Deregulation of cyclin E in human cells interferes with prereplication complex assembly

Journal of Cell Biology

Volumn 165, Issue 6, 2004, Pages 789-800

  Ekholm Reed, Susanna ^a,c   Méndez, Juan ^b   Tedesco, Donato ^a   Zetterberg, Anders ^c   Stillman, Bruce ^b   Reed, Steven I ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c Karolinska Krankenhaus   (Sweden)

Author keywords

Cyclin E; Cyclin E deregulation; DNA replication; MCM protein; Prereplication complex assembly

Indexed keywords

CYCLIN E; MCM4 PROTEIN; MCM7 PROTEIN; MINICHROMOSOME MAINTENANCE COMPLEX PROTEIN; MINICHROMOSOME MAINTENANCE PROTEIN 2; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CHROMATIN; CHROMOSOMAL INSTABILITY; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA FORK MOVEMENT; DNA REPLICATION; HUMAN; HUMAN CELL; MINICHROMOSOME; PREREPLICATION COMPLEX ASSEMBLY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN TRANSPORT; TELOPHASE;

BREAST NEOPLASMS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CYCLIN E; DNA REPLICATION; DNA-BINDING PROTEINS; FEMALE; FLOW CYTOMETRY; G1 PHASE; HUMANS; KB CELLS; NUCLEAR PROTEINS;

EID: 3042687608     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200404092     Document Type: Article

References (69)

