The Development of Classical Swine Fever Marker Vaccines in Recent Years
Abstract
:1. Introduction
2. Live-Attenuated Vaccines (LAVs)
3. DIVA Vaccines
3.1. MLV Vaccine
3.2. Viral Vector Vaccine
3.3. Subunit Vaccine
3.3.1. Expression of the E2 Protein in the Insect Expression System
3.3.2. Expression of E2 Protein by the Plant Expression System
3.3.3. Self-Assembled Nano-Vaccine
3.3.4. Adjuvant
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kleiboeker, S.B. Swine fever: Classical swine fever and African swine fever. Vet. Clin. N. Am. Food Anim. Pract. 2002, 18, 431–451. [Google Scholar] [CrossRef]
- Edwards, S.; Fukusho, A.; Lefèvre, P.C.; Lipowski, A.; Pejsak, Z.; Roehe, P.; Westergaard, J. Classical swine fever: The global situation. Vet. Microbiol. 2000, 73, 103–119. [Google Scholar] [CrossRef]
- Moennig, V.; Floegel-Niesmann, G.; Greiser-Wilke, I. Clinical signs and epidemiology of classical swine fever: A review of new knowledge. Vet. J. 2003, 165, 11–20. [Google Scholar] [CrossRef]
- Meyers, G.; Rümenapf, T.; Thiel, H.J. Molecular cloning and nucleotide sequence of the genome of hog cholera virus. Virology 1989, 171, 555–567. [Google Scholar] [CrossRef]
- Li, D.; Zhang, H.; Yang, L.; Chen, J.; Zhang, Y.; Yu, X.; Zheng, Q.; Hou, J. Surface display of classical swine fever virus E2 glycoprotein on gram-positive enhancer matrix (GEM) particles via the SpyTag/SpyCatcher system. Protein. Expr. Purif. 2020, 167, 105526. [Google Scholar] [CrossRef] [PubMed]
- Lin, M.; Lin, F.; Mallory, M.; Clavijo, A. Deletions of structural glycoprotein E2 of classical swine fever virus strain alfort/187 resolve a linear epitope of monoclonal antibody WH303 and the minimal N-terminal domain essential for binding immunoglobulin G antibodies of a pig hyperimmune serum. J. Virol. 2000, 74, 11619–11625. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Luo, Y.; Li, S.; Sun, Y.; Qiu, H.J. Classical swine fever in China: A minireview. Vet. Microbiol. 2014, 172, 1–6. [Google Scholar] [CrossRef]
- Bohorquez, J.A.; Muñoz-González, S.; Pérez-Simó, M.; Revilla, C.; Domínguez, J.; Ganges, L. Identification of an Immunosuppressive Cell Population during Classical Swine Fever Virus Infection and Its Role in Viral Persistence in the Host. Viruses 2019, 11, 822. [Google Scholar] [CrossRef][Green Version]
- Fahnøe, U.; Pedersen, A.G.; Johnston, C.M.; Orton, R.J.; Höper, D.; Beer, M.; Bukh, J.; Belsham, G.J.; Rasmussen, T.B. Virus Adaptation and Selection Following Challenge of Animals Vaccinated against Classical Swine Fever Virus. Viruses 2019, 11, 932. [Google Scholar] [CrossRef][Green Version]
- Gong, W.; Li, J.; Wang, Z.; Sun, J.; Mi, S.; Lu, Z.; Cao, J.; Dou, Z.; Sun, Y.; Wang, P.; et al. Virulence evaluation of classical swine fever virus subgenotype 2.1 and 2.2 isolates circulating in China. Vet. Microbiol. 2019, 232, 114–120. [Google Scholar] [CrossRef]
- Luo, Y.; Ji, S.; Liu, Y.; Lei, J.L.; Xia, S.L.; Wang, Y.; Du, M.L.; Shao, L.; Meng, X.Y.; Zhou, M.; et al. Isolation and Characterization of a Moderately Virulent Classical Swine Fever Virus Emerging in China. Transbound. Emerg. Dis. 2017, 64, 1848–1857. [Google Scholar] [CrossRef] [PubMed]
- Ma, S.M.; Mao, Q.; Yi, L.; Zhao, M.Q.; Chen, J.D. Apoptosis, Autophagy, and Pyroptosis: Immune Escape Strategies for Persistent Infection and Pathogenesis of Classical Swine Fever Virus. Pathogens 2019, 8, 239. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Pei, J.; Zhao, M.; Ye, Z.; Gou, H.; Wang, J.; Yi, L.; Dong, X.; Liu, W.; Luo, Y.; Liao, M.; et al. Autophagy enhances the replication of classical swine fever virus In Vitro. Autophagy 2014, 10, 93–110. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Pei, J.; Deng, J.; Ye, Z.; Wang, J.; Gou, H.; Liu, W.; Zhao, M.; Liao, M.; Yi, L.; Chen, J. Absence of autophagy promotes apoptosis by modulating the ROS-dependent RLR signaling pathway in classical swine fever virus-infected cells. Autophagy 2016, 12, 1738–1758. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Xie, B.; Zhao, M.; Song, D.; Wu, K.; Yi, L.; Li, W.; Li, X.; Wang, K.; Chen, J. Induction of autophagy and suppression of type I IFN secretion by CSFV. Autophagy 2021, 17, 925–947. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.; Li, N.; Luo, Y.; Liu, Y.; Miao, F.; Chen, T.; Zhang, S.; Cao, P.; Li, X.; Tian, K.; et al. Emergence of African Swine Fever in China, 2018. Transbound. Emerg. Dis. 2018, 65, 1482–1484. [Google Scholar] [CrossRef][Green Version]
- Blome, S.; Meindl-Böhmer, A.; Loeffen, W.; Thuer, B.; Moennig, V. Assessment of classical swine fever diagnostics and vaccine performance. Rev. Sci. Tech. 2006, 25, 1025–1038. [Google Scholar] [CrossRef]
