1887

Abstract

Dengue virus (DENV) is one the most important viral pathogens worldwide. Currently there is an imperative need for a reliable vaccine capable of inducing durable protection against all four serotypes. We have previously reported strongly neutralizing and highly specific antibody responses from all four serotypes to a DNA vaccine based on an engineered version of DENV E protein’s domain III (DIII). Here, we show that monovalent and tetravalent immunizations with the DIII-based DNA vaccines are also capable of inducing highly stable antibody responses that remain strongly neutralizing over long periods of time. Our results demonstrate that DNA-vaccinated mice maintain a strong antibody response in terms of titre, avidity and virus-neutralizing capability 1 year after immunization.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001094
2018-06-20
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/99/8/1078.html?itemId=/content/journal/jgv/10.1099/jgv.0.001094&mimeType=html&fmt=ahah

References

  1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW et al. The global distribution and burden of dengue. Nature 2013; 496:504–507 [View Article][PubMed]
    [Google Scholar]
  2. Flipse J, Smit JM. The complexity of a dengue vaccine: a review of the human antibody response. PLoS Negl Trop Dis 2015; 9:e0003749 [View Article][PubMed]
    [Google Scholar]
  3. Lindenbach BD, Heinz-Jurgen T, Rice CM. Flaviviridae: the viruses and their replication. In Fields BN, Howley PM. (editors) Fields' Virology Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2007
    [Google Scholar]
  4. Modis Y. Relating structure to evolution in class II viral membrane fusion proteins. Curr Opin Virol 2014; 5:34–41 [View Article][PubMed]
    [Google Scholar]
  5. Mukhopadhyay S, Kuhn RJ, Rossmann MG. A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 2005; 3:13–22 [View Article][PubMed]
    [Google Scholar]
  6. Beltramello M, Williams KL, Simmons CP, Macagno A, Simonelli L et al. 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 [View Article][PubMed]
    [Google Scholar]
  7. Dejnirattisai W, Wongwiwat W, Supasa S, Zhang X, Dai X et al. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol 2015; 16:170–177 [View Article][PubMed]
    [Google Scholar]
  8. Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S et al. Cross-reacting antibodies enhance dengue virus infection in humans. Science 2010; 328:745–748 [View Article][PubMed]
    [Google Scholar]
  9. Katzelnick LC, Gresh L, Halloran ME, Mercado JC, Kuan G et al. Antibody-dependent enhancement of severe dengue disease in humans. Science 2017; 358:929–932 [View Article][PubMed]
    [Google Scholar]
  10. Midgley CM, Bajwa-Joseph M, Vasanawathana S, Limpitikul W, Wills B et al. An in-depth analysis of original antigenic sin in dengue virus infection. J Virol 2011; 85:410–421 [View Article][PubMed]
    [Google Scholar]
  11. Crill WD, Roehrig JT. 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 [View Article][PubMed]
    [Google Scholar]
  12. Gromowski GD, Barrett ND, Barrett AD. Characterization of dengue virus complex-specific neutralizing epitopes on envelope protein domain III of dengue 2 virus. J Virol 2008; 82:8828–8837 [View Article][PubMed]
    [Google Scholar]
  13. Vanblargan LA, Goo L, Pierson TC. Deconstructing the antiviral neutralizing-antibody response: implications for vaccine development and immunity. Microbiol Mol Biol Rev 2016; 80:989–1010 [View Article][PubMed]
    [Google Scholar]
  14. Pierson TC, Fremont DH, Kuhn RJ, Diamond MS. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 2008; 4:229–238 [View Article][PubMed]
    [Google Scholar]
