Cell cycle-dependent regulation of human DNA polymerase α-primase activity by phosphorylation

Molecular and Cellular Biology

Volumn 19, Issue 1, 1999, Pages 646-656

  Voitenleitner, Christian ^a,b   Rehfuess, Christoph ^a,b   Hilmes, Melissa ^a,b   O'Rear, Lynda ^a,b   Liao, Pao Chi ^c   Gage, Douglas A ^d   Ott, Robert ^a,b   Nasheuer, Heinz Peter ^e   Fanning, Ellen ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d Michigan State University ^*  (United States)

^e FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA PRIMASE;

ANIMAL CELL; ARTICLE; CELL CYCLE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GROWTH REGULATION; INSECT; NONHUMAN; PRIORITY JOURNAL;

EID: 0032931458     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.19.1.646     Document Type: Article

References (64)

1. Aparicio, O. M., D. M. Weinstein, and S. P. 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.
2. Boyle, W. J., P. van der Geer, and T. Hunter. 1991. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 201:110-149.
3. 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.
4. Braun, K. A., Y. Lao, Z. He, C. J. Ingles, and M. S. Wold. 1997. Role of protein-protein interactions in the function of replication protein A (RP-A): RP-A modulates the activity of DNA polymerase a by multiple mechanisms. Biochemistry 36:8443-8454.
5. Bullock, P. A. 1997. The initiation of simian virus 40 DNA replication in vitro. Crit. Rev. Biochem. Mol. Biol. 32:503-568.
6. Canella, D., J. M. Roberts, and R. Fotedar. 1997. Association of cyclin A and cdk2 with SV40 DNA in replication initiation complexes is cell cycle dependent. Chromosoma 105:349-359.
7. Cardoso, M. C., H. Leonhardt, and B. 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.
8. Coleman, T. R., P. B. Carpenter, and W. G. 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.
9. Colgan, D. F., K. G. K. Murthy, W. Zhao, C. Prives, and J. L. Manley. 1998. Inhibition of poly(A) polymerase requires p34cdc2/cyclin B phosphorylation of multiple consensus and non-consensus sites. EMBO J. 17:1053-1062.
10. Collins, K. L., A. A. R. Russo, B. Y. Tseng, and T. J. Kelly. 1993. The role of the 70 kDa subunit of human polymerase α in DNA replication. EMBO J. 12:4555-4566.
11. Collins, K. L., and T. 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.
12. Dornreiter, I., A. Höß, A. K. Arthur, and E. Fanning. 1990. SV40 T antigen binds directly to the catalytic subunit of DNA polymerase α. EMBO J. 9:3329-3336.
13. Dornreiter, I., F. L. Erdile, I. Gilbert, D. von Winkler, T. J. Kelly, and E. Fanning. 1992. Interaction of DNA polymerase α-primase with replication protein A and SV40 T antigen. EMBO J. 11:769-776.
14. Dornreiter, I., W. C. Copeland, and T. S.-F. 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.
15. Dulic, V., E. Lees, and S. I. Reed. 1992. Association of human cyclin E with a periodic G1-S phase protein kinase. Science 257:1958-1961.
16. Dutta, A., and S. Bell. 1997. Initiation of DNA replication in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 13:293-352.
17. Foiani, M., G. Liberi, G. Lucchini, and P. Plevani. 1995. Cell cycle-dependent phosphorylation and dephosphorylation of the yeast DNA polymerase α-primase B subunit. Mol. Cell. Biol. 15:883-891.
18. Foiani, M., G. Lucchini, and P. Plevani. 1997. The DNA polymerase α-primase complex couples DNA replication, cell-cycle progression and DNA-damage response. Trends Biochem. Sci. 11:411-452.
19. Girard, F., U. Strausfeld, A. Fernandez, and N. Lamb. 1991. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell 67:1169-1179.
20. Hassell, J. A., and 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.
21. Henricksen, L. A., and M. S. Wold. 1994. Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem. 269:11121-11131.
22. Herendeen, D., and 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.
23. Horton, R. M., and 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.
24. 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.
25. 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.
26. Jallepalli, P., and T. J. Kelly. 1997. Cyclin-dcpendent kinase and initiation at eukaryotic origins: a replication switch? Curr. Opin. Cell Biol. 9:358-363.
27. Koff, A., A. Giordano, D. Desai, Y. Katsumi, J. W. Harper, S. Elledge, T. Nishimoto, D. O. Morgan, B. R. Franza, and J. M. Roberts. 1992. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257:1689-1694.
28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Lane, D. Unpublished data.
30. 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.
