doi: 10.15389/agrobiology.2016.6.763eng

UDC 636.4:619:578.842.1:616-097:57.083.3

Supported by Russian Science Foundation (the research project «Design of African swine fever virus candidate vaccine based on chimeric viruses», contract No 16-16-00090)



A.D. Sereda1, A.R. Imatdinov1, V.V. Makarov2

1All-Russian Institute of Veterinary Virology and Microbiology, Federal Agency of Scientific Organizations, 1, ul. Akademika Bakuleva, pos. Vol’ginskii, Petushinskii Region, Vladimir Province, 601125 Russia, e-mail;
2Peoples' Friendship University of Russia, Agro-Technological Institute, 8/2, ul. Miklukho-Maklaya, Moscow, 117198 Russia, e-mail

Received August 29, 2016


The capability of causing haemadsorption at African swine fever (ASF) virus (ASFV) reproduction in swine bone marrow cell cultures, leukocytes or continuous cells in the presence of swine erythrocytes is characteristic of the majority of the virus isolates (W.A. Malmquist, D. Hay, 1960). This trait is used for ASF diagnosis based on autohaemadsorption in porcine blood, the virus titration in cell culture, and selection of its attenuated variants in vitro (A.D. Sereda et al., 2014). The haemadsorption inhibition assay (HIA) in tandem with the bioassay using the disease-resistant pigs is applied for seroimmunotype-based classification of ASFV isolates (N.I. Mitin et al., 1985). The heterogeneity of an ASFV population for quantitative haemadsorption characteristic (like «dense», «moderate» or «loose») is a phenotypic trait of ASFV isolates, strains and/or variants (V. Makarov et al., 2016). Also, the proportion of the circumference of red blood cells as observed at their contact with infected macrophages serves as another quantifiable feature of haemadsorption. Some quantitative differences in HIA activity levels of swine blood sera are determined in the assays carried out using virulent reference variants and their attenuated derivatives, and the obtained results require some interpretation. The loss of ability to induce haemadsorption is not critical for ASFV reproduction and often accompanied by a decrease in the pathogen virulence levels. Hence, as a rule, attenuated ASFV variants are prepared through a selection by limiting dilution from populations of virulent isolates of the virus clones that are characterized by a reduced potential to induce haemadsorption (D.V. Kolbasov et al., 2014). In the course of the virus reproduction, haemadsorption precedes the exocytosis. Virions do not play a significant role in the mechanism of haemadsorption, nevertheless, their interaction with erythrocyte membranes promotes the virus dissemination throughout the swine organism and more effective introduction into the gut cells of ticks (L.K. Dixon et al., 2004). ASFV haemadsorbing potentiality is determined by highly glycosylated transmembrane protein CD2v (J.M. Rodríguez et al., 1993). Probably, nonhaemadsorbing avirulent isolates emerge as a result of some shift of the open reading frames for EP402R and EP153R encoding the CD2v and lectin-like proteins, respectively (D.A. Chapman et al., 2008). An assumption is made that the haemadsorption phenomenon is due to an interaction between carbohydrate residues of glycoproteins of ASFV oligosaccharides and lectin-like receptors of swine red blood cells.

Keywords: African swine fever, haemadsorption, non-haemadsorbing isolates.


Full article (Rus)

Full text (Eng)



