LUMPY SKIN DISEASE VIRUS: APPROACHES TO ATTENUATION FOR VACCINE DEVELOPMENT

Main Article Content

Authors

O.V. Chervyakova

Research Institute for Biological Safety Problems, Gvardeiskiy, Korday district, Zhambyl region, 080409, Kazakhstan

K.T. Sultankulova

Research Institute for Biological Safety Problems, Gvardeiskiy, Korday district, Zhambyl region, 080409, Kazakhstan

R.K. Nissanova

Research Institute for Biological Safety Problems, Gvardeiskiy, Korday district, Zhambyl region, 080409, Kazakhstan

M.B. Orynbayev

Research Institute for Biological Safety Problems, Gvardeiskiy, Korday district, Zhambyl region, 080409, Kazakhstan

Abstract

Lumpy skin disease (LSD) is a disease caused by the lumpy skin disease virus (LSDV) of the genus capripoxvirus. The disease is responsible for serious losses to the cattle industry globally. Vaccination is the most effective way of controlling LSDV. The currently available live attenuated vaccines are used in many countries and provide stable immunity. However, use of these vaccines can sometimes cause postvaccinal complications in animals. Attenuation of viruses by the classical method is associated with random mutations in the genome, and some vaccines can contain a mixture of viruses of different genotypes and virulence. Hence, there is a need to develop a safe immunogenic vaccine that will provide improved protection against LSDV. The most promising approach is gene modification to develop an attenuated capripoxvirus strain with high immunogenicity and protectivity. Sequencing and analysis of capripoxvirus DNA genomes has resulted in the identification of a number of genes whose protein products effectively stimulate antibody production in the host organism. These proteins are able to function both inside and outside the cell, neutralizing the complement factors, inhibiting apoptosis and synthesis of interferons, and reducing counter-inflammatory cytokines and chemokines. Here, we review the literature for instances of genetic manipulation of genes encoding the above proteins, resulting in capripoxvirus attenuation.

Keywords

Lumpy skin disease virus, attenuation, vaccine, capripoxvirus, virulence genes, gene knockout

Article Details

References

Al-Salihi K.A., Hassan I.Q. Lumpy Skin Disease in Iraq: Study of the Disease Emergence. Transbound Emerg Dis., 2015, vol. 62, no. 5, pp. 457-462. doi: 10.1111/tbed.12386.

Sheep pox and goat pox. In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals URL _S_POX_G_POX.pdf (accessed 27 February 2019)

Lumpy skin disease. In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals URL (accessed 27 February 2019)

Tuppurainen E. Vaccination against Lumpy skin disease virus // URL (accessed 27 February 2019)

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, vol. 75, pp. 7122–7130. Crossref

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, vol. 76, pp. 6054–6061. Crossref

Kitching R.P. Vaccines for lumpy skin disease, sheep pox and goat pox. Dev. Biol. (Basel)., 2003, vol. 114, pp. 161-167.

Davies F.G., Mbugwa G. The alterations in pathogenicity and immunogenicity of a Kenya sheep and goat pox virus on serial passage in bovine foetal muscle cell cultures. J. Comp. Pathol., 1985, vol. 95, pp. 565-576 [PMID: 2999199]

Khalafalla A.I., Gaffar Elamin M.A., Abbas Z. Lumpy skin disease: observations on the recent outbreaks of the disease in the Sudan. Rev. Elev. Med. Vet. Pays Trop., 1993, vol. 46, pp. 548–550.[PubMed]

Yeruham I., Perl S., Nyska A., Abraham A., Davidson M., Haymovitch M., Zamir O., and Grinstein H. Adverse reactions in cattle to a capripox vaccine. Vet. Rec., 1994, vol. 135, pp. 330-332. [PubMed]

Somasundaram M.K. An outbreak of lumpy skin disease in a Holstein Dairy Herd in Oman: a clinical report. Asian J. Anim. Vet. Adv., 2011, vol. 6, pp. 851-859.

