A Chimeric Sudan Virus-Like Particle Vaccine Candidate Produced by a Recombinant Baculovirus System Induces Specific Immune Responses in Mice and Horses
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cells and Animals
2.2. Construction of Recombinant Baculoviruses
2.3. Expression and Purification of SUDV GP and VP40 Antigens and Preparation of Polyclonal Antibodies
2.4. Immunofluorescence Testing of the Recombinant Baculoviruses
2.5. VLP Preparation
2.6. Western Blotting and Transmission Electron Microscopy (TEM) Analysis of VLPs
2.7. Animal Immunizations
2.8. Detection of SUDV GP-Specific Antibody by ELISA
2.9. Detection of SUDV Neutralizing Antibodies by a Pseudotyped Virus
2.10. Cell-Mediated Immune Responses in Mice
2.11. SUDV VLPs Induce Activation of B cells
2.12. Horse Immunoglobulin Purification
2.13. Laboratory Facility and Ethics Statement
3. Results
3.1. Expression of SUDV GP and VP40 Proteins
3.2. Verification of Baculovirus-Expressed SUDV GP and VP40 Proteins
3.3. Production and Characterization of SUDV VLPs
3.4. SUDV VLPs Elicit Antibody Responses in Vaccinated Mice
3.5. Antigen-Specific Cellular Immune Responses in Vaccinated Mice
3.6. SUDV VLPs-Enhanced Splenocytes Cytokine Secretion
3.7. Enhancing Effects of SUDV VLP on B Cell Activation
3.8. Antibody Response in Vaccinated Horses
4. Discussion
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Baseler, L.; Chertow, D.S.; Johnson, K.M.; Feldmann, H.; Morens, D.M. The Pathogenesis of Ebola Virus Disease. Annu. Rev. Pathol. 2017, 12, 387–418. [Google Scholar] [CrossRef] [PubMed]
- Brès, P. Ebola haemorrhagic fever in Zaire, 1976. Bull. World Health Organ. 1978, 56, 271–293. [Google Scholar]
- Brès, P. Ebola haemorrhagic fever in Sudan, 1976. Report of a WHO/International Study Team. Bull. World Health Organ. 1978, 56, 247–270. [Google Scholar]
- Adams, M.J.; Lefkowitz, E.J.; King, A.M.Q.; Harrach, B.; Harrison, R.L.; Knowles, N.J.; Kropinski, A.M.; Krupovic, M.; Kuhn, J.H.; Mushegian, A.R.; et al. Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Arch. Virol. 2017, 162, 2505–2538. [Google Scholar] [CrossRef] [PubMed]
- Pourrut, X.; Kumulungui, B.; Wittmann, T.; Moussavou, G.; Delicat, A.; Yaba, P.; Nkoghe, D.; Gonzalez, J.P.; Leroy, E.M. The natural history of Ebola virus in Africa. Microbes Infect. 2005, 7, 1005–1014. [Google Scholar] [CrossRef]
- Bukreyev, A.A.; Chandran, K.; Dolnik, O.; Dye, J.M.; Ebihara, H.; Leroy, E.M.; Muhlberger, E.; Netesov, S.V.; Patterson, J.L.; Paweska, J.T.; et al. Discussions and decisions of the 2012–2014 International Committee on Taxonomy of Viruses (ICTV) Filoviridae Study Group, January 2012–June 2013. Arch. Virol. 2014, 159, 821–830. [Google Scholar] [CrossRef]
- Coltart, C.E.; Lindsey, B.; Ghinai, I.; Johnson, A.M.; Heymann, D.L. The Ebola outbreak, 2013–2016: Old lessons for new epidemics. Philos. Trans. R Soc. Lond. B Biol. Sci. 2017, 372, 20160297. [Google Scholar] [CrossRef]
- Leroy, E.; Baize, S.; Gonzalez, J.P. Ebola and Marburg hemorrhagic fever viruses: Update on filoviruses. Med. Trop. 2011, 71, 111–121. [Google Scholar]
