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. 1988 Jan;62(1):75–83. doi: 10.1128/jvi.62.1.75-83.1988

The avian retrovirus env gene family: molecular analysis of host range and antigenic variants.

C A Bova 1, J C Olsen 1, R Swanstrom 1
PMCID: PMC250503  PMID: 2824857

Abstract

The nucleotide sequence of the env gp85-coding domain from two avian sarcoma and leukosis retrovirus isolates was determined to identify host range and antigenic determinants. The predicted amino acid sequence of gp85 from a subgroup D virus isolate of the Schmidt-Ruppin strain of Rous sarcoma virus was compared with the previously reported sequences of subgroup A, B, C, and E avian sarcoma and leukosis retroviruses. Subgroup D viruses are closely related to the subgroup B viruses but have an extended host range that includes the ability to penetrate certain mammalian cells. There are 27 amino acid differences shared between the subgroup D sequence and three subgroup B sequences. At 16 of these sites, the subgroup D sequence is identical to the sequence of one or more of the other subgroup viruses (A, C, and E). The remaining 11 sites are specific to subgroup D and show some clustering in the two large variable regions that are thought to be major determinants of host range. Biological analysis of recombinant viruses containing a dominant selectable marker confirmed the role of the gp85-coding domain in determining the host range of the subgroup D virus in the infection of mammalian cells. We also compared the sequence of the gp85-coding domain from two subgroup A viruses, Rous-associated virus type 1 and a subgroup A virus of the Schmidt-Ruppin strain of Rous sarcoma virus. The comparison revealed 24 nonconservative amino acid changes, of which 6 result in changes in potential glycosylation sites. The positions of 10 amino acid differences are coincident with the positions of 10 differences found between two subgroup B virus env gene sequences. These 10 sites identify seven domains in the sequence which may constitute determinants of type-specific antigenicity. Using a molecular recombinant, we demonstrated that type-specific neutralization of two subgroup A viruses was associated with the gp85-coding domain of the virus.

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Selected References

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  1. Bauer H., Graf T. Evidence for the possible existence of two envelope antigenic determinants and corresponding cell receptors for avian tumor viruses. Virology. 1969 Jan;37(1):157–161. doi: 10.1016/0042-6822(69)90322-5. [DOI] [PubMed] [Google Scholar]
  2. Benn S., Rutledge R., Folks T., Gold J., Baker L., McCormick J., Feorino P., Piot P., Quinn T., Martin M. Genomic heterogeneity of AIDS retroviral isolates from North America and Zaire. Science. 1985 Nov 22;230(4728):949–951. doi: 10.1126/science.2997922. [DOI] [PubMed] [Google Scholar]
  3. Berstine E. G., Hooper M. L., Grandchamp S., Ephrussi B. Alkaline phosphatase activity in mouse teratoma. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3899–3903. doi: 10.1073/pnas.70.12.3899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bigner D. D., Bigner S. H., Pontén J., Westermark B., Mahaley M. S., Ruoslahti E., Herschman H., Eng L. F., Wikstrand C. J. Heterogeneity of Genotypic and phenotypic characteristics of fifteen permanent cell lines derived from human gliomas. J Neuropathol Exp Neurol. 1981 May;40(3):201–229. doi: 10.1097/00005072-198105000-00001. [DOI] [PubMed] [Google Scholar]
  5. Boettiger D., Love D. N., Weiss R. A. Virus envelope markers in mammalian tropism of avian RNA tumor viruses. J Virol. 1975 Jan;15(1):108–114. doi: 10.1128/jvi.15.1.108-114.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bolognesi D. P., Bauer H., Gelderblom H., Hüper G. Polypeptides of avian RNA tumor viruses. IV. Components of the viral envelope. Virology. 1972 Mar;47(3):551–566. doi: 10.1016/0042-6822(72)90545-4. [DOI] [PubMed] [Google Scholar]
  7. Bova C. A., Manfredi J. P., Swanstrom R. env genes of avian retroviruses: nucleotide sequence and molecular recombinants define host range determinants. Virology. 1986 Jul 30;152(2):343–354. doi: 10.1016/0042-6822(86)90137-6. [DOI] [PubMed] [Google Scholar]
  8. Buchhagen D. L., Hanafusa H. Intracellular precursors to the major glycoprotein of avian oncoviruses in chicken embryo fibroblasts. J Virol. 1978 Mar;25(3):845–851. doi: 10.1128/jvi.25.3.845-851.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. CRITTENDEN L. B., OKAZAKI W., REAMER R. GENETIC RESISTANCE TO ROUS SARCOMA VIRUS IN EMBRYO CELL CULTURES AND EMBRYOS. Virology. 1963 Jul;20:541–544. doi: 10.1016/0042-6822(63)90107-7. [DOI] [PubMed] [Google Scholar]
  10. Clements J. E., Pedersen F. S., Narayan O., Haseltine W. A. Genomic changes associated with antigenic variation of visna virus durig persistent infection. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4454–4458. doi: 10.1073/pnas.77.8.4454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Coffin J. M., Champion M., Chabot F. Nucleotide sequence relationships between the genomes of an endogenous and an exogenous avian tumor virus. J Virol. 1978 Dec;28(3):972–991. doi: 10.1128/jvi.28.3.972-991.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Colbère-Garapin F., Horodniceanu F., Kourilsky P., Garapin A. C. A new dominant hybrid selective marker for higher eukaryotic cells. J Mol Biol. 1981 Jul 25;150(1):1–14. doi: 10.1016/0022-2836(81)90321-1. [DOI] [PubMed] [Google Scholar]
  13. Crittenden L. B., Stone H. A., Reamer R. H., Okazaki W. Two loci controlling genetic cellular resistance to avian leukosis-sarcoma viruses. J Virol. 1967 Oct;1(5):898–904. doi: 10.1128/jvi.1.5.898-904.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dorner A. J., Coffin J. M. Determinants for receptor interaction and cell killing on the avian retrovirus glycoprotein gp85. Cell. 1986 May 9;45(3):365–374. doi: 10.1016/0092-8674(86)90322-3. [DOI] [PubMed] [Google Scholar]
  15. Dorner A. J., Stoye J. P., Coffin J. M. Molecular basis of host range variation in avian retroviruses. J Virol. 1985 Jan;53(1):32–39. doi: 10.1128/jvi.53.1.32-39.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Duesberg P. H., Martin G. S., Vogt P. K. Glycoprotein components of avian and murine RNA tumor viruses. Virology. 1970 Aug;41(4):631–646. doi: 10.1016/0042-6822(70)90428-9. [DOI] [PubMed] [Google Scholar]
  17. Duff R. G., Vogt P. K. Characteristics of two new avian tumor virus subgroups. Virology. 1969 Sep;39(1):18–30. doi: 10.1016/0042-6822(69)90344-4. [DOI] [PubMed] [Google Scholar]
  18. Edwards M. K., McBurney M. W. The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev Biol. 1983 Jul;98(1):187–191. doi: 10.1016/0012-1606(83)90348-2. [DOI] [PubMed] [Google Scholar]
