Development of a Recombinant Thermostable Newcastle Disease Virus (NDV) Vaccine Express Infectious Bronchitis Virus (IBV) Multiple Epitopes for Protecting against IBV and NDV Challenges
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cells, Viruses, Antibodies, and Ethics Statement
2.2. Construction of Recombinant NDV Containing a Thermostable HN Gene and IBV S1 Protein Multiple Epitope Cassette
2.3. Virus Titration and Growth Kinetics
2.4. Antigenicity of the Recombinant rLS-T-HN-T/B Strain
2.5. Recombinant Virus rLS-T-HN-T/B Detection by Transmission Electron Microscopy (TEM)
2.6. Assessment of the Thermostability of the rLS-T-HN-T/B Strain
2.7. The Protective Efficacy of Thermostable rLS-T-HN-T/B
2.8. Serological Assays
2.9. Ciliostasis Test
2.10. Statistical Analysis
3. Results
3.1. The Construction of a Recombinant Thermostable NDV Expressing IBV S1 Protein Multiple Epitope Vaccine (rLS-T-HN-T/B)
3.2. TEM Detection and Antigenicity Analysis of the Thermostable rLS-T-HN-T/B Strain
3.3. Biological Characterization of the rLS-T-HN-T/B Strain
3.4. Determination of the Thermostability of rLS-T-N-T/B
3.5. VN and HI Responses Induced by rLS-T-HN-T/B Candidate Vaccine
3.6. Protective Efficacy of rLS-T-HN-T/B against NDV and IBV Challenges
3.7. The Tracheal Ciliary Activity of Vaccinated Chickens Post IBV Challenge
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Abozeid, H.H.; Paldurai, A.; Varghese, B.P.; Khattar, S.K.; Afifi, M.A.; Zouelfakkar, S.; El-Deeb, A.H.; El-Kady, M.F.; Samal, S.K. Development of a recombinant Newcastle disease virus-vectored vaccine for infectious bronchitis virus variant strains circulating in Egypt. Vet. Res. 2019, 50, 12. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.; Zhou, Y.; Li, J.; Fu, L.; Ji, G.; Zeng, F.; Zhou, L.; Gao, W.; Wang, H. Recombinant infectious bronchitis virus (IBV) H120 vaccine strain expressing the hemagglutinin-neuraminidase (HN) protein of Newcastle disease virus (NDV) protects chickens against IBV and NDV challenge. Arch. Virol. 2016, 161, 1209–1216. [Google Scholar] [CrossRef]
- El-Tholoth, M.; Branavan, M.; Naveenathayalan, A.; Balachandran, W. Recombinase polymerase amplification-nucleic acid lateral flow immunoassays for Newcastle disease virus and infectious bronchitis virus detection. Mol. Biol. Rep. 2019, 46, 6391–6397. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abolnik, C.; Strydom, C. Complete Genome Sequence of a Class I Avian Orthoavulavirus 1 Isolated from Commercial Ostriches. Microbiol. Resour. Announc. 2019, 8, e00543-19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ferreira, H.L.; Taylor, T.L.; Dimitrov, K.M.; Sabra, M.; Afonso, C.L.; Suarez, D.L. Virulent Newcastle disease viruses from chicken origin are more pathogenic and transmissible to chickens than viruses normally maintained in wild birds. Vet. Microbiol. 2019, 235, 25–34. [Google Scholar] [CrossRef] [PubMed]
