Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1979 Oct;76(10):5023–5027. doi: 10.1073/pnas.76.10.5023

Structure and specific sequences of avian erythroblastosis virus RNA: Evidence for multiple classes of transforming genes among avian tumor viruses

Klaus Bister 1, Peter H Duesberg 1
PMCID: PMC413071  PMID: 228273

Abstract

Two major RNA species were found in several clonal isolates of avian erythroblastosis virus (AEV) and avian erythroblastosis-associated helper virus (AEAV) complexes: one of 8.7 kilobases (kb), the other of 5.5 kb. The 5.5-kb species was identified as AEV RNA because (i) it was absent from non-transforming AEAV isolated from the same virus complex, (ii) it was present in complexes of AEV and different helper viruses, and (iii) its structure is similar to that of avian acute leukemia viruses of the MC29 group. Molecular hybridization indicated that 54% of AEV RNA is specific and 46% is related to other viruses of the avian tumor virus group, particularly to AEAV, therefore termed group-specific. The genetic structure of AEV RNA was deduced by mapping oligonucleotides representing specific and group-specific sequences and by comparing the resulting map to maps of AEAV and of other avian tumor viruses derived previously. AEV RNA contains a gag gene-related, 5′ group-specific section of 1 kb, an internal AEV-specific section of 3 kb unrelated to any other viral RNA tested, and a 3′ group-specific section of 1.5 kb. The 5′ section of AEV RNA is closely related to analogous 5′ sections of the MC29 group viruses and is homologous with a 5′ RNA section that is part of the gag gene of AEAV. The 3′ section is also shared with AEAV RNA and includes a variant C-oligonucleotide near the 3′ end that is different from the highly conserved counterparts of all other exogenous avian tumor viruses. By analogy with Rous sarcoma virus and the acute leukemia viruses of the MC29 group, the internal specific section of AEV RNA is thought to signal a third class of onc genes in avian tumor viruses. Comparisons with AEAV and the MC29 group viruses suggest that both the 5′ gag-related and the internal specific RNA sections of AEV are necessary for onc gene function.

Keywords: cloning of defective virus, RNA electrophoresis, RNA-DNA hybridization, oligonucleotide fingerprinting, onc genes