- Graham, S.P.; Haines, F.J.; Johns, H.L.; Sosan, O.; La Rocca, S.A.; Lamp, B.; Rümenapf, T.; Everett, H.E.; Crooke, H.R. Characterisation of vaccine-induced, broadly cross-reactive IFN-γ secreting T cell responses that correlate with rapid protection against classical swine fever virus. Vaccine 2012, 30, 2742–2748. [Google Scholar] [CrossRef]
- Graham, S.P.; Everett, H.E.; Haines, F.J.; Johns, H.L.; Sosan, O.A.; Salguero, F.J.; Clifford, D.J.; Steinbach, F.; Drew, T.W.; Crooke, H.R. Challenge of pigs with classical swine fever viruses after C-strain vaccination reveals remarkably rapid protection and insights into early immunity. PLoS ONE 2012, 7, e29310. [Google Scholar] [CrossRef][Green Version]
- Xu, L.; Fan, X.Z.; Zhao, Q.Z.; Zhang, Z.X.; Chen, K.; Ning, Y.B.; Zhang, Q.Y.; Zou, X.Q.; Zhu, Y.Y.; Li, C.; et al. Effects of Vaccination with the C-Strain Vaccine on Immune Cells and Cytokines of Pigs against Classical Swine Fever Virus. Viral. Immunol. 2018, 31, 34–39. [Google Scholar] [CrossRef]
- Kunu, W.; Jiwakanon, J.; Porntrakulpipat, S. A bread-based lyophilized C-strain CSF virus vaccine as an oral vaccine in pigs. Transbound. Emerg. Dis. 2019, 66, 1597–1601. [Google Scholar] [CrossRef] [PubMed]
- Rossi, S.; Staubach, C.; Blome, S.; Guberti, V.; Thulke, H.H.; Vos, A.; Koenen, F.; Le Potier, M.F. Controlling of CSFV in European wild boar using oral vaccination: A review. Front. Microbiol. 2015, 6, 1141. [Google Scholar] [CrossRef] [PubMed]
- Lamothe-Reyes, Y.; Bohórquez, J.A.; Wang, M.; Alberch, M.; Pérez-Simó, M.; Rosell, R.; Ganges, L. Early and Solid Protection Afforded by the Thiverval Vaccine Provides Novel Vaccination Alternatives Against Classical Swine Fever Virus. Vaccines 2021, 9, 464. [Google Scholar] [CrossRef] [PubMed]
- Kim, T.; Huynh, L.T.; Hirose, S.; Igarashi, M.; Hiono, T.; Isoda, N.; Sakoda, Y. Characteristics of Classical Swine Fever Virus Variants Derived from Live Attenuated GPE(-) Vaccine Seed. Viruses 2021, 13, 1672. [Google Scholar] [CrossRef] [PubMed]
- Mendoza, S.; Correa-Giron, P.; Aguilera, E.; Colmenares, G.; Torres, O.; Cruz, T.; Romero, A.; Hernandez-Baumgarten, E.; Ciprián, A. Antigenic differentiation of classical swine fever vaccinal strain PAV-250 from other strains, including field strains from Mexico. Vaccine 2007, 25, 7120–7124. [Google Scholar] [CrossRef]
- van Oirschot, J.T.; Gielkens, A.L.; Moormann, R.J.; Berns, A.J. Marker vaccines, virus protein-specific antibody assays and the control of Aujeszky’s disease. Vet. Microbiol. 1990, 23, 85–101. [Google Scholar] [CrossRef]
- Ozaki, H.; Sugiura, T.; Sugita, S.; Imagawa, H.; Kida, H. Detection of antibodies to the nonstructural protein (NS1) of influenza A virus allows distinction between vaccinated and infected horses. Vet. Microbiol. 2001, 82, 111–119. [Google Scholar] [CrossRef]
- Blome, S.; Wernike, K.; Reimann, I.; König, P.; Moß, C.; Beer, M. A decade of research into classical swine fever marker vaccine CP7_E2alf (Suvaxyn(®) CSF Marker): A review of vaccine properties. Vet. Res. 2017, 48, 51. [Google Scholar] [CrossRef][Green Version]
- Blome, S.; Gabriel, C.; Schmeiser, S.; Meyer, D.; Meindl-Böhmer, A.; Koenen, F.; Beer, M. Efficacy of marker vaccine candidate CP7_E2alf against challenge with classical swine fever virus isolates of different genotypes. Vet. Microbiol. 2014, 169, 8–17. [Google Scholar] [CrossRef]
- Meyer, D.; Fritsche, S.; Luo, Y.; Engemann, C.; Blome, S.; Beyerbach, M.; Chang, C.Y.; Qiu, H.J.; Becher, P.; Postel, A. The double-antigen ELISA concept for early detection of E(rns)-specific classical swine fever virus antibodies and application as an accompanying test for differentiation of infected from marker vaccinated animals. Transbound. Emerg. Dis. 2017, 64, 2013–2022. [Google Scholar] [CrossRef]
- Meyer, D.; Loeffen, W.; Postel, A.; Fritsche, S.; Becher, P. Reduced specificity of E(rns) antibody ELISAs for samples from piglets with maternally derived antibodies induced by vaccination of sows with classical swine fever marker vaccine CP7_E2alf. Transbound. Emerg. Dis. 2018, 65, e505–e508. [Google Scholar] [CrossRef] [PubMed]
- Schroeder, S.; von Rosen, T.; Blome, S.; Loeffen, W.; Haegeman, A.; Koenen, F.; Uttenthal, A. Evaluation of classical swine fever virus antibody detection assays with an emphasis on the differentiation of infected from vaccinated animals. Rev. Sci. Tech. 2012, 31, 997–1010. [Google Scholar] [CrossRef] [PubMed]
