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. 1995 Jul 3;14(13):3215–3225. doi: 10.1002/j.1460-2075.1995.tb07324.x

Unwinding of chromatin by the SV40 large T antigen DNA helicase.

U Ramsperger 1, H Stahl 1
PMCID: PMC394383  PMID: 7621834

Abstract

We have analysed the unwinding of nucleosomally organized DNA by simian virus 40 large tumour (T) antigen. Isolated T antigen can bind to existing nucleosome cores containing the viral replication origin sequence, which results in displacement of the histone octamer and unwinding of the DNA. However, specific binding to nucleosome cores is salt sensitive and nearly completely blocked under ionic conditions that otherwise support DNA replication. Once started, the progressing T antigen helicase, like an elongating RNA polymerase, is not further repressed by histone octamers, irrespective of the presence or absence of linker histone H1. Disruption of the nucleosomal structure in the process of unwinding may be assisted by the demonstrated interaction of the hexameric T antigen complex with histone proteins H1 and H3. Finally, our studies reveal the inability of topoisomerase I and/or II to continually relieve the superhelical tension of covalently closed circular minichromosomes as generated during their unwinding by T antigen. This may indicate that chromatin relaxation during the process of DNA replication can only be efficiently performed by a topoisomerase that is (trans)activated by other factors.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams C. C., Workman J. L. Nucleosome displacement in transcription. Cell. 1993 Feb 12;72(3):305–308. doi: 10.1016/0092-8674(93)90109-4. [DOI] [PubMed] [Google Scholar]
  2. Avemann K., Knippers R., Koller T., Sogo J. M. Camptothecin, a specific inhibitor of type I DNA topoisomerase, induces DNA breakage at replication forks. Mol Cell Biol. 1988 Aug;8(8):3026–3034. doi: 10.1128/mcb.8.8.3026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baer B. W., Rhodes D. Eukaryotic RNA polymerase II binds to nucleosome cores from transcribed genes. Nature. 1983 Feb 10;301(5900):482–488. doi: 10.1038/301482a0. [DOI] [PubMed] [Google Scholar]
  4. Beard P., Kaneko M., Cerutti P. N-Acetoxy-acetylaminofluorene reacts preferentially with a control region of intracellular SV40 chromosome. Nature. 1981 May 7;291(5810):84–85. doi: 10.1038/291084a0. [DOI] [PubMed] [Google Scholar]
  5. Bedinger P., Hochstrasser M., Jongeneel C. V., Alberts B. M. Properties of the T4 bacteriophage DNA replication apparatus: the T4 dda DNA helicase is required to pass a bound RNA polymerase molecule. Cell. 1983 Aug;34(1):115–123. doi: 10.1016/0092-8674(83)90141-1. [DOI] [PubMed] [Google Scholar]
  6. Bonne-Andrea C., Wong M. L., Alberts B. M. In vitro replication through nucleosomes without histone displacement. Nature. 1990 Feb 22;343(6260):719–726. doi: 10.1038/343719a0. [DOI] [PubMed] [Google Scholar]
  7. Borowiec J. A., Dean F. B., Bullock P. A., Hurwitz J. Binding and unwinding--how T antigen engages the SV40 origin of DNA replication. Cell. 1990 Jan 26;60(2):181–184. doi: 10.1016/0092-8674(90)90730-3. [DOI] [PubMed] [Google Scholar]
  8. Borowiec J. A., Hurwitz J. 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):64–68. doi: 10.1073/pnas.85.1.64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bradbury E. M. Reversible histone modifications and the chromosome cell cycle. Bioessays. 1992 Jan;14(1):9–16. doi: 10.1002/bies.950140103. [DOI] [PubMed] [Google Scholar]
