Lumpy Skin Disease Virus with Four Knocked Out Genes Was Attenuated In Vivo and Protects Cattle from Infection
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cells and Viruses
2.2. Construction of the Integration Plasmids
2.3. Generation of Recombinant Lumpy Skin Disease Viruses with Knocked out Virulence Genes
2.4. Western Blotting
2.5. Animals
2.6. Safety of LSDV Atyrau-5BJN(IL18) in Cattle
2.7. Immunogenicity and Protectiveness of LSDV Atyrau-5BJN(IL18) in Cattle
2.8. Statistical Analyses
3. Results
3.1. Generation of Recombinant Viruses with Targeted Knock out of Virulence Genes
3.2. Safety of Recombinant LSDV Atyrau-5BJN(IL18)
3.3. Immunogenicity and Protectiveness of LSDV Atyrau-5BJN(IL18)
4. Discussion
5. Patents
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tuppurainen, E.S.; Oura, C.A. Review: Lumpy skin disease: An emerging threat to Europe, the Middle East and Asia. Transbound. Emerg. Dis. 2012, 59, 40–48. [Google Scholar] [CrossRef]
- Ylmaz, E.; Arayici, P.; Maharramov, A.; Mustafaeva, Z. Approaches to designing of new generation vaccines against the sheep pox disease. Biotechnol. Acta 2016, 9, 7. [Google Scholar] [CrossRef] [Green Version]
- European Food Safety Authority (EFSA); Calistri, P.; De Clercq, K.; Gubbins, S.; Klement, E.; Stegeman, A.; Abrahantes, J.C.; Antoniou, S.; Broglia, A.; Gogin, A. Lumpy skin disease: III. Data collection and analysis. EFSA J. 2019, 17, e05638. [Google Scholar] [CrossRef]
- Bhanuprakash, V.; Indrani, B.K.; Hegde, R.; Kumar, M.M.; Moorthy, A.R. A classical live attenuated vaccine for sheep pox. Trop. Anim. Health Prod. 2004, 36, 307–320. [Google Scholar] [CrossRef]
- Artenstein, A.W.; Grabenstein, J.D. Smallpox vaccines for biodefense: Need and feasibility, Expert Review of Vaccines. Expert Rev. Vaccines 2008, 7, 1225–1237. [Google Scholar] [CrossRef]
- Moss, B. Reflections on the early development of poxvirus vectors. Vaccine 2013, 31, 4220–4222. [Google Scholar] [CrossRef] [Green Version]
- Yakubitskiy, S.N.; Kolosova, I.V.; Maksyutov, R.A.; Shchelkunov, S.N. Attenuation of Vaccinia Virus. Acta Nat. 2015, 7, 113–121. [Google Scholar]
- Tulman, E.R.; Afonso, C.L.; Lu, Z.; Zsak, L.; Kutish, G.F.; Rock, D.L. Genome of lumpy skin disease virus. J. Virol. 2001, 75, 7122–7130. [Google Scholar] [CrossRef] [Green Version]
- Boshra, H.; Cao, J.; Babiuk, S. Generation of Recombinant Capripoxvirus Vectors for Vaccines and Gene Knockout Function Studies. Methods Mol. Biol. 2016, 1349, 151–161. [Google Scholar] [CrossRef]
- Zhu, Y.; Li, Y.; Bai, B.; Fang, J.; Zhang, K.; Yin, X.; Li, S.; Li, W.; Ma, Y.; Cui, Y.; et al. Construction of an attenuated goatpox virus AV41 strain by deleting the TK gene and ORF8-18. Antivir. Res. 2018, 157, 111–119. [Google Scholar] [CrossRef]
- Balinsky, C.A.; Delhon, G.; Afonso, C.L.; Risatti, G.R.; Borca, M.V.; French, R.A.; Tulman, E.R.; Geary, S.J.; Rock, D.L. Sheeppox virus kelch-like gene SPPV-019 affects virus virulence. J. Virol. 2007, 81, 11392–11401. [Google Scholar] [CrossRef]
- Kara, P.D.; Mather, A.S.; Pretorius, A.; Chetty, T.; Babiuk, S.; Wallace, D.B. Characterisation of putative immunomodulatory gene knockouts of lumpy skin disease virus in cattle towards an improved vaccine. Vaccine 2018, 36, 4708–4715. [Google Scholar] [CrossRef]
- Aspden, K.; van Dijk, A.A.; Bingham, J.; Cox, D.; Passmore, J.A.; Williamson, A.L. Immunogenicity of a recombinant lumpy skin disease virus (neethling vaccine strain) expressing the rabies virus glycoprotein in cattle. Vaccine 2002, 20, 2693–2701. [Google Scholar] [CrossRef]
- Wallace, D.B.; Viljoen, G.J. Immune responses to recombinants of the South African vaccine strain of lumpy skin disease virus generated by using thymidine kinase gene insertion. Vaccine 2005, 23, 3061–3067. [Google Scholar] [CrossRef]