- Pannhorst, K.; Fröhlich, A.; Staubach, C.; Meyer, D.; Blome, S.; Becher, P. Evaluation of an Erns-based enzyme-linked immunosorbent assay to distinguish Classical swine fever virus-infected pigs from pigs vaccinated with CP7_E2alf. J. Vet. Diagn. Investig. 2015, 27, 449–460. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Postel, A.; Becher, P. Genetically distinct pestiviruses pave the way to improved classical swine fever marker vaccine candidates based on the chimeric pestivirus concept. Emerg. Microbes. Infect. 2020, 9, 2180–2189. [Google Scholar] [CrossRef]
- Lim, S.I.; Choe, S.; Kim, K.S.; Jeoung, H.Y.; Cha, R.M.; Park, G.S.; Shin, J.; Park, G.N.; Cho, I.S.; Song, J.Y.; et al. Assessment of the efficacy of an attenuated live marker classical swine fever vaccine (Flc-LOM-BE(rns)) in pregnant sows. Vaccine 2019, 37, 3598–3604. [Google Scholar] [CrossRef]
- Choe, S.; Kim, K.S.; Shin, J.; Song, S.; Park, G.N.; Cha, R.M.; Choi, S.H.; Jung, B.I.; Lee, K.W.; Hyun, B.H.; et al. Comparative Analysis of the Productivity and Immunogenicity of an Attenuated Classical Swine Fever Vaccine (LOM) and an Attenuated Live Marker Classical Swine Fever Vaccine (Flc-LOM-BE(rns)) from Laboratory to Pig Farm. Vaccines 2021, 9, 381. [Google Scholar] [CrossRef]
- Han, Y.; Xie, L.; Yuan, M.; Ma, Y.; Sun, H.; Sun, Y.; Li, Y.; Qiu, H.J. Development of a marker vaccine candidate against classical swine fever based on the live attenuated vaccine C-strain. Vet. Microbiol. 2020, 247, 108741. [Google Scholar] [CrossRef]
- Holinka, L.G.; Fernandez-Sainz, I.; O’Donnell, V.; Prarat, M.V.; Gladue, D.P.; Lu, Z.; Risatti, G.R.; Borca, M.V. Development of a live attenuated antigenic marker classical swine fever vaccine. Virology 2009, 384, 106–113. [Google Scholar] [CrossRef][Green Version]
- Holinka, L.G.; Fernandez-Sainz, I.; Sanford, B.; O’Donnell, V.; Gladue, D.P.; Carlson, J.; Lu, Z.; Risatti, G.R.; Borca, M.V. Development of an improved live attenuated antigenic marker CSF vaccine strain candidate with an increased genetic stability. Virology 2014, 471–473, 13–18. [Google Scholar] [CrossRef]
- Holinka, L.G.; O’Donnell, V.; Risatti, G.R.; Azzinaro, P.; Arzt, J.; Stenfeldt, C.; Velazquez-Salinas, L.; Carlson, J.; Gladue, D.P.; Borca, M.V. Early protection events in swine immunized with an experimental live attenuated classical swine fever marker vaccine, FlagT4G. PLoS ONE 2017, 12, e0177433. [Google Scholar] [CrossRef]
- Fernandez-Sainz, I.; Ramanathan, P.; O’Donnell, V.; Diaz-San Segundo, F.; Velazquez-Salinas, L.; Sturza, D.F.; Zhu, J.; de los Santos, T.; Borca, M.V. Treatment with interferon-alpha delays disease in swine infected with a highly virulent CSFV strain. Virology 2015, 483, 284–290. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Shimotohno, K.; Temin, H.M. Formation of infectious progeny virus after insertion of herpes simplex thymidine kinase gene into DNA of an avian retrovirus. Cell 1981, 26, 67–77. [Google Scholar] [CrossRef]
- Tabin, C.J.; Hoffmann, J.W.; Goff, S.P.; Weinberg, R.A. Adaptation of a retrovirus as a eucaryotic vector transmitting the herpes simplex virus thymidine kinase gene. Mol. Cell. Biol. 1982, 2, 426–436. [Google Scholar] [CrossRef]
- Wei, C.M.; Gibson, M.; Spear, P.G.; Scolnick, E.M. Construction and isolation of a transmissible retrovirus containing the src gene of Harvey murine sarcoma virus and the thymidine kinase gene of herpes simplex virus type 1. J. Virol. 1981, 39, 935–944. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Adam, E.; Nasz, I. Significance of recombinant adenoviruses in experimental gene therapy. Orvosi. Hetilap. 1995, 136, 755–761. [Google Scholar] [PubMed]
- Adam, M.; Lepottier, M.F.; Eloit, M. Vaccination of pigs with replication-defective adenovirus vectored vaccines: The example of pseudorabies. Vet. Microbiol. 1994, 42, 205–215. [Google Scholar] [CrossRef]
- Wang, X.; Jiang, P.; Li, Y.; Jiang, W.; Dong, X. Protection of pigs against post-weaning multisystemic wasting syndrome by a recombinant adenovirus expressing the capsid protein of porcine circovirus type 2. Vet. Microbiol. 2007, 121, 215–224. [Google Scholar] [CrossRef]
- Sun, Y.; Liu, D.F.; Wang, Y.F.; Liang, B.B.; Cheng, D.; Li, N.; Qi, Q.F.; Zhu, Q.H.; Qiu, H.J. Generation and efficacy evaluation of a recombinant adenovirus expressing the E2 protein of classical swine fever virus. Res. Vet. Sci. 2010, 88, 77–82. [Google Scholar] [CrossRef]
- Li, N.; Zhao, J.J.; Zhao, H.P.; Sun, Y.; Zhu, Q.H.; Tong, G.Z.; Qiu, H.J. Protection of pigs from lethal challenge by a DNA vaccine based on an alphavirus replicon expressing the E2 glycoprotein of classical swine fever virus. J. Virol. Methods 2007, 144, 73–78. [Google Scholar] [CrossRef]
