Binding of equine infectious anemia virus to the equine lentivirus receptor-1 is mediated by complex discontinuous sequences in the viral envelope gp90 protein Free

Abstract

The identification and characterization of a functional cellular receptor for equine infectious anemia virus (EIAV), designated equine lentivirus receptor-1 (ELR1), a member of the tumour necrosis factor receptor protein family, has been reported previously [ Zhang, B. (2005). ,  , 9918–9923 ]. The finding of a single receptor for EIAV is distinct from feline, simian and human immunodeficiency viruses, which typically utilize two co-receptors for infection, but is similar to avian and murine oncoviruses, which use single receptors. This study sought to determine ELR1-binding domains of EIAV gp90. Towards this goal, a GFP-tagged gp90 fusion protein (gp90GFP) expression vector was constructed and a specific cell–cell binding assay was developed to measure EIAV gp90 binding to ELR1. Using these assays, the receptor-binding properties of 41 gp90GFP mutants were evaluated, each with a sequential replacement 11 aa linear epitope peptide from the vesicular stomatitis virus glycoprotein (VSV-G tag), as well as eight mutants containing individual gp90 variable-domain deletions. The results of these studies demonstrated that, in general, gp90 constructs containing substitutions or deletions in the N-terminal third of gp90 retained their receptor-binding activity. In contrast, segment substitutions or deletions in the C-terminal two-thirds of gp90 eliminated receptor-binding activity. Thus, these results reveal for the first time that the ELR1-binding domains of EIAV gp90 are located in the C-terminal two-thirds of EIAV gp90, apparently as a complex of discontinuous determinants.

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2008-08-01
2024-03-29
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References

  1. Adkins H. B., Brojatsch J., Naughton J., Rolls M. M., Pesola J. M., Young J. A. 1997; Identification of a cellular receptor for subgroup E avian leukosis virus. Proc Natl Acad Sci U S A 94:11617–11622 [CrossRef]
    [Google Scholar]
  2. Adkins H. B., Brojatsch J., Young J. A. 2000; Identification and characterization of a shared TNFR-related receptor for subgroup B, D, and E avian leukosis viruses reveal cysteine residues required specifically for subgroup E viral entry. J Virol 74:3572–3578 [CrossRef]
    [Google Scholar]
  3. Ball J. M., Rushlow K. E., Issel C. J., Montelaro R. C. 1992; Detailed mapping of the antigenicity of the surface unit glycoprotein of equine infectious anemia virus by using synthetic peptide strategies. J Virol 66:732–742
    [Google Scholar]
  4. Barnard R. J., Elleder D., Young J. A. 2006; Avian sarcoma and leukosis virus–receptor interactions: from classical genetics to novel insights into virus–cell membrane fusion. Virology 344:25–29 [CrossRef]
    [Google Scholar]
  5. Battini J. L., Heard J. M., Danos O. 1992; Receptor choice determinants in the envelope glycoproteins of amphotropic, xenotropic, and polytropic murine leukemia viruses. J Virol 66:1468–1475
    [Google Scholar]
  6. Battini J. L., Danos O., Heard J. M. 1995; Receptor-binding domain of murine leukemia virus envelope glycoproteins. J Virol 69:713–719
    [Google Scholar]
  7. Battini J. L., Danos O., Heard J. M. 1998; Definition of a 14-amino-acid peptide essential for the interaction between the murine leukemia virus amphotropic envelope glycoprotein and its receptor. J Virol 72:428–435
    [Google Scholar]
  8. Brojatsch J., Naughton J., Rolls M. M., Zingler K., Young J. A. 1996; CAR1, a TNFR-related protein, is a cellular receptor for cytopathic avian leukosis-sarcoma viruses and mediates apoptosis. Cell 87:845–855 [CrossRef]
    [Google Scholar]
  9. Chiang H. Y., Cohen G. H., Eisenberg R. J. 1994; Identification of functional regions of herpes simplex virus glycoprotein gD by using linker-insertion mutagenesis. J Virol 68:2529–2543
    [Google Scholar]
  10. Connolly S. A., Landsburg D. J., Carfi A., Wiley D. C., Eisenberg R. J., Cohen G. H. 2002; Structure-based analysis of the herpes simplex virus glycoprotein D binding site present on herpesvirus entry mediator HveA (HVEM).. J Virol 76:10894–10904 [CrossRef]
