Human CD4+ T cell responses to an attenuated tetravalent dengue vaccine parallel those induced by natural infection in magnitude, HLA restriction, and antigen specificity

Journal of Virology

Volumn 91, Issue 5, 2017, Pages

  Angelo, Michael A ^a,b   Grifoni, Alba ^a,b   O'Rourke, Patrick H ^a,b   Sidney, John ^a,b   Paul, Sinu ^a,b   Peters, Bjoern ^a,b   de Silva, Aruna D ^a,b,g   Phillips, Elizabeth ^c,d   Mallal, Simon ^c,d   Diehl, Sean A ^e   Kirkpatrick, Beth D ^e   Whitehead, Stephen S ^f   Durbin, Anna P ^g   Sette, Alessandro ^a,b   Weiskopf, Daniela ^a,b  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b MURDOCH UNIVERSITY   (Australia)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

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

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

^g Genetech Research Institute   (Sri Lanka)

Author keywords

CD4; CD4+ T cell; Dengue virus; HLA; Live attenuated; Live attenuated vaccine; MHC; T cells; tetravalent; TV005; vaccines

Indexed keywords

CAPSID PROTEIN; DENGUE VACCINE; HLA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5; LIVE VACCINE; VIRAL PROTEIN; VIRUS ANTIBODY;

ADULT; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MEDIATED CYTOTOXICITY; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DENGUE; DONOR; FEMALE; HUMAN; HUMAN EXPERIMENT; IMMUNOREGULATION; INNATE IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MALE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; SCREENING; VIRUS IMMUNITY; ADOLESCENT; ANTIBODY SPECIFICITY; CELL CULTURE; DENGUE VIRUS; GENETICS; IMMUNOLOGY; MIDDLE AGED; VACCINATION; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DENGUE; DENGUE VACCINES; DENGUE VIRUS; FEMALE; HLA ANTIGENS; HUMANS; MALE; MIDDLE AGED; VACCINATION; VACCINES, ATTENUATED; VIRAL PROTEINS; YOUNG ADULT;

EID: 85013887418     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02147-16     Document Type: Article

References (33)