- Perri, S.; Greer, C.E.; Thudium, K.; Doe, B.; Legg, H.; Liu, H.; Romero, R.E.; Tang, Z.; Bin, Q.; Dubensky, T.W., Jr.; et al. An alphavirus replicon particle chimera derived from venezuelan equine encephalitis and sindbis viruses is a potent gene-based vaccine delivery vector. J. Virol. 2003, 77, 10394–10403. [Google Scholar] [CrossRef][Green Version]
- Sun, Y.; Li, H.Y.; Tian, D.Y.; Han, Q.Y.; Zhang, X.; Li, N.; Qiu, H.J. A novel alphavirus replicon-vectored vaccine delivered by adenovirus induces sterile immunity against classical swine fever. Vaccine 2011, 29, 8364–8372. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Tian, D.Y.; Li, S.; Meng, Q.L.; Zhao, B.B.; Li, Y.; Li, D.; Ling, L.J.; Liao, Y.J.; Qiu, H.J. Comprehensive evaluation of the adenovirus/alphavirus-replicon chimeric vector-based vaccine rAdV-SFV-E2 against classical swine fever. Vaccine 2013, 31, 538–544. [Google Scholar] [CrossRef] [PubMed]
- Hong, Q.; Qian, P.; Li, X.M.; Yu, X.L.; Chen, H.C. A recombinant pseudorabies virus co-expressing capsid proteins precursor P1-2A of FMDV and VP2 protein of porcine parvovirus: A trivalent vaccine candidate. Biotechnol. Lett. 2007, 29, 1677–1683. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Jin, M.; Zhang, S.; Xu, X.; Xiao, S.; Cao, S.; Chen, H. Generation and immunogenicity of a recombinant pseudorabies virus expressing cap protein of porcine circovirus type 2. Vet. Microbiol. 2007, 119, 97–104. [Google Scholar] [CrossRef] [PubMed]
- He, Y.; Qian, P.; Zhang, K.; Yao, Q.; Wang, D.; Xu, Z.; Wu, B.; Jin, M.; Xiao, S.; Chen, H. Construction and immune response characterization of a recombinant pseudorabies virus co-expressing capsid precursor protein (P1) and a multiepitope peptide of foot-and-mouth disease virus in swine. Virus Genes 2008, 36, 393–400. [Google Scholar] [CrossRef]
- Chen, Y.; Guo, W.; Xu, Z.; Yan, Q.; Luo, Y.; Shi, Q.; Chen, D.; Zhu, L.; Wang, X. A novel recombinant pseudorabies virus expressing parvovirus VP2 gene: Immunogenicity and protective efficacy in swine. Virol. J. 2011, 8, 307. [Google Scholar] [CrossRef][Green Version]
- Cong, X.; Lei, J.L.; Xia, S.L.; Wang, Y.M.; Li, Y.; Li, S.; Luo, Y.; Sun, Y.; Qiu, H.J. Pathogenicity and immunogenicity of a gE/gI/TK gene-deleted pseudorabies virus variant in susceptible animals. Vet. Microbiol. 2016, 182, 170–177. [Google Scholar] [CrossRef]
- Jiang, Y.; Fang, L.; Xiao, S.; Zhang, H.; Pan, Y.; Luo, R.; Li, B.; Chen, H. Immunogenicity and protective efficacy of recombinant pseudorabies virus expressing the two major membrane-associated proteins of porcine reproductive and respiratory syndrome virus. Vaccine 2007, 25, 547–560. [Google Scholar] [CrossRef]
- Lei, J.L.; Xia, S.L.; Wang, Y.; Du, M.; Xiang, G.T.; Cong, X.; Luo, Y.; Li, L.F.; Zhang, L.; Yu, J.; et al. Safety and immunogenicity of a gE/gI/TK gene-deleted pseudorabies virus variant expressing the E2 protein of classical swine fever virus in pigs. Immunol. Lett. 2016, 174, 63–71. [Google Scholar] [CrossRef]
- Abid, M.; Teklue, T.; Li, Y.; Wu, H.; Wang, T.; Qiu, H.J.; Sun, Y. Generation and Immunogenicity of a Recombinant Pseudorabies Virus Co-Expressing Classical Swine Fever Virus E2 Protein and Porcine Circovirus Type 2 Capsid Protein Based on Fosmid Library Platform. Pathogens 2019, 8, 279. [Google Scholar] [CrossRef][Green Version]
- Xu, Y.Z.; Zhou, Y.J.; Tong, W.; Li, L.; Jiang, Y.F.; Tong, G.Z. Study on using NSP2 protein of porcine reproductive and respiratory syndrome virus (HuN4-F112) to express E2 neutralizing epitope of classical swine fever virus. Chin. J. Virol. 2013, 29, 17–25. [Google Scholar]
- Gao, F.; Jiang, Y.; Li, G.; Zhou, Y.; Yu, L.; Li, L.; Tong, W.; Zheng, H.; Zhang, Y.; Yu, H.; et al. Porcine reproductive and respiratory syndrome virus expressing E2 of classical swine fever virus protects pigs from a lethal challenge of highly-pathogenic PRRSV and CSFV. Vaccine 2018, 36, 3269–3277. [Google Scholar] [CrossRef] [PubMed]
- Gao, F.; Jiang, Y.; Li, G.; Zhang, Y.; Zhao, K.; Zhu, H.; Li, L.; Yu, L.; Zheng, H.; Zhou, Y.; et al. Immune duration of a recombinant PRRSV vaccine expressing E2 of CSFV. Vaccine 2020, 38, 7956–7962. [Google Scholar] [CrossRef] [PubMed]
- Gao, F.; Jiang, Y.; Li, G.; Li, L.; Zhang, Y.; Yu, L.; Zheng, H.; Tong, W.; Zhou, Y.; Liu, C.; et al. Evaluation of immune efficacy of recombinant PRRSV vectored vaccine rPRRSV-E2 in piglets with maternal derived antibodies. Vet. Microbiol. 2020, 248, 108833. [Google Scholar] [CrossRef] [PubMed]
- Tripathy, D.N. Swinepox virus as a vaccine vector for swine pathogens. Adv. Vet. Med. 1999, 41, 463–480. [Google Scholar] [CrossRef]
