Abstract
10A1 murine leukemia virus can enter cells by using either of two different cell surface phosphate transport proteins, the gibbon ape leukemia virus receptor Glvr-1 (Pit-1) or the amphotropic retrovirus receptor Ram-1 (Pit-2). Glvr-1 and Ram-1 are widely expressed in different tissues, but the relative amounts of each are highly variable. We have developed retrovirus packaging cell lines based on 10A1 virus to take advantage of this dual receptor utilization to improve gene transfer rates in somatic cells of animals and humans, in which the relative levels of the two receptors are not always known. Optimization of the Env expression vector allowed the generation of packaging lines that produce helper-free vector titers up to 10(7)/ml. By interference analysis, we found that a 10A1 pseudotype retroviral vector can utilize Ram-1 for efficient entry into mouse, rat, and human cells and can utilize Glvr-1 for entry into mouse and human cells but not for entry into rat cells. The 10A1 pseudotype vector efficiently enters mouse cells by using Glvr-1, while entry into human cells is much less efficient. Thus, the 10A1 pseudotype packaging cells may be advantageous compared with the standard amphotropic packaging cells because vectors produced by the cells can use an additional receptor for cell entry. These packaging cells will also be useful to further explore the complicated pattern of receptor usage conferred by the 10A1 viral surface protein.
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Selected References
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- Bauer T. R., Jr, Miller A. D., Hickstein D. D. Improved transfer of the leukocyte integrin CD18 subunit into hematopoietic cell lines by using retroviral vectors having a gibbon ape leukemia virus envelope. Blood. 1995 Sep 15;86(6):2379–2387. [PubMed] [Google Scholar]
- Bayle J. Y., Johnson L. G., St George J. A., Boucher R. C., Olsen J. C. High-efficiency gene transfer to primary monkey airway epithelial cells with retrovirus vectors using the gibbon ape leukemia virus receptor. Hum Gene Ther. 1993 Apr;4(2):161–170. doi: 10.1089/hum.1993.4.2-161. [DOI] [PubMed] [Google Scholar]
- Bender M. A., Palmer T. D., Gelinas R. E., Miller A. D. Evidence that the packaging signal of Moloney murine leukemia virus extends into the gag region. J Virol. 1987 May;61(5):1639–1646. doi: 10.1128/jvi.61.5.1639-1646.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bunnell B. A., Muul L. M., Donahue R. E., Blaese R. M., Morgan R. A. High-efficiency retroviral-mediated gene transfer into human and nonhuman primate peripheral blood lymphocytes. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7739–7743. doi: 10.1073/pnas.92.17.7739. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burns J. C., Friedmann T., Driever W., Burrascano M., Yee J. K. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8033–8037. doi: 10.1073/pnas.90.17.8033. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chattopadhyay S. K., Oliff A. I., Linemeyer D. L., Lander M. R., Lowy D. R. Genomes of murine leukemia viruses isolated from wild mice. J Virol. 1981 Sep;39(3):777–791. doi: 10.1128/jvi.39.3.777-791.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cone R. D., Mulligan R. C. High-efficiency gene transfer into mammalian cells: generation of helper-free recombinant retrovirus with broad mammalian host range. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6349–6353. doi: 10.1073/pnas.81.20.6349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cosset F. L., Takeuchi Y., Battini J. L., Weiss R. A., Collins M. K. High-titer packaging cells producing recombinant retroviruses resistant to human serum. J Virol. 1995 Dec;69(12):7430–7436. doi: 10.1128/jvi.69.12.7430-7436.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dunn K. J., Yuan C. C., Blair D. G. A phenotypic host range alteration determines RD114 virus restriction in feline embryonic cells. J Virol. 1993 Aug;67(8):4704–4711. doi: 10.1128/jvi.67.8.4704-4711.1993. [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]
- Gardner M. B. Retroviruses and wild mice: an historical and personal perspective. Adv Cancer Res. 1994;65:169–201. doi: 10.1016/s0065-230x(08)60068-8. [DOI] [PubMed] [Google Scholar]
- Haapala D. K., Robey W. G., Oroszlan S. D., Tsai W. P. Isolation from cats of an endogenous type C virus with a novel envelope glycoprotein. J Virol. 1985 Mar;53(3):827–833. doi: 10.1128/jvi.53.3.827-833.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartley J. W., Rowe W. P. Naturally occurring murine leukemia viruses in wild mice: characterization of a new "amphotropic" class. J Virol. 1976 Jul;19(1):19–25. doi: 10.1128/jvi.19.1.19-25.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kasahara N., Dozy A. M., Kan Y. W. Tissue-specific targeting of retroviral vectors through ligand-receptor interactions. Science. 1994 Nov 25;266(5189):1373–1376. doi: 10.1126/science.7973726. [DOI] [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]
- Lin S., Gaiano N., Culp P., Burns J. C., Friedmann T., Yee J. K., Hopkins N. Integration and germ-line transmission of a pseudotyped retroviral vector in zebrafish. Science. 1994 Jul 29;265(5172):666–669. doi: 10.1126/science.8036514. [DOI] [PubMed] [Google Scholar]
- Lusky M., Botchan M. Inhibition of SV40 replication in simian cells by specific pBR322 DNA sequences. Nature. 1981 Sep 3;293(5827):79–81. doi: 10.1038/293079a0. [DOI] [PubMed] [Google Scholar]
- Lynch C. M., Miller A. D. Production of high-titer helper virus-free retroviral vectors by cocultivation of packaging cells with different host ranges. J Virol. 1991 Jul;65(7):3887–3890. doi: 10.1128/jvi.65.7.3887-3890.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MOLONEY J. B. Biological studies on a lymphoid-leukemia virus extracted from sarcoma 37. I. Origin and introductory investigations. J Natl Cancer Inst. 1960 Apr;24:933–951. [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., Law M. F., Verma I. M. Generation of helper-free amphotropic retroviruses that transduce a dominant-acting, methotrexate-resistant dihydrofolate reductase gene. Mol Cell Biol. 1985 Mar;5(3):431–437. doi: 10.1128/mcb.5.3.431. [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. A family of retroviruses that utilize related phosphate transporters for cell entry. J Virol. 1994 Dec;68(12):8270–8276. doi: 10.1128/jvi.68.12.8270-8276.1994. [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]
- Rasheed S., Gardner M. B., Chan E. Amphotropic host range of naturally occuring wild mouse leukemia viruses. J Virol. 1976 Jul;19(1):13–18. doi: 10.1128/jvi.19.1.13-18.1976. [DOI] [PMC free article] [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]
- Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
- Simonsen C. C., Levinson A. D. Isolation and expression of an altered mouse dihydrofolate reductase cDNA. Proc Natl Acad Sci U S A. 1983 May;80(9):2495–2499. doi: 10.1073/pnas.80.9.2495. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Somia N. V., Zoppé M., Verma I. M. Generation of targeted retroviral vectors by using single-chain variable fragment: an approach to in vivo gene delivery. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7570–7574. doi: 10.1073/pnas.92.16.7570. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sorge J., Wright D., Erdman V. D., Cutting A. E. Amphotropic retrovirus vector system for human cell gene transfer. Mol Cell Biol. 1984 Sep;4(9):1730–1737. doi: 10.1128/mcb.4.9.1730. [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]
- von Kalle C., Kiem H. P., Goehle S., Darovsky B., Heimfeld S., Torok-Storb B., Storb R., Schuening F. G. Increased gene transfer into human hematopoietic progenitor cells by extended in vitro exposure to a pseudotyped retroviral vector. Blood. 1994 Nov 1;84(9):2890–2897. [PubMed] [Google Scholar]