1. Guzman MG, Alvarez M, Halstead SB. 2013. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158:1445-1459. https://doi.org/10.1007/s00705-013-1645-3.
2. Srikiatkhachorn A, Yoon IK. 2016. Immune correlates for dengue vaccine development. Expert Rev Vaccines 15:455-465. https://doi.org/10.1586/14760584.2016.1116949.
3. Hoft DF, Babusis E, Worku S, Spencer CT, Lottenbach K, Truscott SM, Abate G, Sakala IG, Edwards KM, Creech CB, Gerber MA, Bernstein DI, Newman F, Graham I, Anderson EL, Belshe RB. 2011. Live and inactivated influenza vaccines induce similar humoral responses, but only live vaccines induce diverse T-cell responses in young children. J Infect Dis 204:845-853. https://doi.org/10.1093/infdis/jir436.
4. Endy TP, Nisalak A, Chunsuttitwat S, Vaughn DW, Green S, Ennis FA, Rothman AL, Libraty DH. 2004. Relationship of preexisting dengue virus (DV) neutralizing antibody levels to viremia and severity of disease in a prospective cohort study of DV infection in Thailand. J Infect Dis 189: 990-1000. https://doi.org/10.1086/382280.
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, 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. https://doi.org/10.1016/S0140-6736(14)61060-6.
6. Gordon A, Kuan G, Mercado JC, Gresh L, Aviles W, Balmaseda A, Harris E. 2013. The Nicaraguan pediatric dengue cohort study: incidence of inapparent and symptomatic dengue virus infections, 2004-2010. PLoS Negl Trop Dis 7:e2462. https://doi.org/10.1371/journal.pntd.0002462.
7. Kirkpatrick BD, Whitehead SS, Pierce KK, Tibery CM, Grier PL, Hynes NA, Larsson CJ, Sabundayo BP, Talaat KR, Janiak A, Carmolli MP, Luke CJ, Diehl SA, Durbin AP. 2016. The live attenuated dengue vaccine TV003 elicits complete protection against dengue in a human challenge model. Sci Transl Med 8:330ra336. https://doi.org/10.1126/scitranslmed.aaf1517.
8. 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, CYD15 Study Group. 2015. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med 372:113-123. https://doi.org/10.1056/NEJMoa1411037.
9. Yauch LE, Zellweger RM, Kotturi MF, Qutubuddin A, Sidney J, Peters B, Prestwood TR, Sette A, Shresta S. 2009. A protective role for dengue virus-specific CD8+ T cells. J Immunol 182:4865-4873. https://doi.org/10.4049/jimmunol.0801974.
10. Elong Ngono A, Chen HW, Tang WW, Joo Y, King K, Weiskopf D, Sidney J, Sette A, Shresta S. 2016. Protective role of cross-reactive CD8 T cells against dengue virus infection. EBioMedicine 13:284-293. https://doi.org/10.1016/j.ebiom.2016.10.006.
11. Zellweger RM, Tang WW, Eddy WE, King K, Sanchez MC, Shresta S. 2015. CD8+ T cells can mediate short-term protection against heterotypic dengue virus reinfection in mice. J Virol 89:6494-6505. https://doi.org/10.1128/JVI.00036-15.
12. Weiskopf D, Angelo MA, de Azeredo EL, Sidney J, Greenbaum JA, Fernando AN, Broadwater A, Kolla RV, De Silva AD, de Silva AM, Mattia KA, Doranz BJ, Grey HM, Shresta S, Peters B, Sette A. 2013. Comprehensive analysis of dengue virus-specific responses supports an HLA-linked protective role for CD8+ T cells. Proc Natl Acad Sci U S A 110: E2046-E2053. https://doi.org/10.1073/pnas.1305227110.
13. Sallusto F. 2016. Heterogeneity of human CD4(+) T cells against microbes. Annu Rev Immunol 34:317-334. https://doi.org/10.1146/annurev-immunol-032414-112056.
14. Crotty S. 2011. Follicular helper CD4 T cells (TFH). Annu Rev Immunol 29:621-663. https://doi.org/10.1146/annurev-immunol-031210-101400.
15. Yauch LE, Prestwood TR, May MM, Morar MM, Zellweger RM, Peters B, Sette A, Shresta S. 2010. CD4+ T cells are not required for the induction of dengue virus-specific CD8+ T cell or antibody responses but contribute to protection after vaccination. J Immunol 185:5405-5416. https://doi.org/10.4049/jimmunol.1001709.
16. Weiskopf D, Bangs DJ, Sidney J, Kolla RV, De Silva AD, de Silva AM, Crotty S, Peters B, Sette A. 2015. Dengue virus infection elicits highly polarized CX3CR1+ cytotoxic CD4+ T cells associated with protective immunity. Proc Natl Acad Sci U S A 112:E4256-E4263. https://doi.org/10.1073/pnas.1505956112.
17. Weiskopf D, Angelo MA, Grifoni A, O'Rourke PH, Sidney J, Paul S, De Silva AD, Phillips E, Mallal S, Premawansa S, Premawansa G, Wijewickrama A, Peters B, Sette A. 2016. HLA DRB1 alleles are associated with different response magnitudes of dengue virus specific CD4+ T cell responses. J Infect Dis 214:1117-1124. https://doi.org/10.1093/infdis/jiw309.