- Ascenzi, P.; Bocedi, A.; Heptonstall, J.; Capobianchi, M.R.; Di Caro, A.; Mastrangelo, E.; Bolognesi, M.; Ippolito, G. Ebolavirus and Marburgvirus: Insight the Filoviridae family. Mol. Asp. Med. 2008, 29, 151–185. [Google Scholar] [CrossRef] [Green Version]
- Carette, J.E.; Raaben, M.; Wong, A.C.; Herbert, A.S.; Obernosterer, G.; Mulherkar, N.; Kuehne, A.I.; Kranzusch, P.J.; Griffin, A.M.; Ruthel, G.; et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011, 477, 340–343. [Google Scholar] [CrossRef] [Green Version]
- Jones, S.M.; Feldmann, H.; Stroher, U.; Geisbert, J.B.; Fernando, L.; Grolla, A.; Klenk, H.D.; Sullivan, N.J.; Volchkov, V.E.; Fritz, E.A.; et al. Live attenuated recombinant vaccine protects nonhuman primates against Ebola and Marburg viruses. Nat. Med. 2005, 11, 786–790. [Google Scholar] [CrossRef] [PubMed]
- Wong, G.; Audet, J.; Fernando, L.; Fausther-Bovendo, H.; Alimonti, J.B.; Kobinger, G.P.; Qiu, X. Immunization with vesicular stomatitis virus vaccine expressing the Ebola glycoprotein provides sustained long-term protection in rodents. Vaccine 2014, 32, 5722–5729. [Google Scholar] [CrossRef] [PubMed]
- Sullivan, N.J.; Geisbert, T.W.; Geisbert, J.B.; Shedlock, D.J.; Xu, L.; Lamoreaux, L.; Custers, J.H.; Popernack, P.M.; Yang, Z.Y.; Pau, M.G.; et al. Immune protection of nonhuman primates against Ebola virus with single low-dose adenovirus vectors encoding modified GPs. PLoS Med. 2006, 3, e177. [Google Scholar] [CrossRef]
- Sullivan, N.J.; Sanchez, A.; Rollin, P.E.; Yang, Z.Y.; Nabel, G.J. Development of a preventive vaccine for Ebola virus infection in primates. Nature 2000, 408, 605–609. [Google Scholar] [CrossRef] [PubMed]
- Bukreyev, A.; Rollin, P.E.; Tate, M.K.; Yang, L.; Zaki, S.R.; Shieh, W.J.; Murphy, B.R.; Collins, P.L.; Sanchez, A. Successful topical respiratory tract immunization of primates against Ebola virus. J. Virol. 2007, 81, 6379–6388. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blaney, J.E.; Marzi, A.; Willet, M.; Papaneri, A.B.; Wirblich, C.; Feldmann, F.; Holbrook, M.; Jahrling, P.; Feldmann, H.; Schnell, M.J. Antibody quality and protection from lethal Ebola virus challenge in nonhuman primates immunized with rabies virus based bivalent vaccine. PLoS Pathog. 2013, 9, e1003389. [Google Scholar] [CrossRef]
- Shuai, L.; Wang, X.; Wen, Z.; Ge, J.; Wang, J.; Zhao, D.; Bu, Z. Genetically modified rabies virus-vectored Ebola virus disease vaccines are safe and induce efficacious immune responses in mice and dogs. Antivir. Res. 2017, 146, 36–44. [Google Scholar] [CrossRef]
- Quinn, M.; Erkes, D.A.; Snyder, C.M. Cytomegalovirus and immunotherapy: Opportunistic pathogen, novel target for cancer and a promising vaccine vector. Immunotherapy 2016, 8, 211–221. [Google Scholar] [CrossRef] [Green Version]
- Pushko, P.; Bray, M.; Ludwig, G.V.; Parker, M.; Schmaljohn, A.; Sanchez, A.; Jahrling, P.B.; Smith, J.F. Recombinant RNA replicons derived from attenuated Venezuelan equine encephalitis virus protect guinea pigs and mice from Ebola hemorrhagic fever virus. Vaccine 2000, 19, 142–153. [Google Scholar] [CrossRef]
- Sunay, M.M.E.; Martins, K.A.O.; Steffens, J.T.; Gregory, M.; Vantongeren, S.A.; Van Hoeven, N.; Garnes, P.G.; Bavari, S. Glucopyranosyl lipid adjuvant enhances immune response to Ebola virus-like particle vaccine in mice. Vaccine 2019, 37, 3902–3910. [Google Scholar] [CrossRef]
