Home LiteratureArticle Details
PMID: 7494263 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Sequences flanking the pentanucleotide T-antigen binding sites in the polyomavirus core origin help determine selectivity of DNA replication.

Journal of virology ·Vol. 69 ·No. 12 ·1995-12-00 ·Pages 7570-8

Li L, Li BL, Hock M, Wang E, Folk WR

Abstract

Replication of the genomes of the polyomaviruses requires two virus-specified elements, the cis-acting origin of DNA replication, with its auxiliary DNA elements, and the trans-acting viral large tumor antigen (T antigen). Appropriate interactions between them initiate the assembly of a replication complex which, together with cellular proteins, is responsible for primer synthesis and DNA chain elongation. The organization of cis-acting elements within the origins of the polyomaviruses which replicate in mammalian cells is conserved; however, these origins are sufficiently distinct that the T antigen of one virus may function inefficiently or not at all to initiate replication at the origin of another virus. We have studied the basis for such replication selectivity between the murine polyomavirus T antigen and the primate lymphotropic polyomavirus origin. The murine polyomavirus T antigen is capable of carrying out the early steps of the assembly of an initiation complex at the lymphotropic papovavirus origin, including binding to and deformation of origin sequences in vitro. However, the T antigen inefficiently unwinds the origin, and unwinding is influenced by sequences flanking the T antigen pentanucleotide binding sites on the late side of the viral core origin. These same sequences contribute to the replication selectivity observed in vivo and in vitro, suggesting that the inefficient unwinding is the cause of the replication defect. These observations suggest a mechanism by which origins of DNA replication can evolve replication selectivity and by which the function of diverse cellular origins might be temporally activated during the S phase of the eukaryotic cell cycle.

MeSH Terms
Animals Antigens, Polyomavirus Transforming/metabolism Base Sequence Binding Sites Cell Line Conserved Sequence DNA Replication DNA, Viral/biosynthesis,chemistry Enhancer Elements, Genetic Humans Mammals Mice Molecular Sequence Data Polyomavirus/genetics,metabolism Primates Tumor Cells, Cultured
Chemicals
Antigens, Polyomavirus Transforming DNA, Viral
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Li L
Department of Biochemistry, University of Missouri-Columbia 65211, USA.
Li B L
Hock M
Wang E
Folk W R
References (120)
120 references, click to expand
  1. Mutational analysis of the simian virus 40 replicon: pseudorevertants of mutants with a defective replication origin.
    Proc Natl Acad Sci U S A. 1979 Dec;76(12):6128-31 PMID: 230499
  2. 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
  3. The nucleotide sequence and restriction enzyme sites of the polyoma genome.
    Nucleic Acids Res. 1980 Feb 25;8(4):855-60 PMID: 6253927
  4. DNA helicase and duplex DNA fragment unwinding activities of polyoma and simian virus 40 large T antigen display similarities and differences.