  15. Poggianella M, Slon Campos JL, Chan KR, Tan HC, Bestagno M et al. Dengue E protein domain III-based DNA immunisation induces strong antibody responses to all four viral serotypes. PLoS Negl Trop Dis 2015; 9:e0003947 [View Article][PubMed]
    [Google Scholar]
  16. Slon Campos JL, Poggianella M, Marchese S, Mossenta M, Rana J et al. DNA-immunisation with dengue virus E protein domains I/II, but not domain III, enhances Zika, West Nile and Yellow Fever virus infection. PLoS One 2017; 12:e0181734 [View Article][PubMed]
    [Google Scholar]
  17. de Souza VA, Fernandes S, Araújo ES, Tateno AF, Oliveira OM et al. Use of an immunoglobulin G avidity test to discriminate between primary and secondary dengue virus infections. J Clin Microbiol 2004; 42:1782–1784 [View Article][PubMed]
    [Google Scholar]
  18. Rey FA, Stiasny K, Heinz FX. Flavivirus structural heterogeneity: implications for cell entry. Curr Opin Virol 2017; 24:132–139 [View Article][PubMed]
    [Google Scholar]
  19. Dowd KA, Demaso CR, Pierson TC. Genotypic differences in dengue virus neutralization are explained by a single amino acid mutation that modulates virus breathing. MBio 2015; 6:e01559-15 [View Article][PubMed]
    [Google Scholar]
  20. Rey FA, Stiasny K, Vaney MC, Dellarole M, Heinz FX. The bright and the dark side of human antibody responses to flaviviruses: lessons for vaccine design. EMBO Rep 2018; 19:206–224 [View Article][PubMed]
    [Google Scholar]
  21. Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS et al. Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci USA 2013; 110:6795–6799 [View Article][PubMed]
    [Google Scholar]
  22. Fibriansah G, Ng TS, Kostyuchenko VA, Lee J, Lee S et al. Structural changes in dengue virus when exposed to a temperature of 37°C. J Virol 2013; 87:7585–7592 [View Article][PubMed]
    [Google Scholar]
  23. Fibriansah G, Ibarra KD, Ng TS, Smith SA, Tan JL et al. Dengue virus. Cryo-EM structure of an antibody that neutralizes dengue virus type 2 by locking E protein dimers. Science 2015; 349:88–91 [View Article][PubMed]
    [Google Scholar]
  24. Guy B, Barban V, Mantel N, Aguirre M, Gulia S et al. Evaluation of interferences between dengue vaccine serotypes in a monkey model. Am J Trop Med Hyg 2009; 80:302–311[PubMed]
    [Google Scholar]
  25. Hadinegoro SR, Arredondo-García JL, Capeding MR, Deseda C, Chotpitayasunondh T et al. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N Engl J Med 2015; 373:1195–1206 [View Article][PubMed]
    [Google Scholar]
  26. Arredondo-García JL, Hadinegoro SR, Reynales H, Chua MN, Rivera Medina DM et al. Four-year safety follow-up of the tetravalent dengue vaccine efficacy randomized controlled trials in Asia and Latin America. Clin Microbiol Infect 2018 [View Article][PubMed]
    [Google Scholar]
  27. Halstead SB. Safety issues from a Phase 3 clinical trial of a live-attenuated chimeric yellow fever tetravalent dengue vaccine. Hum Vaccin Immunother 2018 [View Article][PubMed]
    [Google Scholar]
  28. Torresi J, Ebert G, Pellegrini M. Vaccines licensed and in clinical trials for the prevention of dengue. Hum Vaccin Immunother 2017; 13:1059–1072 [View Article][PubMed]
    [Google Scholar]
  29. Porter KR, Raviprakash K. Nucleic acid (DNA) immunization as a platform for dengue vaccine development. Vaccine 2015; 33:7135–7140 [View Article][PubMed]
    [Google Scholar]
  30. Vannice KS, Durbin A, Hombach J. Status of vaccine research and development of vaccines for dengue. Vaccine 2016; 34:2934–2938 [View Article][PubMed]
    [Google Scholar]
  31. Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A et al. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 2016; 353:823–826 [View Article][PubMed]
    [Google Scholar]
  32. Priyamvada L, Quicke KM, Hudson WH, Onlamoon N, Sewatanon J et al. Human antibody responses after dengue virus infection are highly cross-reactive to Zika virus. Proc Natl Acad Sci USA 2016; 113:7852–7857 [View Article][PubMed]
    [Google Scholar]
  33. Bardina SV, Bunduc P, Tripathi S, Duehr J, Frere JJ et al. Enhancement of Zika virus pathogenesis by preexisting antiflavivirus immunity. Science 2017; 356:175–180 [View Article][PubMed]
    [Google Scholar]
  34. Pulendran B, Ahmed R. Immunological mechanisms of vaccination. Nat Immunol 2011; 12:509–517 [View Article][PubMed]
    [Google Scholar]
  35. Makhluf H, Shresta S. Development of Zika virus vaccines. Vaccines 2018; 6:7 [View Article][PubMed]
    [Google Scholar]
  36. Danko JR, Kochel T, Teneza-Mora N, Luke TC, Raviprakash K et al. Safety and immunogenicity of a tetravalent dengue DNA vaccine administered with a cationic lipid-based adjuvant in a phase 1 clinical trial. Am J Trop Med Hyg 2018; 98:849–856 [View Article][PubMed]
    [Google Scholar]
  37. Gaudinski MR, Houser KV, Morabito KM, Hu Z, Yamshchikov G et al. Safety, tolerability, and immunogenicity of two Zika virus DNA vaccine candidates in healthy adults: randomised, open-label, phase 1 clinical trials. Lancet 2018; 391:552–562 [View Article][PubMed]
    [Google Scholar]
  38. Richner JM, Himansu S, Dowd KA, Butler SL, Salazar V et al. Modified mRNA vaccines protect against zika virus infection. Cell 2017; 1681125:1114.e10–1125.e10
    [Google Scholar]
  39. Graham BS, Koup RA, Roederer M, Bailer RT, Enama ME et al. Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 DNA candidate vaccine. J Infect Dis 2006; 194:1650–1660 [View Article][PubMed]
    [Google Scholar]
  40. Martin JE, Pierson TC, Hubka S, Rucker S, Gordon IJ et al. A West Nile virus DNA vaccine induces neutralizing antibody in healthy adults during a phase 1 clinical trial. J Infect Dis 2007; 196:1732–1740 [View Article][PubMed]
    [Google Scholar]
  41. Sarwar UN, Costner P, Enama ME, Berkowitz N, Hu Z et al. Safety and immunogenicity of DNA vaccines encoding Ebolavirus and Marburgvirus wild-type glycoproteins in a phase I clinical trial. J Infect Dis 2015; 211:549–557 [View Article][PubMed]
    [Google Scholar]
  42. Shedlock DJ, Weiner DB. DNA vaccination: antigen presentation and the induction of immunity. J Leukoc Biol 2000; 68:793–806[PubMed]
    [Google Scholar]
  43. Khan KH. DNA vaccines: roles against diseases. Germs 2013; 3:26–35 [View Article][PubMed]
    [Google Scholar]
  44. Wang G, Pan L, Zhang Y. Approaches to improved targeting of DNA vaccines. Hum Vaccin 2011; 7:1271–1281 [View Article][PubMed]
    [Google Scholar]
  45. Slon Campos JL, Poggianella M, Marchese S, Bestagno M, Burrone OR. Secretion of dengue virus envelope protein ectodomain from mammalian cells is dependent on domain II serotype and affects the immune response upon DNA vaccination. J Gen Virol 2015; 96:3265–3279 [View Article][PubMed]
    [Google Scholar]
  46. Hombach J. Guidelines for clinical trials of dengue vaccine in endemic areas. J Clin Virol 2009; 46:S7–S9 [View Article][PubMed]
    [Google Scholar]
  47. Toh YX, Gan V, Balakrishnan T, Zuest R, Poidinger M et al. Dengue serotype cross-reactive, anti-e protein antibodies confound specific immune memory for 1 year after infection. Front Immunol 2014; 5:388 [View Article][PubMed]
    [Google Scholar]
  48. Tsen SW, Paik AH, Hung CF, Wu TC. Enhancing DNA vaccine potency by modifying the properties of antigen-presenting cells. Expert Rev Vaccines 2007; 6:227–239 [View Article][PubMed]
    [Google Scholar]
  49. Hammarlund E, Thomas A, Amanna IJ, Holden LA, Slayden OD et al. Plasma cell survival in the absence of B cell memory. Nat Commun 2017; 8:1781 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001094
Loading
/content/journal/jgv/10.1099/jgv.0.001094
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error