  10. Capranico G., Jaxel C., Roberge M., Kohn K. W., Pommier Y. Nucleosome positioning as a critical determinant for the DNA cleavage sites of mammalian DNA topoisomerase II in reconstituted simian virus 40 chromatin. Nucleic Acids Res. 1990 Aug 11;18(15):4553–4559. doi: 10.1093/nar/18.15.4553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cheng L. Z., Workman J. L., Kingston R. E., Kelly T. J. Regulation of DNA replication in vitro by the transcriptional activation domain of GAL4-VP16. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):589–593. doi: 10.1073/pnas.89.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cheng L., Kelly T. J. Transcriptional activator nuclear factor I stimulates the replication of SV40 minichromosomes in vivo and in vitro. Cell. 1989 Nov 3;59(3):541–551. doi: 10.1016/0092-8674(89)90037-8. [DOI] [PubMed] [Google Scholar]
  13. Clark D. J., Felsenfeld G. A nucleosome core is transferred out of the path of a transcribing polymerase. Cell. 1992 Oct 2;71(1):11–22. doi: 10.1016/0092-8674(92)90262-b. [DOI] [PubMed] [Google Scholar]
  14. Clark D. J., Felsenfeld G. Formation of nucleosomes on positively supercoiled DNA. EMBO J. 1991 Feb;10(2):387–395. doi: 10.1002/j.1460-2075.1991.tb07960.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. DeLucia A. L., Deb S., Partin K., Tegtmeyer P. Functional interactions of the simian virus 40 core origin of replication with flanking regulatory sequences. J Virol. 1986 Jan;57(1):138–144. doi: 10.1128/jvi.57.1.138-144.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DePamphilis M. L. Eukaryotic DNA replication: anatomy of an origin. Annu Rev Biochem. 1993;62:29–63. doi: 10.1146/annurev.bi.62.070193.000333. [DOI] [PubMed] [Google Scholar]
  17. DePamphilis M. L. Transcriptional elements as components of eukaryotic origins of DNA replication. Cell. 1988 Mar 11;52(5):635–638. doi: 10.1016/0092-8674(88)90398-4. [DOI] [PubMed] [Google Scholar]
  18. Dean F. B., Borowiec J. A., Eki T., Hurwitz J. The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin. J Biol Chem. 1992 Jul 15;267(20):14129–14137. [PubMed] [Google Scholar]
  19. Deb S. P., Tegtmeyer P. ATP enhances the binding of simian virus 40 large T antigen to the origin of replication. J Virol. 1987 Dec;61(12):3649–3654. doi: 10.1128/jvi.61.12.3649-3654.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dilworth S. M., Black S. J., Laskey R. A. Two complexes that contain histones are required for nucleosome assembly in vitro: role of nucleoplasmin and N1 in Xenopus egg extracts. Cell. 1987 Dec 24;51(6):1009–1018. doi: 10.1016/0092-8674(87)90587-3. [DOI] [PubMed] [Google Scholar]
  21. Dornreiter I., Höss A., Arthur A. K., Fanning E. SV40 T antigen binds directly to the large subunit of purified DNA polymerase alpha. EMBO J. 1990 Oct;9(10):3329–3336. doi: 10.1002/j.1460-2075.1990.tb07533.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Dunn S. D. Effects of the modification of transfer buffer composition and the renaturation of proteins in gels on the recognition of proteins on Western blots by monoclonal antibodies. Anal Biochem. 1986 Aug 15;157(1):144–153. doi: 10.1016/0003-2697(86)90207-1. [DOI] [PubMed] [Google Scholar]
  23. Dutta A., Ruppert J. M., Aster J. C., Winchester E. Inhibition of DNA replication factor RPA by p53. Nature. 1993 Sep 2;365(6441):79–82. doi: 10.1038/365079a0. [DOI] [PubMed] [Google Scholar]
  24. Fanning E., Knippers R. Structure and function of simian virus 40 large tumor antigen. Annu Rev Biochem. 1992;61:55–85. doi: 10.1146/annurev.bi.61.070192.000415. [DOI] [PubMed] [Google Scholar]
  25. Felsenfeld G. Chromatin as an essential part of the transcriptional mechanism. Nature. 1992 Jan 16;355(6357):219–224. doi: 10.1038/355219a0. [DOI] [PubMed] [Google Scholar]
  26. Fiers W., Contreras R., Haegemann G., Rogiers R., Van de Voorde A., Van Heuverswyn H., Van Herreweghe J., Volckaert G., Ysebaert M. Complete nucleotide sequence of SV40 DNA. Nature. 1978 May 11;273(5658):113–120. doi: 10.1038/273113a0. [DOI] [PubMed] [Google Scholar]
