Insights into African swine fever virus immunoevasion strategies

doi:10.1016/S2095-3119(19)62762-0

摘要/Abstract

Abstract:

African swine fever (ASF) is an acute and highly contagious disease that causes severe economic losses to the swine industry. ASF is caused by infection of African swine fever virus (ASFV) in domestic pigs, leading to almost 100% mortality. However, no effective vaccines and pharmacologic treatment against ASF are available. ASF poses a severe threat to the swine industry and the economy. Here we summarize potential virus-host cell interaction mechanisms involving the suppression of innate and adaptive immune responses to ASFV entry and infection. These mechanisms include modulation of apoptosis, inhibition of inflammatory responses, reduction of IFN production, inhibition of autophagy, and suppression of MHC-I expression. Insights into immunoevasion strategies by ASFV may shed light on the development of vaccines, as well as preventive and therapeutic drugs.

Key words: African swine fever virus , immunoevasion , apoptosis

. [J]. Journal of Integrative Agriculture, 2020, 19(1): 11-22.

WANG Jun, SHI xin-jin, SUN Hai-wei, CHEN Hong-jun. Insights into African swine fever virus immunoevasion strategies[J]. Journal of Integrative Agriculture, 2020, 19(1): 11-22.

参考文献

Abrams C C, Goatley L, Fishbourne E, Chapman D, Cooke L, Oura C A, Netherton C L, Takamatsu H H, Dixon L K. 2013. Deletion of virulence associated genes from attenuated African swine fever virus isolate OUR T88/3 decreases its ability to protect against challenge with virulent virus. Virology, 443, 99–105.
Afonso C L, Neilan J G, Kutish G F, Rock D L. 1996. An African swine fever virus Bc1-2 homolog, 5-HL, suppresses apoptotic cell death. Journal of Virology, 70, 4858–4863.
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, Zsak L, Rock D L. 2004. African swine fever virus multigene family 360 and 530 genes affect host interferon response. Journal of Virology, 78, 1858–1864.
Afonso C L, Zsak L, Carrillo C, Borca M V, Rock D L. 1998. African swine fever virus NL gene is not required for virus virulence. Journal of General Virology, 79, 2543–2547.
Alcami A, Smith G L. 1992. A soluble receptor for interleukin-1 beta encoded by vaccinia virus: A novel mechanism of virus modulation of the host response to infection. Cell, 71, 153–167.
Alonso C, Miskin J, Hernaez B, Fernandez-Zapatero P, Soto L, Canto C, Rodriguez-Crespo I, Dixon L, Escribano J M. 2001. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. Journal of Virology, 75, 9819–9827.
Anderson E C, Hutchings G H, Mukarati N, Wilkinson P J. 1998. African swine fever virus infection of the bushpig (Potamochoerus porcus) and its significance in the epidemiology of the disease. Veterinary Microbiology, 62, 1–15.
Banjara S, Caria S, Dixon L K, Hinds M G, Kvansakul M. 2017. Structural insight into African swine fever virus A179L-mediated inhibition of apoptosis. Journal of Virology, 91, e02228-e02244.
Barber C, Netherton C, Goatley L, Moon A, Goodbourn S, Dixon L. 2017. Identification of residues within the African swine fever virus DP71L protein required for dephosphorylation of translation initiation factor eIF2α and inhibiting activation of pro-apoptotic CHOP. Virology, 504, 107–113.
Barber G N, Wambach M, Wong M L, Dever T E, Hinnebusch A G, Katze M G. 1993. Translational regulation by the interferon-induced double-stranded-RNA-activated 68-kDa protein kinase. Proceeding of the National Academy Sciences of the United States of America, 90, 4621–4625.
Basta S, Gerber H, Schaub A, Summerfield A, McCullough K C. 2010. Cellular processes essential for African swine fever virus to infect and replicate in primary macrophages. Veterinary Microbiology, 140, 9–17.
Berlanga J J, Santoyo J, De Haro C. 1999. Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2α kinase. European Journal of Biochemistry, 265, 754–762.
