Butyrate suppresses Cox-2 activation in colon cancer cells through HDAC inhibition

Biochemical and Biophysical Research Communications

Volumn 317, Issue 2, 2004, Pages 463-471

  Tong, Xin ^a   Yin, Lei ^a,b   Giardina, Charles ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Butyrate; Colon cancer cells; Cox 2; p21; p38 MAP kinase; PGE 2; TNF ; Trichostatin A

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTINEOPLASTIC AGENT; BUTYRIC ACID; CYCLOHEXIMIDE; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; TRICHOSTATIN A; TSA; TUMOR NECROSIS FACTOR ALPHA;

ACETYLATION; ARTICLE; CELL STRAIN HT29; COLITIS; COLON ADENOCARCINOMA; COLON CARCINOGENESIS; CONTROLLED STUDY; DEACYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MESSENGER RNA SYNTHESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN STABILITY;

BUTYRATES; CELL LINE, TUMOR; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; ISOENZYMES; MEMBRANE PROTEINS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 1842531133     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2004.03.066     Document Type: Article

References (67)

1. Marnett L.J., DuBois R.N. COX-2: a target for colon cancer prevention. Annu. Rev. Pharmacol. Toxicol. 42:2002;55-80.
2. Turini M.E., DuBois R.N. Cyclooxygenase-2: a therapeutic target. Annu. Rev. Med. 53:2002;35-57.
3. Arakawa T., Higuchi K., Fukuda T., Fujiwara Y., Kobayashi K., Kuroki T. Prostaglandins in the stomach: an update. J. Clin. Gastroenterol. 27(Suppl. 1):1998;S1-S11.
4. Tsujii M., Kawano S., Tsuji S., Sawaoka H., Hori M., DuBois R.N. Cyclooxygenase regulates angiogenesis induced by colon cancer cells. Cell. 93:1998;705-716.
5. Smalley W.E., DuBois R.N. Colorectal cancer and nonsteroidal anti-inflammatory drugs. Adv. Pharmacol. 39:1997;1-20.
6. Tsujii M., DuBois R.N. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell. 83:1995;493-501.
7. Cao Y., Pearman A.T., Zimmerman G.A., McIntyre T.M., Prescott S.M. Intracellular unesterified arachidonic acid signals apoptosis. Proc. Natl. Acad. Sci. USA. 97:2000;11280-11285.
8. Cao Y., Prescott S.M. Many actions of cyclooxygenase-2 in cellular dynamics and in cancer. J. Cell. Physiol. 190:2002;279-286.
9. Videla S., Vilaseca J., Antolin M., Garcia-Lafuente A., Guarner F., Crespo E., Casalots J., Salas A., Malagelada J.R. Dietary inulin improves distal colitis induced by dextran sodium sulfate in the rat. Am. J. Gastroenterol. 96:2001;1486-1493.
10. Jacobasch G., Schmiedl D., Kruschewski M., Schmehl K. Dietary resistant starch and chronic inflammatory bowel diseases. Int. J. Colorectal. Dis. 14:1999;201-211.
11. Scheppach W., Sommer H., Kirchner T., Paganelli G.M., Bartram P., Christl S., Richter F., Dusel G., Kasper H. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology. 103:1992;51-56.
12. Butzner J.D., Parmar R., Bell C.J., Dalal V. Butyrate enema therapy stimulates mucosal repair in experimental colitis in the rat. Gut. 38:1996;568-573.
13. Gibson P., Rosella O. Interleukin 8 secretion by colonic crypt cells in vitro: response to injury suppressed by butyrate and enhanced in inflammatory bowel disease. Gut. 37:1995;536-543.
14. Augenlicht L.H., Mariadason J.M., Wilson A., Arango D., Yang W., Heerdt B.G., Velcich A. Short chain fatty acids and colon cancer. J. Nutr. 132:2002;3804S-3808S.
