Home LiteratureArticle Details
PMID: 8491198 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Integration of murine leukemia virus DNA depends on mitosis.

The EMBO journal ·Vol. 12 ·No. 5 ·1993-05-00 ·Pages 2099-108

Roe T, Reynolds TC, Yu G, Brown PO

Abstract

In synchronized rat or mouse cells infected with Moloney murine leukemia virus (MLV), integration of viral DNA and production of viral proteins occur only after the cells traverse mitosis. Integration is blocked when cells are prevented from progressing through mitosis. Viral nucleoprotein complexes isolated from arrested cells contain full-length viral DNA and can integrate this viral DNA in vitro, showing that the block to integration in arrested cells is not due to a lack of mature integration machinery. When infected cells traverse mitosis, there is a sharp increase in nuclear accumulation of viral DNA. The dependence of integration on mitosis may therefore be due to a requirement for mitosis and nuclear envelope breakdown for entry of the viral integration complex into the nucleus.

MeSH Terms
Animals Cell Nucleus/metabolism Cells, Cultured DNA, Viral/metabolism G2 Phase Genome, Viral Metaphase Mice Mitosis Moloney murine leukemia virus/genetics,physiology Nucleoproteins/metabolism Rats Viral Proteins/biosynthesis Virus Integration
Chemicals
DNA, Viral Nucleoproteins Viral Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Roe T
Department of Biochemistry, Stanford University, CA 94305.
Reynolds T C
Yu G
Brown P O
References (57)
57 references, click to expand
  1. Cell cycle-dependent activation of rous sarcoma virus-infected stationary chicken cells: avian leukosis virus group-specific antigens and ribonucleic acid.
    J Virol. 1972 Jul;10(1):82-7 PMID: 4339198
  2. Structural and functional properties of DNA polymerase delta from rabbit bone marrow.
    Mol Cell Biochem. 1984 Apr;62(1):13-24 PMID: 6330522
  3. Cellular functions are required for the synthesis and integration of avian sarcoma virus-specific DNA.
    Cell. 1977 Jun;11(2):307-19 PMID: 196759
  4. Interaction of oncodazole (R 17934), a new antitumoral drug, with rat brain tubulin.
    Biochem Biophys Res Commun. 1976 Mar 22;69(2):319-24 PMID: 1267789
  5. Nuclear import-export: in search of signals and mechanisms.
    Cell. 1991 Jul 12;66(1):15-22 PMID: 1712670
  6. Covalently closed circular DNA of avian sarcoma virus: purification from nuclei of infected quail tumor cells and measurement by electron microscopy and gel electrophoresis.
    J Mol Biol. 1976 Sep 15;106(2):337-57 PMID: 185393
  7. Selective extraction of polyoma DNA from infected mouse cell cultures.
    J Mol Biol. 1967 Jun 14;26(2):365-9 PMID: 4291934
  8. Import of simian virus 40 virions through nuclear pore complexes.
    Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7333-7 PMID: 1651501
  9. A role for the nuclear envelope in controlling DNA replication within the cell cycle.
    Nature. 1988 Apr 7;332(6164):546-8 PMID: 3357511
  10. A simple method of reducing the fading of immunofluorescence during microscopy.
    J Immunol Methods. 1981;43(3):349-50 PMID: 7019347
  11. Determination of viral proteins present in the human immunodeficiency virus type 1 preintegration complex.
    J Virol. 1991 Apr;65(4):1910-5 PMID: 2002549
  12. Correct integration of retroviral DNA in vitro.
    Cell. 1987 May 8;49(3):347-56 PMID: 3032450
  13. Cellular localization and cell cycle regulation by a temperature-sensitive p53 protein.
    Genes Dev. 1991 Feb;5(2):151-9 PMID: 1995413
  14. Metabolic requirements for infection by Rous sarcoma virus. IV. Virus reproduction and cellular transformation without cellular division.
    Virology. 1972 May;48(2):494-501 PMID: 4337033
  15. The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SWI5.
    Cell. 1991 Aug 23;66(4):743-58 PMID: 1652372
  16. Active nuclear import of human immunodeficiency virus type 1 preintegration complexes.
    Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6580-4 PMID: 1631159
  17. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport.
    J Cell Biol. 1991 Oct;115(1):1-17 PMID: 1717476
  18. Fv-1 restriction and its effects on murine leukemia virus integration in vivo and in vitro.
    J Virol. 1992 Oct;66(10):5959-66 PMID: 1326652
  19. Infection efficiency of T lymphocytes with amphotropic retroviral vectors is cell cycle dependent.
    J Virol. 1989 Sep;63(9):3865-9 PMID: 2788225
  20. A radiological study of cell-virus interaction in the Rous sarcoma.
    Virology. 1959 Jan;7(1):75-91 PMID: 13636057
  21. Subcellular localization of yeast CDC46 varies with the cell cycle.
    Genes Dev. 1990 Dec;4(12B):2252-63 PMID: 2279699
  22. Electron microscopic observations on granulosis virus entry, uncoating and replication processes during infection of the midgut cells of Trichoplusia ni.
    J Ultrastruct Res. 1971 Jun;35(5):606-25 PMID: 5142394
  23. A change in growth potential of cells after conversion by Rous sarcoma virus.
    J Cell Physiol. 1967 Dec;70(3):301-8 PMID: 4296860
  24. The Fv-1 gene of the mouse and its control of murine leukemia virus replication.
    Curr Top Microbiol Immunol. 1979;86:67-122 PMID: 227645
  25. 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):104-4 PMID: 202729