    J Biol Chem. 1991 Jul 5;266(19):12668-75 PMID: 1648101
  5. Complete nucleotide sequence of SV40 DNA.
    Nature. 1978 May 11;273(5658):113-20 PMID: 205802
  6. Common and unique features of T antigens encoded by the polyomavirus group.
    J Virol. 1992 Jul;66(7):3979-85 PMID: 1318392
  7. Involvement of DNA polymerase alpha in simian virus 40 DNA replication.
    J Biol Chem. 1978 May 10;253(9):3273-80 PMID: 205546
  8. The unwinding of duplex regions in DNA by the simian virus 40 large tumor antigen-associated DNA helicase activity.
    J Biol Chem. 1988 Jan 5;263(1):383-92 PMID: 2826443
  9. A question of time: replication origins of eukaryotic chromosomes.
    Cell. 1992 Oct 30;71(3):363-6 PMID: 1423601
  10. Nucleotide sequence and genome organization of the murine polyomavirus, Kilham strain.
    Virology. 1991 Apr;181(2):469-80 PMID: 1849675
  11. Nucleotides in the polyomavirus enhancer that control viral transcription and DNA replication.
    Mol Cell Biol. 1987 May;7(5):1681-90 PMID: 3037332
  12. Cooperative assembly of simian virus 40 T-antigen hexamers on functional halves of the replication origin.
    J Virol. 1991 Jun;65(6):2798-806 PMID: 1851855
  13. Biological and biochemical studies of African green monkey lymphotropic papovavirus.
    J Virol. 1982 May;42(2):502-9 PMID: 7086969
  14. Simian agent 12 is a BK virus-like papovavirus which replicates in monkey cells.
    J Virol. 1985 May;54(2):483-92 PMID: 2985810
  15. Genetic analysis of the enhancer requirements for polyomavirus DNA replication in mice.
    J Virol. 1990 Feb;64(2):476-85 PMID: 2153218
  16. Transcription factor Oct1 binds to the AT-rich segment of the simian virus 40 replication origin.
    J Virol. 1995 Jan;69(1):575-8 PMID: 7983758
  17. DNA helicase activity of SV40 large tumor antigen.
    EMBO J. 1986 Aug;5(8):1939-44 PMID: 3019672
  18. The murine p53 protein blocks replication of SV40 DNA in vitro by inhibiting the initiation functions of SV40 large T antigen.
    Cell. 1989 May 5;57(3):379-92 PMID: 2541911
  19. Human polyomavirus JC virus genome.
    J Virol. 1984 Aug;51(2):458-69 PMID: 6086957
  20. DNA supercoiling promotes formation of a bent repression loop in lac DNA.
    J Mol Biol. 1987 Jul 5;196(1):101-11 PMID: 3656441
  21. The role of the 70 kDa subunit of human DNA polymerase alpha in DNA replication.
    EMBO J. 1993 Dec;12(12):4555-66 PMID: 8223465
  22. Two DNA polymerases may be required for synthesis of the lagging DNA strand of simian virus 40.
    J Virol. 1990 Dec;64(12):5912-8 PMID: 2173773
  23. DNA replication of chimeric JC virus-simian virus 40 genomes.
    Virology. 1994 Nov 1;204(2):819-22 PMID: 7941353
  24. A unique subpopulation of murine DNA polymerase alpha/primase specifically interacts with polyomavirus T antigen and stimulates DNA replication.
    Mol Cell Biol. 1994 Apr;14(4):2767-76 PMID: 8139575
  25. A pancreas specificity results from the combination of polyomavirus and Moloney murine leukemia virus enhancer.
    Proc Natl Acad Sci U S A. 1987 Jan;84(2):449-53 PMID: 3025873
  26. Simian virus 40 origin auxiliary sequences weakly facilitate T-antigen binding but strongly facilitate DNA unwinding.
    Mol Cell Biol. 1990 Apr;10(4):1719-28 PMID: 2157141
  27. Three domains in the simian virus 40 core origin orchestrate the binding, melting, and DNA helicase activities of T antigen.
    J Virol. 1990 Feb;64(2):509-18 PMID: 2153220
  28. Smart machines at the DNA replication fork.
    Cell. 1994 Sep 9;78(5):725-8 PMID: 8087839
  29. Species-specific functional interactions of DNA polymerase alpha-primase with simian virus 40 (SV40) T antigen require SV40 origin DNA.
    Mol Cell Biol. 1994 May;14(5):3176-85 PMID: 8164673
  30. 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
  31. The DNA-binding properties of polyomavirus large T antigen are altered by ATP and other nucleotides.
    J Virol. 1991 Feb;65(2):687-99 PMID: 1846192
  32. DNA binding activity of polyoma virus large tumor antigen.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1941-5 PMID: 6326093
  33. The genome of human papovavirus BKV.
    Cell. 1979 Dec;18(4):963-77 PMID: 229976
  34. A new member of the polyomavirus family: the hamster papovavirus. Complete nucleotide sequence and transformation properties.
    EMBO J. 1985 May;4(5):1279-86 PMID: 2988942
  35. Cellular and viral control of the initiation of DNA replication.
    J Cell Sci Suppl. 1989;12:171-82 PMID: 2561423
  36. 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
  37. Identification of critical elements within the JC virus DNA replication origin.
    J Virol. 1990 Dec;64(12):5812-22 PMID: 2173768
  38. Critical spatial requirement within the origin of simian virus 40 DNA replication.
    J Virol. 1984 Jul;51(1):91-6 PMID: 6328047
  39. Initiation of SV40 DNA replication: mechanism and control.
    Cold Spring Harb Symp Quant Biol. 1991;56:303-13 PMID: 1668084
  40. Evidence suggesting that the ARS elements associated with silencers of the yeast mating-type locus HML do not function as chromosomal DNA replication origins.
