The E3 ubiquitin ligases β-TrCP and FBXW7 cooperatively mediates GSK3-dependent Mcl-1 degradation induced by the Akt inhibitor API-1, resulting in apoptosis

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Ren, Hui ^a,b   Koo, Junghui ^b   Guan, Baoxiang ^b   Yue, Ping ^b   Deng, Xingming ^b   Chen, Mingwei ^a   Khuri, Fadlo R ^b   Sun, Shi Yong ^b  

^a THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

API 1; Apoptosis; E3 ubiquitin ligase; GSK3; Lung cancer; Mcl 1

Indexed keywords

API 1; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BETA TRCP PROTEIN; CASPASE 3; CASPASE 8; CASPASE 9; FBXW7 PROTEIN; GLYCOGEN SYNTHASE KINASE 3; PROTEASOME; PROTEIN KINASE B INHIBITOR; PROTEIN MCL 1; SURVIVIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL ASSAY; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

APOPTOSIS; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE PROTEINS; CELL LINE, TUMOR; F-BOX PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GLYCOGEN SYNTHASE KINASE 3; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; LEUPEPTINS; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NUCLEOSIDES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-AKT; UBIQUITIN-PROTEIN LIGASES;

EID: 84887881695     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-146     Document Type: Article

References (28)

1. Kim D, Sun M, He L, Zhou QH, Chen J, Sun XM, Bepler G, Sebti SM, Cheng JQ. A small molecule inhibits Akt through direct binding to Akt and preventing Akt membrane translocation. J Biol Chem 2010, 285:8383-8394. 10.1074/jbc.M109.094060, 2832988, 20068047.
2. Li B, Ren H, Yue P, Chen M, Khuri FR, Sun SY. The novel Akt inhibitor API-1 induces c-FLIP degradation and synergizes with TRAIL to augment apoptosis independent of Akt inhibition. Cancer Prev Res (Phila) 2012, 5:612-620. 10.1158/1940-6207.CAPR-11-0548, 3324640, 22345097.
3. Hengartner MO. The biochemistry of apoptosis. Nature 2000, 407:770-776. 10.1038/35037710, 11048727.
4. Shirley S, Micheau O. Targeting c-FLIP in cancer. Cancer Lett 2013, 332:141-150. 10.1016/j.canlet.2010.10.009, 21071136.
5. Chan SL, Yu VC. Proteins of the bcl-2 family in apoptosis signalling: from mechanistic insights to therapeutic opportunities. Clin Exp Pharmacol Physiol 2004, 31:119-128. 10.1111/j.1440-1681.2004.03975.x, 15008953.
6. Zhang L, Fang B. Mechanisms of resistance to TRAIL-induced apoptosis in cancer. Cancer Gene Ther 2005, 12:228-237. 10.1038/sj.cgt.7700792, 15550937.
7. Thomas LW, Lam C, Edwards SW. Mcl-1; the molecular regulation of protein function. FEBS Lett 2010, 584:2981-2989. 10.1016/j.febslet.2010.05.061, 20540941.
8. Ding Q, He X, Hsu JM, Xia W, Chen CT, Li LY, Lee DF, Liu JC, Zhong Q, Wang X, Hung MC. Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 2007, 27:4006-4017. 10.1128/MCB.00620-06, 1900029, 17387146.
9. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 2006, 21:749-760. 10.1016/j.molcel.2006.02.009, 16543145.
10. Wertz IE, Kusam S, Lam C, Okamoto T, Sandoval W, Anderson DJ, Helgason E, Ernst JA, Eby M, Liu J, Belmont LD, Kaminker JS, O'Rourke KM, Pujara K, Kohli PB, Johnson AR, Chiu ML, Lill JR, Jackson PK, Fairbrother WJ, Seshagiri S, Ludlam MJ, Leong KG, Dueber EC, Maecker H, Huang DC, Dixit VM. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 2011, 471:110-114. 10.1038/nature09779, 21368834.
11. Inuzuka H, Shaik S, Onoyama I, Gao D, Tseng A, Maser RS, Zhai B, Wan L, Gutierrez A, Lau AW, Xiao Y, Christie AL, Aster J, Settleman J, Gygi SP, Kung AL, Look T, Nakayama KI, DePinho RA, Wei W. SCF(FBW7) regulates cellular apoptosis by targeting MCL1 for ubiquitylation and destruction. Nature 2011, 471:104-109. 10.1038/nature09732, 3076007, 21368833.