Borca M V, O’Donnell V, Holinka L G, Ramirez-Medina E, Clark B A, Vuono E A, Berggren K, Alfano M, Carey L B, Richt J A, Risatti G R, Gladue D P. 2018. The L83L ORF of African swine fever virus strain Georgia encodes for a non-essential gene that interacts with the host protein IL-1β. Virus Research, 249, 116–123.
Borden K L, Boddy M N, Lally J, O’Reilly N J, Martin S, Howe K, Solomon E, Freemont P S. 1995. The solution structure of the RING finger domain from the acute promyelocytic leukaemia proto-oncoprotein PML. The EMBO Journal, 14, 1532–1541.
Bowie A, Kiss-Toth E, Symons J A, Smith G L, Dower S K, O’Neill L A. 2000. A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proceeding of the National Academy Sciences of the United States of America, 97, 10162–10167.
Boyington J C, Riaz A N, Patamawenu A, Coligan J E, Brooks A G, Sun P D. 1999. Structure of CD94 reveals a novel C-type lectin fold: Implications for the NK cell-associated CD94/NKG2 receptors. Immunity, 10, 75–82.
Brun A, Rivas C, Esteban M, Escribano J M, Alonso C. 1996. African swine fever virus gene A179L, a viral homologue of bcl-2, protects cells from programmed cell death. Virology, 225, 227–230.
Brun A, Rodriguez F, Escribano J M, Alonso C. 1998. Functionality and cell anchorage dependence of the African swine fever virus gene A179L, a viral bcl-2 homolog, in insect cells. Journal of Virology, 72, 10227–10233.
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. Journal of Virology, 78, 2445–2453.
Carrascosa A L, Bustos M J, Nogal M L, Gonzalez de Buitrago G, Revilla Y. 2002. Apoptosis induced in an early step of African swine fever virus entry into Vero cells does not require virus replication. Virology, 294, 372–382.
Chacon M R, Almazan F, Nogal M L, Vinuela E, Rodriguez J F. 1995. The African swine fever virus IAP homolog is a late structural polypeptide. Virology, 214, 670–674.
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. Journal of General Virology, 89, 397–408.
Chaumorcel M, Lussignol M, Mouna L, Cavignac Y, Fahie K, Cotte-Laffitte J, Geballe A, Brune W, Beau I, Codogno P, Esclatine A. 2012. The human cytomegalovirus protein TRS1 inhibits autophagy via its interaction with Beclin 1. Journal of Virology, 86, 2571–2584.
Correia S, Ventura S, Parkhouse R M. 2013. Identification and utility of innate immune system evasion mechanisms of ASFV. Virus Research, 173, 87–100.
Dixon L K, Sanchez-Cordon P J, Galindo I, Alonso C. 2017. Investigations of pro- and anti-apoptotic factors affecting African swine fever virus replication and pathogenesis. Viruses, 9, 241–256.
Dixon L K, Sun H, Roberts H. 2019. African swine fever. Antiviral Research, 165, 34–41.
Eustace Montgomery R. 1921. On a form of swine fever occurring in british East Africa (Kenya Colony). Journal of Comparative Pathology and Therapeutics, 34, 159–191.
Galindo I, Cuesta-Geijo M A, Hlavova K, Munoz-Moreno R, Barrado-Gil L, Dominguez J, Alonso C. 2015. African swine fever virus infects macrophages, the natural host cells, via clathrin- and cholesterol-dependent endocytosis. Virus Research, 200, 45–55.
Galindo I, Hernaez B, Diaz-Gil G, Escribano J M, Alonso C. 2008. A179L, a viral Bcl-2 homologue, targets the core Bcl-2 apoptotic machinery and its upstream BH3 activators with selective binding restrictions for Bid and Noxa. Virology, 375, 561–572.
Galindo I, Hernaez B, Munoz-Moreno R, Cuesta-Geijo M A, Dalmau-Mena I, Alonso C. 2012. The ATF6 branch of unfolded protein response and apoptosis are activated to promote African swine fever virus infection. Cell Death & Disease, 3, e341.