  19. England J. M., Bolognesi D. P., Dietzschold B., Halpern M. S. Evidence that a precursor glycoprotein is cleaved to yield the major glycoprotein of avian tumor virus. J Virol. 1977 Feb;21(2):810–814. doi: 10.1128/jvi.21.2.810-814.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Giard D. J., Aaronson S. A., Todaro G. J., Arnstein P., Kersey J. H., Dosik H., Parks W. P. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst. 1973 Nov;51(5):1417–1423. doi: 10.1093/jnci/51.5.1417. [DOI] [PubMed] [Google Scholar]
  21. Glaser R., Rapp F. Rescue of Epstein-Barr virus from somatic cell hybrids of Burkitt lymphoblastoid cells. J Virol. 1972 Aug;10(2):288–296. doi: 10.1128/jvi.10.2.288-296.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gluzman Y. SV40-transformed simian cells support the replication of early SV40 mutants. Cell. 1981 Jan;23(1):175–182. doi: 10.1016/0092-8674(81)90282-8. [DOI] [PubMed] [Google Scholar]
  23. Hanafusa H., Hanafusa T. Determining factor in the capacity of Rous sarcoma virus to induce tumors in mammals. Proc Natl Acad Sci U S A. 1966 Mar;55(3):532–538. doi: 10.1073/pnas.55.3.532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hanafusa T., Hanafusa H., Miyamoto T. Recovery of a new virus from apparently normal chick cells by infection with avian tumor viruses. Proc Natl Acad Sci U S A. 1970 Dec;67(4):1797–1803. doi: 10.1073/pnas.67.4.1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hayman M. Synthesis and processing of avian sarcoma virus glycoproteins. Virology. 1978 Apr;85(2):475–486. doi: 10.1016/0042-6822(78)90454-3. [DOI] [PubMed] [Google Scholar]
  26. Hughes S., Kosik E. Mutagenesis of the region between env and src of the SR-A strain of Rous sarcoma virus for the purpose of constructing helper-independent vectors. Virology. 1984 Jul 15;136(1):89–99. doi: 10.1016/0042-6822(84)90250-2. [DOI] [PubMed] [Google Scholar]
  27. Hunter E., Hill E., Hardwick M., Bhown A., Schwartz D. E., Tizard R. Complete sequence of the Rous sarcoma virus env gene: identification of structural and functional regions of its product. J Virol. 1983 Jun;46(3):920–936. doi: 10.1128/jvi.46.3.920-936.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ishizaki R., Vogt P. K. Immunological relationships among envelope antigens of avian tumor viruses. Virology. 1966 Nov;30(3):375–387. doi: 10.1016/0042-6822(66)90116-4. [DOI] [PubMed] [Google Scholar]
  29. Joho R. H., Billeter M. A., Weissmann C. Mapping of biological functions on RNA of avian tumor viruses: location of regions required for transformation and determination of host range. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4772–4776. doi: 10.1073/pnas.72.12.4772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. KIT S., DUBBS D. R., PIEKARSKI L. J., HSU T. C. DELETION OF THYMIDINE KINASE ACTIVITY FROM L CELLS RESISTANT TO BROMODEOXYURIDINE. Exp Cell Res. 1963 Aug;31:297–312. doi: 10.1016/0014-4827(63)90007-7. [DOI] [PubMed] [Google Scholar]
  31. Kan N. C., Baluda M. A., Papas T. S. Sites of recombination between the transforming gene of avian myeloblastosis virus and its helper virus. Virology. 1985 Sep;145(2):323–329. doi: 10.1016/0042-6822(85)90166-7. [DOI] [PubMed] [Google Scholar]
  32. Kawai S., Nishizawa M. New procedure for DNA transfection with polycation and dimethyl sulfoxide. Mol Cell Biol. 1984 Jun;4(6):1172–1174. doi: 10.1128/mcb.4.6.1172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Klemenz R., Diggelmann H. The generation of the two envelope glycoproteins of Rous sarcoma virus from a common precursor polypeptide. Virology. 1978 Mar;85(1):63–74. doi: 10.1016/0042-6822(78)90411-7. [DOI] [PubMed] [Google Scholar]
  34. Leamnson R. N., Halpern M. S. Subunit structure of the glycoprotein complex of avian tumor virus. J Virol. 1976 Jun;18(3):956–968. doi: 10.1128/jvi.18.3.956-968.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  36. Modrow S., Hahn B. H., Shaw G. M., Gallo R. C., Wong-Staal F., Wolf H. Computer-assisted analysis of envelope protein sequences of seven human immunodeficiency virus isolates: prediction of antigenic epitopes in conserved and variable regions. J Virol. 1987 Feb;61(2):570–578. doi: 10.1128/jvi.61.2.570-578.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Moelling K., Hayami M. Analysis of precursors to the envelope glycoproteins of avian RNA tumor viruses in chicken and quail cells. J Virol. 1977 Jun;22(3):598–607. doi: 10.1128/jvi.22.3.598-607.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Moscovici C., Moscovici M. G., Jimenez H., Lai M. M., Hayman M. J., Vogt P. K. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell. 1977 May;11(1):95–103. doi: 10.1016/0092-8674(77)90320-8. [DOI] [PubMed] [Google Scholar]
