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Science 13 November 1987:
Vol. 238. no. 4829, pp. 964 - 967
DOI: 10.1126/science.2823389
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Articles

Science, Vol 238, Issue 4829, 964-967
Copyright © 1987 by American Association for the Advancement of Science

articles

Unwinding of duplex DNA from the SV40 origin of replication by T antigen

M Dodson, FB Dean, P Bullock, H Echols, and J Hurwitz

Department of Molecular Biology, University of California, Berkeley 94720.

The T antigen specified by SV40 virus is the only viral-encoded protein required for replication of SV40 DNA. T antigen has two activities that appear to be essential for viral DNA replication: specific binding to duplex DNA at the origin of replication and helicase activity that unwinds the two DNA strands. As judged by electron microscopy, DNA unwinding is initiated at the origin of replication and proceeds bidirectionally. Either linear or circular DNA molecules containing the origin of replication are effective substrates; with closed circular DNA, a topoisomerase capable of removing positive superhelical turns is required for an efficient reaction. Presence of an origin sequence on duplex DNA and a single-strand DNA-binding protein appear to be the only requirements for T antigen to catalyze unwinding. This reaction mediated by T antigen defines a likely pathway to precise initiation of DNA replication: (i) the sequence-specific binding activity locates the origin sequence, (ii) the duplex DNA is unwound at this site, and (iii) the DNA polymerase and primase begin DNA replication. A similar pathway has been inferred for the localized initiation of DNA replication by bacteriophage lambda and by Escherichia coli in which a sequence-specific binding protein locates the origin and directs the DnaB helicase to this site. Observations with the SV40 system indicate that localized initiation of duplex DNA replication may be similar for prokaryotes and eukaryotes.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Analyses of the Interaction between the Origin Binding Domain from Simian Virus 40 T Antigen and Single-Stranded DNA Provide Insights into DNA Unwinding and Initiation of DNA Replication.
D. K. Reese, G. Meinke, A. Kumar, S. Moine, K. Chen, J. L. Sudmeier, W. Bachovchin, A. Bohm, and P. A. Bullock (2006)
J. Virol. 80, 12248-12259
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Binding of the Universal Minicircle Sequence Binding Protein at the Kinetoplast DNA Replication Origin.
I. Onn, I. Kapeller, K. Abu-Elneel, and J. Shlomai (2006)
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Interactions Required for Binding of Simian Virus 40 T Antigen to the Viral Origin and Molecular Modeling of Initial Assembly Events.
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J. Virol. 78, 2921-2934
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RPA is an initiation factor for human chromosomal DNA replication.
D. Szuts, L. Kitching, C. Christov, A. Budd, S. Peak-Chew, and T. Krude (2003)
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Chaperone Proteins Abrogate Inhibition of the Human Papillomavirus (HPV) E1 Replicative Helicase by the HPV E2 Protein.
B. Y. Lin, A. M. Makhov, J. D. Griffith, T. R. Broker, and L. T. Chow (2002)
Mol. Cell. Biol. 22, 6592-6604
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Physical and Functional Interaction between the Mini-chromosome Maintenance-like DNA Helicase and the Single-stranded DNA Binding Protein from the Crenarchaeon Sulfolobus solfataricus.
F. Carpentieri, M. De Felice, M. De Falco, M. Rossi, and F. M. Pisani (2002)
J. Biol. Chem. 277, 12118-12127
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In the Simian Virus 40 In Vitro Replication System, Start Site Selection by the Polymerase {alpha}-Primase Complex Is Not Significantly Altered by Changes in the Concentration of Ribonucleotides.
J. D. Purviance, A. E. Prack, B. Barbaro, and P. A. Bullock (2001)
J. Virol. 75, 6392-6401
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Role of Single-Stranded DNA Binding Activity of T Antigen in Simian Virus 40 DNA Replication.
C. Wu, R. Roy, and D. T. Simmons (2001)
J. Virol. 75, 2839-2847
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The Simian Virus 40 Core Origin Contains Two Separate Sequence Modules That Support T-Antigen Double-Hexamer Assembly.