1. Bortner, D.M., and M.P. Rosenberg. 1997. Induction of mammary gland hyperplasia and carcinomas in transgenic mice expressing human cyclin E. Mol. Cell. Biol. 17:453-459.
2. Coue, M., S.E. Kearsey, and M. Mechali. 1996. Chromotin binding, nuclear localization and phosphorylation of Xenopus cdc21 are cell-cycle dependent and associated with the control of initiation of DNA replication. EMBO J. 15: 1085-1097.
3. Coverley, D., H.R. Wilkinson, and C.S. Downes. 1996. A protein kinase-dependent block to reinitiation of DNA replication in G2 phase in mammalian cells. Exp. Cell Res. 225:294-300.
4. Donnellan, R., I. Kleinschmidt, and R. Chetty. 2001. Cyclin E immunoexpression in breast ductal carcinoma: pathologic correlations and prognostic implications. Hum. Pathol. 32:89-94.
5. Drury, L.S., G. Perkins, and J.F. Diffley. 1997. The Cdc4/34/53 pathway targets Cdc6p for proteolysis in budding yeast. EMBO J. 16:5966-5976.
6. Drury, L.S., G. Perkins, and J.F. Diffley. 2000. The cyclin-dependent kinase Cdc28p regulates distinct modes of Cdc6p proteolysis during the budding yeast cell cycle. Curr. Biol. 10:231-240.
7. Duesberg, P., and R. Li. 2003. Multistep carcinogenesis: a chain reaction of aneuploidizations. Cell Cycle. 2:202-210.
8. 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.
9. 1 cyclin-dependent kinases in the mammalian cell cycle. Curr. Opin. Cell Biol. 12:676-684.
10. Ekholm, S.V., P. Zickert, S.I. Reed, and A. Zetterberg. 2001. Accumulation of cyclin E is not a prerequisite for passage through the restriction point. Mol. Cell. Biol. 21:3256-3265.
11. Erlandsson, F., C. Wahlby, S. Ekholm-Reed, A.C. Hellstrom, E. Bengtsson, and A. Zetterberg. 2003. Abnormal expression pattern of cyclin E in tumour cells. Int. J. Cancer. 104:369-375.
12. Erlanson, M., and G. Landberg. 2001. Prognostic implications of p27 and cyclin E protein contents in malignant lymphomas. Leuk. Lymphoma. 40:461-470.
13. Fabarius, A., R. Hehlmann, and P.H. Duesberg. 2003. Instability of chromosome structure in cancer cells increases exponentially with degrees of aneuploidy. Cancer Genet. Cytogenet. 143:59-72.
14. Findeisen, M., M. El-Denary, T. Kapitza, R. Graf, and U. Strausfeld. 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.
15. Fujita, M., T. Kiyono, Y. Hayashi, and M. Ishibashi. 1996. hCDC47, a human member of the MCM family. Dissociation of the nucleus-bound form during S phase. J. Biol. Chem. 271:4349-4354.
16. Fukuda, K., H. Morioka, S. Imajou, S. Ikeda, E. Ohtsuka, and T. Tsurimoto. 1995. Structure-function relationship of the eukaryotic DNA replication factor, proliferating cell nuclear antigen. J. Biol. Chem. 270:22527-22534.
17. Gavin, K.A., M. Hidaka, and B. Stillman. 1995. Conserved initiator proteins in eukaryotes. Science. 270:1667-1671.
18. Hendrickson, M., M. Madine, S. Dalton, and J. Gautier. 1996. Phosphorylation of MCM4 by cdc2 protein kinase inhibits the activity of the minichromosome maintenance complex. Proc. Natl. Acad. Sci. USA. 93:12223-12228.
19. Holthoff, H.P., M. Baack, A. Richter, M. Ritzi, and R. Knippers. 1998. Human protein MCM6 on HeLa cell chromatin. J. Biol. Chem. 273:7320-7325.
20. Hozak, P., A.B. Hassan, D.A. Jackson, and P.R. Cook. 1993. Visualization of replication factories attached to nucleoskeleton. Cell. 73:361-373.
21. Hua, X.H., 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.
22. Huang, D., and D. Koshland. 2003. Chromosome integrity in Saccharomyces cerevisiae: the interplay of DNA replication initiation factors, elongation factors, and origins. Genes Dev. 17:1741-1754.
23. Jallepalli, P.V., and C. Lengauer. 2001. Chromosome segregation and cancer: cutting through the mystery. Nat. Rev. Cancer. 1:109-117.
24. Kelly, T.J., and G.W. Brown. 2000. Regulation of chromosome replication. Annu. Rev. Biochem. 69:829-880.
25. Kelman, Z. 1997. PCNA: structure, functions and interactions. Oncogene. 14: 629-640.
26. Keyomarsi, K., D. Conte Jr., W. Toyofuku, and M.P. Fox. 1995. Deregulation of cyclin E in breast cancer. Oncogene. 11:941-950.
27. Kimura, H., N. Nozaki, and K. Sugimoto. 1994. DNA polymerase alpha associated protein P1, a murine homolog of yeast MCM3, changes its intranuclear distribution during the DNA synthetic period. EMBO J. 13:4311-4320.
28. Krishna, T.S., X.P. Kong, S. Gary, P.M. Burgers, and J. Kuriyan. 1994. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell. 79:1233-1243.
29. Krude, T., C. Musahl, R.A. Laskey, and R. Knippers. 1996. Human replication proteins hCdc21, hCdc46 and P1Mcm3 bind chromatin uniformly before S-phase and are displaced locally during DNA replication. J. Cell Sci. 109: 309-318.
30. Kubota, Y., S. Mimura, S. Nishimoto, H. Takisawa, and H. Nojima. 1995. Identification of the yeast MCM3-related protein as a component of Xenopus DNA replication licensing factor. Cell. 81:601-609.
31. Lei, M., and B.K. Tye. 2001. Initiating DNA synthesis: from recruiting to activating the MCM complex. J. Cell Sci. 114:1447-1454.
32. Lei, M., Y. Kawasaki, and B.K. Tye. 1996. Physical interactions among Mcm proteins and effects of Mcm dosage on DNA replication in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:5081-5090.
33. Lengronne, A., and E. Schwob. 2002. The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Mol. Cell. 9:1067-1078.
34. Loeb, K.R., and L.A. Loeb. 2000. Significance of multiple mutations in cancer. Carcinogenesis. 21:379-385.
35. Maiorano, D., J.M. Lemaitre, and M. Mechali. 2000. Stepwise regulated chromatin assembly of MCM2-7 proteins. J. Biol. Chem. 275:8426-8431.
