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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Jan 4;91(1):78–82. doi: 10.1073/pnas.91.1.78

Cloning of the cellular receptor for amphotropic murine retroviruses reveals homology to that for gibbon ape leukemia virus.

D G Miller 1, R H Edwards 1, A D Miller 1
PMCID: PMC42889  PMID: 8278411

Abstract

The host and tissue specificity of retrovirus infection is largely determined by specific cellular receptors that mediate virus entry. Genes encoding these receptors are widely distributed in the genome, and the receptors identified to date show no sequence similarity. We have identified the cellular receptor for amphotropic murine retroviruses, Ram-1, by screening a rat cDNA expression library introduced into amphotropic virus-resistant hamster cells. The 656-amino acid receptor is homologous to the gibbon ape leukemia virus receptor at both hydrophobic termini but is highly divergent in the central hydrophilic region. Both receptors appear to be integral membrane proteins having multiple membrane-spanning regions. Identification of this family of receptors will help define the evolutionary relationship between retroviruses and their cellular receptors.

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Selected References

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  1. 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]
  2. Ban J., Portetelle D., Altaner C., Horion B., Milan D., Krchnak V., Burny A., Kettmann R. Isolation and characterization of a 2.3-kilobase-pair cDNA fragment encoding the binding domain of the bovine leukemia virus cell receptor. J Virol. 1993 Feb;67(2):1050–1057. doi: 10.1128/jvi.67.2.1050-1057.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Battini J. L., Heard J. M., Danos O. Receptor choice determinants in the envelope glycoproteins of amphotropic, xenotropic, and polytropic murine leukemia viruses. J Virol. 1992 Mar;66(3):1468–1475. doi: 10.1128/jvi.66.3.1468-1475.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Deutscher S. L., Hirschberg C. B. Mechanism of galactosylation in the Golgi apparatus. A Chinese hamster ovary cell mutant deficient in translocation of UDP-galactose across Golgi vesicle membranes. J Biol Chem. 1986 Jan 5;261(1):96–100. [PubMed] [Google Scholar]
  6. Fields-Berry S. C., Halliday A. L., Cepko C. L. A recombinant retrovirus encoding alkaline phosphatase confirms clonal boundary assignment in lineage analysis of murine retina. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):693–697. doi: 10.1073/pnas.89.2.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Garcia J. V., Jones C., Miller A. D. Localization of the amphotropic murine leukemia virus receptor gene to the pericentromeric region of human chromosome 8. J Virol. 1991 Nov;65(11):6316–6319. doi: 10.1128/jvi.65.11.6316-6319.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gazdar A. F., Oie H., Lalley P., Moss W. W., Minna J. D. Identification of mouse chromosomes required for murine leukemia virus replication. Cell. 1977 Aug;11(4):949–956. doi: 10.1016/0092-8674(77)90306-3. [DOI] [PubMed] [Google Scholar]
  9. Isobe M., Huebner K., Maddon P. J., Littman D. R., Axel R., Croce C. M. The gene encoding the T-cell surface protein T4 is located on human chromosome 12. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4399–4402. doi: 10.1073/pnas.83.12.4399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Kaelbling M., Eddy R., Shows T. B., Copeland N. G., Gilbert D. J., Jenkins N. A., Klinger H. P., O'Hara B. Localization of the human gene allowing infection by gibbon ape leukemia virus to human chromosome region 2q11-q14 and to the homologous region on mouse chromosome 2. J Virol. 1991 Apr;65(4):1743–1747. doi: 10.1128/jvi.65.4.1743-1747.1991. [DOI] [PMC free article] [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. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  14. Liu Y., Roghani A., Edwards R. H. Gene transfer of a reserpine-sensitive mechanism of resistance to N-methyl-4-phenylpyridinium. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9074–9078. doi: 10.1073/pnas.89.19.9074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Maddon P. J., Dalgleish A. G., McDougal J. S., Clapham P. R., Weiss R. A., Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 1986 Nov 7;47(3):333–348. doi: 10.1016/0092-8674(86)90590-8. [DOI] [PubMed] [Google Scholar]
  16. Mann B. J., Bowman B. J., Grotelueschen J., Metzenberg R. L. Nucleotide sequence of pho-4+, encoding a phosphate-repressible phosphate permease of Neurospora crassa. Gene. 1989 Nov 30;83(2):281–289. doi: 10.1016/0378-1119(89)90114-5. [DOI] [PubMed] [Google Scholar]
  17. Miller A. D., Garcia J. V., von Suhr N., Lynch C. M., Wilson C., Eiden M. V. Construction and properties of retrovirus packaging cells based on gibbon ape leukemia virus. J Virol. 1991 May;65(5):2220–2224. doi: 10.1128/jvi.65.5.2220-2224.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Miller A. D. Human gene therapy comes of age. Nature. 1992 Jun 11;357(6378):455–460. doi: 10.1038/357455a0. [DOI] [PubMed] [Google Scholar]
  19. Miller A. D., Rosman G. J. Improved retroviral vectors for gene transfer and expression. Biotechniques. 1989 Oct;7(9):980-2, 984-6, 989-90. [PMC free article] [PubMed] [Google Scholar]
  20. Miller A. D., Trauber D. R., Buttimore C. Factors involved in production of helper virus-free retrovirus vectors. Somat Cell Mol Genet. 1986 Mar;12(2):175–183. doi: 10.1007/BF01560664. [DOI] [PubMed] [Google Scholar]
  21. Miller D. G., Miller A. D. Inhibitors of retrovirus infection are secreted by several hamster cell lines and are also present in hamster sera. J Virol. 1993 Sep;67(9):5346–5352. doi: 10.1128/jvi.67.9.5346-5352.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Ott D., Friedrich R., Rein A. Sequence analysis of amphotropic and 10A1 murine leukemia viruses: close relationship to mink cell focus-inducing viruses. J Virol. 1990 Feb;64(2):757–766. doi: 10.1128/jvi.64.2.757-766.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Quade K. Transformation of mammalian cells by avian myelocytomatosis virus and avian erythroblastosis virus. Virology. 1979 Oct 30;98(2):461–465. doi: 10.1016/0042-6822(79)90569-5. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Stanley P., Siminovitch L. Complementation between mutants of CHO cells resistant to a variety of plant lectins. Somatic Cell Genet. 1977 Jul;3(4):391–405. doi: 10.1007/BF01542968. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Yoshimoto T., Yoshimoto E., Meruelo D. Molecular cloning and characterization of a novel human gene homologous to the murine ecotropic retroviral receptor. Virology. 1991 Nov;185(1):10–17. doi: 10.1016/0042-6822(91)90748-z. [DOI] [PubMed] [Google Scholar]

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