- Franzo, G.; Legnardi, M.; Tucciarone, C.M.; Drigo, M.; Martini, M.; Cecchinato, M. Evolution of infectious bronchitis virus in the field after homologous vaccination introduction. Vet. Res. 2019, 50, 92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Absalón, A.E.; Cortés-Espinosa, D.V.; Lucio, E.; Miller, P.J.; Afonso, C.L. Epidemiology, control, and prevention of Newcastle disease in endemic regions: Latin America. Trop. Anim. Health Prod. 2019, 51, 1033–1048. [Google Scholar] [CrossRef] [Green Version]
- Dimitrov, K.M.; Afonso, C.L.; Yu, Q.; Miller, P.J. Newcastle disease vaccines-A solved problem or a continuous challenge? Vet. Microbiol. 2017, 206, 126–136. [Google Scholar] [CrossRef]
- Aston, E.J.; Jordan, B.J.; Williams, S.M.; García, M.; Jackwood, M.W. Effect of Pullet Vaccination on Development and Longevity of Immunity. Viruses 2019, 11, 135. [Google Scholar] [CrossRef] [Green Version]
- Choi, K.-S. Newcastle disease virus vectored vaccines as bivalent or antigen delivery vaccines. Clin. Exp. Vaccine Res. 2017, 6, 72–82. [Google Scholar] [CrossRef]
- Gelb, J.; Ladman, B.S.; Licata, M.J.; Shapiro, M.H.; Campion, L.R. Evaluating viral interference between infectious bronchitis virus and Newcastle disease virus vaccine strains using quantitative reverse transcription-polymerase chain reaction. Avian Dis. 2007, 51, 924–934. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wen, G.; Hu, X.; Zhao, K.; Wang, H.; Zhang, Z.; Zhang, T.; Yang, J.; Luo, Q.; Zhang, R.; Pan, Z.; et al. Molecular basis for the thermostability of Newcastle disease virus. Sci. Rep. 2016, 6, 22492. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patel, A.; Erb, S.M.; Strange, L.; Shukla, R.S.; Kumru, O.S.; Smith, L.; Nelson, P.; Joshi, S.B.; Livengood, J.A.; Volkin, D.B. Combined semi-empirical screening and design of experiments (DOE) approach to identify candidate formulations of a lyophilized live attenuated tetravalent viral vaccine candidate. Vaccine 2018, 36, 3169–3179. [Google Scholar] [CrossRef] [PubMed]
- Chen, D.; Kristensen, D. Opportunities and challenges of developing thermostable vaccines. Expert Rev. Vaccines 2009, 8, 547–557. [Google Scholar] [CrossRef] [PubMed]
- Wen, G.; Chen, C.; Guo, J.; Zhang, Z.; Shang, Y.; Shao, H.; Luo, Q.; Yang, J.; Wang, H.; Wang, H.; et al. Development of a novel thermostable Newcastle disease virus vaccine vector for expression of a heterologous gene. J. Gen. Virol. 2015, 96, 1219–1228. [Google Scholar] [CrossRef] [PubMed]
- Bajrovic, I.; Schafer, S.C.; Romanovicz, D.K.; Croyle, M.A. Novel technology for storage and distribution of live vaccines and other biological medicines at ambient temperature. Sci. Adv. 2020, 6, eaau4819. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, L.; Wang, M.; Wang, G.; Li, L.; Wang, H.; Luo, Q.; Shang, Y.; Zhang, T.; Shao, H.; Wen, G. Genome Sequence of a Thermostable Avirulent Newcastle Disease Virus Isolated from Domestic Ducks in China. Microbiol. Resour. Announc. 2019, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wen, G.; Li, L.; Yu, Q.; Wang, H.; Luo, Q.; Zhang, T.; Zhang, R.; Zhang, W.; Shao, H. Evaluation of a thermostable Newcastle disease virus strain TS09-C as an in-ovo vaccine for chickens. PLoS ONE 2017, 12, e0172812. [Google Scholar] [CrossRef]
