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PMID: 10022856 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Human topoisomerase I promotes initiation of simian virus 40 DNA replication in vitro.

Molecular and cellular biology ·Vol. 19 ·No. 3 ·1999-03-00 ·Pages 1686-94

Trowbridge PW, Roy R, Simmons DT

Abstract

Addition of purified human topoisomerase I (topo I) to simian virus 40 T antigen-driven in vitro DNA replication reactions performed with topo I-deficient extracts results in a greater than 10-fold stimulation of completed molecules as well as a more than 3-fold enhancement of overall DNA replication. To further characterize this stimulation, we first demonstrate that bovine topo I but not Escherichia coli topo I can also enhance DNA replication. By using several human topo I mutants, we show that a catalytically active form of topo I is required. To delineate whether topo I influences the initiation or the elongation step of replication, we performed delayed pulse, pulse-chase, and delayed pulse-chase experiments. The results illustrate that topo I cannot promote the completion of partially replicated molecules but is needed from the beginning of the reaction to initiate replication. Competitive inhibition experiments with the topo I binding T antigen fragment 1-246T and a catalytically inactive topo I mutant suggest that part of topo I's stimulation of replication is mediated through a direct interaction with T antigen. Collectively, our data indicate that topo I enhances the synthesis of fully replicated DNA molecules by forming essential interactions with T antigen and stimulating initiation.