  26. 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):183-95 PMID: 6245227
  27. Construction and recovery of viable retroviral genomes carrying a bacterial suppressor transfer RNA gene.
    Science. 1985 Apr 19;228(4697):329-32 PMID: 2984770
  28. Fluorescence microphotolysis to measure nucleocytoplasmic transport and intracellular mobility.
    Biochim Biophys Acta. 1986 Dec 22;864(3-4):305-59 PMID: 3539193
  29. Retroviral integration: structure of the initial covalent product and its precursor, and a role for the viral IN protein.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2525-9 PMID: 2539592
  30. The FT210 cell line is a mouse G2 phase mutant with a temperature-sensitive CDC2 gene product.
    Cell. 1990 Oct 19;63(2):313-24 PMID: 2208288
  31. Molecular genetics of herpes simplex virus. VIII. further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle.
    J Virol. 1983 Jan;45(1):397-407 PMID: 6296445
  32. A nucleoprotein complex mediates the integration of retroviral DNA.
    Genes Dev. 1989 Apr;3(4):469-78 PMID: 2721960
  33. Morphological aspects of the uptake of simian virus 40 by permissive cells.
    J Virol. 1970 Jul;6(1):87-93 PMID: 4097233
  34. The effects of methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) carbamate, (R 17934; NSC 238159), a new synthetic antitumoral drug interfering with microtubules, on mammalian cells cultured in vitro.
    Cancer Res. 1976 Mar;36(3):905-16 PMID: 766963
  35. Structure and development of viruses as observed in the electron microscope. XI. Entry and uncoating of herpes simplex virus.
    J Virol. 1971 Dec;8(6):910-8 PMID: 4135172
  36. Human immunodeficiency virus infection of cells arrested in the cell cycle.
    EMBO J. 1992 Aug;11(8):3053-8 PMID: 1322294
  37. Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection.
    Mol Cell Biol. 1990 Aug;10(8):4239-42 PMID: 2370865
  38. Study of pp60v-src protein kinase activity in synchronized chicken embryo fibroblasts infected with Rous sarcoma virus.
    Exp Cell Res. 1984 Jan;150(1):242-9 PMID: 6319162
  39. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure.
    Cell. 1990 Apr 20;61(2):213-22 PMID: 2331748
  40. Transport of incoming influenza virus nucleocapsids into the nucleus.
    J Virol. 1991 Jan;65(1):232-44 PMID: 1985199
  41. Cell cycle dependence of synthesis of unintegrated viral DNA in mouse cells newly infected with murine leukemia virus.
    Virology. 1981 Apr 15;110(1):202-7 PMID: 7210505
  42. Early events in the interaction of adenoviruses with HeLa cells. IV. Association with microtubules and the nuclear pore complex during vectorial movement of the inoculum.
    Virology. 1973 Dec;56(2):465-83 PMID: 4271287
  43. Formation and structure of infectious DNA of spleen necrosis virus.
    J Virol. 1977 Jan;21(1):119-30 PMID: 556779
  44. HIV-1 replication is controlled at the level of T cell activation and proviral integration.
    EMBO J. 1990 May;9(5):1551-60 PMID: 2184033
  45. Rous sarcoma virus infection of synchronized cells establishes provirus integration during S-phase DNA synthesis prior to cellular division.
    Proc Natl Acad Sci U S A. 1981 Apr;78(4):2601-5 PMID: 6264483
  46. Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant, causes mitotic arrest in HeLa cells.
    J Cell Biol. 1992 Apr;117(1):213-24 PMID: 1532584
  47. Identification of a Golgi-associated protein that undergoes mitosis dependent phosphorylation and relocation.
    J Cell Biol. 1990 May;110(5):1513-23 PMID: 2186044
  48. Effect of aphidicolin on avian sarcoma virus replication.
    J Virol. 1982 Nov;44(2):493-8 PMID: 6292514
  49. Nuclear translocation of viral Jun but not of cellular Jun is cell cycle dependent.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4290-4 PMID: 1584763
  50. The nuclear membrane prevents replication of human G2 nuclei but not G1 nuclei in Xenopus egg extract.
    Cell. 1992 Apr 3;69(1):151-8 PMID: 1555238
  51. Molecular genetics of herpes simplex virus. V. Characterization of a mutant defective in ability to form plaques at low temperatures and in a viral fraction which prevents accumulation of coreless capsids at nuclear pores late in infection.
    J Virol. 1981 Dec;40(3):870-80 PMID: 6275122
  52. Requirement for cell division for initiation of transcription of Rous sarcoma virus RNA.
    J Virol. 1974 Sep;14(3):531-46 PMID: 4369144
  53. Effect of Fv-1 gene product on proviral DNA formation and integration in cells infected with murine leukemia viruses.
    Proc Natl Acad Sci U S A. 1976 Jul;73(7):2236-40 PMID: 181748
  54. Fluorescence in situ hybridization with DNA probes.
    Methods Cell Biol. 1990;33:383-400 PMID: 2084477
  55. Retroviral integration into minichromosomes in vitro.
    EMBO J. 1992 Jan;11(1):291-303 PMID: 1310932
  56. Productive human immunodeficiency virus type 1 (HIV-1) infection of nonproliferating human monocytes.
    J Exp Med. 1991 Dec 1;174(6):1477-82 PMID: 1720811
  57. Isolation and analysis of a mammalian temperature-sensitive mutant defective in G2 functions.
    Exp Cell Res. 1986 Nov;167(1):53-62 PMID: 2428648
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1993-05-00
Pages
2099-108
Language
English
Region
England
NLM ID
8208664
PMCID
PMC413431
Subset
IM
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2