Ayelet G., Abate Y., Sisay T., Nigussie H., Gelaye E., Jemberie S., Asmare K. Lumpy skin disease: preliminary vaccine efficacy assessment and overview on outbreak impact in dairy cattle at Debre Zeit, central Ethiopia. Antiviral Res., 2013, vol. 98, pp. 261-265. [PubMed]

Tageldin M.H., Wallace D.B., Gerdes G.H., Putterill J.F., Greyling R.R., Phosiwa M.N., Al Busaidy R.M., and Al Ismaaily S.I. Lumpy skin disease of cattle: an emerging problem in the Sultanate of Oman. Trop. Anim. Health Prod., 2014, vol. 46, pp. 241-246. [PubMed]

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, vol. 36, pp. 307-320. Crossref

Artenstein A.W., Grabenstein J.D. Smallpox vaccines for biodefense: need and feasibility. Expert Rev. Vaccines, 2008, vol. 7, pp. 1225-1237. doi: 10.1586/14760584.7.8.1225.

Moss B. Reflections on the early development of poxvirus vectors Vaccine, 2013, vol. 31, pp. 4220-4222. Crossref

Liu F., Wu X., Li L., Zou Y., Liu S., Wang Z. Evolutionary characteristics of morbilliviruses during serial passages in vitro: Gradual attenuation of virus virulence. Comp. Immunol. Microbiol. Infect. Dis., 2016, vol. 47, pp. 7-18. doi: 10.1016/j.cimid.2016.05.007.

Xia J., He X., Du L.J., Liu Y.Y., You G.J., Li S.Y., Liu P., Cao S.J., Han X.F., Huang Y. Preparation and protective efficacy of a chicken embryo kidney cell-attenuation GI-19/QX-like avian infectious bronchitis virus vaccine. Vaccine, 2018, vol. 36, pp. 4087-4094. doi: 10.1016/j.vaccine.2018.05.094.

Sergeyev V.A., Nepoklonov Ye.A., Aliper T.I. Viruses and viral vaccines. Moscow: Biblionica, 2007, 524 p.

Johnston J.B., McFadden G. Technical knockout: understanding poxvirus pathogenesis by selectively deleting viral immunomodulatory genes. Cellular Microbiology, 2004, vol. 6, pp. 695-705. doi:10.1111/j.1462-5822.2004.00423.x

Smith D.R., Johnston S.C., Piper A., Botto M., Donnelly G., Shamblin J., Albariño C.G., Hensley L.E., Schmaljohn C., Nichol S.T., Bird B.H. Attenuation and efficacy of live-attenuated Rift Valley fever virus vaccine candidates in non-human primates. PLoS. Negl. Trop. Dis., 2018, vol. 12(5): e0006474. doi: 10.1371/journal.pntd.0006474.

Li P., Ke X., Wang T., Tan Z., Luo D., Miao Y., Sun J., Zhang Y., Liu Y., Hu Q., Xu F., Wang H., Zheng Z. Zika Virus attenuation by codon pair deoptimization induces sterilizing immunity in mouse models. J Virol., 2018, pii: JVI.00701-18. doi: 10.1128/JVI.00701-18.

Conrad S.J., Silva R.F., Hearn C.J., Climans M., Dunn J.R. Attenuation of Marek's disease virus by codon pair deoptimization of a core gene. Virology, 2018, vol. 516, pp. 219-226. doi: 10.1016/j.virol.2018.01.020.

Eschke K., Trimpert J., Osterrieder N., Kunec D. Attenuation of a very virulent Marek's disease herpesvirus (MDV) by codon pair bias deoptimization. PLoS Pathog., 2018, vol. 14(1):e1006857. doi: 10.1371/journal.ppat.1006857.

Shchelkunov S.N. Smallpox virus – a source of new medical preparations. Soros Weducational Journal, 1995, no. 1, pp. 28-31

Seet B.T., Johnston J.B., Brunetti C.R., Barrett J.W., Everett H., Cameron C., Sypula J., Nazarian S.H., Lucas A., McFadden G. Poxviruses and immune evasion. Annu. Rev. Immunol., 2003, vol. 21, pp. 377-423. Crossref

Smith G.L., Benfield C.T., Maluquer de Motes C., Mazzon M., Ember S.W., Ferguson B.J., Sumner R.P. Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. J. Gen. Virol., 2013, vol. 94, pp. 2367-2392. doi: 10.1099/vir.0.055921-0.

Johnston J.B., McFadden G. Poxvirus immunomodulatory strategies: current perspectives. J. Virol., 2003, vol. 77, no. 11, pp. 6093–6100 Crossref

Lee M.S., Roos J.M., McGuigan L.C., Smith K.A., Cormier N., Cohen L.K., Roberts B.E., Payne L.G. Molecular attenuation of vaccinia virus: mutant generation and animal characterization. J. Virol., 1992, vol. 66, pp. 2617-2630. [PMID: 1560521]

Dallo S., Maa S., Rodriguez R., Rodriguez D., Esteban M. Humoral immune response elicited by highly attenuated variants of vaccinia virus and by an attenuated recombinant expressing HIV-1 envelope protein. Virology, 1989, vol. 173, pp. 323-329. Crossref

Shida H., Hinuma Y., Hatanaka M., Morita M., Kidokoro M., Suzuki K., Maruyama T., Takahashi-Nishimaki F., Sugimoto M., Kitamura R., Miyazawa T., Hayami M. Effects and virulences of recombinant vaccinia viruses derived from attenuated strains that express the human T-cell leukemia virus type I envelope gene. J. Virol., 1988, vol. 62, pp. 4474-4480. [PMID: 3184271]

Shida H., Tochikura T., Sato T., Konno T., Hirayoshi K., Seki M., Ito Y., Hatanaka M., Hinuma Y., Sugimoto M., Takahashi-Nishimaki F., Maruyama T., Miki K., Suzuki K., Morita M., Sashiyama H., Hayami M. Effect of the recombinant vaccinia viruses that express HTLV-I envelope gene on HTLV-I infection. EMBO J., 1987, vol. 6, pp. 3379-3384. [PMID: 2828027]

Kotwal G.J., Hugin A.W., Moss B. Mapping and insertional mutagenesis of a vaccinia virus gene encoding a 13,800-Da secreted protein. Virology, 1989, vol. 171, pp. 579-587. Crossref

Kan S., Jia P., Sun L., Hu N., Li C., Lu H., Tian M., Qi Y., Jin N., Li X. Generation of an attenuated Tiantan vaccinia virus by deletion of the large subunit ribonucleotide reductase. Arch Virol., 2014, vol. 159, pp. 2223-2231. Crossref

Lynn H., Horsington J., Ter L.K., Han S., Chew Y.L., Diefenbach R.J., Way M., Chaudhri G., Karupiah G., Newsome TP. Loss of cytoskeletal transport during egress critically attenuates ectromelia virus infection in vivo. J. Virol., 2012, vol. 86, pp. 7427-43. Crossref

Dénes B., Gridley D.S., Fodor N., Takátsy Z., Timiryasova T.M., Fodor I. Attenuation of a vaccine strain of vaccinia virus via inactivation of interferon viroceptor. J. Gene Med., 2006, vol. 8, pp. 814-823. Crossref

Verardi P.H., Jones L.A., Aziz F.H., Ahmad S., Yilma T.D. Vaccinia virus vectors with an inactivated gamma interferon receptor homolog gene (B8R) are attenuated in vivo without a concomitant reduction in immunogenicity. J. Virol., 2001, vol. 75, pp. 11–18. Crossref

Sroller V., Ludvíková V., Maresová L., Hainz P., Nĕmecková S. Effect of IFN-gamma receptor gene deletion on vaccinia virus virulence. Arch Virol., 2001, vol. 146, pp. 239-249. Crossref

Bartlett N., Symons J.A., Tscharke D.C., Smith G.L. The vaccinia virus N1L protein is an intracellular homodimer that promotes virulence. J Gen Virol., 2002, vol. 83, pp. 1965-1976. Crossref

Ren H., Ferguson B.J., Maluquer de Motes C., Sumner R.P., Harman L.E., Smith G.L. Enhancement of CD8(+) T-cell memory by removal of a vaccinia virus nuclear factor-κB inhibitor. Immunology, 2015, vol. 145, pp. 34-49. Crossref

Engelstad M., Howard S.T., Smith G.L. A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology, 1992, vol. 188, pp. 801–810. Crossref

Law M., Smith G.L. Antibody neutralization of the extracellular enveloped form of vaccinia virus. Virology, 2001, vol. 280, pp. 132-142. Crossref