MeSH Terms
Animals Antigens, Polyomavirus Transforming/genetics,metabolism Catalysis Cattle Cell Line Cell Line, Transformed DNA Replication DNA Topoisomerases, Type I/genetics,metabolism DNA, Viral/biosynthesis Humans Replication Origin Simian virus 40/genetics,metabolism,physiology Spodoptera Virus Replication
Chemicals
Antigens, Polyomavirus Transforming DNA, Viral DNA Topoisomerases, Type I
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Trowbridge P W
Department of Biological Sciences, University of Delaware, Newark, Delaware 19716-2590, USA.
Roy R
Simmons D T
References (73)
73 references, click to expand
  1. The in vitro replication of DNA containing the SV40 origin.
    J Biol Chem. 1990 Oct 25;265(30):18043-6 PMID: 1976634
  2. Studies on the initiation and elongation reactions in the simian virus 40 DNA replication system.
    Proc Natl Acad Sci U S A. 1990 Dec;87(24):9712-6 PMID: 2175912
  3. Patterns of strongly protein-associated simian virus 40 DNA replication intermediates resulting from exposures to specific topoisomerase poisons.
    Biochemistry. 1990 Dec 11;29(49):10934-9 PMID: 2176889
  4. Purification of DNA polymerase delta as an essential simian virus 40 DNA replication factor.
    J Biol Chem. 1991 Jan 25;266(3):1942-9 PMID: 1671044
  5. Replication factors required for SV40 DNA replication in vitro. II. Switching of DNA polymerase alpha and delta during initiation of leading and lagging strand synthesis.
    J Biol Chem. 1991 Jan 25;266(3):1961-8 PMID: 1671046
  6. Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase.
    Mol Cell Biol. 1991 Apr;11(4):2108-15 PMID: 1848671
  7. Topoisomerase II plays an essential role as a swivelase in the late stage of SV40 chromosome replication in vitro.
    J Biol Chem. 1992 Jan 5;267(1):462-6 PMID: 1309747
  8. Overexpression of human topoisomerase I in baby hamster kidney cells: hypersensitivity of clonal isolates to camptothecin.
    Cancer Res. 1992 Feb 1;52(3):525-32 PMID: 1310066
  9. Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen.
    EMBO J. 1992 Feb;11(2):769-76 PMID: 1311258
  10. T antigen and template requirements for SV40 DNA replication in vitro.
    EMBO J. 1985 Nov;4(11):2933-9 PMID: 2998767
  11. Role of DNA polymerase alpha and DNA primase in simian virus 40 DNA replication in vitro.
    Proc Natl Acad Sci U S A. 1986 May;83(9):2869-73 PMID: 3010320
  12. Replication and supercoiling of simian virus 40 DNA in cell extracts from human cells.
    Mol Cell Biol. 1985 Aug;5(8):2051-60 PMID: 3018548
  13. Topoisomerase inhibitors can selectively interfere with different stages of simian virus 40 DNA replication.
    Mol Cell Biol. 1986 Dec;6(12):4221-7 PMID: 3025645
  14. Simian virus 40 (SV40) DNA replication: SV40 large T antigen unwinds DNA containing the SV40 origin of replication.
    Proc Natl Acad Sci U S A. 1987 Jan;84(1):16-20 PMID: 3025851
  15. Roles of DNA topoisomerases in simian virus 40 DNA replication in vitro.
    Proc Natl Acad Sci U S A. 1987 Feb;84(4):950-4 PMID: 3029765
  16. The cell-cycle regulated proliferating cell nuclear antigen is required for SV40 DNA replication in vitro.
    Nature. 1987 Apr 2-8;326(6112):471-5 PMID: 2882422
  17. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein.
    Nature. 1987 Apr 2-8;326(6112):517-20 PMID: 2882424
  18. Replication of simian virus 40 origin-containing DNA in vitro with purified proteins.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1834-8 PMID: 3031654
  19. ATP-dependent formation of a specialized nucleoprotein structure by simian virus 40 (SV40) large tumor antigen at the SV40 replication origin.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):8981-5 PMID: 2827164
  20. ATP stimulates the binding of simian virus 40 (SV40) large tumor antigen to the SV40 origin of replication.
    Proc Natl Acad Sci U S A. 1988 Jan;85(1):64-8 PMID: 2829177
  21. Coordinated leading and lagging strand synthesis during SV40 DNA replication in vitro requires PCNA.
    Cell. 1988 Apr 8;53(1):117-26 PMID: 2894900
  22. Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2523-7 PMID: 2833742
  23. Cellular factors required for multiple stages of SV40 DNA replication in vitro.
    EMBO J. 1988 Apr;7(4):1211-8 PMID: 2841119
  24. Topoisomerase I is preferentially associated with isolated replicating simian virus 40 molecules after treatment of infected cells with camptothecin.
    J Virol. 1988 Oct;62(10):3675-83 PMID: 2843668
  25. Expression of simian virus 40 T antigen in insect cells using a baculovirus expression vector.
    Virology. 1988 Nov;167(1):72-81 PMID: 3055666
  26. Complete enzymatic synthesis of DNA containing the SV40 origin of replication.
    J Biol Chem. 1988 Dec 25;263(36):19723-33 PMID: 2848839
  27. Identification of cellular proteins required for simian virus 40 DNA replication.
    J Biol Chem. 1989 Feb 15;264(5):2801-9 PMID: 2536723
  28. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication.
    Nature. 1989 Apr 20;338(6217):658-62 PMID: 2539565
  29. Simian virus 40 (SV40) large tumor antigen causes stepwise changes in SV40 origin structure during initiation of DNA replication.
    Proc Natl Acad Sci U S A. 1989 Jun;86(11):3939-43 PMID: 2542957
  30. Protein-linked DNA strand breaks induced in mammalian cells by camptothecin, an inhibitor of topoisomerase I.
    Cancer Res. 1989 Sep 15;49(18):5016-22 PMID: 2548707
  31. DNA2 encodes a DNA helicase essential for replication of eukaryotic chromosomes.
    J Biol Chem. 1995 Nov 10;270(45):26766-9 PMID: 7592912
  32. Further characterization of the human cell multiprotein DNA replication complex.
    J Cell Biochem. 1995 Sep;59(1):91-107 PMID: 8530540
  33. Biochemical and biophysical analyses of recombinant forms of human topoisomerase I.
    J Biol Chem. 1996 Mar 29;271(13):7593-601 PMID: 8631793
  34. The domain organization of human topoisomerase I.
    J Biol Chem. 1996 Mar 29;271(13):7602-8 PMID: 8631794
  35. Simian virus 40 large T antigen binds to topoisomerase I.
    Virology. 1996 Aug 15;222(2):365-74 PMID: 8806520
  36. Role for cyclin A-dependent kinase in DNA replication in human S phase cell extracts.
    J Biol Chem. 1996 Dec 6;271(49):31627-37 PMID: 8940182
  37. CDC45, a novel yeast gene that functions with the origin recognition complex and Mcm proteins in initiation of DNA replication.
    Mol Cell Biol. 1997 Feb;17(2):553-63 PMID: 9001208
  38. Topoisomerase I is preferentially associated with normal SV40 replicative intermediates, but is associated with both replicating and nonreplicating SV40 DNAs which are deficient in histones.
    Nucleic Acids Res. 1992 Jul 11;20(13):3347-52 PMID: 1321412
  39. Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6958-62 PMID: 1495986
  40. Initiation of simian virus 40 DNA replication requires the interaction of a specific domain of human DNA polymerase alpha with large T antigen.
    Mol Cell Biol. 1993 Feb;13(2):809-20 PMID: 8380896
  41. An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication.
    J Biol Chem. 1993 Feb 15;268(5):3389-95 PMID: 8381428
  42. Functional interactions between SV40 T antigen and other replication proteins at the replication fork.
    J Biol Chem. 1993 May 25;268(15):11008-17 PMID: 8098707
  43. Further purification and characterization of a multienzyme complex for DNA synthesis in human cells.
    J Cell Biochem. 1993 Dec;53(4):405-19 PMID: 8300757
  44. Reconstitution of complete SV40 DNA replication with purified replication factors.
    J Biol Chem. 1994 Apr 8;269(14):10923-34 PMID: 8144677
  45. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro.
    Nature. 1994 May 19;369(6477):207-12 PMID: 7910375
  46. DNA replication from initiation zones of mammalian cells in a model system.
    Mol Cell Biol. 1994 Oct;14(10):6489-96 PMID: 7935372
  47. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  48. Interaction between DNA and an Escherichia coli protein omega.
    J Mol Biol. 1971 Feb 14;55(3):523-33 PMID: 4927945
  49. Characteristics of a human cell line transformed by DNA from human adenovirus type 5.
    J Gen Virol. 1977 Jul;36(1):59-74 PMID: 886304
  50. Monoclonal antibodies against simian virus 40 T antigens: evidence for distinct sublcasses of large T antigen and for similarities among nonviral T antigens.
    J Virol. 1980 Jun;34(3):752-63 PMID: 6155477
  51. Terminal stages of SV40 DNA replication proceed via multiply intertwined catenated dimers.
    Cell. 1980 Aug;21(1):103-14 PMID: 6250706
  52. Arrest of segregation leads to accumulation of highly intertwined catenated dimers: dissection of the final stages of SV40 DNA replication.
    Cell. 1981 Sep;25(3):659-69 PMID: 6269752
  53. Monoclonal antibodies specific for simian virus 40 tumor antigens.
    J Virol. 1981 Sep;39(3):861-9 PMID: 6169844
  54. DNA strand breakage by wheat germ type 1 topoisomerase.
    Biochim Biophys Acta. 1984 Jul 18;782(3):304-12 PMID: 6329302
  55. Simian virus 40 DNA replication in vitro.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):6973-7 PMID: 6095264
  56. DNA topoisomerases.
    Annu Rev Biochem. 1985;54:665-97 PMID: 2992360
  57. Simian virus 40 DNA replication in vitro: specificity of initiation and evidence for bidirectional replication.
    Mol Cell Biol. 1985 Jun;5(6):1238-46 PMID: 2993858
  58. In vitro replication of duplex circular DNA containing the simian virus 40 DNA origin site.
    Proc Natl Acad Sci U S A. 1985 Sep;82(17):5710-4 PMID: 2994044
  59. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I.
    J Biol Chem. 1985 Nov 25;260(27):14873-8 PMID: 2997227
  60. An immunoaffinity purification procedure for SV40 large T antigen.
    Virology. 1985 Jul 15;144(1):88-100 PMID: 2998049
  61. Mammalian cell DNA replication.
    Crit Rev Eukaryot Gene Expr. 1997;7(1-2):125-57 PMID: 9034719
  62. Reconstitution of human topoisomerase I by fragment complementation.
    J Mol Biol. 1997 Jun 13;269(3):355-72 PMID: 9199405
  63. A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex.
    J Biol Chem. 1997 Sep 26;272(39):24508-13 PMID: 9305914
  64. A DNA helicase purified by replication protein A (RPA) affinity chromatography from mouse FM3A cells.
    Nucleic Acids Res. 1997 Oct 1;25(19):3881-8 PMID: 9380512
  65. Identification of a preinitiation step in DNA replication that is independent of origin recognition complex and cdc6, but dependent on cdk2.
    J Cell Biol. 1998 Jan 26;140(2):271-81 PMID: 9442103
  66. The initiation of simian virus 40 DNA replication in vitro.
    Crit Rev Biochem Mol Biol. 1997;32(6):503-68 PMID: 9444478
  67. Interaction between the N-terminus of human topoisomerase I and SV40 large T antigen.
    Nucleic Acids Res. 1998 Apr 1;26(7):1841-7 PMID: 9512561
  68. Topoisomerase I stimulates SV40 T antigen-mediated DNA replication and inhibits T antigen's ability to unwind DNA at nonorigin sites.
    Virology. 1998 Mar 15;242(2):435-43 PMID: 9514975
  69. Mammalian DNA topoisomerase I activity and poisoning by camptothecin are inhibited by simian virus 40 large T antigen.
    Biochemistry. 1998 Mar 17;37(11):3818-23 PMID: 9521701
  70. Identification of primary initiation sites for DNA replication in the hamster dihydrofolate reductase gene initiation zone.
    Mol Cell Biol. 1998 Jun;18(6):3266-77 PMID: 9584167
  71. The activity of topoisomerase I is modulated by large T antigen during unwinding of the SV40 origin.
    J Biol Chem. 1998 Aug 7;273(32):20390-6 PMID: 9685392
  72. Multiple replication factors augment DNA synthesis by the two eukaryotic DNA polymerases, alpha and delta.
    EMBO J. 1989 Dec 1;8(12):3883-9 PMID: 2573521
  73. A 21S enzyme complex from HeLa cells that functions in simian virus 40 DNA replication in vitro.
    Biochemistry. 1990 Jul 10;29(27):6362-74 PMID: 2169868
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1999-03-00
Pages
1686-94
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC83962
Subset
IM
Grants
NCI NIH HHS · R01 CA036118 · United States
NCI NIH HHS · CA36118 · United States
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