Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1974 Feb;13(2):331–339. doi: 10.1128/jvi.13.2.331-339.1974

Acquisition of New DNA Sequences After Infection of Chicken Cells with Avian Myeloblastosis Virus

M Shoyab 1, M A Baluda 1, R Evans 1
PMCID: PMC355301  PMID: 16789139

Abstract

DNA-RNA hybridization studies between 70S RNA from avian myeloblastosis virus (AMV) and an excess of DNA from (i) AMV-induced leukemic chicken myeloblasts or (ii) a mixture of normal and of congenitally infected K-137 chicken embryos producing avian leukosis viruses revealed the presence of fast- and slow-hybridizing virus-specific DNA sequences. However, the leukemic cells contained twice the level of AMV-specific DNA sequences observed in normal chicken embryonic cells. The fast-reacting sequences were two to three times more numerous in leukemic DNA than in DNA from the mixed embryos. The slow-reacting sequences had a reiteration frequency of approximately 9 and 6, in the two respective systems. Both the fast- and the slow-reacting DNA sequences in leukemic cells exhibited a higher Tm (2 C) than the respective DNA sequences in normal cells. In normal and leukemic cells the slow hybrid sequences appeared to have a Tm which was 2 C higher than that of the fast hybrid sequences. Individual non-virus-producing chicken embryos, either group-specific antigen positive or negative, contained 40 to 100 copies of the fast sequences and 2 to 6 copies of the slowly hybridizing sequences per cell genome. Normal rat cells did not contain DNA that hybridized with AMV RNA, whereas non-virus-producing rat cells transformed by B-77 avian sarcoma virus contained only the slowly reacting sequences. The results demonstrate that leukemic cells transformed by AMV contain new AMV-specific DNA sequences which were not present before infection.

Full text

PDF
331

Selected References

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

  1. Altaner C., Temin H. M. Carcinogenesis by RNA sarcoma viruses. XII. A quantitative study of infection of rat cells in vitro by avian sarcoma viruses. Virology. 1970 Jan;40(1):118–134. doi: 10.1016/0042-6822(70)90384-3. [DOI] [PubMed] [Google Scholar]
  2. Baluda M. A., Drohan W. N. Distribution of deoxyribonucleic acid complementary to the ribonucleic acid of avian myeloblastosis virus in tissues of normal and tumor-bearing chickens. J Virol. 1972 Nov;10(5):1002–1009. doi: 10.1128/jvi.10.5.1002-1009.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baluda M. A., Nayak D. P. DNA complementary to viral RNA in leukemic cells induced by avian myeloblastosis virus. Proc Natl Acad Sci U S A. 1970 Jun;66(2):329–336. doi: 10.1073/pnas.66.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baluda M. A., Nayak D. P. Incorporation of precursors into ribonucleic acid, protein, glycoprotein, and lipoprotein of avian myeloblastosis virions. J Virol. 1969 Nov;4(5):554–566. doi: 10.1128/jvi.4.5.554-566.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baluda M. A. The role of the bursa-dependent lymphoid tissue in oncogenesis by avian myeloblastosis virus. Virology. 1967 Jul;32(3):428–437. doi: 10.1016/0042-6822(67)90294-2. [DOI] [PubMed] [Google Scholar]
  6. Baluda M. A. Widespread presence, in chickens, of DNA complementary to the RNA genome of avian leukosis viruses. Proc Natl Acad Sci U S A. 1972 Mar;69(3):576–580. doi: 10.1073/pnas.69.3.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bishop J. O. DNA-RNA hybridization. Acta Endocrinol Suppl (Copenh) 1972;168:247–276. doi: 10.1530/acta.0.071s247. [DOI] [PubMed] [Google Scholar]
  8. Bishop J. O. Molecular hybridization of ribonucleic acid with a large excess of deoxyribonucleic acid. Biochem J. 1972 Jan;126(1):171–185. doi: 10.1042/bj1260171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Britten R. J., Kohne D. E. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science. 1968 Aug 9;161(3841):529–540. doi: 10.1126/science.161.3841.529. [DOI] [PubMed] [Google Scholar]
  10. Burgess R. R. A new method for the large scale purification of Escherichia coli deoxyribonucleic acid-dependent ribonucleic acid polymerase. J Biol Chem. 1969 Nov 25;244(22):6160–6167. [PubMed] [Google Scholar]
  11. CHAMBERLIN M., BERG P. MECHANISM OF RNA POLYMERASE ACTION: FORMATION OF DNA-RNA HYBRIDS WITH SINGLE-STRANDED TEMPLATES. J Mol Biol. 1964 Feb;8:297–313. doi: 10.1016/s0022-2836(64)80139-x. [DOI] [PubMed] [Google Scholar]
  12. Church R. B., Brown I. R. Tissue specificity of genetic transcription. Results Probl Cell Differ. 1972;3:11–24. doi: 10.1007/978-3-540-37149-6_2. [DOI] [PubMed] [Google Scholar]
  13. Coffin J. M. Rescue of rous sarcoma virus from rous sarcoma virus-transformed mammalian cells. J Virol. 1972 Jul;10(1):153–156. doi: 10.1128/jvi.10.1.153-156.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gelderman A. H., Rake A. V., Britten R. J. Transcription of nonrepeated DNA in neonatal and fetal mice. Proc Natl Acad Sci U S A. 1971 Jan;68(1):172–176. doi: 10.1073/pnas.68.1.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hanafusa T., Hanafusa H. Isolation of leukosis-type virus from pheasant embryo cells: possible presence of viral genes in cells. Virology. 1973 Jan;51(1):247–251. doi: 10.1016/0042-6822(73)90388-7. [DOI] [PubMed] [Google Scholar]
  16. Harel L., Harel J., Frezouls G. DNA copies of viral RNA in rat cells transformed by Rous sarcoma virus (RSV). Biochem Biophys Res Commun. 1972 Aug 21;48(4):796–801. doi: 10.1016/0006-291x(72)90677-8. [DOI] [PubMed] [Google Scholar]
  17. Hayward W. S., Hanafusa H. Detection of avian tumor virus RNA in uninfected chicken embryo cells. J Virol. 1973 Feb;11(2):157–167. doi: 10.1128/jvi.11.2.157-167.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Laird C. D. Chromatid structure: relationship between DNA content and nucleotide sequence diversity. Chromosoma. 1971 Mar 16;32(4):378–406. doi: 10.1007/BF00285251. [DOI] [PubMed] [Google Scholar]
  19. MCCARTHY B. J., BOLTON E. T. INTERACTION OF COMPLEMENTARY RNA AND DNA. J Mol Biol. 1964 Feb;8:184–200. doi: 10.1016/s0022-2836(64)80128-5. [DOI] [PubMed] [Google Scholar]
  20. McCarthy B. J., Church R. B. The specificity of molecular hybridization reactions. Annu Rev Biochem. 1970;39:131–150. doi: 10.1146/annurev.bi.39.070170.001023. [DOI] [PubMed] [Google Scholar]
  21. Melli M., Whitfield C., Rao K. V., Richardson M., Bishop J. O. DNA-RNA hybridization in vast DNA excess. Nat New Biol. 1971 May 5;231(18):8–12. [PubMed] [Google Scholar]
  22. Neiman P. E. Measurement of endogenous leukosis virus nucleotide sequences in the DNA of normal avian embryos by RNA-DNA hybridization. Virology. 1973 May;53(1):196–203. doi: 10.1016/0042-6822(73)90478-9. [DOI] [PubMed] [Google Scholar]
  23. Neiman P. E. Rous sarcoma virus nucleotide sequences in cellular DNA: measurement by RNA-DNA hybridization. Science. 1972 Nov 17;178(4062):750–753. doi: 10.1126/science.178.4062.750. [DOI] [PubMed] [Google Scholar]
  24. Niyogi S. K. The influence of chain length and base composition on the specific association of oligoribonucleotides with denatured deoxyribonucleic acid. J Biol Chem. 1969 Mar 25;244(6):1576–1581. [PubMed] [Google Scholar]
  25. Robinson W. S., Baluda M. A. The nucleic acid from avian myeloblastosis virus compared with the RNA from the Bryan strain of Rous sarcoma virus. Proc Natl Acad Sci U S A. 1965 Dec;54(6):1686–1692. doi: 10.1073/pnas.54.6.1686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rosenthal P. N., Robinson H. L., Robinson W. S., Hanafusa T., Hanafusa H. DNA in uninfected and virus-infected cells complementary to avian tumor virus RNA. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2336–2340. doi: 10.1073/pnas.68.10.2336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. SINSHEIMER R. L., LAWRENCE M. IN VITRO SYNTHESIS AND PROPERTIES OF A PHI-X DNA-RNA HYBRID. J Mol Biol. 1964 Feb;8:289–296. doi: 10.1016/s0022-2836(64)80138-8. [DOI] [PubMed] [Google Scholar]
  28. STUDIER F. W. SEDIMENTATION STUDIES OF THE SIZE AND SHAPE OF DNA. J Mol Biol. 1965 Feb;11:373–390. doi: 10.1016/s0022-2836(65)80064-x. [DOI] [PubMed] [Google Scholar]
  29. SVOBODA J. Presence of chicken tumour virus in the sarcoma of the adult rat inoculated after birth with Rous sarcoma tissue. Nature. 1960 Jun 18;186:980–981. doi: 10.1038/186980b0. [DOI] [PubMed] [Google Scholar]
  30. Temin H. M. Mechanism of cell transformation by RNA tumor viruses. Annu Rev Microbiol. 1971;25:609–648. doi: 10.1146/annurev.mi.25.100171.003141. [DOI] [PubMed] [Google Scholar]
  31. Varmus H. E., Bishop J. M., Vogt P. K. Appearance of virus-specific DNA in mammalian cells following transformation by Rous sarcoma virus. J Mol Biol. 1973 Mar 15;74(4):613–626. doi: 10.1016/0022-2836(73)90052-1. [DOI] [PubMed] [Google Scholar]
  32. Weiss R. A., Friis R. R., Katz E., Vogt P. K. Induction of avian tumor viruses in normal cells by physical and chemical carcinogens. Virology. 1971 Dec;46(3):920–938. doi: 10.1016/0042-6822(71)90091-2. [DOI] [PubMed] [Google Scholar]
  33. Wetmur J. G., Davidson N. Kinetics of renaturation of DNA. J Mol Biol. 1968 Feb 14;31(3):349–370. doi: 10.1016/0022-2836(68)90414-2. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES