1887

Abstract

T-lymphotropic feline leukemia virus (FeLV-T), a highly pathogenic variant of FeLV, induces severe immunosuppression in cats. FeLV-T is fusion defective because in its PHQ motif, a gammaretroviral consensus motif in the N terminus of an envelope protein, histidine is replaced with aspartate. Infection by FeLV-T requires FeLIX, a truncated envelope protein encoded by an endogenous FeLV, for transactivation of infectivity and Pit1 for binding FeLIX. Although Pit1 is present in most tissues in cats, the expression of FeLIX is limited to certain cells in lymphoid organs. Therefore, the host cell range of FeLV-T was thought to be restricted to cells expressing FeLIX. However, because FeLIX is a soluble factor and is expressed constitutively in lymphoid organs, we presumed it to be present in blood and evaluated its activities in sera of various mammalian species using a pseudotype assay. We demonstrated that cat serum has FeLIX activity at a functional level, suggesting that FeLIX is present in the blood and that FeLV-T may be able to infect cells expressing Pit1 regardless of the expression of FeLIX . In addition, FeLIX activities in sera were detected only in domestic cats and not in other feline species tested. To our knowledge, this is the first report to prove that a large amount of truncated envelope protein of endogenous retrovirus is circulating in the blood to facilitate the infection of a pathogenic exogenous retrovirus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.071688-0
2015-03-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/3/681.html?itemId=/content/journal/jgv/10.1099/vir.0.071688-0&mimeType=html&fmt=ahah

References

  1. Anderson M. M., Lauring A. S., Burns C. C., Overbaugh J. 2000; Identification of a cellular cofactor required for infection by feline leukemia virus. Science 287:1828–1830 [View Article][PubMed]
    [Google Scholar]
  2. Bae Y., Kingsman S. M., Kingsman A. J. 1997; Functional dissection of the Moloney murine leukemia virus envelope protein gp70. J Virol 71:2092–2099[PubMed]
    [Google Scholar]
  3. Barnett A. L., Davey R. A., Cunningham J. M. 2001; Modular organization of the Friend murine leukemia virus envelope protein underlies the mechanism of infection. Proc Natl Acad Sci U S A 98:4113–4118 [View Article][PubMed]
    [Google Scholar]
  4. Barnett A. L., Wensel D. L., Li W., Fass D., Cunningham J. M. 2003; Structure and mechanism of a coreceptor for infection by a pathogenic feline retrovirus. J Virol 77:2717–2729 [View Article][PubMed]
    [Google Scholar]
  5. Benveniste R. E., Sherr C. J., Todaro G. J. 1975; Evolution of type C viral genes: origin of feline leukemia virus. Science 190:886–888 [View Article][PubMed]
    [Google Scholar]
  6. Cosset F. L., Takeuchi Y., Battini J. L., Weiss R. A., Collins M. K. L. 1995; High-titer packaging cells producing recombinant retroviruses resistant to human serum. J Virol 69:7430–7436[PubMed]
    [Google Scholar]
  7. Davey R. A., Hamson C. A., Healey J. J., Cunningham J. M. 1997; In vitro binding of purified murine ecotropic retrovirus envelope surface protein to its receptor, MCAT-1. J Virol 71:8096–8102[PubMed]
    [Google Scholar]
  8. Eckert D. M., Kim P. S. 2001; Mechanisms of viral membrane fusion and its inhibition. Annu Rev Biochem 70:777–810 [View Article][PubMed]
    [Google Scholar]
  9. Farrell K. B., Ting Y. T., Eiden M. V. 2002; Fusion-defective gibbon ape leukemia virus vectors can be rescued by homologous but not heterologous soluble envelope proteins. J Virol 76:4267–4274 [View Article][PubMed]
    [Google Scholar]
  10. Hardy W. D. Jr 1993; Feline oncoretroviruses. In The Retroviridae Vol. 2 pp. 109–180 Edited by Levy L. A. NY: Plenum Press; [View Article]
    [Google Scholar]
  11. Herniou E., Martin J., Miller K., Cook J., Wilkinson M., Tristem M. 1998; Retroviral diversity and distribution in vertebrates. J Virol 72:5955–5966[PubMed]
    [Google Scholar]
  12. Jessup D. A., Pettan K. C., Lowenstine L. J., Pedersen N. C. 1993; Feline leukemia virus infection and renal spirochetosis in a free-range cougar (Felis concolor). J Zoo Wildl Med 24:73–79
    [Google Scholar]
  13. Lauring A. S., Anderson M. M., Overbaugh J. 2001; Specificity in receptor usage by T-cell-tropic feline leukemia viruses: implications for the in vivo tropism of immunodeficiency-inducing variants. J Virol 75:8888–8898 [View Article][PubMed]
    [Google Scholar]
  14. Lauring A. S., Cheng H. H., Eiden M. V., Overbaugh J. 2002; Genetic and biochemical analyses of receptor and cofactor determinants for T-cell-tropic feline leukemia virus infection. J Virol 76:8069–8078 [View Article][PubMed]
    [Google Scholar]
  15. Lavillette D., Kabat D. 2004; Porcine endogenous retroviruses infect cells lacking cognate receptors by an alternative pathway: implications for retrovirus evolution and xenotransplantation. J Virol 78:8868–8877 [View Article][PubMed]
    [Google Scholar]
  16. Lavillette D., Ruggieri A., Russell S. J., Cosset F. L. 2000; Activation of a cell entry pathway common to type C mammalian retroviruses by soluble envelope fragments. J Virol 74:295–304 [View Article][PubMed]
    [Google Scholar]
  17. Lavillette D., Ruggieri A., Boson B., Maurice M., Cosset F. L. 2002; Relationship between SU subdomains that regulate the receptor-mediated transition from the native (fusion-inhibited) to the fusion-active conformation of the murine leukemia virus glycoprotein. J Virol 76:9673–9685 [View Article][PubMed]
    [Google Scholar]
  18. Marker L., Munson L., Basson P. A., Quackenbush S. 2003; Multicentric T-cell lymphoma associated with feline leukemia virus infection in a captive Namibian cheetah (Acinonyx jubatus). J Wildl Dis 39:690–695 [View Article][PubMed]
    [Google Scholar]
  19. McDougall A. S., Terry A., Tzavaras T., Cheney C., Rojko J., Neil J. C. 1994; Defective endogenous proviruses are expressed in feline lymphoid cells: evidence for a role in natural resistance to subgroup B feline leukemia viruses. J Virol 68:2151–2160[PubMed]
    [Google Scholar]
  20. Meli M. L., Cattori V., Martínez F., López G., Vargas A., Simón M. A., Zorrilla I., Muñoz A., Palomares F.other authors 2009; Feline leukemia virus and other pathogens as important threats to the survival of the critically endangered Iberian lynx (Lynx pardinus). PLoS ONE 4:e4744 [View Article][PubMed]
    [Google Scholar]
  21. Mendoza R., Anderson M. M., Overbaugh J. 2006; A putative thiamine transport protein is a receptor for feline leukemia virus subgroup A. J Virol 80:3378–3385 [View Article][PubMed]
    [Google Scholar]
  22. Nakata R., Miyazawa T., Shin Y.-S., Watanabe R., Mikami T., Matsuura Y. 2003; Reevaluation of host ranges of feline leukemia virus subgroups. Microbes Infect 5:947–950 [View Article][PubMed]
    [Google Scholar]
  23. Nakaya Y., Shojima T., Hoshino S., Miyazawa T. 2010; Focus assay on FeLIX-dependent feline leukemia virus. J Vet Med Sci 72:117–121 [View Article][PubMed]
    [Google Scholar]
  24. O’Brien S. J., Troyer J. L., Brown M. A., Johnson W. E., Antunes A., Roelke M. E., Pecon-Slattery J. 2012; Emerging viruses in the Felidae: shifting paradigms. Viruses 4:236–257 [View Article][PubMed]
    [Google Scholar]
  25. Overbaugh J., Donahue P. R., Quackenbush S. L., Hoover E. A., Mullins J. I. 1988; Molecular cloning of a feline leukemia virus that induces fatal immunodeficiency disease in cats. Science 239:906–910 [View Article][PubMed]
    [Google Scholar]
  26. Roca A. L., Pecon-Slattery J., O’Brien S. J. 2004; Genomically intact endogenous feline leukemia viruses of recent origin. J Virol 78:4370–4375 [View Article][PubMed]
    [Google Scholar]
  27. Roca A. L., Nash W. G., Menninger J. C., Murphy W. J., O’Brien S. J. 2005; Insertional polymorphisms of endogenous feline leukemia viruses. J Virol 79:3979–3986 [View Article][PubMed]
    [Google Scholar]
  28. Shojima T., Nakata R., Miyazawa T. 2006; Host cell range of T-lymphotropic feline leukemia virus in vitro. Biochem Biophys Res Commun 345:1466–1470 [View Article][PubMed]
    [Google Scholar]
  29. Takeuchi Y., Vile R. G., Simpson G., O’Hara B., Collins M. K., Weiss R. A. 1992; Feline leukemia virus subgroup B uses the same cell surface receptor as gibbon ape leukemia virus. J Virol 66:1219–1222[PubMed]
    [Google Scholar]
  30. Takeuchi Y., Cosset F. L., Lachmann P. J., Okada H., Weiss R. A., Collins M. K. 1994; Type C retrovirus inactivation by human complement is determined by both the viral genome and the producer cell. J Virol 68:8001–8007[PubMed]
    [Google Scholar]
  31. Watanabe R., Miyazawa T., Matsuura Y. 2004; Comparison of serum sensitivities of pseudotype retroviruses produced from newly established packaging cell lines of human and feline origins. Virus Res 99:89–93 [View Article][PubMed]
    [Google Scholar]
  32. Zhao Y., Zhu L., Benedict C. A., Chen D., Anderson W. F., Cannon P. M. 1998; Functional domains in the retroviral transmembrane protein. J Virol 72:5392–5398[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.071688-0
Loading
/content/journal/jgv/10.1099/vir.0.071688-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error