Full text

PDF
5024

Images in this article

5025Image
on p.5025

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bishop D. H., Claybrook J. R., Spiegelman S. Electrophoretic separation of viral nucleic acids on polyacrylamide gels. J Mol Biol. 1967 Jun 28;26(3):373–387. doi: 10.1016/0022-2836(67)90310-5. [DOI] [PubMed] [Google Scholar]
  2. Bister K., Hayman M. J., Vogt P. K. Defectiveness of avian myelocytomatosis virus MC29: isolation of long-term nonproducer cultures and analysis of virus-specific polypeptide synthesis. Virology. 1977 Oct 15;82(2):431–448. doi: 10.1016/0042-6822(77)90017-4. [DOI] [PubMed] [Google Scholar]
  3. Bister K., Löliger H. C., Duesberg P. H. Oligoribonucleotide map and protein of CMII: detection of conserved and nonconserved genetic elements in avian acute leukemia viruses CMII, MC29, and MH2. J Virol. 1979 Oct;32(1):208–219. doi: 10.1128/jvi.32.1.208-219.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bister K., Vogt P. K. Genetic analysis of the defectiveness in strain MC29 avian leukosis virus. Virology. 1978 Jul 15;88(2):213–221. doi: 10.1016/0042-6822(78)90278-7. [DOI] [PubMed] [Google Scholar]
  5. CARR J. G. Renal adenocarcinoma induced by fowl leukaemia virus. Br J Cancer. 1956 Jun;10(2):379–383. doi: 10.1038/bjc.1956.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dina D., Beemon K., Duesberg P. The 30S Moloney sarcoma virus RNA contains leukemia virus nucleotide sequences. Cell. 1976 Oct;9(2):299–309. doi: 10.1016/0092-8674(76)90120-3. [DOI] [PubMed] [Google Scholar]
  7. Duesberg P. H., Bister K., Vogt P. K. The RNA of avian acute leukemia virus MC29. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4320–4324. doi: 10.1073/pnas.74.10.4320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Duesberg P. H., Vogt P. K. Avian acute leukemia viruses MC29 and MH2 share specific RNA sequences: evidence for a second class of transforming genes. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1633–1637. doi: 10.1073/pnas.76.4.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Evans L. H., Duesberg P. H., Troxler D. H., Scolnick E. M. Spleen focus-forming Friend virus: identification of genomic RNA and its relationship to helper virus RNA. J Virol. 1979 Jul;31(1):133–146. doi: 10.1128/jvi.31.1.133-146.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Graf T., Beug H. Avian leukemia viruses: interaction with their target cells in vivo and in vitro. Biochim Biophys Acta. 1978 Nov 17;516(3):269–299. doi: 10.1016/0304-419x(78)90011-2. [DOI] [PubMed] [Google Scholar]
  11. Graf T., Royer-Pokora B., Schubert G. E., Beug H. Evidence for the multiple oncogenic potential of cloned leukemia virus: in vitro and in vitro studies with avian erythroblastosis virus. Virology. 1976 Jun;71(2):423–433. doi: 10.1016/0042-6822(76)90370-6. [DOI] [PubMed] [Google Scholar]
  12. Hayman M. J., Royer-Pokora B., Graf T. Defectiveness of avian erythroblastosis virus: synthesis of a 75K gag-related protein. Virology. 1979 Jan 15;92(1):31–45. doi: 10.1016/0042-6822(79)90212-5. [DOI] [PubMed] [Google Scholar]
  13. Ishizaki R., Shimizu T. Heterogeneity of strain R avian (erythroblastosis) virus. Cancer Res. 1970 Dec;30(12):2827–2831. [PubMed] [Google Scholar]
  14. Lai M. M., Duesberg P. H., Horst J., Vogt P. K. Avian tumor virus RNA: a comparison of three sarcoma viruses and their transformation-defective derivatives by oligonucleotide fingerprinting and DNA-RNA hybridization. Proc Natl Acad Sci U S A. 1973 Aug;70(8):2266–2270. doi: 10.1073/pnas.70.8.2266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Maisel J., Klement V., Lai M. M., Ostertag W., Duesberg P. Ribonucleic acid components of murine sarcoma and leukemia viruses. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3536–3540. doi: 10.1073/pnas.70.12.3536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maisel J., Scolnick E. M., Duesberg P. Base sequence differences between the RNA components of Harvey sarcoma virus. J Virol. 1975 Sep;16(3):749–753. doi: 10.1128/jvi.16.3.749-753.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Martin G. S., Duesberg P. H. The a subunit in the RNA of transforming avian tumor viruses. I. Occurrence in different virus strains. II. Spontaneous loss resulting in nontransforming variants. Virology. 1972 Feb;47(2):494–497. doi: 10.1016/0042-6822(72)90287-5. [DOI] [PubMed] [Google Scholar]
  18. Mellon P., Pawson A., Bister K., Martin G. S., Duesberg P. H. Specific RNA sequences and gene products of MC29 avian acute leukemia virus. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5874–5878. doi: 10.1073/pnas.75.12.5874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Scolnick E. M., Howk R. S., Anisowicz A., Peebles P. T., Scher C. D., Parks W. P. Separation of sarcoma virus-specific and leukemia virus-specific genetic sequences of Moloney sarcoma virus. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4650–4654. doi: 10.1073/pnas.72.11.4650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Scolnick E. M., Rands E., Williams D., Parks W. P. Studies on the nucleic acid sequences of Kirsten sarcoma virus: a model for formation of a mammalian RNA-containing sarcoma virus. J Virol. 1973 Sep;12(3):458–463. doi: 10.1128/jvi.12.3.458-463.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sheiness D., Fanshier L., Bishop J. M. Identification of nucleotide sequences which may encode the oncogenic capacity of avian retrovirus MC29. J Virol. 1978 Nov;28(2):600–610. doi: 10.1128/jvi.28.2.600-610.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Shih T. Y., Williams D. R., Weeks M. O., Maryak J. M., Vass W. C., Scolnick E. M. Comparison of the genomic organization of Kirsten and Harvey sarcoma viruses. J Virol. 1978 Jul;27(1):45–55. doi: 10.1128/jvi.27.1.45-55.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Wang L. H., Duesberg P., Beemon K., Vogt P. K. Mapping RNase T1-resistant oligonucleotides of avian tumor virus RNAs: sarcoma-specific oligonucleotides are near the poly(A) end and oligonucleotides common to sarcoma and transformation-defective viruses are at the poly(A) end. J Virol. 1975 Oct;16(4):1051–1070. doi: 10.1128/jvi.16.4.1051-1070.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wang L. H., Duesberg P., Mellon P., Vogt P. K. Distribution of envelope-specific and sarcoma-specific nucleotide sequences from different parents in the RNAs of avian tumor virus recombinants. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1073–1077. doi: 10.1073/pnas.73.4.1073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wang L., Galehouse D., Mellon P., Duesberg P., Mason W. S., Vogt P. K. Mapping oligonucleotides of Rous sarcoma virus RNA that segregate with polymerase and group-specific antigen markers in recombinants. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3952–3956. doi: 10.1073/pnas.73.11.3952. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES