Mutant K-Ras increases GSK-3Β gene expression via an ETS-p300 transcriptional complex in pancreatic cancer

Oncogene

Volumn 30, Issue 34, 2011, Pages 3705-3715

  Zhang, J S ^a   Koenig, A ^a,b   Harrison, A ^a   Ugolkov, A V ^a,d   Fernandez Zapico, M E ^a   Couch, F J ^c   Billadeau, D D ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c MAYO CLINIC   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

ETS; GSK 3 ; K Ras; MAPK; pancreatic cancer

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; HISTONE ACETYLTRANSFERASE PCAF; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CANCER MODEL; CHROMATIN; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; ONCOGENE K RAS; PANCREAS CANCER; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; GENES, RAS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOHISTOCHEMISTRY; MAP KINASE SIGNALING SYSTEM; MICE; MICE, TRANSGENIC; MUTATION; P300-CBP TRANSCRIPTION FACTORS; PANCREATIC NEOPLASMS; PROMOTER REGIONS, GENETIC; RNA-BINDING PROTEIN EWS; TRANSCRIPTION, GENETIC;

EID: 80052052253     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.90     Document Type: Article

References (47)

1. Arvand A, Denny CT. (2001). Biology of EWS/ETS fusions in Ewing0s family tumors. Oncogene 20: 5747-5754. (Pubitemid 32928112)
2. Bilim V, Ougolkov A, Yuuki K, Naito S, Kawazoe H, Muto A et al. (2009). Glycogen synthase kinase-3: a new therapeutic target in renal cell carcinoma. Br J Cancer 101: 2005-2014.
3. Billadeau DD. (2007). Primers on molecular pathways. The glycogen synthase kinase-3beta. Pancreatology 7: 398-402. (Pubitemid 47587617)
4. Cao Q, Lu X, Feng YJ. (2006). Glycogen synthase kinase-3beta positively regulates the proliferation of human ovarian cancer cells. Cell Res 16: 671-677. (Pubitemid 44091443)
5. Clark JP, Cooper CS. (2009). ETS gene fusions in prostate cancer. Nat Rev Urol 6: 429-439.
6. Daujat S, Bauer M, Shah V, Turner B, Berger S, Kouzarides T. (2002). Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr Biol 12: 2090-2097. (Pubitemid 36021886)
7. Deramaudt T, Rustgi AK. (2005). Mutant KRAS in the initiation of pancreatic cancer. Biochim Biophys Acta 1756: 97-101. (Pubitemid 41773136)
8. Downward J. (2003). Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3: 11-22. (Pubitemid 37328883)
9. Fauquette V, Perrais M, Cerulis S, Jonckheere N, Ducourouble MP, Aubert JP et al. (2005). The antagonistic regulation of human MUC4 and ErbB-2 genes by the Ets protein PEA3 in pancreatic cancer cells: implications for the proliferation/differentiation balance in the cells. Biochem J 386: 35-45. (Pubitemid 40289222)
10. Foulds CE, Nelson ML, Blaszczak AG, Graves BJ. (2004). Ras/mitogen-activated protein kinase signaling activates Ets-1 and Ets-2 by CBP/p300 recruitment. Mol Cell Biol 24: 10954-10964. (Pubitemid 39603149)
11. Gutierrez-Hartmann A, Duval DL, Bradford AP. (2007). ETS transcription factors in endocrine systems. Trends Endocrinol Metab 18: 150-158. (Pubitemid 46629025)
12. Hezel AF, Kimmelman AC, Stanger BZ, Bardeesy N, Depinho RA. (2006). Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev 20: 1218-1249. (Pubitemid 43727584)
13. Hollenhorst PC, Jones DA, Graves BJ. (2004). Expression profiles frame the promoter specificity dilemma of the ETS family of transcription factors. Nucleic Acids Res 32: 5693-5702. (Pubitemid 39545685)
14. Hollenhorst PC, Shah AA, Hopkins C, Graves BJ. (2007). Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev 21: 1882-1894. (Pubitemid 47204928)
15. Ito H, Duxbury M, Benoit E, Clancy TE, Zinner MJ, Ashley SW et al. (2004). Prostaglandin E2 enhances pancreatic cancer invasiveness through an Ets-1-dependent induction of matrix metalloproteinase-2. Cancer Res 64: 7439-7446. (Pubitemid 39372086)
16. Ito T, Nakayama T, Ito M, Naito S, Kanematsu T, Sekine I. (1998). Expression of the ets-1 proto-oncogene in human pancreatic carcinoma. Mod Pathol 11: 209-215. (Pubitemid 28144158)
17. Ito Y, Miyoshi E, Takeda T, Sakon M, Ihara S, Tsujimoto M et al. (2002). Ets-2 overexpression contributes to progression of pancreatic adenocarcinoma. Oncol Rep 9: 853-857.
18. Janknecht R. (2005). EWS-ETS oncoproteins: the linchpins of Ewing tumors. Gene 363: 1-14. (Pubitemid 41691887)
19. Jayaraman G, Srinivas R, Duggan C, Ferreira E, Swaminathan S, Somasundaram K et al. (1999). p300/cAMP-responsive element-binding protein interactions with ets-1 and ets-2 in the transcrip-tional activation of the human stromelysin promoter. J Biol Chem 274: 17342-17352.
20. Jedlicka P, Gutierrez-Hartmann A. (2008). Ets transcription factors in intestinal morphogenesis, homeostasis and disease. Histol Histo-pathol 23: 1417-1424.
21. Jope RS, Johnson GV. (2004). The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29: 95-102. (Pubitemid 38186580)
22. Kim EK, Choi EJ. (2010). Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 1802: 396-405.