- Winslow, B.J.; Kalabat, D.Y.; Brown, S.M.; Cochran, M.D.; Collisson, E.W. Feline B7.1 and B7.2 proteins produced from swinepox virus vectors are natively processed and biologically active: Potential for use as nonchemical adjuvants. Vet. Microbiol. 2005, 111, 1–13. [Google Scholar] [CrossRef]
- Lin, H.; Ma, Z.; Chen, L.; Fan, H. Recombinant Swinepox Virus Expressing Glycoprotein E2 of Classical Swine Fever Virus Confers Complete Protection in Pigs upon Viral Challenge. Front. Vet. Sci. 2017, 4, 81. [Google Scholar] [CrossRef]
- Huang, Z.; Elankumaran, S.; Yunus, A.S.; Samal, S.K. A recombinant Newcastle disease virus (NDV) expressing VP2 protein of infectious bursal disease virus (IBDV) protects against NDV and IBDV. J. Virol. 2004, 78, 10054–10063. [Google Scholar] [CrossRef][Green Version]
- Molouki, A.; Peeters, B. Rescue of recombinant Newcastle disease virus: A short history of how it all started. Arch. Virol. 2017, 162, 1845–1854. [Google Scholar] [CrossRef]
- Park, M.S.; Steel, J.; García-Sastre, A.; Swayne, D.; Palese, P. Engineered viral vaccine constructs with dual specificity: Avian influenza and Newcastle disease. Proc. Natl. Acad. Sci. USA 2006, 103, 8203–8208. [Google Scholar] [CrossRef][Green Version]
- Kumar, R.; Kumar, V.; Kekungu, P.; Barman, N.N.; Kumar, S. Evaluation of surface glycoproteins of classical swine fever virus as immunogens and reagents for serological diagnosis of infections in pigs: A recombinant Newcastle disease virus approach. Arch. Virol. 2019, 164, 3007–3017. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Li, Y.; Xie, L.; Wang, X.; Gao, X.; Sun, Y.; Qiu, H.J. Secreted Expression of the Cap Gene of Porcine Circovirus Type 2 in Classical Swine Fever Virus C-Strain: Potential of C-Strain Used as a Vaccine Vector. Viruses 2017, 9, 298. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Risatti, G.R.; Holinka, L.G.; Carrillo, C.; Kutish, G.F.; Lu, Z.; Tulman, E.R.; Sainz, I.F.; Borca, M.V. Identification of a novel virulence determinant within the E2 structural glycoprotein of classical swine fever virus. Virology 2006, 355, 94–101. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Moormann, R.J.; Bouma, A.; Kramps, J.A.; Terpstra, C.; De Smit, H.J. Development of a classical swine fever subunit marker vaccine and companion diagnostic test. Vet. Microbiol. 2000, 73, 209–219. [Google Scholar] [CrossRef]
- Hsieh, P.; Robbins, P.W. Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells. J. Biol. Chem. 1984, 259, 2375–2382. [Google Scholar] [CrossRef]
- Kukuruzinska, M.A.; Bergh, M.L.; Jackson, B.J. Protein glycosylation in yeast. Annu. Rev. Biochem. 1987, 56, 915–944. [Google Scholar] [CrossRef]
- Wang, Z.; He, X.; Li, J.; Qi, J.; Zhao, C.; Yang, G. Preparation of magnetic steel-slag particle electrode and its performance in a novel electrochemical reactor for oilfield wastewater advanced treatment. J. Ind. Eng. Chem. 2018, 58, 18–23. [Google Scholar] [CrossRef]
- Gong, W.; Li, J.; Wang, Z.; Sun, J.; Mi, S.; Xu, J.; Cao, J.; Hou, Y.; Wang, D.; Huo, X.; et al. Commercial E2 subunit vaccine provides full protection to pigs against lethal challenge with 4 strains of classical swine fever virus genotype 2. Vet. Microbiol. 2019, 237, 108403. [Google Scholar] [CrossRef]
- Larrick, J.W.; Yu, L.; Chen, J.; Jaiswal, S.; Wycoff, K. Production of antibodies in transgenic plants. Res. Immunol. 1998, 149, 603–608. [Google Scholar] [CrossRef]
- Mason, H.S.; Lam, D.M.; Arntzen, C.J. Expression of hepatitis B surface antigen in transgenic plants. Proc. Natl. Acad. Sci. USA 1992, 89, 11745–11749. [Google Scholar] [CrossRef][Green Version]
- Takeyama, N.; Kiyono, H.; Yuki, Y. Plant-based vaccines for animals and humans: Recent advances in technology and clinical trials. Ther. Adv. Vaccines 2015, 3, 139–154. [Google Scholar] [CrossRef] [PubMed]
- Holtz, B.R.; Berquist, B.R.; Bennett, L.D.; Kommineni, V.J.; Munigunti, R.K.; White, E.L.; Wilkerson, D.C.; Wong, K.Y.; Ly, L.H.; Marcel, S. Commercial-scale biotherapeutics manufacturing facility for plant-made pharmaceuticals. Plant Biotechnol. J. 2015, 13, 1180–1190. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Sohn, E.-J.; Lee, Y.; Park, N.; Park, M.; Kim, N.H.; Park, S.; Min, K.; Gu, S.; Park, Y.; Song, J.; et al. Development of Plant-produced E2 Protein for Use as a Green Vaccine Against Classical Swine Fever Virus. J. Plant Biol. 2018, 61, 241–252. [Google Scholar] [CrossRef]
