Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 Dec;86(24):9757–9761. doi: 10.1073/pnas.86.24.9757

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.

M K Kenny 1, S H Lee 1, J Hurwitz 1
PMCID: PMC298580  PMID: 2557626

Abstract

The human single-stranded-DNA binding protein (human SSB) is required for simian virus 40 (SV40) DNA replication in vitro. SV40 large tumor antigen and human SSB can support extensive unwinding of SV40 origin-containing DNA in the presence of ATP and a topoisomerase that relieves positive superhelicity. Although SSBs from viral and prokaryotic sources substituted for human SSB in the DNA-unwinding reaction, they did not substitute in the replication of SV40 DNA. The specificity for human SSB in SV40 DNA replication can be explained, at least in part, by the finding that DNA polymerase alpha was stimulated 10-fold by human SSB but not by other SSBs. Human SSB also stimulated proliferating-cell nuclear antigen-dependent DNA polymerase delta; however, other SSBs stimulated this polymerase as well.

Full text

PDF
9761

Images in this article

9758Image
on p.9758

Selected References

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

  1. Alberts B. M., Frey L. T4 bacteriophage gene 32: a structural protein in the replication and recombination of DNA. Nature. 1970 Sep 26;227(5265):1313–1318. doi: 10.1038/2271313a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Borowiec J. A., Hurwitz J. Localized melting and structural changes in the SV40 origin of replication induced by T-antigen. EMBO J. 1988 Oct;7(10):3149–3158. doi: 10.1002/j.1460-2075.1988.tb03182.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bullock P. A., Seo Y. S., Hurwitz J. Initiation of simian virus 40 DNA replication in vitro: pulse-chase experiments identify the first labeled species as topologically unwound. Proc Natl Acad Sci U S A. 1989 Jun;86(11):3944–3948. doi: 10.1073/pnas.86.11.3944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Challberg M. D., Kelly T. J. Animal virus DNA replication. Annu Rev Biochem. 1989;58:671–717. doi: 10.1146/annurev.bi.58.070189.003323. [DOI] [PubMed] [Google Scholar]
  6. Chang L. M., Lurie K., Plevani P. A stimulatory factor for yeast DNA polymerase. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):587–595. doi: 10.1101/sqb.1979.043.01.065. [DOI] [PubMed] [Google Scholar]
  7. Chase J. W., Williams K. R. Single-stranded DNA binding proteins required for DNA replication. Annu Rev Biochem. 1986;55:103–136. doi: 10.1146/annurev.bi.55.070186.000535. [DOI] [PubMed] [Google Scholar]
  8. Dean F. B., Borowiec J. A., Ishimi Y., Deb S., Tegtmeyer P., Hurwitz J. 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):8267–8271. doi: 10.1073/pnas.84.23.8267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dean F. B., Bullock P., Murakami Y., Wobbe C. R., Weissbach L., Hurwitz J. 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. doi: 10.1073/pnas.84.1.16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dean F. B., Dodson M., Echols H., Hurwitz J. 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):8981–8985. doi: 10.1073/pnas.84.24.8981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Dodson M., Dean F. B., Bullock P., Echols H., Hurwitz J. Unwinding of duplex DNA from the SV40 origin of replication by T antigen. Science. 1987 Nov 13;238(4829):964–967. doi: 10.1126/science.2823389. [DOI] [PubMed] [Google Scholar]
  13. Fairman M. P., Stillman B. Cellular factors required for multiple stages of SV40 DNA replication in vitro. EMBO J. 1988 Apr;7(4):1211–1218. doi: 10.1002/j.1460-2075.1988.tb02933.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fay P. J., Johanson K. O., McHenry C. S., Bambara R. A. Size classes of products synthesized processively by DNA polymerase III and DNA polymerase III holoenzyme of Escherichia coli. J Biol Chem. 1981 Jan 25;256(2):976–983. [PubMed] [Google Scholar]
  15. Fay P. J., Johanson K. O., McHenry C. S., Bambara R. A. Size classes of products synthesized processively by two subassemblies of Escherichia coli DNA polymerase III holoenzyme. J Biol Chem. 1982 May 25;257(10):5692–5699. [PubMed] [Google Scholar]