Gallardo C, Sanchez E G, Perez-Nunez D, Nogal M, de Leon P, Carrascosa A L, Nieto R, Soler A, Arias M L, Revilla Y. 2018. African swine fever virus (ASFV) protection mediated by NH/P68 and NH/P68 recombinant live-attenuated viruses. Vaccine, 36, 2694–2704.
Granja A G, Nogal M L, Hurtado C, Del Aguila C, Carrascosa A L, Salas M L, Fresno M, Revilla Y. 2006. The viral protein A238L inhibits TNF-α expression through a CBP/p300 transcriptional coactivators pathway. Journal of Immunology, 176, 451–462.
Granja A G, Perkins N D, Revilla Y. 2015. Correction: A238L inhibits NF-ATc2, NF-kappaB, and c-Jun activation through a novel mechanism involving protein kinase C-theta-mediated up-regulation of the amino-terminal transactivation domain of p300. Journal of Immunology, 194, 20-32.
Han A P, Yu C, Lu L, Fujiwara Y, Browne C, Chin G, Fleming M, Leboulch P, Orkin S H, Chen J J. 2001. Heme-regulated eIF2α kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. The EMBO Journal, 20, 6909–6918.
Harding H P, Zhang Y, Ron D. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature, 397, 271–274.
He B, Gross M, Roizman B. 1997. The γ134.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1α to dephosphorylate the α subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proceeding of the National Academy Sciences of the United States of America, 94, 843–848.
Hernaez B, Alonso C. 2010. Dynamin- and clathrin-dependent endocytosis in African swine fever virus entry. Journal of Virology, 84, 2100–2109.
Hernaez B, Cabezas M, Munoz-Moreno R, Galindo I, Cuesta-Geijo M A, Alonso C. 2013. A179L, a new viral Bcl2 homolog targeting Beclin 1 autophagy related protein. Current Molecular Medicine, 13, 305–316.
Hernaez B, Diaz-Gil G, Garcia-Gallo M, Ignacio Quetglas J, Rodriguez-Crespo I, Dixon L, Escribano J M, Alonso C. 2004. The African swine fever virus dynein-binding protein p54 induces infected cell apoptosis. FEBS Letters, 569, 224–228.
Hernaez B, Escribano J M, Alonso C. 2006. Visualization of the African swine fever virus infection in living cells by incorporation into the virus particle of green fluorescent protein-p54 membrane protein chimera. Virology, 350, 1–14.
Hozak R R, Manji G A, Friesen P D. 2000. The BIR motifs mediate dominant interference and oligomerization of inhibitor of apoptosis Op-IAP. Molecular and Cellular Biology, 20, 1877–1885.
Hurtado C, Bustos M J, Granja A G, de Leon P, Sabina P, Lopez-Vinas E, Gomez-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. Archives of Virology, 156, 219–234.
Hurtado C, Granja A G, Bustos M J, Nogal M L, Gonzalez de Buitrago G, de Yebenes 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.
Jousse C, Oyadomari S, Novoa I, Lu P, Zhang Y, Harding H P, Ron D. 2003. Inhibition of a constitutive translation initiation factor 2α phosphatase, CReP, promotes survival of stressed cells. The Journal of Cell Biology, 163, 767–775.
Ku B, Woo J S, Liang C, Lee K H, Hong H S, E X, Kim K S, Jung J U, Oh B H. 2008. Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. Plos Pathogens, 4, e25.
Langland J O, Jacobs B L. 2002. The role of the PKR-inhibitory genes, E3L and K3L, in determining vaccinia virus host range. Virology, 299, 133–141.
Li L, Wang Q, Ge S, Liu Y, Liu C, Liu F, Hu Y, Li J, Bao J, Ren W, Zhang Y, Xu T, Sun C, Li L, Wang S, Fan X, Huang B, Wu X, Wang Z. 2018. Infection of African swine fever in wild boar, China, 2018. Transboundary and Emerging Diseases, 00, 1-4.
