, Ooi JS, Kostyuchenko VA, Wang J, de Silva AM, Harris E, Crowe JE, Lok SM. 2015. Dengue virus. Cryo-EM structure of an antibody that neutralizes dengue virus type 2 by locking E protein dimers. Science 349:88-91. http://dx.doi.org/10.1126/science.aaa8651.
16. 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.
17. Mukherjee S, Dowd KA, Manhart CJ, Ledgerwood JE, Durbin AP, Whitehead SS, Pierson TC. 2014. Mechanism and significance of cell type-dependent neutralization of flaviviruses. J Virol 88:7210-7220. http://dx.doi.org/10.1128/JVI.03690-13.
18. Zybert IA, van der Ende-Metselaar H, Wilschut J, Smit JM. 2008. Functional importance of dengue virus maturation: infectious properties of immature virions. J Gen Virol 89:3047-3051. http://dx.doi.org/10.1099/vir.0.2008/002535-0.
19. Smith SA, de Alwis AR, Kose N, Harris E, Ibarra KD, Kahle KM, Pfaff JM, Xiang X, Doranz BJ, de Silva AM, Austin SK, Sukupolvi-Petty S, Diamond MS, Crowe JE. 2013. The potent and broadly neutralizing human dengue virus-specific monoclonal antibody 1C19 reveals a unique cross-reactive epitope on the bc loop of domain II of the envelope protein. mBio 4:e00873-13. http://dx.doi.org/10.1128/mBio.00873-13.
20. De Alwis R, Beltramello M, Messer WB, Sukupolvi-Petty S, Wahala WM, Kraus A, Olivarez NP, Pham Q, Brien JD, Brian J, Tsai WY, Wang WK, Halstead S, Kliks S, Diamond MS, Baric R, Lanzavecchia A, Sallusto F, de Silva AM. 2011. In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl Trop Dis 5:e1188. http://dx.doi.org/10.1371/journal.pntd.0001188.
21. 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.
22. 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.
23. Wahala WM, Huang C, Butrapet S, White LJ, de Silva AM. 2012. Recombinant dengue type 2 viruses with altered e protein domain III epitopes are efficiently neutralized by human immune sera. J Virol 86: 4019-4023. http://dx.doi.org/10.1128/JVI.06871-11.
24. Wahala WM, Kraus AA, Haymore LB, Accavitti-Loper MA, de Silva AM. 2009. Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody. Virology 392:103-113. http://dx.doi.org/10.1016/j.virol.2009.06.037.
25. Durbin AP, Kirkpatrick BD, Pierce KK, Schmidt AC, Whitehead SS. 2011. Development and clinical evaluation of multiple investigational monovalent DENV vaccines to identify components for inclusion in a live attenuated tetravalent DENV vaccine. Vaccine 29:7242-7250. http://dx.doi.org/10.1016/j.vaccine.2011.07.023.
26. Smith SA, de Alwis AR, Kose N, Jadi RS, de Silva AM, Crowe JE. 2014. Isolation of dengue virus-specific memory B cells with live virus antigen from human subjects following natural infection reveals the presence of diverse novel functional groups of antibody clones. J Virol 88: 12233-12241. http://dx.doi.org/10.1128/JVI.00247-14.
27. Lindesmith LC, Ferris MT, Mullan CW, Ferreira J, Debbink K, Swanstrom J, Richardson C, Goodwin RR, Baehner F, Mendelman PM, Bargatze RF, BaricRS. 2015. Broad blockade antibody responses inhumanvolunteers after immunization with a multivalent norovirus VLP candidate vaccine: immunological analyses from a phase I clinical trial. PLoSMed 12:e1001807. http://dx.doi.org/10.1371/journal.pmed.1001807.
28. Scobey T, Yount BL, Sims AC, Donaldson EF, Agnihothram SS, Menachery VD, Graham RL, Swanstrom J, Bove PF, Kim JD, Grego S, Randell SH, Baric RS. 2013. Reverse genetics with a full-length infectious cDNA of the Middle East respiratory syndrome coronavirus. Proc Natl Acad Sci U S A 110:16157-16162. http://dx.doi.org/10.1073/pnas.1311542110.
29. Yount B, Curtis KM, Fritz EA, Hensley LE, Jahrling PB, Prentice E, Denison MR, Geisbert TW, Baric RS. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci U S A 100:12995-13000. http://dx.doi.org/10.1073/pnas.1735582100.
30. Messer WB, Yount B, Hacker KE, Donaldson EF, Huynh JP, de Silva AM, Baric RS. 2012. Development and characterization of a reverse genetic system for studying dengue virus serotype 3 strain variation and neutralization. PLoS Negl Trop Dis 6:e1486. http://dx.doi.org/10.1371/journal.pntd.0001486.
31. White LJ, Sariol CA, Mattocks MD, Wahala WMPB, Yingsiwaphat V, Collier ML, Whitley J, Mikkelsen R, Rodriguez IV, Martinez MI, de Silva A, Johnston RE. 2013. An alphavirus vector-based tetravalent dengue vaccine induces a rapid and protective immune response in macaques that differs qualitatively from immunity induced by live virus infection. J Virol 87:3409-3424. http://dx.doi.org/10.1128/JVI.02298-12.