18. Rivino L, Kumaran EA, Jovanovic V, Nadua K, Teo EW, Pang SW, Teo GH, Gan VC, Lye DC, Leo YS, Hanson BJ, Smith KG, Bertoletti A, Kemeny DM, MacAry PA. 2013. Differential targeting of viral components by CD4+ versus CD8+ T lymphocytes in dengue virus infection. J Virol 87: 2693-2706. https://doi.org/10.1128/JVI.02675-12.
19. Vannice KS, Durbin A, Hombach J. 2016. Status of vaccine research and development of vaccines for dengue. Vaccine 34:2934-2938. https://doi.org/10.1016/j.vaccine.2015.12.073.
20. Durbin AP, Kirkpatrick BD, Pierce KK, Elwood D, Larsson CJ, Lindow JC, Tibery C, Sabundayo BP, Shaffer D, Talaat KR, Hynes NA, Wanionek K, Carmolli MP, Luke CJ, Murphy BR, Subbarao K, Whitehead SS. 2013. A single dose of any of four different live attenuated tetravalent dengue vaccines is safe and immunogenic in flavivirus-naive adults: a randomized, double-blind clinical trial. J Infect Dis 207:957-965. https://doi.org/10.1093/infdis/jis936.
21. Whitehead SS. 2016. Development of TV003/TV005, a single dose, highly immunogenic live attenuated dengue vaccine; what makes this vaccine different from the Sanofi-Pasteur CYD vaccine? Expert Rev Vaccines 15:509-517. https://doi.org/10.1586/14760584.2016.1115727.
22. Weiskopf D, Cerpas C, Angelo MA, Bangs DJ, Sidney J, Paul S, Peters B, Sanches FP, Silvera CG, Costa PR, Kallas EG, Gresh L, de Silva AD, Balmaseda A, Harris E, Sette A. 2015. Human CD8+ T-cell responses against the 4 dengue virus serotypes are associated with distinct patterns of protein targets. J Infect Dis 212:1743-1751. https://doi.org/10.1093/infdis/jiv289.
23. Durbin AP. 2016. A dengue vaccine. Cell 166:1. https://doi.org/10.1016/j.cell.2016.06.036.
24. de Alwis R, Bangs DJ, Angelo MA, Cerpas C, Fernando A, Sidney J, Peters B, Gresh L, Balmaseda A, de Silva AD, Harris E, Sette A, Weiskopf D. 2016. Immunodominant dengue virus-specific CD8+ T cell responses are associated with a memory PD-1α phenotype. J Virol 90:4771-4779. https://doi.org/10.1128/JVI.02892-15.
25. Weiskopf D, Angelo MA, Bangs DJ, Sidney J, Paul S, Peters B, de Silva AD, Lindow JC, Diehl SA, Whitehead S, Durbin A, Kirkpatrick B, Sette A. 2015. The human CD8+ T cell responses induced by a live attenuated tetravalent dengue vaccine are directed against highly conserved epitopes. J Virol 89:120-128. https://doi.org/10.1128/JVI.02129-14.
26. Malavige GN, Rostron T, Rohanachandra LT, Jayaratne SD, Fernando N, De Silva AD, Liyanage M, Ogg G. 2011. HLA class I and class II associations in dengue viral infections in a Sri Lankan population. PLoS One 6:e20581. https://doi.org/10.1371/journal.pone.0020581.
27. Nguyen TP, Kikuchi M, Vu TQ, Do Q H, Tran TT, Vo DT, Ha MT, Vo VT, Cao TP, Tran VD, Oyama T, Morita K, Yasunami M, Hirayama K. 2008. Protective and enhancing HLA alleles, HLA-DRB1*0901 and HLA-A*24, for severe forms of dengue virus infection, dengue hemorrhagic fever and dengue shock syndrome. PLoS Negl Trop Dis 2:e304. https://doi.org/10.1371/journal.pntd.0000304.
28. Weiskopf D, Angelo MA, Sidney J, Peters B, Shresta S, Sette A. 2014. Immunodominance changes as a function of the infecting dengue virus serotype and primary versus secondary infection. J Virol 88: 11383-11394. https://doi.org/10.1128/JVI.01108-14.
29. Wikramaratna PS, Simmons CP, Gupta S, Recker M. 2010. The effects of tertiary and quaternary infections on the epidemiology of dengue. PLoS One 5:e12347. https://doi.org/10.1371/journal.pone.0012347.
30. Lindow JC, Durbin AP, Whitehead SS, Pierce KK, Carmolli MP, Kirkpatrick BD. 2013. Vaccination of volunteers with low-dose, live-attenuated, dengue viruses leads to serotype-specific immunologic and virologic profiles. Vaccine 31:3347-3352. https://doi.org/10.1016/j.vaccine.2013.05.075.
31. Wang P, Sidney J, Dow C, Mothe B, Sette A, Peters B. 2008. A systematic assessment of MHC class II peptide binding predictions and evaluation of a consensus approach. PLoS Comput Biol 4:e1000048. https://doi.org/10.1371/journal.pcbi.1000048.
32. Wang P, Sidney J, Kim Y, Sette A, Lund O, Nielsen M, Peters B. 2010. Peptide binding predictions for HLA DR, DP and DQ molecules. BMC Bioinformatics 11:568. https://doi.org/10.1186/1471-2105-11-568.
33. Bui HH, Sidney J, Li W, Fusseder N, Sette A. 2007. Development of an epitope conservancy analysis tool to facilitate the design of epitopebased diagnostics and vaccines. BMC Bioinformatics 8:361. https://doi.org/10.1186/1471-2105-8-361.