  1. Dixon L.K., Costa J.V., Escribano J.M., Rock D.L., Vinuela E., Wilkinson P.J. Family Asfarviridae. In: Virus taxonomy: seventh report of the International Committee on Taxonomy of Viruses. M.H.V.V. Regenmortel, C.M. Fauquet, D.H.L. Bishop, E.B. Car-stens, M.K. Estes, S.M. Lemon, J. Maniloff, M.A. Mayo, D.J. McGeoch, C.R. Pringle, R.B. Wickner (eds.). Academic Press, San Diego, CA, 2000: 159-165.
  2. Sanchez-Vizca?no J.M., Mur L., Martinez-Lopez B. African swine fever: An epidemiological update. Transbound. Emerg. Dis., 2012, 59(1): 27-35 CrossRef
  3. Malmquist W.A., Hay D. Hemadsorbtion and cytophatic effect produced by African swine fever virus in swine bone marrow and buffy coat culture. Am. J. Vet. Res., 1960, 21: 104-108.
  4. Malogolovkin A., Burmakina G., Titov I., Sereda A., Gogin A., Baryshnikova E., Kolbasov D. Comparative analysis of African swine fever virus genotypes and serogroups. Emerg. Infect. Dis., 2015, 21(2): 312-315 CrossRef
  5. Kolbasov D.V., Balyshev V.M., Sereda A.D. Veterinariya, 2014, 8: 3-8 (in Russ.).
  6. Uhlendorff J., Matrosovich T., Klenk H.D., Matrosovich M. Functional significance of the hemadsorption activity of influenza virus neuraminidase and its alteration in pandemic viruses. Arch. Virol., 2009, 154: 945-957 CrossRef
  7. Saburi Y., Okuda K., Takhashi T. Electron microscopic study of gemadsorbtion on vaccinia virus infected cells.  Microbiol. Immunol., 1977, 21(10): 593-600.
  8. Breese S.S., Hess W.R. Electron microscopy of African swine fever virus hemadsorbtion. J. Bacteriol., 1966, 92(1): 272-274.
  9. Makarov V., Nedosekov V., Sereda A., Matvienko N. Immunological conception of African swine fever. Zoology and Ecology, 2016, 26(3): 236-243 CrossRef
  10. Makarov V.V. Afrikanskaya chuma svinei [African swine fever]. Moscow, 2011 (in Russ.).
  11. Coggins L. Segregation of a non-hemadsorbing African swine fever virus in tissue culture. The Cornell Veterinarian, 1968, 58(1): 12-20.
  12. Coggins L. African swine fever virus. Pathogenesis. Prog. Med. Virol., 1974, 18: 48-65.
  13. Malakhova M.S. Vzaimodeistvie virusa ACHS s immunokompetentnymi kletkami svin'i. Kandidatskaya dissertatsiya [ASF virus interaction with immune cells in pigs. PhD Thesis]. Pokrov, 1987 (in Russ.).
  14. Quintero J.C., Wesley R.D., Whyard T.C., Gregg D., Mebus C.A. In vitro and in vivo association of African swine fever virus with swine erythrocytes. Am. J. Vet. Res., 1986, 47(5): 1125-1131.
  15. Rowlands R.J., Duarte M.M., Boinas F., Hutchings G., Dixon L.K. The CD2v protein enhances African swine fever virus replication in the tick vector, Ornithodoros erraticus. Virology, 2009, 393: 319-328 CrossRef
  16. Sierraj M.A., Gomez-Villamanld C., Rasco O., Fernandeez A., Jover A. In vivo study of hemadsorption in African swine fever virus infected cells. Vet. Pathol., 1991, 28: 178-181.
  17. Makarov V.V., Vishnyakov I.F., Vlasov N.A., Serova A.M. Voprosy virusologii, 1991, 4: 321-324 (in Russ.).
  18. Makarov V.V., Sukharev O.I., Tsvetnova I.V. Veterinarnaya praktika, 2013, 60(1): 6-16 (in Russ.).
  19. Makarov V.V. Veterinarnaya praktika, 2013, 62(3): 7-22 (in Russ.).
  20. Mitin N.I., Shevchenko A.A., Balyshev V.M., Elisova S.N. Differentsiatsiya virulentnykh i attenuirovannykh shtammov virusa ACHS v RZGA. Tezisy nauchnoi konferentsii VNIIVViM, posvyashchennoi 40-letiyu Velikoi Pobedy «Voprosy veterinarnoi virusologii, mikrobiologii i epizootologii» [Proc. Conf. «Veterinary virology, microbiology and epizootology»]. Pokrov, 1985: 39-41 (in Russ.).
  21. Shubina N.G., Kolontsov A.A., Malakhova M.S., Makarov V.V. Byulleten' eksperimental'noi biologii i meditsiny, 1996, 122(10): 418-424 (in Russ.).
  22. Šereš M., Cholujová D., Bubencíkova T., Breier A., Sulová Z. Tunicamycin depresses P-glycoprotein glycosylation without an effect on its membrane localization and drug efflux activity in L1210 cells. Int.J.Mol.Sci., 2011, 12(11): 7772-7784 CrossRef
  23. Makarov V.V., Sereda A.D., Pirya A.A., Malakhova M.S. Voprosy virusologii, 1992, 5-6: 267-270 (in Russ.).
  24. Reszka N., Krol E., Patel A.H., Szewczyk B. Effect of tunicamycin on the biogenesis of hepatitis C virus glycoproteins. Acta biochimika Polonica, 2010, 57(4): 541-546.
  25. Shi X., Brauburger K., Elliott R.M. Role of N-linked glycans on bunyamwera virus glycoproteins in intracellular trafficking, protein folding, and virus infectivity. J. Virol., 2005, 79(21): 13725-13734 CrossRef
  26. Gonzague M., Roger F., Bastos A., Burger C., Randriamparany T., Smondack S., Cruciere C. Isolation of a non-haemadsorbing, non-cytopathic strain of African swine fever virus in Madagascar. Epidemiol. Infect., 2001, 126(3): 453-459 CrossRef
  27. Boinas F.S., Hutchings G.H., Dixon L.K., Wilkinson P.J. Characterization of pathogenic and non-pathogenic African swine fever virus isolates from Ornithodoros erraticus inhabiting pig premises in Portugal. J. Gen. Virol., 2004, 85: 2177-2187 CrossRef  
  28. Oura C.A.L., Denyer M.S., Takamatsu H., Parkhouse R.M.E. In vivo depletion of CD8+ T lymphocytes abrogates protective immunity to African swine fever virus. J. Gen. Virol., 2005, 86(9): 2445-2450 CrossRef
  29. Souto R., Mutowembwa P., van Heerden J., Fosgate G.T., Heath L., Vosloo W. Vaccine potential of two previously uncharacterized African swine fever virus isolates from Southern Africa and heterologous cross protection of an avirulent European isolate. Transbound. Emerg. Dis., 2016, 63: 224-231 CrossRef
  30. Kolbasov D.V., Sereda A.D. Veterinariya, 2013, 1: 19-23 (in Russ.).
  31. Jori F., Bastos A.D.S. Role of wild suids in the epidemiology of African swine fever. EcoHealth, 2009, 6(2): 296-310 CrossRef
  32. Roger F., Crucière C., Randriamahefa N., Zeller H., Uilenberg G., Ra-
    ndriamparany T., Gonzague M., Rousset D., Benkirane A., Diallo A. African swine fever in Madagascar: epidemiological assessment of the recent epizootic. Proc. 9th Int. Symp. on Veterinary Epidemiology and Economics. Breckenridge, Colorado, USA, 2000.
  33. Sereda A.D., Balyshev V.M., Morgunov Yu.P., Kolbasov D.V. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2014, 1: 64-69 CrossRef (in Russ.).
  34. Badaev F.A., Rudobel'skii E.V., Chevelev S.F., Kiselev A.V., Nikishin I.V., Badaeva N.V., Burlakov V.A., Balabanov V.A., Zakharov V.M., Baibikov T.Z., Burdov A.N. Materialy nauchnoi konferentsii VNIIVViM «Voprosy veterinarnoi virusologii, mikrobiologii i epizootologii» [Proc. Conf. «Veterinary virology, microbiology and epizootology»]. Pokrov, 1992, 1: 24-27 (in Russ.).
  35. Badaev F.A., Cheryatnikov L.L., Rudobel'skii E.V., Chevelev S.F., Kiselev A.V., Badaeva N.V., Zakharov V.M., Baibikov T.Z. Materialy nauchnoi konferntsii VNIIVViM «Voprosy veterinarnoi virusologii, mikrobiologii i epizootologii» [Proc. Conf. «Veterinary virology, microbiology and epizootology»]. Pokrov, 1992, 1: 44 (in Russ.).  
