Phosphorylation of ORC2 protein dissociates origin recognition complex from chromatin and replication origins

Journal of Biological Chemistry

Volumn 287, Issue 15, 2012, Pages 11891-11898

  Lee, Kyung Yong ^a   Bang, Sung Woong ^a   Yoon, Sang Wook ^a   Lee, Seung Hoon ^b   Yoon, Jong Bok ^b   Hwang, Deog Su ^a  

^a Seoul National University   (South Korea)

^b Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE; CYCLIN-DEPENDENT KINASE; EUKARYOTIC CHROMOSOMES; ORIGIN RECOGNITION COMPLEXES; REPLICATION ORIGIN; S-PHASE;

PHOSPHORYLATION; PROTEINS;

CHROMOSOMES;

CYCLIN DEPENDENT KINASE; DNA BINDING PROTEIN; ORIGIN REPLICATION COMPLEX 2 PROTEIN; ORIGIN REPLICATION COMPLEX 3 PROTEIN; ORIGIN REPLICATION COMPLEX 4 PROTEIN; ORIGIN REPLICATION COMPLEX 5 PROTEIN; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CHROMATIN; CONTROLLED STUDY; DISSOCIATION; DNA REPLICATION ORIGIN; HELA CELL; HUMAN; HUMAN CELL; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; CHROMATIN; CONSERVED SEQUENCE; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; ORIGIN RECOGNITION COMPLEX; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPLICATION ORIGIN; S PHASE;

EUKARYOTA;

EID: 84859506007     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.338467     Document Type: Article

References (46)