23. Kobberup S, Nyeng P, Juhl K, Hutton J, Jensen J. (2007). ETS-family genes in pancreatic development. Dev Dyn 236: 3100-3110. (Pubitemid 350175007)
24. Koenig A, Linhart T, Schlengemann K, Reutlinger K, Wegele J, Adler G et al. (2010). NFAT-induced histone acetylation relay switch promotes c-Myc-dependent growth in pancreatic cancer cells. Gastroenterology 138: 1189-1199.
25. Kotliarova S, Pastorino S, Kovell LC, Kotliarov Y, Song H, Zhang W et al. (2008). Glycogen synthase kinase-3 inhibition induces glioma cell death through c-MYC, nuclear factor-kappaB, and glucose regulation. Cancer Res 68: 6643-6651.
26. Lau KF, Miller CC, Anderton BH, Shaw PC. (1999a). Molecular cloning and characterization of the human glycogen synthase kinase-3beta promoter. Genomics 60: 121-128. (Pubitemid 29463670)
27. Lau KF, Miller CC, Anderton BH, Shaw PC. (1999b). Expression analysis of glycogen synthase kinase-3 in human tissues. J Pept Res 54: 85-91. (Pubitemid 29334091)
28. Lefter LP, Dima S, Sunamura M, Furukawa T, Sato Y, Abe M et al. (2009). Transcriptional silencing of ETS-1 efficiently suppresses angiogenesis of pancreatic cancer. Cancer Gene Ther 16: 137-148.
29. Li QJ, Yang SH, Maeda Y, Sladek FM, Sharrocks AD, Martins-Green M. (2003a). MAP kinase phosphorylation-dependent activation of Elk-1 leads to activation of the co-activator p300. EMBO J 22: 281-291. (Pubitemid 36119434)
30. Li R, Erdamar S, Dai H, Sayeeduddin M, Frolov A, Wheeler TM et al. (2009b). Cytoplasmic accumulation of glycogen synthase kinase-3beta is associated with aggressive clinicopathological features in human prostate cancer. Anticancer Res 29: 2077-2081.
31. Li YY, Wu Y, Tsuneyama K, Baba T, Mukaida N. (2009). Essential contribution of Ets-1 to constitutive Pim-3 expression in human pancreatic cancer cells. Cancer Sci 100: 396-404.
32. Luo J. (2009). Glycogen synthase kinase 3beta (GSK3beta) in tumori-genesis and cancer chemotherapy. Cancer Lett 273: 194-200.
33. Maitra A, Kern SE, Hruban RH. (2006). Molecular pathogenesis of pancreatic cancer. Best Pract Res Clin Gastroenterol 20: 211-226.
34. Narod SA, Seth A, Nam R. (2008). Fusion in the ETS gene family and prostate cancer. Br J Cancer 99: 847-851.
35. Nelson ML, Kang HS, Lee GM, Blaszczak AG, Lau DK, McIntosh LP et al. (2010). Ras signaling requires dynamic properties of Ets1 for phosphorylation-enhanced binding to coactivator CBP. Proc Natl Acad Sci USA 107: 10026-10031.
36. Ougolkov AV, Fernandez-Zapico ME, Bilim VN, Smyrk TC, Chari ST, Billadeau DD. (2006). Aberrant nuclear accumulation of glycogen synthase kinase-3beta in human pancreatic cancer: association with kinase activity and tumor dedifferentiation. Clin Cancer Res 12: 5074-5081. (Pubitemid 44453333)
37. 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. (Pubitemid 40490111)
38. Polakis P. (2000). Wnt signaling and cancer. Genes Dev 14: 1837-1851. (Pubitemid 30639518)
39. Rowley M, Ohashi A, Mondal G, Mills L, Yang L, Zhang L et al. (2011). Inactivation of Brca2 promotes Trp53-associated but inhibits KrasG12D-dependent pancreatic cancer development in mice. Gastroenterology (e-pub ahead of print 14 March 2011).
40. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. (1996). Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272: 1023-1026. (Pubitemid 26259322)
41. Shakoori A, Ougolkov A, Yu ZW, Zhang B, Modarressi MH, Billadeau DD et al. (2005). Deregulated GSK3beta activity in colorectal cancer: its association with tumor cell survival and proliferation. Biochem Biophys Res Commun 334: 1365-1373. (Pubitemid 41074725)
42. Tootle TL, Rebay I. (2005). Post-translational modifications influence transcription factor activity: a view from the ETS superfamily. Bioessays 27: 285-298. (Pubitemid 40476491)
43. Wai PY, Mi Z, Gao C, Guo H, Marroquin C, Kuo PC. (2006). Ets-1 and runx2 regulate transcription of a metastatic gene, osteopontin, in murine colorectal cancer cells. J Biol Chem 281: 18973-18982. (Pubitemid 44035400)
44. Wasylyk B, Hagman J, Gutierrez-Hartmann A. (1998). Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem Sci 23: 213-216. (Pubitemid 28302618)
45. Yang B, Hauser C, Henkel G, Colman M, Van Beveren C, Stacey K et al. (1996). Ras-mediated phosphorylation of a conserved threonine residue enhances the transactivation activities of c-Ets1 and c-Ets2. Mol Cell Biol 16: 538-547. (Pubitemid 26029092)
46. Yang C, Shapiro LH, Rivera M, Kumar A, Brindle PK. (1998). A role for CREB binding protein and p300 transcriptional coactivators in Ets-1 transactivation functions. Mol Cell Biol 18: 2218-2229. (Pubitemid 28152670)
47. Zhang JS, Moncrieffe MC, Kaczynski J, Ellenrieder V, Prendergast FG, Urrutia R. (2001). A conserved alpha-helical motif mediates the interaction of Sp1-like transcriptional repressors with the corepres-sor mSin3A. Mol Cell Biol 21: 5041-5049. (Pubitemid 32656401)