Bile acid regulates MUC2 transcription in colon cancer cells via positive EGFR/PKC/Ras/ERK/CREB, PI3K/Akt/IκB/NF-κB and p38/MSK1/CREB pathways and negative JNK/c-Jun/AP-1 pathway

International Journal of Oncology

Volumn 36, Issue 4, 2010, Pages 941-953

  Lee, Hwa Young ^a,b   Crawley, Suzanne ^b   Hokari, Ryota ^b   Kwon, Sungwon ^b,c   Kim, Young S ^b,d  

^a CHA University   (South Korea)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Bundang CHA Hospital   (South Korea)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AP 1; Bile acid; Colon cancer; CREB; Deoxycholic acid; MUC2; Mucin; NF B; Signaling

Indexed keywords

BILE ACID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DEOXYCHOLIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MUCIN 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C JUN; PROTEIN KINASE C; RAS PROTEIN; RNA; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; COLON CANCER; CONTROLLED STUDY; DNA FLANKING REGION; GEL MOBILITY SHIFT ASSAY; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; PLASMID; PRIORITY JOURNAL; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSIENT TRANSFECTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; 5' FLANKING REGION; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DEOXYCHOLIC ACID; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; I-KAPPA B PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MUCIN-2; MUTATION; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-JUN; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SIGNAL TRANSDUCTION; SP1 TRANSCRIPTION FACTOR; TIME FACTORS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 77749342704     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo-00000573     Document Type: Article

References (53)

