Phosphorylation of Mcl-1 by CDK1-cyclin B1 initiates its Cdc20-dependent destruction during mitotic arrest

EMBO Journal

Volumn 29, Issue 14, 2010, Pages 2407-2420

  Harley, Margaret E ^a   Allan, Lindsey A ^a   Sanderson, Helen S ^a   Clarke, Paul R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

apoptosis; Cdc20; cyclin dependent kinase; Mcl 1; mitosis

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN 20; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; HISTONE; PROTEASOME; PROTEIN MCL 1; UBIQUITIN PROTEIN LIGASE E3;

APOPTOSIS; ARTICLE; CELL CYCLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MICROTUBULE; MITOSIS; MITOSIS INHIBITION; MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CASPASE 9; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CELL LINE; CYCLIN B1; HUMANS; MITOSIS; MOLECULAR SEQUENCE DATA; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; SERINE; THREONINE;

EID: 77954884045     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.112     Document Type: Article

References (58)

1. Acquaviva C, Pines J (2006) The anaphase-promoting complex/cyclosome: APC/C. J Cell Sci 119: 2401-2404
2. Adams KW, Cooper GM (2007) Rapid turnover of mcl-1 couples translation to cell survival and apoptosis. J Biol Chem 282: 6192-6200
3. Allan LA, Clarke PR (2007) Phosphorylation of caspase-9 by CDK1/cyclin B1 protects mitotic cells against apoptosis. Mol Cell 26: 301-310
4. Allan LA, Clarke PR (2008) A mechanism coupling cell division and the control of apoptosis. SEB Exp Biol Ser 59: 257-265
5. Allan LA, Morrice N, Brady S, Magee G, Pathak S, Clarke PR (2003) Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK. Nat Cell Biol 5: 647-654
6. Bain J, McLauchlan H, Elliott M, Cohen P (2003) The specificities of protein kinase inhibitors: an update. Biochem J 371: 199-204
7. Bashir T, Dorrello NV, Amador V, Guardavaccaro D, Pagano M (2004) Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428: 190-193
8. Bekier ME, Fischbach R, Lee J, Taylor WR (2009) Length of mitotic arrest induced by microtubule-stabilizing drugs determines cell death after mitotic exit. Mol Cancer Ther 8: 1646-1654
9. Bennett LN, Clarke PR (2006) Regulation of claspin degradation by the ubiquitin-proteasome pathway during the cell cycle and in response to ATR-dependent checkpoint activation. FEBS Lett 580: 4176-4181
10. Blagosklonny MV (2007) Mitotic arrest and cell fate: why and how mitotic inhibition of transcription drives mutually exclusive events. Cell Cycle 6: 70-74
11. Brito DA, Rieder CL (2006) Mitotic checkpoint slippage in humans occurs via cyclin B destruction in the presence of an active checkpoint. Curr Biol 16: 1194-1200
12. Brito DA, Rieder CL (2009) The ability to survive mitosis in the presence of microtubule poisons differs significantly between human nontransformed (RPE-1) and cancer (U2OS, HeLa) cells. Cell Motil Cytoskeleton 66: 437-447
13. Clarke PR, Allan LA (2009) Cell-cycle control in the face of damage\a matter of life or death. Trends Cell Biol 19: 89-98
14. De Biasio A, Vrana JA, Zhou P, Qian L, Bieszczad CK, Braley KE, Domina AM, Weintraub SJ, Neveu JM, Lane WS, Craig RW (2007) N-terminal truncation of antiapoptotic MCL1, but not G2/M-induced phosphorylation, is associated with stabilization and abundant expression in tumor cells. J Biol Chem 282: 23919-23936
15. den Elzen N, Pines J (2001) Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J Cell Biol 153: 121-136
16. Ding Q, He X, Hsu JM, Xia W, Chen CT, Li LY, Lee DF, Liu JC, Zhong Q, Wang X, Hung MC (2007) Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 27: 4006-4017
17. Ding Q, Huo L, Yang JY, Xia W, Wei Y, Liao Y, Chang CJ, Yang Y, Lai CC, Lee DF, Yen CJ, Chen YJ, Hsu JM, Kuo HP, Lin CY, Tsai FJ, Li LY, Tsai CH, Hung MC (2008) Down-regulation of myeloid cell leuke-mia-1 through inhibiting Erk/Pin 1 pathway by sorafenib facilitates chemosensitization in breast cancer. Cancer Res 68: 6109-6117
18. Domina AM, Vrana JA, Gregory MA, Hann SR, Craig RW (2004) MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 23: 5301-5315
19. Du L, Lyle CS, Chambers TC (2005) Characterization of vinblastine-induced Bcl-xL and Bcl-2 phosphorylation: evidence for a novel protein kinase and a coordinated phosphorylation/dephosphor-ylation cycle associated with apoptosis induction. Oncogene 24: 107-117
20. Gascoigne KE, Taylor SS (2008) Cancer cells display profound intra-and interline variation following prolonged exposure to antimi-totic drugs. Cancer Cell 14: 111-122
21. Gascoigne KE, Taylor SS (2009) How do anti-mitotic drugs kill cancer cells? J Cell Sci 122: 2579-2585
22. Geley S, Kramer E, Gieffers C, Gannon J, Peters JM, 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
23. Glotzer M, Murray AW, Kirschner MW (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349: 132-138
24. Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, Soengas MS, Elia A, de la Pompa JL, Kagi D, Khoo W, Potter J, Yoshida R, Kaufman SA, Lowe SW, Penninger JM, Mak TW (1998) Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94: 339-352
25. Hames RS, Wattam SL, Yamano H, Bacchieri R, Fry AM (2001) APC/C-mediated destruction of the centrosomal kinase Nek2A occurs in early mitosis and depends upon a cyclin A-type D-box. EMBO J 20: 7117-7127
26. Hartwell L (1992) Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71: 543-546
27. Hayes MJ, Kimata Y, Wattam SL, Lindon C, Mao G, Yamano H, Fry AM (2006) Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nat Cell Biol 8: 607-614
28. Holland AJ, Cleveland DW (2009) Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis. Nat Rev Mol Cell Biol 10: 478-487
29. Huang HC, Shi J, Orth JD, Mitchison TJ (2009) Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly. Cancer Cell 16: 347-358
30. Hutchins JR, Moore WJ, Hood FE, Wilson JS, Andrews PD, Swedlow JR, Clarke PR (2004) Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr Biol 14: 1099-1104
31. Inoshita S, Takeda K, Hatai T, Terada Y, Sano M, Hata J, Umezawa A, Ichijo H (2002) Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J Biol Chem 277: 43730-43734
32. Janssen K, Pohlmann S, Janicke RU, Schulze-Osthoff K, Fischer U (2007) Apaf-1 and caspase-9 deficiency prevents apoptosis in a Bax-controlled pathway and promotes clono-genic survival during paclitaxel treatment. Blood 110: 3662-3672
33. Kimata Y, Baxter JE, Fry AM, Yamano H (2008) A role for the Fizzy/Cdc20 family of proteins in activation of the APC/C distinct from substrate recruitment. Mol Cell 32: 576-583
34. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics 5: 749-757
35. Kobayashi S, Lee SH, Meng XW, Mott JL, Bronk SF, Werneburg NW, Craig RW, Kaufmann SH, Gores GJ (2007) Serine 64 phosphoryla-tion enhances the antiapoptotic function of Mcl-1. J Biol Chem 282: 18407-18417
36. Kozopas KM, Yang T, Buchan HL, Zhou P, Craig RW (1993) MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci USA 90: 3516-3520
37. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, Rakic P, Flavell RA (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94: 325-337
38. Marash L, Liberman N, Henis-Korenblit S, Sivan G, Reem E, Elroy-Stein O, Kimchi A (2008) DAP5 promotes cap-independent translation of Bcl-2 and CDK1 to facilitate cell survival during mitosis. Mol Cell 30: 447-459
39. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR (2006) Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21: 749-760
40. Michels J, Johnson PW, Packham G (2005) Mcl-1. Int J Biochem Cell Biol 37: 267-271
41. Morel C, Carlson SM, White FM, Davis RJ (2009) Mcl-1 integrates the opposing actions of signaling pathways that mediate survival and apoptosis. Mol Cell Biol 29: 3845-3852
42. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393
43. Nasmyth K, Peters JM, Uhlmann F (2000) Splitting the chromosome: cutting the ties that bind sister chromatids. Science 288: 1379-1385
44. Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F, Wang X (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev 17: 1475-1486
45. Nilsson J, Yekezare M, Minshull J, Pines J (2008) The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat Cell Biol 10: 1411-1420
46. O'Connor DS, Wall NR, Porter AC, Altieri DC (2002) A p34(cdc2) survival checkpoint in cancer. Cancer Cell 2: 43-54
47. Pines J (2006) Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol 16: 55-63
48. Rieder CL, Maiato H (2004) Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell 7: 637-651
49. Scatena CD, Stewart ZA, Mays D, Tang LJ, Keefer CJ, Leach SD, Pietenpol JA (1998) Mitotic phosphorylation of Bcl-2 during normal cell cycle progression and Taxol-induced growth arrest. J Biol Chem 273: 30777-30784
50. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J, Yue P, Dornan D, Huang DC, Dixit VM (2010) Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463: 103-107
51. Shi J, Orth JD, Mitchison T (2008) Cell type variation in responses to antimitotic drugs that target microtubules and kinesin-5. Cancer Res 68: 3269-3276
52. Taylor RC, Cullen SP, Martin SJ (2008) Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9: 231-241
53. Terrano DT, Upreti M, Chambers TC (2010) Cyclin-dependent kinase 1-mediated Bcl-xL/Bcl-2 phosphorylation acts as a functional link coupling mitotic arrest and apoptosis. Mol Cell Biol 30: 640-656
54. Vodermaier HC, Gieffers C, Maurer-Stroh S, Eisenhaber F, Peters JM (2003) TPR subunits of the anaphase-promoting complex mediate binding to the activator protein CDH1. Curr Biol 13: 1459-1468
55. Wolthuis R, Clay-Farrace L, van Zon W, Yekezare M, Koop L, Ogink J, Medema R, Pines J (2008) Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol Cell 30: 290-302
56. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59
57. Yu H (2007) Cdc20: a WD40 activator for a cell cycle degradation machine. Mol Cell 27: 3-16
58. Zhong Q, Gao W, Du F, Wang X (2005) Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121: 1085-1095