- Zhao, W.; Zhang, Z.; Zsak, L.; Yu, Q. P and M gene junction is the optimal insertion site in Newcastle disease virus vaccine vector for foreign gene expression. J. Gen. Virol. 2015, 96, 40–45. [Google Scholar] [CrossRef]
- Zhao, R.; Sun, J.; Qi, T.; Zhao, W.; Han, Z.; Yang, X.; Liu, S. Recombinant Newcastle disease virus expressing the infectious bronchitis virus S1 gene protects chickens against Newcastle disease virus and infectious bronchitis virus challenge. Vaccine 2017, 35, 2435–2442. [Google Scholar] [CrossRef]
- Zhao, W.; Spatz, S.; Zhang, Z.; Wen, G.; Garcia, M.; Zsak, L.; Yu, Q. Newcastle disease virus (NDV) recombinants expressing infectious laryngotracheitis virus (ILTV) glycoproteins gB and gD protect chickens against ILTV and NDV challenges. J. Virol. 2014, 88, 8397–8406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schröer, D.; Veits, J.; Keil, G.; Römer-Oberdörfer, A.; Weber, S.; Mettenleiter, T.C. Efficacy of Newcastle disease virus recombinant expressing avian influenza virus H6 hemagglutinin against Newcastle disease and low pathogenic avian influenza in chickens and turkeys. Avian Dis. 2011, 55, 201–211. [Google Scholar] [CrossRef]
- Kim, S.-H.; Samal, S.K. Innovation in Newcastle Disease Virus Vectored Avian Influenza Vaccines. Viruses 2019, 11, 300. [Google Scholar] [CrossRef] [Green Version]
- Tan, L.; Wen, G.; Qiu, X.; Yuan, Y.; Meng, C.; Sun, Y.; Liao, Y.; Song, C.; Liu, W.; Shi, Y.; et al. A Recombinant La Sota Vaccine Strain Expressing Multiple Epitopes of Infectious Bronchitis Virus (IBV) Protects Specific Pathogen-Free (SPF) Chickens against IBV and NDV Challenges. Vaccines 2019, 7, 170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tan, L.; Liao, Y.; Fan, J.; Zhang, Y.; Mao, X.; Sun, Y.; Song, C.; Qiu, X.; Meng, C.; Ding, C. Prediction and identification of novel IBV S1 protein derived CTL epitopes in chicken. Vaccine 2016, 34, 380–386. [Google Scholar] [CrossRef]
- Tan, L.; Zhang, Y.; Liu, F.; Yuan, Y.; Zhan, Y.; Sun, Y.; Qiu, X.; Meng, C.; Song, C.; Ding, C. Infectious bronchitis virus poly-epitope-based vaccine protects chickens from acute infection. Vaccine 2016, 34, 5209–5216. [Google Scholar] [CrossRef]
- Grimes, S.E. A Basic Laboratory Manual for the Small-Scale Production and Testing of 1-2 Newcastle Disease Vaccine; FAO Regional Oce for Asia and the Pacific (RAP): Bangkok, Thailand, 2002. [Google Scholar]
- Reed, L.J.; Muench, H. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 1938, 27, 493–497. [Google Scholar] [CrossRef]
- Santry, L.A.; McAusland, T.M.; Susta, L.; Wood, G.A.; Major, P.P.; Petrik, J.J.; Bridle, B.W.; Wootton, S.K. Production and Purification of High-Titer Newcastle Disease Virus for Use in Preclinical Mouse Models of Cancer. Mol. Ther. Methods Clin. Dev. 2018, 9, 181–191. [Google Scholar] [CrossRef] [Green Version]
- Epizooties, O.C.I. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals; OIE: Paris, France, 2013. [Google Scholar]
- Lopes, P.D.; Okino, C.H.; Fernando, F.S.; Pavani, C.; Casagrande, V.M.; Lopez, R.F.V.; Montassier, M.d.F.S.; Montassier, H.J. Inactivated infectious bronchitis virus vaccine encapsulated in chitosan nanoparticles induces mucosal immune responses and effective protection against challenge. Vaccine 2018, 36, 2630–2636. [Google Scholar] [CrossRef]