- Park, Y.; An, D.J.; Choe, S.; Lee, Y.; Park, M.; Park, S.; Gu, S.; Min, K.; Kim, N.H.; Lee, S.; et al. Development of Recombinant Protein-Based Vaccine against Classical Swine Fever Virus in Pigs Using Transgenic Nicotiana benthamiana. Front. Plant Sci. 2019, 10, 624. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Park, Y.; Lee, S.; Kang, H.; Park, M.; Min, K.; Kim, N.H.; Gu, S.; Kim, J.K.; An, D.J.; Choe, S.; et al. A classical swine fever virus E2 fusion protein produced in plants elicits a neutralizing humoral immune response in mice and pigs. Biotechnol. Lett. 2020, 42, 1247–1261. [Google Scholar] [CrossRef] [PubMed]
- Laughlin, R.C.; Madera, R.; Peres, Y.; Berquist, B.R.; Wang, L.; Buist, S.; Burakova, Y.; Palle, S.; Chung, C.J.; Rasmussen, M.V.; et al. Plant-made E2 glycoprotein single-dose vaccine protects pigs against classical swine fever. Plant Biotechnol. J. 2019, 17, 410–420. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Xu, Y.G.; Guan, X.T.; Liu, Z.M.; Tian, C.Y.; Cui, L.C. Immunogenicity in Swine of Orally Administered Recombinant Lactobacillus plantarum Expressing Classical Swine Fever Virus E2 Protein in Conjunction with Thymosin α-1 as an Adjuvant. Appl. Environ. Microbiol. 2015, 81, 3745–3752. [Google Scholar] [CrossRef][Green Version]
- Xu, Y.; Cui, L.; Tian, C.; Zhang, G.; Huo, G.; Tang, L.; Li, Y. Immunogenicity of recombinant classic swine fever virus CD8(+) T lymphocyte epitope and porcine parvovirus VP2 antigen coexpressed by Lactobacillus casei in swine via oral vaccination. Clin. Vaccine Immunol. 2011, 18, 1979–1986. [Google Scholar] [CrossRef][Green Version]
- Hou, X.L.; Yu, L.Y.; Liu, J.; Wang, G.H. Surface-displayed porcine epidemic diarrhea viral (PEDV) antigens on lactic acid bacteria. Vaccine 2007, 26, 24–31. [Google Scholar] [CrossRef]
- Li, C.L.; Zhang, T.; Saibara, T.; Nemoto, Y.; Ono, M.; Akisawa, N.; Iwasaki, S.; Maeda, T.; Onishi, S. Thymosin alpha1 accelerates restoration of T cell-mediated neutralizing antibody response in immunocompromised hosts. Int. Immunopharmacol. 2002, 2, 39–46. [Google Scholar] [CrossRef]
- Takahashi, W.N.; Ishii, M. An abnormal protein associated with tobacco mosaic virus infection. Nature 1952, 169, 419–420. [Google Scholar] [CrossRef] [PubMed]
- Hilleman, M.R. Vaccines in historic evolution and perspective: A narrative of vaccine discoveries. J. Hum. Virol. 2000, 3, 63–76. [Google Scholar] [CrossRef]
- Valenzuela, P.; Medina, A.; Rutter, W.J.; Ammerer, G.; Hall, B.D. Synthesis and assembly of hepatitis B virus surface antigen particles in yeast. Nature 1982, 298, 347–350. [Google Scholar] [CrossRef] [PubMed]
- McAleer, W.J.; Buynak, E.B.; Maigetter, R.Z.; Wampler, D.E.; Miller, W.J.; Hilleman, M.R. Human hepatitis B vaccine from recombinant yeast. Nature 1984, 307, 178–180. [Google Scholar] [CrossRef]
- Aoshi, T. Modes of Action for Mucosal Vaccine Adjuvants. Viral. Immunol. 2017, 30, 463–470. [Google Scholar] [CrossRef]
- Shukla, R.; Bansal, V.; Chaudhary, M.; Basu, A.; Bhonde, R.R.; Sastry, M. Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: A microscopic overview. Langmuir 2005, 21, 10644–10654. [Google Scholar] [CrossRef]
- Li, Y.; Jin, Q.; Ding, P.; Zhou, W.; Chai, Y.; Li, X.; Wang, Y.; Zhang, G. Gold nanoparticles enhance immune responses in mice against recombinant classical swine fever virus E2 protein. Biotechnol. Lett. 2020, 42, 1169–1180. [Google Scholar] [CrossRef]
- Zhao, Z.; Chen, X.; Chen, Y.; Li, H.; Fang, K.; Chen, H.; Li, X.; Qian, P. A Self-Assembling Ferritin Nanoplatform for Designing Classical Swine Fever Vaccine: Elicitation of Potent Neutralizing Antibody. Vaccines 2021, 9, 45. [Google Scholar] [CrossRef]
- Liu, Z.H.; Xu, H.L.; Han, G.W.; Tao, L.N.; Lu, Y.; Zheng, S.Y.; Fang, W.H.; He, F. A self-assembling nanoparticle: Implications for the development of thermostable vaccine candidates. Int. J. Biol. Macromol. 2021, 183, 2162–2173. [Google Scholar] [CrossRef]
- Hu, M.; Wang, F.; Li, N.; Xing, G.; Sun, X.; Zhang, Y.; Cao, S.; Cui, N.; Zhang, G. An antigen display system of GEM nanoparticles based on affinity peptide ligands. Int. J. Biol. Macromol. 2021, 193, 574–584. [Google Scholar] [CrossRef]
- Ramirez, K.; Ditamo, Y.; Rodriguez, L.; Picking, W.L.; van Roosmalen, M.L.; Leenhouts, K.; Pasetti, M.F. Neonatal mucosal immunization with a non-living, non-genetically modified Lactococcus lactis vaccine carrier induces systemic and local Th1-type immunity and protects against lethal bacterial infection. Mucosal. Immunol. 2010, 3, 159–171. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Yuriev, E.; Ramsland, P.A. Latest developments in molecular docking: 2010–2011 in review. J. Mol. Recognit. 2013, 26, 215–239. [Google Scholar] [CrossRef] [PubMed]
- Perrie, Y.; Mohammed, A.R.; Kirby, D.J.; McNeil, S.E.; Bramwell, V.W. Vaccine adjuvant systems: Enhancing the efficacy of sub-unit protein antigens. Int. J. Pharm. 2008, 364, 272–280. [Google Scholar] [CrossRef] [PubMed]
