Abstract
The amphotropic murine retrovirus receptor Ram-1 shows significant sequence similarity to the gibbon ape leukemia virus (GALV) receptor Glvr-1, and both of these cell surface virus receptors normally function as sodium-dependent phosphate symporters. However, Ram-1 from humans or rats does not serve as a receptor for GALV, and Glvr-1 from humans does not serve as a receptor for amphotropic virus. Here we show that the murine retrovirus 10A1 can enter cells by using either Glvr-1 or Ram-1. Furthermore, we have constructed Ram-1/Glvr-1 hybrid receptors that allow entry of both GALV and amphotropic virus. While GALV and amphotropic virus are in separate interference groups when assayed on human cells, they do interfere with each other in cells expressing the hybrid receptor. These results indicate a close functional relationship between retroviruses that utilize members of this newly defined receptor family and provide a molecular explanation for nonreciprocal and cell type-specific interference observed for some retrovirus classes.
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- 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]
- 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]
- Biber J., Custer M., Werner A., Kaissling B., Murer H. Localization of NaPi-1, a Na/Pi cotransporter, in rabbit kidney proximal tubules. II. Localization by immunohistochemistry. Pflugers Arch. 1993 Aug;424(3-4):210–215. doi: 10.1007/BF00384344. [DOI] [PubMed] [Google Scholar]
- Chattopadhyay S. K., Lander M. R., Gupta S., Rands E., Lowy D. R. Origin of mink cytopathic focus-forming (MCF) viruses:comparison with ecotropic and xenotropic murine leukemia virus genomes. Virology. 1981 Sep;113(2):465–483. doi: 10.1016/0042-6822(81)90175-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Chesebro B., Wehrly K. Different murine cell lines manifest unique patterns of interference to superinfection by murine leukemia viruses. Virology. 1985 Feb;141(1):119–129. doi: 10.1016/0042-6822(85)90188-6. [DOI] [PubMed] [Google Scholar]
- Chong S. S., Kristjansson K., Zoghbi H. Y., Hughes M. R. Molecular cloning of the cDNA encoding a human renal sodium phosphate transport protein and its assignment to chromosome 6p21.3-p23. Genomics. 1993 Nov;18(2):355–359. doi: 10.1006/geno.1993.1476. [DOI] [PubMed] [Google Scholar]
- 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]
- Eglitis M. A., Eiden M. V., Wilson C. A. Gibbon ape leukemia virus and the amphotropic murine leukemia virus 4070A exhibit an unusual interference pattern on E36 Chinese hamster cells. J Virol. 1993 Sep;67(9):5472–5477. doi: 10.1128/jvi.67.9.5472-5477.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Fischinger P. J., Nomura S., Bolognesi D. P. A novel murine oncornavirus with dual eco- and xenotropic properties. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5150–5155. doi: 10.1073/pnas.72.12.5150. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hosie M. J., Willett B. J., Dunsford T. H., Jarrett O., Neil J. C. A monoclonal antibody which blocks infection with feline immunodeficiency virus identifies a possible non-CD4 receptor. J Virol. 1993 Mar;67(3):1667–1671. doi: 10.1128/jvi.67.3.1667-1671.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Kao F. T., Puck T. T. Genetics of somatic mammalian cells, VII. Induction and isolation of nutritional mutants in Chinese hamster cells. Proc Natl Acad Sci U S A. 1968 Aug;60(4):1275–1281. doi: 10.1073/pnas.60.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kavanaugh M. P., Miller D. G., Zhang W., Law W., Kozak S. L., Kabat D., Miller A. D. Cell-surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus are inducible sodium-dependent phosphate symporters. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7071–7075. doi: 10.1073/pnas.91.15.7071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Magagnin S., Werner A., Markovich D., Sorribas V., Stange G., Biber J., Murer H. Expression cloning of human and rat renal cortex Na/Pi cotransport. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):5979–5983. doi: 10.1073/pnas.90.13.5979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- McClary J. A., Witney F., Geisselsoder J. Efficient site-directed in vitro mutagenesis using phagemid vectors. Biotechniques. 1989 Mar;7(3):282–289. [PubMed] [Google Scholar]