    Mol Cell Biol. 1991 Oct;11(10):5346-55 PMID: 1922050
  41. Synthesis of DNA containing the simian virus 40 origin of replication by the combined action of DNA polymerases alpha and delta.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7361-5 PMID: 2571990
  42. 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
  43. Inhibition of structural changes in the simian virus 40 core origin of replication by mutation of essential origin sequences.
    J Virol. 1992 Sep;66(9):5248-55 PMID: 1323692
  44. Eukaryotic DNA replication: anatomy of an origin.
    Annu Rev Biochem. 1993;62:29-63 PMID: 8352592
  45. 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
  46. 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
  47. DNA sequence requirements for replication of polyomavirus DNA in vivo and in vitro.
    Mol Cell Biol. 1987 Oct;7(10):3694-704 PMID: 2824994
  48. Polyomavirus and simian virus 40 large T antigens bind to common DNA sequences.
    J Virol. 1984 Mar;49(3):925-37 PMID: 6321773
  49. How transcription factors regulate origins of DNA replication in eukaryotic cells.
    Trends Cell Biol. 1993 May;3(5):161-7 PMID: 14731611
  50. Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin.
    Nature. 1990 Aug 9;346(6284):534-9 PMID: 2165567
  51. p53 and DNA polymerase alpha compete for binding to SV40 T antigen.
    Nature. 1987 Oct 1-7;329(6138):456-8 PMID: 3309672
  52. Polyomavirus small t antigen: overproduction in bacteria, purification, and utilization for monoclonal and polyclonal antibody production.
    J Virol. 1986 Dec;60(3):1075-84 PMID: 3023660
  53. The origin of bidirectional DNA replication in polyoma virus.
    EMBO J. 1987 Jul;6(7):2011-8 PMID: 2820716
  54. DNA polymerase alpha stimulates the ATP-dependent binding of simian virus tumor T antigen to the SV40 origin of replication.
    J Biol Chem. 1993 May 25;268(15):11018-27 PMID: 8388381
  55. Large T-antigen and sequences within the regulatory region of JC virus both contribute to the features of JC virus DNA replication.
    Virology. 1993 Dec;197(2):537-48 PMID: 8249277
  56. Species-specific in vitro synthesis of DNA containing the polyoma virus origin of replication.
    Proc Natl Acad Sci U S A. 1986 Sep;83(17):6347-51 PMID: 3018726
  57. Initiation of SV40 DNA replication in vivo: location and structure of 5' ends of DNA synthesized in the ori region.
    Cell. 1982 Apr;28(4):767-79 PMID: 6178514
  58. Analysis of nonpermissivity in mouse cells overexpressing simian virus 40 T antigen.
    J Virol. 1987 Mar;61(3):851-7 PMID: 3027411
  59. Turning DNA replication on and off.
    Curr Opin Cell Biol. 1993 Apr;5(2):201-6 PMID: 8507492
  60. Functional organization of the simian virus 40 origin of DNA replication.
    Mol Cell Biol. 1986 Apr;6(4):1117-28 PMID: 3023870
  61. Initiation of simian virus 40 DNA replication in vitro: large-tumor-antigen- and origin-dependent unwinding of the template.
    Proc Natl Acad Sci U S A. 1987 Jun;84(11):3643-7 PMID: 3035543
  62. Simian virus 40 large tumor antigen requires three core replication origin domains for DNA unwinding and replication in vitro.
    Proc Natl Acad Sci U S A. 1987 Dec;84(23):8267-71 PMID: 2825183
  63. Localized melting and structural changes in the SV40 origin of replication induced by T-antigen.
    EMBO J. 1988 Oct;7(10):3149-58 PMID: 2846276
  64. Eukaryotic replication origins: control in space and time.
    Trends Biochem Sci. 1994 Aug;19(8):320-5 PMID: 7940676
  65. Topography of simian virus 40 A protein-DNA complexes: arrangement of pentanucleotide interaction sites at the origin of replication.
    J Virol. 1983 Apr;46(1):143-50 PMID: 6298451
  66. The replication functions of SV40 T antigen are regulated by phosphorylation.
    Cell. 1990 Jun 1;61(5):735-8 PMID: 2160857
  67. Binding of a sequence-specific single-stranded DNA-binding factor to the simian virus 40 core origin inverted repeat domain is cell cycle regulated.
    Mol Cell Biol. 1993 Jan;13(1):408-20 PMID: 8380226
  68. The in vitro replication of DNA containing the SV40 origin.
    J Biol Chem. 1990 Oct 25;265(30):18043-6 PMID: 1976634
  69. 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
  70. Mechanism of activation of simian virus 40 DNA replication by protein phosphatase 2A.
    Mol Cell Biol. 1992 Nov;12(11):4883-95 PMID: 1328866
  71. Assay of transforming activity of tumor virus DNA.
    Methods Enzymol. 1980;65(1):826-39 PMID: 6246378
  72. The T-antigen-binding domain of the simian virus 40 core origin of replication.
    J Virol. 1987 Jul;61(7):2143-9 PMID: 3035215
  73. 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
  74. The mouse DNA polymerase alpha-primase subunit p48 mediates species-specific replication of polyomavirus DNA in vitro.
    Mol Cell Biol. 1995 Mar;15(3):1716-24 PMID: 7862163
  75. Domain structure of the simian virus 40 core origin of replication.
    Mol Cell Biol. 1986 May;6(5):1663-70 PMID: 3023900
  76. Multiple functions of human single-stranded-DNA binding protein in simian virus 40 DNA replication: single-strand stabilization and stimulation of DNA polymerases alpha and delta.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9757-61 PMID: 2557626
  77. Assembly of nascent DNA into nucleosome structures in simian virus 40 chromosomes by HeLa cell extract.
    J Virol. 1990 Oct;64(10):4820-9 PMID: 2168970
  78. The A+T-rich sequence of the simian virus 40 origin is essential for replication and is involved in bending of the viral DNA.
    J Virol. 1987 Jul;61(7):2322-5 PMID: 3035231
  79. Control of simian virus 40 DNA replication by the HeLa cell nuclear kinase casein kinase I.
    Mol Cell Biol. 1993 Feb;13(2):1202-11 PMID: 8380893
  80. 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
  81. Factors contributing to the restricted DNA replicating activity of JC virus.
    Virology. 1991 Jan;180(1):306-17 PMID: 1845827
  82. Binding and unwinding--how T antigen engages the SV40 origin of DNA replication.
    Cell. 1990 Jan 26;60(2):181-4 PMID: 2153460
  83. Strand and face: the topography of interactions between the SV40 origin of replication and T-antigen during the initiation of replication.
    EMBO J. 1994 Feb 15;13(4):982-92 PMID: 8112311
  84. Mouse DNA primase plays the principal role in determination of permissiveness for polyomavirus DNA replication.
    J Virol. 1991 Sep;65(9):4874-81 PMID: 1651410
  85. cdc2 phosphorylation of threonine 124 activates the origin-unwinding functions of simian virus 40 T antigen.
    J Virol. 1993 Sep;67(9):5206-15 PMID: 8394445
  86. The induction of neoplasms with a substance released from mouse tumors by tissue culture.
    Virology. 1957 Apr;3(2):380-400 PMID: 13434017
  87. Monkey B-lymphotropic papovavirus DNA: nucleotide sequence of the region around the origin of replication.
    J Virol. 1984 May;50(2):451-6 PMID: 6323745
  88. 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
  89. Polyoma virus DNA replication requires an enhancer.
    Nature. 1984 Nov 15-21;312(5991):242-6 PMID: 6095089
  90. The adenine-thymine domain of the simian virus 40 core origin directs DNA bending and coordinately regulates DNA replication.