- Suder, E.; Furuyama, W.; Feldmann, H.; Marzi, A.; de Wit, E. The vesicular stomatitis virus-based Ebola virus vaccine: From concept to clinical trials. Hum. Vaccines Immunother. 2018, 14, 2107–2113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Furuyama, W.; Marzi, A. Ebola Virus: Pathogenesis and Countermeasure Development. Annu. Rev. Virol. 2019, 6, 435–458. [Google Scholar] [CrossRef] [PubMed]
- Qiu, X.; Wong, G.; Audet, J.; Bello, A.; Fernando, L.; Alimonti, J.B.; Fausther-Bovendo, H.; Wei, H.; Aviles, J.; Hiatt, E.; et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 2014, 514, 47–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zheng, X.; Wong, G.; Zhao, Y.; Wang, H.; He, S.; Bi, Y.; Chen, W.; Jin, H.; Gai, W.; Chu, D.; et al. Treatment with hyperimmune equine immunoglobulin or immunoglobulin fragments completely protects rodents from Ebola virus infection. Sci. Rep. 2016, 6, 24179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boisgerault, F.; Moron, G.; Leclerc, C. Virus-like particles: A new family of delivery systems. Expert Rev. Vaccines 2002, 1, 101–109. [Google Scholar] [CrossRef] [PubMed]
- Naslund, J.; Lagerqvist, N.; Habjan, M.; Lundkvist, A.; Evander, M.; Ahlm, C.; Weber, F.; Bucht, G. Vaccination with virus-like particles protects mice from lethal infection of Rift Valley Fever Virus. Virology 2009, 385, 409–415. [Google Scholar] [CrossRef] [Green Version]
- Warfield, K.L.; Aman, M.J. Advances in virus-like particle vaccines for filoviruses. J. Infect. Dis. 2011, 204 (Suppl. 3), S1053–S1059. [Google Scholar] [CrossRef]
- Zeltins, A. Construction and characterization of virus-like particles: A review. Mol. Biotechnol. 2013, 53, 92–107. [Google Scholar] [CrossRef]
- Ohimain, E.I. Recent advances in the development of vaccines for Ebola virus disease. Virus Res. 2016, 211, 174–185. [Google Scholar] [CrossRef]
- Pastor, A.R.; Gonzalez-Dominguez, G.; Diaz-Salinas, M.A.; Ramirez, O.T.; Palomares, L.A. Defining the multiplicity and time of infection for the production of Zaire Ebola virus-like particles in the insect cell-baculovirus expression system. Vaccine 2019, 37, 6962–6969. [Google Scholar] [CrossRef]
- Medina, M.F.; Kobinger, G.P.; Rux, J.; Gasmi, M.; Looney, D.J.; Bates, P.; Wilson, J.M. Lentiviral vectors pseudotyped with minimal filovirus envelopes increased gene transfer in murine lung. Mol. Ther. 2003, 8, 777–789. [Google Scholar] [CrossRef] [PubMed]
- Perera, R.A.; Wang, P.; Gomaa, M.R.; El-Shesheny, R.; Kandeil, A.; Bagato, O.; Siu, L.Y.; Shehata, M.M.; Kayed, A.S.; Moatasim, Y.; et al. Seroepidemiology for MERS coronavirus using microneutralisation and pseudoparticle virus neutralisation assays reveal a high prevalence of antibody in dromedary camels in Egypt, June 2013. Eurosurveillance 2013, 18, 7. [Google Scholar] [CrossRef] [PubMed]
- Ewer, K.; Rampling, T.; Venkatraman, N.; Bowyer, G.; Wright, D.; Lambe, T.; Imoukhuede, E.B.; Payne, R.; Fehling, S.K.; Strecker, T.; et al. A Monovalent Chimpanzee Adenovirus Ebola Vaccine Boosted with MVA. N. Engl. J. Med. 2016, 374, 1635–1646. [Google Scholar] [CrossRef] [PubMed]
