APOLLON Protein promotes early Mitotic CYCLIN a degradation independent of the spindle assembly checkpoint

Journal of Biological Chemistry

Volumn 289, Issue 6, 2014, Pages 3457-3467

  Kikuchi, Ryo ^a,b   Ohata, Hirokazu ^a,c,e   Ohoka, Nobumichi ^d   Kawabata, Atsushi ^a,b   Naito, Mikihiko ^a,b,c,d  

^a Institute of Molecular and Cellular Biosciences   (United States)

^b Graduate School of Pharmaceutical Sciences   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^e NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE-PROMOTING COMPLEX/CYCLOSOME; CYCLIN A; CYCLIN-DEPENDENT KINASE; MAMMALIAN CELLS; PROTEASOMAL DEGRADATION; SPINDLE-ASSEMBLY; UBIQUITYLATION;

CELL DEATH;

PROTEINS;

APOLLON PROTEIN; CYCLIN A; CYCLIN B; UBIQUITIN CONJUGATING ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; UBIQUITINATION;

APC/C; APPOLON; CELL CYCLE; CYCLIN A; CYCLINS; MITOSIS; PROTEIN DEGRADATION; SPINDLE ASSEMBLY CHECKPOINT; UBIQUITIN;

CELL CYCLE CHECKPOINTS; CYCLIN A; CYCLIN B; HELA CELLS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; PROTEOLYSIS; SPINDLE APPARATUS; U937 CELLS;

EID: 84896723377     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.514430     Document Type: Article

References (64)

1. Nigg, E. A. (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2, 21-32
2. Malumbres, M., and Barbacid, M. (2009) Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 9, 153-166
3. Murray, A. W. (2004) Recycling the cell cycle: cyclins revisited. Cell 116, 221-234
4. Merrick, K. A., Larochelle, S., Zhang, C., Allen, J. J., Shokat, K. M., and Fisher, R. P. (2008) Distinct activation pathways confer cyclin-binding specificity on Cdk1 and Cdk2 in human cells. Mol. Cell 32, 662-672
5. Peters, J. M. (2002) The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9, 931-943
6. van Leuken, R., Clijsters, L., and Wolthuis, R. (2008) To cell cycle, swing the APC/C. Biochim. Biophys. Acta 1786, 49-59
7. Morgan, D. O. (1999) Regulation of the APC and the exit from mitosis. Nat. Cell Biol. 1, E47-53
8. Peters, J. M. (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7, 644-656
9. Pines, J. (2006) Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol. 16, 55-63
10. Glotzer, M., Murray, A. W., and Kirschner, M. W. (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138
11. Pines, J. (2011) Cubism and the cell cycle: the many faces of the APC/C. Nat. Rev. Mol. Cell Biol. 12, 427-438
12. 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
13. Sudakin, V., Ganoth, D., Dahan, A., Heller, H., Hershko, J., Luca, F. C., Ruderman, J. V., and Hershko, A. (1995) The cyclosome, a large complex containing cyclin-selective ubiquitin ligase activity, targets cyclins for destruction at the end of mitosis. Mol. Biol. Cell 6, 185-197
14. Rape, M., and Kirschner, M. W. (2004) Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 432, 588-595
15. Sigrist, S., Jacobs, H., Stratmann, R., and Lehner, C. F. (1995) Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3. EMBO J. 14, 4827-4838
16. den Elzen, N., and Pines, J. (2001) Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J. Cell Biol. 153, 121-136
17. Kraft, C., Vodermaier, H. C., Maurer-Stroh, S., Eisenhaber, F., and Peters, J. M. (2005) The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell 18, 543-553
18. Raff, J. W., Jeffers, K., and Huang, J. Y. (2002) The roles of Fzy/Cdc20 and Fzr/Cdh1 in regulating the destruction of CYCLIN B in space and time. J. Cell Biol. 157, 1139-1149
19. Zur, A., and Brandeis, M. (2002) Timing of APC/C substrate degradation is determined by fzy/fzr specificity of destruction boxes. EMBO J. 21, 4500-4510
20. Kops, G. J. (2008) The kinetochore and spindle checkpoint in mammals. Front. Biosci. 13, 3606-3620
21. Kulukian, A., Han, J. S., and Cleveland, D. W. (2009) Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell 16, 105-117
22. Sczaniecka, M. M., and Hardwick, K. G. (2008) The spindle checkpoint: how do cells delay anaphase onset? SEB Exp. Biol. Ser. 59, 243-256
23. Nilsson, J., Yekezare, M., Minshull, J., and Pines, J. (2008) The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat. Cell Biol. 10, 1411-1420
24. King, R. W., Glotzer, M., and Kirschner, M. W. (1996) Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell 7, 1343-1357
25. Klotzbücher, A., Stewart, E., Harrison, D., and Hunt, T. (1996) The 'destruction box' of Cyclin A allows B-type cyclins to be ubiquitinated, but not efficiently destroyed. EMBO J. 15, 3053-3064
26. Jacobs, H. W., Keidel, E., and Lehner, C. F. (2001) A complex degradation signal in Cyclin A required for G1 arrest, and a C-terminal region for mitosis. EMBO J. 20, 2376-2386
27. Kaspar, M., Dienemann, A., Schulze, C., and Sprenger, F. (2001) Mitotic degradation of Cyclin A is mediated by multiple and novel destruction signals. Curr. Biol. 11, 685-690
28. Fry, A. M., and Yamano, H. (2006) APC/C-mediated degradation in early mitosis: how to avoid spindle assembly checkpoint inhibition. Cell Cycle 5, 1487-1491
29. Fung, T. K., and Poon, R. Y. (2005) A roller coaster ride with the mitotic cyclins. Semin. Cell Dev. Biol. 16, 335-342
30. Di Fiore, B., and Pines, J. (2010) How cyclin A destruction escapes the spindle assembly checkpoint. J. Cell Biol. 190, 501-509
31. van Zon, W., Ogink, J., ter Riet, B., Medema, R. H., te Riele, H., and Wolthuis, R. M. (2010) The APC/C recruits CYCLIN B1-Cdk1-Cks in prometaphase before D box recognition to control mitotic exit. J. Cell Biol. 190, 587-602
32. Wolthuis, R., Clay-Farrace, L., van Zon, W., Yekezare, M., Koop, L., Ogink, J., Medema, R., and Pines, J. (2008) Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol. Cell 30, 290-302
33. Fung, T. K., Yam, C. H., and Poon, R. Y. (2005) The N-terminal regulatory domain of cyclin A contains redundant ubiquitination targeting sequences and acceptor sites. Cell Cycle 4, 1411-1420
34. Ramachandran, V., Matzkies, M., Dienemann, A., and Sprenger, F. (2007) Cyclin A degradation employs preferentially used lysines and a cyclin box function other than Cdk1 binding. Cell Cycle 6, 171-181
35. Bartke, T., Pohl, C., Pyrowolakis, G., and Jentsch, S. (2004) Dual role of BRUCE as an antiapoptotic IAP and a chimeric E2/E3 ubiquitin ligase. Mol. Cell 14, 801-811
36. Hao, Y., Sekine, K., Kawabata, A., Nakamura, H., Ishioka, T., Ohata, H., Katayama, R., Hashimoto, C., Zhang, X., Noda, T., Tsuruo, T., and Naito, M. (2004) Apollon ubiquitinates SMAC and caspase-9, and has an essential cytoprotection function. Nat. Cell Biol. 6, 849-860
37. Chen, Z., Naito, M., Hori, S., Mashima, T., Yamori, T., and Tsuruo, T. (1999) A human IAP-family gene, apollon, expressed in human brain cancer cells. Biochem. Biophys. Res. Commun. 264, 847-854
38. Hauser, H. P., Bardroff, M., Pyrowolakis, G., and Jentsch, S. (1998) A giant ubiquitin-conjugating enzyme related to IAP apoptosis inhibitors. J. Cell Biol. 141, 1415-1422
39. Sekine, K., Hao, Y., Suzuki, Y., Takahashi, R., Tsuruo, T., and Naito, M. (2005) HtrA2 cleaves Apollon and induces cell death by IAP-binding motif in Apollon-deficient cells. Biochem. Biophys. Res. Commun. 330, 279-285
40. Lotz, K., Pyrowolakis, G., and Jentsch, S. (2004) BRUCE, a giant E2/E3 ubiquitin ligase and inhibitor of apoptosis protein of the trans-Golgi network, is required for normal placenta development and mouse survival. Mol. Cell. Biol. 24, 9339-9350
41. Naito, M., Katayama, R., Ishioka, T., Suga, A., Takubo, K., Nanjo, M., Hashimoto, C., Taira, M., Takada, S., Takada, R., Kitagawa, M., Matsuzawa, S., Reed, J. C., and Tsuruo, T. (2004) Cellular FLIP inhibits-catenin ubiquitylation and enhances Wnt signaling. Mol. Cell. Biol. 24, 8418-8427
42. Ishioka, T., Katayama, R., Kikuchi, R., Nishimoto, M., Takada, S., Takada, R., Matsuzawa, S., Reed, J. C., Tsuruo, T., and Naito, M. (2007) Impairment of the ubiquitin-proteasome system by cellular FLIP. Genes Cells 12, 735-744
43. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstrale, K., Leuchowius, K. J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000
44. Jeffrey, P. D., Russo, A. A., Polyak, K., Gibbs, E., Hurwitz, J., Massagué, J., and Pavletich, N. P. (1995) Mechanism of CDK activation revealed by the structure of a cyclinA-CDK2 complex. Nature 376, 313-320
45. 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. U.S.A. 103, 10660-10665
46. King, R. W., Peters, J. M., Tugendreich, S., Rolfe, M., Hieter, P., and Kirschner, M. W. (1995) A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81, 279-288
47. Thornton, B. R., and Toczyski, D. P. (2006) Precise destruction: an emerging picture of the APC. Genes Dev. 20, 3069-3078
48. Fang, G., Yu, H., and Kirschner, M. W. (1998) Direct binding of CDC20 protein family members activates the anaphase-promoting complex in mitosis and G1. Mol. Cell 2, 163-171
49. Yu, H. (2007) Cdc20: a WD40 activator for a cell cycle degradation machine. Mol. Cell 27, 3-16
50. Zachariae, W., Schwab, M., Nasmyth, K., and Seufert, W. (1998) Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 282, 1721-1724
51. Bharadwaj, R., and Yu, H. (2004) The spindle checkpoint, aneuploidy, and cancer. Oncogene 23, 2016-2027
52. Fang, G., Yu, H., and Kirschner, M. W. (1998) The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev. 12, 1871-1883
53. Sudakin, V., Chan, G. K., and Yen, T. J. (2001) Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J. Cell Biol. 154, 925-936
54. Tang, Z., Bharadwaj, R., Li, B., and Yu, H. (2001) Mad2-Independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev. Cell 1, 227-237
55. Tang, Z., Shu, H., Oncel, D., Chen, S., and Yu, H. (2004) Phosphorylation of Cdc20 by Bub1 provides a catalytic mechanism for APC/C inhibition by the spindle checkpoint. Mol. Cell 16, 387-397
56. Vanoosthuyse, V., and Hardwick, K. G. (2005) Bub1 and the multilayered inhibition of Cdc20-APC/C in mitosis. Trends Cell Biol. 15, 231-233
57. Hames, R. S., Wattam, S. L., Yamano, H., Bacchieri, R., and Fry, A. M. (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
58. Hayes, M. J., Kimata, Y., Wattam, S. L., Lindon, C., Mao, G., Yamano, H., and Fry, A. M. (2006) Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nat. Cell Biol. 8, 607-614
59. Sedgwick, G. G., Hayward, D. G., Di Fiore, B., Pardo, M., Yu, L., Pines, J., and Nilsson, J. (2013) Mechanisms controlling the temporal degradation of Nek2A and Kif18A by the APC/C-Cdc20 complex. EMBO J. 32, 303-314
60. Ren, J., Shi, M., Liu, R., Yang, Q. H., Johnson, T., Skarnes, W. C., and Du, C. (2005) The Birc6 (Bruce) gene regulates p53 and the mitochondrial pathway of apoptosis and is essential for mouse embryonic development. Proc. Natl. Acad. Sci. U.S.A. 102, 565-570
61. Hitz, C., Vogt-Weisenhorn, D., Ruiz, P., Wurst, W., and Floss, T. (2005) Progressive loss of the spongiotrophoblast layer of Birc6/Bruce mutants results in embryonic lethality. Genesis 42, 91-103
62. Arama, E., Agapite, J., and Steller, H. (2003) Caspase activity and a specific cytochrome c are required for sperm differentiation in Drosophila. Dev. Cell 4, 687-697
63. Vernooy, S. Y., Chow, V., Su, J., Verbrugghe, K., Yang, J., Cole, S., Olson, M. R., and Hay, B. A. (2002) Drosophila Bruce can potently suppress Rprand Grim-dependent but not Hid-dependent cell death. Curr. Biol. 12, 1164-1168
64. Pohl, C., and Jentsch, S. (2008) Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 132, 832-845