15. Archer S.Y., Hodin R.A. Histone acetylation and cancer. Curr. Opin. Genet. Dev. 9:1999;171-174.
16. Clausen M.R., Mortensen P.B. Kinetic studies on colonocyte metabolism of short chain fatty acids and glucose in ulcerative colitis. Gut. 37:1995;684-689.
17. Roediger W.E. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut. 21:1980;793-798.
18. Cummings J.H. Colonic absorption: the importance of short chain fatty acids in man. Scand. J. Gastroenterol. Suppl. 93:1984;89-99.
19. Ruppin H., Bar-Meir S., Soergel K.H., Wood C.M., Schmitt M.G. Jr. Absorption of short-chain fatty acids by the colon. Gastroenterology. 78:1980;1500-1507.
20. Luhrs H., Gerke T., Schauber J., Dusel G., Melcher R., Scheppach W., Menzel T. Cytokine-activated degradation of inhibitory kappaB protein alpha is inhibited by the short-chain fatty acid butyrate. Int. J. Colorectal. Dis. 16:2001;195-201.
21. Yin L., Laevsky G., Giardina C. Butyrate suppression of colonocyte NF-kappa B activation and cellular proteasome activity. J. Biol. Chem. 276:2001;44641-44646.
22. Luhrs H., Gerke T., Boxberger F., Backhaus K., Melcher R., Scheppach W., Menzel T. Butyrate inhibits interleukin-1-mediated nuclear factor-kappa B activation in human epithelial cells. Dig. Dis. Sci. 46:2001;1968-1973.
23. Segain J.P., Raingeard de la Bletiere D., Bourreille A., Leray V., Gervois N., Rosales C., Ferrier L., Bonnet C., Blottiere H.M., Galmiche J.P. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut. 47:2000;397-403.
24. Inan M.S., Rasoulpour R.J., Yin L., Hubbard A.K., Rosenberg D.W., Giardina C. The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line. Gastroenterology. 118:2000;724-734.
25. Wu G.D., Huang N., Wen X., Keilbaugh S.A., Yang H. High-level expression of I kappa B-beta in the surface epithelium of the colon: in vitro evidence for an immunomodulatory role. J. Leukoc. Biol. 66:1999;1049-1056.
26. Gilmore T.D., Koedood M., Piffat K.A., White D.W. Rel/NF-kappaB/IkappaB proteins and cancer. Oncogene. 13:1996;1367-1378.
27. LaCasse E.C., Baird S., Korneluk R.G., MacKenzie A.E. The inhibitors of apoptosis (IAPs) and their emerging role in cancer. Oncogene. 17:1998;3247-3259.
28. Yamamoto Y., Gaynor R.B. Therapeutic potential of inhibition of the NF-kappaB pathway in the treatment of inflammation and cancer. J. Clin. Invest. 107:2001;135-142.
29. Chen L., Fischle W., Verdin E., Greene W.C. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science. 293:2001;1653-1657.
30. Sterner D.E., Berger S.L. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64:2000;435-459.
31. Gu W., Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell. 90:1997;595-606.
32. Blobel G.A. CREB-binding protein and p300: molecular integrators of hematopoietic transcription. Blood. 95:2000;745-755.
33. Boyes J., Byfield P., Nakatani Y., Ogryzko V. Regulation of activity of the transcription factor GATA-1 by acetylation. Nature. 396:1998;594-598.
34. Ristimaki A., Garfinkel S., Wessendorf J., Maciag T., Hla T. Induction of cyclooxygenase-2 by interleukin-1 alpha. Evidence for post-transcriptional regulation. J. Biol. Chem. 269:1994;11769-11775.
35. ′ -untranslated region J. Biol. Chem. 275:2000;11750-11757.
36. Ramsay R.G., Ciznadija D., Vanevski M., Mantamadiotis T. Transcriptional regulation of cyclo-oxygenase expression: three pillars of control. Int. J. Immunopathol. Pharmacol. 16:2003;59-67.
