1,186
Views
7
CrossRef citations to date
0
Altmetric
Research Paper

Whole inactivated dengue virus-loaded trimethyl chitosan nanoparticle-based vaccine: immunogenic properties in ex vivo and in vivo models

, , , , , , & show all
Pages 2793-2807 | Received 01 Nov 2020, Accepted 26 Jan 2021, Published online: 16 Apr 2021

References

  • Huang YJ, Higgs S, Horne KM, Vanlandingham DL. Flavivirus-mosquito interactions. Viruses. 2014;6:4703–30. doi:10.3390/v6114703.
  • Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, et al. The global distribution and burden of dengue. Nature. 2013;496:504–07. doi:10.1038/nature12060.
  • Rajapakse S. Dengue shock. J Emerg Trauma Shock. 2011;4:120–27. doi:10.4103/0974-2700.76835.
  • Rather IA, Parray HA, Lone JB, Paek WK, Lim J, Bajpai VK, Park YH. Prevention and control strategies to counter dengue virus infection. Front Cell Infect Microbiol. 2017;7:336. doi:10.3389/fcimb.2017.00336.
  • Pitisuttithum P, Bouckenooghe A. The first licensed dengue vaccine: an important tool for integrated preventive strategies against dengue virus infection. Expert Rev Vaccines. 2016;15:795–98. doi:10.1080/14760584.2016.1189331.
  • Hadinegoro SR, Arredondo-Garcia JL, Capeding MR, Deseda C, Chotpitayasunondh T, Dietze R, Muhammad Ismail HI, Reynales H, Limkittikul K, Rivera-Medina DM, et al. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N Engl J Med. 2015;373:1195–206. doi:10.1056/NEJMoa1506223.
  • Arredondo-Garcia JL, Hadinegoro SR, Reynales H, Chua MN, Rivera Medina DM, Chotpitayasunondh T, Tran NH, Deseda CC, Wirawan DN, Cortes Supelano M, 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;24:755–63. doi:10.1016/j.cmi.2018.01.018.
  • Halstead SB. Dengvaxia sensitizes seronegatives to vaccine enhanced disease regardless of age. Vaccine. 2017;35:6355–58. doi:10.1016/j.vaccine.2017.09.089.
  • Flasche S, Wilder-Smith A, Hombach J, Smith PG. Estimating the proportion of vaccine-induced hospitalized dengue cases among Dengvaxia vaccinees in the Philippines. Wellcome Open Res. 2019;4:165. doi:10.12688/wellcomeopenres.15507.1.
  • Handel A, Li Y, McKay B, Pawelek KA, Zarnitsyna V, Antia R. Exploring the impact of inoculum dose on host immunity and morbidity to inform model-based vaccine design. PLoS Comput Biol. 2018;14:e1006505. doi:10.1371/journal.pcbi.1006505.
  • de Alwis R, Smith SA, Olivarez NP, Messer WB, Huynh JP, Wahala WM, White LJ, Diamond MS, Baric RS, Crowe JE Jr, et al. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc Natl Acad Sci U S A. 2012;109:7439–44. doi:10.1073/pnas.1200566109.
  • Tsai WY, Chen HL, Tsai JJ, Dejnirattisai W, Jumnainsong A, Mongkolsapaya J, Screaton G, Crowe JE Jr, Wang WK. Potent neutralizing human monoclonal antibodies preferentially target mature dengue virus particles: implication for novel strategy for dengue vaccine. J Virol. 2018;92:e00056–18. doi:10.1128/jvi.00556-18.
  • Gallichotte EN, Baric TJ, Yount BL Jr, Widman DG, Durbin A, Whitehead S, Baric RS, de Silva AM. Human dengue virus serotype 2 neutralizing antibodies target two distinct quaternary epitopes. PLoS Pathog. 2018;14:e1006934. doi:10.1371/journal.ppat.1006934.
  • Delrue I, Verzele D, Madder A, Nauwynck HJ. Inactivated virus vaccines from chemistry to prophylaxis: merits, risks and challenges. Expert Rev Vaccines. 2012;11:695–719. doi:10.1586/erv.12.38.
  • Sundaram AK, Ewing D, Blevins M, Liang Z, Sink S, Lassan J, Raviprakash K, Defang G, Williams M, Porter KR, et al. Comparison of purified psoralen-inactivated and formalin-inactivated dengue vaccines in mice and nonhuman primates. Vaccine. 2020;38:3313–20. doi:10.1016/j.vaccine.2020.03.008.
  • Hunsawong T, Sunintaboon P, Warit S, Thaisomboonsuk B, Jarman RG, Yoon IK, Ubol S, Fernandez S. Immunogenic properties of a BCG adjuvanted chitosan nanoparticle-based dengue vaccine in human dendritic cells. PLoS Negl Trop Dis. 2015;9:e0003958. doi:10.1371/journal.pntd.0003958.
  • Yam-Puc JC, Cedillo-Barron L, Aguilar-Medina EM, Ramos-Payan R, Escobar-Gutierrez A, Flores-Romo L. The cellular bases of antibody responses during dengue virus infection. Front Immunol. 2016;7:218. doi:10.3389/fimmu.2016.00218.
  • Gregory AE, Titball R, Williamson D. Vaccine delivery using nanoparticles. Front Cell Infect Microbiol. 2013;3:13. doi:10.3389/fcimb.2013.00013.
  • Pati R, Shevtsov M, Sonawane A. Nanoparticle vaccines against infectious diseases. Front Immunol. 2018;9:2224. doi:10.3389/fimmu.2018.02224.
  • Lim M, Badruddoza AZM, Firdous J, Azad M, Mannan A, Al-Hilal TA, Cho CS, Islam MA. Engineered nanodelivery systems to improve DNA vaccine technologies. Pharmaceutics. 2020;12:30. doi:10.3390/pharmaceutics12010030.
  • Jearanaiwitayakul T, Sunintaboon P, Chawengkittikul R, Limthongkul J, Midoeng P, Warit S, Ubol S. Nanodelivery system enhances the immunogenicity of dengue-2 nonstructural protein 1, DENV-2 NS1. Vaccine. 2020;38:6814–25. doi:10.1016/j.vaccine.2020.08.021.
  • Kirkpatrick BD, Durbin AP, Pierce KK, Carmolli MP, Tibery CM, Grier PL, Hynes N, Diehl SA, Elwood D, Jarvis AP, et al. Robust and balanced immune responses to all 4 dengue virus serotypes following administration of a single dose of a live attenuated tetravalent dengue vaccine to healthy, flavivirus-naive adults. J Infect Dis. 2015;212:702–10. doi:10.1093/infdis/jiv082.
  • Wang R, Zheng X, Sun J, Feng K, Gao N, Fan D, Chen H, Jin X, An J. Vaccination with a single consensus envelope protein ectodomain sequence administered in a heterologous regimen induces tetravalent immune responses and protection against dengue viruses in mice. Front Microbiol. 2019;10:1113. doi:10.3389/fmicb.2019.01113.
  • Hunsawong T, Sunintaboon P, Warit S, Thaisomboonsuk B, Jarman RG, Yoon IK, Ubol S, Fernandez S. A novel dengue virus serotype-2 nanovaccine induces robust humoral and cell-mediated immunity in mice. Vaccine. 2015;33:1702–10. doi:10.1016/j.vaccine.2015.02.016.
  • Gil-Jaramillo N, Motta FN, Favali CB, Bastos IM, Santana JM. Dendritic cells: a double-edged sword in immune responses during chagas disease. Front Microbiol. 2016;7:1076. doi:10.3389/fmicb.2016.01076.
