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. 1993 Sep;67(9):5153–5162. doi: 10.1128/jvi.67.9.5153-5162.1993

Distinct superinfection interference properties yet similar receptor utilization by cytopathic and noncytopathic feline leukemia viruses.

T A Reinhart 1, A K Ghosh 1, E A Hoover 1, J I Mullins 1
PMCID: PMC237913  PMID: 8394443

Abstract

Cell killing by cytopathic retroviruses is often associated with a delay or failure in the establishment of superinfection interference. Superinfection has been observed during T-cell killing and fatal immunodeficiency disease induction by the feline leukemia virus (FeLV) chimera FeLV-FAIDS-EECC, containing the surface envelope glycoprotein (SU) of FeLV-FAIDS clone 61C. We demonstrate here that 61C SU has a defect that results in a nearly complete failure to establish superinfection interference against homologous virus challenge. This failure was evident only in feline T (FeT) cell clones expressing envelope protein, not in the rare cells that have survived cytopathic infection to become chronically infected. The regions of SU responsible for this defect were the same as those previously identified as responsible for T-cell killing. The superinfection interference properties of a noncytophatic molecular clone, FeLV-FAIDS-61E, were different in that 61E established interference to homologous virus challenge, both in SU-expressing cell clones and in chronically infected cells. Neither 61E nor EECC established interference against heterologous virus challenge. Viruses expressing chimeric SU proteins displayed varied and intermediate interference properties. Purified 61E and 61C SU competed for binding sites on FeT cell surfaces, and purified 61E SU blocked infection of virus bearing 61E or 61C SU. In addition, purified 61E and 61C SU each coprecipitated 70-kDa FeT cell surface proteins. Our data are consistent with the hypothesis that there are multiple cellular components necessary for 61E and 61C attachment to and penetration of FeT cells, a primary receptor that is utilized by both 61E and 61C, and secondary receptors that are likely to be virus specific.

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  1. Aizawa S., Suda Y., Furuta Y., Yagi T., Takeda N., Watanabe N., Nagayoshi M., Ikawa Y. Env-derived gp55 gene of Friend spleen focus-forming virus specifically induces neoplastic proliferation of erythroid progenitor cells. EMBO J. 1990 Jul;9(7):2107–2116. doi: 10.1002/j.1460-2075.1990.tb07379.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bole D. G., Hendershot L. M., Kearney J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986 May;102(5):1558–1566. doi: 10.1083/jcb.102.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Clapham P. R., Blanc D., Weiss R. A. Specific cell surface requirements for the infection of CD4-positive cells by human immunodeficiency virus types 1 and 2 and by Simian immunodeficiency virus. Virology. 1991 Apr;181(2):703–715. doi: 10.1016/0042-6822(91)90904-P. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Copeland C. S., Doms R. W., Bolzau E. M., Webster R. G., Helenius A. Assembly of influenza hemagglutinin trimers and its role in intracellular transport. J Cell Biol. 1986 Oct;103(4):1179–1191. doi: 10.1083/jcb.103.4.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Copeland C. S., Zimmer K. P., Wagner K. R., Healey G. A., Mellman I., Helenius A. Folding, trimerization, and transport are sequential events in the biogenesis of influenza virus hemagglutinin. Cell. 1988 Apr 22;53(2):197–209. doi: 10.1016/0092-8674(88)90381-9. [DOI] [PubMed] [Google Scholar]
  6. Crise B., Ruusala A., Zagouras P., Shaw A., Rose J. K. Oligomerization of glycolipid-anchored and soluble forms of the vesicular stomatitis virus glycoprotein. J Virol. 1989 Dec;63(12):5328–5333. doi: 10.1128/jvi.63.12.5328-5333.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Delwart E. L., Panganiban A. T. Role of reticuloendotheliosis virus envelope glycoprotein in superinfection interference. J Virol. 1989 Jan;63(1):273–280. doi: 10.1128/jvi.63.1.273-280.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Donahue P. R., Hoover E. A., Beltz G. A., Riedel N., Hirsch V. M., Overbaugh J., Mullins J. I. Strong sequence conservation among horizontally transmissible, minimally pathogenic feline leukemia viruses. J Virol. 1988 Mar;62(3):722–731. doi: 10.1128/jvi.62.3.722-731.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Donahue P. R., Quackenbush S. L., Gallo M. V., deNoronha C. M., Overbaugh J., Hoover E. A., Mullins J. I. Viral genetic determinants of T-cell killing and immunodeficiency disease induction by the feline leukemia virus FeLV-FAIDS. J Virol. 1991 Aug;65(8):4461–4469. doi: 10.1128/jvi.65.8.4461-4469.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Earl P. L., Doms R. W., Moss B. Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein. Proc Natl Acad Sci U S A. 1990 Jan;87(2):648–652. doi: 10.1073/pnas.87.2.648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Einfeld D., Hunter E. Oligomeric structure of a prototype retrovirus glycoprotein. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8688–8692. doi: 10.1073/pnas.85.22.8688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  13. Gething M. J., McCammon K., Sambrook J. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell. 1986 Sep 12;46(6):939–950. doi: 10.1016/0092-8674(86)90076-0. [DOI] [PubMed] [Google Scholar]
  14. Ghosh A. K., Bachmann M. H., Hoover E. A., Mullins J. I. Identification of a putative receptor for subgroup A feline leukemia virus on feline T cells. J Virol. 1992 Jun;66(6):3707–3714. doi: 10.1128/jvi.66.6.3707-3714.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grant C. K., Ernisse B. J., Jarrett O., Jones F. R. Feline leukemia virus envelope gp70 of subgroups B and C defined by monoclonal antibodies with cytotoxic and neutralizing functions. J Immunol. 1983 Dec;131(6):3042–3048. [PubMed] [Google Scholar]
  16. Haase A. T., Stowring L., Harris J. D., Traynor B., Ventura P., Peluso R., Brahic M. Visna DNA synthesis and the tempo of infection in vitro. Virology. 1982 Jun;119(2):399–410. doi: 10.1016/0042-6822(82)90099-x. [DOI] [PubMed] [Google Scholar]
  17. Hartman S. C., Mulligan R. C. Two dominant-acting selectable markers for gene transfer studies in mammalian cells. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8047–8051. doi: 10.1073/pnas.85.21.8047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Higuchi R., Krummel B., Saiki R. K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 1988 Aug 11;16(15):7351–7367. doi: 10.1093/nar/16.15.7351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Keshet E., Temin H. M. Cell killing by spleen necrosis virus is correlated with a transient accumulation of spleen necrosis virus DNA. J Virol. 1979 Aug;31(2):376–388. doi: 10.1128/jvi.31.2.376-388.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
  22. Kristal B. S., Reinhart T. A., Hoover E. A., Mullins J. I. Interference with superinfection and with cell killing and determination of host range and growth kinetics mediated by feline leukemia virus surface glycoproteins. J Virol. 1993 Jul;67(7):4142–4153. doi: 10.1128/jvi.67.7.4142-4153.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lin A. Y., Devaux B., Green A., Sagerström C., Elliott J. F., Davis M. M. Expression of T cell antigen receptor heterodimers in a lipid-linked form. Science. 1990 Aug 10;249(4969):677–679. doi: 10.1126/science.1696397. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Mullins J. I., Casey J. W., Nicolson M. O., Davidson N. Sequence organization of feline leukemia virus DNA in infected cells. Nucleic Acids Res. 1980 Aug 11;8(15):3287–3305. doi: 10.1093/nar/8.15.3287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mullins J. I., Chen C. S., Hoover E. A. Disease-specific and tissue-specific production of unintegrated feline leukaemia virus variant DNA in feline AIDS. Nature. 1986 Jan 23;319(6051):333–336. doi: 10.1038/319333a0. [DOI] [PubMed] [Google Scholar]
  27. Mullins J. I., Hoover E. A., Quackenbush S. L., Donahue P. R. Disease progression and viral genome variants in experimental feline leukemia virus-induced immunodeficiency syndrome. J Acquir Immune Defic Syndr. 1991;4(6):547–557. [PubMed] [Google Scholar]
