SCF-FBXO31 E3 ligase targets DNA replication factor Cdt1 for proteolysis in the G2 phase of cell cycle to prevent Re-replication

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18514-18525

  Johansson, Pegah ^a   Jeffery, Jessie ^b   Al Ejeh, Fares ^b   Schulz, Renèe B ^c   Callen, David F ^c   Kumar, Raman ^d   Khanna, Kum Kum ^b  

^a SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DIAGNOSIS; DISEASES; PROTEOLYSIS; TUMORS;

CELL CYCLE REGULATION; DNA REPLICATIONS; GENOMIC INTEGRITY; PRE-REPLICATION COMPLEXES; PROSTATE CANCERS; TUMOR SUPPRESSOR GENES; TUMOR SUPPRESSORS; UBIQUITYLATION;

CELLS;

REPLICATION LICENSING FACTOR CDT1; SCF FBXO31 E3 UBIQUITIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL DIVISION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; REGULATORY MECHANISM; UBIQUITINATION;

CDT1; CELL CYCLE; DNA REPLICATION; E3 UBIQUITIN LIGASE; FBXO31; GENOMIC INSTABILITY; PROTEIN DEGRADATION;

CELL CYCLE; CELL CYCLE PROTEINS; DNA REPLICATION; F-BOX PROTEINS; G2 PHASE; HUMANS; PROTEIN BINDING; PROTEOLYSIS; TUMOR SUPPRESSOR PROTEINS; UBIQUITINATION;

EID: 84903519467     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.559930     Document Type: Article

References (47)