- Cook, J.K.; Orbell, S.J.; Woods, M.A.; Huggins, M.B. Breadth of protection of the respiratory tract provided by different live-attenuated infectious bronchitis vaccines against challenge with infectious bronchitis viruses of heterologous serotypes. Avian Pathol. 1999, 28, 477–485. [Google Scholar] [CrossRef] [Green Version]
- Lomniczi, B. Thermostability of Newcastle disease virus strains of different virulence. Arch. Virol. 1975, 47, 249–255. [Google Scholar] [CrossRef] [PubMed]
- Cho, Y.; Lamichhane, B.; Nagy, A.; Chowdhury, I.R.; Samal, S.K.; Kim, S.-H. Co-expression of the Hemagglutinin and Neuraminidase by Heterologous Newcastle Disease Virus Vectors Protected Chickens against H5 Clade 2.3.4.4 HPAI Viruses. Sci. Rep. 2018, 8, 16854. [Google Scholar] [CrossRef] [PubMed]
- Roy Chowdhury, I.; Yeddula, S.G.R.; Pierce, B.G.; Samal, S.K.; Kim, S.-H. Newcastle disease virus vectors expressing consensus sequence of the H7 HA protein protect broiler chickens and turkeys against highly pathogenic H7N8 virus. Vaccine 2019, 37, 4956–4962. [Google Scholar] [CrossRef]
- Yu, Q.; Li, Y.; Dimitrov, K.; Afonso, C.L.; Spatz, S.; Zsak, L. Genetic stability of a Newcastle disease virus vectored infectious laryngotracheitis virus vaccine after serial passages in chicken embryos. Vaccine 2020, 38, 925–932. [Google Scholar] [CrossRef]
- Ellis, S.; Keep, S.; Britton, P.; de Wit, S.; Bickerton, E.; Vervelde, L. Recombinant Infectious Bronchitis Viruses Expressing Chimeric Spike Glycoproteins Induce Partial Protective Immunity against Homologous Challenge despite Limited Replication. J. Virol. 2018, 92. [Google Scholar] [CrossRef] [Green Version]
- Azimi, T.; Franzel, L.; Probst, N. Seizing market shaping opportunities for vaccine cold chain equipment. Vaccine 2017, 35, 2260–2264. [Google Scholar] [CrossRef]
- Lennon, P.; Atuhaire, B.; Yavari, S.; Sampath, V.; Mvundura, M.; Ramanathan, N.; Robertson, J. Root cause analysis underscores the importance of understanding, addressing, and communicating cold chain equipment failures to improve equipment performance. Vaccine 2017, 35, 2198–2202. [Google Scholar] [CrossRef]
- Omony, J.B.; Wanyana, A.; Mugimba, K.K.; Kirunda, H.; Nakavuma, J.L.; Otim-Onapa, M.; Byarugaba, D.K. Disparate thermostability profiles and HN gene domains of field isolates of Newcastle disease virus from live bird markets and waterfowl in Uganda. Virol. J. 2016, 13, 103. [Google Scholar] [CrossRef] [Green Version]
- Bello, M.B.; Yusoff, K.; Ideris, A.; Hair-Bejo, M.; Peeters, B.P.H.; Omar, A.R. Diagnostic and Vaccination Approaches for Newcastle Disease Virus in Poultry: The Current and Emerging Perspectives. Biomed. Res. Int. 2018, 2018, 7278459. [Google Scholar] [CrossRef]
- Bensink, Z.; Spradbrow, P. Newcastle disease virus strain I2--a prospective thermostable vaccine for use in developing countries. Vet. Microbiol. 1999, 68, 131–139. [Google Scholar] [CrossRef]