31. Ludlow, J. W. 1992. Selective ability of S phase cell extracts to dephosphorylate large T antigen in vitro. Oncogene 7:1011-1014.
32. Melendy, T., and B. 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.
33. 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 E. 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.
34. Moreno, S., J. Hayles, and P. Nurse. 1989. Regulation of p34cdc2 kinase during mitosis. Cell 58:361-372.
35. 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.
36. 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.
37. Nasheuer, H. P., A. Moore, A. F. Wahl, and T. S. F. Wang. 1991. Cell cycle dependent phosphorylation of human DNA polymerase α. J. Biol. Chem. 266:7893-7903.
38. 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.
39. Nigg, E. 1995, Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. BioEssays 17:471-480.
40. Ohtsubo, M., A. M. Theodoras, J. Schumacher, J. M. Roberts, and M. Pagano. 1995. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol. Cell. Biol. 15:2612-2624.
41. Pagano, M., R. Pepperkok, F. Verde, W. Ansorge, and G. Draetta. 1992. Cyclin A is required at two points in the human cell cycle. EMBO J. 11:961-971.
42. Park, H., R. Davis, and T. S. F. Wang. 1995. Studies of Schizosacchammyces pombe DNA polymerase a at different stages of the cell cycle. Nucleic Acids Res. 23:4337-4344.
43. Pines, J., and T. Hunter. 1990. P34cdc2, the S and M kinase? New Biol. 2:389-401.
44. Rao, P. T., and R. T. Johnson. 1970. Mammalian cell fusion: studies on the regulation of DNA synthesis and mitosis. Nature 225:159-164.
45. Rosenblatt, J., Y. Gu, and D. O. 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.
46. Saha, P., J. Chen, K. C. Thome, S. J. Lawlis, Z.-H. Hou, M. Hendricks, J. D. Parvin, and A. 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.
47. Schneider, C., K. Weißhart, L. A. Guarino, I. Dornreiter, and E. 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.
48. Sobczak-Thepot, J., F. Harper, Y. Florentin, F. Zindy, C. Brechot, and E. Puvion. 1993. Localization of cyclin A at the sites of cellular DNA replication. Exp. Cell Res. 206:43-48.
49. Sorger, P. K., and H. R. Pelham. 1988. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855-864.
50. Stadlbauer, F., A. Brückner, C. Rehfuess, C. Eckerskorn, F. Lottspeich, V. Förster, B. Y. Tseng, and H.-P. Nasheuer. 1994. DNA replication in vitro by recombinant DNA-polymerase-α-primase. Eur. J. Biochem. 222:781-793.
51. Stadlbauer, F., C. Voitenleitner, A. Bruckner, E. Fanning, and H.-P. 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.
52. Takada-Takayama, R., S. Tada, F. Hanaoka, and M. Ui. 1990. Peptide mapping of the four subunits of the mouse DNA polymerase-α primase complex. Biochem. Biophys. Res. Commun. 170:589-595.
53. Tanaka, S., S.-Z. Hu, T. S. F. Wang, and D. Korn. 1982. Preparation and preliminary characterization of monoclonal antibodies against human DNA polymerase alpha. J. Biol. Chem. 257:8386-8390.
54. Tanaka, T., D. Knapp, and K. Nasmyth. 1997. Loading of an Mem protein onto DNA replication origins is regulated by Cdc6p and CDKs. Cell 90:649-660.
55. Tsai, L. H., E. Harlow, and M. Meyerson. 1991. Isolation of the human cdk2 gene that encodes the cyclin A- and adenovirus E1A-associated p33 kinase. Nature 353:174-177.
56. Tsai, L. H., E. Lees, B. Faha, E. Harlow, and K. Riabowol. 1993. The cdk2 kinase is required for the G1-to-S transition in mammalian cells. Oncogene 8:1593-1602.
57. Voitenleitner, C., D. Reese, and E. Fanning. Unpublished data.
58. Voitenleitner, C., E. Fanning, and H.-P. Nasheuer. 1997. Phosphorylation of DNA polymerase α-primase by cyclin A-dependent kinases regulates initiation of DNA replication in vitro. Oncogene 14:1611-1615.
59. Waga, S., and B. Stillman. 1994. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 369:207-212.
60. 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.
61. Weisshart, K., and 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.
62. Wittmeyer, J., and T. Formosa. 1997. The Saccharomyces cerevisiae DNA polymerase a catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17:4178-4190.
63. Yan, Z., J. DeGregori, R. Shohet, G. Leone, B. Stillman, J. R. Nevins, and R. S. Williams. 1998. Cdc6 is regulated by E2F and is essential for DNA replication in mammalian cells. Proc. Natl. Acad. Sci. USA 95:3603-3608.
64. Zindy, F., F. Lamas, X. Chenivesse, J. Sobczak, J. Wang, D. Fesquet, B. Henglein, and C. Brechot. 1992. Cyclin A is required in S phase in normal epithelial cells. Biochem. Biophys. Res. Commun. 182:1144-1154.