Cell cycle modulation of protein-DNA interactions at a human replication origin (original) (raw)
Abstract
We followed the variations of protein-DNA interactions occurring in vivo over the early firing replication origin located near the human lamin B2 gene, in IMR-90 cells synchronized in different moments of the cell cycle. In G0 phase cells no protection is present; as the cells progress in G1 phase an extended footprint covering over 100 bp appears, particularly marked at the G1/S border. As the cells enter S phase the protection shrinks to 70 bp and remains unchanged throughout this phase. In mitosis the protection totally disappears, only to reappear in its extended form as the cells move into the next G1. These variations are reminiscent of those corresponding to the formation of the pre- and post-replicative complexes described in yeast and Xenopus cells.
Full Text
The Full Text of this article is available as a PDF (464.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aparicio O. M., Weinstein D. M., Bell S. P. Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell. 1997 Oct 3;91(1):59–69. doi: 10.1016/s0092-8674(01)80009-x. [DOI] [PubMed] [Google Scholar]
- Bell S. P., Stillman B. ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature. 1992 May 14;357(6374):128–134. doi: 10.1038/357128a0. [DOI] [PubMed] [Google Scholar]
- Burhans W. C., Vassilev L. T., Caddle M. S., Heintz N. H., DePamphilis M. L. Identification of an origin of bidirectional DNA replication in mammalian chromosomes. Cell. 1990 Sep 7;62(5):955–965. doi: 10.1016/0092-8674(90)90270-o. [DOI] [PubMed] [Google Scholar]
- Chong J. P., Thömmes P., Blow J. J. The role of MCM/P1 proteins in the licensing of DNA replication. Trends Biochem Sci. 1996 Mar;21(3):102–106. [PubMed] [Google Scholar]
- Cocker J. H., Piatti S., Santocanale C., Nasmyth K., Diffley J. F. An essential role for the Cdc6 protein in forming the pre-replicative complexes of budding yeast. Nature. 1996 Jan 11;379(6561):180–182. doi: 10.1038/379180a0. [DOI] [PubMed] [Google Scholar]
- Coleman T. R., Carpenter P. B., Dunphy W. G. The Xenopus Cdc6 protein is essential for the initiation of a single round of DNA replication in cell-free extracts. Cell. 1996 Oct 4;87(1):53–63. doi: 10.1016/s0092-8674(00)81322-7. [DOI] [PubMed] [Google Scholar]
- Dahmann C., Diffley J. F., Nasmyth K. A. S-phase-promoting cyclin-dependent kinases prevent re-replication by inhibiting the transition of replication origins to a pre-replicative state. Curr Biol. 1995 Nov 1;5(11):1257–1269. doi: 10.1016/s0960-9822(95)00252-1. [DOI] [PubMed] [Google Scholar]
- Diffley J. F., Cocker J. H., Dowell S. J., Rowley A. Two steps in the assembly of complexes at yeast replication origins in vivo. Cell. 1994 Jul 29;78(2):303–316. doi: 10.1016/0092-8674(94)90299-2. [DOI] [PubMed] [Google Scholar]
- Diffley J. F. Once and only once upon a time: specifying and regulating origins of DNA replication in eukaryotic cells. Genes Dev. 1996 Nov 15;10(22):2819–2830. doi: 10.1101/gad.10.22.2819. [DOI] [PubMed] [Google Scholar]
- Dimitrova D. S., Giacca M., Demarchi F., Biamonti G., Riva S., Falaschi A. In vivo protein-DNA interactions at human DNA replication origin. Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1498–1503. doi: 10.1073/pnas.93.4.1498. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Donovan S., Harwood J., Drury L. S., Diffley J. F. Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc Natl Acad Sci U S A. 1997 May 27;94(11):5611–5616. doi: 10.1073/pnas.94.11.5611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dowell S. J., Romanowski P., Diffley J. F. Interaction of Dbf4, the Cdc7 protein kinase regulatory subunit, with yeast replication origins in vivo. Science. 1994 Aug 26;265(5176):1243–1246. doi: 10.1126/science.8066465. [DOI] [PubMed] [Google Scholar]
- Falaschi A., Giacca M. The quest for a human ori. Genetica. 1994;94(2-3):255–266. doi: 10.1007/BF01443439. [DOI] [PubMed] [Google Scholar]
- Gavin K. A., Hidaka M., Stillman B. Conserved initiator proteins in eukaryotes. Science. 1995 Dec 8;270(5242):1667–1671. doi: 10.1126/science.270.5242.1667. [DOI] [PubMed] [Google Scholar]
- Giacca M., Zentilin L., Norio P., Diviacco S., Dimitrova D., Contreas G., Biamonti G., Perini G., Weighardt F., Riva S. Fine mapping of a replication origin of human DNA. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7119–7123. doi: 10.1073/pnas.91.15.7119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huberman J. A., Riggs A. D. On the mechanism of DNA replication in mammalian chromosomes. J Mol Biol. 1968 Mar 14;32(2):327–341. doi: 10.1016/0022-2836(68)90013-2. [DOI] [PubMed] [Google Scholar]
- Hyrien O., Maric C., Méchali M. Transition in specification of embryonic metazoan DNA replication origins. Science. 1995 Nov 10;270(5238):994–997. doi: 10.1126/science.270.5238.994. [DOI] [PubMed] [Google Scholar]