  28. O'Brien W. A., Chen I. S., Ho D. D., Daar E. S. Mapping genetic determinants for human immunodeficiency virus type 1 resistance to soluble CD4. J Virol. 1992 May;66(5):3125–3130. doi: 10.1128/jvi.66.5.3125-3130.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Onions D., Jarrett O., Testa N., Frassoni F., Toth S. Selective effect of feline leukaemia virus on early erythroid precursors. Nature. 1982 Mar 11;296(5853):156–158. doi: 10.1038/296156a0. [DOI] [PubMed] [Google Scholar]
  30. Overbaugh J., Donahue P. R., Quackenbush S. L., Hoover E. A., Mullins J. I. Molecular cloning of a feline leukemia virus that induces fatal immunodeficiency disease in cats. Science. 1988 Feb 19;239(4842):906–910. doi: 10.1126/science.2893454. [DOI] [PubMed] [Google Scholar]
  31. Paquette Y., Hanna Z., Savard P., Brousseau R., Robitaille Y., Jolicoeur P. Retrovirus-induced murine motor neuron disease: mapping the determinant of spongiform degeneration within the envelope gene. Proc Natl Acad Sci U S A. 1989 May;86(10):3896–3900. doi: 10.1073/pnas.86.10.3896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pauza C. D., Galindo J. E., Richman D. D. Reinfection results in accumulation of unintegrated viral DNA in cytopathic and persistent human immunodeficiency virus type 1 infection of CEM cells. J Exp Med. 1990 Oct 1;172(4):1035–1042. doi: 10.1084/jem.172.4.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Poss M. L., Mullins J. I., Hoover E. A. Posttranslational modifications distinguish the envelope glycoprotein of the immunodeficiency disease-inducing feline leukemia virus retrovirus. J Virol. 1989 Jan;63(1):189–195. doi: 10.1128/jvi.63.1.189-195.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Poss M. L., Quackenbush S. L., Mullins J. I., Hoover E. A. Characterization and significance of delayed processing of the feline leukemia virus FeLV-FAIDS envelope glycoprotein. J Virol. 1990 Sep;64(9):4338–4345. doi: 10.1128/jvi.64.9.4338-4345.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Quackenbush S. L., Donahue P. R., Dean G. A., Myles M. H., Ackley C. D., Cooper M. D., Mullins J. I., Hoover E. A. Lymphocyte subset alterations and viral determinants of immunodeficiency disease induction by the feline leukemia virus FeLV-FAIDS. J Virol. 1990 Nov;64(11):5465–5474. doi: 10.1128/jvi.64.11.5465-5474.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Resnick-Roguel N., Burstein H., Hamburger J., Panet A., Eldor A., Vlodavsky I., Kotler M. Cytocidal effect caused by the envelope glycoprotein of a newly isolated avian hemangioma-inducing retrovirus. J Virol. 1989 Oct;63(10):4325–4330. doi: 10.1128/jvi.63.10.4325-4330.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Riedel N., Hoover E. A., Dornsife R. E., Mullins J. I. Pathogenic and host range determinants of the feline aplastic anemia retrovirus. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2758–2762. doi: 10.1073/pnas.85.8.2758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Riedel N., Hoover E. A., Gasper P. W., Nicolson M. O., Mullins J. I. Molecular analysis and pathogenesis of the feline aplastic anemia retrovirus, feline leukemia virus C-Sarma. J Virol. 1986 Oct;60(1):242–250. doi: 10.1128/jvi.60.1.242-250.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Robinson H. L., Zinkus D. M. Accumulation of human immunodeficiency virus type 1 DNA in T cells: results of multiple infection events. J Virol. 1990 Oct;64(10):4836–4841. doi: 10.1128/jvi.64.10.4836-4841.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sarma P. S., Log T. Subgroup classification of feline leukemia and sarcoma viruses by viral interference and neutralization tests. Virology. 1973 Jul;54(1):160–169. doi: 10.1016/0042-6822(73)90125-6. [DOI] [PubMed] [Google Scholar]
  41. Shapiro A. L., Viñuela E., Maizel J. V., Jr Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels. Biochem Biophys Res Commun. 1967 Sep 7;28(5):815–820. doi: 10.1016/0006-291x(67)90391-9. [DOI] [PubMed] [Google Scholar]
  42. Shaw G. M., Hahn B. H., Arya S. K., Groopman J. E., Gallo R. C., Wong-Staal F. Molecular characterization of human T-cell leukemia (lymphotropic) virus type III in the acquired immune deficiency syndrome. Science. 1984 Dec 7;226(4679):1165–1171. doi: 10.1126/science.6095449. [DOI] [PubMed] [Google Scholar]
  43. Snyder H. W., Jr, Hardy W. D., Jr, Zuckerman E. E., Fleissner E. Characterisation of a tumour-specific antigen on the surface of feline lymphosarcoma cells. Nature. 1978 Oct 19;275(5681):656–658. doi: 10.1038/275656a0. [DOI] [PubMed] [Google Scholar]
  44. Stevenson M., Meier C., Mann A. M., Chapman N., Wasiak A. Envelope glycoprotein of HIV induces interference and cytolysis resistance in CD4+ cells: mechanism for persistence in AIDS. Cell. 1988 May 6;53(3):483–496. doi: 10.1016/0092-8674(88)90168-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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]
  46. Temin H. M. Mechanisms of cell killing/cytopathic effects by nonhuman retroviruses. Rev Infect Dis. 1988 Mar-Apr;10(2):399–405. doi: 10.1093/clinids/10.2.399. [DOI] [PubMed] [Google Scholar]
  47. Wang H., Paul R., Burgeson R. E., Keene D. R., Kabat D. Plasma membrane receptors for ecotropic murine retroviruses require a limiting accessory factor. J Virol. 1991 Dec;65(12):6468–6477. doi: 10.1128/jvi.65.12.6468-6477.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Weller S. K., Joy A. E., Temin H. M. Correlation between cell killing and massive second-round superinfection by members of some subgroups of avian leukosis virus. J Virol. 1980 Jan;33(1):494–506. doi: 10.1128/jvi.33.1.494-506.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Weller S. K., Temin H. M. Cell killing by avian leukosis viruses. J Virol. 1981 Sep;39(3):713–721. doi: 10.1128/jvi.39.3.713-721.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yewdell J. W., Yellen A., Bächi T. Monoclonal antibodies localize events in the folding, assembly, and intracellular transport of the influenza virus hemagglutinin glycoprotein. Cell. 1988 Mar 25;52(6):843–852. doi: 10.1016/0092-8674(88)90426-6. [DOI] [PubMed] [Google Scholar]

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