Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1983 Sep;47(3):434–441. doi: 10.1128/jvi.47.3.434-441.1983

Molecular cloning of the unintegrated squirrel monkey retrovirus genome: organization and distribution of related sequences in primate DNAs.

I M Chiu, P R Andersen, S A Aaronson, S R Tronick
PMCID: PMC255284  PMID: 6312076

Abstract

The closed circular form of the endogenous squirrel monkey type D retrovirus (SMRV) was molecularly cloned in a bacteriophage vector. The restriction map of the biologically active clone was determined and found to be identical to that of the parental SMRV linear DNA except for the deletion of one long terminal repeat. Restriction enzyme analysis and Southern blotting indicated that the SMRV long terminal repeat was approximately 300 base pairs long. The SMRV restriction map was oriented to the viral RNA by using a gene-specific probe from baboon endogenous virus. Restriction enzyme digests of a variety of vertebrate DNAs were analyzed for DNA sequence homology with SMRV by using the cloned SMRV genome as a probe. Consistent with earlier studies, multiple copies of SMRV were detected in squirrel monkey DNA. Related fragments were also detected in the DNAs from other primate species, including humans.

Full text

PDF
434

Images in this article

436Image
on p.436
437Image
on p.437
438Image
on p.438
438Image
on p.438
439Image
on p.439
439Image
on p.439

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. Barbacid M., Long L. K., Aaronson S. A. Major structural proteins of type B, type C, and type D oncoviruses share interspecies antigenic determinants. Proc Natl Acad Sci U S A. 1980 Jan;77(1):72–76. doi: 10.1073/pnas.77.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Battula N., Hager G. L., Todaro G. J. Organization of type C viral DNA sequences endogenous to baboons: analysis with cloned viral DNA. J Virol. 1982 Feb;41(2):583–592. doi: 10.1128/jvi.41.2.583-592.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benveniste R. E., Todaro G. J. Evolution of primate oncornaviruses: An endogenous virus from langurs (Presbytis spp.) with related virogene sequences in other Old World monkeys. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4557–4561. doi: 10.1073/pnas.74.10.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blin N., Stafford D. W. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res. 1976 Sep;3(9):2303–2308. doi: 10.1093/nar/3.9.2303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  7. 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]
  8. Callahan R., Drohan W., Tronick S., Schlom J. Detection and cloning of human DNA sequences related to the mouse mammary tumor virus genome. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5503–5507. doi: 10.1073/pnas.79.18.5503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chopra H. C., Mason M. M. A new virus in a spontaneous mammary tumor of a rhesus monkey. Cancer Res. 1970 Aug;30(8):2081–2086. [PubMed] [Google Scholar]
  10. Cohen M., Rice N., Stephens R., O'Connell C. DNA sequence relationship of the baboon endogenous virus genome to the genomes of other type C and type D retroviruses. J Virol. 1982 Mar;41(3):801–812. doi: 10.1128/jvi.41.3.801-812.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Colcher D., Heberling R. L., Kalter S. S., Schlom J. Squirrel monkey retrovirus: an endogenous virus of a new world primate. J Virol. 1977 Aug;23(2):294–301. doi: 10.1128/jvi.23.2.294-301.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  13. Devare S. G., Hanson R. E., Jr, Stephenson J. R. Primate retroviruses: envelope glycoproteins of endogenous type C and type D viruses possess common interspecies antigenic determinants. J Virol. 1978 May;26(2):316–324. doi: 10.1128/jvi.26.2.316-324.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dhar R., McClements W. L., Enquist L. W., Vande Woude G. F. Nucleotide sequences of integrated Moloney sarcoma provirus long terminal repeats and their host and viral junctions. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3937–3941. doi: 10.1073/pnas.77.7.3937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Donehower L. A., Huang A. L., Hager G. L. Regulatory and coding potential of the mouse mammary tumor virus long terminal redundancy. J Virol. 1981 Jan;37(1):226–238. doi: 10.1128/jvi.37.1.226-238.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Duesberg P. H., Robinson W. S. Nucleic acid and proteins isolated from the Rauscher mouse leukemia virus (MLV). Proc Natl Acad Sci U S A. 1966 Jan;55(1):219–227. doi: 10.1073/pnas.55.1.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gallo R. C., Mann D., Broder S., Ruscetti F. W., Maeda M., Kalyanaraman V. S., Robert-Guroff M., Reitz M. S., Jr Human T-cell leukemia-lymphoma virus (HTLV) is in T but not B lymphocytes from a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5680–5683. doi: 10.1073/pnas.79.18.5680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gilboa E., Mitra S. W., Goff S., Baltimore D. A detailed model of reverse transcription and tests of crucial aspects. Cell. 1979 Sep;18(1):93–100. doi: 10.1016/0092-8674(79)90357-x. [DOI] [PubMed] [Google Scholar]
  19. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  20. Hager G. L., Chang E. H., Chan H. W., Garon C. F., Israel M. A., Martin M. A., Scolnick E. M., Lowy D. R. Molecular cloning of the Harvey sarcoma virus closed circular DNA intermediates: initial structural and biological characterization. J Virol. 1979 Sep;31(3):795–809. doi: 10.1128/jvi.31.3.795-809.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Heberling R. L., Barker S. T., Kalter S. S., Smith G. C., Helmke R. J. Oncornavirus: isolation from a squirrel monkey (Saimiri sciureus) lung culture. Science. 1977 Jan 21;195(4275):289–292. doi: 10.1126/science.63993. [DOI] [PubMed] [Google Scholar]
  22. Hino S., Tronick S. R., Heberling R. L., Kalter S. S., Hellman A., Aaronson S. A. Endogenous New World primate retrovirus: interspecies antigenic determinants shared with the major structural protein of type-D RNA viruses of Old World monkeys. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5734–5738. doi: 10.1073/pnas.74.12.5734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Hishinuma F., DeBona P. J., Astrin S., Skalka A. M. Nucleotide sequence of acceptor site and termini of integrated avian endogenous provirus ev1: integration creates a 6 bp repeat of host DNA. Cell. 1981 Jan;23(1):155–164. doi: 10.1016/0092-8674(81)90280-4. [DOI] [PubMed] [Google Scholar]
  25. Hsu T. W., Sabran J. L., Mark G. E., Guntaka R. V., Taylor J. M. Analysis of unintegrated avian RNA tumor virus double-stranded DNA intermediates. J Virol. 1978 Dec;28(3):810–818. doi: 10.1128/jvi.28.3.810-818.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Leder P., Tiemeier D., Enquist L. EK2 derivatives of bacteriophage lambda useful in the cloning of DNA from higher organisms: the lambdagtWES system. Science. 1977 Apr 8;196(4286):175–177. doi: 10.1126/science.322278. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Noda M., Kurihara M., Takano T. Retrovirus-related sequences in human DNA: detection and cloning of sequences which hybridize with the long terminal repeat of baboon endogenous virus. Nucleic Acids Res. 1982 May 11;10(9):2865–2878. doi: 10.1093/nar/10.9.2865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pulciani S., Santos E., Lauver A. V., Long L. K., Robbins K. C., Barbacid M. Oncogenes in human tumor cell lines: molecular cloning of a transforming gene from human bladder carcinoma cells. Proc Natl Acad Sci U S A. 1982 May;79(9):2845–2849. doi: 10.1073/pnas.79.9.2845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Radloff R., Bauer W., Vinograd J. A dye-buoyant-density method for the detection and isolation of closed circular duplex DNA: the closed circular DNA in HeLa cells. Proc Natl Acad Sci U S A. 1967 May;57(5):1514–1521. doi: 10.1073/pnas.57.5.1514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Reddy E. P., Smith M. J., Canaani E., Robbins K. C., Tronick S. R., Zain S., Aaronson S. A. Nucleotide sequence analysis of the transforming region and large terminal redundancies of Moloney murine sarcoma virus. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5234–5238. doi: 10.1073/pnas.77.9.5234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Shank P. R., Cohen J. C., Varmus H. E., Yamamoto K. R., Ringold G. M. Mapping of linear and circular forms of mouse mammary tumor virus DNA with restriction endonucleases: evidence for a large specific deletion occurring at high frequency during circularization. Proc Natl Acad Sci U S A. 1978 May;75(5):2112–2116. doi: 10.1073/pnas.75.5.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shank P. R., Hughes S. H., Kung H. J., Majors J. E., Quintrell N., Guntaka R. V., Bishop J. M., Varmus H. E. Mapping unintegrated avian sarcoma virus DNA: termini of linear DNA bear 300 nucleotides present once or twice in two species of circular DNA. Cell. 1978 Dec;15(4):1383–1395. doi: 10.1016/0092-8674(78)90063-6. [DOI] [PubMed] [Google Scholar]
  35. Shimotohno K., Mizutani S., Temin H. M. Sequence of retrovirus provirus resembles that of bacterial transposable elements. Nature. 1980 Jun 19;285(5766):550–554. doi: 10.1038/285550a0. [DOI] [PubMed] [Google Scholar]
  36. Shoemaker C., Goff S., Gilboa E., Paskind M., Mitra S. W., Baltimore D. Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3932–3936. doi: 10.1073/pnas.77.7.3932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Stephenson J. R., Hino S., Garrett E. W., Aaronson S. A. Immunological cross reactivity of Mason-Pfizer monkey virus with type C RNA viruses endogenous to primates. Nature. 1976 Jun 17;261(5561):609–611. doi: 10.1038/261609a0. [DOI] [PubMed] [Google Scholar]
  39. Sternberg N., Tiemeier D., Enquist L. In vitro packaging of a lambda Dam vector containing EcoRI DNA fragments of Escherichia coli and phage P1. Gene. 1977 May;1(3-4):255–280. doi: 10.1016/0378-1119(77)90049-x. [DOI] [PubMed] [Google Scholar]
  40. Swanstrom R., DeLorbe W. J., Bishop J. M., Varmus H. E. Nucleotide sequence of cloned unintegrated avian sarcoma virus DNA: viral DNA contains direct and inverted repeats similar to those in transposable elements. Proc Natl Acad Sci U S A. 1981 Jan;78(1):124–128. doi: 10.1073/pnas.78.1.124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Taylor J. M. DNA intermediates of avian RNA tumor viruses. Curr Top Microbiol Immunol. 1979;87:23–41. doi: 10.1007/978-3-642-67344-3_2. [DOI] [PubMed] [Google Scholar]
  42. Taylor J. M., Illmensee R., Summers J. Efficeint transcription of RNA into DNA by avian sarcoma virus polymerase. Biochim Biophys Acta. 1976 Sep 6;442(3):324–330. doi: 10.1016/0005-2787(76)90307-5. [DOI] [PubMed] [Google Scholar]
  43. Tronick S. R., Robbins K. C., Canaani E., Devare S. G., Andersen P. R., Aaronson S. A. Molecular cloning of Moloney murine sarcoma virus: arrangement of virus-related sequences within the normal mouse genome. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6314–6318. doi: 10.1073/pnas.76.12.6314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tronick S. R., Stephenson J. R., Aaronson S. A. Immunological properties of two polypeptides of Mason-Pfizer monkey virus. J Virol. 1974 Jul;14(1):125–132. doi: 10.1128/jvi.14.1.125-132.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wigler M., Silverstein S., Lee L. S., Pellicer A., Cheng Y. c., Axel R. Transfer of purified herpes virus thymidine kinase gene to cultured mouse cells. Cell. 1977 May;11(1):223–232. doi: 10.1016/0092-8674(77)90333-6. [DOI] [PubMed] [Google Scholar]
  46. Yoshida M., Miyoshi I., Hinuma Y. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc Natl Acad Sci U S A. 1982 Mar;79(6):2031–2035. doi: 10.1073/pnas.79.6.2031. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES