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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
. 1992 Feb 1;89(3):1055–1059. doi: 10.1073/pnas.89.3.1055

Nonconservative segregation of parental nucleosomes during simian virus 40 chromosome replication in vitro.

K Sugasawa 1, Y Ishimi 1, T Eki 1, J Hurwitz 1, A Kikuchi 1, F Hanaoka 1
PMCID: PMC48384  PMID: 1346554

Abstract

Simian virus 40 chromosomes can be replicated in vitro with the same set of purified proteins required for the replication of naked DNA containing the viral origin. With these reconstituted systems, the fate of parental histones during replication was examined in vitro. The assembly of nucleosomes on replicating chromosomes was hardly affected by the presence of simultaneously replicating naked DNA competitor, suggesting that replication forks can traverse nucleosomes without the displacement of histones. Moreover, we demonstrate that the nascent nucleosomes were distributed almost equally between the leading and lagging strands. This distributive mode of nucleosome segregation favors the propagation of parental chromatin structures to both daughter cells, which can maintain cellular functions dictated by these structures during cell proliferation.

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Selected References

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  1. Albright S. C., Wiseman J. M., Lange R. A., Garrard W. T. Subunit structures of different electrophoretic forms of nucleosomes. J Biol Chem. 1980 Apr 25;255(8):3673–3684. [PubMed] [Google Scholar]
  2. Bauer G. A., Heller H. M., Burgers P. M. DNA polymerase III from Saccharomyces cerevisiae. I. Purification and characterization. J Biol Chem. 1988 Jan 15;263(2):917–924. [PubMed] [Google Scholar]
  3. 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]
  4. Boulet A., Simon M., Faye G., Bauer G. A., Burgers P. M. Structure and function of the Saccharomyces cerevisiae CDC2 gene encoding the large subunit of DNA polymerase III. EMBO J. 1989 Jun;8(6):1849–1854. doi: 10.1002/j.1460-2075.1989.tb03580.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burhans W. C., Vassilev L. T., Wu J., Sogo J. M., Nallaseth F. S., DePamphilis M. L. Emetine allows identification of origins of mammalian DNA replication by imbalanced DNA synthesis, not through conservative nucleosome segregation. EMBO J. 1991 Dec;10(13):4351–4360. doi: 10.1002/j.1460-2075.1991.tb05013.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Cusick M. E., DePamphilis M. L., Wassarman P. M. Dispersive segregation of nucleosomes during replication of simian virus 40 chromosomes. J Mol Biol. 1984 Sep 15;178(2):249–271. doi: 10.1016/0022-2836(84)90143-8. [DOI] [PubMed] [Google Scholar]
  8. Decker R. S., Yamaguchi M., Possenti R., Bradley M. K., DePamphilis M. L. In vitro initiation of DNA replication in simian virus 40 chromosomes. J Biol Chem. 1987 Aug 5;262(22):10863–10872. [PubMed] [Google Scholar]
  9. Handeli S., Klar A., Meuth M., Cedar H. Mapping replication units in animal cells. Cell. 1989 Jun 16;57(6):909–920. doi: 10.1016/0092-8674(89)90329-2. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Ishimi Y., Hirosumi J., Sato W., Sugasawa K., Yokota S., Hanaoka F., Yamada M. Purification and initial characterization of a protein which facilitates assembly of nucleosome-like structure from mammalian cells. Eur J Biochem. 1984 Aug 1;142(3):431–439. doi: 10.1111/j.1432-1033.1984.tb08305.x. [DOI] [PubMed] [Google Scholar]
  12. Ishimi Y., Sugasawa K., Hanaoka F., Kikuchi A. Replication of the simian virus 40 chromosome with purified proteins. J Biol Chem. 1991 Aug 25;266(24):16141–16148. [PubMed] [Google Scholar]
  13. Jackson V. Deposition of newly synthesized histones: hybrid nucleosomes are not tandemly arranged on daughter DNA strands. Biochemistry. 1988 Mar 22;27(6):2109–2120. doi: 10.1021/bi00406a044. [DOI] [PubMed] [Google Scholar]