    [Google Scholar]
  11. Connolly S. A., Landsburg D. J., Carfi A., Wiley D. C., Cohen G. H., Eisenberg R. J. 2003; Structure-based mutagenesis of herpes simplex virus glycoprotein D defines three critical regions at the gD-HveA/HVEM binding interface. J Virol 77:8127–8140 [CrossRef]
    [Google Scholar]
  12. Cordonnier A., Riviere Y., Montagnier L., Emerman M. 1989; Effects of mutations in hyperconserved regions of the extracellular glycoprotein of human immunodeficiency virus type 1 on receptor binding. J Virol 63:4464–4468
    [Google Scholar]
  13. de Parseval A., Chatterji U., Sun P., Elder J. H. 2004; Feline immunodeficiency virus targets activated CD4+ T cells by using CD134 as a binding receptor. Proc Natl Acad Sci U S A 101:13044–13049 [CrossRef]
    [Google Scholar]
  14. de Parseval A., Chatterji U., Morris G., Sun P., Olson A. J., Elder J. H. 2005; Structural mapping of CD134 residues critical for interaction with feline immunodeficiency virus. Nat Struct Mol Biol 12:60–66 [CrossRef]
    [Google Scholar]
  15. Doms R. W., Lamb R. A., Rose J. K., Helenius A. 1993; Folding and assembly of viral membrane proteins. Virology 193:545–562 [CrossRef]
    [Google Scholar]
  16. Douglas N. W., Munro G. H., Daniels R. S. 1997; HIV/SIV glycoproteins: structure–function relationships. J Mol Biol 273:122–149 [CrossRef]
    [Google Scholar]
  17. Eiden M. V., Farrell K., Warsowe J., Mahan L. C., Wilson C. A. 1993; Characterization of a naturally occurring ecotropic receptor that does not facilitate entry of all ecotropic murine retroviruses. J Virol 67:4056–4061
    [Google Scholar]
  18. Fass D., Davey R. A., Hamson C. A., Kim P. S., Cunningham J. M., Berger J. M. 1997; Structure of a murine leukemia virus receptor-binding glycoprotein at 2.0 Å resolution. Science 277:1662–1666 [CrossRef]
    [Google Scholar]
  19. Gallaher W. R., Ball J. M., Garry R. F., Griffin M. C., Montelaro R. C. 1989; A general model for the transmembrane proteins of HIV and other retroviruses. AIDS Res Hum Retroviruses 5:431–440 [CrossRef]
    [Google Scholar]
  20. Gallaher W. R., Ball J. M., Garry R. F., Martin-Amedee A. M., Montelaro R. C. 1995; A general model for the surface glycoproteins of HIV and other retroviruses. AIDS Res Hum Retroviruses 11:191–202 [CrossRef]
    [Google Scholar]
  21. Gomez C., Hope T. J. 2005; The ins and outs of HIV replication. Cell Microbiol 7:621–626 [CrossRef]
    [Google Scholar]
  22. Heard J. M., Danos O. 1991; An amino-terminal fragment of the Friend murine leukemia virus envelope glycoprotein binds the ecotropic receptor. J Virol 65:4026–4032
    [Google Scholar]
  23. Hussain K. A., Issel C. J., Schnorr K. L., Rwambo P. M., Montelaro R. C. 1987; Antigenic analysis of equine infectious anemia virus (EIAV) variants by using monoclonal antibodies: epitopes of glycoprotein gp90 of EIAV stimulate neutralizing antibodies. J Virol 61:2956–2961
    [Google Scholar]
  24. Hussain K. A., Issel C. J., Schnorr K. L., Rwambo P. M., West M., Montelaro R. C. 1988; Antigenic mapping of the envelope proteins of equine infectious anemia virus: identification of a neutralization domain and a conserved region on glycoprotein 90. Arch Virol 98:213–224 [CrossRef]
    [Google Scholar]
  25. Jin S., Zhang B., Weisz O. A., Montelaro R. C. 2005; Receptor-mediated entry by equine infectious anemia virus utilizes a pH-dependent endocytic pathway. J Virol 79:14489–14497 [CrossRef]
    [Google Scholar]
  26. Kreis T. E. 1986; Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotein block its transport to the cell surface. EMBO J 5:931–941
    [Google Scholar]
  27. Kwong P. D., Wyatt R., Robinson J., Sweet R. W., Sodroski J., Hendrickson W. A. 1998; Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648–659 [CrossRef]
    [Google Scholar]
  28. Leonard C. K., Spellman M. W., Riddle L., Harris R. J., Thomas J. N., Gregory T. J. 1990; Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J Biol Chem 265:10373–10382
    [Google Scholar]