- Miller A. D., Buttimore C. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol Cell Biol. 1986 Aug;6(8):2895–2902. doi: 10.1128/mcb.6.8.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Miller A. D., Miller D. G., Garcia J. V., Lynch C. M. Use of retroviral vectors for gene transfer and expression. Methods Enzymol. 1993;217:581–599. doi: 10.1016/0076-6879(93)17090-r. [DOI] [PubMed] [Google Scholar]
- 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]
- Miller D. G., Edwards R. H., Miller A. D. Cloning of the cellular receptor for amphotropic murine retroviruses reveals homology to that for gibbon ape leukemia virus. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):78–82. doi: 10.1073/pnas.91.1.78. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Ott D., Rein A. Basis for receptor specificity of nonecotropic murine leukemia virus surface glycoprotein gp70SU. J Virol. 1992 Aug;66(8):4632–4638. doi: 10.1128/jvi.66.8.4632-4638.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Rao N. N., Torriani A. Molecular aspects of phosphate transport in Escherichia coli. Mol Microbiol. 1990 Jul;4(7):1083–1090. doi: 10.1111/j.1365-2958.1990.tb00682.x. [DOI] [PubMed] [Google Scholar]
- Rasheed S., Pal B. K., Gardner M. B. Characterization of a highly oncogenic murine leukemia virus from wild mice. Int J Cancer. 1982 Mar 15;29(3):345–350. doi: 10.1002/ijc.2910290319. [DOI] [PubMed] [Google Scholar]
- Rein A., Schultz A. Different recombinant murine leukemia viruses use different cell surface receptors. Virology. 1984 Jul 15;136(1):144–152. doi: 10.1016/0042-6822(84)90255-1. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Sorribas V., Markovich D., Hayes G., Stange G., Forgo J., Biber J., Murer H. Cloning of a Na/Pi cotransporter from opossum kidney cells. J Biol Chem. 1994 Mar 4;269(9):6615–6621. [PubMed] [Google Scholar]
- Tailor C. S., Takeuchi Y., O'Hara B., Johann S. V., Weiss R. A., Collins M. K. 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. J Virol. 1993 Nov;67(11):6737–6741. doi: 10.1128/jvi.67.11.6737-6741.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Wei C. M., Gibson M., Spear P. G., Scolnick E. M. Construction and isolation of a transmissible retrovirus containing the src gene of Harvey murine sarcoma virus and the thymidine kinase gene of herpes simplex virus type 1. J Virol. 1981 Sep;39(3):935–944. doi: 10.1128/jvi.39.3.935-944.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Werner A., Moore M. L., Mantei N., Biber J., Semenza G., Murer H. Cloning and expression of cDNA for a Na/Pi cotransport system of kidney cortex. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9608–9612. doi: 10.1073/pnas.88.21.9608. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willett B. J., Hosie M. J., Jarrett O., Neil J. C. Identification of a putative cellular receptor for feline immunodeficiency virus as the feline homologue of CD9. Immunology. 1994 Feb;81(2):228–233. [PMC free article] [PubMed] [Google Scholar]
- Young J. A., Bates P., Varmus H. E. Isolation of a chicken gene that confers susceptibility to infection by subgroup A avian leukosis and sarcoma viruses. J Virol. 1993 Apr;67(4):1811–1816. doi: 10.1128/jvi.67.4.1811-1816.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van Zeijl M., Johann S. V., Closs E., Cunningham J., Eddy R., Shows T. B., O'Hara B. A human amphotropic retrovirus receptor is a second member of the gibbon ape leukemia virus receptor family. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1168–1172. doi: 10.1073/pnas.91.3.1168. [DOI] [PMC free article] [PubMed] [Google Scholar]