Mathew E., Sanderson C.M., Hollinshead M., Smith G.L. The extracellular domain of vaccinia virus protein B5R affects plaque phenotype, extracellular enveloped virus release, and intracellular actin tail formation. J Virol., 1998, vol. 72, pp. 2429-2438. [PMC109543]

Estep R.D., Messaoudi I., O'Connor M.A., Li H., Sprague J., Barron A., Engelmann F., Yen B., Powers M.F., Jones J.M., Robinson B.A., Orzechowska B.U., Manoharan M., Legasse A., Planer S., Wilk J., Axthelm M.K., Wong S.W. Deletion of the monkeypox virus inhibitor of complement enzymes locus impacts the adaptive immune response to monkeypox virus in a nonhuman primate model of infection. J Virol., 2011, vol. 85, pp. 9527-9542. Crossref

Legrand F.A., Verardi P.H., Jones L.A., Chan K.S., Peng Y., Yilma T.D. Induction of potent humoral and cell-mediated immune responses by attenuated vaccinia virus vectors with deleted serpin genes. J. Virol., 2004, vol. 78, pp. 2770-2779. Crossref

Zhu W., Fang Q., Zhuang K., Wang H., Yu W., Zhou J., Liu .L, Tien P., Zhang L., Chen Z. The attenuation of vaccinia Tian Tan strain by the removal of the viral M1L-K2L genes. J. Virol. Methods, 2007, vol. 144, pp. 17-26. Crossref

Li Y., Zhu Y., Chen S., Li W., Yin X., Li S., Xiao P., Han J., Li X., Sun L., Jin N. Generation of an attenuated Tiantan vaccinia virus strain by deletion of multiple genes. Front Cell Infect. Microbiol., 2017, vol. 31, pp. 7:462. Crossref

Yakubitskiy S.N., Kolosova I.V., Maksyutov R.A., Shchelkunov S.N. Attenuation of Vaccinia Virus. Acta Naturae, 2015, vol. 7, no. 4, pp. 113-121.

Tartaglia J., Perkus M.E., Taylor J., Norton E.K., Audonnet J.-C., Cox W.I., Davis S.W., Van Der Hoeven J., Meignier B., Riviere M., Languet B., Paoletti E. NYVAC: A highly attenuated strain of vaccinia virus. Virology, 1992, vol. 188, pp. 217-232. Crossref

Meyer H., Sutter G., Mayr A. Mapping of deletions in the genome of the highly attenuated vaccinia virus MVA and their influence on virulence. J. Gen. Virol., 1991, vol. 72, pp. 1031-1038. Crossref

Najera J.L., Gomez C.E., Domingo-Gil E., Gherardi M.M., Esteban M. Cellular and biochemical differences between two attenuated poxvirus vaccine candidates (MVA and NYVAC) and role of the C7L gene. J. Virol., 2006, vol. 80, pp. 6033-6047. Crossref

Najera J.L., Gomez C.E., Garcia-Arriaza J., Sorzano C.O., Esteban M. Insertion of vaccinia virus C7L host range gene into NYVAC-B genome potentiates immune responses against HIV-1 antigens. PLoS One. 2010; vol. 30, no. 5(6):e11406 Crossref

Quakkelaar E.D., Redeker A., Haddad E.K., Harari A., McCaughey S.M., Duhen T., Filali-Mouhim A., Goulet J.P., Loof N.M., Ossendorp F., Perdiguero B., Heinen P., Gomez C.E., Kibler K.V., Koelle D.M., Sékaly R.P., Sallusto F., Lanzavecchia A., Pantaleo G., Esteban M., Tartaglia J., Jacobs B.L., Melief C.J. Improved innate and adaptive immunostimulation by genetically modified HIV-1 protein expressing NYVAC vectors. PLoS One, 2011, vol. 6:e16819. Crossref

Wyatt L.S., Carroll M.W., Czerny C.P., Merchlinsky M., Sisler J.R., Moss B. Marker rescue of the host range restriction defects of modified vaccinia virus Ankara. Virology, 1998, vol. 251, pp. 334-342. Crossref

Liu Z., Wang S., Zhang Q., Tian M., Hou J., Wang R., Liu C., Ji X., Liu Y., Shao Y. Deletion of C7L and K1L genes leads to significantly decreased virulence of recombinant vaccinia virus TianTan. PLoS One, 2013, vol. 8(7):e68115. Crossref