36. Masuda, A., and T. Takahashi. 2002. Chromosome instability in human lung cancers: possible underlying mechanisms and potential consequences in the pathogenesis. Oncogene. 21:6884-6897.
37. Méndez, J., and B. Stillman. 2000. Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20:8602-8612.
38. Méndez, J., and B. Stillman. 2003. Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins. Bioessays. 25:1158-1167.
39. Méndez, J., X.H. Zou-Yang, S.Y. Kim, M. Hidaka, W.P. Tansey, and B. Stillman. 2002. Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol. Cell. 9:481-491.
40. Moberg, K.H., D.W. Bell, D.C. Wahrer, D.A. Haber, and I.K. Hariharan. 2001. Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature. 413:311-316.
41. Nakamura, H., T. Morita, and C. Sato. 1986. Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp. Cell Res. 165:291-297.
42. Nakayasu, H., and R. Berezney. 1989. Mapping replicational sites in the eucaryotic cell nucleus. J. Cell Biol. 108:1-11.
43. Nielsen, N.H., S.O. Emdin, J. Cajander, and G. Landberg. 1997. Deregulation of cyclin E and D1 in breast cancer is associated with inactivation of the retinoblastoma protein. Oncogene. 14:295-304.
44. Nielsen, N.H., C. Arnerlov, S. Cajander, and G. Landberg. 1998. Cyclin E expression and proliferation in breast cancer. Anal. Cell. Pathol. 17:177-188.
45. Nielsen, N.H., M. Loden, J. Cajander, S.O. Emdin, and G. Landberg. 1999. G1-S transition defects occur in most breast cancers and predict outcome. Breast Cancer Res. Treat. 56:105-112.
46. Nishitani, H., and Z. Lygerou. 2002. Control of DNA replication licensing in a cell cycle. Genes Cells. 7:523-534.
47. Ohtsubo, M., and J.M. Roberts. 1993. Cyclin-dependent regulation of G1 in mammalian fibroblasts. Science. 259:1908-1912.
48. Prelich, G., C.K. Tan, M. Kostura, M.B. Mathews, A.G. So, K.M. Downey, and B. Stillman. 1987. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature. 326:517-520.
49. Rajagopalan, H., P.V. Jallepalli, C. Rago, V.E. Velculescu, K.W. Kinzler, B. Vogelstein, and C. Lengauer. 2004. Inactivation of hCDC4 can cause chromosomal instability. Nature. 428:77-81.
50. Reed, S.E., C.H. Spruck, O. Sangfelt, F. van Drogen, E. Mueller-Holzner, M. Widschwendter, A. Zetterberg, and S.I. Reed. 2004. Mutation of hCDC4 leads to cell cycle deregulation of cyclin E in cancer. Cancer Res. 64:795-800.
51. Resnitzky, D., M. Gossen, H. Bujard, and S.I. Reed. 1994. Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system. Mol. Cell. Biol. 14:1669-1679.
52. Ritzi, M., M. Baack, C. Musahl, P. Romanowski, R.A. Laskey, and R. Knippers. 1998. Human minichromosome maintenance proteins and human origin recognition complex 2 protein on chromatin. J. Biol. Chem. 273:24543-24549.
53. Sandhu, C., and J. Slingerland. 2000. Deregulation of the cell cycle in cancer. Cancer Detect. Prev. 24:107-118.
54. Sauer, K., and C.F. Lehner. 1995. The role of cyclin E in the regulation of entry into S phase. Prog. Cell Cycle Res. 1:125-139.
55. Schraml, P., C. Bucher, H. Bissig, A. Nocito, P. Haas, K. Wilber, S. Seelig, J. Kononen, M.J. Mihatsch, S. Dirnhofer, and G. Sauter. 2003. Cyclin E overexpression and amplification in human tumours. J. Pathol. 200:375-382.
56. Schwacha, A., and S.P. Bell. 2001. Interactions between two catalytically distinct MCM subgroups are essential for coordinated ATP hydrolysis and DNA replication. Mol. Cell. 8:1093-1104.
57. Somanathan, S., T.M. Suchyna, A.J. Siegel, and R. Berezney. 2001. Targeting of PCNA to sites of DNA replication in the mammalian cell nucleus. J. Cell. Biochem. 81:56-67.
58. Spruck, C.H., K.A. Won, and S.I. Reed. 1999. Deregulated cyclin E induces chromosome instability. Nature. 401:297-300.
59. Spruck, C.H., H. Strohmaier, O. Sangfelt, H.M. Muller, M. Hubalek, E. Muller-Holzner, C. Marth, M. Widschwendter, and S.I. Reed. 2002. hCDC4 gene mutations in endometrial cancer. Cancer Res. 62:4535-4539.
60. Strohmaier, H., C.H. Spruck, P. Kaiser, K.A. Won, O. Sangfelt, and S.I. Reed. 2001. Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature. 413:316-322.
61. Takanari, H., H. Yamanaka, H. Mitani, and K. Izutsu. 1994. Replication sites as revealed by double label immunofluorescence against proliferating cell nuclear antigen (PCNA) and bromodeoxyuridine (BrdU) in synchronized CHO cells and vincristine-induced multinucleate cells. Biol. Cell. 82:23-31.
62. Tanaka, S., and J.F. Diffley. 2002. Deregulated G1-cyclin expression induces genomic instability by preventing efficient pre-RC formation. Genes Dev. 16: 2639-2649.
63. Todorov, I.T., A. Attaran, and S.E. Kearsey. 1995. BM28, a human member of the MCM2-3-5 family, is displaced from chromatin during DNA replication. J. Cell Biol. 129:1433-1445.
64. Waseem, N.H., and D.P. Lane. 1990. Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA). Structural conservation and the detection of a nucleolar form. J. Cell Sci. 96:121-129.
65. Wimmel, A., F.C. Lucibello, A. Sewing, S. Adolph, and R. Muller. 1994. Inducible acceleration of G1 progression through tetracycline-regulated expression of human cyclin E. Oncogene. 9:995-997.
66. Woo, R.A., and R.Y. Poon. 2003. Cyclin-dependent kinases and S phase control in mammalian cells. Cell Cycle. 2:316-324.
67. Wuarin, J., and P. Nurse. 1996. Regulating S phase: CDKs, licensing and proteolysis. Cell. 85:785-787.
68. Yan, H., and J. Newport. 1995. An analysis of the regulation of DNA synthesis by cdk2, Cip1, and licensing factor. J. Cell Biol. 129:1-15.
69. Zachariae, W., and K. Nasmyth. 1999. Whose end is destruction: cell division and the anaphase-promoting complex. Genes Dev. 13:2039-2058.