  16. Fowlkes D. M., Lord S. T., Linné T., Pettersson U., Philipson L. Interaction between the adenovirus DNA-binding protein and double-stranded DNA. J Mol Biol. 1979 Aug 5;132(2):163–180. doi: 10.1016/0022-2836(79)90389-9. [DOI] [PubMed] [Google Scholar]
  17. Guo Z. S., Gutierrez C., Heine U., Sogo J. M., Depamphilis M. L. Origin auxiliary sequences can facilitate initiation of simian virus 40 DNA replication in vitro as they do in vivo. Mol Cell Biol. 1989 Sep;9(9):3593–3602. doi: 10.1128/mcb.9.9.3593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hay R. T., Russell W. C. Recognition mechanisms in the synthesis of animal virus DNA. Biochem J. 1989 Feb 15;258(1):3–16. doi: 10.1042/bj2580003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Herrick G., Alberts B. Nucleic acid helix-coil transitions mediated by helix-unwinding proteins from calf thymus. J Biol Chem. 1976 Apr 10;251(7):2133–2141. [PubMed] [Google Scholar]
  20. Herrick G., Alberts B. Purification and physical characterization of nucleic acid helix-unwinding proteins from calf thymus. J Biol Chem. 1976 Apr 10;251(7):2124–2132. [PubMed] [Google Scholar]
  21. Herrick G., Delius H., Alberts B. Single-stranded DNA structure and DNA polymerase activity in the presence of nucleic acid helix-unwinding proteins from calf thymus. J Biol Chem. 1976 Apr 10;251(7):2142–2146. [PubMed] [Google Scholar]
  22. Hurwitz J., Wickner S. Involvement of two protein factors and ATP in in vitro DNA synthesis catalyzed by DNA polymerase 3 of Escherichia coli. Proc Natl Acad Sci U S A. 1974 Jan;71(1):6–10. doi: 10.1073/pnas.71.1.6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ikeda J. E., Enomoto T., Hurwitz J. Replication of adenovirus DNA-protein complex with purified proteins. Proc Natl Acad Sci U S A. 1981 Feb;78(2):884–888. doi: 10.1073/pnas.78.2.884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ishimi Y., Claude A., Bullock P., Hurwitz J. Complete enzymatic synthesis of DNA containing the SV40 origin of replication. J Biol Chem. 1988 Dec 25;263(36):19723–19733. [PubMed] [Google Scholar]
  25. Jong A. Y., Aebersold R., Campbell J. L. Multiple species of single-stranded nucleic acid-binding proteins in Saccharomyces cerevisiae. J Biol Chem. 1985 Dec 25;260(30):16367–16374. [PubMed] [Google Scholar]
  26. Kelly T. J. SV40 DNA replication. J Biol Chem. 1988 Dec 5;263(34):17889–17892. [PubMed] [Google Scholar]
  27. LaBonne S. G., Dumas L. B. Isolation of a yeast single-strand deoxyribonucleic acid binding protein that specifically stimulates yeast DNA polymerase I. Biochemistry. 1983 Jun 21;22(13):3214–3219. doi: 10.1021/bi00282a027. [DOI] [PubMed] [Google Scholar]
  28. Lamothe P., Baril B., Chi A., Lee L., Baril E. Accessory proteins for DNA polymerase alpha activity with single-strand DNA templates. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4723–4727. doi: 10.1073/pnas.78.8.4723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lee S. H., Eki T., Hurwitz J. 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):7361–7365. doi: 10.1073/pnas.86.19.7361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lee S. H., Ishimi Y., Kenny M. K., Bullock P., Dean F. B., Hurwitz J. An inhibitor of the in vitro elongation reaction of simian virus 40 DNA replication is overcome by proliferating-cell nuclear antigen. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9469–9473. doi: 10.1073/pnas.85.24.9469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lee S. H., Kwong A. D., Ishimi Y., Hurwitz J. Studies on the DNA elongation inhibitor and its proliferating cell nuclear antigen-dependent control in simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4877–4881. doi: 10.1073/pnas.86.13.4877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Li J. J., Kelly T. J. Simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A. 1984 Nov;81(22):6973–6977. doi: 10.1073/pnas.81.22.6973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Murakami Y., Wobbe C. R., Weissbach L., Dean F. B., Hurwitz J. 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):2869–2873. doi: 10.1073/pnas.83.9.2869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Prelich G., Kostura M., Marshak D. R., Mathews M. B., Stillman B. The cell-cycle regulated proliferating cell nuclear antigen is required for SV40 DNA replication in vitro. Nature. 1987 Apr 2;326(6112):471–475. doi: 10.1038/326471a0. [DOI] [PubMed] [Google Scholar]
