Cell Cycle-Dependent Regulation of Human DNA Polymerase α-Primase Activity by Phosphorylation

REFERENCES

• Aparicio, O. M., D. M. Weinstein, and J. Bell 1997. Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell 91:59–69.
   PubMed Web of Science ®Google Scholar
• Boyle, W. J., P. van der Geer, and J. Hunter 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110–149.
   PubMed Web of Science ®Google Scholar
• Bradford, M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.
   PubMed Web of Science ®Google Scholar
• Braun, K. A., Y. Lao, Z. He, C. J. Ingles, and J. Wold 1997. Role of protein-protein interactions in the function of replication protein A (RP-A): RP-A modulates the activity of DNA polymerase α by multiple mechanisms. Biochemistry 36:8443–8454.
   PubMed Web of Science ®Google Scholar
• Bullock, P. A. 1997. The initiation of simian virus 40 DNA replication in vitro. Crit. Rev. Biochem. Mol. Biol. 32:503–568.
   PubMed Web of Science ®Google Scholar
• Canella, D., J. M. Roberts, and J. Fotedar 1997. Association of cyclin A and cdk2 with SV40 DNA in replication initiation complexes is cell cycle dependent. Chromosoma 105:349–359.
   PubMedGoogle Scholar
• Cardoso, M. C., H. Leonhardt, and J. Nadal-Ginard 1993. Reversal of terminal differentiation and control of DNA replication: cyclin A and cdk2 specifically localize at subnuclear sites of DNA replication. Cell 74:979–992.
   PubMedGoogle Scholar
• Coleman, T. R., P. B. Carpenter, and J. Dunphy 1996. The Xenopus Cdc6 protein is essential for the initiation of a single round of DNA replication in cell-free extracts. Cell 87:53–63.
   PubMed Web of Science ®Google Scholar
• Colgan, D. F., K. G. K. Murthy, W. Zhao, C. Prives, and J. Manley 1998. Inhibition of poly(A) polymerase requires p34cdc2/cyclin B phosphorylation of multiple consensus and non-consensus sites. EMBO J. 17:1053–1062.
   PubMed Web of Science ®Google Scholar
• Collins, K. L., A. A. R. Russo, B. Y. Tseng, and J. Kelly 1993. The role of the 70 kDa subunit of human polymerase α in DNA replication. EMBO J. 12:4555–4566.
   PubMedGoogle Scholar
• Collins, K. L., and J. Kelly 1991. Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase α-primase. Mol. Cell. Biol. 11:2108–2115.
   PubMed Web of Science ®Google Scholar
• Dornreiter, I., A. Höß, A. K. Arthur, and J. Fanning 1990. SV40 T antigen binds directly to the catalytic subunit of DNA polymerase α. EMBO J. 9:3329–3336.
   PubMedGoogle Scholar
• Dornreiter, I., F. L. Erdile, I. Gilbert, D. von Winkler, T. J. Kelly, and J. Fanning 1992. Interaction of DNA polymerase α-primase with replication protein A and SV40 T antigen. EMBO J. 11:769–776.
   PubMed Web of Science ®Google Scholar
• Dornreiter, I., W. C. Copeland, and J. Wang 1993. Initiation of simian virus 40 DNA replication requires the interaction of a specific domain of human DNA polymerase α with large T antigen. Mol. Cell. Biol. 13:809–820.
   PubMedGoogle Scholar
• Dulic, V., E. Lees, and J. Reed 1992. Association of human cyclin E with a periodic G1-S phase protein kinase. Science 257:1958–1961.
   PubMed Web of Science ®Google Scholar
• Dutta, A., and J. Bell 1997. Initiation of DNA replication in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 13:293–352.
   PubMed Web of Science ®Google Scholar
• Foiani, M., G. Liberi, G. Lucchini, and J. Plevani 1995. Cell cycle-dependent phosphorylation and dephosphorylation of the yeast DNA polymerase α-primase B subunit. Mol. Cell. Biol. 15:883–891.
   PubMedGoogle Scholar
• Foiani, M., G. Lucchini, and J. Plevani 1997. The DNA polymerase α-primase complex couples DNA replication, cell-cycle progression and DNA-damage response. Trends Biochem. Sci. 11:411–452.
   Google Scholar
• Girard, F., U. Strausfeld, A. Fernandez, and J. Lamb 1991. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67:1169–1179.
   PubMed Web of Science ®Google Scholar
• Hassell, J. A., B. T. Brinton 1996. SV40 and polyoma DNA replication, p. 461–493. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Henricksen, L. A., and J. Wold 1994. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269:11121–11131.
   PubMed Web of Science ®Google Scholar
• Herendeen, D., T. J. Kelly 1997. SV40 DNA replication, p. 29–65. In J. J. Blow (ed.), Eukaryotic DNA replication. Oxford University Press, New York, N.Y.