  29. Leroux C., Issel C. J., Montelaro R. C. 1997; Novel and dynamic evolution of equine infectious anemia virus genomic quasispecies associated with sequential disease cycles in an experimentally infected pony. J Virol 71:9627–9639
    [Google Scholar]
  30. Leroux C., Craigo J. K., Issel C. J., Montelaro R. C. 2001; Equine infectious anemia virus genomic evolution in progressor and nonprogressor ponies. J Virol 75:4570–4583 [CrossRef]
    [Google Scholar]
  31. Modrow S., Hahn B. H., Shaw G. M., Gallo R. C., Wong-Staal F., Wolf H. 1987; Computer-assisted analysis of envelope protein sequences of seven human immunodeficiency virus isolates: prediction of antigenic epitopes in conserved and variable regions. J Virol 61:570–578
    [Google Scholar]
  32. Montelaro R. C., Parekh B., Orrego A., Issel C. J. 1984; Antigenic variation during persistent infection by equine infectious anemia virus, a retrovirus. J Biol Chem 259:10539–10544
    [Google Scholar]
  33. Moore J. P., Sattentau Q. J., Wyatt R., Sodroski J. 1994; Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies. J Virol 68:469–484
    [Google Scholar]
  34. Morgan R. A., Nussbaum O., Muenchau D. D., Shu L., Couture L., Anderson W. F. 1993; Analysis of the functional and host range-determining regions of the murine ecotropic and amphotropic retrovirus envelope proteins. J Virol 67:4712–4721
    [Google Scholar]
  35. Ott D., Rein A. 1992; Basis for receptor specificity of nonecotropic murine leukemia virus surface glycoprotein gp70SU. J Virol 66:4632–4638
    [Google Scholar]
  36. Poignard P., Saphire E. O., Parren P. W., Burton D. R. 2001; gp120: biologic aspects of structural features. Annu Rev Immunol 19:253–274 [CrossRef]
    [Google Scholar]
  37. Rizzuto C. D., Wyatt R., Hernandez-Ramos N., Sun Y., Kwong P. D., Hendrickson W. A., Sodroski J. 1998; A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280:1949–1953 [CrossRef]
    [Google Scholar]
  38. Rose J. K., Gallione C. J. 1981; Nucleotide sequences of the mRNAs encoding the vesicular stomatitis virus G and M proteins determined from cDNA clones containing the complete coding regions. J Virol 39:519–528
    [Google Scholar]
  39. Shimojima M., Miyazawa T., Ikeda Y., McMonagle E. L., Haining H., Akashi H., Takeuchi Y., Hosie M. J., Willett B. J. 2004; Use of CD134 as a primary receptor by the feline immunodeficiency virus. Science 303:1192–1195 [CrossRef]
    [Google Scholar]
  40. Suphaphiphat P., Thitithanyanont A., Paca-Uccaralertkun S., Essex M., Lee T. H. 2003; Effect of amino acid substitution of the V3 and bridging sheet residues in human immunodeficiency virus type 1 subtype C gp120 on CCR5 utilization. J Virol 77:3832–3837 [CrossRef]
    [Google Scholar]
  41. Suphaphiphat P., Essex M., Lee T. H. 2007; Mutations in the V3 stem versus the V3 crown and C4 region have different effects on the binding and fusion steps of human immunodeficiency virus type 1 gp120 interaction with the CCR5 coreceptor. Virology 360:182–190 [CrossRef]
    [Google Scholar]
  42. Wyatt R., Moore J., Accola M., Desjardin E., Robinson J., Sodroski J. 1995; Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J Virol 69:5723–5733
    [Google Scholar]
  43. Wyatt R., Kwong P. D., Desjardins E., Sweet R. W., Robinson J., Hendrickson W. A., Sodroski J. G. 1998; The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705–711 [CrossRef]
    [Google Scholar]
  44. Zhang B., Jin S., Jin J., Li F., Montelaro R. C. 2005; A tumor necrosis factor receptor family protein serves as a cellular receptor for the macrophage-tropic equine lentivirus. Proc Natl Acad Sci U S A 102:9918–9923 [CrossRef]
    [Google Scholar]
  45. Zhang B., Sun C., Jin S., Cascio M., Montelaro R. C. 2008; Mapping of equine lentivirus receptor-1 residues critical for EIAV envelope binding. J Virol 82:1204–1213 [CrossRef]
    [Google Scholar]
  46. Zheng Y. H., Nakaya T., Sentsui H., Kameoka M., Kishi M., Hagiwara K., Takahashi H., Kono Y., Ikuta K. 1997; Insertions, duplications and substitutions in restricted gp90 regions of equine infectious anaemia virus during febrile episodes in an experimentally infected horse. J Gen Virol 78:807–820
    [Google Scholar]
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