1. Thornton DJ, Rousseau K and McGuckin MA: Structure and function of the polymeric mucins in airway mucus. Annu Rev Physiol 70: 459-486, 2007.
2. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L and Hansson GC: The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci USA 105: 15064-15069, 2008.
3. Kim YS, Gum J and Brockhausen I: Mucin glycoproteins in neoplasia. Glycoconj J 13: 693-707, 1996.
4. Hollingsworth MA and Swanson BJ: Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 4: 45-60, 2004.
5. Andianifahanana M, Moniaux N and Batra SK: Regulation of mucin expression; mechanistic aspects and implications for cancer and inflammatory diseases. Biochim Biophys Acta 1765: 189-222, 2006.
6. Chang SK, Dohrman AF, Basbaum C, Ho SB, Toribara NW, Gum JR and Kim YS: Localization of mucins (MUC2 and MUC3) messenger RNA and peptide expression in human normal intestine and colon cancer. Gastroenterology 107: 28-36, 1994.
7. Gum JR, Byrd JC, Hicks JW, Toribara NW, Lamport DT and Kim YS: Molecular cloning of human intestinal mucin cDNAs: sequence analysis and evidence for genetic polymorphism. J Biol Chem 264: 6480-6487, 1989.
8. Monte MJ, Marin JJ, Antelo A and Vaszquez-Tato J: Bile acids: chemistry, physiology and pathophysiology. World J Gastroenterol 15: 804-816, 2009.
9. Reddy BS, Watababe K, Weisburger JH and Wynder EL: Promoting effect of bile acids in colorectal carcinogenesis in germ-free and conventional F344 rats. Cancer Res 37: 3238-3242, 1977.
10. Debruyne PR, Bruyneel EA, Li X, Zimber A, Gespach C and Mareel MM: The role of bile acids in carcinogenesis. Mutat Res 480-481: 359-369, 2001.
11. Jenkins DJ, Jenkins AL, Rao AV and Thompson LU: Cancer risk: possible protective role of high carbohydrate, high fiber diets. Am J Gastorenterol 81: 931-935, 1986.
12. Kishida T, Taguchi F, Feng L, Tatsuguchi A, Sato J, Fujimori S, Tachikawa H, Tamagawa Y, Yoshida Y and Kobayashi M: Analysis of bile acids in colon residual liquid or fecal material in patients with colorectal neoplasia and control subjects. J Gastroenterol 32: 306-311, 1997.
13. McMichael AJ and Potter JD: Host factors in carcinogenesis: certain bile acid metabolic profiles that selectively increase the risk of proximal colon cancer. J Natl Cancer Inst 75: 185-191, 1985.
14. Klinkspoor JH, Mok KS, Van Klinken BJ, Tytgat GNJ, Lee SP and Groen AK: Mucin secretion by the human colon cell line LS174T is regulated by bile salts. Glycobiology 9: 13-19, 1999.
15. Shekels LL, Lyftogt CT and Ho SB: Bile acid-induced alteration of mucin production in differentiated human colon cancer cell lines. Int J Biochem Cell Biol 28: 193-201, 1996.
16. Song S, Byrd JC, Koo JS and Bresalier RS: Bile acids induce MUC2 overexpression in human colon carcinoma cells. Cancer 103: 1606-1614, 2005.
17. Gum JR, Hicks JW and Kim YS: Identification and characterization of the MUC2 (human intestinal mucin) gene 5′-flanking region: promoter activity in cultured cells. Biochem J 325: 259-267, 1997.
18. Beauparlant P, Kwon H, Clarke M, Lin R, Sonenberg N, Wainberg M and Hiscott J: Transdominant mutants of IκBαblock Tat-tumor necrosis factor synergistic activation of human immunodeficiency virus type I gene expression and virus multiplication. J Virol 70: 5777-5785, 1996.
19. Lin X, Mu Y, Cunningham ET, Marcu KB, Geleziunas R and Greene WC: Molecular determinants of NF-κB-inducing kinase action. Mol Cell Biol 18: 5899-5907, 1998.
20. Li JD, Feng W, Gallup M, Kim JH, Gum J, Kim YS and Basbaum C: Activation of NF-kappaB via a Src-dependent Ras-MAPK-pp90rsk pathway is required for Pseudomonas aeruginosa-induced mucin overproduction in epithelial cells. Proc Natl Acad Sci USA 95: 5718-5723, 1998.
21. Shuto T, Xu H, Wang B, Han J, Kai H, Gu XX, Murphy TF, Lim DJ and Li JD: Activation of NF-kappa B by nontypeable Hemophilus influenzae is mediated by toll-like receptor 2-TAK 1-dependent NIK-IKK alpha/beta-I kappa B alpha and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc Natl Acad Sci USA 98: 8774-8779, 2001.
22. Walton KM, Rehfuss RP, Chrivia JC, Lochner JE and Goodman RH: A dominant repressor of cyclic adenosine 3′5′- monophosphate(cAMP)-regulated enhancer-binding protein activity inhibits the cAMP-mediated induction of the somatostatin promoter in vivo. Mol Endocrinol 6: 647-655, 1992.
23. Busca R, Abbe P, Mantoux F, Aberdam E, Peyssonnaux C, Eychen A, Ortonne JP and Ballotti R: Ras mediated the cAMPdependent activation of extracellular signal-regulated kinases (ERKs) in melanocytes. EMBO J 19: 2900-2910, 2000.
24. Brown PH, Chen TK and Birrer MJ: Mechanism of action of a dominant-negative mutant of c-Jun. Oncogene 9: 791-799, 1994.
25. Hashimoto Y, Jiang H, Niikura T, Ito Y, Hagiwara A, Umezawa K, YAbe Y, Murayama Y and Nishimoto I: Neural apoptosis by apolipoprotein E4 through low-density lipoprotein receptor-related protein and heterotrimeric GTPases. J Neurosci 20: 8401-8409, 2000.
26. Andrews NC and Faller DV: A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 19: 2499, 1991.
