Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1985 Mar;53(3):719–726. doi: 10.1128/jvi.53.3.719-726.1985

Recombination between a defective retrovirus and homologous sequences in host DNA: reversion by patch repair.

P Schwartzberg, J Colicelli, S P Goff
PMCID: PMC254699  PMID: 2983084

Abstract

The genomes of mammalian species contain multiple copies of sequences homologous to exogenous retroviruses. When a mutant retrovirus carrying a lethal deletion in an essential viral gene was introduced into mammalian cells, revertant viruses appeared and spread throughout the culture. Analysis of one such revertant showed that the mutation had been repaired by homologous recombination with endogenous sequences. Our results suggest that defective retroviruses can draw upon the genetic complement of the host cell to repair lesions in viral genes.

Full text

PDF
719

Images in this article

720Image
on p.720
721Image
on p.721
724Image
on p.724

Selected References

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

  1. Aaronson S. A., Stephenson J. R. Endogenous type-C RNA viruses of mammalian cells. Biochim Biophys Acta. 1976 Dec 23;458(4):323–354. doi: 10.1016/0304-419x(76)90006-8. [DOI] [PubMed] [Google Scholar]
  2. Aaronson S. A., Todaro G. J., Scolnick E. M. Induction of murine C-type viruses from clonal lines of virus-free BALB-3T3 cells. Science. 1971 Oct 8;174(4005):157–159. doi: 10.1126/science.174.4005.157. [DOI] [PubMed] [Google Scholar]
  3. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  4. Blair D. G. Genetic recombination between avian leukosis and sarcoma viruses. Experimental variables and the frequencies of recombination. Virology. 1977 Apr;77(2):534–544. doi: 10.1016/0042-6822(77)90479-2. [DOI] [PubMed] [Google Scholar]
  5. Bonner T. I., O'Connell C., Cohen M. Cloned endogenous retroviral sequences from human DNA. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4709–4713. doi: 10.1073/pnas.79.15.4709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chattopadhyay S. K., Lander M. R., Gupta S., Rands E., Lowy D. R. Origin of mink cytopathic focus-forming (MCF) viruses:comparison with ecotropic and xenotropic murine leukemia virus genomes. Virology. 1981 Sep;113(2):465–483. doi: 10.1016/0042-6822(81)90175-6. [DOI] [PubMed] [Google Scholar]
  7. Chattopadhyay S. K., Lander M. R., Rands E., Lowy D. R. Structure of endogenous murine leukemia virus DNA in mouse genomes. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5774–5778. doi: 10.1073/pnas.77.10.5774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chattopadhyay S. K., Rowe W. P., Teich N. M., Lowy D. R. Definitive evidence that the murine C-type virus inducing locus Akv-1 is viral genetic material. Proc Natl Acad Sci U S A. 1975 Mar;72(3):906–910. doi: 10.1073/pnas.72.3.906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chiu I. M., Callahan R., Tronick S. R., Schlom J., Aaronson S. A. Major pol gene progenitors in the evolution of oncoviruses. Science. 1984 Jan 27;223(4634):364–370. doi: 10.1126/science.6197754. [DOI] [PubMed] [Google Scholar]
  10. Coffin J. M. Structure, replication, and recombination of retrovirus genomes: some unifying hypotheses. J Gen Virol. 1979 Jan;42(1):1–26. doi: 10.1099/0022-1317-42-1-1. [DOI] [PubMed] [Google Scholar]
  11. Fischinger P. J., Nomura S., Bolognesi D. P. A novel murine oncornavirus with dual eco- and xenotropic properties. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5150–5155. doi: 10.1073/pnas.72.12.5150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gelb L. D., Milstien J. B., Martin M. A., Aaronson S. A. Characterization of murine leukaemia virus-specific DNA present in normal mouse cells. Nat New Biol. 1973 Jul 18;244(133):76–79. doi: 10.1038/newbio244076a0. [DOI] [PubMed] [Google Scholar]
