1887

Abstract

Two strains of African swine fever virus (ASFV), the high-virulence Lisboa60 (L60) and the low-virulence NH/P68 (NHV), which have previously been used in effective immunization/protection studies, were sequenced. Both were isolated in Portugal during the 11-year period after the introduction of ASFV to the European Continent in 1957. The predicted proteins coded by both strains were compared, and where differences were found these were also compared to other strains of known virulence. This highlighted several genes with significant alterations in low-virulence strains of ASFV that may constitute virulence factors, several of which are still uncharacterized regarding their function. Phylogenetic analysis grouped L60 and NHV closest to other P72 genotype I ASFV strains from Europe and West Africa, consistent with the assumed West African origin of all European strains. Interestingly, a relatively lower genomic identity exists between L60 and NHV, both isolated in a similar geographical location 8 years apart, than with other European and west African strains isolated subsequently and in more distant locations. This may reflect the intensive passage in tissue culture, during the early 1960s, of a Portuguese isolate to obtain an attenuated vaccine, which may have led to NHV. This study contributes to a better understanding of the evolution of ASFV, and defines additional potential virulence genes for future studies of pathogenesis towards the development of effective vaccines.

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2015-02-01
2024-04-23
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References

  1. Afonso C. L., Alcaraz C., Brun A., Sussman M. D., Onisk D. V., Escribano J. M., Rock D. L. 1992; Characterization of p30, a highly antigenic membrane and secreted protein of African swine fever virus. Virology 189:368–373 [View Article][PubMed]
    [Google Scholar]
  2. Afonso C. L., Piccone M. E., Zaffuto K. M., Neilan J., Kutish G. F., Lu Z., Balinsky C. A., Gibb T. R., Bean T. J.other authors 2004; African swine fever virus multigene family 360 and 530 genes affect host interferon response. J Virol 78:1858–1864 [View Article][PubMed]
    [Google Scholar]
  3. Agüero M., Blasco R., Wilkinson P., Viñuela E. 1990; Analysis of naturally occurring deletion variants of African swine fever virus: multigene family 110 is not essential for infectivity or virulence in pigs. Virology 176:195–204 [View Article][PubMed]
    [Google Scholar]
  4. Bastos A. D., Penrith M. L., Crucière C., Edrich J. L., Hutchings G., Roger F., Couacy-Hymann E., R Thomson G. 2003; Genotyping field strains of African swine fever virus by partial p72 gene characterisation. Arch Virol 148:693–706 [View Article][PubMed]
    [Google Scholar]
  5. Blasco R., de la Vega I., Almazán F., Agüero M., Viñuela E. 1989; Genetic variation of African swine fever virus: variable regions near the ends of the viral DNA. Virology 173:251–257 [View Article][PubMed]
    [Google Scholar]
  6. Blome S., Gabriel C., Beer M. 2013; Pathogenesis of African swine fever in domestic pigs and European wild boar. Virus Res 173:122–130 [View Article][PubMed]
    [Google Scholar]
  7. Boinas F. S., Hutchings G. H., Dixon L. K., Wilkinson P. J. 2004; Characterization of pathogenic and non-pathogenic African swine fever virus isolates from Ornithodoros erraticus inhabiting pig premises in Portugal. J Gen Virol 85:2177–2187 [View Article][PubMed]
    [Google Scholar]
  8. Borca M. V., Kutish G. F., Afonso C. L., Irusta P., Carrillo C., Brun A., Sussman M., Rock D. L. 1994; An African swine fever virus gene with similarity to the T-lymphocyte surface antigen CD2 mediates hemadsorption. Virology 199:463–468 [View Article][PubMed]
    [Google Scholar]
  9. Borca M. V., Carrillo C., Zsak L., Laegreid W. W., Kutish G. F., Neilan J. G., Burrage T. G., Rock D. L. 1998; Deletion of a CD2-like gene, 8-DR, from African swine fever virus affects viral infection in domestic swine. J Virol 72:2881–2889[PubMed]
    [Google Scholar]
  10. Bulimo W. D., Miskin J. E., Dixon L. K. 2000; An ARID family protein binds to the African swine fever virus encoded ubiquitin conjugating enzyme, UBCv1. FEBS Lett 471:17–22 [View Article][PubMed]
    [Google Scholar]
  11. Burrage T. G. 2013; African swine fever virus infection in Ornithodoros ticks. Virus Res 173:131–139 [View Article][PubMed]
    [Google Scholar]
  12. Burrage T. G., Lu Z., Neilan J. G., Rock D. L., Zsak L. 2004; African swine fever virus multigene family 360 genes affect virus replication and generalization of infection in Ornithodoros porcinus ticks. J Virol 78:2445–2453 [View Article][PubMed]
    [Google Scholar]
  13. Chapman D. A., Tcherepanov V., Upton C., Dixon L. K. 2008; Comparison of the genome sequences of non-pathogenic and pathogenic African swine fever virus isolates. J Gen Virol 89:397–408 [View Article][PubMed]
    [Google Scholar]
  14. Chapman D. A., Darby A. C., Da Silva M., Upton C., Radford A. D., Dixon L. K. 2011; Genomic analysis of highly virulent Georgia 2007/1 isolate of African swine fever virus. Emerg Infect Dis 17:599–605 [View Article][PubMed]
    [Google Scholar]
  15. Cobbold C., Windsor M., Wileman T. 2001; A virally encoded chaperone specialized for folding of the major capsid protein of African swine fever virus. J Virol 75:7221–7229 [View Article][PubMed]
    [Google Scholar]
  16. Colson P., De Lamballerie X., Yutin N., Asgari S., Bigot Y., Bideshi D. K., Cheng X. W., Federici B. A., Van Etten J. L.other authors 2013; Megavirales”, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch Virol 158:2517–2521 [View Article][PubMed]
    [Google Scholar]
  17. Correia S., Ventura S., Parkhouse R. M. 2013; Identification and utility of innate immune system evasion mechanisms of ASFV. Virus Res 173:87–100 [View Article][PubMed]
    [Google Scholar]
  18. Costard S., Jones B. A., Martínez-López B., Mur L., de la Torre A., Martínez M., Sánchez-Vizcaíno F., Sánchez-Vizcaíno J. M., Pfeiffer D. U., Wieland B. 2013a; Introduction of African swine fever into the European Union through illegal importation of pork and pork products. PLoS ONE 8:e61104 [View Article][PubMed]
    [Google Scholar]
  19. Costard S., Mur L., Lubroth J., Sanchez-Vizcaino J. M., Pfeiffer D. U. 2013b; Epidemiology of African swine fever virus. Virus Res 173:191–197 [View Article][PubMed]
    [Google Scholar]
  20. Darriba D., Taboada G. L., Doallo R., Posada D. 2011; ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165 [View Article][PubMed]
    [Google Scholar]
  21. Darriba D., Taboada G. L., Doallo R., Posada D. 2012; jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772 [View Article][PubMed]
    [Google Scholar]
  22. de Villiers E. P., Gallardo C., Arias M., da Silva M., Upton C., Martin R., Bishop R. P. 2010; Phylogenomic analysis of 11 complete African swine fever virus genome sequences. Virology 400:128–136 [View Article][PubMed]
    [Google Scholar]
  23. Dixon L. K., Twigg S. R., Baylis S. A., Vydelingum S., Bristow C., Hammond J. M., Smith G. L. 1994; Nucleotide sequence of a 55 kbp region from the right end of the genome of a pathogenic African swine fever virus isolate (Malawi LIL20/1). J Gen Virol 75:1655–1684 [View Article][PubMed]
    [Google Scholar]
  24. 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. 2004; African swine fever virus proteins involved in evading host defence systems. Vet Immunol Immunopathol 100:117–134 [View Article][PubMed]
    [Google Scholar]
  25. Dixon L. K., Escribano J. M., Martins C., Rock D. L., Salas M. L., Wilkinson P. J. 2005; Asfarviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses pp. 135–143 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Elsevier/Academic Press;
    [Google Scholar]
  26. Dixon L. K., Chapman D. A., Netherton C. L., Upton C. 2013; African swine fever virus replication and genomics. Virus Res 173:3–14 [View Article][PubMed]
    [Google Scholar]
  27. Epifano C., Krijnse-Locker J., Salas M. L., Rodríguez J. M., Salas J. 2006; The African swine fever virus nonstructural protein pB602L is required for formation of the icosahedral capsid of the virus particle. J Virol 80:12260–12270 [View Article][PubMed]
    [Google Scholar]
  28. Galindo I., Almazán F., Bustos M. J., Viñuela E., Carrascosa A. L. 2000; African swine fever virus EP153R open reading frame encodes a glycoprotein involved in the hemadsorption of infected cells. Virology 266:340–351 [View Article][PubMed]
    [Google Scholar]
  29. Gallardo C., Mwaengo D. M., Macharia J. M., Arias M., Taracha E. A., Soler A., Okoth E., Martín E., Kasiti J., Bishop R. P. 2009; Enhanced discrimination of African swine fever virus isolates through nucleotide sequencing of the p54, p72, and pB602L (CVR) genes. Virus Genes 38:85–95 [View Article][PubMed]
    [Google Scholar]
  30. Gil S., Sepúlveda N., Albina E., Leitão A., Martins C. 2008; The low-virulent African swine fever virus (ASFV/NH/P68) induces enhanced expression and production of relevant regulatory cytokines (IFNalpha, TNFalpha and IL12p40) on porcine macrophages in comparison to the highly virulent ASFV/L60. Arch Virol 153:1845–1854 [View Article][PubMed]
    [Google Scholar]
  31. Gogin A., Gerasimov V., Malogolovkin A., Kolbasov D. 2013; African swine fever in the North Caucasus region and the Russian Federation in years 2007-2012. Virus Res 173:198–203 [View Article][PubMed]
    [Google Scholar]
  32. Gómez-Puertas P., Rodríguez F., Oviedo J. M., Brun A., Alonso C., Escribano J. M. 1998; The African swine fever virus proteins p54 and p30 are involved in two distinct steps of virus attachment and both contribute to the antibody-mediated protective immune response. Virology 243:461–471 [View Article][PubMed]
    [Google Scholar]
  33. Gonzague M., Roger F., Bastos A., Burger C., Randriamparany T., Smondack S., Cruciere C. 2001; Isolation of a non-haemadsorbing, non-cytopathic strain of African swine fever virus in Madagascar. Epidemiol Infect 126:453–459 [View Article][PubMed]
    [Google Scholar]
  34. González A., Talavera A., Almendral J. M., Viñuela E. 1986; Hairpin loop structure of African swine fever virus DNA. Nucleic Acids Res 14:6835–6844 [View Article][PubMed]
    [Google Scholar]
  35. Goujon M., McWilliam H., Li W., Valentin F., Squizzato S., Paern J., Lopez R. 2010; A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:Web Server issueW695–W699 [View Article][PubMed]
    [Google Scholar]
  36. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321 [View Article][PubMed]
    [Google Scholar]
  37. Hakim M., Fass D. 2009; Dimer interface migration in a viral sulfhydryl oxidase. J Mol Biol 391:758–768 [View Article][PubMed]
    [Google Scholar]
  38. Haresnape J. M., Wilkinson P. J. 1989; A study of African swine fever virus infected ticks (Ornithodoros moubata) collected from three villages in the ASF enzootic area of Malawi following an outbreak of the disease in domestic pigs. Epidemiol Infect 102:507–522 [View Article][PubMed]
    [Google Scholar]
  39. Hillary W., Lin S. H., Upton C. 2011; Base-By-Base version 2: single nucleotide-level analysis of whole viral genome alignments. Microb Inform Exp 1:2 [View Article][PubMed]
    [Google Scholar]
  40. Hingamp P. M., Arnold J. E., Mayer R. J., Dixon L. K. 1992; A ubiquitin conjugating enzyme encoded by African swine fever virus. EMBO J 11:361–366[PubMed]
    [Google Scholar]
  41. Hingamp P. M., Leyland M. L., Webb J., Twigger S., Mayer R. J., Dixon L. K. 1995; Characterization of a ubiquitinated protein which is externally located in African swine fever virions. J Virol 69:1785–1793[PubMed]
    [Google Scholar]
  42. Hurtado C., Granja A. G., Bustos M. J., Nogal M. L., González de Buitrago G., de Yébenes V. G., Salas M. L., Revilla Y., Carrascosa A. L. 2004; The C-type lectin homologue gene (EP153R) of African swine fever virus inhibits apoptosis both in virus infection and in heterologous expression. Virology 326:160–170 [View Article][PubMed]
    [Google Scholar]
  43. Hurtado C., Bustos M. J., Granja A. G., de León P., Sabina P., López-Viñas E., Gómez-Puertas P., Revilla Y., Carrascosa A. L. 2011; The African swine fever virus lectin EP153R modulates the surface membrane expression of MHC class I antigens. Arch Virol 156:219–234 [View Article][PubMed]
    [Google Scholar]
  44. Iyer L. M., Balaji S., Koonin E. V., Aravind L. 2006; Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117:156–184 [View Article][PubMed]
    [Google Scholar]
  45. Jori F., Vial L., Penrith M. L., Pérez-Sánchez R., Etter E., Albina E., Michaud V., Roger F. 2013; Review of the sylvatic cycle of African swine fever in sub-Saharan Africa and the Indian ocean. Virus Res 173:212–227 [View Article][PubMed]
    [Google Scholar]
  46. Keil G. M., Giesow K., Portugal R. 2014; A novel bromodeoxyuridine-resistant wild boar lung cell line facilitates generation of African swine fever virus recombinants. Arch Virol 159:2421–2428 [View Article][PubMed]
    [Google Scholar]
  47. Kollnberger S. D., Gutierrez-Castañeda B., Foster-Cuevas M., Corteyn A., Parkhouse R. M. 2002; Identification of the principal serological immunodeterminants of African swine fever virus by screening a virus cDNA library with antibody. J Gen Virol 83:1331–1342[PubMed]
    [Google Scholar]
  48. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A.other authors 2007; clustal w and clustal_x version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  49. Leitão A., Cartaxeiro C., Coelho R., Cruz B., Parkhouse R. M., Portugal F., Vigário J. D., Martins C. L. 2001; 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 82:513–523[PubMed]
    [Google Scholar]
  50. Lewis T., Zsak L., Burrage T. G., Lu Z., Kutish G. F., Neilan J. G., Rock D. L. 2000; An African swine fever virus ERV1-ALR homologue, 9GL, affects virion maturation and viral growth in macrophages and viral virulence in swine. J Virol 74:1275–1285 [View Article][PubMed]
    [Google Scholar]
  51. Manso Ribeiro J. J., Azevedo J. A. 1961; La peste porcine Africaine au Portugal. Bull Off Int Epizoot 55:88–108
    [Google Scholar]
  52. Manso Ribeiro J., Nunes Petisca J. L., Lopes Frazao F., Sobral M. 1963; Vaccination contre la Peste Porcine Africaine. Bull Off Int Epizoot 60:921–937
    [Google Scholar]
  53. Montgomery R. E. 1921; On a form of swine fever occurring in British East Africa (Kenya colony). J Comp Pathol 34:159–191 [View Article]
    [Google Scholar]
  54. Neilan J. G., Borca M. V., Lu Z., Kutish G. F., Kleiboeker S. B., Carrillo C., Zsak L., Rock D. L. 1999; 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 80:2693–2697[PubMed]
    [Google Scholar]
  55. Neilan J. G., Zsak L., Lu Z., Kutish G. F., Afonso C. L., Rock D. L. 2002; Novel swine virulence determinant in the left variable region of the African swine fever virus genome. J Virol 76:3095–3104 [View Article][PubMed]
    [Google Scholar]
  56. [Google Scholar]
  57. Pan I. C. 1992; African swine fever virus: generation of subpopulations with altered immunogenicity and virulence following passage in cell cultures. J Vet Med Sci 54:43–52 [View Article][PubMed]
    [Google Scholar]
  58. Pan I. C., Hess W. R. 1984; Virulence in African swine fever: its measurement and implications. Am J Vet Res 45:361–366[PubMed]
    [Google Scholar]
  59. Portugal R., Leitão A., Martins C. 2009; Characterization of African swine fever virus IAP homologue expression in porcine macrophages infected with different virulence isolates. Vet Microbiol 139:140–146 [View Article][PubMed]
    [Google Scholar]
  60. Prados F. J., Viñuela E., Alcamí A. 1993; Sequence and characterization of the major early phosphoprotein p32 of African swine fever virus. J Virol 67:2475–2485[PubMed]
    [Google Scholar]
  61. Rahimi P., Sohrabi A., Ashrafihelan J., Edalat R., Alamdari M., Masoudi M., Mostofi S., Azadmanesh K. 2010; Emergence of African swine fever virus, northwestern Iran. Emerg Infect Dis 16:1946–1948 [View Article][PubMed]
    [Google Scholar]
  62. Reis A. L., Parkhouse R. M., Penedos A. R., Martins C., Leitão A. 2007; Systematic analysis of longitudinal serological responses of pigs infected experimentally with African swine fever virus. J Gen Virol 88:2426–2434 [View Article][PubMed]