  36. Prelich G., Stillman B. Coordinated leading and lagging strand synthesis during SV40 DNA replication in vitro requires PCNA. Cell. 1988 Apr 8;53(1):117–126. doi: 10.1016/0092-8674(88)90493-x. [DOI] [PubMed] [Google Scholar]
  37. Pritchard C. G., DePamphilis M. L. Preparation of DNA polymerase alpha X C1C2 by reconstituting DNA polymerase alpha with its specific stimulatory cofactors, C1C2. J Biol Chem. 1983 Aug 25;258(16):9801–9809. [PubMed] [Google Scholar]
  38. Roberts J. M., D'Urso G. An origin unwinding activity regulates initiation of DNA replication during mammalian cell cycle. Science. 1988 Sep 16;241(4872):1486–1489. doi: 10.1126/science.2843984. [DOI] [PubMed] [Google Scholar]
  39. Sapp M., König H., Riedel H. D., Richter A., Knippers R. A newly detected class of mammalian single strand-specific DNA-binding proteins. Effects on DNA polymerase alpha-catalyzed DNA synthesis. J Biol Chem. 1985 Feb 10;260(3):1550–1556. [PubMed] [Google Scholar]
  40. Smith S., Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell. 1989 Jul 14;58(1):15–25. doi: 10.1016/0092-8674(89)90398-x. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. Stillman B. Initiation of eukaryotic DNA replication in vitro. Annu Rev Cell Biol. 1989;5:197–245. doi: 10.1146/annurev.cb.05.110189.001213. [DOI] [PubMed] [Google Scholar]
  43. Tsurimoto T., Stillman B. Purification of a cellular replication factor, RF-C, that is required for coordinated synthesis of leading and lagging strands during simian virus 40 DNA replication in vitro. Mol Cell Biol. 1989 Feb;9(2):609–619. doi: 10.1128/mcb.9.2.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Valentini O., Biamonti G., Pandolfo M., Morandi C., Riva S. Mammalian single-stranded DNA binding proteins and heterogeneous nuclear RNA proteins have common antigenic determinants. Nucleic Acids Res. 1985 Jan 25;13(2):337–346. doi: 10.1093/nar/13.2.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Virshup D. M., Kelly T. J. Purification of replication protein C, a cellular protein involved in the initial stages of simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A. 1989 May;86(10):3584–3588. doi: 10.1073/pnas.86.10.3584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wickner S. Mechanism of DNA elongation catalyzed by Escherichia coli DNA polymerase III, dnaZ protein, and DNA elongation factors I and III. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3511–3515. doi: 10.1073/pnas.73.10.3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wickner W., Kornberg A. DNA polymerase 3 star requires ATP to start synthesis on a primed DNA. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3679–3683. doi: 10.1073/pnas.70.12.3679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wobbe C. R., Dean F., Weissbach L., Hurwitz J. 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):5710–5714. doi: 10.1073/pnas.82.17.5710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wobbe C. R., Weissbach L., Borowiec J. A., Dean F. B., Murakami Y., Bullock P., Hurwitz J. Replication of simian virus 40 origin-containing DNA in vitro with purified proteins. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1834–1838. doi: 10.1073/pnas.84.7.1834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. 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]
  51. Wold M. S., Li J. J., Kelly T. J. 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):3643–3647. doi: 10.1073/pnas.84.11.3643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wold M. S., Weinberg D. H., Virshup D. M., Li J. J., Kelly T. J. Identification of cellular proteins required for simian virus 40 DNA replication. J Biol Chem. 1989 Feb 15;264(5):2801–2809. [PubMed] [Google Scholar]
  53. 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]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES