1887

Abstract

A tail fibroblast (MDTF) cell line is highly resistant to infection by ecotropic Moloney murine leukemia virus (Mo-MLV). The cationic amino acid transporter type 1 (CAT1) paralogues of murine NIH 3T3 and MDTF cells (mCAT1 and dCAT1, respectively) contain two conserved -linked glycosylation sites in the third extracellular loop (ECL3, the putative Mo-MLV binding site). Glycosylation of dCAT1 inhibits Mo-MLV infection, but that of mCAT1 does not. Compared with mCAT1, dCAT1 possesses an Ile-to-Val substitution at position 214 and a Gly insertion at position 236 in the ECL3. To determine the residues responsible for the loss of dCAT1 receptor function, mutants of mCAT1 were constructed. The mCAT1/insG receptor (with a Gly residue inserted at mCAT1 position 236) had greatly reduced Mo-MLV receptor function compared with mCAT1. Treatment of mCAT1/insG-expressing cells with tunicamycin, an -linked glycosylation inhibitor, increased the transduction titre. In addition, the reduced susceptibility to Mo-MLV observed with mCAT1/insG-expressing cells correlated with impaired binding of Mo-MLV. These results show that a single amino acid insertion confers mCAT1 receptor properties on dCAT1 and provide an important insight into the co-evolution of virus–host interactions.

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2008-01-01
2021-02-25
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References

  1. Albritton L. M., Tseng L., Scadden D., Cunningham J. M. 1989; A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57:659–666 [CrossRef]
    [Google Scholar]
  2. Albritton L. M., Kim J. W., Tseng L., Cunningham J. M. 1993; Envelope-binding domain in the cationic amino acid transporter determines the host range of ecotropic murine retroviruses. J Virol 67:2091–2096
    [Google Scholar]
  3. Bae E. H., Park S. H., Jung Y. T. 2006; Role of a third extracellular domain of an ecotropic receptor in Moloney murine leukemia virus infection. J Microbiol 44:447–452
    [Google Scholar]
  4. Chang L.-J., Urlacher V., Iwakuma T., Cui Y., Zucali J. 1999; Efficacy and safety analyses of a recombinant human immunodeficiency virus type 1 derived vector system. Gene Ther 6:715–728 [CrossRef]
    [Google Scholar]
  5. Chesebro B., Wehrly K. 1985; Different cell lines manifest unique patterns of interference to superinfection by murine viruses. Virology 141:119–129 [CrossRef]
    [Google Scholar]
  6. Cosset F.-L., Takeuchi Y., Battini J.-L., Weiss R. A. 1995; High-titer packaging cells producing recombinant retroviruses resistant to human serum. J Virol 69:7430–7436
    [Google Scholar]
  7. 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]
  8. Eiden M. V., Farrell K., Wilson C. A. 1994; Glycosylation-dependent inactivation of the ecotropic murine leukemia virus receptor. J Virol 68:626–631
    [Google Scholar]
  9. Helenius A., Aebi M. 2001; Intracellular functions of N -linked glycans. Science 291:2364–2369 [CrossRef]
    [Google Scholar]
  10. Helenius A., Aebi M. 2004; Roles of N -linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019–1049 [CrossRef]
    [Google Scholar]
  11. Ishimoto A. 1985; Infectivity of Friend murine leukemia virus for hamster cells. J Natl Cancer Inst 74:905–908
    [Google Scholar]
  12. Jung Y. T., Wu T., Kozak C. A. 2004; Novel host range and cytopathic variant of ecotropic Friend murine leukemia virus. J Virol 78:12189–12197 [CrossRef]
    [Google Scholar]
  13. Kim J. W., Closs E. I., Albritton L. M., Cunningham J. M. 1991; Transport of cationic amino acids by the mouse ecotropic retrovirus receptor. Nature 352:725–728 [CrossRef]
    [Google Scholar]
  14. Kubo Y., Amanuma H. 2003; Mutational analysis of the R peptide cleavage site of Moloney murine leukemia virus envelope protein. J Gen Virol 84:2253–2257 [CrossRef]
    [Google Scholar]
  15. Kubo Y., Ono T., Ogura M., Ishimoto A., Amanuma H. 2002; A glycosylation-defective variant of the ecotropic murine retrovirus receptor is expressed in rat XC cells. Virology 303:338–344 [CrossRef]
    [Google Scholar]
  16. Kubo Y., Ishimoto A., Ono T., Yoshii H., Tominaga C., Mitani C., Amanuma H., Yamamoto N. 2004; Determinant for the inhibition of ecotropic murine leukemia virus infection by N -linked glycosylation of the rat receptor. Virology 330:82–91 [CrossRef]
    [Google Scholar]
  17. Lander M. R., Chattopadhyay S. K. 1984; A Mus dunni cell line that lacks sequences closely related to endogenous murine leukemia viruses and can be infected by ecotropic, amphotropic, xenotropic, and mink cell focus-forming viruses. J Virol 52:695–698
    [Google Scholar]
  18. Lavillette D., Ruggieri A., Russell S. J., Cosset F.-L. 2000; Activation of a cell entry pathway common to type C mammalian retroviruses by soluble envelope fragments. J Virol 74:295–304 [CrossRef]
    [Google Scholar]
  19. Masuda M., Masuda M., Hanson C. A., Hoffman P. M., Ruscetti S. K. 1996; Analysis of the unique hamster cell tropism of ecotropic murine leukemia virus PVC-211. J Virol 70:8534–8539
    [Google Scholar]
  20. Miller D. G., Miller A. D. 1992; Tunicamycin treatment of CHO cells abrogates multiple blocks to retrovirus infection, one of which is due to a secreted inhibitor. J Virol 66:78–84
    [Google Scholar]
  21. Onishi M., Kinoshita S., Morikawa Y., Shibuya A., Phillips J., Lanier L. L., Gorman D. M., Nolan G. P., Miyajima A., Kitamura T. 1996; Applications of retroviruses-mediated expression cloning. Exp Hematol 24:324–329
    [Google Scholar]
  22. Overbaugh J., Miller A. D., Eiden M. V. 2001; Receptor and entry cofactors for retroviruses include single and multiple transmembrane-spanning proteins as well as newly described glycophosphatidylinositol-anchored and secreted proteins. Microbiol Mol Biol Rev 65:371–389 [CrossRef]
    [Google Scholar]
  23. Perkins C. P., Mar V., Shutter J. R., Castillo J., Danilenko D. M., Medlock E. S., Ponting I. L., Graham M., Stark K. L. other authors 1997; Anemia and perinatal death result from loss of the murine ecotropic retrovirus receptor mCAT-1. Genes Dev 11:914–925 [CrossRef]
    [Google Scholar]
  24. Soda Y., Shimizu N., Jinno A., Liu H., Kanbe K., Kitamura T., Hoshino H. 1999; Establishment of a new system for determination of coreceptor usage of HIV based on the human glioma NP-2 cell line. Biochem Biophys Res Commun 258:313–321 [CrossRef]
    [Google Scholar]
  25. Sommerfelt M. A. 1999; Retrovirus receptors. J Gen Virol 80:3049–3064
    [Google Scholar]
  26. Tailor C. S., Nouri A., Kabat D. 2000; Cellular and species resistance to murine amphotropic, gibbon ape, and feline subgroup C leukemia viruses is strongly influenced by receptor expression levels and by receptor masking mechanisms. J Virol 74:9797–9801 [CrossRef]
    [Google Scholar]
  27. Tailor C. S., Lavilette D., Martin M., Kabat D. 2003; Cell surface receptors for gamma retroviruses. Curr Top Microbiol Immunol 281:29–106
    [Google Scholar]
  28. Takase-Yoden S., Watanabe R. 1999; Contribution of virus–receptor interaction to distinct viral proliferation of neuropathogenic and non-neuropathogenic murine leukemia viruses in rat glial cells. J Virol 73:4461–4464
    [Google Scholar]
  29. Tavoloni N., Rudenholz A. 1997; Variable transduction efficiency of murine leukemia retroviral vector on mammalian cells: role of cellular glycosylation. Virology 229:49–56 [CrossRef]
    [Google Scholar]
  30. Wang H., Kavanaugh M. P., North R. A., Kabat D. 1991; Cell-surface receptor for ecotropic murine retroviruses is a basic amino acid transporter. Nature 352:729–731 [CrossRef]
    [Google Scholar]
  31. Wang H., Klamo E., Kuhmann S. E., Kozak S. L., Kavanaugh M. P., Kabat D. 1996; Modulation of ecotropic murine retroviruses by N -linked glycosylation of the cell surface receptor/amino acid transporter. J Virol 70:6884–6891
    [Google Scholar]
  32. Wilson C. A., Eiden M. V. 1991; Viral and cellular factors governing hamster cell infection by murine leukemia and gibbon ape leukemia viruses. J Virol 65:5975–5982
    [Google Scholar]
  33. Yoshimoto T., Yoshimoto E., Meruelo D. 1991; Molecular cloning and characterization of a novel human gene homologous to the murine ecotropic retrovirus receptor. Virology 185:10–17 [CrossRef]
    [Google Scholar]
  34. Yoshimoto T., Yoshimoto E., Meruelo D. 1993; Identification of amino acid residues critical for infection with ecotropic murine leukemia retrovirus. J Virol 67:1310–1314
    [Google Scholar]
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