1. Bell, S. P., and Dutta, A. (2002) DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71, 333-374 (Pubitemid 34800224)
2. Diffley, J. F. (2004) Regulation of early events in chromosome replication. Curr. Biol. 14, R778-R786
3. Sclafani, R. A., and Holzen, T. M. (2007) Annu. Rev. Genet. 41, 237-280
4. Blow, J. J., and Dutta, A. (2005) Preventing re-replication of chromosomal DNA. Nat. Rev. Mol. Cell Biol. 6, 476-486 (Pubitemid 40780559)
5. DePamphilis, M. L., Blow, J. J., Ghosh, S., Saha, T., Noguchi, K., and Vassilev, A. (2006) Regulating the licensing of DNA replication origins in metazoa. Curr. Opin. Cell Biol. 18, 231-239
6. Tsakraklides, V., and Bell, S. P. (2010) Dynamics of prereplicative complex assembly. J. Biol. Chem. 285, 9437-9443
7. Evrin, C., Clarke, P., Zech, J., Lurz, R., Sun, J., Uhle, S., Li, H., Stillman, B., and Speck, C. (2009) A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl. Acad. Sci. U.S.A. 106, 20240-20245
8. Chen, S., and Bell, S. P. (2011) CDK prevents Mcm2-7 helicase loading by inhibiting Cdt1 interaction with Orc6. Genes Dev. 25, 363-372
9. Bell, S. P., and Stillman, B. (1992) ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357, 128-134
10. Dutta, A., and Bell, S. P. (1997) Initiation of DNA replication in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 13, 293-332 (Pubitemid 28034528)
11. Vashee, S., Cvetic, C., Lu, W., Simancek, P., Kelly, T. J., and Walter, J. C. (2003) Sequence-independent DNA binding and replication initiation by the human origin recognition complex. Genes Dev. 17, 1894-1908 (Pubitemid 36944566)
12. Giordano-Coltart, J., Ying, C. Y., Gautier, J., and Hurwitz, J. (2005) Studies of the properties of human origin recognition complex and its Walker A motif mutants. Proc. Natl. Acad. Sci. U.S.A. 102, 69-74 (Pubitemid 40094430)
13. Ranjan, A., and Gossen, M. (2006) A structural role for ATP in the formation and stability of the human origin recognition complex. Proc. Natl. Acad. Sci. U.S.A. 103, 4864-4869
14. Dhar, S. K., Yoshida, K., Machida, Y., Khaira, P., Chaudhuri, B., Wohlschlegel, J. A., Leffak, M., Yates, J., and Dutta, A. (2001) Replication from oriP of Epstein-Barr virus requires human ORC and is inhibited by geminin. Cell 106, 287-296 (Pubitemid 32772613)
15. Kreitz, S., Ritzi, M., Baack, M., and Knippers, R. (2001) The human origin recognition complex protein 1 dissociates from chromatin during S phase in HeLa cells. J. Biol. Chem. 276, 6337-6342
16. Siddiqui, K., and Stillman, B. (2007) ATP-dependent assembly of the human origin recognition complex. J. Biol. Chem. 282, 32370-32383 (Pubitemid 350106415)
17. Méndez, J., Zou-Yang, X. H., Kim, S. Y., Hidaka, M., Tansey, W. P., and Stillman, B. (2002) Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol. Cell 9, 481-491 (Pubitemid 34273780)
18. Tatsumi, Y., Ohta, S., Kimura, H., Tsurimoto, T., and Obuse, C. (2003) The ORC1 cycle in human cells. I. Cell cycle-regulated oscillation of human ORC1. J. Biol. Chem. 278, 41528-41534 (Pubitemid 37280982)
19. Gerhardt, J., Jafar, S., Spindler, M. P., Ott, E., and Schepers, A. (2006) Identification of new human origins of DNA replication by an origin-trapping assay. Mol. Cell Biol. 26, 7731-7746 (Pubitemid 44547719)
20. Findeisen, M., El-Denary, M., Kapitza, T., Graf, R., and Strausfeld, U. (1999) Cyclin A-dependent kinase activity affects chromatin binding of ORC, Cdc6, and MCM in egg extracts of Xenopus laevis. Eur. J. Biochem. 264, 415-426 (Pubitemid 29424445)
21. Laman, H., Peters, G., and Jones, N. (2001) Cyclin-mediated export of human Orc1. Exp. Cell Res. 271, 230-237 (Pubitemid 33141204)
22. Remus, D., Blanchette, M., Rio, D. C., and Botchan, M. R. (2005) CDK phosphorylation inhibits the DNA-binding and ATP-hydrolysis activities of the Drosophila origin recognition complex. J. Biol. Chem. 280, 39740-39751 (Pubitemid 41779107)
23. Vas, A., Mok, W., and Leatherwood, J. (2001) Control of DNA rereplication via Cdc2 phosphorylation sites in the origin recognition complex. Mol. Cell Biol. 21, 5767-5777 (Pubitemid 32737794)
24. Makise, M., Takehara, M., Kuniyasu, A., Matsui, N., Nakayama, H., and Mizushima, T. (2009) Linkage between phosphorylation of the origin recognition complex and its ATP binding activity in Saccharomyces cerevisiae. J. Biol. Chem. 284, 3396-3407
