The novel protective role of P27 in MLN4924-treated gastric cancer cells

Cell Death and Disease

Volumn 6, Issue 8, 2015, Pages

  Zhang, Q ^a,b   Hou, D ^b   Luo, Z ^a   Chen, P ^b   Lv, B ^a   Wu, L ^a   Ma, Y ^a   Chu, Y ^c   Liu, H ^d   Liu, F ^d   Yu, S ^b   Zhang, J ^a   Yang, D ^a   Liu, J ^a,c  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

^d SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; BH3 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYTOCHROME; PEVONEDISTAT; REACTIVE OXYGEN METABOLITE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; ((1S,2S,4R)-4-(4-((1S)-2,3-DIHYDRO-1H-INDEN-1-YLAMINO)-7H-PYRROLO(2,3-D)PYRIMIDIN-7-YL)-2-HYDROXYCYCLOPENTYL)METHYL SULPHAMATE; AIFM1 PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; ANTIOXIDANT; CULLIN; CULLIN 1; CYCLOPENTANE DERIVATIVE; CYTOCHROME C; DIABLO PROTEIN, HUMAN; F BOX PROTEIN; MITOCHONDRIAL PROTEIN; PYRIMIDINE DERIVATIVE; S PHASE KINASE ASSOCIATED PROTEIN; SIGNAL PEPTIDE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG EFFICACY; EMBRYO; G2 PHASE CELL CYCLE CHECKPOINT; GASTRIC CANCER CELL LINE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; ZEBRA FISH; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NONMAMMALIAN EMBRYO; PATHOLOGY; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; APOPTOSIS INDUCING FACTOR; CELL LINE, TUMOR; CULLIN PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLOPENTANES; CYTOCHROMES C; EMBRYO, NONMAMMALIAN; F-BOX PROTEINS; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MITOCHONDRIAL PROTEINS; PYRIMIDINES; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; S-PHASE KINASE-ASSOCIATED PROTEINS; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS; ZEBRAFISH;

EID: 84989328296     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.215     Document Type: Article

References (51)

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M et al. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015; 136: E359-E386.
2. Masuda TA, Inoue H, Sonoda H, Mine S, Yoshikawa Y, Nakayama K et al. Clinical and biological significance of S-phase kinase-associated protein 2 (Skp2) gene expression in gastric carcinoma: Modulation of malignant phenotype by Skp2 overexpression, possibly via p27 proteolysis. Cancer Res 2002; 62: 3819-3825.
3. Bai J, Zhou Y, Chen G, Zeng J, Ding J, Tan Y et al. Overexpression of Cullin1 is associated with poor prognosis of patients with gastric cancer. Hum Pathol 2011; 42: 375-383.
4. Wei Z, Jiang X, Liu F, Qiao H, Zhou B, Zhai B et al. Downregulation of Skp2 inhibits the growth and metastasis of gastric cancer cells in vitro and in vivo. Tumour Biol 2013; 34: 181-192.
5. Soucy TA, Smith PG, Milhollen MA, Berger AJ, Gavin JM, Adhikari S et al. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 2009; 458: U732-U67.
6. Tsvetkov LM, Yeh KH, Lee SJ, Sun H, Zhang H. p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr Biol 1999; 9: 661-664.
7. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1999; 1: 193-199.
8. Morimoto M, Nishida T, Honda R, Yasuda H. Modification of cullin-1 by ubiquitin-like protein Nedd8 enhances the activity of SCF(skp2) toward p27(kip1). Biochem Biophys Res Commun 2000; 270: 1093-1096.
9. Polyak K, Lee MH, Erdjument-Bromage H, Koff A, Roberts JM, Tempst P et al. Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 1994; 78: 59-66.
10. Besson A, Dowdy SF, Roberts JM. CDK inhibitors: Cell cycle regulators and beyond. Dev Cell 2008; 14: 159-169.
11. Ladha MH, Lee KY, Upton TM, Reed MF, Ewen ME. Regulation of exit from quiescence by p27 and cyclin D1-CDK4. Mol Cell Biol 1998; 18: 6605-6615.
12. Ray A, James MK, Larochelle S, Fisher RP, Blain SW. p27Kip1 inhibits cyclin D-cyclindependent kinase 4 by two independent modes. Mol Cell Biol 2009; 29: 986-999.
13. Kwon TK, Nordin AA. Identification of cdk2 binding sites on the p27Kip1 cyclin-dependent kinase inhibitor. Oncogene 1998; 16: 755-762.
14. Teixeira LT, Kiyokawa H, Peng XD, Christov KT, Frohman LA, Kineman RD. p27Kip1- deficient mice exhibit accelerated growth hormone-releasing hormone (GHRH)-induced somatotrope proliferation and adenoma formation. Oncogene 2000; 19: 1875-1884.
15. Fero ML, Randel E, Gurley KE, Roberts JM, Kemp CJ. The murine gene p27Kip1 is haploinsufficient for tumour suppression. Nature 1998; 396: 177-180.
16. Philipp-Staheli J, Payne SR, Kemp CJ. p27(Kip1): Regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp Cell Res 2001; 264: 148-168.
17. Di Cristofano A, De Acetis M, Koff A, Cordon-Cardo C, Pandolfi PP. Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat Genet 2001; 27: 222-224.
18. Nohara T, Ryo T, Iwamoto S, Gon G, Tanigawa N. Expression of cell-cycle regulator p27 is correlated to the prognosis and ER expression in breast carcinoma patients. Oncology 2001; 60: 94-100.
19. Ogino S, Shima K, Nosho K, Irahara N, Baba Y, Wolpin BM et al. A cohort study of p27 localization in colon cancer, body mass index, and patient survival. Cancer Epidemiol Biomarkers Prev 2009; 18: 1849-1858.
20. Zhuang Y, Yin HT, Yin XL, Wang J, Zhang DP. High p27 expression is associated with a better prognosis in East Asian non-small cell lung cancer patients. Clin Chim Acta 2011; 412: 2228-2231.
21. Chetty R. University Health Network PMHUAFFSTONMGMCrcuoc p27 Protein and cancers of the gastrointestinal tract and liver: An overview. J Clin Gastroenterol 2003; 37: 23-27.
22. Aoyagi K, Kouhuji K, Miyagi M, Imaizumi T, Kizaki J, Isobe T et al. Expression of p27Kip1 protein in gastric carcinoma. Hepato-gastroenterology 2013; 60: 390-394.
23. Wiksten JP, Lundin J, Nordling S, Kokkola A, von Boguslawski K, Haglund C. The prognostic value of p27 in gastric cancer. Oncology 2002; 63: 180-184.
24. So JB, Samarasinge K, Raju GC, Moochhala SM, Ti TK. Expression of cell-cycle regulators p27 and cyclin E correlates with survival in gastric carcinoma patients. J Surg Res 2000; 94: 56-60.
25. Feakins RM, Mulcahy HE, Quaglia A, Jawhari A, Zhang Z, Patchett SE. p27(Kip1) loss does not predict survival in patients with advanced gastric carcinoma. Cancer 2000; 89: 1684-1691.