  36. Rodríguez J.M., Moreno L.T., Alejo A., Lacasta A., Rodríguez F., Salas M.L. Genome sequence of African swine fever virus BA71, the virulent parental strain of the nonpathogenic and tissue-culture adapted BA71V. PLoS ONE, 2015, 10(11): e0142889 CrossRef
  37. Portugal R., Coelho J., Hoper D., Little N.S., Smithson C., Upton C., Martins C., Leitão A., Keil G.M. Related strains of African swine fever virus with different virulence: genome comparison and analysis. J. Gen. Virol., 2015, 96: 408-419 CrossRef
  38. Morgunov Yu.P., Malogolovkin A.S., Morgunov S.Yu., Burmakina G.S., Kushnir S.D., Yurkov S.G., Tsybanov S.Zh., Kolbasov D.V. Veterinariya, 2015, 10: 53-57 (in Russ.).
  39. Krug P.W., Holinka L.G., O’Donnell V.,  Reese B., Sanford B.,  Fernandez-Sainz I., Gladue D.P., Arzt J., Rodriguez L., Risatti G.R., Borca M.V.  The progressive adaptation of a Georgian isolate of African swine fever virus to Vero cells leads to a gradual attenuation of virulence in swine corresponding to major modifications of the viral genome. J. Virol., 2015, 89(4): 2324-2332 CrossRef
  40. Neser J.A., Pidllips T., Thomson G.R., Gainaru M.D., Coetzee T. African swine fever. I. Morphological changes and virus replication in blood platelets of pigs infected with virulent haemadsorbing and non-haemadsorbing isolates. Onderstepoort J. Vet., 1986, 53: 133-141.
  41. Reis A.L., Parkhouse R.M., Penedos A.R., Martins C., Leitão A. Systematic analysis of longitudinal serological responses of pigs infected experimentally with African swine fever virus. J. Gen. Virol., 2007, 88(9): 2426-2434 CrossRef 
  42. Takamatsu H.H., Denyer M.S., Lacasta A., Stirling C.M.A., Argilaguet J.M., Netherton C.L., Oura C.A.L., Martins C., Rodríguez F. Cellular immunity in ASFV responses. Virus Res., 2013, 173(1): 110-121 CrossRef
  43. Bredikhina T.T., Kolosov V.M., Arkhipova S.N. Tezisy nauchno-teoreticheskoi konferentsii VNIIVViM, posvyashchennoi 60-letiyu obrazovaniya SSSR [Proc. Conf. of ARRIVV&M]. Pokrov, 1983: 120-123 (in Russ.).
  44. Bredikhina T.G., Kolosov V.M. Tezisy nauchno-teoreticheskoi konferentii VNIIVViM, posvyashchennoi 60-letiyu obrazovaniya SSSR [Proc. Conf. of ARRIVV&M]. Pokrov, 1983: 123-124 (in Russ.).
  45. Sereda A.D. Nauchnyi zhurnal KubGAU, 2010, 62(8). Available No date (in Russ.).
  46. Vigario I.D., Terrinha A.M., Moura Nunes J.F. Antigenic relationships among strains of African swine fever virus. Archiv fur die gesamte Virusforschung, 1974, 45(3): 272-277.
  47. Borca M.V., Kutish G.F., Afonso C.L., Irusta P., Carrillo C., Brun A., Sussman M., Rock D.L. An African swine fever virus gene with similarity to the T-lymphocyte surface-antigen Cd2 mediates hemadsorption. Virology, 1994, 199(2): 463-468 CrossRef
  48. Rodríguez J.M., Yáñez R.J., Almazán F., Viñuela E., Rodriguez J.F. African swine fever virus encodes a Cd2 homolog responsible for the adhesion of erythrocytes to infected-cells. J. Virol., 1993, 67(9): 5312-5320.
  49. Kay-Jackson P.C., Goatley L.C., Cox L., Miskin J.E., Parkhouse R.M., Wienands J., Dixon L.K. The CD2v protein of African swine fever virus interacts with the actin-binding adaptor protein SH3P7. J. Gen. Virol., 2004, 85(1): 119-130 CrossRef
  50. Mima K.A., Burmakina G.S., Titov I.A., Malogolovkin A.S. African swine fever virus glycoproteins p54 and CD2v in the context of immune response modulation: bioinformatic analysis of genetic variability and heterogeneity. Agricultural Biology, 2015, 50(6): 785-793 CrossRef (in Engl.).