1. Härkönen, P., Kyllönen, A. P., Nordling, S., and Vihko, P. (2005) Loss of heterozygosity in chromosomal region 16q24.3 associated with progression of prostate cancer. Prostate 62, 267-274
2. Kumar, R., Neilsen, P. M., Crawford, J., McKirdy, R., Lee, J., Powell, J. A., Saif, Z., Martin, J. M., Lombaerts, M., Cornelisse, C. J., Cleton-Jansen, A. M., and Callen, D. F. (2005) FBXO31 is the chromosome 16q24.3 senescence gene, a candidate breast tumor suppressor, and a component of an SCF complex. Cancer Res. 65, 11304-11313
3. Launonen, V., Mannermaa, A., Stenbäck, F., Kosma, V. M., Puistola, U., Huusko, P., Anttila, M., Bloigu, R., Saarikoski, S., Kauppila, A., and Winqvist, R. (2000) Loss of heterozygosity at chromosomes 3, 6, 8, 11, 16, and 17 in ovarian cancer: correlation to clinicopathological variables. Cancer Genet. Cytogenet. 122, 49-54
4. Lin, Y. W., Lee, I. N., Chen, C H., Huang, G. T., Lee, H. S., Lee, P. H., Lu, F. J., and Sheu, J. C (2001) Deletion mapping of chromosome 16q24 in hepatocellular carcinoma in Taiwan and mutational analysis of the 17-β3-HSD gene localized to the region. Int. J. Cancer 93, 74-79
5. Miller, B. J., Wang, D., Krahe, R., and Wright, F. A. (2003) Pooled analysis of loss of heterozygosity in breast cancer: a genome scan provides comparative evidence for multiple tumor suppressors and identifies novel candidate regions. Am. J. Hum. Genet. 73, 748-767
6. Zheng, N, Schulman, B. A., Song, L., Miller, J. J., Jeffrey, P. D., Wang, P., Chu, C, Koepp, D. M., Elledge, S. J., Pagano, M., Conaway, R. C, Conaway, J. W., Harper, J. W., and Pavletich, N. P. (2002) Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416, 703-709
7. Schwartz, A. L., and Ciechanover, A. (1999) The ubiquitin-proteasome pathway and pathogenesis of human diseases. Annu. Rev. Med. 50, 57-74
8. Jin, J., Cardozo, T., Lovering, R. C, Elledge, S. J., Pagano, M., and Harper, J. W. (2004) Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev. 18, 2573-2580
9. Cardozo, T., and Pagano, M. (2004) The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751
10. Skaar, J. R., D'Angiolella, V., Pagan, J. K., and Pagano, M. (2009) SnapShot: F Box Proteins II. Cell 137, 1358
11. 1 arrest after DNA damage. Nature 459, 722-725
12. Kanie, T., Onoyama, I., Matsumoto, A., Yamada, M., Nakatsumi, H, Tateishi, Y., Yamamura, S., Tsunematsu, R., Matsumoto, M., and Nakayama, K. I. (2012) Genetic reevaluation of the role of F-box proteins in cyclin D1 degradation. Mol. Cell Biol. 32, 590-605
13. Vadhvani, M., Schwedhelm-Domeyer, N, Mukherjee, C, and Stegmüller, J. (2013) The centrosomal E3 ubiquitin ligase FBXO31-SCF regulates neuronal morphogenesis and migration. PLoS ONE 8, e57530
14. Huang, H. L., Zheng, W. L., Zhao, R., Zhang, B., and Ma, W. L. (2010) FBXO31 is down-regulated and may function as a tumor suppressor in hepatocellular carcinoma. Oncol. Rep. 24, 715-720
15. Kogo, R., Mimori, K., Tanaka, F., Komune, S., and Mori, M. (2011) FBXO31 determines poor prognosis in esophageal squamous cell carcinoma. Int. J. Oncol. 39, 155-159
16. Stillman, B. (2005) Origin recognition and the chromosome cycle. FEBS Lett. 579, 877-884
17. Blow, J. J., and Dutta, A. (2005) Preventing re-replication of chromosomal DNA. Nat Rev. Mol. Cell Biol. 6, 476-486
18. Fujita, M. (2006) Cdt1 revisited: complex and tight regulation during the cell cycle and consequences of deregulation in mammalian cells. CellDiv. 1, 22
19. Nishitani, H, Sugimoto, N, Roukos, V., Nakanishi, Y., Saijo, M., Obuse, C, Tsurimoto, T., Nakayama, K. I., Nakayama, K., Fujita, M., Lygerou, Z., and Nishimoto, T. (2006) Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBOJ. 25, 1126-1136
20. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
21. Chandrasekaran, S., Tan, T. X., Hall, J. R., and Cook, J. G. (2011) Stressstimulated mitogen-activated protein kinases control the stability and activity of the Cdt1 DNA replication licensing factor. Mol. Cell Biol. 31, 4405-4416
22. 2 and is enhanced by checkpoint activation. J. CellSci. 125, 2436-2445
23. Jarvius, M., Paulsson, J., Weibrecht, I., Leuchowius, K. J., Andersson, A. C, Wählby, C, Gullberg, M., Botling, J., Sjöblom, T., Markova, B., Ostman, A., Landegren, U., and Söderberg, O. (2007) In situ detection of phosphorylated platelet-derived growth factor receptor β using a generalized proximity ligation method. Mol. Cell. Proteomics 6, 1500-1509