- Zhang, M.; Sun, Y.; Chen, W.; Bu, Z. The 135 Gene of Goatpox Virus Encodes an Inhibitor of NF-κB and Apoptosis and May Serve as an Improved Insertion Site to Generate Vectored Live Vaccine. J. Virol. 2018, 92, e00190-18. [Google Scholar] [CrossRef] [Green Version]
- Cêtre-Sossah, C.; Dickmu, S.; Kwiatek, O.; Albina, E. A G-protein-coupled chemokine receptor: A putative insertion site for a multi-pathogen recombinant capripoxvirus vaccine strategy. J. Immunol. Methods 2017, 448, 112–115. [Google Scholar] [CrossRef] [Green Version]
- Chervyakova, O.; Sultankulova, K.; Nissanova, R.; Orynbayev, M. Lumpy skin disease virus: Approaches to attenuation for vaccine development. Eurasian J. Appl. Biotechnol. 2022. [Google Scholar] [CrossRef]
- Orynbayev, M.B.; Nissanova, R.K.; Khairullin, B.M.; Issimov, A.; Zakarya, K.D.; Sultankulova, K.T.; Kutumbetov, L.B.; Tulendibayev, A.B.; Myrzakhmetova, B.S.; Burashev, E.D.; et al. Lumpy skin disease in Kazakhstan. Trop. Anim. Health Prod. 2021, 53, 166. [Google Scholar] [CrossRef]
- Chervyakova, O.; Strochkov, V.; Tailakova, E.; Sultankulova, K.; Sandybayev, N.; Construction of Intergrative Plasmids for Recombination of Sheeppox Virus Genome. Eurasian J. Appl. Biotechnol. 2017. Available online: https://biotechlink.org/index.php/journal/article/view/157 (accessed on 15 September 2022).
- Chervyakova, O.; Tailakova, E.; Kozhabergenov, N.; Sadikaliyeva, S.; Sultankulova, K.; Zakarya, K.; Maksyutov, R.A.; Strochkov, V.; Sandybayev, N. Engineering of Recombinant Sheep Pox Viruses Expressing Foreign Antigens. Microorganisms 2021, 9, 1005. [Google Scholar] [CrossRef]
- Chervyakova, O.V.; Zaitsev, V.L.; Iskakov, B.K.; Tailakova, E.T.; Strochkov, V.M.; Sultankulova, K.T.; Sandybayev, N.T.; Stanbekova, G.E.; Beisenov, D.K.; Abduraimov, Y.O.; et al. Recombinant Sheep Pox Virus Proteins Elicit Neutralizing Antibodies. Viruses 2016, 8, 159. [Google Scholar] [CrossRef]
- Falkner, F.G.; Moss, B. Transient dominant selection of recombinant vaccinia viruses. J. Virol. 1990, 64, 3108–3111. [Google Scholar]
- World Organisation for Animal Health (WOAH). Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2022. Available online: https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.04.12_LSD.pdf (accessed on 3 October 2022).
- Tulman, E.R.; Afonso, C.L.; Lu, Z.; Zsak, L.; Sur, J.H.; Sandybaev, N.T.; Kerembekova, U.Z.; Zaitsev, V.L.; Kutish, G.F.; Rock, D.L. The genomes of sheeppox and goatpox viruses. J. Virol. 2002, 76, 6054–6061. [Google Scholar]
- Kitching, R.P. Vaccines for lumpy skin disease, sheep pox and goat pox. Dev. Biol. 2003, 114, 161–167. [Google Scholar]
- Orynbayev, M.B.; Nissanova, R.K.; Argimbayeva, T.U.; Zakarya, K.D.; Myrzakhmetova, B.S.; Melisbek, A.M.; Barmak, S.M.; Issabek, A.U.; Nakhanov, A.K.; Shevtsov, A.; et al. Genomic Sequence of the New Attenuated Vaccine Strain Neethling-RIBSP of the Lumpy Skin Disease Virus. Microbiol. Resour. Announc. 2020, 9, e00318-20. [Google Scholar] [CrossRef]
- Johnston, J.B.; McFadden, G. Technical knockout: Understanding poxvirus pathogenesis by selectively deleting viral immunomodulatory genes. Cell. Microbiol. 2004, 6, 695–705. [Google Scholar] [CrossRef] [Green Version]
- Fleming, S.B.; McCaughan, C.A.; Andrews, A.E.; Nash, A.D.; Mercer, A.A. A homolog of interleukin-10 is encoded by the poxvirus orf virus. J. Virol. 1997, 71, 4857–4861. [Google Scholar] [CrossRef] [Green Version]
- Lee, H.J.; Essani, K.; Smith, G.L. The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 2001, 281, 170–192. [Google Scholar] [CrossRef] [Green Version]