27. Hylemon PB, Zhou H, Pandak WP, Ren S, Gil G and Dent P: Bile acids as regulatory molecules. J Lipid Res 50: 1509-1520, 2009.
28. Lee HW, Ahn DH, Crawley SC, Li JD, Gum JR, Basbaum CB, Fan NQ, Szymkowski DE, Han SY, Lee BH, Sleisenger MH and Kim YS: Phorbol 12-myristate 13-acetate up-regulates the transcription of MUC2 intestinal mucin via Ras, ERK, and NF-kappa B. J Biol Chem 277: 32624-32631, 2002.
29. Roux PP and Blenis J: Erk and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344, 2001.
30. Vo N and Goodman RH: CREB-binding protein and P300 in transcriptional regulation. J Biol Chem 276: 13505-13508, 2001.
31. Ju JW, Kim SJ, Jun CD and Chun JS: p38 kinase and c-Jun N-terminal kinase oppositely regulates tumor necrosis factor alphainduced vascular cell adhesion molecule-1 expression and cell adhesion in chondrosarcoma cells. IUBMB Life 54: 293-299, 2002.
32. Chen G, Hitomi M, Han J and Stacey DW: The p38 pathway provides negative feedback for Ras proliferative signaling. J Biol Chem 275: 38973-38980, 2000.
33. Angel P and Karin M: The role of Jun, Fos and the AP-1 complex in cell proliferation and transformation. Biochim Biophys Acta 1072: 129-157, 1991.
34. Minden A, Lin A, Smeal T, Derijard B, Cobb M, Davis R and Karin M: c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogenactivated protein kinases. Mol Cell Biol 14: 6683-6688, 1994.
35. Nowak I, Seipel K, Schwarz M, Jans DA and Hemmings BA: Isolation of a cDNA and characterization of the 5′ flanking region of the gene encoding the type I regulatory subunit of the cAMP-dependent protein kinase. Eur J Biochem 167: 27-33, 1987.
36. Hess J, Angel P and Schorpp-Kistner M: AP-1 subunits: quarrel and harmony among siblings. J Cell Sci 117: 5965-5973, 2004.
37. Delgado M, Munoz-Elias EJ, Kan Y, Gozes I, Fridkin M, Brenneman DE, Gomariz RP and Ganea D: Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit tumor necrosis factor alpha transcriptional activation by regulation nuclear factor-κB and cAMP response element-binding protein/c-Jun. J Biol Chem 273: 31427-31436, 1998.
38. Rolo AP, Oliveira PJ, Moreno AJM and Palmeira CM: Bile acids affect liver mitochondrial bioenegetics: possible relevance for cholestasis therapy. Toxicol Sci 57: 177-185, 2000.
39. Lechner S, Muller-Ladner U, Schlotlmann K, Jung B, McClelland M, Rüschoff J, Welsh J, Schölmerich J and Kullmann F: Bile acids mimic oxidative stress induced upregulation of thioredoxin reductase in colon cancer cell lines. Carcinogenesis 23: 1281-1288, 2002.
40. Wang X, Martindale LL, Liu Y and Holbrook NJ: The cellular response to oxidative stress: influence of mitogent-activated protein kinase signaling pathway on cell survival: Biochem J 333: 291-300, 1998.
41. Summerton J, Flynn M, Cooke T and Talor I: Bile acid receptors in colorectal cancer. Br J Surg 70: 549-551, 1983.
42. Fischer EH, Charbonneau H and Tonks NK: Protein tyrosine phosphatase: a diverse family of intracellular and transmembrane enzymes. Science 253: 401-406, 1991.
43. Cheng K and Raufman JP: Bile acid-induced proliferation of a human colon cancer cell line is mediated by transactivation of epidermal growth factor receptors. Biochem Pharmacol 70: 1035-1047, 2005.
44. Bouwman P and Philipsen S: Regulation of the activity of Sp1-related transcription factors. Mol Cell Endocrinol 195: 27-38, 2002.
45. Prenzel N, Fischer OM, Streit S Hart S and Ullrich A: The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr Relat Cancer 8: 11-31, 2001.
46. Schlessinger J: Cell signaling by receptor tyrosine kinases. Cell 103: 211-225, 2000.
47. Qiao D, Chen W, Stratagoules ED and Martinez JD: Bile acid-induced activation of activator protein-1 requires both extracellular signal-regulated kinase and protein kinase C signaling. J Biol Chem 275: 15090-15098, 2000.
48. Looby E, Ling A, Kelleher D and Volkov Y: Bile acid deoxycholate induces different subcellular localization of the PKC isoenzymes beta1, epsilon and delta in colon epithelial cells in a sodium butyrate insensitive manner. Int J Cancer 114: 887-895, 2005.
49. Pomerance M, Abdullah HB, Kamerji S, Correze C and Blondeau JP: Thyroid-stimulating hormone and cyclic AMP activate p38 mitogen-activated protein kinase cascade. Involvement of pretein kinase A, rac 1, and reactive oxygen species. J Biol Chem 275: 40539-40546, 2000.
50. Sarkar FH, Li Y, Wang Z and Kong D: NF-κB signaling pathway and its therapeutic implication in human diseases. Int Rev Immunol 27: 293-319, 2008.
51. Gilmore TD: NF-κB: from basic research to human diseases. Oncogene 51: 6879-6899, 2006.
52. Jenkins GJS, Harries K, Doak SH, Wilmes A, Griffiths AP, Baxter JN and Parry JM: The bile acid deoxycholic acid (DCA) at neutral pH activates NF-κB and induces IL-8 expression in oesophageal cells in vitro. Carcinogenesis 25: 317-323, 2004.
53. Perkins ND: Integrating cell-signalling pathways with NF-κB and IKK function. Nat Rev Mol Cell Biol 8: 40-62, 2007.