25. Nguyen, V. Q., Co, C., and Li, J. J. (2001) Cyclin-dependent kinases prevent DNA re-replication through multiple mechanisms. Nature 411, 1068-1073 (Pubitemid 32612333)
26. Li, C. J., Vassilev, A., and DePamphilis, M. L. (2004) Role for Cdk1 (Cdc2)/ cyclin A in preventing the mammalian origin recognition complex's largest subunit (Orc1) from binding to chromatin during mitosis. Mol. Cell Biol. 24, 5875-5886 (Pubitemid 38787972)
27. Braunstein, M., Rose, A. B., Holmes, S. G., Allis, C. D., and Broach, J. R. (1993) Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev. 7, 592-604 (Pubitemid 23125260)
28. Chen, H., Lin, R. J., Xie, W., Wilpitz, D., and Evans, R. M. (1999) Regulation of hormone-induced histone hyperacetylation and gene activation via acetylation of an acetylase. Cell 98, 675-686 (Pubitemid 29418958)
29. Ladenburger, E. M., Keller, C., and Knippers, R. (2002) Identification of a binding region for human origin recognition complex proteins 1 and 2 that coincides with an origin of DNA replication. Mol. Cell Biol. 22, 1036-1048 (Pubitemid 34094841)
30. Geley, S., Kramer, E., Gieffers, C., Gannon, J., Peters, J. M., and Hunt, T. (2001) Anaphase-promoting complex/cyclosome-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J. Cell Biol. 153, 137-148
31. Ubersax, J. A., and Ferrell, J. E., Jr. (2007) Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 8, 530-541 (Pubitemid 46985383)
32. Malumbres, M., and Barbacid, M. (2009) Cell cycle, CDKs, and cancer. A changing paradigm. Nat. Rev. Cancer 9, 153-166
33. Woetmann, A., Nielsen, M., Christensen, S. T., Brockdorff, J., Kaltoft, K., Engel, A. M., Skov, S., Brender, C., Geisler, C., Svejgaard, A., Rygaard, J., Leick, V., and Odum, N. (1999) Inhibition of protein phosphatase 2A induces serine/threonine phosphorylation, subcellular redistribution, and functional inhibition of STAT3. Proc. Natl. Acad. Sci. U.S.A. 96, 10620-10625 (Pubitemid 29442193)
34. Vashee, S., Simancek, P., Challberg, M. D., and Kelly, T. J. (2001) Assembly of the human origin recognition complex. J. Biol. Chem. 276, 26666-26673
35. Prasanth, S. G., Prasanth, K. V., Siddiqui, K., Spector, D. L., and Stillman, B. (2004) Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. EMBO J. 23, 2651-2663 (Pubitemid 38988236)
36. Ohta, S., Tatsumi, Y., Fujita, M., Tsurimoto, T., and Obuse, C. (2003) The ORC1 cycle in human cells. II. Dynamic changes in the human ORC complex during the cell cycle. J. Biol. Chem. 278, 41535-41540 (Pubitemid 37280983)
37. Noguchi, K., Vassilev, A., Ghosh, S., Yates, J. L., and DePamphilis, M. L. (2006) The BAH domain facilitates the ability of human Orc1 protein to activate replication origins in vivo. EMBO J. 25, 5372-5382 (Pubitemid 44764146)
38. Baldinger, T., and Gossen, M. (2009) Binding of Drosophila ORC proteins to anaphase chromosomes requires cessation of mitotic cyclin-dependent kinase activity. Mol. Cell Biol. 29, 140-149
39. Sun, W. H., Coleman, T. R., and DePamphilis, M. L. (2002) Cell cycle-dependent regulation of the association between origin recognition proteins and somatic cell chromatin. EMBO J. 21, 1437-1446 (Pubitemid 34246522)
40. Lygerou, Z., and Nurse, P. (1999) The fission yeast origin recognition complex is constitutively associated with chromatin and is differentially modified through the cell cycle. J. Cell Sci. 112, 3703-3712
41. DePamphilis, M. L. (2005) Cell cycle-dependent regulation of the origin recognition complex. Cell Cycle 4, 70-79
42. Sugimoto, N., Tatsumi, Y., Tsurumi, T., Matsukage, A., Kiyono, T., Nishitani, H., and Fujita, M. (2004) Cdt1 phosphorylation by cyclin A-dependent kinases negatively regulates its function without affecting geminin binding. J. Biol. Chem. 279, 19691-19697 (Pubitemid 38623406)
43. Saha, P., Chen, J., Thome, K. C., Lawlis, S. J., Hou, Z. H., Hendricks, M., Parvin, J. D., and Dutta, A. (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 (Pubitemid 28183445)
44. Delmolino, L. M., Saha, P., and Dutta, A. (2001) Multiple mechanisms regulate subcellular localization of human CDC6. J. Biol. Chem. 276, 26947-26954
45. Ishimi, Y., Komamura-Kohno, Y., You, Z., Omori, A., and Kitagawa, M. (2000) Inhibition of Mcm4,6,7 helicase activity by phosphorylation with cyclin A/Cdk2. J. Biol. Chem. 275, 16235-16241 (Pubitemid 30366936)
46. Arias, E. E., and Walter, J. C. (2007) Strength in numbers. Preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497-518 (Pubitemid 46409465)