Europe PMC

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration.

Proceedings of the National Academy of Sciences of the United States of America, 01 Jul 1980, 77(7):3932-3936
https://doi.org/10.1073/pnas.77.7.3932 PMID: 6449003 PMCID: PMC349741

Free full text in Europe PMC

Abstract 

Closed circular Moloney murine leukemia virus (M-MuLV) DNA was prepared from recently infected cells and cloned in a lambda vector. Four classes of cloned M-MuLV inserts were found: Class I, full length 8.8-kilobase (kb) inserts with two tandem long terminal repeats (LTRs) of 600 base pairs; class 2, 8.2-kb inserts with a single copy of a LTR; class 3, M-MuLV DNA inserts with various portions deleted; and class 4, an 8.8-kb insert with an internal sequence inversion. Determination of nucleotide sequence at the junction between the two LTRs from a class 1 insert suggested that circularization occurred by blunt-end ligation of an 8.8-kb linear DNA. The class 4 molecule had an inversion that was flanked by inverted LTRs, each of which had lost two terminal base pairs at the inversion end points. Also, four base pairs that were present only once in standard M-MuLV DNA were duplicated at either end of the inversion. This molecule was interpreted as resulting from an integrative inversion in which M-MuLV DNA has integrated into itself. Its analysis thus provided explicit information concerning the mechanism by which retrovirus DNA integrates into host cell DNA. Models of retrovirus integration based on bacterial DNA transposition mechanisms are proposed.

Free full text 

Logo of pnasLink to Publisher's site
Proc Natl Acad Sci U S A. 1980 Jul; 77(7): 3932–3936.
PMCID: PMC349741
PMID: 6449003

Structure of a cloned circular Moloney murine leukemia virus DNA molecule containing an inverted segment: implications for retrovirus integration.

C Shoemaker, S Goff, E Gilboa, M Paskind, S W Mitra, and D Baltimore
Copyright and License information Disclaimer

Abstract

Closed circular Moloney murine leukemia virus (M-MuLV) DNA was prepared from recently infected cells and cloned in a lambda vector. Four classes of cloned M-MuLV inserts were found: Class I, full length 8.8-kilobase (kb) inserts with two tandem long terminal repeats (LTRs) of 600 base pairs; class 2, 8.2-kb inserts with a single copy of a LTR; class 3, M-MuLV DNA inserts with various portions deleted; and class 4, an 8.8-kb insert with an internal sequence inversion. Determination of nucleotide sequence at the junction between the two LTRs from a class 1 insert suggested that circularization occurred by blunt-end ligation of an 8.8-kb linear DNA. The class 4 molecule had an inversion that was flanked by inverted LTRs, each of which had lost two terminal base pairs at the inversion end points. Also, four base pairs that were present only once in standard M-MuLV DNA were duplicated at either end of the inversion. This molecule was interpreted as resulting from an integrative inversion in which M-MuLV DNA has integrated into itself. Its analysis thus provided explicit information concerning the mechanism by which retrovirus DNA integrates into host cell DNA. Models of retrovirus integration based on bacterial DNA transposition mechanisms are proposed.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.1M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.
 
icon of scanned page 3932
3932
icon of scanned page 3933
3933
icon of scanned page 3934
3934
icon of scanned page 3935
3935
icon of scanned page 3936
3936
 

