Oscillation of APC/C activity during cell cycle arrest promotes centrosome amplification

Journal of Cell Science

Volumn 125, Issue 22, 2012, Pages 5353-5368

  Prosser, Suzanna L ^a,b   Samant, Mugdha D ^a,c   Baxter, Joanne E ^a   Morrison, Ciaran G ^b   Fry, Andrew M ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

APC C; Centriole disengagement; Centrosome amplification; Emi1; Plk1; Separase

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CYCLIN A; CYCLIN DEPENDENT KINASE 2; HYDROXYUREA; POLO LIKE KINASE 1; SECURIN; SEPARASE;

ARTICLE; CELL CYCLE ARREST; CENTRIOLE; CENTROSOME; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; G2 PHASE CELL CYCLE CHECKPOINT; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MITOSIS; OSCILLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CENTRIOLES; CENTROSOME; ENDOPEPTIDASES; ENZYME ACTIVATION; HELA CELLS; HUMANS; HYDROXYUREA; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RADIATION, IONIZING; SEPARASE; SIGNAL TRANSDUCTION; SPINDLE APPARATUS; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 84868021612     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.106096     Document Type: Article

References (93)

1. Balczon, R., Bao, L., Zimmer, W. E., Brown, K., Zinkowski, R. P. and Brinkley, B. R. (1995). Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J. Cell Biol. 130, 105-115.
2. Bassermann, F., Frescas, D., Guardavaccaro, D., Busino, L., Peschiaroli, A. and Pagano, M. (2008). The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damageresponse checkpoint. Cell 134, 256-267.
3. Basto, R., Brunk, K., Vinadogrova, T., Peel, N., Franz, A., Khodjakov, A. and Raff, J. W. (2008). Centrosome amplification can initiate tumorigenesis in flies. Cell 133, 1032-1042.
4. Beauchene, N. A., Díaz-Martínez, L. A., Furniss, K., Hsu, W. S., Tsai, H. J., Chamberlain, C., Esponda, P., Giménez-Abián, J. F. and Clarke, D. J. (2010). Rad21 is required for centrosome integrity in human cells independently of its role in chromosome cohesion. Cell Cycle 9, 1774-1780.
5. Bernis, C., Vigneron, S., Burgess, A., Labbé, J. C., Fesquet, D., Castro, A. and Lorca, T. (2007). Pin1 stabilizes Emi1 during G2 phase by preventing its association with SCF(betatrcp). EMBO Rep. 8, 91-98.
6. Bettencourt-Dias, M. and Glover, D. M. (2007). Centrosome biogenesis and function: centrosomics brings new understanding. Nat. Rev. Mol. Cell Biol. 8, 451-463.
7. Bettencourt-Dias, M., Rodrigues-Martins, A., Carpenter, L., Riparbelli, M., Lehmann, L., Gatt, M. K., Carmo, N., Balloux, F., Callaini, G. and Glover, D. M. (2005). SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15, 2199-2207.
8. Bourke, E., Dodson, H., Merdes, A., Cuffe, L., Zachos, G., Walker, M., Gillespie, D. and Morrison, C. G. (2007). DNA damage induces Chk1-dependent centrosome amplification. EMBO Rep. 8, 603-609.
9. Bourke, E., Brown, J. A., Takeda, S., Hochegger, H. and Morrison, C. G. (2010). DNA damage induces Chk1-dependent threonine-160 phosphorylation and activation of Cdk2. Oncogene 29, 616-624.
10. Chestukhin, A., Pfeffer, C., Milligan, S., DeCaprio, J. A. and Pellman, D. (2003). Processing, localization, and requirement of human separase for normal anaphase progression. Proc. Natl. Acad. Sci. USA 100, 4574-4579.
11. Conduit, P. T., Brunk, K., Dobbelaere, J., Dix, C. I., Lucas, E. P. and Raff, J. W. (2010). Centrioles regulate centrosome size by controlling the rate of Cnn incorporation into the PCM. Curr. Biol. 20, 2178-2186.
12. Decker, M., Jaensch, S., Pozniakovsky, A., Zinke, A., O'Connell, K. F., Zachariae, W., Myers, E. and Hyman, A. A. (2011). Limiting amounts of centrosome material set centrosome size in C. elegans embryos. Curr. Biol. 21, 1259-1267.
13. Delattre, M., Canard, C. and Gönczy, P. (2006). Sequential protein recruitment in C. elegans centriole formation. Curr. Biol. 16, 1844-1849.