  51. Ruiz-Gonzalvo F., Rodríguez F., Escribano J.M. Functional and immunological properties of the baculovirus-expressed hemagglutinin of African swine fever virus. Virology, 1996,218(1): 285-289 CrossRef
  52. Goatley L.C., Dixon L.K. Processing and localization of the African swine fever virus CD2v transmembrane Protein.  J. Virol., 2011, 85(7): 3294-3305 CrossRef
  53. Tulman E.R., Delhon G.A., Ku B.K., Rock D.L. African swine fever virus. Curr. Top. Microbiol. Immunol., 2009, 328: 43-87.
  54. Dixon L.K., Abrams C.C., Bowick G., Goatley L.C., Kay-Jackson P.C., Chapman D., Liverani E., Nix R., Silk R., Zhang F. African swine fever virus proteins involved in evading host defense systems. Vet. Immunol. Immunopathol., 2004, 100(3-4): 117-134 CrossRef
  55. Galindo I., Almazán F., Bustos M.J., Viñuela E., Carrascosa A.L. African swine fever virus EP153R open reading frame encodes a glycoprotein involved in the hemadsorption of infected cells. Virology, 2000, 266(2): 340-351 CrossRef
  56. Burmakina G., Malogolovkin A., Tulman E.R., Zsak L., Delhon G., Di-
    el D.G., Shobogorov N.M., Morgunov Y.P., Morgunov S.Y., Kutish G.F., Kolbasov D., Rock D.L. African swine fever virus serotype-specific proteins are significant protective antigens for African swine fever. J. Gen. Virol., 2016, 97(7): 1670-1675 CrossRef
  57. Neilan J.G., Borca M.V., Lu Z., Kutish G.F., Kleiboeker S.B., Carrillo C., Zsak L., Rock D.L. An African swine fever virus ORF with similarity to C-type lectins is non-essential for growth in swine macrophages in vitro and for virus virulence in domestic swine. J. Gen. Virol., 1999, 80(10): 2693-2697 CrossRef
  58. Hurtado C., Granja A.G., Bustos M.J., Nogal M.L., Buitrago G.G., Yébenes V.G., Salas M.L., Revilla Y., Carrascosa A.L. The C-type lectin homologue gene (EP153R) of African swine fever virus inhibits apoptosis both in virus infection and in heterologous expression. Virology, 2004, 326(1): 160-170 CrossRef
  59. Hurtado C., Bustos M.J., Granja A.G., León P., Sabina P., López-Vinñas E., Gómez-Puertas P., Revilla Y., Carrascosa A.L. The African swine fever virus lectin EP153R modulates the surface membrane expression of MHC class I antigens. Arch. Virol., 2011, 156: 219-234 CrossRef
  60. Chapman D.A., Tcherepanov V., Upton C., Dixon L.K. Comparison of the genome sequences of nonpathogenic and pathogenic African swine fever virus isolates. J.Gen. Virol., 2008, 89: 397-408 CrossRef  
  61. Leitão A., Cartaxeiro C., Coelho R., Cruz B., Parkhouse R.M., Portugal F., Vigario J.D., Martins C.L. The non-haemadsorbing African swine fever virus isolate ASFV/NH/P68 provides a model for defining the protective anti-virus immune response. J. Gen. Virol., 2001, 82(3): 513-523 CrossRef
  62. Malogolovkin A., Burmakina G., Tulman E.R., Delhon G., Diel D.G, Salnikov N., Kutish G.F., Kolbasov D., Rock D.L. African swine fever virus CD2v and C-type lectin gene loci mediate serological specificity. J. Gen. Virol., 2015, 96: 866-873 CrossRef
  63. Rowlands R.J., Duarte M.M., Boinas F., Hutchings G., Dixon L.K. The CD2v protein enhances African swine fever virus replication in the tick vector, Ornithodoros erraticus. Virology, 2009, 393(2): 319-328 CrossRef
  64. Sereda A.D., Anokhina E.G., Fugina L.G., Makarov V.V. Veterinariya, 1993, 1: 26-28 (in Russ.).