APCCdc20 suppresses apoptosis through targeting Bim for ubiquitination and destruction

Developmental Cell

Volumn 29, Issue 4, 2014, Pages 377-391

  Wan, Lixin ^a   Tan, Mingjia ^b   Yang, Jie ^b,c   Inuzuka, Hiroyuki ^a   Dai, Xiangpeng ^a   Wu, Tao ^a   Liu, Jia ^a,d   Shaik, Shavali ^a   Chen, Guoan ^b   Deng, Jing ^e   Malumbres, Marcos ^f   Letai, Anthony ^e   Kirschner, Marc W ^a   Sun, Yi ^b   Wei, Wenyi ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d XI'AN JIAOTONG UNIVERSITY   (China)

^e DANA FARBER CANCER INSTITUTE   (United States)

^f Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; ANAPHASE PROMOTING COMPLEX; BH3 PROTEIN; BIM PROTEIN; CELL CYCLE PROTEIN 20; DIMETHYL SULFOXIDE; ETOPOSIDE; FLUOROURACIL; PACLITAXEL; SMALL INTERFERING RNA; TAX PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL LINE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER RESISTANCE; CELL STIMULATION; CHEMORADIOTHERAPY; CONTROLLED STUDY; FEMALE; GENE SILENCING; HCT116 CELL LINE; HEAD AND NECK CANCER; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; JURKAT CELL LINE; MITOSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REDUCTION; SENSITIZATION; T CELL LEUKEMIA; UBIQUITINATION;

ANTIMITOTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CDC20 PROTEINS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHEMORADIOTHERAPY; GENE PRODUCTS, TAX; HCT116 CELLS; HELA CELLS; HTLV-I INFECTIONS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; LEUKEMIA-LYMPHOMA, ADULT T-CELL; M PHASE CELL CYCLE CHECKPOINTS; MEMBRANE PROTEINS; MITOSIS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPINDLE APPARATUS; UBIQUITINATION;

EID: 84901433308     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.04.022     Document Type: Article

References (50)

1. Amador V., Ge S., Santamaría P.G., Guardavaccaro D., Pagano M. APC/C(Cdc20) controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol. Cell 2007, 27:462-473.
2. Begg A.C., Stewart F.A., Vens C. Strategies to improve radiotherapy with targeted drugs. Nat. Rev. Cancer 2011, 11:239-253.
3. Bouillet P., Metcalf D., Huang D.C., Tarlinton D.M., Kay T.W., Köntgen F., Adams J.M., Strasser A. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 1999, 286:1735-1738.
4. Brooks C.L., Gu W. p53 regulation by ubiquitin. FEBS Lett. 2011, 585:2803-2809.
5. Certo M., Del Gaizo Moore V., Nishino M., Wei G., Korsmeyer S., Armstrong S.A., Letai A. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell 2006, 9:351-365.
6. Chipuk J.E., Moldoveanu T., Llambi F., Parsons M.J., Green D.R. The BCL-2 family reunion. Mol. Cell 2010, 37:299-310.
7. Cragg M.S., Harris C., Strasser A., Scott C.L. Unleashing the power of inhibitors of oncogenic kinases through BH3 mimetics. Nat. Rev. Cancer 2009, 9:321-326.
8. Dehan E., Bassermann F., Guardavaccaro D., Vasiliver-Shamis G., Cohen M., Lowes K.N., Dustin M., Huang D.C., Taunton J., Pagano M. betaTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol. Cell 2009, 33:109-116.
9. Deng J., Carlson N., Takeyama K., Dal Cin P., Shipp M., Letai A. BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 and conventional chemotherapeutic agents. Cancer Cell 2007, 12:171-185.
10. Fang G., Yu H., Kirschner M.W. The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev. 1998, 12:1871-1883.
11. Gao D., Inuzuka H., Tseng A., Chin R.Y., Toker A., Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat. Cell Biol. 2009, 11:397-408.
12. Gascoigne K.E., Taylor S.S. Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 2008, 14:111-122.
13. Gavathiotis E., Suzuki M., Davis M.L., Pitter K., Bird G.H., Katz S.G., Tu H.C., Kim H., Cheng E.H., Tjandra N., Walensky L.D. BAX activation is initiated at a novel interaction site. Nature 2008, 455:1076-1081.
14. Gross A., McDonnell J.M., Korsmeyer S.J. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 1999, 13:1899-1911.
15. Hagting A., Den Elzen N., Vodermaier H.C., Waizenegger I.C., Peters J.M., Pines J. Human securin proteolysis is controlled by the spindle checkpoint and reveals when the APC/C switches from activation by Cdc20 to Cdh1. J.Cell Biol. 2002, 157:1125-1137.
16. Happo L., Cragg M.S., Phipson B., Haga J.M., Jansen E.S., Herold M.J., Dewson G., Michalak E.M., Vandenberg C.J., Smyth G.K., et al. Maximal killing of lymphoma cells by DNA damage-inducing therapy requires not only the p53 targets Puma and Noxa, but also Bim. Blood 2010, 116:5256-5267.
17. Hara H., Friedlander R.M., Gagliardini V., Ayata C., Fink K., Huang Z., Shimizu-Sasamata M., Yuan J., Moskowitz M.A. Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. Natl. Acad. Sci. USA 1997, 94:2007-2012.
18. Harper J.W., Burton J.L., Solomon M.J. The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 2002, 16:2179-2206.
19. Huang H.C., Shi J., Orth J.D., Mitchison T.J. Evidence that mitotic exit is a better cancer therapeutic target than spindle assembly. Cancer Cell 2009, 16:347-358.
20. Inuzuka H., Shaik S., Onoyama I., Gao D., Tseng A., Maser R.S., Zhai B., Wan L., Gutierrez A., Lau A.W., et al. SCF(FBW7) regulates cellular apoptosis by targeting MCL1 for ubiquitylation and destruction. Nature 2011, 471:104-109.
21. Jiang J., Jedinak A., Sliva D. Ganodermanontriol (GDNT) exerts its effect on growth and invasiveness of breast cancer cells through the down-regulation of CDC20 and uPA. Biochem. Biophys. Res. Commun. 2011, 415:325-329.
22. Jin J., Shirogane T., Xu L., Nalepa G., Qin J., Elledge S.J., Harper J.W. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 2003, 17:3062-3074.
23. Kato T., Daigo Y., Aragaki M., Ishikawa K., Sato M., Kaji M. Overexpression of CDC20 predicts poor prognosis in primary non-small cell lung cancer patients. J.Surg. Oncol. 2012, 106:423-430.
24. Kidokoro T., Tanikawa C., Furukawa Y., Katagiri T., Nakamura Y., Matsuda K. CDC20, a potential cancer therapeutic target, is negatively regulated by p53. Oncogene 2008, 27:1562-1571.
25. King R.W., Deshaies R.J., Peters J.M., Kirschner M.W. How proteolysis drives the cell cycle. Science 1996, 274:1652-1659.
26. Kuwana T., Bouchier-Hayes L., Chipuk J.E., Bonzon C., Sullivan B.A., Green D.R., Newmeyer D.D. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 2005, 17:525-535.