Lithgow P, Takamatsu H, Werling D, Dixon L, Chapman D. 2014. Correlation of cell surface marker expression with African swine fever virus infection. Veterinary Microbiology, 168, 413–419.
Llera A S, Viedma F, Sanchez-Madrid F, Tormo J. 2001. Crystal structure of the C-type lectin-like domain from the human hematopoietic cell receptor CD69. Journal of Biological Chemistry, 276, 7312–7319.
Marakasova E S, Eisenhaber B, Maurer-Stroh S, Eisenhaber F, Baranova A. 2017. Prenylation of viral proteins by enzymes of the host: Virus-driven rationale for therapy with statins and FT/GGT1 inhibitors. BioEssays, 39, 10–25.
Miskin J E, Abrams C C, Dixon L K. 2000. African swine fever virus protein A238L interacts with the cellular phosphatase calcineurin via a binding domain similar to that of NFAT. Journal of Virology, 74, 9412–9420.
de Moissac D, Zheng H, Kirshenbaum L A. 1999. Linkage of the BH4 domain of Bcl-2 and the nuclear factor kappaB signaling pathway for suppression of apoptosis. Journal of Biological Chemistry, 274, 29505–29509.
Monaco G, Decrock E, Akl H, Ponsaerts R, Vervliet T, Luyten T, De Maeyer M, Missiaen L, Distelhorst C W, De Smedt H, Parys J B, Leybaert L, Bultynck G. 2012. Selective regulation of IP3-receptor-mediated Ca2+ signaling and apoptosis by the BH4 domain of Bcl-2 versus Bcl-Xl. Cell Death and Differentiation, 19, 295–309.
Nogal M L, Gonzalez de Buitrago G, Rodriguez C, Cubelos B, Carrascosa A L, Salas M L, Revilla Y. 2001. African swine fever virus IAP homologue inhibits caspase activation and promotes cell survival in mammalian cells. Journal of Virology, 75, 2535–2543.
Novoa I, Zeng H, Harding H P, Ron D. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. The Journal of Cell Biology, 153, 1011–1022.
O’Donnell V, Holinka L G, Gladue D P, Sanford B, Krug P W, Lu X, Arzt J, Reese B, Carrillo C, Risatti G R, Borca M V. 2015. African swine fever virus georgia isolate harboring deletions of MGF360 and MGF505 genes is attenuated in swine and confers protection against challenge with virulent parental virus. Journal of Virology, 89, 6048–6056.
O’Donnell V, Holinka L G, Sanford B, Krug P W, Carlson J, Pacheco J M, Reese B, Risatti G R, Gladue D P, Borca M V. 2016. African swine fever virus Georgia isolate harboring deletions of 9GL and MGF360/505 genes is highly attenuated in swine but does not confer protection against parental virus challenge. Virus Research, 221, 8–14.
O’Donnell V, Risatti G R, Holinka L G, Krug P W, Carlson J, Velazquez-Salinas L, Azzinaro P A, Gladue D P, Borca M V. 2017. Simultaneous deletion of the 9GL and UK genes from the African swine fever virus Georgia 2007 isolate offers increased safety and protection against homologous challenge. Journal of Virology, 91, e01760–e01675.
de Oliveira V L, Almeida S C, Soares H R, Crespo A, Marshall-Clarke S, Parkhouse R M. 2011. A novel TLR3 inhibitor encoded by African swine fever virus (ASFV). Archives of Virology, 156, 597–609.
Orvedahl A, Alexander D, Talloczy Z, Sun Q, Wei Y, Zhang W, Burns D, Leib D A, Levine B. 2007. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe, 1, 23–35.
Pattingre S, Tassa A, Qu X, Garuti R, Liang X H, Mizushima N, Packer M, Schneider M D, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell, 122, 927–939.
Penrith M L, Vosloo W. 2009. Review of African swine fever: transmission, spread and control. Journal of South African Veterinary Association, 80, 58–62.