- Fickenscher, H.; Hör, S.; Küpers, H.; Knappe, A.; Wittmann, S.; Sticht, H. The interleukin-10 family of cytokines. Trends Immunol. 2002, 23, 89–96. [Google Scholar] [CrossRef]
- Imlach, W.; McCaughan, C.A.; Mercer, A.A.; Haig, D.; Fleming, S.B. Orf virus-encoded interleukin-10 stimulates the proliferation of murine mast cells and inhibits cytokine synthesis in murine peritoneal macrophages. J. Gen. Virol. 2002, 83 Pt 5, 1049–1058. [Google Scholar] [CrossRef]
- Johnston, J.B.; McFadden, G. Poxvirus immunomodulatory strategies: Current perspectives. J. Virol. 2003, 77, 6093–6100. [Google Scholar] [CrossRef] [Green Version]
- Nash, P.; Barrett, J.; Cao, J.X.; Hota-Mitchell, S.; Lalani, A.S.; Everett, H.; Xu, X.-M.; Robichaud, J.; Hnatiuk, S.; Ainslie, C.; et al. Immunomodulation by viruses: The myxoma virus story. Immunol. Rev. 1999, 168, 103–120. [Google Scholar] [CrossRef]
- Cooray, S.; Bahar, M.W.; Abrescia, N.G.A.; McVey, C.; Bartlett, N.; Chen, R.; Stuart, D.; Grimes, J.M.; Smith, G.L. Functional and structural studies of the vaccinia virus virulence factor N1 reveal a Bcl-2-like anti-apoptotic protein. J. Gen. Virol. 2007, 88 Pt 6, 1656–1666. [Google Scholar] [CrossRef]
- Maluquer de Motes, C.; Cooray, S.; Ren, H.; Almeida, G.; McGourty, K.; Bahar, M.W.; Stuart, D.; Grimes, J.M.; Graham, S.; Smith, G.L. Inhibition of apoptosis and NF-κB activation by vaccinia protein N1 occur via distinct binding surfaces and make different contributions to virulence. PLoS Pathog. 2011, 7, e1002430. [Google Scholar] [CrossRef] [Green Version]
- Issabek, A.U.; Orynbayev, M.B.; Sultankulova, K.T.; Amirgazin, A.; Zakarya, K.D.; Omarova, Z.; Chervyakova, O.V. Genome Sequence of Atyrau-5BJN(IL18), a Recombinant Lumpy Skin Disease Virus with Knockout of Virulence Genes. Microbiol. Resour. Announc. 2022, 11, e0038022. [Google Scholar] [CrossRef]
Target Gene | Primer Name | Sequence (5′–3′) | Product Size, bp | |
---|---|---|---|---|
Recombinant Type | Wild Type | |||
LSDV005 | RCR005ΔF | agtagtatttaccaccaacatg | 1152 | 1587 |
RCR005ΔR | caagtatgatgatataataacg | |||
LSDV008 | RCR008ΔF | tcaaatactttagactcttccc | 432 | 1169 |
RCR008ΔR | agggtaagtatccaagtttt | |||
LSDV066 | RCR-TK-F | aattataggacctatgttttctggc | 1085 | 413 |
RCR-TK-R | cagcgtctttataacattccat | |||
LSDV142 | RCR142ΔF | tataagatgtcgattcccag | 816 | 1102 |
RCR142ΔR | attttgtgacttgtgcgc |
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Chervyakova, O.; Issabek, A.; Sultankulova, K.; Bopi, A.; Kozhabergenov, N.; Omarova, Z.; Tulendibayev, A.; Aubakir, N.; Orynbayev, M. Lumpy Skin Disease Virus with Four Knocked Out Genes Was Attenuated In Vivo and Protects Cattle from Infection. Vaccines 2022, 10, 1705. https://doi.org/10.3390/vaccines10101705
Chervyakova O, Issabek A, Sultankulova K, Bopi A, Kozhabergenov N, Omarova Z, Tulendibayev A, Aubakir N, Orynbayev M. Lumpy Skin Disease Virus with Four Knocked Out Genes Was Attenuated In Vivo and Protects Cattle from Infection. Vaccines. 2022; 10(10):1705. https://doi.org/10.3390/vaccines10101705
Chicago/Turabian StyleChervyakova, Olga, Aisha Issabek, Kulyaisan Sultankulova, Arailym Bopi, Nurlan Kozhabergenov, Zamira Omarova, Ali Tulendibayev, Nurdos Aubakir, and Mukhit Orynbayev. 2022. "Lumpy Skin Disease Virus with Four Knocked Out Genes Was Attenuated In Vivo and Protects Cattle from Infection" Vaccines 10, no. 10: 1705. https://doi.org/10.3390/vaccines10101705
APA StyleChervyakova, O., Issabek, A., Sultankulova, K., Bopi, A., Kozhabergenov, N., Omarova, Z., Tulendibayev, A., Aubakir, N., & Orynbayev, M. (2022). Lumpy Skin Disease Virus with Four Knocked Out Genes Was Attenuated In Vivo and Protects Cattle from Infection. Vaccines, 10(10), 1705. https://doi.org/10.3390/vaccines10101705