14. Di Fiore, B. and Pines, J. (2007). Emi1 is needed to couple DNA replication with mitosis but does not regulate activation of the mitotic APC/C. J. Cell Biol. 177, 425-437.
15. Díaz-Martínez, L. A., Beauchene, N. A., Furniss, K., Esponda, P., Giménez-Abián, J. F. and Clarke, D. J. (2010). Cohesin is needed for bipolar mitosis in human cells. Cell Cycle 9, 1764-1773.
16. Dix, C. I. and Raff, J. W. (2007). Drosophila Spd-2 recruits PCM to the sperm centriole, but is dispensable for centriole duplication. Curr. Biol. 17, 1759-1764.
17. Dobbelaere, J., Josué, F., Suijkerbuijk, S., Baum, B., Tapon, N. and Raff, J. (2008). A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS Biol. 6, e224.
18. Dodson, H., Bourke, E., Jeffers, L. J., Vagnarelli, P., Sonoda, E., Takeda, S., Earnshaw, W. C., Merdes, A. and Morrison, C. (2004). Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J. 23, 3864-3873.
19. Eldridge, A. G., Loktev, A. V., Hansen, D. V., Verschuren, E. W., Reimann, J. D. and Jackson, P. K. (2006). The evi5 oncogene regulates cyclin accumulation by stabilizing the anaphase-promoting complex inhibitor emi1. Cell 124, 367-380.
20. Faragher, A. J. and Fry, A. M. (2003). Nek2A kinase stimulates centrosome disjunction and is required for formation of bipolar mitotic spindles. Mol. Biol. Cell 14, 2876-2889.
21. Fry, A. M., Mayor, T., Meraldi, P., Stierhof, Y.-D., Tanaka, K. and Nigg, E. A. (1998). C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell Biol. 141, 1563-1574.
22. Ganem, N. J., Godinho, S. A. and Pellman, D. (2009). A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282.
23. Giménez-Abián, J. F., Sumara, I., Hirota, T., Hauf, S., Gerlich, D., de la Torre, C., Ellenberg, J. and Peters, J. M. (2004). Regulation of sister chromatid cohesion between chromosome arms. Curr. Biol. 14, 1187-1193.
24. Giménez-Abián, J. F., Díaz-Martínez, L. A., Beauchene, N. A., Hsu, W. S., Tsai, H. J. and Clarke, D. J. (2010). Determinants of Rad21 localization at the centrosome in human cells. Cell Cycle 9, 1759-1763.
25. Gregson, H. C., Schmiesing, J. A., Kim, J. S., Kobayashi, T., Zhou, S. and Yokomori, K. (2001). A potential role for human cohesin in mitotic spindle aster assembly. J. Biol. Chem. 276, 47575-47582.
26. Guan, J., Ekwurtzel, E., Kvist, U. and Yuan, L. (2008). Cohesin protein SMC1 is a centrosomal protein. Biochem. Biophys. Res. Commun. 372, 761-764.
27. Guichard, P., Chrétien, D., Marco, S. and Tassin, A. M. (2010). Procentriole assembly revealed by cryo-electron tomography. EMBO J. 29, 1565-1572.
28. Habedanck, R., Stierhof, Y. D., Wilkinson, C. J. and Nigg, E. A. (2005). The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7, 1140-1146.
29. Hansen, D. V., Loktev, A. V., Ban, K. H. and Jackson, P. K. (2004). Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCFbetaTrCP-dependent destruction of the APC inhibitor Emi1. Mol. Biol. Cell 15, 5623-5634.
30. Hardcastle, I. R., Arris, C. E., Bentley, J., Boyle, F. T., Chen, Y., Curtin, N. J., Endicott, J. A., Gibson, A. E., Golding, B. T., Griffin, R. J. et al. (2004). N2- substituted O6-cyclohexylmethylguanine derivatives: potent inhibitors of cyclindependent kinases 1 and 2. J. Med. Chem. 47, 3710-3722.
31. Hauf, S., Roitinger, E., Koch, B., Dittrich, C. M., Mechtler, K. and Peters, J. M. (2005). Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2. PLoS Biol. 3, e69.
32. Hayles, J., Fisher, D., Woollard, A. and Nurse, P. (1994). Temporal order of S phase and mitosis in fission yeast is determined by the state of the p34cdc2-mitotic B cyclin complex. Cell 78, 813-822.