24. Söderberg, O., Leuchowius, K. J., Kamali-Moghaddam, M., Jarvius, M., Gustafsdottir, S., Schallmeiner, E., Gullberg, M., Jarvius, J., and Landegren, U. (2007) Proximity ligation: a specific and versatile tool for the proteomic era. Genetic engineering 28, 85-93
25. Fredriksson, S., Gullberg, M., Jarvius, J., Olsson, C, Pietras, K., Gústafsdóttir, S. M., Ostman, A., and Landegren, U. (2002) Protein detection using proximity-dependent DNA ligation assays. Nat. Biotechnol. 20, 473-477
26. Li, X., Zhao, Q., Liao, R., Sun, P., and Wu, X. (2003) The SCF (Skp2) ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation. J. Biol. Chem. 278, 30854-30858
27. Liu, E., Li, X., Yan, F., Zhao, Q., and Wu, X. (2004) Cyclin-dependent kinases phosphorylate human Cdt1 and induce its degradation. J. Biol. Chem. 279, 17283-17288
28. 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
29. Arias, E. E., and Walter, J. C. (2006) PCNA functions as a molecular platform totrigger Cdt1 destruction and prevent re-replication. Nat. Cell Biol. 8, 84-90
30. Nishitani, H., Lygerou, Z., and Nishimoto, T. (2004) Proteolysis of DNA replication licensing factor Cdt1in S-phase is performed independently of geminin through its N-terminal region. J. Biol. Chem. 279, 30807-30816
31. Arias, E. E., and Walter, J. C. (2005) Replication-dependent destruction of Cdt1 limits DNA replicationto asingle round per cell cycle inXenopusegg extracts. Genes Dev. 19, 114-126
32. 2 nuclei in Xenopus egg extracts. Curr. Biol. 15, 146-153
33. Tatsumi, Y., Sugimoto, N., Yugawa, T., Narisawa-Saito, M., Kiyono, T., and Fujita, M. (2006) Deregulation of Cdt1 induces chromosomal damage without rereplication and leadsto chromosomal instability. J. Cell Sci. 119, 3128-3140
34. Vaziri, C., Saxena, S., Jeon, Y., Lee, C., Murata, K., Machida, Y., Wagle, N., Hwang, D. S., and Dutta, A. (2003) A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell 11, 997-1008
35. Tada, S., Li, A., Maiorano, D., Méchali, M., and Blow, J. J. (2001) Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat. Cell Biol. 3, 107-113
36. Wohlschlegel, J. A., Dwyer, B. T., Dhar, S. K., Cvetic, C., Walter, J. C., and Dutta, A. (2000) Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290, 2309-2312
37. Xouri, G., Lygerou, Z., Nishitani, H., Pachnis, V., Nurse, P., and Taraviras, S. (2004) Cdt1 and geminin are down-regulated upon cell cycle exit and are over-expressed in cancer-derived cell lines. Eur. J. Biochem. 271, 3368-3378
38. Nakayama, K. I., and Nakayama, K. (2006) Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 6, 369-381
39. Yen, H. C., and Elledge, S. J. (2008) Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 322, 923-929
40. Varma, D., Chandrasekaran, S., Sundin, L. J., Reidy, K. T., Wan, X., Chasse, D. A., Nevis, K. R., DeLuca, J. G., Salmon, E. D., and Cook, J. G. (2012) Recruitment of the human Cdt1 replication licensing protein by the loop domain of Hec1 is required for stable kinetochore-microtubule attachment. Nat. Cell Biol. 14, 593-603
41. Bassermann, F., von Klitzing, C., Münch, S., Bai, R. Y., Kawaguchi, H., Morris, S. W., Peschel, C., and Duyster, J. (2005) NIPA defines an SCF-type mammalian E3 ligase that regulates mitotic entry. Cell 122, 45-57
42. Chan, C. H., Lee, S. W., Wang, J., and Lin, H. K. (2010) Regulation of Skp2 expression and activity and its role in cancer progression. Scientific World-Journal 10, 1001-1015
43. Arentson, E., Faloon, P., Seo, J., Moon, E., Studts, J. M., Fremont, D. H., and Choi, K. (2002) Oncogenic potential of the DNA replication licensing protein CDT1. Oncogene 21, 1150-1158
44. Li, A., and Blow, J. J. (2005) Cdt1 downregulation by proteolysis and geminin inhibition prevents DNA re-replication in Xenopus. EMBO J. 24, 395-404
45. Thomer, M., May, N. R., Aggarwal, B. D., Kwok, G., and Calvi, B. R. (2004) Drosophila double-parked is sufficient to induce re-replication during development and is regulated by cyclin E/CDK2. Development 131, 4807-4818
46. Yoshida, K., Takisawa, H., and Kubota, Y. (2005) Intrinsic nuclear import activity of geminin is essential to prevent re-initiation of DNA replication in Xenopus eggs. Genes Cells 10, 63-73
47. Takeda, D. Y., Parvin, J. D., and Dutta, A. (2005) Degradation of Cdt1 during S phase is Skp2-independent and is required for efficient progression of mammalian cells through S phase. J. Biol. Chem. 280, 23416-23423