  13. Goff S., Traktman P., Baltimore D. Isolation and properties of Moloney murine leukemia virus mutants: use of a rapid assay for release of virion reverse transcriptase. J Virol. 1981 Apr;38(1):239–248. doi: 10.1128/jvi.38.1.239-248.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  17. Hoggan M. D., Buckler C. E., Sears J. F., Rowe W. P., Martin M. A. Organization and stability of endogenous xenotropic murine leukemia virus proviral DNA in mouse genomes. J Virol. 1983 Jan;45(1):473–477. doi: 10.1128/jvi.45.1.473-477.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hohn B. In vitro packaging of lambda and cosmid DNA. Methods Enzymol. 1979;68:299–309. doi: 10.1016/0076-6879(79)68021-7. [DOI] [PubMed] [Google Scholar]
  19. Jenkins N. A., Copeland N. G., Taylor B. A., Lee B. K. Organization, distribution, and stability of endogenous ecotropic murine leukemia virus DNA sequences in chromosomes of Mus musculus. J Virol. 1982 Jul;43(1):26–36. doi: 10.1128/jvi.43.1.26-36.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Junghans R. P., Boone L. R., Skalka A. M. Retroviral DNA H structures: displacement-assimilation model of recombination. Cell. 1982 Aug;30(1):53–62. doi: 10.1016/0092-8674(82)90011-3. [DOI] [PubMed] [Google Scholar]
  21. Keshet E., Shaul Y., Kaminchik J., Aviv H. Heterogeneity of "virus-like" genes encoding retrovirus-associated 30S RNA and their organization within the mouse genome. Cell. 1980 Jun;20(2):431–439. doi: 10.1016/0092-8674(80)90629-7. [DOI] [PubMed] [Google Scholar]
  22. Khan A. S. Nucleotide sequence analysis establishes the role of endogenous murine leukemia virus DNA segments in formation of recombinant mink cell focus-forming murine leukemia viruses. J Virol. 1984 Jun;50(3):864–871. doi: 10.1128/jvi.50.3.864-871.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Khan A. S., Rowe W. P., Martin M. A. Cloning of endogenous murine leukemia virus-related sequences from chromosomal DNA of BALB/c and AKR/J mice: identification of an env progenitor of AKR-247 mink cell focus-forming proviral DNA. J Virol. 1982 Nov;44(2):625–636. doi: 10.1128/jvi.44.2.625-636.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kopchick J. J., Karshin W. L., Arlinghaus R. B. Tryptic peptide analysis of gag and gag-pol gene products of Rauscher murine leukemia virus. J Virol. 1979 May;30(2):610–623. doi: 10.1128/jvi.30.2.610-623.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Levy J. A. Xenotropic type C viruses. Curr Top Microbiol Immunol. 1978;79:111–213. doi: 10.1007/978-3-642-66853-1_4. [DOI] [PubMed] [Google Scholar]
  26. Lobel L. I., Goff S. P. Construction of mutants of Moloney murine leukemia virus by suppressor-linker insertional mutagenesis: positions of viable insertion mutations. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4149–4153. doi: 10.1073/pnas.81.13.4149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lueders K. K., Kuff E. L. Sequences associated with intracisternal A particles are reiterated in the mouse genome. Cell. 1977 Dec;12(4):963–972. doi: 10.1016/0092-8674(77)90161-1. [DOI] [PubMed] [Google Scholar]
  28. Martin M. A., Bryan T., Rasheed S., Khan A. S. Identification and cloning of endogenous retroviral sequences present in human DNA. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4892–4896. doi: 10.1073/pnas.78.8.4892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Oliff A. I., Hager G. L., Chang E. H., Scolnick E. M., Chan H. W., Lowy D. R. Transfection of molecularly cloned Friend murine leukemia virus DNA yields a highly leukemogenic helper-independent type C virus. J Virol. 1980 Jan;33(1):475–486. doi: 10.1128/jvi.33.1.475-486.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Panganiban A. T., Temin H. M. The terminal nucleotides of retrovirus DNA are required for integration but not virus production. Nature. 1983 Nov 10;306(5939):155–160. doi: 10.1038/306155a0. [DOI] [PubMed] [Google Scholar]
  32. Repaske R., O'Neill R. R., Steele P. E., Martin M. A. Characterization and partial nucleotide sequence of endogenous type C retrovirus segments in human chromosomal DNA. Proc Natl Acad Sci U S A. 1983 Feb;80(3):678–682. doi: 10.1073/pnas.80.3.678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  34. Rowe W. P., Pugh W. E., Hartley J. W. Plaque assay techniques for murine leukemia viruses. Virology. 1970 Dec;42(4):1136–1139. doi: 10.1016/0042-6822(70)90362-4. [DOI] [PubMed] [Google Scholar]
  35. Schwartzberg P., Colicelli J., Goff S. P. Construction and analysis of deletion mutations in the pol gene of Moloney murine leukemia virus: a new viral function required for productive infection. Cell. 1984 Jul;37(3):1043–1052. doi: 10.1016/0092-8674(84)90439-2. [DOI] [PubMed] [Google Scholar]
  36. Schwartzberg P., Colicelli J., Goff S. P. Deletion mutants of Moloney murine leukemia virus which lack glycosylated gag protein are replication competent. J Virol. 1983 May;46(2):538–546. doi: 10.1128/jvi.46.2.538-546.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schwartzberg P., Colicelli J., Gordon M. L., Goff S. P. Mutations in the gag gene of Moloney murine leukemia virus: effects on production of virions and reverse transcriptase. J Virol. 1984 Mar;49(3):918–924. doi: 10.1128/jvi.49.3.918-924.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  39. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  40. Steele R. E., Bakken A. H., Reeder R. H. Plasmids containing mouse rDNA do not recombine with cellular ribosomal genes when introduced into cultured mouse cells. Mol Cell Biol. 1984 Apr;4(4):576–582. doi: 10.1128/mcb.4.4.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Steffen D. L., Mural R., Cowing D., Mielcarz J., Young J., Roblin R. Most of the murine leukemia virus sequences in the DNA of NIH/swiss mice consist of two closely related proviruses, each repeated several times. J Virol. 1982 Jul;43(1):127–135. doi: 10.1128/jvi.43.1.127-135.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Steffen D., Bird S., Rowe W. P., Weinberg R. A. Identification of DNA fragments carrying ecotropic proviruses of AKR mice. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4554–4558. doi: 10.1073/pnas.76.9.4554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Steffen D., Weinberg R. A. The integrated genome of murine leukemia virus. Cell. 1978 Nov;15(3):1003–1010. doi: 10.1016/0092-8674(78)90284-2. [DOI] [PubMed] [Google Scholar]
  44. Teich N., Lowy D. R., Hartley J. W., Rowe W. P. Studies of the mechanism of induction of infectious murine leukemia virus from AKR mouse embryo cell lines by 5-iododeoxyuridine and 5-bromodeoxyuridine. Virology. 1973 Jan;51(1):163–173. doi: 10.1016/0042-6822(73)90376-0. [DOI] [PubMed] [Google Scholar]
  45. Toh H., Hayashida H., Miyata T. Sequence homology between retroviral reverse transcriptase and putative polymerases of hepatitis B virus and cauliflower mosaic virus. 1983 Oct 27-Nov 2Nature. 305(5937):827–829. doi: 10.1038/305827a0. [DOI] [PubMed] [Google Scholar]
  46. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wang L. H., Halpern C. C., Nadel M., Hanafusa H. Recombination between viral and cellular sequences generates transforming sarcoma virus. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5812–5816. doi: 10.1073/pnas.75.12.5812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Weiss R. A., Mason W. S., Vogt P. K. Genetic recombinants and heterozygotes derived from endogenous and exogenous avian RNA tumor viruses. Virology. 1973 Apr;52(2):535–552. doi: 10.1016/0042-6822(73)90349-8. [DOI] [PubMed] [Google Scholar]
  49. Wigler M., Sweet R., Sim G. K., Wold B., Pellicer A., Lacy E., Maniatis T., Silverstein S., Axel R. Transformation of mammalian cells with genes from procaryotes and eucaryotes. Cell. 1979 Apr;16(4):777–785. doi: 10.1016/0092-8674(79)90093-x. [DOI] [PubMed] [Google Scholar]
  50. Wyke J. A., Bell J. G., Beamand J. A. Genetic recombination among temperature-sensitive mutnats of Rous sarcoma virus. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 2):897–905. doi: 10.1101/sqb.1974.039.01.104. [DOI] [PubMed] [Google Scholar]

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

RESOURCES