33. Hinchcliffe, E. H., Li, C., Thompson, E. A., Maller, J. L. and Sluder, G. (1999). Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283, 851-854.
34. Hochegger, H., Dejsuphong, D., Sonoda, E., Saberi, A., Rajendra, E., Kirk, J., Hunt, T. and Takeda, S. (2007). An essential role for Cdk1 in S phase control is revealed via chemical genetics in vertebrate cells. J. Cell Biol. 178, 257-268.
35. Holland, A. J. and Taylor, S. S. (2006). Cyclin-B1-mediated inhibition of excess separase is required for timely chromosome disjunction. J. Cell Sci. 119, 3325-3336.
36. Hut, H. M., Lemstra, W., Blaauw, E. H., Van Cappellen, G. W., Kampinga, H. H. and Sibon, O. C. (2003). Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol. Biol. Cell 14, 1993-2004.
37. Inanç, B., Dodson, H. and Morrison, C. G. (2010). A centrosome-autonomous signal that involves centriole disengagement permits centrosome duplication in G2 phase after DNA damage. Mol. Biol. Cell 21, 3866-3877.
38. Itzhaki, J. E., Gilbert, C. S. and Porter, A. C. (1997). Construction by gene targeting in human cells of a ''conditional' CDC2 mutant that rereplicates its DNA. Nat. Genet. 15, 258-265.
39. Kastan, M. B. and Bartek, J. (2004). Cell-cycle checkpoints and cancer. Nature 432, 316-323.
40. Kitagawa, D., Vakonakis, I., Olieric, N., Hilbert, M., Keller, D., Olieric, V., Bortfeld, M., Erat, M. C., Flückiger, I., Gönczy, P. et al. (2011). Structural basis of the 9-fold symmetry of centrioles. Cell 144, 364-375.
41. Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Habedanck, R., Stierhof, Y. D. and Nigg, E. A. (2007). Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202.
42. Koepp, D. M., Schaefer, L. K., Ye, X., Keyomarsi, K., Chu, C., Harper, J. W. and Elledge, S. J. (2001). Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294, 173-177.
43. Kong, X., Ball, A. R., Jr, Sonoda, E., Feng, J., Takeda, S., Fukagawa, T., Yen, T. J. and Yokomori, K. (2009). Cohesin associates with spindle poles in a mitosis-specific manner and functions in spindle assembly in vertebrate cells. Mol. Biol. Cell 20, 1289-1301.
44. Kraft, C., Herzog, F., Gieffers, C., Mechtler, K., Hagting, A., Pines, J. and Peters, J. M. (2003). Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 22, 6598-6609.
45. Lacey, K. R., Jackson, P. K. and Stearns, T. (1999). Cyclin-dependent kinase control of centrosome duplication. Proc. Natl. Acad. Sci. USA 96, 2817-2822.
46. Lee, J., Kim, J. A., Barbier, V., Fotedar, A. and Fotedar, R. (2009). DNA damage triggers p21WAF1-dependent Emi1 down-regulation that maintains G2 arrest. Mol. Biol. Cell 20, 1891-1902.
47. Loncarek, J. and Khodjakov, A. (2009). Ab ovo or de novo? Mechanisms of centriole duplication. Mol. Cells 27, 135-142.
48. Loncarek, J., Hergert, P., Magidson, V. and Khodjakov, A. (2008). Control of daughter centriole formation by the pericentriolar material. Nat. Cell Biol. 10, 322- 328.
49. Loncarek, J., Hergert, P. and Khodjakov, A. (2010). Centriole reduplication during prolonged interphase requires procentriole maturation governed by Plk1. Curr. Biol. 20, 1277-1282.
50. Losada, A., Yokochi, T. and Hirano, T. (2005). Functional contribution of Pds5 to cohesin-mediated cohesion in human cells and Xenopus egg extracts. J. Cell Sci. 118, 2133-2141.
51. Ma, H. T., Tsang, Y. H., Marxer, M. and Poon, R. Y. (2009). Cyclin A2-cyclindependent kinase 2 cooperates with the PLK1-SCFbeta-TrCP1-EMI1-anaphasepromoting complex/cyclosome axis to promote genome reduplication in the absence of mitosis. Mol. Cell. Biol. 29, 6500-6514.
52. Macůrek, L., Lindqvist, A., Lim, D., Lampson, M. A., Klompmaker, R., Freire, R., Clouin, C., Taylor, S. S., Yaffe, M. B. and Medema, R. H. (2008). Polo-like kinase- 1 is activated by aurora A to promote checkpoint recovery. Nature 455, 119-123.