- Zhao, Y.; Liu, H.; Cong, F.; Wu, W.; Zhao, R.; Kong, X. Phosphoprotein Contributes to the Thermostability of Newcastle Disease Virus. Biomed. Res. Int. 2018, 2018, 8917476. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Simmons, G.C. The isolation of Newcastle disease virus in Queensland. Aust. Vet. J. 1967, 43, 29–30. [Google Scholar] [CrossRef] [PubMed]
- Wen, G.; Shang, Y.; Guo, J.; Chen, C.; Shao, H.; Luo, Q.; Yang, J.; Wang, H.; Cheng, G. Complete genome sequence and molecular characterization of thermostable Newcastle disease virus strain TS09-C. Virus Genes 2013, 46, 542–545. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Liu, H.; Liu, P.; Peeters, B.P.H.; Zhao, C.; Kong, X. Recovery of avirulent, thermostable Newcastle disease virus strain NDV4-C from cloned cDNA and stable expression of an inserted foreign gene. Arch. Virol. 2013, 158, 2115–2120. [Google Scholar] [CrossRef] [PubMed]
- Liu, T.; Song, Y.; Yang, Y.; Bu, Y.; Cheng, J.; Zhang, G.; Xue, J. Hemagglutinin-Neuraminidase and fusion genes are determinants of NDV thermostability. Vet. Microbiol. 2019, 228, 53–60. [Google Scholar] [CrossRef] [PubMed]
- Omony, J.B.; Wanyana, A.; Kirunda, H.; Mugimba, K.K.; Nakavuma, J.L.; Otim-Onapa, M.; Byarugaba, D.K. Immunogenicity and protection efficacy evaluation of avian paramyxovirus serotype-1 (APMV-1) isolates in experimentally infected chickens. Avian Pathol. 2017, 46, 386–395. [Google Scholar] [CrossRef] [Green Version]
Virus | HA | EID50/mL | TCID50/mL | MDT (h) | ICPI |
---|---|---|---|---|---|
LaSota | 210 | 9.23 | 3.2 × 107 | >120 | 0.05 |
rLS-T-HN-T/B | 210 | 9.55 | 3.5 × 107 | >120 | 0.03 |
Virus | Titers after Storage for Days | ||||
---|---|---|---|---|---|
0 | 4 | 8 | 12 | 16 | |
LaSota | 9.22 ± 0.42 | 7.87 ± 0.38 | 5.82 ± 0.72 | 2.46 ± 1.22 | 1.85 ± 0.62 |
rLS-T-HN-T/B | 9.51 ± 0.37 | 8.82 ± 0.52 | 8.15 ± 0.46 | 7.67 ± 0.34 | 6.62 ± 0.57 |
Immunogen | VN Titer | HI Titer |
---|---|---|
rLS-T-HN-T/B | 6.78 ± 0.41 | 7.26 ± 0.53 |
LaSota | 0 | 2.18 ± 0.46 |
PBS | 0 | 0 |
© 2020 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 (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tan, L.; Wen, G.; Yuan, Y.; Huang, M.; Sun, Y.; Liao, Y.; Song, C.; Liu, W.; Shi, Y.; Shao, H.; et al. Development of a Recombinant Thermostable Newcastle Disease Virus (NDV) Vaccine Express Infectious Bronchitis Virus (IBV) Multiple Epitopes for Protecting against IBV and NDV Challenges. Vaccines 2020, 8, 564. https://doi.org/10.3390/vaccines8040564
Tan L, Wen G, Yuan Y, Huang M, Sun Y, Liao Y, Song C, Liu W, Shi Y, Shao H, et al. Development of a Recombinant Thermostable Newcastle Disease Virus (NDV) Vaccine Express Infectious Bronchitis Virus (IBV) Multiple Epitopes for Protecting against IBV and NDV Challenges. Vaccines. 2020; 8(4):564. https://doi.org/10.3390/vaccines8040564
Chicago/Turabian StyleTan, Lei, Guoyuan Wen, Yanmei Yuan, Meizhen Huang, Yingjie Sun, Ying Liao, Cuiping Song, Weiwei Liu, Yonghong Shi, Huabin Shao, and et al. 2020. "Development of a Recombinant Thermostable Newcastle Disease Virus (NDV) Vaccine Express Infectious Bronchitis Virus (IBV) Multiple Epitopes for Protecting against IBV and NDV Challenges" Vaccines 8, no. 4: 564. https://doi.org/10.3390/vaccines8040564