Glycogen synthase kinase-3 inhibition sensitizes pancreatic cancer cells to TRAIL-induced apoptosis

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Mamaghani, Shadi ^a,b,c   Simpson, Craig D ^c   Cao, Pinjiang M ^a,c   Cheung, May ^a,c   Chow, Sue ^a,c   Bandarchi, Bizhan ^c   Schimmer, Aaron D ^c   Hedley, David W ^a,b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 METHOXYBENZYL) 3 (5 NITRO 2 THIAZOLYL)UREA; BETA CATENIN; CASPASE 3; CASPASE 8; CYTOKINE RESPONSE MODIFIER A; DEATH RECEPTOR; GLYCOGEN SYNTHASE KINASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHEMOSENSITIZATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PANCREAS CANCER; PROSTATE CANCER; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

APOPTOSIS; BCL-X PROTEIN; CELL LINE, TUMOR; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

MUS;

EID: 84864052222     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041102     Document Type: Article

References (50)

1. Papenfuss K, Cordier SM, Walczak H, (2008) Death receptors as targets for anti-cancer therapy. J Cell Mol Med 12: 2566-2585.
2. Wiezorek J, Holland P, Graves J, (2010) Death receptor agonists as a targeted therapy for cancer. Clin Cancer Res 16: 1701-1708.
3. Ashkenazi A, Holland P, Eckhardt SG, (2008) Ligand-based targeting of apoptosis in cancer: the potential of recombinant human apoptosis ligand 2/Tumor necrosis factor-related apoptosis-inducing ligand (rhApo2L/TRAIL). J Clin Oncol 26: 3621-3630.
4. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, et al. (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104: 155-162.
5. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, et al. (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5: 157-163.
6. Ashkenazi A, (2008) Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 7: 1001-1012.
7. Ozawa F, Friess H, Kleeff J, Xu ZW, Zimmermann A, et al. (2001) Effects and expression of TRAIL and its apoptosis-promoting receptors in human pancreatic cancer. Cancer Lett 163: 71-81.
8. Vogler M, Durr K, Jovanovic M, Debatin KM, Fulda S, (2007) Regulation of TRAIL-induced apoptosis by XIAP in pancreatic carcinoma cells. Oncogene 26: 248-257.
9. Hinz S, Trauzold A, Boenicke L, Sandberg C, Beckmann S, et al. (2000) Bcl-XL protects pancreatic adenocarcinoma cells against CD95- and TRAIL-receptor-mediated apoptosis. Oncogene 19: 5477-5486.
10. Beurel E, Blivet-Van Eggelpoel MJ, Kornprobst M, Moritz S, Delelo R, et al. (2009) Glycogen synthase kinase-3 inhibitors augment TRAIL-induced apoptotic death in human hepatoma cells. Biochem Pharmacol 77: 54-65.
11. Todaro M, Lombardo Y, Francipane MG, Alea MP, Cammareri P, et al. (2008) Apoptosis resistance in epithelial tumors is mediated by tumor-cell-derived interleukin-4. Cell Death Differ 15: 762-772.
12. Arlt A, Gehrz A, Muerkoster S, Vorndamm J, Kruse ML, et al. (2003) Role of NF-kappaB and Akt/PI3K in the resistance of pancreatic carcinoma cell lines against gemcitabine-induced cell death. Oncogene 22: 3243-3251.
13. Holcomb B, Yip-Schneider M, Schmidt CM, (2008) The role of nuclear factor kappaB in pancreatic cancer and the clinical applications of targeted therapy. Pancreas 36: 225-235.
14. Mamaghani S, Patel S, Hedley DW, (2009) Glycogen synthase kinase-3 inhibition disrupts nuclear factor-kappaB activity in pancreatic cancer, but fails to sensitize to gemcitabine chemotherapy. BMC Cancer 9: 132.
15. Beurel E, Jope RS, (2006) The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 79: 173-189.
16. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, et al. (2000) Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406: 86-90.
17. Schwabe RF, Brenner DA, (2002) Role of glycogen synthase kinase-3 in TNF-alpha-induced NF-kappa B activation and apoptosis in hepatocytes. Am J Physiol Gastrointest Liver Physiol 283: G204-211.
18. Song L, Zhou T, Jope RS, (2004) Lithium facilitates apoptotic signaling induced by activation of the Fas death domain-containing receptor. BMC Neurosci 5: 20.
19. Rottmann S, Wang Y, Nasoff M, Deveraux QL, Quon KC, (2005) A TRAIL receptor-dependent synthetic lethal relationship between MYC activation and GSK3beta/FBW7 loss of function. Proc Natl Acad Sci U S A 102: 15195-15200.
20. Liao X, Zhang L, Thrasher JB, Du J, Li B, (2003) Glycogen synthase kinase-3beta suppression eliminates tumor necrosis factor-related apoptosis-inducing ligand resistance in prostate cancer. Mol Cancer Ther 2: 1215-1222.
21. Khanbolooki S, Nawrocki ST, Arumugam T, Andtbacka R, Pino MS, et al. (2006) Nuclear factor-kappaB maintains TRAIL resistance in human pancreatic cancer cells. Mol Cancer Ther 5: 2251-2260.
22. Simpson CD, Mawji IA, Anyiwe K, Williams MA, Wang X, et al. (2009) Inhibition of the sodium potassium adenosine triphosphatase pump sensitizes cancer cells to anoikis and prevents distant tumor formation. Cancer Res 69: 2739-2747.
23. Belmokhtar CA, Hillion J, Segal-Bendirdjian E, (2001) Staurosporine induces apoptosis through both caspase-dependent and caspase-independent mechanisms. Oncogene 20: 3354-3362.
24. Pham N-A, Robinson BH, Hedley DW, (2000) Simultaneous detection of mitochondrial respiratory chain activity and reactive oxygen in digitonin-permeabilized cells using flow cytometry. Cytometry 41: 245-251.
25. Pham NA, Jacobberger JW, Schimmer AD, Cao P, Gronda M, et al. (2004) The dietary isothiocyanate sulforaphane targets pathways of apoptosis, cell cycle arrest, and oxidative stress in human pancreatic cancer cells and inhibits tumor growth in severe combined immunodeficient mice. Mol Cancer Ther 3: 1239-1248.
26. Kerfoot C, Huang W, Rotenberg SA, (2004) Immunohistochemical analysis of advanced human breast carcinomas reveals downregulation of protein kinase C alpha. J Histochem Cytochem 52: 419-422.
27. Slebos RJC, Hoppin JA, Tolbert PE, Holly EA, Brock JW, et al. (2000) K-ras and p53 in Pancreatic Cancer: Association with Medical History, Histopathology, and Environmental Exposures in a Population-based Study. Cancer Epidemiology Biomarkers & Prevention 9: 1223-1232.
28. Pellegata NS, Sessa F, Renault B, Bonato M, Leone BE, et al. (1994) K-ras and p53 gene mutations in pancreatic cancer: ductal and nonductal tumors progress through different genetic lesions. Cancer Res 54: 1556-1560.
29. Ashkenazi A, Herbst RS, (2008) To kill a tumor cell: the potential of proapoptotic receptor agonists. J Clin Invest 118: 1979-1990.
30. Drosopoulos KG, Roberts ML, Cermak L, Sasazuki T, Shirasawa S, et al. (2005) Transformation by oncogenic RAS sensitizes human colon cells to TRAIL-induced apoptosis by up-regulating death receptor 4 and death receptor 5 through a MEK-dependent pathway. J Biol Chem 280: 22856-22867.
31. Oikonomou E, Kosmidou V, Katseli A, Kothonidis K, Mourtzoukou D, et al. (2009) TRAIL receptor upregulation and the implication of KRAS/BRAF mutations in human colon cancer tumors. Int J Cancer 125: 2127-2135.
32. Salvesen GS, Duckett CS, (2002) IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 3: 401-410.
33. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, et al. (2008) Targeting XIAP bypasses Bcl-2-mediated resistance to TRAIL and cooperates with TRAIL to suppress pancreatic cancer growth in vitro and in vivo. Cancer Res 68: 7956-7965.
34. Aggarwal BB, (2004) Nuclear factor-kappaB: the enemy within. Cancer Cell 6: 203-208.
35. Fakler M, Loeder S, Vogler M, Schneider K, Jeremias I, et al. (2009) Small molecule XIAP inhibitors cooperate with TRAIL to induce apoptosis in childhood acute leukemia cells and overcome Bcl-2-mediated resistance. Blood 113: 1710-1722.
36. Braeuer SJ, Buneker C, Mohr A, Zwacka RM, (2006) Constitutively activated nuclear factor-kappaB, but not induced NF-kappaB, leads to TRAIL resistance by up-regulation of X-linked inhibitor of apoptosis protein in human cancer cells. Mol Cancer Res 4: 715-728.
37. Kim SH, Ricci MS, El-Deiry WS, (2008) Mcl-1: a gateway to TRAIL sensitization. Cancer Res 68: 2062-2064.
38. Ougolkov AV, Fernandez-Zapico ME, Savoy DN, Urrutia RA, Billadeau DD, (2005) Glycogen synthase kinase-3beta participates in nuclear factor kappaB-mediated gene transcription and cell survival in pancreatic cancer cells. Cancer Res 65: 2076-2081.
39. Hirpara JL, Clement MV, Pervaiz S, (2001) Intracellular acidification triggered by mitochondrial-derived hydrogen peroxide is an effector mechanism for drug-induced apoptosis in tumor cells. J Biol Chem 276: 514-521.
40. Jung EM, Lim JH, Lee TJ, Park JW, Choi KS, et al. (2005) Curcumin sensitizes tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis through reactive oxygen species-mediated upregulation of death receptor 5 (DR5). Carcinogenesis 26: 1905-1913.
41. Kwon D, Choi IH, (2006) Hydrogen peroxide upregulates TNF-related apoptosis-inducing ligand (TRAIL) expression in human astroglial cells, and augments apoptosis of T cells. Yonsei Med J 47: 551-557.
42. Xia T, Jiang C, Li L, Chen Q, Wu C, et al. (2002) Mechanism of mitochondrial respiratory control in caspase-3 induced positive feedback loop in apoptosis. Chinese Science Bulletin 47: 480-484.
43. Masood A, Azmi AS, Mohammad RM, (2011) Small Molecule Inhibitors of Bcl-2 Family Proteins for Pancreatic Cancer Therapy. Cancers (Basel) 3: 1527-1549.
44. Ali A, Hoeflich KP, Woodgett JR, (2001) Glycogen synthase kinase-3: properties, functions, and regulation. Chem Rev 101: 2527-2540.
45. Zeng G, Germinaro M, Micsenyi A, Monga NK, Bell A, et al. (2006) Aberrant Wnt/beta-catenin signaling in pancreatic adenocarcinoma. Neoplasia 8: 279-289.
46. Dessimoz J, Grapin-Botton A, (2006) Pancreas development and cancer: Wnt/beta-catenin at issue. Cell Cycle 5: 7-10.
47. De Toni EN, Thieme SE, Herbst A, Behrens A, Stieber P, et al. (2008) OPG is regulated by beta-catenin and mediates resistance to TRAIL-induced apoptosis in colon cancer. Clin Cancer Res 14: 4713-4718.
48. Doble BW, Woodgett JR, (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116: 1175-1186.
49. Zhou F-Q, Snider WD, (2005) GSK-3β and Microtubule Assembly in Axons. Science 308: 211-214.
50. Ougolkov AV, Fernandez-Zapico ME, Bilim VN, Smyrk TC, Chari ST, et al. (2006) Aberrant Nuclear Accumulation of Glycogen Synthase Kinase-3β in Human Pancreatic Cancer: Association with Kinase Activity and Tumor Dedifferentiation. Clin Cancer Res 12: 5074-5081.