53. Matsumoto, Y., Hayashi, K. and Nishida, E. (1999). Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells. Curr. Biol. 9, 429- 432.
54. Matsuo, K., Ohsumi, K., Iwabuchi, M., Kawamata, T., Ono, Y. and Takahashi, M. (2012). Kendrin is a novel substrate for separase involved in the licensing of centriole duplication. Curr. Biol. 22, 915-921.
55. Mazia, D. (1987). The chromosome cycle and the centrosome cycle in the mitotic cycle. Int. Rev. Cytol. 100, 49-92.
56. Meraldi, P., Lukas, J., Fry, A. M., Bartek, J. and Nigg, E. A. (1999). Centrosome duplication in mammalian somatic cells requires E2F and Cdk2-cyclin A. Nat. Cell Biol. 1, 88-93.
57. Moshe, Y., Boulaire, J., Pagano, M. and Hershko, A. (2004). Role of Polo-like kinase in the degradation of early mitotic inhibitor 1, a regulator of the anaphase promoting complex/cyclosome. Proc. Natl. Acad. Sci. USA 101, 7937-7942.
58. Moshe, Y., Bar-On, O., Ganoth, D. and Hershko, A. (2011). Regulation of the action of early mitotic inhibitor 1 on the anaphase-promoting complex/cyclosome by cyclindependent kinases. J. Biol. Chem. 286, 16647-16657.
59. Nakamura, A., Arai, H. and Fujita, N. (2009). Centrosomal Aki1 and cohesin function in separase-regulated centriole disengagement. J. Cell Biol. 187, 607-614.
60. Nasmyth, K. (2002). Segregating sister genomes: the molecular biology of chromosome separation. Science 297, 559-565.
61. Nigg, E. A. and Raff, J. W. (2009). Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663-678.
62. Pelletier, L., O'Toole, E., Schwager, A., Hyman, A. A. and Mü ller-Reichert, T. (2006). Centriole assembly in Caenorhabditis elegans. Nature 444, 619-623.
63. Peters, J. M., Tedeschi, A. and Schmitz, J. (2008). The cohesin complex and its roles in chromosome biology. Genes Dev. 22, 3089-3114.
64. Prosser, S. L., Straatman, K. R. and Fry, A. M. (2009). Molecular dissection of the centrosome overduplication pathway in S-phase-arrested cells. Mol. Cell. Biol. 29, 1760-1773.
65. Rogers, G. C., Rusan, N. M., Roberts, D. M., Peifer, M. and Rogers, S. L. (2009). The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol. 184, 225-239.
66. Saladino, C., Bourke, E., Conroy, P. C. and Morrison, C. G. (2009). Centriole separation in DNA damage-induced centrosome amplification. Environ. Mol. Mutagen. 50, 725-732.
67. Sato, N., Mizumoto, K., Nakamura, M., Ueno, H., Minamishima, Y. A., Farber, J. L. and Tanaka, M. (2000). A possible role for centrosome overduplication in radiation-induced cell death. Oncogene 19, 5281-5290.
68. Schöckel, L., Möckel, M., Mayer, B., Boos, D. and Stemmann, O. (2011). Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat. Cell Biol. 13, 966-972.
69. Seki, A., Coppinger, J. A., Jang, C. Y., Yates, J. R. and Fang, G. (2008). Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science 320, 1655-1658.
70. Skaar, J. R. and Pagano, M. (2009). Control of cell growth by the SCF and APC/C ubiquitin ligases. Curr. Opin. Cell Biol. 21, 816-824.
71. Smits, V. A., Klompmaker, R., Arnaud, L., Rijksen, G., Nigg, E. A. and Medema, R. H. (2000). Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat. Cell Biol. 2, 672-676.
72. Song, M. H., Aravind, L., Mü ller-Reichert, T. and O'Connell, K. F. (2008). The conserved protein SZY-20 opposes the Plk4-related kinase ZYG-1 to limit centrosome size. Dev. Cell 15, 901-912.
73. Steere, N., Wagner, M., Beishir, S., Smith, E., Breslin, L., Morrison, C. G., Hochegger, H. and Kuriyama, R. (2011). Centrosome amplification in CHO and DT40 cells by inactivation of cyclin-dependent kinases. Cytoskeleton (Hoboken) 68, 446-458.
