SEROTYPE-SPECIFIC AND HAEMADSORPTION PROTEIN OF THE AFRICAN SWINE FEVER VIRUS
DOI:
https://doi.org/10.26873/SVR-454-2018Abstract
This review presents comparative results of simultaneously conducted studies on proteins responsible for the haemadsorption and serotype-specific properties of African swine fever virus (ASFV). An ASFV gene EP402R (or LMW8-DR) encoding protein CD2v homologous to murine, human or porcine T-cell adhesive receptor was found. The CD2v was shown to be directly involved into a haemadsorption process, and expressed in ASFV-infected cells as a glycoprotein with a molecular weight of approximately 105-110 kDa. In the presence of a glycosylation inhibitor, tunicamycin, its molecular weight is about 42 kDa. In ASFV-infected cells labeled with 3H-glucosamine or 14C-sodium acetate, a virus-specific major glycoprotein with a molecular weight of 110-140 kDa (gp 110-140) was identified using radioimmunoprecipitation assay. Using ASFV reference strains belonging to seroimmunotypes I-IV and the corresponding antisera active in haemadsorption inhibition assay (HADIA), we determined that gp 110-140 defines the serotype specificity. Genotyping on the basis of the genetic locus encoding the CD2v and a C-type lectin protein also showed a concurrence with the grouping of ASFV isolates and strains based on their seroimmunotypes. Immunization of pigs with the gp 110-140 within liposomes, or a recombinant haemagglutinin (CD2v) protected 67 to 100% of animals from death due to their subsequent infection with homologous virulent ASFV strains. Based on the physico-chemical and biological characteristics of the gp 110-140 and CD2v it is suggested that they are one and the same virus-specific glycoprotein crucial for induction of the immunological protection against ASF.
Key words: ASFV; seroimmunotypes; serotype; glycoproteins; gp 110-140; CD2v; protectivity
SEROTIPNO-SPECIFIČEN IN HEMADSORPCIJSKI PROTEIN VIRUSA AFRIŠKE PRAŠIČJE KUGE A.D
Povzetek: Pregledni članek predstavlja primerjavo rezultatov sočasno izvedenih raziskav o beljakovinah, ki so pomembne za hemadsorpcijo in serotipno specifične lastnosti virusa afriške prašičje kuge (ASFV; iz angl. african swine fever virus). Pri virusu ASFV je bil odkrit gen EP402R (imenovan tudi LMW8-DR), ki kodira beljakovino CD2v, ki je homologna glodavskemu, človeškemu in prašičjemu T-celičnemu adhezivnemu receptorju. Pokazalo se je, da je CD2v neposredno vpletena v proces hemadsorpcije in je izražena v celicah, okuženih z ASFV kot glikoprotein z molekulsko maso okrog 105-110 kDa. V prisotnosti zaviralca glikozilacije tunicamicina je njegova molekulska masa približno 42 kDa. V celicah, okuženih z ASFV, označenih s 3H-glukozaminom ali 14C-natrijevim acetatom, je bil s testom radioimunoprecipitacije ugotovljen virusno specifični osrednji glikoprotein z molekulsko maso 110-140 kDa (gp 110-140). Z uporabo referenčnih sevov ASFV, ki pripadajo seroimunotipom I-IV, in ustreznim antiserumom, ki so bili aktivni pri preizkusu zaviranja hemadsorpcije (HADIA), smo ugotovili, da gp 110-140 določa specifičnost serotipa. Genotipizacija na osnovi genskega lokusa, ki kodira CD2v in C-tip lektinske beljakovine, je pokazala soizražanje s skupino izolatov in sevov ASFV na podlagi njihovih seroimunotipov. Imunizacija prašičev z gp 110-140 v liposomih ali z rekombinantnim hemaglutininom (CD2v) je zaščitila od 67 do 100 odstotkov živali pred smrtjo zaradi njihove naknadne okužbe z virulentnimi sevi ASFV. Na podlagi fizikalno-kemičnih in bioloških značilnosti beljakovin gp 110-140 in CD2v menimo, da gre za isti virusni glikoprotein, ki je ključnega pomena za vzpodbuditev imunološke zaščite pred ASF.
Ključne besede: ASFV; seroimunotipi; serotip; glikoproteini; gp 110-140; CD2v; zaščita
References
(1) Dixon LK, Alonso C, Escribano JM, et al. Asfarviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, eds. Virus taxonomy. Classification and nomenclature of viruses. Ninth Report of the International Committee on Taxonomy of Viruses (ICTV). Oxford: Elsevier, 2011: 153–62.
(2) Sanchez-Vizcaino JM, Arias M. African swine fever virus. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, eds. Diseases of swine. 10th ed, Ames: Wiley-Blackwell, 2012: 396–404.
(3) Malmquist WA, Hay D. Hemadsorption and cytopathic effect produced by African swine fever virus in swine bone marrow and buffy coat cultures. Am J Vet Res 1960; 21: 104–8.
(4) Hess WR, De Tray DE. The use of leukocyte cultures for diagnosing African swine fever (ASF). Bull Epizoot Dis Afr 1960; 8: 317–20.
(5) Enjuanes L, Carrascosa AL, Moreno MA, Vinuela E. Titration of African swine fever (ASF) virus. J Gen Virol 1976; 32: 471–7.
(6) Sereda AD, Balyshev VM, Morgunov YP, Kolbasov DV. Ðntigenic characteristics of African swine fever virus in artificial and natural mixed populations [in Russian]. Sel'skokhozyaistvennaya biologiya [Agric Biol] 2014; 4: 64–9.
(7) Malmquist WA. Serologic and immunologic studies with African swine fever virus. Am J Vet Res 1963; 24: 450–9.
(8) Lucas A, Haag J, Larenaudie B. La peste porcine africane. Collection monographique. Paris: Expansion scientifique française, 1967.
(9) Sanchez-Botija C, Ordas A. Laboratory manual for diagnosis of african swine fever. Madrid: Instituto Nacional de Investigaciones Agrarias, 1977: 133–6.
(10) Vigario JD, Terrinha AM, Bastos AL, Moura Nunes JF, Marques D, Silva JF. Serological behaviour of isolated African swine fever virus: brief report. Arch Gesamte Virusforsch 1970; 31: 387–9.
(11) Vishnyakov IF, Mitin NI, Karpov G, Kurinnov VV, Yashin A. Differentiation of African and classical swine fever viruses [in Russian]. Veterinariya 1991; 4: 28–31.
(12) Vishnyakov IF, Mitin NI, Petrov YI, et al. Seroimmunological classification of natural African swine fever virus isolates [in Russian]. Actual’nye voprosy veterinarnoi virusologii: mater. nauchn.- prakt. konf. VNIIVViM “Klassicheskaya chuma svinei – neotlozhnye problemy, nauki I praktiki†(Current Problems of Veterinary Virology: Proc Sci Pract Conf VNIIVViM “Classical Swine Fever – Pressing Problems of Science and Practiceâ€). Pokrov, 1995: 141–3.
(13) Balyshev VM, Kalantaenko YF, Bolgova MV, Prudnikova EY. Seroimmunological affiliation of African swine fever virus isolated in the Russian Federation. Russ Agric Sci 2011; 37: 427–9.
(14) Sereda AD, Balyshev VM. Antigenic diversity of African swine fever viruses [in Russian]. Vopr Virusol 2011; 56: 38-42.
(15) Balyshev VM, Bolgova MV, Balysheva VI, Knyazeva NV, Zhivoderov SP. Рreparation of standard haemadsorption-inhibiting reference sera against African swine fever virus [in Russian]. Voprosy normativno-pravovogo regulirovaniya v veterinarii 2015; 2: 23–5. https://rucont.ru/ efd/379353 (July 22, 2017).
(16) Bastos ADS, Penrith ML, Cruciere C, et al. Genotyping field strains of African swine fever virus by partial p72 gene characterisation. Arch Virol 2003; 148: 693–706.
(17) Achenbach JE, Gallardo C, Nieto-Pelegrin E, et al. Identification of a new genotype of African swine fever virus in domestic pigs from Ethiopia. Transbound Emerg Dis 2017; 64(5): 1393–404.
(18) Malogolovkin A, Burmakina G, Titov I, et al. Comparative analysis of African swine fever virus genotypes and serogroups. Emerg Infect Dis 2015; 21: 312–15.
(19) Rodriguez JM, Yanez RJ, Almazan F, Vinuela E, Rodriguez JF. African swine fever virus en codes a CD2 homolog responsible for the adhesion of erythrocytes to infected cells. J Virol 1993; 67: 5312–20.
(20) Borca MV, Kutish GF, Afonso CL, et al. An African swine fever virus gene with similarity to the T-lymphocyte surface antigen CD2 mediates hemadsorption. Virology 1994; 199: 463–8.
(21) Borca MV, Carrillo C, Zsak L, et al. Deletion of a CD2-like gene, 8-DR, from African swine fever virus affects viral infection in domestic swine. J Virol 1998; 72: 2881–9.
(22) Peterson A, Seed B. Monoclonal-antibody and ligand-binding sites of the T-cell erythrocyte receptor (CD2). Nature 1987; 329: 842–6.
(23) Goatley LC, Dixon LK. Processing and localisation of the African swine fever virus CD2v transmembrane protein. J Virol 2011; 85: 3294– 305.
(24) Ruiz-Gonzalvo F, Rodriguezv, Escribano JM. Functional and immunological properties of the baculovirus-expressed hemagglutinin of African swine fever virus. Virology 1996; 218: 285–9.
(25) Kay-Jackson PC, Goatley LC, Cox L, et al. The CD2v protein of African swine fever virus interacts with the actin-binding adaptor protein SH3P7. J Gen Virol 2004; 85: 119–30.
(26) Sereda AD, Makarov VV. Identification of isolate-specific glycopolypeptide of African swine fever virus [in Russian]. Veterinariya 1992; 1: 22–4.
(27) Sereda AD, Anokhina EG, Fugina LG, Makarov VV. Serological and physical-chemical properties of gp 110-140 of African swine fever virus [in Russian]. Veterinariya 1993; 1: 26–8.
(28) Sereda AD, Anokhina EG, Makarov VV. Glycoproteins from the African swine fever virus [in Russian]. Vopr Virusol 1994; 39: 278–81.
(29) Sereda AD. Quantitative determination of the antigenic relatedness of haemadsorbing ASFV strains [in Russian]. Veterinariya 2011; 6: 26–8.
(30) Tulman ER, Delhon GA, Ku BK, Rock DL. African swine fever virus. Curr Top Microbiol Immunol 2009; 328: 43–87.
(31) Chapman DA, Tcherepanov V, Upton C, Dixon LK. Comparison of the genome sequences of non-pathogenic and pathogenic African swine fever virus isolates. J Gen Virol 2008; 89: 397– 408.
(32) Makarov VV, Sereda AD, Piria AA, Malakhova MS. The functional role of the glycosylation of viral components [in Russian]. Vopr Virusol 1992; 37: 267–70.
(33) Mebus CA, Dardiri AH. Western hemisphere isolates of African swine fever virus: asymptomatic carriers and resistance to challenge inoculation. Am J Vet Res 1980; 41: 1867–9.
(34) Ruiz-Gonzalvo F, Carnero E, Bruvel V. Immunological responses of pigs to partially attenuated African swine fever virus and their resistance to virulent homologous and heterologous viruses. In: Wilkinson PJ, eds. Proceedings of CEC/FAO Research Seminar, Sardinia. ASF, EUR 8466 EN. Luxembourg: Commission of the European Communities, 1983: 2066–216.
(35) Hamdy FM, Dardiri AH. Clinic and immunologic responses of pigs to African swine virus isolated from the Western hemisphere. Am J Vet Res 1984; 45: 711–4.
(36) Kolbasov DV, Balyshev VM, Sereda AD. Results of research works on the development of live vaccines against African swine fever [in Russian]. Veterinariya 2014; 8: 3–8.