K. R. Sreekumar, A. E. Prack, D. R. Winters, B. A. Barbaro, and P. A. Bullock (2000)
J. Virol. 74, 8589-8600
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Phosphorylation of Simian Virus 40 T Antigen on Thr 124 Selectively Promotes Double-Hexamer Formation on Subfragments of the Viral Core Origin.
B. A. Barbaro, K. R. Sreekumar, D. R. Winters, A. E. Prack, and P. A. Bullock (2000)
J. Virol. 74, 8601-8613
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Large T-Antigen Double Hexamers Imaged at the Simian Virus 40 Origin of Replication.
M. Valle, C. Gruss, L. Halmer, J. M. Carazo, and L. E. Donate (2000)
Mol. Cell. Biol. 20, 34-41
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Sequence Requirements for the Assembly of Simian Virus 40 T Antigen and the T-Antigen Origin Binding Domain on the Viral Core Origin of Replication.
H. Y. Kim, B. A. Barbaro, W. S. Joo, A. E. Prack, K. R. Sreekumar, and P. A. Bullock (1999)
J. Virol. 73, 7543-7555
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Two Regions of Simian Virus 40 T Antigen Determine Cooperativity of Double-Hexamer Assembly on the Viral Origin of DNA Replication and Promote Hexamer Interactions during Bidirectional Origin DNA Unwinding.
K. Weisshart, P. Taneja, A. Jenne, U. Herbig, D. T. Simmons, and E. Fanning (1999)
J. Virol. 73, 2201-2211
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Interaction of the Transcription Factor TFIID with Simian Virus 40 (SV40) Large T Antigen Interferes with Replication of SV40 DNA In Vitro.
U. Herbig, K. Weisshart, P. Taneja, and E. Fanning (1999)
J. Virol. 73, 1099-1107
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The Replication Protein A Binding Site in Simian Virus 40 (SV40) T Antigen and Its Role in the Initial Steps of SV40 DNA Replication.
K. Weisshart, P. Taneja, and E. Fanning (1998)
J. Virol. 72, 9771-9781
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The Origin DNA-Binding and Single-Stranded DNA-Binding Domains of Simian Virus 40 Large T Antigen Are Distinct.
C. Wu, D. Edgil, and D. T. Simmons (1998)
J. Virol. 72, 10256-10259
   Abstract »    Full Text »    PDF »
Assembly of T-Antigen Double Hexamers on the Simian Virus 40 Core Origin Requires Only a Subset of the Available Binding Sites.
W. S. Joo, H. Y. Kim, J. D. Purviance, K. R. Sreekumar, and P. A. Bullock (1998)
Mol. Cell. Biol. 18, 2677-2687
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The Herpes Simplex Virus Type-1 Single-strand DNA-binding Protein, ICP8, Increases the Processivity of the UL9 Protein DNA Helicase.
P. E. Boehmer (1998)
J. Biol. Chem. 273, 2676-2683
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The Evolutionarily Conserved Zinc Finger Motif in the Largest Subunit of Human Replication Protein A Is Required for DNA Replication and Mismatch Repair but Not for Nucleotide Excision Repair.
Y.-L. Lin, M. K. K. Shivji, C. Chen, R. Kolodner, R. D. Wood, and A. Dutta (1998)
J. Biol. Chem. 273, 1453-1461
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Mapping of Amino Acid Residues in the p34 Subunit of Human Single-stranded DNA-binding Protein Phosphorylated by DNA-dependent Protein Kinase and Cdc2 Kinase in Vitro.
H. Niu, H. Erdjument-Bromage, Z.-Q. Pan, S.-H. Lee, P. Tempst, and J. Hurwitz (1997)
J. Biol. Chem. 272, 12634-12641
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Role for Cyclin A-dependent Kinase in DNA Replication in Human S Phase Cell Extracts.
A. Fotedar, D. Cannella, P. Fitzgerald, T. Rousselle, S. Gupta, M. Doree, and R. Fotedar (1996)
J. Biol. Chem. 271, 31627-31637
   Abstract »    Full Text »    PDF »
T Antigens Encoded by Replication-defective Simian Virus 40 Mutants dl1135 and 5080.
B. S. Collins and J. M. Pipas (1995)
J. Biol. Chem. 270, 15377-15384
   Abstract »    Full Text »    PDF »
An origin unwinding activity regulates initiation of DNA replication during mammalian cell cycle.
J. Roberts and G D'Urso (1988)
Science 241, 1486-1489
   Abstract »    PDF »
Action at a distance along a DNA.
J. Wang and G. Giaever (1988)
Science 240, 300-304
   Abstract »    PDF »
Protein-Protein Interactions of the Primase Subunits p58 and p48 with Simian Virus 40 T Antigen Are Required for Efficient Primer Synthesis in a Cell-free System.
K. Weisshart, H. Forster, E. Kremmer, B. Schlott, F. Grosse, and H.-P. Nasheuer (2000)
J. Biol. Chem. 275, 17328-17337
   Abstract »    Full Text »    PDF »


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