26. Philipp-Staheli J, Kim KH, Liggitt D, Gurley KE, Longton G, Kemp CJ. Distinct roles for p53, p27Kip1, and p21Cip1 during tumor development. Oncogene 2004; 23: 905-913.
27. Luo Z, Yu G, Lee HW, Li L, Wang L, Yang D et al. The Nedd8-activating enzyme inhibitor MLN4924 induces autophagy and apoptosis to suppress liver cancer cell growth. Cancer Res 2012; 72: 3360-3371.
28. Godbersen JC, Humphries LA, Danilova OV, Kebbekus PE, Brown JR, Eastman A et al. The Nedd8-activating enzyme inhibitor MLN4924 thwarts microenvironment-driven NF-kappaB activation and induces apoptosis in chronic lymphocytic leukemia B cells. Clin Cancer Res 2014; 20: 1576-1589.
29. Nicoli S, Presta M. The zebrafish/tumor xenograft angiogenesis assay. Nat Protoc 2007; 2: 2918-2923.
30. Tan DSW, Haaland B, Gan JM, Tham SC, Sinha I, Tan EH et al. Bosutinib inhibits migration and invasion via ack1 in kras mutant non-small cell lung cancer. Mol Cancer 2014; 13: 13.
31. White R, Rose K, Zon L. Zebrafish cancer: The state of the art and the path forward. Nat Rev Cancer 2013; 13: 624-636.
32. Tobia C, Gariano G, De Sena G, Presta M. Zebrafish embryo as a tool to study tumor/ endothelial cell cross-talk. Biochim Biophys Acta 2013; 1832: 1371-1377.
33. Liu S, Leach SD. Zebrafish models for cancer. Annu Rev Pathol 2011; 6: 71-93.
34. Yee C, Yang W, Hekimi S. The intrinsic apoptosis pathway mediates the pro-longevity response to mitochondrial ROS in C. elegans. Cell 2014; 157: 897-909.
35. Du C, Fang M, Li Y, Li L, Wang X. Smac a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102: 33-42.
36. Kim JY, Kim YJ, Seok KO, Lee S, Park JH. Caspase-9-dependent nuclear translocation of cytochrome c in hypoxic injury. Pathobiology 2010; 77: 320-327.
37. Gao CF, Ren S, Zhang L, Nakajima T, Ichinose S, Hara T et al. Caspase-dependent cytosolic release of cytochrome c and membrane translocation of Bax in p53-induced apoptosis. Exp Cell Res 2001; 265: 145-151.
38. Dejean LM, Martinez-Caballero S, Kinnally KW. Is MAC the knife that cuts cytochrome c from mitochondria during apoptosis? Cell Death Differ 2006; 13: 1387-1395.
39. Deng X, Gao F, May Jr. WS Bcl2 retards G1/S cell cycle transition by regulating intracellular ROS. Blood 2003; 102: 3179-3185.
40. Cao X, Deng X, May WS. Cleavage of Bax to p18 Bax accelerates stress-induced apoptosis, and a cathepsin-like protease may rapidly degrade p18 Bax. Blood 2003; 102: 2605-2614.
41. Cao XH, Zhao SS, Liu DY, Wang Z, Niu LL, Hou LH et al. ROS-Ca(2+) is associated with mitochondria permeability transition pore involved in surfactin-induced MCF-7 cells apoptosis. Chem Biol Interact 2011; 190: 16-27.
42. Wood DE, Thomas A, Devi LA, Berman Y, Beavis RC, Reed JC et al. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 1998; 17: 1069-1078.
43. Toyota H, Yanase N, Yoshimoto T, Moriyama M, Sudo T, Mizuguchi J. Calpain-induced Baxcleavage product is a more potent inducer of apoptotic cell death than wild-type Bax. Cancer Lett 2003; 189: 221-230.
44. Patel YM, Lane MD. Mitotic clonal expansion during preadipocyte differentiation: Calpainmediated turnover of p27. J Biol Chem 2000; 275: 17653-17660.
45. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med 2002; 8: 1153-1160.
46. Shin I, Yakes FM, Rojo F, Shin NY, Bakin AV, Baselga J et al. PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat Med 2002; 8: 1145-1152.
47. Sekimoto T, Fukumoto M, Yoneda Y. 14-3-3 suppresses the nuclear localization of threonine 157-phosphorylated p27(Kip1). EMBO J 2004; 23: 1934-1942.
48. Serres MP, Zlotek-Zlotkiewicz E, Concha C, Gurian-West M, Daburon V, Roberts JM et al. Cytoplasmic p27 is oncogenic and cooperates with Ras both in vivo and in vitro. Oncogene 2011; 30: 2846-2858.
49. Drexler HC, Pebler S. Inducible p27(Kip1) expression inhibits proliferation of K562 cells and protects against apoptosis induction by proteasome inhibitors. Cell Death Differ 2003; 10: 290-301.
50. Achenbach TV, Slater EP, Brummerhop H, Bach T, Muller R. Inhibition of cyclin-dependent kinase activity and induction of apoptosis by preussin in human tumor cells. Antimicrob Agents Chemother 2000; 44: 2794-2801.
51. Delmore JE, Issa GC, Lemieux ME, Rahl PB, Shi J, Jacobs HM et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011; 146: 904-917.