Aberrant Glycogen Synthase Kinase 3β Is Involved in Pancreatic Cancer Cell Invasion and Resistance to Therapy

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Kitano, Ayako ^a   Shimasaki, Takeo ^a,b   Chikano, Yuri ^a   Nakada, Mitsutoshi ^a   Hirose, Mayumi ^a   Higashi, Tomomi ^a   Ishigaki, Yasuhito ^b   Endo, Yoshio ^a   Takino, Takahisa ^a   Sato, Hiroshi ^a   Sai, Yoshimichi ^a   Miyamoto, Ken ichi ^a   Motoo, Yoshiharu ^b   Kawakami, Kazuyuki ^a   Minamoto, Toshinari ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 METHOXYBENZYL) 3 (5 NITRO 2 THIAZOLYL)UREA; CYCLIN D1; F ACTIN; FOCAL ADHESION KINASE; GELATINASE A; GEMCITABINE; GLYCOGEN SYNTHASE KINASE 3BETA; RAC1 PROTEIN; RETINOBLASTOMA PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CANCER INVASION; CANCER RESISTANCE; CELL INVASION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IONIZING RADIATION; LAMELLIPODIUM; MIGRATION INHIBITION; MOUSE; NONHUMAN; PANCREAS CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RNA INTERFERENCE; TUMOR XENOGRAFT; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; DEOXYCYTIDINE; DRUG RESISTANCE, NEOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; PHOSPHORYLATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84873640559     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055289     Document Type: Article

References (52)