Piya S, White E J, Klein S R, Jiang H, McDonnell T J, Gomez-Manzano C, Fueyo J. 2011. The E1B19K oncoprotein complexes with Beclin 1 to regulate autophagy in adenovirus-infected cells. PLoS ONE, 6, e29467.
Popescu L, Gaudreault N N, Whitworth K M, Murgia M V, Nietfeld J C, Mileham A, Samuel M, Wells K D, Prather R S, Rowland R R R. 2017. Genetically edited pigs lacking CD163 show no resistance following infection with the African swine fever virus isolate, Georgia 2007/1. Virology, 501, 102–106.
Ray C A, Black R A, Kronheim S R, Greenstreet T A, Sleath P R, Salvesen G S, Pickup D J. 1992. Viral inhibition of inflammation: Cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell, 69, 597–604.
Reis A L, Abrams C C, Goatley L C, Netherton C, Chapman D G, Sanchez-Cordon P, Dixon L K. 2016. Deletion of African swine fever virus interferon inhibitors from the genome of a virulent isolate reduces virulence in domestic pigs and induces a protective response. Vaccine, 34, 4698–4705.
Revilla Y, Cebrian A, Baixeras E, Martinez C, Vinuela E, Salas M L. 1997. Inhibition of apoptosis by the African swine fever virus Bcl-2 homologue: Role of the BH1 domain. Virology, 228, 400–404.
Rivera J, Abrams C, Hernaez B, Alcazar A, Escribano J M, Dixon L, Alonso C. 2007. The MyD116 African swine fever virus homologue interacts with the catalytic subunit of protein phosphatase 1 and activates its phosphatase activity. Journal of Virology, 81, 2923–2929.
Rodriguez F, Alcaraz C, Eiras A, Yanez R J, Rodriguez J M, Alonso C, Rodriguez J F, Escribano J M. 1994. Characterization and molecular basis of heterogeneity of the African swine fever virus envelope protein p54. Journal of Virology, 68, 7244–7252.
Rodriguez F, Ley V, Gomez-Puertas P, Garcia R, Rodriguez J F, Escribano J M. 1996. The structural protein p54 is essential for African swine fever virus viability. Virus Research, 40, 161–167.
Rodriguez-Crespo I, Yelamos B, Roncal F, Albar J P, de Montellano P R O, Gavilanes F. 2001. Identification of novel cellular proteins that bind to the LC8 dynein light chain using a pepscan technique. FEBS Letters, 503, 135–141.
Sanchez E G, Perez-Nunez D, Revilla Y. 2017a. Mechanisms of entry and endosomal pathway of African swine fever virus. Vaccines (Basel), 5, 42–55.
Sanchez E G, Quintas A, Perez-Nunez D, Nogal M, Barroso S, Carrascosa A L, Revilla Y. 2012. African swine fever virus uses macropinocytosis to enter host cells. PLoS Pathogens, 8, e1002754.
Sanchez E G, Riera E, Nogal M, Gallardo C, Fernandez P, Bello-Morales R, Lopez-Guerrero J A, Chitko-McKown C G, Richt J A, Revilla Y. 2017b. Phenotyping and susceptibility of established porcine cells lines to African swine fever virus infection and viral production. Scientific Reports, 7, 10369.
Sanchez-Torres C, Gomez-Puertas P, Gomez-del-Moral M, Alonso F, Escribano J M, Ezquerra A, Dominguez J. 2003. Expression of porcine CD163 on monocytes/macrophages correlates with permissiveness to African swine fever infection. Archives of Virology, 148, 2307–2323.
Schneider W M, Chevillotte M D, Rice C M. 2014. Interferon-stimulated genes: A complex web of host defenses. Annual Review of Immunology, 32, 513–545.
Silk R N, Bowick G C, Abrams C C, Dixon L K. 2007. African swine fever virus A238L inhibitor of NF-kappaB and of calcineurin phosphatase is imported actively into the nucleus and exported by a CRM1-mediated pathway. Journal of General Virology, 88, 411–419.