- Genmei, L.; Manlin, L.; Ruiai, C.; Hongliang, H.; Dangshuai, P. Construction and immunogenicity of recombinant adenovirus expressing ORF2 of PCV2 and porcine IFN gamma. Vaccine 2011, 29, 8677–8682. [Google Scholar] [CrossRef]
- Suárez, M.; Sordo, Y.; Prieto, Y.; Rodríguez, M.P.; Méndez, L.; Rodríguez, E.M.; Rodríguez-Mallon, A.; Lorenzo, E.; Santana, E.; González, N.; et al. A single dose of the novel chimeric subunit vaccine E2-CD154 confers early full protection against classical swine fever virus. Vaccine 2017, 35, 4437–4443. [Google Scholar] [CrossRef]
- Pérez-Pérez, D.; Sordo-Puga, Y.; Rodríguez-Moltó, M.P.; Sardina, T.; Santana, E.; Montero, C.; Ancizar, J.; Cabrera, Y.; Tuero, Á.; Naranjo, P.; et al. E2-CD154 vaccine candidate is safe and immunogenic in pregnant sows, and the maternal derived neutralizing antibodies protect piglets from classical swine fever virus challenge. Vet. Microbiol. 2021, 260, 109153. [Google Scholar] [CrossRef]
- Sordo-Puga, Y.; Pérez-Pérez, D.; Montero-Espinosa, C.; Oliva-Cárdenas, A.; Sosa-Teste, I.; Duarte, C.A.; Rodríguez-Moltó, M.P.; Sardina-González, T.; Santana-Rodríguez, E.; Vargas-Hernández, M.; et al. Immunogenicity of E2CD154 Subunit Vaccine Candidate against Classical Swine Fever in Piglets with Different Levels of Maternally Derived Antibodies. Vaccines 2020, 9, 7. [Google Scholar] [CrossRef]
- Moraes, M.P.; de Los Santos, T.; Koster, M.; Turecek, T.; Wang, H.; Andreyev, V.G.; Grubman, M.J. Enhanced antiviral activity against foot-and-mouth disease virus by a combination of type I and II porcine interferons. J. Virol. 2007, 81, 7124–7135. [Google Scholar] [CrossRef][Green Version]
- Wang, Y.P.; Liu, D.; Guo, L.J.; Tang, Q.H.; Wei, Y.W.; Wu, H.L.; Liu, J.B.; Li, S.B.; Huang, L.P.; Liu, C.M. Enhanced protective immune response to PCV2 subunit vaccine by co-administration of recombinant porcine IFN-γ in mice. Vaccine 2013, 31, 833–838. [Google Scholar] [CrossRef]
- Eichinger, K.M.; Resetar, E.; Orend, J.; Anderson, K.; Empey, K.M. Age predicts cytokine kinetics and innate immune cell activation following intranasal delivery of IFNγ and GM-CSF in a mouse model of RSV infection. Cytokine 2017, 97, 25–37. [Google Scholar] [CrossRef]
- Zhang, H.; Wen, W.; Zhao, Z.; Wang, J.; Chen, H.; Qian, P.; Li, X. Enhanced protective immunity to CSFV E2 subunit vaccine by using IFN-γ as immunoadjuvant in weaning piglets. Vaccine 2018, 36, 7353–7360. [Google Scholar] [CrossRef] [PubMed]
- Madera, R.; Gong, W.; Wang, L.; Burakova, Y.; Lleellish, K.; Galliher-Beckley, A.; Nietfeld, J.; Henningson, J.; Jia, K.; Li, P.; et al. Pigs immunized with a novel E2 subunit vaccine are protected from subgenotype heterologous classical swine fever virus challenge. BMC Vet. Res. 2016, 12, 197. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Madera, R.F.; Wang, L.; Gong, W.; Burakova, Y.; Buist, S.; Nietfeld, J.; Henningson, J.; Cino-Ozuna, A.G.; Tu, C.; Shi, J. Toward the development of a one-dose classical swine fever subunit vaccine: Antigen titration, immunity onset, and duration of immunity. J. Vet. Sci. 2018, 19, 393–405. [Google Scholar] [CrossRef] [PubMed]
- Burakova, Y.; Madera, R.; Wang, L.; Buist, S.; Lleellish, K.; Schlup, J.R.; Shi, J. Food-Grade Saponin Extract as an Emulsifier and Immunostimulant in Emulsion-Based Subunit Vaccine for Pigs. J. Immunol. Res. 2018, 2018, 8979838. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Lu, X.; Fang, W. Expression and purification of classical swine fever virus E2 protein from Sf9 cells using a modified vector. Biotechnol. Lett. 2017, 39, 1821–1825. [Google Scholar] [CrossRef] [PubMed]
- Chuang, K.H.; Wang, H.E.; Cheng, T.C.; Tzou, S.C.; Tseng, W.L.; Hung, W.C.; Tai, M.H.; Chang, T.K.; Roffler, S.R.; Cheng, T.L. Development of a universal anti-polyethylene glycol reporter gene for noninvasive imaging of PEGylated probes. J. Nucl. Med. 2010, 51, 933–941. [Google Scholar] [CrossRef][Green Version]
- Xu, H.; Wang, Y.; Han, G.; Fang, W.; He, F. Identification of E2 with improved secretion and immunogenicity against CSFV in piglets. BMC Microbiol. 2020, 20, 26. [Google Scholar] [CrossRef][Green Version]
Type of Vaccine | Vaccine | Marker | Results and References |
---|---|---|---|
Live marker vaccine | CP7_E2Alf | Erns | Resistance to wild virus infection of genotypes 2.1 and 2.3 [29]. |
Live marker vaccine | Ra, Pro, RaPro | Erns | Protection of animals from CSFV infection 28 days after a single vaccination. No cross-reactivity in serological diagnosis [34]. |
