Prior Dengue Virus Serotype 3 Infection Modulates Subsequent Plasmablast Responses to Zika Virus Infection in Rhesus Macaques

Overview

Journal mBio

Publisher American Society for Microbiology

Specialty Microbiology

Date 2024 Feb 13

PMID 38349142

Authors

Tulika Singh

Itzayana G Miller

Sravani Venkatayogi

Helen Webster

Holly J Heimsath

Josh A Eudailey

Dawn M Dudley

Amit Kumar

Riley J Mangan

Amelia Thein

Matthew T Aliota

Christina M Newman

Mariel S Mohns

Meghan E Breitbach

Madison Berry

Thomas C Friedrich

Kevin Wiehe

David H OConnor

Sallie R Permar

Affiliations

Soon will be listed here.

Abstract

Importance: The Zika virus epidemic of 2015-2016 in the Americas revealed that this mosquito-transmitted virus could be congenitally transmitted during pregnancy and cause birth defects in newborns. Currently, there are no interventions to mitigate this disease and Zika virus is likely to re-emerge. Understanding how protective antibody responses are generated against Zika virus can help in the development of a safe and effective vaccine. One main challenge is that Zika virus co-circulates with related viruses like dengue, such that prior exposure to one can generate cross-reactive antibodies against the other which may enhance infection and disease from the second virus. In this study, we sought to understand how prior dengue virus infection impacts subsequent immunity to Zika virus by single-cell sequencing of antibody producing cells in a second Zika virus infection. Identifying specific qualities of Zika virus immunity that are modulated by prior dengue virus immunity will enable optimal immunization strategies.

Citing Articles

Reconciling heterogeneous dengue virus infection risk estimates from different study designs.

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PMID: 39739790 PMC: 11725863. DOI: 10.1073/pnas.2411768121.

Reconciling heterogeneous dengue virus infection risk estimates from different study designs.

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PMID: 39314937 PMC: 11419196. DOI: 10.1101/2024.09.09.24313375.

References

Puschnik A, Lau L, Cromwell E, Balmaseda A, Zompi S, Harris E . Correlation between dengue-specific neutralizing antibodies and serum avidity in primary and secondary dengue virus 3 natural infections in humans. PLoS Negl Trop Dis. 2013; 7(6):e2274. PMC: 3681624. DOI: 10.1371/journal.pntd.0002274. View

Whitehead S, Blaney J, Durbin A, Murphy B . Prospects for a dengue virus vaccine. Nat Rev Microbiol. 2007; 5(7):518-28. DOI: 10.1038/nrmicro1690. View

Parameswaran P, Liu Y, Roskin K, Jackson K, Dixit V, Lee J . Convergent antibody signatures in human dengue. Cell Host Microbe. 2013; 13(6):691-700. PMC: 4136508. DOI: 10.1016/j.chom.2013.05.008. View

Fahad A, Timm M, Madan B, Burgomaster K, Dowd K, Normandin E . Functional Profiling of Antibody Immune Repertoires in Convalescent Zika Virus Disease Patients. Front Immunol. 2021; 12:615102. PMC: 7959826. DOI: 10.3389/fimmu.2021.615102. View

Priyamvada L, Cho A, Onlamoon N, Zheng N, Huang M, Kovalenkov Y . B Cell Responses during Secondary Dengue Virus Infection Are Dominated by Highly Cross-Reactive, Memory-Derived Plasmablasts. J Virol. 2016; 90(12):5574-85. PMC: 4886779. DOI: 10.1128/JVI.03203-15. View

Sirohi D, Chen Z, Sun L, Klose T, Pierson T, Rossmann M . The 3.8 Å resolution cryo-EM structure of Zika virus. Science. 2016; 352(6284):467-70. PMC: 4845755. DOI: 10.1126/science.aaf5316. View

Singh T, Hwang K, Miller A, Jones R, Lopez C, Dulson S . A Zika virus-specific IgM elicited in pregnancy exhibits ultrapotent neutralization. Cell. 2022; 185(25):4826-4840.e17. PMC: 9742325. DOI: 10.1016/j.cell.2022.10.023. View

