Activator protein-1 has an essential role in pancreatic cancer cells and is regulated by a novel Akt-mediated mechanism

Molecular Cancer Research

Volumn 7, Issue 5, 2009, Pages 745-754

  Shin, Sonyo ^a,d,e   Asano, Takayuki ^a,d   Yao, Yixin ^a   Zhang, Ronghua ^a   Claret, Francois Xavier ^a   Korc, Murray ^b   Sabapathy, Kanaga ^c   Menter, David G ^a   Abbruzzese, James L ^a   Reddy, Shrikanth A G ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^c DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^d ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e East Tennessee State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; GLYCOGEN SYNTHASE KINASE 3; PROTEIN C JUN; SERINE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1; TRANSCRIPTION FACTOR FRA 2; TRANSCRIPTION FACTOR JUND;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CANCER CELL; CELL ANCHORAGE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE ACTIVATION; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MUTANT; ONCOGENE C FOS; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; TRANSIENT TRANSFECTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOBLOTTING; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LUCIFERASES; MUTATION; PANCREATIC NEOPLASMS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-JUN; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSFECTION;

EID: 66349088584     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-08-0462     Document Type: Article

References (50)

1. Hezel AF, Kimmelman AC, Stanger BZ, Bardeesy N, Depinho RA. Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev 2006;20:1218-1249 (Pubitemid 43727584)
2. Fujioka S, Sclabas GM, Schmidt C, et al. Inhibition of constitutive NF-κB activity by IκBαM suppresses tumorigenesis. Oncogene 2003;22:1365-1370 (Pubitemid 36384598)
3. Arlt A, Vorndamm J, Muerkoster S, et al. Autocrine production of interleukin 1β confers constitutive nuclear factor κB activity and chemoresistance in pancreatic carcinoma cell lines. Cancer Res 2002;62:910-916 (Pubitemid 34126972)
4. Niu J, Li Z, Peng B, Chiao PJ. Identification of an autoregulatory feedback pathway involving interleukin-1α in induction of constitutive NF-κB activation in pancreatic cancer cells. J Biol Chem 2004;279:16452-16462 (Pubitemid 38509343)
5. Asano T, Yao Y, Zhu J, Li D, Abbruzzese JL, Reddy SA. The PI 3-kinase/Akt signaling pathway is activated due to aberrant Pten expression and targets transcription factors NF-κB and c-Myc in pancreatic cancer cells. Oncogene 2004;23:8571-8580 (Pubitemid 39576463)
6. Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 2003;3:859-868 (Pubitemid 37383716)
7. Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol 2002;4:E131-6. (Pubitemid 34521026)
8. Jochum W, Passegue E, Wagner EF. AP-1 in mouse development and tumorigenesis. Oncogene 2001;20:2401-2412 (Pubitemid 32531298)
9. Eferl R, Ricci R, Kenner L, et al. Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell 2003;112:181-192 (Pubitemid 36144108)
10. Mathas S, Hinz M, Anagnostopoulos I, et al. Aberrantly expressed c-Jun and JunB are a hallmark of Hodgkin lymphoma cells, stimulate proliferation and synergize with NF-κB. EMBO J 2002;21:4104-4113
11. Ferrara C, Tessari G, Poletti A, et al. Ki-67 and c-jun expression in pancreatic cancer: a prognostic marker? Oncol Rep 1999;6:1117-1122
12. Tessari G, Ferrara C, Poletti A, et al. The expression of proto-oncogene c-jun in human pancreatic cancer. Anticancer Res 1999;19:863-867 (Pubitemid 29168346)
13. Wakita K, Ohyanagi H,Yamamoto K, Tokuhisa T, Saitoh Y. Overexpression of c-Ki-ras and c-fos in human pancreatic carcinomas. Int J Pancreatol 1992;11:43-47
14. Murphy LO, Cluck MW, Lovas S, et al. Pancreatic cancer cells require an EGF receptor-mediated autocrine pathway for proliferation in serum-free conditions. Br J Cancer 2001;84:926-935 (Pubitemid 32385836)
15. Wagner M, Cao T, Lopez ME, et al. Expression of a truncated EGF receptor is associated with inhibition of pancreatic cancer cell growth and enhanced sensitivity to cisplatinum. Int J Cancer 1996;68:782-787 (Pubitemid 27062041)
16. Fralix KD, Zhao S, Venkatasubbarao K, Freeman JW. Rap1 reverses transcriptional repression of TGF-β type II receptor by a mechanism involving AP-1 in the human pancreatic cancer cell line, UK Pan-1. J Cell Physiol 2003;194:88-99. (Pubitemid 35424231)
17. Wisdom R, Johnson RS, Moore C. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J 1999;18:188-197 (Pubitemid 29005035)
18. Behrens A, Sibilia M, David JP, et al. Impaired postnatal hepatocyte proliferation and liver regeneration in mice lacking c-jun in the liver. EMBO J 2002;21:1782-1790 (Pubitemid 34614634)
19. Hilberg F, Aguzzi A, Howells N, Wagner EF. c-jun is essential for normal mouse development and hepatogenesis. Nature 1993;365:179-181 (Pubitemid 23282066)
20. Eferl R, Sibilia M, Hilberg F, et al. Functions of c-Jun in liver and heart development. J Cell Biol 1999;145:1049-1061 (Pubitemid 29270062)
21. Le-Niculescu H, Bonfoco E, Kasuya Y, Claret FX, Green DR, Karin M.Withdrawal of survival factors results in activation of the JNK pathway in neuronal cells leading to Fas ligand induction and cell death. Mol Cell Biol 1999;19:751-763 (Pubitemid 29018476)
22. Fujioka S, Niu J, Schmidt C, et al. NF-κB and AP-1 connection: mechanism of NF-κB-dependent regulation of AP-1 activity.Mol Cell Biol 2004;24:7806-7819
23. Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene 2001;20:2390-2400 (Pubitemid 32531297)
24. Chang F, Steelman LS, Lee JT, et al. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia 2003;17:1263-1293 (Pubitemid 36857335)
25. Dunn C, Wiltshire C, MacLaren A, Gillespie DA. Molecular mechanism and biological functions of c-Jun N-terminal kinase signalling via the c-Jun transcription factor. Cell Signal 2002;14:585-593 (Pubitemid 34304343)
26. Tiwari G, Sakaue H, Pollack JR, Roth RA. Gene expression profiling in prostate cancer cells with Akt activation reveals Fra-1 as an Akt-inducible gene. Mol Cancer Res 2003;1:475-484 (Pubitemid 36459258)
27. Boyle WJ, Smeal T, Defize LH, et al. Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell 1991;64:573-584 (Pubitemid 121002973)
28. de Groot RP, Auwerx J, Bourouis M, Sassone-Corsi P. Negative regulation of Jun/AP-1: conserved function of glycogen synthase kinase 3 and the Drosophila kinase shaggy. Oncogene 1993;8:841-847 (Pubitemid 23087414)
29. Morton S, Davis RJ, McLaren A, Cohen P. A reinvestigation of the multisite phosphorylation of the transcription factor c-Jun. EMBO J 2003;22:3876-3886 (Pubitemid 36975714)
30. Troussard AA, Tan C, Yoganathan TN, Dedhar S. Cell-extracellular matrix interactions stimulate the AP-1 transcription factor in an integrin-linked kinase- and glycogen synthase kinase 3-dependent manner. Mol Cell Biol 1999;19:7420-7427 (Pubitemid 29493405)
31. Wei W, Jin J, Schlisio S, Harper JW, Kaelin WG, Jr. The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin ligase. Cancer Cell 2005;8:25-33.
32. Salas TR, Reddy SA, Clifford JL, et al. Alleviating the suppression of glycogen synthase kinase-3β by Akt leads to the phosphorylation of cAMP-response element-binding protein and its transactivation in intact cell nuclei. J Biol Chem 2003;278:41338-41346 (Pubitemid 37280963)
33. Leaner VD, Donninger H, Ellis CA, Clark GJ, Birrer MJ. p75-Ras-GRF1 is a c-Jun/AP-1 target protein: its up regulation results in increased Ras activity and is necessary for c-Jun-induced nonadherent growth of Rat1a cells. Mol Cell Biol 2005;25:3324-3337 (Pubitemid 40464332)
34. Hettinger K, Vikhanskaya F, Poh MK, et al. c-Jun promotes cellular survival by suppression of PTEN. Cell Death Differ 2007;14:218-229 (Pubitemid 46092225)
35. Hirano T, Shino Y, Saito T, et al. Dominant negative MEKK1 inhibits survival of pancreatic cancer cells. Oncogene 2002;21:5923-5928
36. Asano T, Yao Y, Shin S, McCubrey J, Abbruzzese JL, Reddy SA. Insulin receptor substrate is a mediator of phosphoinositide 3-kinase activation in quiescent pancreatic cancer cells. Cancer Res 2005;65:9164-9168 (Pubitemid 41507979)
37. Ehlers RA, Zhang Y, Hellmich MR, Evers BM. Neurotensin-mediated activation of MAPK pathways and AP-1 binding in the human pancreatic cancer cell line, MIA PaCa-2. Biochem Biophys Res Commun 2000;269:704-708 (Pubitemid 30440365)
38. Besirli CG, Johnson EM, Jr. JNK-independent activation of c-Jun during neuronal apoptosis induced by multiple DNA-damaging agents. J Biol Chem 2003;278:22357-22366 (Pubitemid 36830285)
39. Naumann M, Bech-Otschir D, Huang X, Ferrell K, Dubiel W. COP9 signalosome- directed c-Jun activation/stabilization is independent of JNK. J Biol Chem 1999;274:35297-35300 (Pubitemid 129512813)
40. Coso OA, Montaner S, Fromm C, et al. Signaling from G protein-coupled receptors to the c-jun promoter involves the MEF2 transcription factor. Evidence for a novel c-jun amino-terminal kinase-independent pathway. J Biol Chem 1997;272:20691-20697 (Pubitemid 27355633)
41. Cruzalegui FH, Hardingham GE, Bading H. c-Jun functions as a calcium-regulated transcriptional activator in the absence of JNK/SAPK1 activation. EMBO J 1999;18:1335-1344 (Pubitemid 29110317)
42. Zanger K, Radovick S, Wondisford FE. CREB binding protein recruitment to the transcription complex requires growth factor-dependent phosphorylation of its GF box. Mol Cell 2001;7:551-558 (Pubitemid 32706347)
43. Zhang L, Xing G, Tie Y, et al. Role for the pleckstrin homology domain-containing protein CKIP-1 in AP-1 regulation and apoptosis. EMBO J 2005;24:766-778 (Pubitemid 40396106)
44. Piu F, Aronheim A, Katz S, Karin M. AP-1 repressor protein JDP-2: inhibition of UV-mediated apoptosis through p53 down-regulation. Mol Cell Biol 2001;21:3012-3024 (Pubitemid 32298369)
45. Palamarchuk A, Efanov A, Maximov V, Aqeilan RI, Croce CM, Pekarsky Y. Akt phosphorylates and regulates Pdcd4 tumor suppressor protein. Cancer Res 2005;65:11282-11286 (Pubitemid 41821683)
46. Minden A, Lin A, Claret FX, Abo A, Karin M. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 1995;81:1147-1157
47. Claret FX, Hibi M, Dhut S, Toda T, Karin M. A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 1996;383:453-457 (Pubitemid 26330837)
48. Lin A, Minden A, Martinetto H, et al. Identification of a dual specificity kinase that activates the Jun kinases and p38-2. Science 1995;268:286-290
49. Lamothe B, Besse A, Campos AD, Webster WK, Wu H, Darnay BG. Sitespecific Lys-63-linked tumor necrosis factor receptor-associated factor 6 auto-ubiquitination is a critical determinant of IêB kinase activation. J Biol Chem 2007;282:4102-4112 (Pubitemid 47084488)
50. Koul D, Yao Y, Abbruzzese JL, Yung WK, Reddy SA. Tumor suppressor MMAC/PTEN inhibits cytokine-induced NFêB activation without interfering with the IκB degradation pathway. J Biol Chem 2001;276:11402-11408 (Pubitemid 38089333)