74. Stemmann, O., Zou, H., Gerber, S. A., Gygi, S. P. and Kirschner, M. W. (2001). Dual inhibition of sister chromatid separation at metaphase. Cell 107, 715-726.
75. Stevens, N. R., Roque, H. and Raff, J. W. (2010). DSas-6 and Ana2 coassemble into tubules to promote centriole duplication and engagement. Dev. Cell 19, 913-919.
76. Strnad, P. and Gönczy, P. (2008). Mechanisms of procentriole formation. Trends Cell Biol. 18, 389-396.
77. Strohmaier, H., Spruck, C. H., Kaiser, P., Won, K. A., Sangfelt, O. and Reed, S. I. (2001). Human F-box protein hCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature 413, 316-322.
78. Sudo, T., Ota, Y., Kotani, S., Nakao, M., Takami, Y., Takeda, S. and Saya, H. (2001). Activation of Cdh1-dependent APC is required for G1 cell cycle arrest and DNA damage-induced G2 checkpoint in vertebrate cells. EMBO J. 20, 6499-6508.
79. Thein, K. H., Kleylein-Sohn, J., Nigg, E. A. and Gruneberg, U. (2007). Astrin is required for the maintenance of sister chromatid cohesion and centrosome integrity. J. Cell Biol. 178, 345-354.
80. Tsou, M. F. and Stearns, T. (2006a). Controlling centrosome number: licenses and blocks. Curr. Opin. Cell Biol. 18, 74-78.
81. Tsou, M. F. and Stearns, T. (2006b). Mechanism limiting centrosome duplication to once per cell cycle. Nature 442, 947-951.
82. Tsou, M. F., Wang, W. J., George, K. A., Uryu, K., Stearns, T. and Jallepalli, P. V. (2009). Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev. Cell 17, 344-354.
83. van Breugel, M., Hirono, M., Andreeva, A., Yanagisawa, H. A., Yamaguchi, S., Nakazawa, Y., Morgner, N., Petrovich, M., Ebong, I. O., Robinson, C. V. et al. (2011). Structures of SAS-6 suggest its organization in centrioles. Science 331, 1196- 1199.
84. Vassilev, L. T. (2006). Cell cycle synchronization at the G2/M phase border by reversible inhibition of CDK1. Cell Cycle 5, 2555-2556.
85. Vassilev, L. T., Tovar, C., Chen, S., Knezevic, D., Zhao, X., Sun, H., Heimbrook, D. C. and Chen, L. (2006). Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc. Natl. Acad. Sci. USA 103, 10660-10665.
86. Walczak, C. E. and Heald, R. (2008). Mechanisms of mitotic spindle assembly and function. Int. Rev. Cytol. 265, 111-158.
87. Wang, X., Yang, Y., Duan, Q., Jiang, N., Huang, Y., Darzynkiewicz, Z. and Dai, W. (2008). sSgo1, a major splice variant of Sgo1, functions in centriole cohesion where it is regulated by Plk1. Dev. Cell 14, 331-341.
88. Wang, W. J., Soni, R. K., Uryu, K. and Tsou, M. F. (2011). The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol. 193, 727-739.
89. Watanabe, N., Arai, H., Nishihara, Y., Taniguchi, M., Watanabe, N., Hunter, T. and Osada, H. (2004). M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Proc. Natl. Acad. Sci. USA 101, 4419-4424.
90. Wiebusch, L. and Hagemeier, C. (2010). p53- and p21-dependent premature APC/CCdh1 activation in G2 is part of the long-term response to genotoxic stress. Oncogene 29, 3477-3489.
91. Wong, R. W. and Blobel, G. (2008). Cohesin subunit SMC1 associates with mitotic microtubules at the spindle pole. Proc. Natl. Acad. Sci. USA 105, 15441-15445.
92. Yata, K., Lloyd, J., Maslen, S., Bleuyard, J. Y., Skehel, M., Smerdon, S. J. and Esashi, F. (2012). Plk1 and CK2 act in concert to regulate Rad51 during DNA double strand break repair. Mol. Cell 45, 371-383.
93. Zeng, X., Sigoillot, F., Gaur, S., Choi, S., Pfaff, K. L., Oh, D. C., Hathaway, N., Dimova, N., Cuny, G. D. and King, R. W. (2010). Pharmacologic inhibition of the anaphase-promoting complex induces a spindle checkpoint-dependent mitotic arrest in the absence of spindle damage. Cancer Cell 18, 382-395.