GSK-3α promotes oncogenic KRAS function in pancreatic cancer via TAK1-TAB stabilization and regulation of noncanonical NF-κB

Cancer Discovery

Volumn 3, Issue 6, 2013, Pages 690-703

  Bang, Deepali ^a   Wilson, Willie ^a,c   Ryan, Meagan ^a   Yeh, Jen Jen ^a   Baldwin, Albert S ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 METHOXYBENZYL) 3 (5 NITRO 2 THIAZOLYL) UREA; GLYCOGEN SYNTHASE KINASE 3ALPHA; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONCOGENE K RAS; PANCREAS CANCER; RNA INTERFERENCE; TUMOR GROWTH; UPREGULATION; WESTERN BLOTTING;

ANIMALS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DOWN-REGULATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE KINASES; MICE; NF-KAPPA B; PANCREATIC NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84878884564     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-12-0541     Document Type: Article

References (50)

1. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer2 003;3:11-22.
2. Ying H, Kimmelman AC, Lyssiotis CA, Hua S, Chu GC, FletcherSananikone E, et al. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell 2012;149: 656-70.
3. Vaccaro V, Melisi D, Bria E, Cuppone F, Ciuffreda L, Pino MS, et al. Emerging pathways and future targets for the molecular therapy of pancreatic cancer. Expert Opin Ther Targets 2011;15:1183-96.
4. Wolff RA. Chemotherapy for pancreatic cancer: from metastatic disease to adjuvant therapy. Cancer J 2007;13:175-84.
5. Singh A, Sweeney MF, Yu M, Burger A, Greninger P, Benes C, etal. TAK1 inhibition promotes apoptosis in KRAS-dependent colon cancers. Cell 2012;148:639-50.
6. Melisi D, Xia Q, Paradiso G, Ling J, Moccia T, Carbone C, etal. Modulation of pancreatic cancer chemoresistance by inhibition of TAK1. J Natl Cancer Inst 2011;103:1190-204.
7. Ougolkov AV, Billadeau DD. Targeting GSK-3: a promising approach for cancer therapy?Future Oncol 2006;2:91-100.
8. Hayden MS, Ghosh S. NF-B, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 2012;26:203-34.
9. Karin M, Cao Y, Greten FR, Li Z-W. NF-κB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2002;2:301-10.
10. Bassères DS, Baldwin AS. Nuclear factor-κB and inhibitor of κB kinase pathways in oncogenic initiation and progression. Oncogene 2006;25:6817-30.
11. Perkins ND. The diverse and complex roles of NF-κB subunits in cancer. Nat Rev Cancer 2012;19:121-32.
12. Bonizzi G, Bebien M, Otero DC, Johnson-Vroom KE, Cao Y, Vu D, etal. Activation of IKK α target genes depends on recognition of specific κB binding sites by RelB: p52 dimers. EMBO J 2004;23:4202-10.
13. Mayo MW, Wang CY, Cogswell PC, Rogers-Graham KS, Lowe SW, Der CJ, etal. Requirement of NFκB activation to suppress p53-independent apoptosis induced by oncogenic Ras. Science 1997;278:1812-5.
14. MeylanE, DooleyA L, FeldserD M, Shen L, TurkE, OuyangC, etal. Requirement for NF-κB signalling in a mouse model of lung adenocarcinoma. Nature 2009;461:104-7.
15. Yang J, Splittgerber R, Yull FE, Kantrow S, Ayers GD, Karin M, etal. Conditional ablation of Ikkβ inhibits melanoma tumor development in mice. J Clin Invest 2010;120:2563-74.
16. Bassères DS, Ebbs A, Levantini E, Baldwin AS. Requirement of the NF-κB subunit p65/RelA for K-Ras-induced lung tumorigenesis. Cancer Res 2010;70:3537-46.
17. Xia Y, Yeddula N, Leblanc M, Ke E, Zhang Y, Oldfield E, etal. Reduced cell proliferation by IKK2 depletion in a mouse lung-cancer model. Nat Cell Biol 2012;14:257-65.
18. Carbone C, Melisi D. NF-κB as a target for pancreatic cancer therapy. Expert Opin Ther Targets 2012;26(Suppl 2):S1-10.
19. Li L, Aggarwal BB, Shishodia S, Abbruzzese J, Kurzrock R. Nuclear factor-κB and IκB kinase are constitutively active in human pancreatic cells, and their down-regulation by curcumin (diferuloylmethane) is associated with the suppression of proliferation and the induction of apoptosis. Cancer 2004;101:2351-62.
20. Liptay S, Weber CK, Ludwig L, Wagner, M, Adler G, Schmid R.M. Mitogenic and antiapoptotic role of constitutive NF-κB/Rel activity in pancreatic cancer. Int J Cancer 2003;105:735-46.
21. Wilson W, Baldwin AS. Maintenance of constitutive I B kinase activity by glycogen synthase kinase-3/in pancreatic cancer. Cancer Res 2008;68:8156-63.
22. Wang W, Abbruzzese JL, Evans DB, Larry L, Cleary KR, Chiao PJ. The nuclear factor-κB RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells. Clin Cancer Res 1999;5:119-27.
23. Ling J, Kang Y, Zhao R, Xia Q, Lee D-F, Chang Z, et al. KrasG12Dinduced IKK2/β/NF-κB activation by IL-1α and p62 feedforward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell 2012;21:105-20.
24. Duran A, Linares JF, Galvez AS, Wikenheiser K, Flores JM, Diaz-Meco MT, etal. The signaling adaptor p62 is an important NFκB mediator in tumorigenesis. Cancer Cell 2008;13:343-54.
25. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature 2001;412: 346-51.
26. Pickett TD, Ninomiya-Tsuji J. TAB4 stimulates TAK1-TAB1 phosphorylation and binds polyubiquitin to direct signaling to NF-κB. J Biol Chem 2008;283:19245-54.
27. Omori E, Inagaki M, Mishina Y, Matsumoto K, Ninomiya-Tsuji J. Epithelial transforming growth factor β-activated kinase 1 (TAK1) is activated through two independent mechanisms and regulates reactive oxygen species. Proc Natl Acad Sci U S A 2012;109: 3365-70.
28. Raman M, Chen W, Cobb MH. Differential regulation and properties of MAPKs. Oncogene 2007;26:3100-12.
29. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin OU, Woodgett JR. Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 2000;406:86-90.
30. Doble BW. GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 2003;116:1175-86.
31. Ougolkov AV, Fernandez-Zapico ME, Savoy DN, Urrutia RA Billadeau DD. Glycogen synthase kinase-3β participates in nuclear factor κB-mediated gene transcription and cell survival in pancreatic cancer cells. Cancer Res 2005;65:2076-81.
32. Wang Z, Smith KS, MurphyM, PilotoO, Somervaille TCP, Cleary ML. Glycogen synthase kinase 3 in MLL leukaemia maintenance and targeted therapy. Nature 2008;455:1205-9.
33. Banerji V, Frumm SM, Ross KN, Li LS, Schinzel AC, Hahn CK, etal. The intersection of genetic and chemical genomic screens identifies GSK-3α as a target in human acute myeloid leukemia. J Clin Invest 2012;122:935-47.
34. Ougolkov AV. Aberrant nuclear accumulation of glycogen synthase kinase-3 in human pancreatic cancer: association with kinase activity and tumor dedifferentiation. Clin Cancer Res 2006;12:5074-81.
35. Zhang J-S, Koenig A, Harrison A, Ugolkov AV, Fernandez-Zapico ME, Couch FJ, etal. Mutant K-Ras increases GSK-3 β gene expression via an ETS-p300 transcriptional complex in pancreatic cancer. Oncogene 2011;30:3705-15.
36. Wharry C, Haines KM, Carroll RG, May MJ. Constitutive noncanonical NFκB signaling in pancreatic cancer cells. Cancer Biol Ther 2009;8:1567-76.
37. Nishina T, Yamaguchi N, Gohda J, Semba K, Inoue J-I. NIK is involved in constitutive activation of the alternative NF-κB pathway and proliferation of pancreatic cancer cells. Biochem Biophys Res Commun 2009;388:96-101.
38. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010;60:277-300.
39. Marchand B, Tremblay I, Cagnol S, Boucher MJ. Inhibition of glycogen synthase kinase-3 activity triggers an apoptotic response in pancreatic cancer cells through JNK-dependent mechanisms. Carcinogenesis 2012;33:529-37.
40. Taelman VF, Dobrowolski R, Plouhinec J-L, Fuentealba LC, Vorwald PP, Gumper I, et al. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 2010;143:1136-48.
41. Busino L, Millman SE, Scotto L, Kyratsous CA, Basrur V, O'Connor O, et al. Fbxw7\alphaand GSK3-mediated degradation of p100 is a pro-survival mechanism in multiple myeloma. Nat Cell Biol 2012;14:1-12.
42. Arabi A, Ullah K, Branca RMM, Johansson J, Bandarra D, Haneklaus M, etal. Proteomic screen reveals Fbw7 as a modulator of the NF-κB pathway. Nat Commun 2012;3:976-11.
43. Hanson JL. The nuclear factor B subunits RelA/p65 and c-Rel potentiate but are not required for Ras-induced cellular transformation. Cancer Res 2004;64:7248-55.
44. Steinbrecher KA, Wilson W, Cogswell PC, Baldwin AS. Glycogen synthase kinase 3 functions to specify gene-specific, NF-B-dependent transcription. Mol Cell Biol 2005;25:8444-55.
45. Gibb EA, Brown CJ, Lam WL. The functional role of long non-coding RNA in human carcinomas. Mol Cancer 2011;10:38.
46. Woodgett JR. Can a two-faced kinase be exploited for osteosarcoma? J Natl Cancer Inst 2012;104:722-3.
47. de Hoon MJL, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004;20:1453-4.
48. Saldanha AJ. Java Treeview-extensible visualization of microarray data. Bioinformatics 2004;20:3246-8.
49. Smyth G. Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W editors. Bioinformatics and computational biology solutions using R and Bioconductor. New York: Springer; 2005. p. 397-420.
50. BenjaminiY,.HochbergY, Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995;57:289-300.