- Marzi, A.; Engelmann, F.; Feldmann, F.; Haberthur, K.; Shupert, W.L.; Brining, D.; Scott, D.P.; Geisbert, T.W.; Kawaoka, Y.; Katze, M.G.; et al. Antibodies are necessary for rVSV/ZEBOV-GP-mediated protection against lethal Ebola virus challenge in nonhuman primates. Proc. Natl. Acad. Sci. USA 2013, 110, 1893–1898. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Warfield, K.L.; Swenson, D.L.; Olinger, G.G.; Kalina, W.V.; Aman, M.J.; Bavari, S. Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. J. Infect. Dis. 2007, 196 (Suppl. 2), S430–S437. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martins, K.A.; Steffens, J.T.; van Tongeren, S.A.; Wells, J.B.; Bergeron, A.A.; Dickson, S.P.; Dye, J.M.; Salazar, A.M.; Bavari, S. Toll-like receptor agonist augments virus-like particle-mediated protection from Ebola virus with transient immune activation. PLoS ONE 2014, 9, e89735. [Google Scholar] [CrossRef] [Green Version]
- Squaiella-Baptistao, C.C.; Magnoli, F.C.; Marcelino, J.R.; Sant'Anna, O.A.; Tambourgi, D.V. Quality of horse F (ab’) 2 antitoxins and anti-rabies immunoglobulins: Protein content and anticomplementary activity. J. Venom. Anim. Toxins Incl. Trop. Dis. 2018, 24, 16. [Google Scholar] [CrossRef]
- Zhang, X.J.; Li, H.L.; Deng, D.Y.; Ji, C.; Yao, X.D.; Liu, J.X. Functional and proteomic comparison of different techniques to produce equine anti-tetanus immunoglobulin F (ab’) 2 fragments. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2018, 1092, 29–39. [Google Scholar] [CrossRef]
- Perry, A.L.; Hayes, A.J.; Cox, H.A.; Alcock, F.; Parker, A.R. Comparison of five commercial anti-tetanus toxoid immunoglobulin G enzyme-linked immunosorbent assays. Clin. Vaccine Immunol. 2009, 16, 1837–1839. [Google Scholar] [CrossRef] [Green Version]
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Wu, F.; Zhang, S.; Zhang, Y.; Mo, R.; Yan, F.; Wang, H.; Wong, G.; Chi, H.; Wang, T.; Feng, N.; et al. A Chimeric Sudan Virus-Like Particle Vaccine Candidate Produced by a Recombinant Baculovirus System Induces Specific Immune Responses in Mice and Horses. Viruses 2020, 12, 64. https://doi.org/10.3390/v12010064
Wu F, Zhang S, Zhang Y, Mo R, Yan F, Wang H, Wong G, Chi H, Wang T, Feng N, et al. A Chimeric Sudan Virus-Like Particle Vaccine Candidate Produced by a Recombinant Baculovirus System Induces Specific Immune Responses in Mice and Horses. Viruses. 2020; 12(1):64. https://doi.org/10.3390/v12010064
Chicago/Turabian StyleWu, Fangfang, Shengnan Zhang, Ying Zhang, Ruo Mo, Feihu Yan, Hualei Wang, Gary Wong, Hang Chi, Tiecheng Wang, Na Feng, and et al. 2020. "A Chimeric Sudan Virus-Like Particle Vaccine Candidate Produced by a Recombinant Baculovirus System Induces Specific Immune Responses in Mice and Horses" Viruses 12, no. 1: 64. https://doi.org/10.3390/v12010064
APA StyleWu, F., Zhang, S., Zhang, Y., Mo, R., Yan, F., Wang, H., Wong, G., Chi, H., Wang, T., Feng, N., Gao, Y., Xia, X., Zhao, Y., & Yang, S. (2020). A Chimeric Sudan Virus-Like Particle Vaccine Candidate Produced by a Recombinant Baculovirus System Induces Specific Immune Responses in Mice and Horses. Viruses, 12(1), 64. https://doi.org/10.3390/v12010064