12. Ren H, Chen M, Yue P, Tao H, Owonikoko TK, Ramalingam SS, Khuri FR, Sun SY. The combination of RAD001 and NVP-BKM120 synergistically inhibits the growth of lung cancer in vitro and in vivo. Cancer Lett 2012, 325:139-146. 10.1016/j.canlet.2012.06.018, 22781393.
13. Ren H, Zhao L, Li Y, Yue P, Deng X, Owonikoko TK, Chen M, Khuri FR, Sun SY. The PI3 kinase inhibitor NVP-BKM120 induces GSK3/FBXW7-dependent Mcl-1 degradation, contributing to induction of apoptosis and enhancement of TRAIL-induced apoptosis. Cancer Lett 2013, 338:229-238. 10.1016/j.canlet.2013.03.032, 23562472.
14. Lin Y, Liu X, Yue P, Benbrook DM, Berlin KD, Khuri FR, Sun SY. Involvement of c-FLIP and survivin down-regulation in flexible heteroarotinoid-induced apoptosis and enhancement of TRAIL-initiated apoptosis in lung cancer cells. Mol Cancer Ther 2008, 7:3556-3565. 10.1158/1535-7163.MCT-08-0648, 19001438.
15. Sun SY, Yue P, Dawson MI, Shroot B, Michel S, Lamph WW, Heyman RA, Teng M, Chandraratna RA, Shudo K, Hong WK, Lotan R. Differential effects of synthetic nuclear retinoid receptor-selective retinoids on the growth of human non-small cell lung carcinoma cells. Cancer Res 1997, 57:4931-4939.
16. Liu X, Yue P, Zhou Z, Khuri FR, Sun SY. Death receptor regulation and celecoxib-induced apoptosis in human lung cancer cells. J Natl Cancer Inst 2004, 96:1769-1780. 10.1093/jnci/djh322, 15572759.
17. Sun SY, Yue P, Wu GS, El-Deiry WS, Shroot B, Hong WK, Lotan R. Mechanisms of apoptosis induced by the synthetic retinoid CD437 in human non-small cell lung carcinoma cells. Oncogene 1999, 18:2357-2365. 10.1038/sj.onc.1202543, 10327056.
18. Mao JH, Perez-Losada J, Wu D, Delrosario R, Tsunematsu R, Nakayama KI, Brown K, Bryson S, Balmain A. Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene. Nature 2004, 432:775-779. 10.1038/nature03155, 15592418.
19. Yang W, Xia Y, Ji H, Zheng Y, Liang J, Huang W, Gao X, Aldape K, Lu Z. Nuclear PKM2 regulates beta-catenin transactivation upon EGFR activation. Nature 2011, 480:118-122. 3235705, 22056988.
20. Yokobori T, Mimori K, Iwatsuki M, Ishii H, Tanaka F, Sato T, Toh H, Sudo T, Iwaya T, Tanaka Y, Onoyama I, Kuwano H, Nakayama KI, Mori M. Copy number loss of FBXW7 is related to gene expression and poor prognosis in esophageal squamous cell carcinoma. Int J Oncol 2012, 41:253-259.
21. Liu Z, Liu M, Niu G, Cheng Y, Fei J. Genome-wide identification of target genes repressed by the zinc finger transcription factor REST/NRSF in the HEK 293 cell line. Acta Biochim Biophys Sin (Shanghai) 2009, 41:1008-1017. 10.1093/abbs/gmp095, 20011975.
22. Li R, Hu Z, Sun SY, Chen ZG, Owonikoko TK, Sica GL, Ramalingam SS, Curran WJ, Khuri FR, Deng X. Niclosamide Overcomes Acquired Resistance to Erlotinib through Suppression of STAT3 in Non-Small Cell Lung Cancer. Mol Cancer Ther 2013, 12:2200-2212. 10.1158/1535-7163.MCT-13-0095, 23894143.
23. Inuzuka H, Fukushima H, Shaik S, Liu P, Lau AW, Wei W. Mcl-1 ubiquitination and destruction. Oncotarget 2011, 2:239-244. 3260810, 21608150.
24. Warr MR, Shore GC. Unique biology of Mcl-1: therapeutic opportunities in cancer. Curr Mol Med 2008, 8:138-147. 10.2174/156652408783769580, 18336294.
25. Jia L, Sun Y. SCF E3 ubiquitin ligases as anticancer targets. Curr Cancer Drug Targets 2011, 11:347-356. 10.2174/156800911794519734, 3323109, 21247385.
26. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer 2003, 3:46-54. 10.1038/nrc968, 12509766.
27. Viswanath V, Wu Y, Boonplueang R, Chen S, Stevenson FF, Yantiri F, Yang L, Beal MF, Andersen JK. Caspase-9 activation results in downstream caspase-8 activation and bid cleavage in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson's disease. J Neurosci 2001, 21:9519-9528.
28. Ferreira KS, Kreutz C, Macnelly S, Neubert K, Haber A, Bogyo M, Timmer J, Borner C. Caspase-3 feeds back on caspase-8, Bid and XIAP in type I Fas signaling in primary mouse hepatocytes. Apoptosis 2012, 17:503-515. 10.1007/s10495-011-0691-0, 22246639.