PTEN regulates colorectal epithelial apoptosis through Cdc42 signalling

British Journal of Cancer

Volumn 105, Issue 9, 2011, Pages 1313-1321

  Deevi, R ^a   Fatehullah, A ^a   Jagan, I ^a   Nagaraju, M ^a   Bingham, V ^a   Campbell, F C ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

apoptosis; Cdc42; GSK3 ; PARP; PTEN

Indexed keywords

ANTINEOPLASTIC AGENT; BUTYRIC ACID; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CHLORIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN CDC42; RETROVIRUS VECTOR; SHORT HAIRPIN RNA; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; EPITHELIUM CELL; FLOW CYTOMETRY; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; UPREGULATION;

APOPTOSIS; CACO-2 CELLS; CELL CYCLE PROTEINS; GENE KNOCKOUT TECHNIQUES; HCT116 CELLS; HUMANS; POLY(ADP-RIBOSE) POLYMERASES; PTEN PHOSPHOHYDROLASE; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 80055008724     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2011.384     Document Type: Article

References (69)

1. Al-Khouri AM, Ma Y, Togo SH, Williams S, Mustelin T (2005) Cooperative phosphorylation of the tumor suppressor phosphatase and tensin homologue (PTEN) by casein kinases and glycogen synthase kinase 3beta. J Biol Chem 280(42): 35195-35202 (Pubitemid 41532706)
2. Argiris A, Cohen E, Karrison T, Esparaz B, Mauer A, Ansari R, Wong S, Lu Y, Pins M, Dancey J, Vokes E (2006) A phase II trial of perifosine, an oral alkylphospholipid, in recurrent or metastatic head and neck cancer. Cancer Biology Ther 5(7): 766-770 (Pubitemid 44775131)
3. Bai Z, Zhang Z, Ye Y, Wang S (2010) Sodium butyrate induces differentiation of gastric cancer cells to intestinal cells via the PTEN/phosphoinositide 3-kinase pathway. Cell Biol Int 34(12): 1141-1145
4. Bailey HH, Mahoney MR, Ettinger DS, Maples WJ, Fracasso PM, Traynor AM, Erlichman C, Okuno SH (2006) Phase II study of daily oral perifosine in patients with advanced soft tissue sarcoma. Cancer 107(10): 2462-2467 (Pubitemid 44748530)
5. Beurel E, Jope RS (2006) The paradoxical pro-and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signalling pathways. Prog Neurobiol 79(4): 173-189 (Pubitemid 44331500)
6. Biggs 3rd WH, Meisenhelder J, Hunter T, Cavenee WK, Arden KC (1999) Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci USA 96(13): 7421-7426 (Pubitemid 29299677)
7. Boehm JS, Hession MT, Bulmer SE, Hahn WC (2005) Transformation of human and murine fibroblasts without viral oncoproteins. Mol Cell Biol 25(15): 6464-6474 (Pubitemid 41023222)
8. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282(5392): 1318-1321 (Pubitemid 28524494)
9. Cau J, Hall A (2005) Cdc42 controls the polarity of the actin and microtubule cytoskeletons through two distinct signal transduction pathways. J Cell Sci 118(Pt 12): 2579-2587 (Pubitemid 40932884)
10. Cerione RA (2004) Cdc42: new roads to travel. Trends Cell Biol 14(3): 127-132 (Pubitemid 38293455)
11. Chee KG, Longmate J, Quinn DI, Chatta G, Pinski J, Twardowski P, Pan CX, Cambio A, Evans CP, Gandara DR, Lara Jr PN (2007) The AKT inhibitor perifosine in biochemically recurrent prostate cancer: a phase II California/Pittsburgh cancer consortium trial. Clin Genitourin ancer 5(7): 433-437 (Pubitemid 351219696)
12. Cheng TL, Symons M, Jou TS (2004) Regulation of anoikis by Cdc42 and Rac1. Exp Cell Res 295(2): 497-511 (Pubitemid 38490502)
13. Chuang TH, Hahn KM, Lee JD, Danley DE, Bokoch GM (1997) The small GTPase Cdc42 initiates an apoptotic signalling pathway in Jurkat T lymphocytes. Mol Biol Cell 8(9): 1687-1698 (Pubitemid 27411134)