  27. Gale K. C., Osheroff N. Uncoupling the DNA cleavage and religation activities of topoisomerase II with a single-stranded nucleic acid substrate: evidence for an active enzyme-cleaved DNA intermediate. Biochemistry. 1990 Oct 16;29(41):9538–9545. doi: 10.1021/bi00493a007. [DOI] [PubMed] [Google Scholar]
  28. Gross D. S., Garrard W. T. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159–197. doi: 10.1146/annurev.bi.57.070188.001111. [DOI] [PubMed] [Google Scholar]
  29. Grunstein M. Histone function in transcription. Annu Rev Cell Biol. 1990;6:643–678. doi: 10.1146/annurev.cb.06.110190.003235. [DOI] [PubMed] [Google Scholar]
  30. Gruss C., Sogo J. M. Chromatin replication. Bioessays. 1992 Jan;14(1):1–8. doi: 10.1002/bies.950140102. [DOI] [PubMed] [Google Scholar]
  31. Gruss C., Wu J., Koller T., Sogo J. M. Disruption of the nucleosomes at the replication fork. EMBO J. 1993 Dec;12(12):4533–4545. doi: 10.1002/j.1460-2075.1993.tb06142.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Gurney E. G., Harrison R. O., Fenno J. 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):752–763. doi: 10.1128/jvi.34.3.752-763.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hamelin C., D'Amours B., Pagé C., Chung Y. S. DNA topoisomerase activity associated with simian virus 40 nucleoprotein complexes. Biochem Cell Biol. 1994 May-Jun;72(5-6):195–201. doi: 10.1139/o94-029. [DOI] [PubMed] [Google Scholar]
  34. He Z., Brinton B. T., Greenblatt J., Hassell J. A., Ingles C. J. The transactivator proteins VP16 and GAL4 bind replication factor A. Cell. 1993 Jun 18;73(6):1223–1232. doi: 10.1016/0092-8674(93)90650-f. [DOI] [PubMed] [Google Scholar]
  35. Hertz G. Z., Mertz J. E. Bidirectional promoter elements of simian virus 40 are required for efficient replication of the viral DNA. Mol Cell Biol. 1986 Oct;6(10):3513–3522. doi: 10.1128/mcb.6.10.3513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ishimi Y. Preincubation of T antigen with DNA overcomes repression of SV40 DNA replication by nucleosome assembly. J Biol Chem. 1992 May 25;267(15):10910–10913. [PubMed] [Google Scholar]
  37. Jackson V. In vivo studies on the dynamics of histone-DNA interaction: evidence for nucleosome dissolution during replication and transcription and a low level of dissolution independent of both. Biochemistry. 1990 Jan 23;29(3):719–731. doi: 10.1021/bi00455a019. [DOI] [PubMed] [Google Scholar]
  38. Jackson V. Studies on histone organization in the nucleosome using formaldehyde as a reversible cross-linking agent. Cell. 1978 Nov;15(3):945–954. doi: 10.1016/0092-8674(78)90278-7. [DOI] [PubMed] [Google Scholar]
  39. Jakobovits E. B., Bratosin S., Aloni Y. A nucleosome-free region in SV40 minichromosomes. Nature. 1980 May 22;285(5762):263–265. doi: 10.1038/285263a0. [DOI] [PubMed] [Google Scholar]
  40. Kelly T. J. SV40 DNA replication. J Biol Chem. 1988 Dec 5;263(34):17889–17892. [PubMed] [Google Scholar]
  41. Kleinschmidt J. A., Steinbeisser H. DNA-dependent phosphorylation of histone H2A.X during nucleosome assembly in Xenopus laevis oocytes: involvement of protein phosphorylation in nucleosome spacing. EMBO J. 1991 Oct;10(10):3043–3050. doi: 10.1002/j.1460-2075.1991.tb07855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kornberg R. D., Lorch Y. Irresistible force meets immovable object: transcription and the nucleosome. Cell. 1991 Nov 29;67(5):833–836. doi: 10.1016/0092-8674(91)90354-2. [DOI] [PubMed] [Google Scholar]
  43. Krude T., Knippers R. Transfer of nucleosomes from parental to replicated chromatin. Mol Cell Biol. 1991 Dec;11(12):6257–6267. doi: 10.1128/mcb.11.12.6257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  45. Lanford R. E. Expression of simian virus 40 T antigen in insect cells using a baculovirus expression vector. Virology. 1988 Nov;167(1):72–81. doi: 10.1016/0042-6822(88)90055-4. [DOI] [PubMed] [Google Scholar]
