Inhibition of glycogen synthase kinase-3 activity triggers an apoptotic response in pancreatic cancer cells through JNK-dependent mechanisms

Carcinogenesis

Volumn 33, Issue 3, 2012, Pages 529-537

  Marchand, Benoît ^a   Tremblay, Isabelle ^a   Cagnol, Sébastien ^b   Boucher, Marie Josée ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; DEATH RECEPTOR; GLYCOGEN SYNTHASE KINASE 3; MESSENGER RNA; STRESS ACTIVATED PROTEIN KINASE;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CELL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; METASTASIS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84857986934     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgr309     Document Type: Article

References (59)

1. Hezel, A.F. et al. (2006) Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev., 20, 1218-1249.
2. Schneider, G. et al. (2005) Pancreatic cancer: basic and clinical aspects. Gastroenterology, 128, 1606-1625.
3. Billadeau, D.D. (2007) Primers on molecular pathways: the glycogen synthase kinase-3β. Pancreatology, 7, 398-402.
4. Garcea, G. et al. (2007) Glycogen synthase kinase-3 beta; a new target in pancreatic cancer? Curr. Cancer Drug Targets, 7, 209-215.
5. Martinez, A. (2008) Preclinical efficacy on GSK-3 inhibitors: toward a future generation of powerful drugs. Med. Res. Rev., 28, 773-796.
6. Miyashita, K. et al. (2009) An emerging strategy for cancer treatment targeting aberrant glycogen synthase kinase 3 beta. Anticancer Agents Med. Chem., 9, 1114-1122.
7. Kockeritz, L. et al. (2006) Glycogen synthase kinase-3-an overview of an over-achieving protein kinase. Curr. Drug Targets, 7, 1377-1388.
8. Ougolkov, A.V. et al. (2005) Glycogen synthase kinase-3β participates in nuclear factor κB-mediated gene transcription and cell survival in pancreatic cancer cells. Cancer Res., 65, 2076-2081.
9. Wilson, W. III et al. (2008) Maintenance of constitutive IκB kinase activity by glycogen synthase kinase-3α/β in pancreatic cancer. Cancer Res., 68, 8156-8163.
10. Mamaghani, S. et al. (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.
11. Mai, W. et al. (2009) Deregulated GSK3β sustains gastrointestinal cancer cells survival by modulating human telomerase reverse transcriptase and telomerase. Clin. Cancer Res., 15, 6810-6819.
12. Ougolkov, A.V. 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.
13. Shakoori, A. et al. (2005) Deregulated GSK3β activity in colorectal cancer: its association with tumor cell survival and proliferation. Biochem. Biophys. Res. Commun., 334, 1365-1373.
14. Shakoori, A. et al. (2007) Inhibition of GSK-3β activity attenuates proliferation of human colon cancer cells in rodents. Cancer Sci., 98, 1388-1393.
15. Kotliarova, S. et al. (2008) Glycogen synthase kinase-3 inhibition induces glioma cell death through c-MYC, nuclear factor-κB, and glucose regulation. Cancer Res., 68, 6643-6651.
16. Vené, R. et al. (2008) Glycogen synthase kinase 3β regulates cell death induced by synthetic triterpenoids. Cancer Res., 68, 6987-6996.
17. Kunnimalaiyaan, M. et al. (2007) Inactivation of glycogen synthase kinase-3β, a downstream target of the raf-1 pathway, is associated with growth suppression in medullary thyroid cancer cells. Mol. Cancer Ther., 6, 1151-1158.
18. Mai, W. et al. (2006) Detection of active fraction of glycogen synthase kinase 3beta in cancer cells by nonradioisotopic in vitro kinase assay. Oncology, 71, 297-305.
19. Pasca di Magliano, M. et al. (2007) Common activation of canonical Wnt signaling in pancreatic adenocarcinoma. PLoS One, 2, e1155.
20. Al-Aynati, M. et al. (2004) Epithelial-cadherin and beta-catenin expression changes in pancreatic intraepithelial neoplasia. Clin. Cancer Res., 10, 1235-1240.
21. Cohen, P. et al. (2004) GSK3 inhibitors: development and therapeutic potential. Nat. Rev. Drug Discov., 3, 479-487.
22. Furukawa, T. et al. (1996) Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am. J. Pathol., 148, 1763-1770.
23. Ouyang, H. et al. (2000) Immortal human pancreatic duct epithelial cell lines with near normal genotype and phenotype. Am. J. Pathol., 157, 1623-1631.
24. Boucher, M.J. et al. (2006) Phosphorylation marks IPF1/PDX1 protein for degradation by glycogen synthase kinase 3-dependent mechanisms. J. Biol. Chem., 281, 6395-6403.
25. Molton, S.A. et al. (2003) Selective activation of the c-Jun N-terminal kinase (JNK) pathway fails to elicit Bax activation or apoptosis unless the phosphoinositide 3'-kinase (PI3K) pathway is inhibited. Oncogene, 22, 4690-4701.
26. Boucher, M.J. et al. (2004) Dual role of Mek/Erk signaling in senescence and transformation of intestinal epithelial cells.Am. J. Physiol., 286, G736-G746.
27. Boucher, M.J. et al. (2000) Mek/Erk signaling pathway regulates the expression of Bcl-2, Bcl-Xl and Mcl-1 and promotes survival of human pancreatic cancer cells. J. Cell. Biochem., 79, 335-369.
28. Coghlan, M.P. et al. (2000) Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol., 7, 793-802.
29. Hamacher, R. et al. (2008) Apoptotic pathways in pancreatic ductal adenocarcinoma. Mol. Cancer, 7, 64.
30. Boucher, M.J. et al. (2001) cAMP protection of pancreatic cancer cells against apoptosis induced by ERK inhibition. Biochem. Biophys. Res. Commun., 285, 207-216.
31. Hoeflich, K.P. et al. (2000) Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature, 406, 86-90.
32. Chang, K.J. et al. (2009) Multicenter randomized controlled phase III clinical trial using TNFerade (TNF) with chemoradiation (CRT) in patients with locally advanced pancreatic cancer (LAPC): interim analysis (IA) of overall survival (OS). ASCO Meeting Abstracts, 27, 4605.
33. Rosevear, H.M. et al. (2010) Conatumumab, a fully human mAb against death receptor 5 for the treatment of cancer. Curr. Opin. Investig. Drugs, 11, 688-698.
34. Rajeskumar, N.V. et al. (2010) A combination of DR5 agonistic monoclonal antibody with gemcitabine targets pancreatic cancer stem cells and results in long-term disease control in human pancreatic cancer model. Mol. Cancer Ther., 9, 2582-2592.
35. Pan, X. et al. (2008) Nuclear factor-κB p65/relA silencing induces apoptosis and increases gemcitabine effectiveness in a subset of pancreatic cancer cells. Clin. Cancer Res., 14, 8143-8151.
36. Zhang, Y. et al. (2008) IκBα kinase inhibitor IKI-1 conferred tumor necrosis factor a sensitivity to pancreatic cancer cells and a xenograft tumor model. Cancer Res., 68, 9519-9524.
37. Wei, W. et al. (2005) The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin ligase. Cancer Cell, 8, 25-33.
38. Abell, A.N. et al. (2007) MEKK4 stimulation of p38 and JNK activity is negatively regulated by GSK3β. J. Biol. Chem., 282, 30476-30484.
39. Dhanasekaran, D.N. et al. (2008) JNK signaling and apoptosis. Oncogene, 27, 6245-6251.
40. Mizukami, Y. et al. (2001) Requirement of cJun N-terminal kinase for apoptotic cell death induced by farnesyltransferase inhibitor, farnesylamine, in human pancreatic cancer cells. Biochem. Biophys. Res. Commun., 288, 198-204.
41. Nawrocki, S.T. et al. (2005) Bortezomib sensitizes pancreatic cancer cells to endoplasmic reticulum stress-mediated apoptosis. Cancer Res., 65, 11658-11666.
42. Sahu, R.P. et al. (2009) Benzyl isothiocyanate-mediated generation of reactive oxygen species causes cell cycle arrest and induces apoptosis via activation of MAPK in human pancreatic cancer cells. Carcinogenesis, 30, 1744-1753.
43. Spokoini, R. et al. (2010) Glycogen synthase kinase-3 plays a central role in mediating glucocorticoid-induced apoptosis. Mol. Endocrinol., 24, 1136-1150.
44. Hongisto, V. et al. (2003) Lithium blocks the c-Jun stress response and protects neurons via its action on glycogen synthase kinase 3. Mol. Cell. Biol., 23, 6027-6036.
45. Whitfield, J. et al. (2001) Dominant-negative cJun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron, 29, 629-643.
46. Harris, C.A. et al. (2001) BH3-only Bcl-2 family members are coordinately regulated by the JNK pathway and require Bax to induce apoptosis in neurons. J. Biol. Chem., 276, 37754-37760.
47. Biswas, S.C. et al. (2007) Pro-apoptotic Bim induction in response to nerve growth factor deprivation requires simultaneous activation of three different death signaling pathways. J. Biol. Chem., 282, 29368-29374.
48. Putcha, G.V. et al. (2003) JNK-mediated BIM phosphorylation potentiates BAX-dependent apoptosis. Neuron, 38, 899-914.
49. Lei, K. et al. (2003) JNK phosphorylation of Bim-related members of the Bcl-2 family induces Bax-dependent apoptosis. Proc. Natl Acad. Sci. USA, 100, 2432-2437.
50. Klein, P.S. et al. (1996) A molecular mechanism for the effect of lithium on development. Proc. Natl Acad. Sci. USA, 93, 8455-8459.
51. Bayaert, R. et al. (1989) Lithium chloride potentiates tumor necrosis factormediated cytotoxicity in vitro and in vivo. Proc. Natl Acad. Sci. USA, 86, 9494-9498.
52. Rottman, S. et al. (2005) A TRAIL receptor-dependent synthetic lethal relationship between MYC activation and GSK3β/FBW7 loss of function. Proc. Natl Acad. Sci. USA, 102, 15195-15200.
53. Song, L. et al. (2004) Lithium facilitates apoptotic signaling induced by activation of the Fas death domain-containing receptor. BMC Neurosci., 5, 20.
54. Liao, X. et al. (2003) Glycogen synthase kinase-3β suppression eliminates tumor necrosis factor-related apoptosis-inducing ligand resistance in prostate cancer. Mol. Cancer Ther., 2, 1215-1222.
55. Sun, M. et al. (2008) Identification of an antiapoptotic protein complex at death receptors. Cell Death Differ., 15, 1887-1900.
56. Beurel, E. et al. (2009) Glycogen synthase kinase-3 inhibitors augment TRAIL-induced apoptotic death in human hepatoma cells. Biochem. Pharmacol., 77, 54-65.
57. Weichselbaum, R.R. et al. (2009) Translation of the radio- and chemoinducible TNFerade vector to the treatment of human cancers. Cancer Gene Ther., 16, 609-619.
58. Huang, Y. (2007) TRAIL death receptors and cancer therapeutics. Toxicol. Appl. Pharmacol., 224, 284-289.
59. Cohen, Y. et al. (1998) Cancer morbidity in psychiatric patients: influence of lithium carbonate treatment. Med. Oncol., 15, 32-36.