Images in this article

Image
Image
on p.3933
Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bishop JM. Retroviruses. Annu Rev Biochem. 1978;47:35–88. [Abstract] [Google Scholar]
  • Shank PR, Hughes SH, Kung HJ, Majors JE, Quintrell N, Guntaka RV, Bishop JM, Varmus HE. 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. [Abstract] [Google Scholar]
  • Gilboa E, Goff S, Shields A, Yoshimura F, Mitra S, Baltimore D. In vitro synthesis of a 9 kbp terminally redundant DNA carrying the infectivity of Moloney murine leukemia virus. Cell. 1979 Apr;16(4):863–874. [Abstract] [Google Scholar]
  • Shank PR, Cohen JC, Varmus HE, Yamamoto KR, Ringold GM. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Shank PR, Varmus HE. Virus-specific DNA in the cytoplasm of avian sarcoma virus-infected cells is a precursor to covalently closed circular viral DNA in the nucleus. J Virol. 1978 Jan;25(1):104–104. [Europe PMC free article] [Abstract] [Google Scholar]
  • Yoshimura FK, Weinberg RA. Restriction endonuclease cleavage of linear and closed circular murine leukemia viral DNAs: discovery of a smaller circular form. Cell. 1979 Feb;16(2):323–332. [Abstract] [Google Scholar]
  • Jolicoeur P, Rassart E. Effect of Fv-1 gene product on synthesis of linear and supercoiled viral DNA in cells infected with murine leukemia virus. J Virol. 1980 Jan;33(1):183–195. [Europe PMC free article] [Abstract] [Google Scholar]
  • Steffen D, Weinberg RA. The integrated genome of murine leukemia virus. Cell. 1978 Nov;15(3):1003–1010. [Abstract] [Google Scholar]
  • Cohen JC, Shank PR, Morris VL, Cardiff R, Varmus HE. Integration of the DNA of mouse mammary tumor virus in virus-infected normal and neoplastic tissue of the mouse. Cell. 1979 Feb;16(2):333–345. [Abstract] [Google Scholar]
  • Hughes SH, Shank PR, Spector DH, Kung HJ, Bishop JM, Varmus HE, Vogt PK, Breitman ML. Proviruses of avian sarcoma virus are terminally redundant, co-extensive with unintegrated linear DNA and integrated at many sites. Cell. 1978 Dec;15(4):1397–1410. [Abstract] [Google Scholar]
  • Sabran JL, Hsu TW, Yeater C, Kaji A, Mason WS, Taylor JM. Analysis of integrated avian RNA tumor virus DNA in transformed chicken, duck and quail fibroblasts. J Virol. 1979 Jan;29(1):170–178. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hager GL, Chang EH, Chan HW, Garon CF, Israel MA, Martin MA, Scolnick EM, Lowy DR. Molecular cloning of the Harvey sarcoma virus closed circular DNA intermediates: initial structural and biological characterization. J Virol. 1979 Sep;31(3):795–809. [Europe PMC free article] [Abstract] [Google Scholar]
  • Tronick SR, Robbins KC, Canaani E, Devare SG, Andersen PR, Aaronson SA. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Oliff AI, Hager GL, Chang EH, Scolnick EM, Chan HW, Lowy DR. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Grindley ND, Sherratt DJ. Sequence analysis at IS1 insertion sites: models for transposition. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 2):1257–1261. [Abstract] [Google Scholar]
  • Shapiro JA. Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1933–1937. [Europe PMC free article] [Abstract] [Google Scholar]
  • Fan H, Paskind M. Measurement of the sequence complexity of cloned Moloney murine leukemia virus 60 to 70S RNA: evidence for a haploid genome. J Virol. 1974 Sep;14(3):421–429. [Europe PMC free article] [Abstract] [Google Scholar]
  • Shields A, Witte WN, Rothenberg E, Baltimore D. High frequency of aberrant expression of Moloney murine leukemia virus in clonal infections. Cell. 1978 Jul;14(3):601–609. [Abstract] [Google Scholar]
  • Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. [Abstract] [Google Scholar]
  • 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Blattner FR, Blechl AE, Denniston-Thompson K, Faber HE, Richards JE, Slightom JL, Tucker PW, Smithies O. Cloning human fetal gamma globin and mouse alpha-type globin DNA: preparation and screening of shotgun collections. Science. 1978 Dec 22;202(4374):1279–1284. [Abstract] [Google Scholar]
  • 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. [Abstract] [Google Scholar]
  • Benton WD, Davis RW. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. [Abstract] [Google Scholar]
  • Enquist L, Tiemeier D, Leder P, Weisberg R, Sternberg N. Safer derivatives of bacteriophage lambdagt-lambdaC for use in cloning of recombinant DNA molecules. Nature. 1976 Feb 19;259(5544):596–598. [Abstract] [Google Scholar]
  • Maxam AM, Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. [Europe PMC free article] [Abstract] [Google Scholar]
  • Maat J, Smith AJ. A method for sequencing restriction fragments with dideoxynucleoside triphosphates. Nucleic Acids Res. 1978 Dec;5(12):4537–4545. [Europe PMC free article] [Abstract] [Google Scholar]
  • Pereira WC, Neves VJ, Rodrigues Y. Craniotomia descompressive bifrontal no tratamento do edema cerebral grave. Arq Neuropsiquiatr. 1977 Jun;35(2):99–111. [Abstract] [Google Scholar]
  • Enea V, Vovis GF, Zinder ND. Genetic studies with heteroduplex DNA of bacteriophage fl. Asymmetric segregation, base correction and implications for the mechanism of genetic recombination. J Mol Biol. 1975 Aug 15;96(3):495–509. [Abstract] [Google Scholar]
  • Katz L, Kingsbury DT, Helinski DR. Stimulation by cyclic adenosine monophosphate of plasmid deoxyribonucleic acid replication and catabolite repression of the plasmid deoxyribonucleic acid-protein relaxation complex. J Bacteriol. 1973 May;114(2):577–591. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gilboa E, Mitra SW, Goff S, Baltimore D. A detailed model of reverse transcription and tests of crucial aspects. Cell. 1979 Sep;18(1):93–100. [Abstract] [Google Scholar]
  • Haseltine WA, Kleid DG, Panet A, Rothenberg E, Baltimore D. Ordered transcription of RNA tumor virus genomes. J Mol Biol. 1976 Sep 5;106(1):109–131. [Abstract] [Google Scholar]
  • Dhar R, McClements WL, Enquist LW, Vande Woude GF. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. [Abstract] [Google Scholar]
  • Kleckner N. Translocatable elements in procaryotes. Cell. 1977 May;11(1):11–23. [Abstract] [Google Scholar]
  • Reed RR, Young RA, Steitz JA, Grindley ND, Guyer MS. Transposition of the Escherichia coli insertion element gamma generates a five-base-pair repeat. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4882–4886. [Europe PMC free article] [Abstract] [Google Scholar]
  • Calos MP, Johnsrud L, Miller JH. DNA sequence at the integration sites of the insertion element IS1. Cell. 1978 Mar;13(3):411–418. [Abstract] [Google Scholar]
  • Ohtsubo E, Zenilman M, Ohtsubo H. Plasmids containing insertion elements are potential transposons. Proc Natl Acad Sci U S A. 1980 Feb;77(2):750–754. [Europe PMC free article] [Abstract] [Google Scholar]
  • Potter SS, Brorein WJ, Jr, Dunsmuir P, Rubin GM. Transposition of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell. 1979 Jun;17(2):415–427. [Abstract] [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

Full text links 

Read article at publisher's site: https://doi.org/10.1073/pnas.77.7.3932

Read article for free, from open access legal sources, via Unpaywall: https://europepmc.org/articles/pmc349741?pdf=renderUnpaywall

Citations & impact 

Impact metrics

168
Citations
Jump to Citations

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/41516529
Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/41516529

Article citations

Go to all (168) article citations

Similar Articles 

To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.

Funding 

Funders who supported this work.

NCI NIH HHS (3)