  • Conde JN, Silva EM, Barbosa AS, Mohana-Borges R. The complement system in flavivirus infections. Front Microbiol. 2017;8:213. doi:10.3389/fmicb.2017.00213.
  • Osorio JE, Wallace D, Stinchcomb DT. A recombinant, chimeric tetravalent dengue vaccine candidate based on a dengue virus serotype 2 backbone. Expert Rev Vaccines. 2016;15:497–508. doi:10.1586/14760584.2016.1128328.
  • Whitehead SS. 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. 2016;15:509–17. doi:10.1586/14760584.2016.1115727.
  • Fernandez S, Thomas SJ, De La Barrera R, Im-Erbsin R, Jarman RG, Baras B, Toussaint JF, Mossman S, Innis BL, Schmidt A, et al. An adjuvanted, tetravalent dengue virus purified inactivated vaccine candidate induces long-lasting and protective antibody responses against dengue challenge in rhesus macaques. Am J Trop Med Hyg. 2015;92:698–708. doi:10.4269/ajtmh.14-0268.
  • Schmidt AC, Lin L, Martinez LJ, Ruck RC, Eckels KH, Collard A, De La Barrera R, Paolino KM, Toussaint JF, Lepine E, et al. Phase 1 randomized study of a tetravalent dengue purified inactivated vaccine in healthy adults in the United States. Am J Trop Med Hyg. 2017;96:1325–37. doi:10.4269/ajtmh.16-0634.
  • Nantachit N, Sunintaboon P, Ubol S. EDIII-DENV3 nanospheres drive immature dendritic cells into a mature phenotype in an in vitro model. Microbiol Immunol. 2017;61:305–17. doi:10.1111/1348-0421.12497.
  • Rungrojcharoenkit K, Sunintaboon P, Ellison D, Macareo L, Midoeng P, Chaisuwirat P, Fernandez S, Ubol S. Development of an adjuvanted nanoparticle vaccine against influenza virus, an in vitro study. PLoS One. 2020;15:e0237218. doi:10.1371/journal.pone.0237218.
  • Zhang P, Liu W, Peng Y, Han B, Yang Y. Toll like receptor 4 (TLR4) mediates the stimulating activities of chitosan oligosaccharide on macrophages. Int Immunopharmacol. 2014;23:254–61. doi:10.1016/j.intimp.2014.09.007.
  • Carroll EC, Jin L, Mori A, Munoz-Wolf N, Oleszycka E, Moran HBT, Mansouri S, McEntee CP, Lambe E, Agger EM, et al. The vaccine adjuvant chitosan promotes cellular immunity via DNA sensor cGAS-STING-dependent induction of type I interferons. Immunity. 2016;44:597–608. doi:10.1016/j.immuni.2016.02.004.
  • Smeltz RB, Chen J, Ehrhardt R, Shevach EM. Role of IFN-gamma in Th1 differentiation: IFN-gamma regulates IL-18R alpha expression by preventing the negative effects of IL-4 and by inducing/maintaining IL-12 receptor beta 2 expression. J Immunol. 2002;168:6165–72. doi:10.4049/jimmunol.168.12.6165.
  • Yu S, Jia L, Zhang Y, Zhong J, Yang B, Wu C. IL-12 induced the generation of IL-21- and IFN-gamma-co-expressing poly-functional CD4+ T cells from human naive CD4+ T cells. Cell Cycle. 2015;14:3362–72. doi:10.1080/15384101.2015.1093703.
  • Cox MA, Harrington LE, Zajac AJ. Cytokines and the inception of CD8 T cell responses. Trends Immunol. 2011;32:180–86. doi:10.1016/j.it.2011.01.004.
  • Walker JA, McKenzie ANJ. TH2 cell development and function. Nat Rev Immunol. 2018;18:121–33. doi:10.1038/nri.2017.118.
  • Dienz O, Eaton SM, Bond JP, Neveu W, Moquin D, Noubade R, Briso EM, Charland C, Leonard WJ, Ciliberto G, et al. The induction of antibody production by IL-6 is indirectly mediated by IL-21 produced by CD4+ T cells. J Exp Med. 2009;206:69–78. doi:10.1084/jem.20081571.
  • Abkar M, Fasihi-Ramandi M, Kooshki H, Sahebghadam Lotfi A. Oral immunization of mice with Omp31-loaded N-trimethyl chitosan nanoparticles induces high protection against Brucella melitensis infection. Int J Nanomedicine. 2017;12:8769–78. doi:10.2147/ijn.S149774.
  • Najminejad H, Kalantar SM, Mokarram AR, Dabaghian M, Abdollahpour-Alitappeh M, Ebrahimi SM, Tebianian M, Fasihi Ramandi M, Sheikhha MH. Bordetella pertussis antigens encapsulated into N-trimethyl chitosan nanoparticulate systems as a novel intranasal pertussis vaccine. Artif Cells Nanomed Biotechnol. 2019;47:2605–11. doi:10.1080/21691401.2019.1629948.
  • Mosafer J, Sabbaghi AH, Badiee A, Dehghan S, Tafaghodi M. Preparation, characterization and in vivo evaluation of alginate-coated chitosan and trimethylchitosan nanoparticles loaded with PR8 influenza virus for nasal immunization. Asian J Pharm Sci. 2019;14:216–21. doi:10.1016/j.ajps.2018.04.005.
  • Tsai MH, Chuang CC, Chen CC, Yen HJ, Cheng KM, Chen XA, Shyu HF, Lee CY, Young JJ, Kau JH. Nanoparticles assembled from fucoidan and trimethylchitosan as anthrax vaccine adjuvant: in vitro and in vivo efficacy in comparison to CpG. Carbohydr Polym. 2020;236:116041. doi:10.1016/j.carbpol.2020.116041.
  • Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, Lenches E, Jones CT, Mukhopadhyay S, Chipman PR, Strauss EG, et al. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell. 2002;108:717–25. doi:10.1016/s0092-8674(02)00660-8.
  • Kiermayr S, Stiasny K, Heinz FX. Impact of quaternary organization on the antigenic structure of the tick-borne encephalitis virus envelope glycoprotein E. J Virol. 2009;83:8482–91. doi:10.1128/jvi.00660-09.
  • Fibriansah G, Tan JL, Smith SA, de Alwis R, Ng TS, Kostyuchenko VA, Jadi RS, Kukkaro P, de Silva AM, Crowe JE, et al. A highly potent human antibody neutralizes dengue virus serotype 3 by binding across three surface proteins. Nat Commun. 2015;6:6341. doi:10.1038/ncomms7341.
  • Mehlhop E, Ansarah-Sobrinho C, Johnson S, Engle M, Fremont DH, Pierson TC, Diamond MS. Complement protein C1q inhibits antibody-dependent enhancement of flavivirus infection in an IgG subclass-specific manner. Cell Host Microbe. 2007;2:417–26. doi:10.1016/j.chom.2007.09.015.
  • Mehlhop E, Whitby K, Oliphant T, Marri A, Engle M, Diamond MS. Complement activation is required for induction of a protective antibody response against West Nile virus infection. J Virol. 2005;79:7466–77. doi:10.1128/jvi.79.12.7466-7477.2005.
  • Friberg H, Martinez LJ, Lin L, Blaylock JM, De La Barrera RA, Rothman AL, Putnak JR, Eckels KH, Thomas SJ, Jarman RG, et al. Cell-mediated immunity generated in response to a purified inactivated vaccine for dengue virus type 1. mSphere. 2020;5:e00671–19. doi:10.1128/mSphere.00671-19.
  • Smith SA, Selby LI, Johnston APR, Such GK. The endosomal escape of nanoparticles: toward more efficient cellular delivery. Bioconjug Chem. 2019;30:263–72. doi:10.1021/acs.bioconjchem.8b00732.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.