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. 1993 Nov;67(11):6737–6741. doi: 10.1128/jvi.67.11.6737-6741.1993

Mutation of amino acids within the gibbon ape leukemia virus (GALV) receptor differentially affects feline leukemia virus subgroup B, simian sarcoma-associated virus, and GALV infections.

C S Tailor 1, Y Takeuchi 1, B O'Hara 1, S V Johann 1, R A Weiss 1, M K Collins 1
PMCID: PMC238114  PMID: 8411376

Abstract

The three type C retroviruses, gibbon ape leukemia virus (GALV), simian sarcoma-associated virus (SSAV), and feline leukemia virus subgroup B (FeLV-B), infect human cells by interacting with the same cell surface receptor, GLVR1. Using LacZ retroviral pseudotypes and murine cells transfected with mutant GLVR1 expression vectors, we show that the same 9-amino-acid region of human GLVR1 is critical for infection by the three viruses. Rat cells were not susceptible to infection by LacZ (FeLV-B) pseudotypes because of a block at the receptor level. We found multiple amino acid differences from human GLVR1 in the 9-amino-acid critical region of rat GLVR1. Expression of a human-rat chimeric GLVR1 in murine cells demonstrated that rat GLVR1 could function as a receptor for GALV and SSAV but not for FeLV-B. Substitution of human GLVR1 amino acids in the critical region of rat GLVR1 identified three amino acids as responsible for resistance to FeLV-B infection; two of these affect SSAV infection, but none affects GALV infection.