(37) Lacasta A, Monteagudo PL, Jiménez-MarÃn Ã, et al. Live attenuated African swine fever viruses as ideal tools to dissect the mechanisms involved in viral pathogenesis and immune protection. Vet Res 2015; 46: 135 (1–16). https://veterinaryresearch.biomedcentral.com/track/pdf/10.1186/ s13567-015-0275-z (July 22, 2017)
(38) Makarov VV, Perzashkevich VS, Sereda AD, Vlasov NA, Kadetov VV. Immunological estimation algorithm of protective potential of viral components. [Study of preparations of purified inactivated African swine fever virus] [in Russian]. Vestnik Rossiiskoi Akademii Sel'skokhozyaistvennykh Nauk 1995; 6: 60–2.
(39) Sereda AD. Immunogenic and protective characteristics of African swine fever virus glycoproteins [in Russian]. Actual’nye Voprosy Veterinarnoi Biologii 2013; 4: 31–5.
(40) Ruiz-Gonzalvo F, Coll JM. Characterization of a soluble hemagglutinin induced in African swine fever virus-infected cells. Virology 1993; 196: 769–77.
(41) Argilaguet JM, Perez-Martin E, Nofrarias M, et al. DNA vaccination partially protects against African swine fever virus lethal challenge in the absence of antibodies. PLoS ONE 2012; 7(9): e40942 (1–11).
(42) Argilaguet JM, Perez-Martin E, Lopez S, et al. BacMam immunization partially protects pigs against sublethal challenge with African swine fever virus. Antiviral Res 2013; 98: 61–5.
(43) Garcia-Barreno B, Sanz A, Nogal ML, Vinuela E, Enjuanes L. Monoclonal antibodies of Afri can swine fever virus: antigenic differences among field virus isolates and viruses passaged in cell culture. J Virol 1986; 58: 385–92.
(44) Wesley RD, Tuthill AE. Genome relatedness among African swine fever field isolates by restriction endonuclease analysis. Prev Vet Med 1984; 2: 53–62.
(45) Dixon LK, Wilkinson PJ. Genetic diversity of African swine fever virus isolates from soft ticks (Ornithodoros moubata) inhabiting burrows in Zambia. J Gen Virol 1988; 69: 2981–93.
(46) Sumption KJ, Hutchings GH, Wilkinson PJ, Dixon LK. Variable regions on the genome of the Malawi isolate of African swine fever virus. J Gen Virol 1990; 71: 2331–40.
(47) Ekue NF, Wilkinson PJ. Comparison of genomes of African swine fever virus isolates from Cameroon, other African countries and Europe. Rev Elev Med Vet Pays Trop 2000; 53: 229–36.
(48) Selyaninov JO, Balyshev VM, Tsybanov SZ. African swine fever virus: physical mapping of the genome of the strains [in Russian]. Vestnik Rossiiskoi Akademii Sel'skokhozyaistvennykh Nauk 2000; 5: 75–6.
(49) Lubisi BA, Bastos AD, Dwarka RM, Vosloo W. Molecular epidemiology of African swine fever in East Africa. Arch Virol 2005; 150: 2439–52.
(50) Boshoff CI, Bastos AD, Gerber LJ, Vosloo W. Genetic characterisation of African swine fever viruses from outbreaks in southern Africa (1973– 1999). Vet Microbiol 2007; 121: 45–55.
(51) Nix RJ, Gallardo C, Hutchings G, Blanco E, Dixon LK. Molecular epidemiology of African swine fever virus studied by analysis of four variable genome regions. Arch Virol 2006; 151: 2475–94.
(52) Chapman DA, Darby AC, Da Silva M, Upton C, Radford AD, Dixon LK. Genomic analysis of highly virulent Georgia 2007/1 isolate of African swine fever virus. Emerg Infect Dis 2011; 17: 599–605.
(53) Malogolovkin A, Burmakina G, Tulman MS, et al. African swine fever virus CD2v and C-type lectin gene loci mediate serological specificity. J Gen Virol 2015; 96: 866–73.