Shchelkunov S., Totmenin A., Kolosova I. Species-specific differences in organization of orthopoxvirus kelch-like proteins. Virus Genes, 2002, vol. 24, pp. 157-162. [PMID: 12018707]

Xue F., Cooley L. kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell., 1993, vol. 72, pp. 681-693. [PMID: 8453663]

Laezza F., Wilding T.J., Sequeira S., Coussen F., Zhang X.Z., Hill-Robinson R., Mulle C., Huettner J.E., Craig A.M. KRIP6: a novel BTB/kelch protein regulating function of kainate receptors. Mol. Cell. Neurosci., 2007, vol. 34(4), pp. 539-550. Crossref

Shchelkunov S.N., Totmenin A.V., Loparev V.N., Safronov P.F., Gutorov V.V., Chizhikov V.E., Knight J.C., Parsons J.M., Massung R.F., Esposito J.J. Alastrim smallpox variola minor virus genome DNA sequences. Virology, 2000, vol. 266, pp. 361-386. Crossref

Perkus M.E., Goebel S.J., Davis S.W., Johnson G.P., Norton E.K., Paoletti E. Deletion of 55 open reading frames from the termini of vaccinia virus. Virology, 1991, vol. 180, pp. 406-410. Crossref

de Miranda M.P., Reading P.C., Tscharke D.C., Murphy B.J., Smith G.L. The vaccinia virus kelch-like protein C2L affects calcium-independent adhesion to the extracellular matrix and inflammation in a murine intradermal model. J. Gen.Virol., 2003, vol. 84, pp. 2459-2471. Crossref

Kochneva G., Kolosova I., Maksyutova T., Ryabchikova E., Shchelkunov S. Effects of deletions of kelch-like genes on cowpox virus biological properties. Arch Virol., 2005, vol. 150(9), pp. 1857-1870. Crossref

Egilmez N.K. Cytokines as vaccine adjuvants. In: Vaccine Adjuvants and Delivery Systems, ed. M. Singh, John Wiley & Sons, Inc., 2007, pp. 327-354. Crossref

Flexner C., Moss B., London W.T., Murphy B.R. Attenuation and immunogenicity in primates of vaccinia virus recombinants expressing human interleukin-2. Vaccine, 1990, vol. 8(1), pp. 17-21. Crossref

Hügin A.W., Flexner C., Moss B. Clearance of recombinant vaccinia virus expressing IL-2: role of local host immune responses. Cell Immunol., 1993, vol. 152(2), pp. 499-509. Crossref

Perera L.P., Goldman C.K., Waldmann T.A. Comparative assessment of virulence of recombinant vaccinia viruses expressing IL-2 and IL-15 in immunodeficient mice. Proc. Natl. Acad. Sci. USA, 2001, vol. 98(9), pp. 5146-5151. Crossref

Verardi P.H., Legrand F.A., Chan K.S., Peng Y., Jones L.A., Yilma T.D. IL-18 expression results in a recombinant vaccinia virus that is highly attenuated and immunogenic. J. Interferon Cytokine Res., 2014, vol. 34(3), pp. 169-178. Crossref

Weiss K.E. Lumpy Skin Disease Virus. In: Cytomegaloviruses. Rinderpest Virus. Lumpy Skin Disease Virus. Virology Monographs (Die Virusforschung in Einzeldarstellungen). Springer, Berlin, Heidelberg, 1968, pp. 111–131. 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, vol. 81(20), pp. 11392-11401. Crossref

Boshra H., Truong T., Nfon C., Bowden T.R., Gerdts V., Tikoo S., Babiuk L.A., Kara P., Mather A., Wallace D.B., Babiuk S. A lumpy skin disease virus deficient of an IL-10 gene homologue provides protective immunity against virulent capripoxvirus challenge in sheep and goats. Antiviral Res., 2015, vol. 123, pp. 39-49. 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, vol. 36(31), pp. 4708-4715. Crossref

Chakrabarti S., Sisler J.R., and Moss B. Compact, Synthetic, Vaccinia Virus Early/Late Promoter for Protein Expression. BioTechniques, 1997, vol. 23, no. 6, pp. 1094-1097. Crossref