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Selected References

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  1. Albritton L. M., Kim J. W., Tseng L., Cunningham J. M. Envelope-binding domain in the cationic amino acid transporter determines the host range of ecotropic murine retroviruses. J Virol. 1993 Apr;67(4):2091–2096. doi: 10.1128/jvi.67.4.2091-2096.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albritton L. M., Tseng L., Scadden D., Cunningham J. M. A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell. 1989 May 19;57(4):659–666. doi: 10.1016/0092-8674(89)90134-7. [DOI] [PubMed] [Google Scholar]
  3. Dalgleish A. G., Beverley P. C., Clapham P. R., Crawford D. H., Greaves M. F., Weiss R. A. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature. 1984 Dec 20;312(5996):763–767. doi: 10.1038/312763a0. [DOI] [PubMed] [Google Scholar]
  4. Delassus S., Sonigo P., Wain-Hobson S. Genetic organization of gibbon ape leukemia virus. Virology. 1989 Nov;173(1):205–213. doi: 10.1016/0042-6822(89)90236-5. [DOI] [PubMed] [Google Scholar]
  5. Elder J. H., Mullins J. I. Nucleotide sequence of the envelope gene of Gardner-Arnstein feline leukemia virus B reveals unique sequence homologies with a murine mink cell focus-forming virus. J Virol. 1983 Jun;46(3):871–880. doi: 10.1128/jvi.46.3.871-880.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Etienne-Julan M., Roux P., Carillo S., Jeanteur P., Piechaczyk M. The efficiency of cell targeting by recombinant retroviruses depends on the nature of the receptor and the composition of the artificial cell-virus linker. J Gen Virol. 1992 Dec;73(Pt 12):3251–3255. doi: 10.1099/0022-1317-73-12-3251. [DOI] [PubMed] [Google Scholar]
  7. Ferry N., Duplessis O., Houssin D., Danos O., Heard J. M. Retroviral-mediated gene transfer into hepatocytes in vivo. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8377–8381. doi: 10.1073/pnas.88.19.8377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jarrett O., Hardy W. D., Jr, Golder M. C., Hay D. The frequency of occurrence of feline leukaemia virus subgroups in cats. Int J Cancer. 1978 Mar 15;21(3):334–337. doi: 10.1002/ijc.2910210314. [DOI] [PubMed] [Google Scholar]
  9. Johann S. V., Gibbons J. J., O'Hara B. GLVR1, a receptor for gibbon ape leukemia virus, is homologous to a phosphate permease of Neurospora crassa and is expressed at high levels in the brain and thymus. J Virol. 1992 Mar;66(3):1635–1640. doi: 10.1128/jvi.66.3.1635-1640.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Johann S. V., van Zeijl M., Cekleniak J., O'Hara B. Definition of a domain of GLVR1 which is necessary for infection by gibbon ape leukemia virus and which is highly polymorphic between species. J Virol. 1993 Nov;67(11):6733–6736. doi: 10.1128/jvi.67.11.6733-6736.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kawakami T. G., Huff S. D., Buckley P. M., Dungworth D. L., Synder S. P., Gilden R. V. C-type virus associated with gibbon lymphosarcoma. Nat New Biol. 1972 Feb 9;235(58):170–171. doi: 10.1038/newbio235170a0. [DOI] [PubMed] [Google Scholar]
  12. Kim J. W., Closs E. I., Albritton L. M., Cunningham J. M. Transport of cationic amino acids by the mouse ecotropic retrovirus receptor. Nature. 1991 Aug 22;352(6337):725–728. doi: 10.1038/352725a0. [DOI] [PubMed] [Google Scholar]
  13. Klatzmann D., Champagne E., Chamaret S., Gruest J., Guetard D., Hercend T., Gluckman J. C., Montagnier L. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature. 1984 Dec 20;312(5996):767–768. doi: 10.1038/312767a0. [DOI] [PubMed] [Google Scholar]
  14. Li J. P., Baltimore D. Mechanism of leukemogenesis induced by mink cell focus-forming murine leukemia viruses. J Virol. 1991 May;65(5):2408–2414. doi: 10.1128/jvi.65.5.2408-2414.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Li J. P., D'Andrea A. D., Lodish H. F., Baltimore D. Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor. Nature. 1990 Feb 22;343(6260):762–764. doi: 10.1038/343762a0. [DOI] [PubMed] [Google Scholar]
  16. Lieber M. M., Sherr C. J., Todaro G. J., Benveniste R. E., Callahan R., Coon H. G. Isolation from the asian mouse Mus caroli of an endogenous type C virus related to infectious primate type C viruses. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2315–2319. doi: 10.1073/pnas.72.6.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Miller D. G., Miller A. D. Tunicamycin treatment of CHO cells abrogates multiple blocks to retrovirus infection, one of which is due to a secreted inhibitor. J Virol. 1992 Jan;66(1):78–84. doi: 10.1128/jvi.66.1.78-84.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. O'Hara B., Johann S. V., Klinger H. P., Blair D. G., Rubinson H., Dunn K. J., Sass P., Vitek S. M., Robins T. Characterization of a human gene conferring sensitivity to infection by gibbon ape leukemia virus. Cell Growth Differ. 1990 Mar;1(3):119–127. [PubMed] [Google Scholar]
  19. Sattentau Q. J., Clapham P. R., Weiss R. A., Beverley P. C., Montagnier L., Alhalabi M. F., Gluckmann J. C., Klatzmann D. The human and simian immunodeficiency viruses HIV-1, HIV-2 and SIV interact with similar epitopes on their cellular receptor, the CD4 molecule. AIDS. 1988 Apr;2(2):101–105. doi: 10.1097/00002030-198804000-00005. [DOI] [PubMed] [Google Scholar]
  20. Sheets R. L., Pandey R., Klement V., Grant C. K., Roy-Burman P. Biologically selected recombinants between feline leukemia virus (FeLV) subgroup A and an endogenous FeLV element. Virology. 1992 Oct;190(2):849–855. doi: 10.1016/0042-6822(92)90924-e. [DOI] [PubMed] [Google Scholar]
  21. Sommerfelt M. A., Weiss R. A. Receptor interference groups of 20 retroviruses plating on human cells. Virology. 1990 May;176(1):58–69. doi: 10.1016/0042-6822(90)90230-o. [DOI] [PubMed] [Google Scholar]
  22. Stewart M. A., Warnock M., Wheeler A., Wilkie N., Mullins J. I., Onions D. E., Neil J. C. Nucleotide sequences of a feline leukemia virus subgroup A envelope gene and long terminal repeat and evidence for the recombinational origin of subgroup B viruses. J Virol. 1986 Jun;58(3):825–834. doi: 10.1128/jvi.58.3.825-834.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Takeuchi Y., Simpson G., Vile R. G., Weiss R. A., Collins M. K. Retroviral pseudotypes produced by rescue of a Moloney murine leukemia virus vector by C-type, but not D-type, retroviruses. Virology. 1992 Feb;186(2):792–794. doi: 10.1016/0042-6822(92)90049-u. [DOI] [PubMed] [Google Scholar]
  24. Takeuchi Y., Vile R. G., Simpson G., O'Hara B., Collins M. K., Weiss R. A. Feline leukemia virus subgroup B uses the same cell surface receptor as gibbon ape leukemia virus. J Virol. 1992 Feb;66(2):1219–1222. doi: 10.1128/jvi.66.2.1219-1222.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Taylor J. W., Ott J., Eckstein F. The rapid generation of oligonucleotide-directed mutations at high frequency using phosphorothioate-modified DNA. Nucleic Acids Res. 1985 Dec 20;13(24):8765–8785. doi: 10.1093/nar/13.24.8765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wang H., Kavanaugh M. P., North R. A., Kabat D. Cell-surface receptor for ecotropic murine retroviruses is a basic amino-acid transporter. Nature. 1991 Aug 22;352(6337):729–731. doi: 10.1038/352729a0. [DOI] [PubMed] [Google Scholar]
  27. Yoshimoto T., Yoshimoto E., Meruelo D. Identification of amino acid residues critical for infection with ecotropic murine leukemia retrovirus. J Virol. 1993 Mar;67(3):1310–1314. doi: 10.1128/jvi.67.3.1310-1314.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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