Sinha S, Colbert C L, Becker N, Wei Y, Levine B. 2008. Molecular basis of the regulation of Beclin 1-dependent autophagy by the γ-herpesvirus 68 Bcl-2 homolog M11. Autophagy, 4, 989–997.
Strasser A. 2005. The role of BH3-only proteins in the immune system. Nature Reviews Immunology, 5, 189–200.
Szegezdi E, Logue S E, Gorman A M, Samali A. 2006. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Reports, 7, 880–885.
Tait S W, Reid E B, Greaves D R, Wileman T E, Powell P P. 2000. Mechanism of inactivation of NF-κB by a viral homologue of IκBα. Journal of Biological Chemistry, 275, 34656–34664.
Tan X, Sun L, Chen J, Chen Z J. 2018. Detection of microbial infections through innate immune sensing of nucleic acids. Annual Review of Microbiology, 72, 447–478.
Thomson G R, Gainaru M D, Van Dellen A F. 1980. Experimental infection of warthos (Phacochoerus aethiopicus) with African swine fever virus. The Onderstepoort Journal of Veterinary Research, 47, 19–22.
Tormo J, Natarajan K, Margulies D H, Mariuzza R A. 1999. Crystal structure of a lectin-like natural killer cell receptor bound to its MHC class I ligand. Nature, 402, 623–631.
Vallee I, Tait S W, Powell P P. 2001. African swine fever virus infection of porcine aortic endothelial cells leads to inhibition of inflammatory responses, activation of the thrombotic state, and apoptosis. Journal of Virology, 75, 10372–10382.
Wang X, Wu J, Wu Y, Chen H, Zhang S, Li J, Xin T, Jia H, Hou S, Jiang Y, Zhu H, Guo X. 2018. Inhibition of cGAS-STING-TBK1 signaling pathway by DP96R of ASFV China 2018/1. Biochemical and Biophysical Research Communications, 506, 437–443.
Wilcox D R, Longnecker R. 2016. The herpes simplex virus neurovirulence factor γ34.5: Revealing virus-host interactions. Plos Pathogens, 12, e1005449.
Wozniakowski G, Kozak E, Kowalczyk A, Lyjak M, Pomorska-Mol M, Niemczuk K, Pejsak Z. 2016. Current status of African swine fever virus in a population of wild boar in eastern Poland (2014–2015). Archives of Virology, 161, 189–195.
Yamamoto M, Sato S, Mori K, Hoshino K, Takeuchi O, Takeda K, Akira S. 2002. Cutting edge: A novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-β promoter in the Toll-like receptor signaling. Journal of Immunology, 169, 6668–6672.
Yanez R J, Rodriguez J M, Nogal M L, Yuste L, Enriquez C, Rodriguez J F, Vinuela E. 1995. Analysis of the complete nucleotide sequence of African swine fever virus. Virology, 208, 249–278.
Youle R J, Strasser A. 2008. The BCL-2 protein family: Opposing activities that mediate cell death. Nature Reviews. Molecular Cell Biology, 9, 47–59.
Zhang F, Moon A, Childs K, Goodbourn S, Dixon L K. 2010. The African swine fever virus DP71L protein recruits the protein phosphatase 1 catalytic subunit to dephosphorylate eIF2α and inhibits CHOP induction but is dispensable for these activities during virus infection. Journal of Virology, 84, 10681–10689.
Zhou X T, Li N, Luo Y Z, Liu Y, Miao F M, Chen T, Zhang S F, Cao P L, Li X D, Tian K G, Qiu H J, Hu R L. 2018. Emergence role of African swine fever in China, 2018. Transboundry and Emerging Diseases, 65, 1482–1484.
Zsak L, Caler E, Lu Z, Kutish G F, Neilan J G, Rock D L. 1998. A nonessential African swine fever virus gene UK is a significant virulence determinant in domestic swine. Journal of Virology, 72, 1028–1035.
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. Journal of Virology, 75, 3066–3076.