  46. Lee-Chen G. J., Woodworth-Gutai M. Simian virus 40 DNA replication: functional organization of regulatory elements. Mol Cell Biol. 1986 Sep;6(9):3086–3093. doi: 10.1128/mcb.6.9.3086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Lee M. S., Garrard W. T. Transcription-induced nucleosome 'splitting': an underlying structure for DNase I sensitive chromatin. EMBO J. 1991 Mar;10(3):607–615. doi: 10.1002/j.1460-2075.1991.tb07988.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Linxweiler W., Hörz W. Reconstitution of mononucleosomes: characterization of distinct particles that differ in the position of the histone core. Nucleic Acids Res. 1984 Dec 21;12(24):9395–9413. doi: 10.1093/nar/12.24.9395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Lässle M., Richter A., Knippers R. Comparison of replicative and non-replicative chromatin assembly pathways in HeLa cell extracts. Biochim Biophys Acta. 1992 Aug 17;1132(1):1–10. doi: 10.1016/0167-4781(92)90045-2. [DOI] [PubMed] [Google Scholar]
  50. Mann K. Topoisomerase activity is associated with purified SV40 T antigen. Nucleic Acids Res. 1993 Apr 25;21(8):1697–1704. doi: 10.1093/nar/21.8.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Marton A., Jean D., Delbecchi L., Simmons D. T., Bourgaux P. Topoisomerase activity associated with SV40 large tumor antigen. Nucleic Acids Res. 1993 Apr 25;21(8):1689–1695. doi: 10.1093/nar/21.8.1689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Mastrangelo I. A., Hough P. V., Wall J. S., Dodson M., Dean F. B., Hurwitz J. ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication. Nature. 1989 Apr 20;338(6217):658–662. doi: 10.1038/338658a0. [DOI] [PubMed] [Google Scholar]
  53. Miskimins W. K., Roberts M. P., McClelland A., Ruddle F. H. Use of a protein-blotting procedure and a specific DNA probe to identify nuclear proteins that recognize the promoter region of the transferrin receptor gene. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6741–6744. doi: 10.1073/pnas.82.20.6741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Moarefi I. F., Small D., Gilbert I., Höpfner M., Randall S. K., Schneider C., Russo A. A., Ramsperger U., Arthur A. K., Stahl H. 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. doi: 10.1128/jvi.67.8.4992-5002.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Mohr I. J., Stillman B., Gluzman Y. Regulation of SV40 DNA replication by phosphorylation of T antigen. EMBO J. 1987 Jan;6(1):153–160. doi: 10.1002/j.1460-2075.1987.tb04733.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Morse R. H. Transcribed chromatin. Trends Biochem Sci. 1992 Jan;17(1):23–26. doi: 10.1016/0968-0004(92)90422-6. [DOI] [PubMed] [Google Scholar]
  57. Müller U., Zentgraf H., Eicken I., Keller W. Higher order structure of simian virus 40 chromatin. Science. 1978 Aug 4;201(4354):406–415. doi: 10.1126/science.208155. [DOI] [PubMed] [Google Scholar]
  58. Palter K. B., Foe V. E., Alberts B. M. Evidence for the formation of nucleosome-like histone complexes on single-stranded DNA. Cell. 1979 Oct;18(2):451–467. doi: 10.1016/0092-8674(79)90064-3. [DOI] [PubMed] [Google Scholar]
  59. Parsons R., Anderson M. E., Tegtmeyer P. 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):509–518. doi: 10.1128/jvi.64.2.509-518.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Parsons R., Tegtmeyer P. Spacing is crucial for coordination of domain functions within the simian virus 40 core origin of replication. J Virol. 1992 Apr;66(4):1933–1942. doi: 10.1128/jvi.66.4.1933-1942.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Pfaffle P., Gerlach V., Bunzel L., Jackson V. In vitro evidence that transcription-induced stress causes nucleosome dissolution and regeneration. J Biol Chem. 1990 Oct 5;265(28):16830–16840. [PubMed] [Google Scholar]
  62. Randall S. K., Kelly T. J. The fate of parental nucleosomes during SV40 DNA replication. J Biol Chem. 1992 Jul 15;267(20):14259–14265. [PubMed] [Google Scholar]
  63. Richter A., Ruff J. DNA topoisomerase I cleavage sites in DNA and in nucleoprotein complexes. Biochemistry. 1991 Oct 8;30(40):9741–9748. doi: 10.1021/bi00104a025. [DOI] [PubMed] [Google Scholar]
  64. Robinson G. W., Hallick L. M. Mapping the in vivo arrangement of nucleosomes on simian virus 40 chromatin by the photoaddition of radioactive hydroxymethyltrimethylpsoralen. J Virol. 1982 Jan;41(1):78–87. doi: 10.1128/jvi.41.1.78-87.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Saragosti S., Moyne G., Yaniv M. Absence of nucleosomes in a fraction of SV40 chromatin between the origin of replication and the region coding for the late leader RNA. Cell. 1980 May;20(1):65–73. doi: 10.1016/0092-8674(80)90235-4. [DOI] [PubMed] [Google Scholar]
  66. Scheffner M., Wessel R., Stahl H. Sequence independent duplex DNA opening reaction catalysed by SV40 large tumor antigen. Nucleic Acids Res. 1989 Jan 11;17(1):93–106. doi: 10.1093/nar/17.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Schreier A. A., Gruber J. Viral T-antigen interactions with cellular proto-oncogene and anti-oncogene products. J Natl Cancer Inst. 1990 Mar 7;82(5):354–360. doi: 10.1093/jnci/82.5.354. [DOI] [PubMed] [Google Scholar]
  68. SenGupta D. J., Borowiec J. A. 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):982–992. doi: 10.1002/j.1460-2075.1994.tb06343.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. SenGupta D. J., Borowiec J. A. Strand-specific recognition of a synthetic DNA replication fork by the SV40 large tumor antigen. Science. 1992 Jun 19;256(5064):1656–1661. doi: 10.1126/science.256.5064.1656. [DOI] [PubMed] [Google Scholar]
  70. Shimamura A., Tremethick D., Worcel A. Characterization of the repressed 5S DNA minichromosomes assembled in vitro with a high-speed supernatant of Xenopus laevis oocytes. Mol Cell Biol. 1988 Oct;8(10):4257–4269. doi: 10.1128/mcb.8.10.4257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Simpson R. T. Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature. 1990 Jan 25;343(6256):387–389. doi: 10.1038/343387a0. [DOI] [PubMed] [Google Scholar]
  72. Smith M. M. Histone structure and function. Curr Opin Cell Biol. 1991 Jun;3(3):429–437. doi: 10.1016/0955-0674(91)90070-f. [DOI] [PubMed] [Google Scholar]
  73. Sogo J. M., Stahl H., Koller T., Knippers R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol. 1986 May 5;189(1):189–204. doi: 10.1016/0022-2836(86)90390-6. [DOI] [PubMed] [Google Scholar]
  74. Solomon M. J., Varshavsky A. Formaldehyde-mediated DNA-protein crosslinking: a probe for in vivo chromatin structures. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6470–6474. doi: 10.1073/pnas.82.19.6470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Stahl H., Dröge P., Knippers R. DNA helicase activity of SV40 large tumor antigen. EMBO J. 1986 Aug;5(8):1939–1944. doi: 10.1002/j.1460-2075.1986.tb04447.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Stahl H., Dröge P., Zentgraf H., Knippers R. A large-tumor-antigen-specific monoclonal antibody inhibits DNA replication of simian virus 40 minichromosomes in an in vitro elongation system. J Virol. 1985 May;54(2):473–482. doi: 10.1128/jvi.54.2.473-482.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Strausfeld U., Richter A. Simultaneous purification of DNA topoisomerase I and II from eukaryotic cells. Prep Biochem. 1989;19(1):37–48. doi: 10.1080/10826068908544895. [DOI] [PubMed] [Google Scholar]
  78. Studitsky V. M., Clark D. J., Felsenfeld G. A histone octamer can step around a transcribing polymerase without leaving the template. Cell. 1994 Jan 28;76(2):371–382. doi: 10.1016/0092-8674(94)90343-3. [DOI] [PubMed] [Google Scholar]
  79. Sugasawa K., Ishimi Y., Eki T., Hurwitz J., Kikuchi A., Hanaoka F. Nonconservative segregation of parental nucleosomes during simian virus 40 chromosome replication in vitro. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):1055–1059. doi: 10.1073/pnas.89.3.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol. 1979 Nov;83(2 Pt 1):403–427. doi: 10.1083/jcb.83.2.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Varshavsky A. J., Sundin O. H., Bohn M. J. SV40 viral minichromosome: preferential exposure of the origin of replication as probed by restriction endonucleases. Nucleic Acids Res. 1978 Oct;5(10):3469–3477. doi: 10.1093/nar/5.10.3469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Vollenweider H. J., Sogo J. M., Koller T. A routine method for protein-free spreading of double- and single-stranded nucleic acid molecules. Proc Natl Acad Sci U S A. 1975 Jan;72(1):83–87. doi: 10.1073/pnas.72.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Waga S., Stillman B. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature. 1994 May 19;369(6477):207–212. doi: 10.1038/369207a0. [DOI] [PubMed] [Google Scholar]
  84. Wessel R., Müller H., Hoffmann-Berling H. Electron microscopy of DNA.helicase-I complexes in the act of strand separation. Eur J Biochem. 1990 Apr 30;189(2):277–285. doi: 10.1111/j.1432-1033.1990.tb15487.x. [DOI] [PubMed] [Google Scholar]
  85. Wessel R., Schweizer J., Stahl H. 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):804–815. doi: 10.1128/jvi.66.2.804-815.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Wiekowski M., Dröge P., Stahl H. Monoclonal antibodies as probes for a function of large T antigen during the elongation process of simian virus 40 DNA replication. J Virol. 1987 Feb;61(2):411–418. doi: 10.1128/jvi.61.2.411-418.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Wold M. S., Kelly T. 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):2523–2527. doi: 10.1073/pnas.85.8.2523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Wolffe A. P. Transcription: in tune with the histones. Cell. 1994 Apr 8;77(1):13–16. doi: 10.1016/0092-8674(94)90229-1. [DOI] [PubMed] [Google Scholar]
  89. Worcel A., Han S., Wong M. L. Assembly of newly replicated chromatin. Cell. 1978 Nov;15(3):969–977. doi: 10.1016/0092-8674(78)90280-5. [DOI] [PubMed] [Google Scholar]
  90. Workman J. L., Kingston R. E. Nucleosome core displacement in vitro via a metastable transcription factor-nucleosome complex. Science. 1992 Dec 11;258(5089):1780–1784. doi: 10.1126/science.1465613. [DOI] [PubMed] [Google Scholar]
  91. Wray W., Boulikas T., Wray V. P., Hancock R. Silver staining of proteins in polyacrylamide gels. Anal Biochem. 1981 Nov 15;118(1):197–203. doi: 10.1016/0003-2697(81)90179-2. [DOI] [PubMed] [Google Scholar]
  92. Yancey-Wrona J. E., Matson S. W. Bound Lac repressor protein differentially inhibits the unwinding reactions catalyzed by DNA helicases. Nucleic Acids Res. 1992 Dec 25;20(24):6713–6721. doi: 10.1093/nar/20.24.6713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Yang L., Wold M. S., Li J. J., Kelly T. J., Liu L. F. Roles of DNA topoisomerases in simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A. 1987 Feb;84(4):950–954. doi: 10.1073/pnas.84.4.950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. van Holde K. E., Lohr D. E., Robert C. What happens to nucleosomes during transcription? J Biol Chem. 1992 Feb 15;267(5):2837–2840. [PubMed] [Google Scholar]

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