14. Collett GP, Campbell FC (2006) Overexpression of p65/RelA potentiates curcumin-induced apoptosis in HCT116 human colon cancer cells. Carcinogenesis 27(6): 1285-1291 (Pubitemid 43985444)
15. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378(6559): 785-789 (Pubitemid 26004411)
16. Database-Wellcome Trust Sanger Cancer cell line project (2011) www.sanger.ac.uk/genetics/CGP/CellLines/
17. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91(2): 231-241 (Pubitemid 27456390)
18. De Sarno P, Li X, Jope RS (2002) Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 43(7): 1158-1164 (Pubitemid 36009369)
19. Dihlmann S, Klein S, Doeberitz Mv MK (2003) Reduction of beta-catenin/T-cell transcription factor signaling by aspirin and indomethacin is caused by an increased stabilization of phosphorylated beta-catenin. Mol Cancer Ther 2(6): 509-516
20. Doble BW, Woodgett JR (2003) GSK-3: tricks of the trade for a multitasking kinase. J Cell Sci 116(Pt 7): 1175-1186 (Pubitemid 36410657)
21. El-Tanani M, Platt-Higgins A, Rudland PS, Campbell FC (2004) Ets gene PEA3 cooperates with beta-catenin-Lef-1 and c-Jun in regulation of osteopontin transcription. J Biol Chem 279(20): 20794-20806 (Pubitemid 38656476)
22. Ericson K, Gan C, Cheong I, Rago C, Samuels Y, Velculescu VE, Kinzler KW, Huso DL, Vogelstein B, Papadopoulos N (2010) Genetic inactivation of AKT1, AKT2, and PDPK1 in human colorectal cancer cells clarifies their roles in tumor growth regulation. Proc Natl Acad Sci USA 107(6): 2598-2603
23. Etienne-Manneville S (2004) Cdc42-the centre of polarity. J Cell Sci 117(Pt 8): 1291-1300
24. Etienne-Manneville S, Hall A (2003) Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421(6924): 753-756 (Pubitemid 36227627)
25. Feig LA (1999) Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat Cell Biol 1(2): E25-E27
26. Frame S, Cohen P (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359(Pt 1): 1-16 (Pubitemid 32939202)
27. Gaschott T, Stein J (2003) Short-chain fatty acids and colon cancer cells: the vitamin D receptor-butyrate connection. Recent Results Cancer Res 164: 247-257
28. Geng D, Zheng L, Srivastava R, Velasco-Gonzalez C, Riker A, Markovic SN, Davila E (2010) Amplifying TLR-MyD88 signals within tumor-specific T cells enhances antitumor activity to suboptimal levels of weakly immunogenic tumor antigens. Cancer Res 70(19): 7442-7454
29. Gilbert T, Le Bivic A, Quaroni A, Rodriguez-Boulan E (1991) Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco2 intestinal epithelial cells. J Cell Biol 113(2): 275-288 (Pubitemid 21909692)
30. Gills JJ, Dennis PA (2009) Perifosine: update on a novel Akt inhibitor. Curr Oncol Rep 11(2): 102-110
31. Hague A, Paraskeva C (1995) The short-chain fatty acid butyrate induces apoptosis in colorectal tumour cell lines. Eur J Cancer Prev 4(5): 359-364
32. Hao H, Muniz-Medina VM, Mehta H, Thomas NE, Khazak V, Der CJ, Shields JM (2007) Context-dependent roles of mutant B-Raf signaling in melanoma and colorectal carcinoma cell growth. Mol Cancer Ther 6(8): 2220-2229 (Pubitemid 47294750)
33. Higuchi M, Masuyama N, Fukui Y, Suzuki A, Gotoh Y (2001) Akt mediates Rac/Cdc42-regulated cell motility in growth factor-stimulated cells and in invasive PTEN knockout cells. Curr Biol 11(24): 1958-1962 (Pubitemid 33146422)
34. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, Woodgett JR (2000) Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406(6791): 86-90 (Pubitemid 30460216)