37. Gorgoni B., Caivano M., Arizmendi C., Poli V. The transcription factor C/EBPbeta is essential for inducible expression of the cox-2 gene in macrophages but not in fibroblasts. J. Biol. Chem. 276:2001;40769-40777.
38. Kanekura T., Goorha S., Kirtikara K., Ballou L.R. The involvement of NF-kappaB in the constitutive overexpression of cyclooxygenase-2 in cyclooxygenase-1 null cells. Biochim. Biophys. Acta. 1542:2002;14-22.
39. Thomas B., Berenbaum F., Humbert L., Bian H., Bereziat G., Crofford L., Olivier J.L. Critical role of C/EBPdelta and C/EBPbeta factors in the stimulation of the cyclooxygenase-2 gene transcription by interleukin-1beta in articular chondrocytes. Eur. J. Biochem. 267:2000;6798-6809.
40. Chen C.C., Sun Y.T., Chen J.J., Chiu K.T. TNF-alpha-induced cyclooxygenase-2 expression in human lung epithelial cells: involvement of the phospholipase C-gamma 2, protein kinase C-alpha, tyrosine kinase, NF-kappa B-inducing kinase, I-kappa B kinase 1/2 pathway. J. Immunol. 165:2000;2719-2728.
41. Wadleigh D.J., Reddy S.T., Kopp E., Ghosh S., Herschman H.R. Transcriptional activation of the cyclooxygenase-2 gene in endotoxin-treated RAW 264.7 macrophages. J. Biol. Chem. 275:2000;6259-6266.
42. Jang B.C., Munoz-Najar U., Paik J.H., Claffey K., Yoshida M., Hla T. Leptomycin B, an inhibitor of the nuclear export receptor CRM1, inhibits COX-2 expression. J. Biol. Chem. 278:2003;2773-2776.
43. Dean J.L., Brook M., Clark A.R., Saklatvala J. p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes. J. Biol. Chem. 274:1999;264-269.
44. Ridley S.H., Dean J.L., Sarsfield S.J., Brook M., Clark A.R., Saklatvala J. A p38 MAP kinase inhibitor regulates stability of interleukin-1-induced cyclooxygenase-2 mRNA. FEBS Lett. 439:1998;75-80.
45. Hinnebusch B.F., Meng S., Wu J.T., Archer S.Y., Hodin R.A. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J. Nutr. 132:2002;1012-1017.
46. Siavoshian S., Segain J.P., Kornprobst M., Bonnet C., Cherbut C., Galmiche J.P., Blottiere H.M. Butyrate and trichostatin A effects on the proliferation/differentiation of human intestinal epithelial cells: induction of cyclin D3 and p21 expression. Gut. 46:2000;507-514.
47. Mariadason J.M., Corner G.A., Augenlicht L.H. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, curcumin and implications for chemoprevention of colon cancer. Cancer Res. 60:2000;4561-4572.
48. Vigushin D.M., Coombes R.C. Histone deacetylase inhibitors in cancer treatment. Anticancer Drugs. 13:2002;1-13.
49. Momparler R.L. Cancer epigenetics. Oncogene. 22:2003;6479-6483.
50. Richon V.M., Sandhoff T.W., Rifkind R.A., Marks P.A. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc. Natl. Acad. Sci. USA. 97:2000;10014-10019.
51. Sambucetti L.C., Fischer D.D., Zabludoff S., Kwon P.O., Chamberlin H., Trogani N., Xu H., Cohen D. Histone deacetylase inhibition selectively alters the activity and expression of cell cycle proteins leading to specific chromatin acetylation and antiproliferative effects. J. Biol. Chem. 274:1999;34940-34947.
52. Guan Z., Baier L.D., Morrison A.R. p38 mitogen-activated protein kinase down-regulates nitric oxide and up-regulates prostaglandin E2 biosynthesis stimulated by interleukin-1beta. J. Biol. Chem. 272:1997;8083-8089.