    Mol Cell Biol. 1986 Dec;6(12):4578-84 PMID: 3025662
  91. A position effect on the time of replication origin activation in yeast.
    Cell. 1992 Jan 24;68(2):333-9 PMID: 1733502
  92. Initiation of eukaryotic DNA replication in vitro.
    Annu Rev Cell Biol. 1989;5:197-245 PMID: 2557059
  93. T antigen and template requirements for SV40 DNA replication in vitro.
    EMBO J. 1985 Nov;4(11):2933-9 PMID: 2998767
  94. SV40 T antigen binds directly to the large subunit of purified DNA polymerase alpha.
    EMBO J. 1990 Oct;9(10):3329-36 PMID: 1698613
  95. T-antigen-DNA polymerase alpha complex implicated in simian virus 40 DNA replication.
    Mol Cell Biol. 1986 Nov;6(11):4077-87 PMID: 3025630
  96. Complete DNA sequence of lymphotropic papovavirus: prototype of a new species of the polyomavirus genus.
    Virology. 1985 May;143(1):196-211 PMID: 2998001
  97. Requirements for species-specific papovavirus DNA replication.
    J Virol. 1989 Dec;63(12):5371-85 PMID: 2555562
  98. 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
  99. Control of SV40 DNA replication by protein phosphorylation: a model for cellular DNA replication?
    Trends Cell Biol. 1994 Jul;4(7):250-5 PMID: 14731665
  100. Yeast replication factor-A functions in the unwinding of the SV40 origin of DNA replication.
    Nature. 1989 Nov 2;342(6245):92-5 PMID: 2554144
  101. DNA helical instability facilitates initiation at the SV40 replication origin.
    J Mol Biol. 1994 Jan 14;235(2):496-507 PMID: 8289278
  102. Sequence-specific interactions between a cellular DNA-binding protein and the simian virus 40 origin of DNA replication.
    Mol Cell Biol. 1988 Feb;8(2):903-11 PMID: 2832743
  103. Requirement for two DNA polymerases in the replication of simian virus 40 DNA in vitro.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9742-6 PMID: 2574863
  104. Primer-DNA formation during simian virus 40 DNA replication in vitro.
    Mol Cell Biol. 1993 May;13(5):2882-90 PMID: 8097277
  105. Spacing is crucial for coordination of domain functions within the simian virus 40 core origin of replication.
    J Virol. 1992 Apr;66(4):1933-42 PMID: 1312612
  106. Mouse p53 inhibits SV40 origin-dependent DNA replication.
    Nature. 1987 Oct 1-7;329(6138):458-60 PMID: 2821401
  107. Murine polyomavirus and simian virus 40 large T antigens produce different structural alterations in viral origin DNA.
    J Virol. 1995 Dec;69(12):7579-85 PMID: 7494264
  108. Mutation of the cyclin-dependent kinase phosphorylation site in simian virus 40 (SV40) large T antigen specifically blocks SV40 origin DNA unwinding.
    J Virol. 1993 Aug;67(8):4992-5002 PMID: 8392624
  109. Functional analysis of the role of the A + T-rich region and upstream flanking sequences in simian virus 40 DNA replication.
    Mol Cell Biol. 1986 Dec;6(12):4570-7 PMID: 3025661
  110. Simian virus 40 T-antigen DNA helicase is a hexamer which forms a binary complex during bidirectional unwinding from the viral origin of DNA replication.
    J Virol. 1992 Feb;66(2):804-15 PMID: 1309914
  111. Essential nucleotides in the polyomavirus origin region.
    J Virol. 1984 Aug;51(2):437-44 PMID: 6086955
  112. Genome structure and host range restriction of the lymphotropic papovavirus (LPV): identification of a viral lymphocyte specific enhancer element.
    Curr Top Microbiol Immunol. 1984;113:26-30 PMID: 6090066
  113. 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
  114. Enchancement of the infectivity of simian virus 40 deoxyribonucleic acid with diethylaminoethyl-dextran.
    J Natl Cancer Inst. 1968 Aug;41(2):351-7 PMID: 4299537
  115. Constitutive expression of simian virus 40 large T antigen in monkey cells activates their capacity to support polyomavirus replication.
    J Virol. 1989 Dec;63(12):5478-82 PMID: 2555568
  116. The AT-rich tract of the SV40 ori core: negative synergism and specific recognition by single stranded and duplex DNA binding proteins.
    Nucleic Acids Res. 1992 Jul 11;20(13):3333-9 PMID: 1321411
  117. The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin.
    J Biol Chem. 1992 Jul 15;267(20):14129-37 PMID: 1321135
  118. ATP enhances the binding of simian virus 40 large T antigen to the origin of replication.
    J Virol. 1987 Dec;61(12):3649-54 PMID: 2824805
  119. Unwinding of duplex DNA from the SV40 origin of replication by T antigen.
    Science. 1987 Nov 13;238(4829):964-7 PMID: 2823389
  120. E1A represses wild-type and F9-selected polyomavirus DNA replication by a mechanism not requiring depression of large tumor antigen transcription.
    J Virol. 1991 Jun;65(6):2921-8 PMID: 1851864
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
DOI
10.1128/JVI.69.12.7570-7578.1995
Published
1995-12-00
Pages
7570-8
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC189695
Subset
IM
Grants
NCI NIH HHS · CA38538 · United States
External Links
PubMed source DOI: 10.1128/JVI.69.12.7570-7578.1995 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: product@genelibs.com

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