    [Google Scholar]
  63. Rodríguez I., Redrejo-Rodríguez M., Rodríguez J. M., Alejo A., Salas J., Salas M. L. 2006; African swine fever virus pB119L protein is a flavin adenine dinucleotide-linked sulfhydryl oxidase. J Virol 80:3157–3166 [View Article][PubMed]
    [Google Scholar]
  64. Rodriguez J. M., Salas M. L., Viñuela E. 1992; Genes homologous to ubiquitin-conjugating proteins and eukaryotic transcription factor SII in African swine fever virus. Virology 186:40–52 [View Article][PubMed]
    [Google Scholar]
  65. Rodríguez J. M., Yáñez R. J., Almazán F., Viñuela E., Rodriguez J. F. 1993; African swine fever virus encodes a CD2 homolog responsible for the adhesion of erythrocytes to infected cells. J Virol 67:5312–5320[PubMed]
    [Google Scholar]
  66. Rowlands R. J., Michaud V., Heath L., Hutchings G., Oura C., Vosloo W., Dwarka R., Onashvili T., Albina E., Dixon L. K. 2008; African swine fever virus isolate, Georgia, 2007. Emerg Infect Dis 14:1870–1874 [View Article][PubMed]
    [Google Scholar]
  67. Rowlands R. J., Duarte M. M., Boinas F., Hutchings G., Dixon L. K. 2009; The CD2v protein enhances African swine fever virus replication in the tick vector, Ornithodoros erraticus. Virology 393:319–328 [View Article][PubMed]
    [Google Scholar]
  68. Sánchez-Vizcaíno J. M., Mur L., Martínez-López B. 2012; African Swine Fever: an epidemiological update. Transbound Emerg Dis 59:27–35 [View Article][PubMed]
    [Google Scholar]
  69. Schmitt J., Keil G. M. 1996; Identification and characterization of the bovine herpesvirus 1 UL7 gene and gene product which are not essential for virus replication in cell culture. J Virol 70:1091–1099[PubMed]
    [Google Scholar]
  70. Sievers F., Wilm A., Dineen D., Gibson T. J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M.other authors 2011; Fast, scalable generation of high-quality protein multiple sequence alignments using clustal Omega. Mol Syst Biol 7:539 [View Article][PubMed]
    [Google Scholar]
  71. Takamatsu H. H., Denyer M. S., Lacasta A., Stirling C. M., Argilaguet J. M., Netherton C. L., Oura C. A., Martins C., Rodríguez F. 2013; Cellular immunity in ASFV responses. Virus Res 173:110–121 [View Article][PubMed]
    [Google Scholar]
  72. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  73. Tcherepanov V., Ehlers A., Upton C. 2006; Genome Annotation Transfer Utility (GATU): rapid annotation of viral genomes using a closely related reference genome. BMC Genomics 7:150 [View Article][PubMed]
    [Google Scholar]
  74. Upton C., Hogg D., Perrin D., Boone M., Harris N. L. 2000; Viral genome organizer: a system for analyzing complete viral genomes. Virus Res 70:55–64 [View Article][PubMed]
    [Google Scholar]
  75. Vigário J. D., Terrinha A. M., Moura Nunes J. F. 1974; Antigenic relationships among strains of African swine fecre virus. Arch Gesamte Virusforsch 45:272–277 [View Article][PubMed]
    [Google Scholar]
  76. Waterhouse A. M., Procter J. B., Martin D. M., Clamp M., Barton G. J. 2009; Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191 [View Article][PubMed]
    [Google Scholar]
  77. Yáñez R. J., Rodríguez J. M., Nogal M. L., Yuste L., Enríquez C., Rodriguez J. F., Viñuela E. 1995; Analysis of the complete nucleotide sequence of African swine fever virus. Virology 208:249–278 [View Article][PubMed]
    [Google Scholar]
  78. Zsak L., Lu Z., Burrage T. G., Neilan J. G., Kutish G. F., Moore D. M., Rock D. L. 2001; African swine fever virus multigene family 360 and 530 genes are novel macrophage host range determinants. J Virol 75:3066–3076 [View Article][PubMed]
    [Google Scholar]
  79. Zsak L., Borca M. V., Risatti G. R., Zsak A., French R. A., Lu Z., Kutish G. F., Neilan J. G., Callahan J. D.other authors 2005; Preclinical diagnosis of African swine fever in contact-exposed swine by a real-time PCR assay. J Clin Microbiol 43:112–119 [View Article][PubMed]
    [Google Scholar]
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