1. Siegel R, Naishadham D, Jemal A, (2012) Cancer statistics, 2012. CA Cancer J Clin 62: 10-29.
2. Bardeesy N, DePinho RA, (2002) Pancreatic cancer biology and genetics. Nat Rev Cancer 2: 897-909.
3. Li D, Xie K, Wolff R, Abbruzzese JL, (2004) Pancreatic cancer. Lancet 363: 1049-1057.
4. Hidalgo M, (2010) Pancreatic cancer. N Engl J Med 362: 1605-1617.
5. Furukawa T, (2008) Molecular targeting therapy for pancreatic cancer: Current knowledge and perspectives from bench to bedside. J Gastroenterol 43: 905-911.
6. Morgan MA, Parsels LA, Maybaum J, Lawrence TS, (2008) Improving gemcitabine-mediated radiosensitization using molecularly targeted therapy: a review. Clin Cancer Res 14: 6744-6750.
7. Jope RS, Johnson GV, (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29: 95-102.
8. Jope RS, Yuskaitis CJ, Beurel E, (2007) Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem Res 32: 577-595.
9. Shakoori A, Ougolkov A, Yu ZW, Zhang B, Modarressi MH, et al. (2005) Deregulated GSK3β activity in colorectal cancer: its association with tumor cell survival and proliferation. Biochem Biophys Res Commun 334: 1365-1373.
10. Shakoori A, Mai W, Miyashita K, Yasumoto K, Takahashi Y, et al. (2007) Inhibition of GSK3β attenuates proliferation of human colon cancer cells in rodents. Cancer Sci 98: 1388-93.
11. Miyashita K, Kawakami K, Mai W, Shakoori A, Fujisawa H, et al. (2009) Potential therapeutic effect of glycogen synthase kinase 3β inhibition against human glioblastoma. Clin Cancer Res 15: 887-897.
12. Mai W, Kawakami K, Shakoori A, Kyo S, Miyashita K, et al. (2009) Deregulated glycogen synthase kinase 3β sustains gastrointestinal cancer cells survival by modulating human telomerase reverse transcriptase and telomerase. Clin Cancer Res 15: 6810-6819.
13. Luo J, (2009) Glycogen synthase kinase 3β (GSK3β) in tumorigenesis and cancer chemotherapy. Cancer Lett 273: 194-200.
14. Miyashita K, Nakada M, Shakoori A, Ishigaki Y, Shimasaki T, et al. (2009) An emerging strategy for cancer treatment targeting aberrant glycogen synthase kinase 3β. Anticancer Agents Med Chem 9: 1114-1122.
15. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, et al. (2000) Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406: 86-90.
16. Ougolkov AV, Fernandez-Zapico ME, Savoy DN, Urrutia RA, Billadeau DD, (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.
17. Wilson W 3rd, Baldwin AS (2008) Maintenance of constitutive IκB kinase activity by glycogen synthase kinase-3α/β in pancreatic cancer. Cancer Res 68: 8156-8163.
18. Sun T, Rodriguez M, Kim L, (2009) Glycogen synthase kinase 3 in the world of cell migration. Develop Growth Differ 51: 735-742.
19. Mai W, Miyashita K, Shakoori A, Zhang B, Yu ZW, et al. (2006) Detection of active fraction of GSK3β in cancer cells by non-radioisotopic in vitro kinase assay. Oncology 71: 297-305.
20. Bhat R, Xue Y, Berg S, Hellberg S, Ormö M, et al. (2003) Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J Biol Chem 278: 45937-45945.
21. Tallarida RJ, (2006) An overview of drug combination analysis with isobolograms. J Pharmacol Exp Ther 319: 1-7.
22. Kudo T, Takino T, Miyamori H, Thompson EW, Sato H, (2007) Substrate choice of membnrane-type 1 matrix metalloproteinases is dictated by tissue inhibitor of metalloproteinase-2 levels. Cancer Sci 98: 563-568.
23. Shimasaki T, Ishigaki Y, Nakamura Y, Takata T, Nakaya N, et al. (2012) Glycogen synthase kinase 3β inhibition sensitizes pancreatic cancer cells to gemcitabine. J Gastroenterol 47: 321-333.
24. Knudsen E, Knudsen K, (2008) Tailoring to RB: tumour suppressor status and therapeutic response. Nat Rev Cancer 8: 714-724.
25. Polyak K, Weinberg RA, (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273.
26. Machesky LM, (2008) Lamellipodia and filopodia in metastasis and invasion. FEBS Lett 582: 2102-2111.
27. Sahai E, Marshall CJ, (2002) Rho-GTPases and cancer. Nat Rev Cancer 2: 133-142.
28. Chan AY, Coniglio SJ, Chuang Y, Michaelson D, Knaus UG, et al. (2005) Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 24: 7821-7829.
29. McLean GW, Carragher NO, Avizienyte E, Evans J, Brunton VG, et al. (2005) The role of focal adhesion kinase in cancer-a new therapeutic opportunity. Nat Rev Cancer 5: 505-515.
30. Zhou BP, Deng J, Xia W, Xu J, Li YM, et al. (2004) Dual regulation of Snail by GSK-3β-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6: 931-940.
31. Lazer G, Katzav S, (2011) Guanine nucleotide exchange factors for Rho GTPases: good therapeutic targets for cancer therapy? Cell Signal 23: 969-979.
32. Fernandez-Zapico ME, Gonzalez-Paz NC, Weiss E, Savoy DN, Molina JR, et al. (2005) Ectopic expression of VAV1 reveals an unexpected role in pancreatic cancer tumorigenesis. Cancer Cell 7: 39-49.
33. Brandt D, Grosse R, (2007) Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep 8: 1019-1023.
34. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, et al. (2005) GSK-3β regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120: 137-149.
35. Etienne-Manneville S, Hall A, (2003) Cdc42 regulates GSK-3β and adenomatous polyposis coli to control cell polarity. Nature 421: 753-756.
36. Dong P, Nabeshima K, Nishimura N, Kawakami T, Hachisuga T, et al. (2006) Overexpression and diffuse expression pattern of IQGAP1 at invasion fronts are independent prognostic parameters in ovarian carcinomas. Cancer Lett 243: 120-127.
37. McDonald KL, O'Sullivan MG, Parkinson JF, Shaw JM, Payne CA, et al. (2007) IQGAP1 and IGFBP2: valuable biomarkers for determining prognosis in glioma patients. J Neuropathol Exp Neurol 66: 405-417.
38. Hage B, Meinel K, Baum I, Giehl K, Menke A, (2009) Rac1 activaion inhibits E-cadherin-mediated adherens junctions via binding to IQGAP1 in pancreatic carcinoma cells. Cell Commun Signal 7: 23.
39. Holcomb B, Yip-Schneider M, Schmidt CM, (2008) The role of nuclear factor κB in pancreatic cancer and the clinical applications of targeted therapy. Pancreas 36: 225-235.
40. Mamaghani S, Patel S, Hedley DW, (2009) Glycogen synthase kinase-3 inhibition disrupts nuclear factor-κB activity in pancreatic cancer, but fails to sensitize to gemcitabine chemotherapy. BMC Cancer 9: 132.
41. Ishida S, Huang E, Zuzan H, Spang R, Leone G, et al. (2001) Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol 21: 4684-4699.
42. Nakahira S, Nakamori S, Tsujie M, Takahashi Y, Okami J, et al. (2007) Involvement of ribonucleotide reductase M1 subunit overexpression in gemcitabine resistance of human pancreatic cancer. Int J Cancer 120: 1355-1363.
43. Watson RL, Spalding AC, Zielske SP, Morgan M, Kim AC, et al. (2010) GSK3β and β-catenin modulate radiation cytotoxicity in pancreatic cancer. Neoplasia 12: 357-365.
44. Surjit M, Lal S, (2007) Glycogen synthase kinase-3 phosphorylates and regulates the stability of p27kip1 protein. Cell Cycle 6: 580-588.
45. Wang Z, Smith K, Murphy M, Piloto O, Somervaille T, et al. (2008) Glycogen synthase kinase 3 in MLL leukaemia maintenance and targeted therapy. Nature 455: 1205-1209.
46. Cao Q, Lu X, Feng YJ, (2006) Glycogen synthase kinase-3β positively regulates the proliferation of human ovarian cancer cells. Cell Res 16: 671-677.
47. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou A, (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10: 55-63.
48. Trowbridge JJ, Xenocostas A, Moon RT, Bhatia M, (2006) Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation. Nat Med 12: 89-98.
49. Korur S, Huber RM, Sivasankaran B, Petrich M, Morin P Jr, et al. (2009) GSK3β regulates differentiation and growth arrest in glioblastoma. PLoS One 4: e7443.
50. Yuan H, Mao J, Li L, Wu D, (1999) Suppression of glycogen synthase kinase activity is not sufficient for leukemia enhancer factor-1 activation. J Biol Chem 274: 30419-30423.
51. Zeng X, Tamai K, Doble B, Li S, Huang H, et al. (2005) A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438: 873-877.
52. Chico LK, Van Eldik LJ, Watterson DM, (2009) Targeting protein kinases in central nervous system disorders. Nat Rev Drug Discov 8: 892-909.