Skip to main content
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
. 1978 Dec;75(12):5812–5816. doi: 10.1073/pnas.75.12.5812

Recombination between viral and cellular sequences generates transforming sarcoma virus

L-H Wang 1, C C Halpern 1, M Nadel 1, H Hanafusa 1
PMCID: PMC393065  PMID: 215998

Abstract

A series of sarcoma viruses has been obtained from tumors induced by transformation-defective (td) mutants of the Schmidt-Ruppin strain of Rous sarcoma virus, subgroup A (SR-A). The RNA sequences of these “recovered avian sarcoma viruses” (rASVs) were compared with those of td mutants and of SR-A by oligonucleotide fingerprinting. Of six sarcoma-specific oligonucleotides present in SR-A RNA, three to six were missing in the RNAs of the four td mutants examined. All six isolates of rASV examined have regained these six oligonucleotides. In addition, most rASV RNAs have three new oligonucleotides not present in the RNA either of td mutants or of SR-A. The newly obtained oligonucleotides are located between 800 and 2600 nucleotides from the 3′ end of rASV RNA, which corresponds to the src region of SR-A RNA mapped previously. Furthermore, viral RNAs of two td mutants isolated from a clone of rASV lack most src-specific oligonucleotides, including the three new ones. No differences were found among RNAs of td, SR-A, and rASV in the regions outside of src. Our results indicate that RNA sequences that rASVs have acquired from cells in the process of conversion from td virus to transforming virus are mapped within the src region and segregate with the transforming function. Some of the sequences are new and some are identical with those in SR-A RNA.

Keywords: transformation-defective mutants, recovered avian sarcoma virus, src-specific sequences, oligonucleotide fingerprinting

Full text

PDF
5812

Images in this article

Selected References

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

  1. Baltimore D. Tumor viruses: 1974. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):1187–1200. doi: 10.1101/sqb.1974.039.01.137. [DOI] [PubMed] [Google Scholar]
  2. Coffin J. M., Billeter M. A. A physical map of the Rous sarcoma virus genome. J Mol Biol. 1976 Jan 25;100(3):293–318. doi: 10.1016/s0022-2836(76)80065-4. [DOI] [PubMed] [Google Scholar]
  3. Duesberg P. H., Vogt P. K. RNA species obtained from clonal lines of avian sarcoma and from avian leukosis virus. Virology. 1973 Jul;54(1):207–219. doi: 10.1016/0042-6822(73)90130-x. [DOI] [PubMed] [Google Scholar]
  4. Frankel A. E., Fischinger P. J. Nucleotide sequences in mouse DNA and RNA specific for Moloney sarcoma virus. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3705–3709. doi: 10.1073/pnas.73.10.3705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. HARVEY J. J. AN UNIDENTIFIED VIRUS WHICH CAUSES THE RAPID PRODUCTION OF TUMOURS IN MICE. Nature. 1964 Dec 12;204:1104–1105. doi: 10.1038/2041104b0. [DOI] [PubMed] [Google Scholar]
  6. Hanafusa H., Halpern C. C., Buchhagen D. L., Kawai S. Recovery of avian sarcoma virus from tumors induced by transformation-defective mutants. J Exp Med. 1977 Dec 1;146(6):1735–1747. doi: 10.1084/jem.146.6.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hanafusa H. Rapid transformation of cells by Rous sarcoma virus. Proc Natl Acad Sci U S A. 1969 Jun;63(2):318–325. doi: 10.1073/pnas.63.2.318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hayward W. S. Size and genetic content of viral RNAs in avian oncovirus-infected cells. J Virol. 1977 Oct;24(1):47–63. doi: 10.1128/jvi.24.1.47-63.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Kawai S., Duesberg P. H., Hanafusa H. Transformation-defective mutants of Rous sarcoma virus with src gene deletions of varying length. J Virol. 1977 Dec;24(3):910–914. doi: 10.1128/jvi.24.3.910-914.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kawai S., Hanafusa H. Genetic recombination with avian tumor virus. Virology. 1972 Jul;49(1):37–44. doi: 10.1016/s0042-6822(72)80005-9. [DOI] [PubMed] [Google Scholar]
  12. Lai M. M., Hu S. S., Vogt P. K. Occurrence of partial deletion and substitution of the src gene in the RNA genome of avian sarcoma virus. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4781–4785. doi: 10.1073/pnas.74.11.4781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Moloney J. B. A virus-induced rhabdomyosarcoma of mice. Natl Cancer Inst Monogr. 1966 Sep;22:139–142. [PubMed] [Google Scholar]
  14. Roy-Burman P., Klement V. Derivation of mouse sarcoma virus (Kirsten) by acquisition of genes from heterologous host. J Gen Virol. 1975 Aug;28(2):193–198. doi: 10.1099/0022-1317-28-2-193. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Spector D. H., Baker B., Varmus H. E., Bishop J. M. Characteristics of cellular RNA related to the transforming gene of avian sarcoma viruses. Cell. 1978 Feb;13(2):381–386. doi: 10.1016/0092-8674(78)90206-4. [DOI] [PubMed] [Google Scholar]
  17. Stehelin D., Guntaka R. V., Varmus H. E., Bishop J. M. Purification of DNA complementary to nucleotide sequences required for neoplastic transformation of fibroblasts by avian sarcoma viruses. J Mol Biol. 1976 Mar 5;101(3):349–365. doi: 10.1016/0022-2836(76)90152-2. [DOI] [PubMed] [Google Scholar]
  18. Stehelin D., Varmus H. E., Bishop J. M., Vogt P. K. DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature. 1976 Mar 11;260(5547):170–173. doi: 10.1038/260170a0. [DOI] [PubMed] [Google Scholar]
  19. Vogt P. K. Spontaneous segregation of nontransforming viruses from cloned sarcoma viruses. Virology. 1971 Dec;46(3):939–946. doi: 10.1016/0042-6822(71)90092-4. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Wang L. H., Duesberg P. H., Robins T., Yokota H., Vogt P. K. The terminal oligonucleotides of avian tumor virus RNAs are genetically linked. Virology. 1977 Oct 15;82(2):472–492. doi: 10.1016/0042-6822(77)90020-4. [DOI] [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. Wang S. Y., Hayward W. S., Hanafusa H. Genetic variation in the RNA transcripts of endogenous virus genes in uninfected chicken cells. J Virol. 1977 Oct;24(1):64–73. doi: 10.1128/jvi.24.1.64-73.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yoshida M., Ikawa Y. Induction of some transformation-related properties by a transformation-defective mutant of avian sarcoma virus. Virology. 1977 Dec;83(2):444–448. doi: 10.1016/0042-6822(77)90192-1. [DOI] [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