27. Letai A., Bassik M.C., Walensky L.D., Sorcinelli M.D., Weiler S., Korsmeyer S.J. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2002, 2:183-192.
28. Liu B., Hong S., Tang Z., Yu H., Giam C.Z. HTLV-I Tax directly binds the Cdc20-associated anaphase-promoting complex and activates it ahead of schedule. Proc. Natl. Acad. Sci. USA 2005, 102:63-68.
29. Mailand N., Diffley J.F. CDKs promote DNA replication origin licensing in human cells by protecting Cdc6 from APC/C-dependent proteolysis. Cell 2005, 122:915-926.
30. Manchado E., Guillamot M., de Cárcer G., Eguren M., Trickey M., García-Higuera I., Moreno S., Yamano H., Cañamero M., Malumbres M. Targeting mitotic exit leads to tumor regression invivo: Modulation by Cdk1, Mastl, and the PP2A/B55α,δ phosphatase. Cancer Cell 2010, 18:641-654.
31. Matsuoka M., Jeang K.T. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat. Rev. Cancer 2007, 7:270-280.
32. McDaid H.M., Lopez-Barcons L., Grossman A., Lia M., Keller S., Pérez-Soler R., Horwitz S.B. Enhancement of the therapeutic efficacy of taxol by the mitogen-activated protein kinase kinase inhibitor CI-1040 in nude mice bearing human heterotransplants. Cancer Res. 2005, 65:2854-2860.
33. Moujalled D., Weston R., Anderton H., Ninnis R., Goel P., Coley A., Huang D.C., Wu L., Strasser A., Puthalakath H. Cyclic-AMP-dependent protein kinase A regulates apoptosis by stabilizing the BH3-only protein Bim. EMBO Rep. 2011, 12:77-83.
34. Nilsson J., Yekezare M., Minshull J., Pines J. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat. Cell Biol. 2008, 10:1411-1420.
35. Reddy S.K., Rape M., Margansky W.A., Kirschner M.W. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 2007, 446:921-925.
36. Reimann J.D., Gardner B.E., Margottin-Goguet F., Jackson P.K. Emi1 regulates the anaphase-promoting complex by a different mechanism than Mad2 proteins. Genes Dev. 2001, 15:3278-3285.
37. Ren D., Tu H.C., Kim H., Wang G.X., Bean G.R., Takeuchi O., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 2010, 330:1390-1393.
38. Rufini A., Melino G. Cell death pathology: the war against cancer. Biochem. Biophys. Res. Commun. 2011, 414:445-450.
39. Searle J.S., Schollaert K.L., Wilkins B.J., Sanchez Y. The DNA damage checkpoint and PKA pathways converge on APC substrates and Cdc20 to regulate mitotic progression. Nat. Cell Biol. 2004, 6:138-145.
40. Tan T.T., Degenhardt K., Nelson D.A., Beaudoin B., Nieves-Neira W., Bouillet P., Villunger A., Adams J.M., White E. Key roles of BIM-driven apoptosis in epithelial tumors and rational chemotherapy. Cancer Cell 2005, 7:227-238.
41. Thien C.B., Dagger S.A., Steer J.H., Koentgen F., Jansen E.S., Scott C.L., Langdon W.Y. c-Cbl promotes Tcell receptor-induced thymocyte apoptosis by activating the phosphatidylinositol 3-kinase/Akt pathway. J.Biol. Chem. 2010, 285:10969-10981.
42. Wan L., Zou W., Gao D., Inuzuka H., Fukushima H., Berg A.H., Drapp R., Shaik S., Hu D., Lester C., et al. Cdh1 regulates osteoblast function through an APC/C-independent modulation of Smurf1. Mol. Cell 2011, 44:721-733.
43. Wei W., Kaelin W.G. Good COP1 or bad COP1? Invivo veritas. J.Clin. Invest. 2011, 121:1263-1265.
44. Wertz I.E., Kusam S., Lam C., Okamoto T., Sandoval W., Anderson D.J., Helgason E., Ernst J.A., Eby M., Liu J., et al. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 2011, 471:110-114.
45. Wu T., Merbl Y., Huo Y., Gallop J.L., Tzur A., Kirschner M.W. UBE2S drives elongation of K11-linked ubiquitin chains by the anaphase-promoting complex. Proc. Natl. Acad. Sci. USA 2010, 107:1355-1360.
46. Youle R.J., Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 2008, 9:47-59.
47. Yu H. Cdc20: a WD40 activator for a cell cycle degradation machine. Mol. Cell 2007, 27:3-16.
48. Zeng X., Sigoillot F., Gaur S., Choi S., Pfaff K.L., Oh D.C., Hathaway N., Dimova N., Cuny G.D., King R.W. Pharmacologic inhibition of the anaphase-promoting complex induces a spindle checkpoint-dependent mitotic arrest in the absence of spindle damage. Cancer Cell 2010, 18:382-395.
49. Zhang W., Cheng G.Z., Gong J., Hermanto U., Zong C.S., Chan J., Cheng J.Q., Wang L.H. RACK1 and CIS mediate the degradation of BimEL in cancer cells. J.Biol. Chem. 2008, 283:16416-16426.
50. Zheng M., Morgan-Lappe S.E., Yang J., Bockbrader K.M., Pamarthy D., Thomas D., Fesik S.W., Sun Y. Growth inhibition and radiosensitization of glioblastoma and lung cancer cells by small interfering RNA silencing of tumor necrosis factor receptor-associated factor 2. Cancer Res. 2008, 68:7570-7578.