   Google Scholar
• Horton, R. M., L. R. Pease 1991. Recombination and mutagenesis of DNA sequences using PCR, p. 217–249. In M. J. McPherson (ed.), Directed mutagenesis—a practical approach. Oxford University Press, New York, N.Y.
   Google Scholar
• Hua, H. X., and J. Newport 1998. Identification of a preinitiation step in DNA replication that is independent of origin recognition complex and cdc6, but dependent on cdk2. J. Cell Biol. 140:271–281.
   PubMed Web of Science ®Google Scholar
• Hua, H. X., H. Yan, and J. Newport 1997. A role for Cdk2 kinase in negatively regulating DNA replication during S phase of the cell cycle. J. Cell Biol. 137:183–192.
   PubMedGoogle Scholar
• Jallepalli, P., and J. Kelly 1997. Cyclin-dependent kinase and initiation at eukaryotic origins: a replication switch? Curr. Opin. Cell Biol. 9:358–363.
   PubMedGoogle Scholar
• Koff, A., A. Giordano, D. Desai, Y. Katsumi, J. W. Harper, S. Elledge, T. Nishimoto, D. O. Morgan, B. R. Franza, and J. Roberts 1992. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257:1689–1694.
   PubMed Web of Science ®Google Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685.
   PubMed Web of Science ®Google Scholar
• Lane, D. Unpublished data.
   Google Scholar
• Liao, P. C., J. Leykam, P. C. Andrews, D. A. Gage, and J. Allison 1994. An approach to locate phosphorylation sites in a phosphoprotein: mass mapping by combining specific enzymatic degradation with matrix-assisted laser desorption/ionization mass spectrometry. Anal. Biochem. 219:9–20.
   PubMed Web of Science ®Google Scholar
• Ludlow, J. W. 1992. Selective ability of S phase cell extracts to dephosphorylate large T antigen in vitro. Oncogene 7:1011–1014.
   PubMedGoogle Scholar
• Melendy, T., and J. Stillman 1993. An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J. Biol. Chem. 268:3389–3395.
   PubMedGoogle Scholar
• Moarefi, I. F., D. Small, I. Gilbert, M. Höpfner, S. K. Randall, C. Schneider, A. A. R. Russo, U. Ramsperger, A. K. Arthur, H. Stahl, T. J. Kelly, and J. Fanning 1993. Mutation of the cyclin-dependent kinase phosphorylation site in simian virus 40 (SV40) large T antigen specifically blocks SV40 origin DNA unwinding. J. Virol. 67:4992–5002.
   PubMedGoogle Scholar
• Moreno, S., J. Hayles, and J. Nurse 1989. Regulation of p34cdc2 kinase during mitosis. Cell 58:361–372.
   PubMed Web of Science ®Google Scholar
• Murakami, Y., and J. Hurwitz 1993. Functional interactions between SV40 T antigen and other replication proteins at the replication fork. J. Biol. Chem. 268:11008–11017.
   PubMedGoogle Scholar
• Murakami, Y., and J. Hurwitz 1993. DNA polymerase α stimulates the ATP-dependent binding of simian virus 40 T antigen to the SV40 origin of replication in vitro. J. Biol. Chem. 268:11018–11027.
   PubMedGoogle Scholar
• Nasheuer, H. P., A. Moore, A. F. Wahl, and J. Wang 1991. Cell cycle dependent phosphorylation of human DNA polymerase α. J. Biol. Chem. 266:7893–7903.
   PubMedGoogle Scholar
• Nasmyth, K. 1996. Control of S phase, p. 331–386. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Nigg, E. 1995. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. BioEssays 17:471–480.
   PubMed Web of Science ®Google Scholar
• Ohtsubo, M., A. M. Theodoras, J. Schumacher, J. M. Roberts, and J. Pagano 1995. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell. Biol. 15:2612–2624.
   PubMed Web of Science ®Google Scholar
• Pagano, M., R. Pepperkok, F. Verde, W. Ansorge, and J. Draetta 1992. Cyclin A is required at two points in the human cell cycle. EMBO J. 11:961–971.
   PubMed Web of Science ®Google Scholar
• Park, H., R. Davis, and J. Wang 1995. Studies of Schizosaccharomyces pombe DNA polymerase α at different stages of the cell cycle. Nucleic Acids Res. 23:4337–4344.
   PubMedGoogle Scholar
• Pines, J., and J. Hunter 1990. p34cdc2, the S and M kinase? New Biol. 2:389–401.
   PubMedGoogle Scholar
• Rao, P. T., and J. Johnson 1970. Mammalian cell fusion: studies on the regulation of DNA synthesis and mitosis. Nature 225:159–164.
   PubMed Web of Science ®Google Scholar
• Rosenblatt, J., Y. Gu, and J. Morgan 1992. Human cyclin-dependent kinase 2 is activated during the S and G2 phases of the cell cycle and associates with cyclin A. Proc. Natl. Acad. Sci. USA 89:2824–2828.
   PubMed Web of Science ®Google Scholar
• Saha, P., J. Chen, K. C. Thome, S. J. Lawlis, Z.-H. Hou, M. Hendricks, J. D. Parvin, and J. Dutta 1998. Human CDC6/Cdc18 associates with Orc1 and cyclin-cdk and is selectively eliminated from the nucleus at the onset of S phase. Mol. Cell. Biol. 18:2758–2767.
   PubMed Web of Science ®Google Scholar
• Schneider, C., K. Weißhart, L. A. Guarino, I. Dornreiter, and J. Fanning 1994. Species-specific functional interactions of DNA polymerase α-primase with simian virus 40 (SV40) T antigen require SV40 origin DNA. Mol. Cell. Biol. 14:3176–3185.
   PubMedGoogle Scholar
• Sobczak-Thepot, J., F. Harper, Y. Florentin, F. Zindy, C. Brechot, and J. Puvion 1993. Localization of cyclin A at the sites of cellular DNA replication. Exp. Cell Res. 206:43–48.
   PubMedGoogle Scholar
• Sorger, P. K., and J. Pelham 1988. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864.
   PubMed Web of Science ®Google Scholar
• Stadlbauer, F., A. Brückner, C. Rehfuess, C. Eckerskorn, F. Lottspeich, V. Förster, B. Y. Tseng, and J. Nasheuer 1994. DNA replication in vitro by recombinant DNA-polymerase-α-primase. Eur. J. Biochem. 222:781–793.
   PubMedGoogle Scholar
• Stadlbauer, F., C. Voitenleitner, A. Brückner, E. Fanning, and J. Nasheuer 1996. Species-specific replication of simian virus 40 DNA in vitro requires the p180 subunit of human DNA polymerase α-primase. Mol. Cell. Biol. 16:94–104.
   PubMedGoogle Scholar
• Takada-Takayama, R., S. Tada, F. Hanaoka, and J. Ui 1990. Peptide mapping of the four subunits of the mouse DNA polymerase-α primase complex. Biochem. Biophys. Res. Commun. 170:589–595.
   PubMed Web of Science ®Google Scholar
• Tanaka, S., S.-Z. Hu, T. S. F. Wang, and J. Korn 1982. Preparation and preliminary characterization of monoclonal antibodies against human DNA polymerase alpha. J. Biol. Chem. 257:8386–8390.
   PubMedGoogle Scholar
• Tanaka, T., D. Knapp, and J. Nasmyth 1997. Loading of an Mcm protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell 90:649–660.
   PubMed Web of Science ®Google Scholar
• Tsai, L. H., E. Harlow, and J. Meyerson 1991. Isolation of the human cdk2 gene that encodes the cyclin A- and adenovirus E1A-associated p33 kinase. Nature 353:174–177.
   PubMed Web of Science ®Google Scholar
• Tsai, L. H., E. Lees, B. Faha, E. Harlow, and J. Riabowol 1993. The cdk2 kinase is required for the G1-to-S transition in mammalian cells. Oncogene 8:1593–1602.
   PubMed Web of Science ®Google Scholar
• Voitenleitner, C., D. Reese, and E. Fanning. Unpublished data.
   Google Scholar
• Voitenleitner, C., E. Fanning, and J. Nasheuer 1997. Phosphorylation of DNA polymerase α-primase by cyclin A-dependent kinases regulates initiation of DNA replication in vitro. Oncogene 14:1611–1615.
   PubMedGoogle Scholar
• Waga, S., and J. Stillman 1994. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369:207–212.
   PubMed Web of Science ®Google Scholar
• Wang, T. S. F. 1996. Cellular DNA polymerases, p. 461–493. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Weisshart, K., E. Fanning 1996. Phosphorylation of replication proteins, p. 295–330. In M. L. DePamphilis (ed.), DNA replication in eukaryotic cells. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
   Google Scholar
• Wittmeyer, J., and J. Formosa 1997. The Saccharomyces cerevisiae DNA polymerase α catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17:4178–4190.
   PubMed Web of Science ®Google Scholar
• Yan, Z., J. DeGregori, R. Shohet, G. Leone, B. Stillman, J. R. Nevins, and J. Williams 1998. Cdc6 is regulated by E2F and is essential for DNA replication in mammalian cells. Proc. Natl. Acad. Sci. USA 95:3603–3608.
   PubMed Web of Science ®Google Scholar
• Zindy, F., F. Lamas, X. Chenivesse, J. Sobczak, J. Wang, D. Fesquet, B. Henglein, and J. Brechot 1992. Cyclin A is required in S phase in normal epithelial cells. Biochem. Biophys. Res. Commun. 182:1144–1154.
   PubMed Web of Science ®Google Scholar