- Kumar S., Giacca M., Norio P., Biamonti G., Riva S., Falaschi A. Utilization of the same DNA replication origin by human cells of different derivation. Nucleic Acids Res. 1996 Sep 1;24(17):3289–3294. doi: 10.1093/nar/24.17.3289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lei M., Kawasaki Y., Tye B. K. Physical interactions among Mcm proteins and effects of Mcm dosage on DNA replication in Saccharomyces cerevisiae. Mol Cell Biol. 1996 Sep;16(9):5081–5090. doi: 10.1128/mcb.16.9.5081. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liang C., Spitzer J. D., Smith H. S., Gerbi S. A. Replication initiates at a confined region during DNA amplification in Sciara DNA puff II/9A. Genes Dev. 1993 Jun;7(6):1072–1084. doi: 10.1101/gad.7.6.1072. [DOI] [PubMed] [Google Scholar]
- Liang C., Weinreich M., Stillman B. ORC and Cdc6p interact and determine the frequency of initiation of DNA replication in the genome. Cell. 1995 Jun 2;81(5):667–676. doi: 10.1016/0092-8674(95)90528-6. [DOI] [PubMed] [Google Scholar]
- Marahrens Y., Stillman B. A yeast chromosomal origin of DNA replication defined by multiple functional elements. Science. 1992 Feb 14;255(5046):817–823. doi: 10.1126/science.1536007. [DOI] [PubMed] [Google Scholar]
- Pelizon C., Diviacco S., Falaschi A., Giacca M. High-resolution mapping of the origin of DNA replication in the hamster dihydrofolate reductase gene domain by competitive PCR. Mol Cell Biol. 1996 Oct;16(10):5358–5364. doi: 10.1128/mcb.16.10.5358. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quivy J. P., Becker P. B. An improved protocol for genomic sequencing and footprinting by ligation-mediated PCR. Nucleic Acids Res. 1993 Jun 11;21(11):2779–2781. doi: 10.1093/nar/21.11.2779. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rao H., Marahrens Y., Stillman B. Functional conservation of multiple elements in yeast chromosomal replicators. Mol Cell Biol. 1994 Nov;14(11):7643–7651. doi: 10.1128/mcb.14.11.7643. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Romanowski P., Madine M. A., Rowles A., Blow J. J., Laskey R. A. The Xenopus origin recognition complex is essential for DNA replication and MCM binding to chromatin. Curr Biol. 1996 Nov 1;6(11):1416–1425. doi: 10.1016/s0960-9822(96)00746-4. [DOI] [PubMed] [Google Scholar]
- Rowles A., Blow J. J. Chromatin proteins involved in the initiation of DNA replication. Curr Opin Genet Dev. 1997 Apr;7(2):152–157. doi: 10.1016/s0959-437x(97)80123-2. [DOI] [PubMed] [Google Scholar]
- Rowles A., Chong J. P., Brown L., Howell M., Evan G. I., Blow J. J. Interaction between the origin recognition complex and the replication licensing system in Xenopus. Cell. 1996 Oct 18;87(2):287–296. doi: 10.1016/s0092-8674(00)81346-x. [DOI] [PubMed] [Google Scholar]
- Rowley A., Cocker J. H., Harwood J., Diffley J. F. Initiation complex assembly at budding yeast replication origins begins with the recognition of a bipartite sequence by limiting amounts of the initiator, ORC. EMBO J. 1995 Jun 1;14(11):2631–2641. doi: 10.1002/j.1460-2075.1995.tb07261.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Santocanale C., Diffley J. F. ORC- and Cdc6-dependent complexes at active and inactive chromosomal replication origins in Saccharomyces cerevisiae. EMBO J. 1996 Dec 2;15(23):6671–6679. [PMC free article] [PubMed] [Google Scholar]
- Schwob E., Böhm T., Mendenhall M. D., Nasmyth K. The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell. 1994 Oct 21;79(2):233–244. doi: 10.1016/0092-8674(94)90193-7. [DOI] [PubMed] [Google Scholar]
- Stillman B. Cell cycle control of DNA replication. Science. 1996 Dec 6;274(5293):1659–1664. doi: 10.1126/science.274.5293.1659. [DOI] [PubMed] [Google Scholar]
- Tanaka T., Knapp D., Nasmyth K. Loading of an Mcm protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell. 1997 Aug 22;90(4):649–660. doi: 10.1016/s0092-8674(00)80526-7. [DOI] [PubMed] [Google Scholar]
- Theis J. F., Newlon C. S. Domain B of ARS307 contains two functional elements and contributes to chromosomal replication origin function. Mol Cell Biol. 1994 Nov;14(11):7652–7659. doi: 10.1128/mcb.14.11.7652. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tóth E. C., Marusic L., Ochem A., Patthy A., Pongor S., Giacca M., Falaschi A. Interactions of USF and Ku antigen with a human DNA region containing a replication origin. Nucleic Acids Res. 1993 Jul 11;21(14):3257–3263. doi: 10.1093/nar/21.14.3257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vaughn J. P., Dijkwel P. A., Hamlin J. L. Replication initiates in a broad zone in the amplified CHO dihydrofolate reductase domain. Cell. 1990 Jun 15;61(6):1075–1087. doi: 10.1016/0092-8674(90)90071-l. [DOI] [PubMed] [Google Scholar]
- Wang T. A., Li J. J. Eukaryotic DNA replication. Curr Opin Cell Biol. 1995 Jun;7(3):414–420. doi: 10.1016/0955-0674(95)80098-0. [DOI] [PubMed] [Google Scholar]
- Williams R. S., Shohet R. V., Stillman B. A human protein related to yeast Cdc6p. Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):142–147. doi: 10.1073/pnas.94.1.142. [DOI] [PMC free article] [PubMed] [Google Scholar]