  14. Jackson V. Deposition of newly synthesized histones: new histones H2A and H2B do not deposit in the same nucleosome with new histones H3 and H4. Biochemistry. 1987 Apr 21;26(8):2315–2325. doi: 10.1021/bi00382a037. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Kenny M. K., Schlegel U., Furneaux H., Hurwitz J. The role of human single-stranded DNA binding protein and its individual subunits in simian virus 40 DNA replication. J Biol Chem. 1990 May 5;265(13):7693–7700. [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Lee S. H., Kwong A. D., Pan Z. Q., Hurwitz J. Studies on the activator 1 protein complex, an accessory factor for proliferating cell nuclear antigen-dependent DNA polymerase delta. J Biol Chem. 1991 Jan 5;266(1):594–602. [PubMed] [Google Scholar]
  21. Leffak I. M. Conservative segregation of nucleosome core histones. Nature. 1984 Jan 5;307(5946):82–85. doi: 10.1038/307082a0. [DOI] [PubMed] [Google Scholar]
  22. O'Reilly D. R., Miller L. K. Expression and complex formation of simian virus 40 large T antigen and mouse p53 in insect cells. J Virol. 1988 Sep;62(9):3109–3119. doi: 10.1128/jvi.62.9.3109-3119.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pospelov V., Russev G., Vassilev L., Tsanev R. Nucleosome segregation in chromatin replicated in the presence of cycloheximide. J Mol Biol. 1982 Mar 25;156(1):79–91. doi: 10.1016/0022-2836(82)90460-0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Riley D., Weintraub H. Conservative segregation of parental histones during replication in the presence of cycloheximide. Proc Natl Acad Sci U S A. 1979 Jan;76(1):328–332. doi: 10.1073/pnas.76.1.328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roufa D. J., Marchionni M. A. Nucleosome segregation at a defined mammalian chromosomal site. Proc Natl Acad Sci U S A. 1982 Mar;79(6):1810–1814. doi: 10.1073/pnas.79.6.1810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Russev G., Hancock R. Assembly of new histones into nucleosomes and their distribution in replicating chromatin. Proc Natl Acad Sci U S A. 1982 May;79(10):3143–3147. doi: 10.1073/pnas.79.10.3143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schlaeger E. J. Replicative conformation of parental nucleosomes: salt sensitivity of deoxyribonucleic acid-histone interaction and alteration of histone H1 binding. Biochemistry. 1982 Jun 22;21(13):3167–3174. doi: 10.1021/bi00256a021. [DOI] [PubMed] [Google Scholar]
  29. Seidman M. M., Levine A. J., Weintraub H. The asymmetric segregation of parental nucleosomes during chrosome replication. Cell. 1979 Oct;18(2):439–449. doi: 10.1016/0092-8674(79)90063-1. [DOI] [PubMed] [Google Scholar]
  30. Senshu T., Yamasu K., Ohsawa T. Fractionation of newly replicated nucleosomes by density labeling and rate zonal centrifugation for the analysis of the deposition sites of newly synthesized nucleosomal core histones. Eur J Biochem. 1985 Aug 1;150(3):575–580. doi: 10.1111/j.1432-1033.1985.tb09059.x. [DOI] [PubMed] [Google Scholar]
  31. Sitney K. C., Budd M. E., Campbell J. L. DNA polymerase III, a second essential DNA polymerase, is encoded by the S. cerevisiae CDC2 gene. Cell. 1989 Feb 24;56(4):599–605. doi: 10.1016/0092-8674(89)90582-5. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Sugasawa K., Murakami Y., Miyamoto N., Hanaoka F., Ui M. Assembly of nascent DNA into nucleosome structures in simian virus 40 chromosomes by HeLa cell extract. J Virol. 1990 Oct;64(10):4820–4829. doi: 10.1128/jvi.64.10.4820-4829.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Todd R. D., Garrard W. T. Two-dimensional electrophoretic analysis of polynucleosomes. J Biol Chem. 1977 Jul 10;252(13):4729–4738. [PubMed] [Google Scholar]
  36. Tsurimoto T., Melendy T., Stillman B. 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):534–539. doi: 10.1038/346534a0. [DOI] [PubMed] [Google Scholar]
  37. Tsurimoto T., Stillman B. Multiple replication factors augment DNA synthesis by the two eukaryotic DNA polymerases, alpha and delta. EMBO J. 1989 Dec 1;8(12):3883–3889. doi: 10.1002/j.1460-2075.1989.tb08567.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weinberg D. H., Kelly T. J. 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):9742–9746. doi: 10.1073/pnas.86.24.9742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. 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]

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