35. Ilyas M, Tomlinson IP, Rowan A, Pignatelli M, Bodmer WF (1997) Beta-catenin mutations in cell lines established from human colorectal cancers. Proc Natl Acad Sci USA 94(19): 10330-10334 (Pubitemid 27407041)
36. Johnson DI (1999) Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol Mol Biol Rev 63(1): 54-105 (Pubitemid 29116087)
37. Jope RS, Johnson GV (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29(2): 95-102 (Pubitemid 38186580)
38. Kim M, Datta A, Brakeman P, Yu W, Mostov KE (2007) Polarity proteins PAR6 and aPKC regulate cell death through GSK-3beta in 3D epithelial morphogenesis. J Cell Sci 120(Pt 14): 2309-2317 (Pubitemid 47225934)
39. Koch S, Capaldo CT, Samarin S, Nava P, Neumaier I, Skerra A, Sacks DB, Parkos CA, Nusrat A (2009) Dkk-1 inhibits intestinal epithelial cell migration by attenuating directional polarization of leading edge cells. Mol Biol Cell 20(22): 4816-4825
40. Kolsch V, Charest PG, Firtel RA (2008) The regulation of cell motility and chemotaxis by phospholipid signalling. J Cell Sci 121(Pt 5): 551-559 (Pubitemid 351524153)
41. Koseoglu S, Lu Z, Kumar C, Kirschmeier P, Zou J (2007) AKT1, AKT2 and AKT3-dependent cell survival is cell line-specific and knockdown of all three isoforms selectively induces apoptosis in 20 human tumor cell lines. Cancer Biol Therapy 6(5): 755-762 (Pubitemid 47328358)
42. Langlois MJ, Bergeron S, Bernatchez G, Boudreau F, Saucier C, Perreault N, Carrier JC, Rivard N (2010) The PTEN phosphatase controls intestinal epithelial cell polarity and barrier function: role in colorectal cancer progression. PLoS One 5(12): e15742
43. Lawson KR, Ignatenko NA, Piazza GA, Cui H, Gerner EW (2000) Influence of K-ras activation on the survival responses of Caco-2 cells to the chemopreventive agents sulindac and difluoromethylornithine. Cancer Epidemiol Biomarkers Prev 9(11): 1155-1162
44. Lee C, Kim JS, Waldman T (2004) PTEN gene targeting reveals a radiation-induced size checkpoint in human cancer cells. Cancer Res 64(19): 6906-6914 (Pubitemid 39330998)
45. Lee SH, Poulogiannis G, Pyne S, Jia S, Zou L, Signoretti S, Loda M, Cantley LC, Roberts TM (2010) A constitutively activated form of the p110beta isoform of PI3-kinase induces prostatic intraepithelial neoplasia in mice. Proc Natl Acad Sci USA 107(24): 11002-11007
46. Liliental J, Moon SY, Lesche R, Mamillapalli R, Li D, Zheng Y, Sun H, Wu H (2000) Genetic deletion of the Pten tumor suppressor gene promotes cell motility by activation of Rac1 and Cdc42 GTPases. Curr Biol 10(7): 401-404 (Pubitemid 30213387)
47. Liu SG, Wang BS, Jiang YY, Zhang TT, Shi ZZ, Yang Y, Yang YL, Wang XC, Lin DC, Zhang Y, Yang H, Cai Y, Zhan QM, Wang MR (2011) Atypical protein kinase C(iota) (PKC(iota)) promotes metastasis of esophageal squamous cell carcinoma by enhancing resistance to anoikis via PKC(iota)-SKP2-AKT pathway. Mol Cancer Res
48. Lu Y, Lin YZ, LaPushin R, Cuevas B, Fang X, Yu SX, Davies MA, Khan H, Furui T, Mao M, Zinner R, Hung MC, Steck P, Siminovitch K, Mills GB (1999) The PTEN/MMAC1/TEP tumor suppressor gene decreases cell growth and induces apoptosis and anoikis in breast cancer cells. Oncogene 18(50): 7034-7045 (Pubitemid 30028874)
49. Maccario H, Perera NM, Davidson L, Downes CP, Leslie NR (2007) PTEN is destabilized by phosphorylation on Thr366. Biochem J 405(3): 439-444
50. Maehama T, Dixon JE (1999) PTEN: a tumour suppressor that functions as a phospholipid phosphatase. Trends Cell Biol 9(4): 125-128 (Pubitemid 29161437)