  39. PAYNE L. N., BIGGS P. M. DIFFERENCES BETWEEN HIGHLY INBRED LINES OF CHICKENS IN THE RESPONSE TO ROUS SARCOMA VIRUS OF THE CHORIOALLANTOIC MEMBRANE AND OF EMBRYONIC CELLS IN TISSUE CULTURE. Virology. 1964 Dec;24:610–616. doi: 10.1016/0042-6822(64)90215-6. [DOI] [PubMed] [Google Scholar]
  40. Rogers G. N., Paulson J. C., Daniels R. S., Skehel J. J., Wilson I. A., Wiley D. C. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature. 1983 Jul 7;304(5921):76–78. doi: 10.1038/304076a0. [DOI] [PubMed] [Google Scholar]
  41. SVOBODA J. Further findings on the induction of tumors by Rous sarcoma in rats and on the Rous virus-producing capacity of one of the induced tumours (XC) in chicks. Folia Biol (Praha) 1962;8:215–220. [PubMed] [Google Scholar]
  42. Salinovich O., Payne S. L., Montelaro R. C., Hussain K. A., Issel C. J., Schnorr K. L. Rapid emergence of novel antigenic and genetic variants of equine infectious anemia virus during persistent infection. J Virol. 1986 Jan;57(1):71–80. doi: 10.1128/jvi.57.1.71-80.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Schwartz D. E., Tizard R., Gilbert W. Nucleotide sequence of Rous sarcoma virus. Cell. 1983 Mar;32(3):853–869. doi: 10.1016/0092-8674(83)90071-5. [DOI] [PubMed] [Google Scholar]
  45. Sealy L., Privalsky M. L., Moscovici G., Moscovici C., Bishop J. M. Site-specific mutagenesis of avian erythroblastosis virus: erb-B is required for oncogenicity. Virology. 1983 Oct 15;130(1):155–178. doi: 10.1016/0042-6822(83)90125-3. [DOI] [PubMed] [Google Scholar]
  46. Shalloway D., Zelenetz A. D., Cooper G. M. Molecular cloning and characterization of the chicken gene homologous to the transforming gene of Rous sarcoma virus. Cell. 1981 May;24(2):531–541. doi: 10.1016/0092-8674(81)90344-5. [DOI] [PubMed] [Google Scholar]
  47. Skehel J. J., Stevens D. J., Daniels R. S., Douglas A. R., Knossow M., Wilson I. A., Wiley D. C. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1779–1783. doi: 10.1073/pnas.81.6.1779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Southern P. J., Berg P. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. J Mol Appl Genet. 1982;1(4):327–341. [PubMed] [Google Scholar]
  49. Starcich B. R., Hahn B. H., Shaw G. M., McNeely P. D., Modrow S., Wolf H., Parks E. S., Parks W. P., Josephs S. F., Gallo R. C. Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS. Cell. 1986 Jun 6;45(5):637–648. doi: 10.1016/0092-8674(86)90778-6. [DOI] [PubMed] [Google Scholar]
  50. Steck F. T., Rubin H. The mechanism of interference between an avian leukosis virus and Rous sarcoma virus. II. Early steps of infection by RSV of cells under conditions of interference. Virology. 1966 Aug;29(4):642–653. doi: 10.1016/0042-6822(66)90288-1. [DOI] [PubMed] [Google Scholar]
  51. Tabin C. J., Hoffmann J. W., Goff S. P., Weinberg R. A. Adaptation of a retrovirus as a eucaryotic vector transmitting the herpes simplex virus thymidine kinase gene. Mol Cell Biol. 1982 Apr;2(4):426–436. doi: 10.1128/mcb.2.4.426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Tereba A., Murti K. G. A very sensitive biochemical assay for detecting and quantitating avian oncornaviruses. Virology. 1977 Jul 1;80(1):166–176. doi: 10.1016/0042-6822(77)90389-0. [DOI] [PubMed] [Google Scholar]
  53. Toyoshima K., Vogt P. K. Enhancement and inhibition of avian sarcoma viruses by polycations and polyanions. Virology. 1969 Jul;38(3):414–426. doi: 10.1016/0042-6822(69)90154-8. [DOI] [PubMed] [Google Scholar]
  54. Tozawa H., Bauer H., Graf T., Gelderblom H. Strain-specific antigen of the avian leukosis sarcoma virus group. I. Isolation and immunological characterization. Virology. 1970 Mar;40(3):530–539. doi: 10.1016/0042-6822(70)90196-0. [DOI] [PubMed] [Google Scholar]
  55. Wang L. H., Duesberg P. H., Kawai S., Hanafusa H. Location of envelope-specific and sarcoma-specific oligonucleotides on RNA of Schmidt-Ruppin Rous sarcoma virus. Proc Natl Acad Sci U S A. 1976 Feb;73(2):447–451. doi: 10.1073/pnas.73.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Wiley D. C., Wilson I. A., Skehel J. J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature. 1981 Jan 29;289(5796):373–378. doi: 10.1038/289373a0. [DOI] [PubMed] [Google Scholar]
  57. ZIMMERMAN H. M. The nature of gliomas as revealed by animal experimentation. Am J Pathol. 1955 Jan-Feb;31(1):1–29. [PMC free article] [PubMed] [Google Scholar]

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