Live marker vaccine | FLC-LOM-BErns | Erns | Complete protection for gestating sows and increased productivity [35,36]. |
Live marker vaccine | rHCLV-E2P122A | 116LFDGTNP122 epitope, recognized by the mAb HQ06 | Intramuscular injection induces neutralizing antibody production at 28 days [37]. |
Live marker vaccine | FlagT4Gv | Flag epitope or mAbWH303 epitope | Protective effect on day 3 after inoculation and increased IFN-α levels in immunized animals [39,40] |
Viral vector vaccine | rAdV-SFV-E2 | Erns | Two doses of 6.25 × 105 TCID50 or single dose of 107 TCID50 provided complete protection against the challenge of deadly CSFV, and maternal antibodies did not inhibit the efficacy of the vaccine [51,52]. |
Viral vector vaccine | rPRVTJ-delgE/gI/TK-E2 | Erns | Induced production of anti-CSFV and anti-PRV neutralizing antibodies, and complete protection against CSFV Shimon strain and variant PRV TJ strain attacks [59]. |
Viral vector vaccine | rPRRSV-E2 | Erns | A single intramuscular injection protects piglets from the lethal challenge of highly pathogenic (HP)-PRRSV and CSFV, and the immunity lasts for up to 5 months [63,64]. |
Viral vector vaccine | rSPV-E2 | Erns | Immunization at 7 dpi can detect csfv specific neutralizing antibody and induce humoral and cellular immune responses [67]. |
Viral vector vaccine | rNDV-E2 | Erns | Intranasal inoculation induces the production of neutralizing antibodies against CSFV [71]. |
Subunit vaccine | TWJ-E2® | Erns | Two vaccinations provide complete protection against the highly virulent genotype 1.1 Shimen strain and protection against genotype 2 [77,78]. |
Subunit vaccine | ppE2-CBD | CBD | CBD-E2 fusion protein had high immunogenicity to piglets. A total of 50 or 100 µg injection could produce anti-E2 antibodies [84]. |
Subunit vaccine | pmE2:pFc2 | Erns | Production of 302 mg of recombinant pmE2 protein in 1 kg of tobacco leaves. A single dose of l µg of vaccine is sufficient to induce immune responses in mice [85]. |
Subunit vaccine | L. plantarum/pYG-E2 -Tα1 | Erns | Oral immunization produces anti-CSFV E2 IgG with high viral neutralizing activity, which significantly enhances cellular immunity [87]. |
Subunit vaccine | E2-AuNPs | Erns | The AuNPs vector is non-toxic to antigen-presenting cells, and the combination of E2 and AuNPs provides better induction of humoral and cellular immunity [97]. |
Subunit vaccine | pE2-fe/Gel02 | Erns | Stimulates strong levels of neutralizing antibodies and can induce both humoral and cellular immunity [98]. |
Subunit vaccine | SP-E2-mi3 NPs | Erns | A single dose of 10 µg of SP-E2-mi3 NPs provides clinical protection against a CSFV challenge. Cross-protective for different genotypes [99]. |
Subunit vaccine | GEM-PL-E2 | Erns | GEM-PL-E2 particles promote innate immune responses and induce higher neutralizing antibodies and anti-CSFV antibodies than CSFV E2 protein [100]. |
Subunit vaccine | E2-CD154 | Erns | Complete protection against classical swine fever virus at 7 dpi, preventing vertical transmission, and the CD154 molecule enhances cellular immunity [105,106,107] |
Subunit vaccine | E2-IFN-γ | Erns | Combination of E2 and IFN-γ significantly enhances expression of classical swine fever virus-specific IFN-γ [111]. |
Subunit vaccine | SPZJ-E2ZJ | Erns | The level of E2 protein secretion induced was at least 50% higher than that induced by other signal peptides, and a single injection of 5 μg of E2ZJ induced protective antibodies in piglets [117]. |
Subunit vaccine | KNB-E2 | Erns | A single dose of KNB-E2 containing 25 µg of recombinant CSFV E2 protein can prevent CSFV genotype 1.1 in pigs. Produces higher levels of E2-specific IgG and virus-neutralizing antibodies [113]. |
Subunit vaccine | OWq-E2 | Erns | Two doses of vaccination produced high levels of E2-specific IgG and virus-neutralizing antibodies in pigs [114]. |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Li, F.; Li, B.; Niu, X.; Chen, W.; Li, Y.; Wu, K.; Li, X.; Ding, H.; Zhao, M.; Chen, J.; et al. The Development of Classical Swine Fever Marker Vaccines in Recent Years. Vaccines 2022, 10, 603. https://doi.org/10.3390/vaccines10040603
Li F, Li B, Niu X, Chen W, Li Y, Wu K, Li X, Ding H, Zhao M, Chen J, et al. The Development of Classical Swine Fever Marker Vaccines in Recent Years. Vaccines. 2022; 10(4):603. https://doi.org/10.3390/vaccines10040603
Chicago/Turabian StyleLi, Fangfang, Bingke Li, Xinni Niu, Wenxian Chen, Yuwan Li, Keke Wu, Xiaowen Li, Hongxing Ding, Mingqiu Zhao, Jinding Chen, and et al. 2022. "The Development of Classical Swine Fever Marker Vaccines in Recent Years" Vaccines 10, no. 4: 603. https://doi.org/10.3390/vaccines10040603