51. Mai W, Kawakami K, Shakoori A, Kyo S, Miyashita K, Yokoi K, Jin M, Shimasaki T, Motoo Y, Minamoto T (2009) Deregulated GSK3(beta) sustains gastrointestinal cancer cells survival by modulating human telomerase reverse transcriptase and telomerase. Clin Cancer Res 15(22): 6810-6819
52. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, Gerke V, Mostov K (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128(2): 383-397 (Pubitemid 46123512)
53. Melendez J, Grogg M, Zheng Y (2011) Signalling role of Cdc42 in regulating mammalian physiology. J Biol Chem 286(4): 2375-2381
54. Na S, Li B, Grewal IS, Enslen H, Davis RJ, Hanke JH, Flavell RA (1999) Expression of activated CDC42 induces T cell apoptosis in thymus and peripheral lymph organs via different pathways. Oncogene 18(56): 7966-7974 (Pubitemid 30050557)
55. Pap M, Cooper GM (1998) Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. J Biol Chem 273(32): 19929-19932 (Pubitemid 28377539)
56. Riccardi C, Nicoletti I (2006) Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc 1(3): 1458-1461
57. Schlessinger K, McManus EJ, Hall A (2007) Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J Cell Biol 178(3): 355-361 (Pubitemid 47196145)
58. Sun H, Lesche R, Li DM, Liliental J, Zhang H, Gao J, Gavrilova N, Mueller B, Liu X, Wu H (1999) PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signalling pathway. Proc Natl Acad Sci USA 96(11): 6199-6204 (Pubitemid 29256643)
59. Tang M, Iijima M, Kamimura Y, Chen L, Long Y, Devreotes P (2011) Disruption of PKB signalling restores polarity to cells lacking tumor suppressor PTEN. Mol Biol Cell 22(4): 437-447
60. UKCCCR guidelines for the use of cell lines in cancer research (2000) Br J Cancer 82(9): 1495-509
61. Vitolo MI, Weiss MB, Szmacinski M, Tahir K, Waldman T, Park BH, Martin SS, Weber DJ, Bachman KE (2009) Deletion of PTEN promotes tumorigenic signalling, resistance to anoikis, and altered response to chemotherapeutic agents in human mammary epithelial cells. Cancer Res 69(21): 8275-8283
62. Walker GE, Wilson EM, Powell D, Oh Y (2001) Butyrate, a histone deacetylase inhibitor, activates the human IGF binding protein-3 promoter in breast cancer cells: molecular mechanism involves an Sp1/Sp3 multiprotein complex. Endocrinology 142(9): 3817-3827 (Pubitemid 32802652)
63. Wang L, Yang L, Luo Y, Zheng Y (2003) A novel strategy for specifically down-regulating individual Rho GTPase activity in tumor cells. J Biol Chem 278(45): 44617-44625 (Pubitemid 37377216)
64. Wang Q, Wang X, Hernandez A, Kim S, Evers BM (2001) Inhibition of the phosphatidylinositol 3-kinase pathway contributes to HT29 and Caco2 intestinal cell differentiation. Gastroenterology 120(6): 1381-1392 (Pubitemid 32322312)
65. Wang Q, Zhou Y, Wang X, Chung DH, Evers BM (2007) Regulation of PTEN expression in intestinal epithelial cells by c-Jun NH2-terminal kinase activation and nuclear factor-kappaB inhibition. Cancer Res 67(16): 7773-7781 (Pubitemid 47281371)
66. Warner SJ, Yashiro H, Longmore GD (2010) The Cdc42/Par6/aPKC Polarity Complex Regulates Apoptosis-Induced Compensatory Proliferation in Epithelia. Current Biol 20(8): 677-686
67. Weng L, Brown J, Eng C (2001) PTEN induces apoptosis and cell cycle arrest through phosphoinositol-3-kinase/Akt-dependent and-independent pathways. Hum Mol Genet 10(3): 237-242 (Pubitemid 32123982)
68. Yap TA, Garrett MD, Walton MI, Raynaud F, de Bono JS, Workman P (2008) Targeting the PI3K-AKT-mTOR pathway: progress, pitfalls, and promises. Curr Opin Pharmacol 8(4): 393-412
69. Zhou FQ, Snider WD (2005) Cell biology. GSK-3beta and microtubule assembly in axons. Science 308(5719): 211-214 (Pubitemid 40558846)