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Role of conserved cysteine residues in the CAIC motif of the SU glycoprotein in the maturation and fusion activity of bovine leukaemia virus

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Abstract

The surface (SU) and transmembrane (TM) glycoproteins of many retroviruses are linked by disulphide bonds, and the interaction of SU with a cellular receptor results in disulphide bond isomerisation triggered by the CXXC motif in SU. This reaction leads to the fusion of viral and host cell membranes. In this work, we show that the cysteine at amino acid position 212 in the CAIC motif of the SU glycoprotein of bovine leukaemia virus has a free thiol group. A C-to-A mutation at position 212, either individually or in combination with a C-to-A mutation at position 215, was found to inhibit the maturation process, suggesting its involvement in the formation of the covalent bond with TM.

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References

  1. Burny A, Cleuter Y, Kettmann R, Mammerickx M, Marbaix G, Portetelle D et al (1988) Bovine leukaemia: facts and hypotheses derived from the study of an infectious cancer. Vet Microbiol 17(3):197–218

    Article  CAS  PubMed  Google Scholar 

  2. Wolfe ND, Heneine W, Carr JK, Garcia AD, Tamoufe U, Torimiro JN et al (2005) Emergence of among central unique African primate viruses bushmeat hunters. PNAS 102(22):7994–7999

    Article  CAS  PubMed  Google Scholar 

  3. Barez PY, de Brogniez A, Carpentier A, Gazon H, Gillet N, Gutiérrez G et al (2015) Recent advances in BLV research. Viruses 7(11):6080–6088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ghysdael J, Kettmann R, Burny A (1978) Translation of bovine leukemia virus genome information in heterologous protein synthesizing system programmed with virion RNA and in cell-lines persistently infected by BLV. Ann Rech Vet 9:627–634

    CAS  PubMed  Google Scholar 

  5. Mamoun RZ, Astier T, Guillemain B, Duplan JF (1983) Bovine lymphosarcoma: processing of bovine leukaemia virus-coded proteins. J Gen Virol 64(12):2791–2795

    Article  CAS  PubMed  Google Scholar 

  6. Bruck C, Portetelle D, Burny A, Zavada J (1982) Topographical analysis by monoclonal antibodies of BLV-gp51 epitopes involved in viral functions. Virology 122(2):353–362

    Article  CAS  PubMed  Google Scholar 

  7. Rizzo G, Forti K, Serroni A, Cagiola M, Baglivo S, Scoccia E et al (2016) Single N-glycosylation site of bovine leukemia virus SU is involved in conformation and viral escape. Vet Microbiol 197:21–26. https://doi.org/10.1016/j.vetmic.2016.10.024

    Article  CAS  PubMed  Google Scholar 

  8. Pinter A, Kopelman R, Li Z, Kayman SC, Sanders DA (1997) Localization of the labile disulfide bond between SU and TM of the murine leukemia virus envelope protein complex to a highly conserved CWLC motif in SU that resembles the active-site sequence of thiol-disulfide exchange enzymes. J Virol 71(10):8073–8077

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Wallin M, Ekström M, Garoff H (2004) Isomerization of the intersubunit disulphide-bond in Env controls retrovirus fusion. EMBO J 23(1):54–65

    Article  CAS  PubMed  Google Scholar 

  10. Johnston ER, Radke K (2000) The SU and TM envelope protein subunits of bovine leukemia virus are linked by disulfide bonds, both in cells and in virions. J Virol 74(6):2930–2935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Forti K, Rizzo G, Cagiola M, Ferrante G, Marini C, Feliziani F et al (2014) Identification of a novel overlapping sequential E epitope (E′) on the bovine leukaemia virus SU glycoprotein and analysis of immunological data. Vet Microbiol 172(1–2):157–167

    Article  CAS  PubMed  Google Scholar 

  12. Sagata N, Yasunaga T, Tsuzuku-Kawamura J, Ohishi K, Ogawa Y, Ikawa Y (1985) Complete nucleotide sequence of the genome of bovine leukaemia virus: its evolutionary relationship to other retroviruses. Proc Natl Acad Sci 82:677–681

    Article  CAS  PubMed  Google Scholar 

  13. Greig AS, Chander S, Samagh B, Bouillant AM (1978) A simple, rapid syncytial-inhibition test for antibodies to bovine leukemia virus. Can J Comp Med 42(4):446–451

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Gatot J-S, Callebaut I, Van Lint C, Demonte D, Kerkhofs P, Portetelle D et al (2002) Bovine leukemia virus SU protein interacts with zinc, and mutations within two interacting regions differently affect viral fusion and infectivity in vivo. J Virol 76(16):7956–7967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wallin M, Loving R, Ekstrom M, Li K, Garoff H (2005) Kinetic analyses of the surface-transmembrane disulfide bond isomerization-controlled fusion activation pathway in moloney murine leukemia virus. J Virol 79(22):13856–13864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wallin M, Ekström M, Garoff H (2005) The fusion-controlling disulfide bond isomerase in retrovirus Env is triggered by protein destabilization. J Virol 79(3):1678–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Liu ZI, Blaschek HP, Lid ZL, Blaschek HP (1996) Monoclonal antibody-based ELISA for detection of clostridium perfringens alpha-toxin. J Food Prot 59(6):621–625

    Article  CAS  PubMed  Google Scholar 

  18. Gu J, Pathasarathi S, Varela-Echavarría A, Ron Y, Dougherty JP (1995) Mutation of conserved cysteine residues in the CWLC motif of the oncoretrovirus SU protein affect maturation and traslocation. Virology 206:885–893

    Article  CAS  PubMed  Google Scholar 

  19. Li K, Zhang S, Kronqvist M, Wallin M, Ekstrom M, Derse D et al (2008) Intersubunit disulfide isomerization controls membrane fusion of human T-cell leukemia virus Env. J Virol 82(14):7135–7143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Johnston ER (1999) PhD thesis. University of California, Davis

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This research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.

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Correspondence to Katia Forti.

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Serroni, A., Forti, K. & De Giuseppe, A. Role of conserved cysteine residues in the CAIC motif of the SU glycoprotein in the maturation and fusion activity of bovine leukaemia virus. Arch Virol 164, 2309–2314 (2019). https://doi.org/10.1007/s00705-019-04294-x

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  • DOI: https://doi.org/10.1007/s00705-019-04294-x

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