53. Ramsay R.G., Friend A., Vizantios Y., Freeman R., Sicurella C., Hammett F., Armes J., Venter D. Cyclooxygenase-2, a colorectal cancer nonsteroidal anti-inflammatory drug target, is regulated by c-MYB. Cancer Res. 60:2000;1805-1809.
54. Araki Y., Okamura S., Hussain S.P., Nagashima M., He P., Shiseki M., Miura K., Harris C.C. Regulation of cyclooxygenase-2 expression by the Wnt and ras pathways. Cancer Res. 63:2003;728-734.
55. Dixon D.A., Tolley N.D., King P.H., Nabors L.B., McIntyre T.M., Zimmerman G.A., Prescott S.M. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest. 108:2001;1657-1665.
56. ′ -untranslated region of murine cyclooxygenase-2 contains multiple regulatory elements that alter message stability and translational efficiency J. Biol. Chem. 276:2001;23179-23185.
57. Jang B.C., Sanchez T., Schaefers H.J., Trifan O.C., Liu C.H., Creminon C., Huang C.K., Hla T. Serum withdrawal-induced post-transcriptional stabilization of cyclooxygenase-2 mRNA in MDA-MB-231 mammary carcinoma cells requires the activity of the p38 stress-activated protein kinase. J. Biol. Chem. 275:2000;39507-39515.
58. Cok S.J., Acton S.J., Sexton A.E., Morrison A.R. Identification of RNA binding proteins in RAW 264.7 cells that recognize an LPS responsive element in the 3-UTR of the murine COX-2 mRNA. J. Biol. Chem. 2003.
59. Sengupta S., Jang B.C., Wu M.T., Paik J.H., Furneaux H., Hla T. The RNA-binding protein HuR regulates the expression of cyclooxygenase-2. J. Biol. Chem. 278:2003;25227-25233.
60. Sully G., Dean J.L., Wait R., Rawlinson L., Santalucia T., Saklatvala J., Clark A.R. Structural and functional dissection of a conserved destabilizing element of cyclo-oxygenase-2 mRNA: evidence against the involvement of AUF-1 [AU-rich element/poly(U)-binding/degradation factor-1], AUF-2, tristetraprolin, HuR (Hu antigen R) or FBP1 (far-upstream-sequence-element-binding protein 1). Biochem. J. 377:2004;629-639.
61. Dixon D.A., Balch G.C., Kedersha N., Anderson P., Zimmerman G.A., Beauchamp R.D., Prescott S.M. Regulation of cyclooxygenase-2 expression by the translational silencer TIA-1. J. Exp. Med. 198:2003;475-481.
62. Vernia P., Marcheggiano A., Caprilli R., Frieri G., Corrao G., Valpiani D., Di Paolo M.C., Paoluzi P., Torsoli A. Short-chain fatty acid topical treatment in distal ulcerative colitis. Aliment. Pharmacol. Ther. 9:1995;309-313.
63. Vernia P., Cittadini M., Caprilli R., Torsoli A. Topical treatment of refractory distal ulcerative colitis with 5-ASA and sodium butyrate. Dig. Dis. Sci. 40:1995;305-307.
64. Steinhart A.H., Brzezinski A., Baker J.P. Treatment of refractory ulcerative proctosigmoiditis with butyrate enemas. Am. J. Gastroenterol. 89:1994;179-183.
65. Ogawa H., Rafiee P., Fisher P.J., Johnson N.A., Otterson M.F., Binion D.G. Butyrate modulates gene and protein expression in human intestinal endothelial cells. Biochem. Biophys. Res. Commun. 309:2003;512-519.
66. Kamitani H., Geller M., Eling T. Expression of 15-lipoxygenase by human colorectal carcinoma Caco-2 cells during apoptosis and cell differentiation. J. Biol. Chem. 273:1998;21569-21577.
67. Crew T.E., Elder D.J., Paraskeva C. A cyclooxygenase-2 (COX-2) selective non-steroidal anti-inflammatory drug enhances the growth inhibitory effect of butyrate in colorectal carcinoma cells expressing COX-2 protein: regulation of COX-2 by butyrate. Carcinogenesis. 21:2000;69-77.