Oliveira W, Araujo de Franca G, Carmo E, Duncan B, de Souza Kuchenbecker R, Schmidt M . Infection-related microcephaly after the 2015 and 2016 Zika virus outbreaks in Brazil: a surveillance-based analysis. Lancet. 2017; 390(10097):861-870. DOI: 10.1016/S0140-6736(17)31368-5. View

Silveira E, Kasturi S, Kovalenkov Y, Rasheed A, Yeiser P, Jinnah Z . Vaccine-induced plasmablast responses in rhesus macaques: phenotypic characterization and a source for generating antigen-specific monoclonal antibodies. J Immunol Methods. 2014; 416:69-83. PMC: 4324134. DOI: 10.1016/j.jim.2014.11.003. View

10.

Van Rompay K, Keesler R, Ardeshir A, Watanabe J, Usachenko J, Singapuri A . DNA vaccination before conception protects Zika virus-exposed pregnant macaques against prolonged viremia and improves fetal outcomes. Sci Transl Med. 2019; 11(523). PMC: 7093037. DOI: 10.1126/scitranslmed.aay2736. View

11.

Breitbach M, Newman C, Dudley D, Stewart L, Aliota M, Koenig M . Primary infection with dengue or Zika virus does not affect the severity of heterologous secondary infection in macaques. PLoS Pathog. 2019; 15(8):e1007766. PMC: 6675051. DOI: 10.1371/journal.ppat.1007766. View

12.

Kuhn R, Zhang W, Rossmann M, Pletnev S, Corver J, Lenches E . Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell. 2002; 108(5):717-25. PMC: 4152842. DOI: 10.1016/s0092-8674(02)00660-8. View

13.

Dudley D, Aliota M, Mohr E, Weiler A, Lehrer-Brey G, Weisgrau K . A rhesus macaque model of Asian-lineage Zika virus infection. Nat Commun. 2016; 7:12204. PMC: 4931337. DOI: 10.1038/ncomms12204. View

14.

Katzelnick L, Bos S, Harris E . Protective and enhancing interactions among dengue viruses 1-4 and Zika virus. Curr Opin Virol. 2020; 43:59-70. PMC: 7655628. DOI: 10.1016/j.coviro.2020.08.006. View

15.

Katzelnick L, Montoya M, Gresh L, Balmaseda A, Harris E . Neutralizing antibody titers against dengue virus correlate with protection from symptomatic infection in a longitudinal cohort. Proc Natl Acad Sci U S A. 2016; 113(3):728-33. PMC: 4725482. DOI: 10.1073/pnas.1522136113. View

16.

Collins M, McGowan E, Jadi R, Young E, Lopez C, Baric R . Lack of Durable Cross-Neutralizing Antibodies Against Zika Virus from Dengue Virus Infection. Emerg Infect Dis. 2017; 23(5):773-781. PMC: 5403059. DOI: 10.3201/eid2305.161630. View

17.

Montoya M, Collins M, Dejnirattisai W, Katzelnick L, Puerta-Guardo H, Jadi R . Longitudinal Analysis of Antibody Cross-neutralization Following Zika Virus and Dengue Virus Infection in Asia and the Americas. J Infect Dis. 2018; 218(4):536-545. PMC: 6047418. DOI: 10.1093/infdis/jiy164. View

18.

Nguyen S, Antony K, Dudley D, Kohn S, Simmons H, Wolfe B . Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. PLoS Pathog. 2017; 13(5):e1006378. PMC: 5444831. DOI: 10.1371/journal.ppat.1006378. View

19.

Murphy B, Whitehead S . Immune response to dengue virus and prospects for a vaccine. Annu Rev Immunol. 2011; 29:587-619. DOI: 10.1146/annurev-immunol-031210-101315. View

20.

Fink K . Origin and Function of Circulating Plasmablasts during Acute Viral Infections. Front Immunol. 2012; 3:78. PMC: 3341968. DOI: 10.3389/fimmu.2012.00078. View