Dual effect of butyrate on IL-1β-mediated intestinal epithelial cell inflammatory response

DNA and Cell Biology

Volumn 26, Issue 3, 2007, Pages 133-147

  Blais, Mylène ^a   Seidman, Ernest G ^b   Asselin, Claude ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID; INTERLEUKIN 1BETA; TRICHOSTATIN A;

ARTICLE; C3 GENE; CCL20 GENE; CONTROLLED STUDY; CRYPT CELL; CXCL11 GENE; CXCL5 GENE; CXCL8 GENE; DRUG EFFECT; ENTERITIS; GENE; GENE EXPRESSION REGULATION; GENE INDUCTION; HUMAN; HUMAN CELL; IL 1ALPHA GENE; IL 1BETA GENE; IL 6 GENE; INTESTINE EPITHELIUM CELL; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; REGULATORY MECHANISM; SAA2 GENE; TRANSIENT TRANSFECTION;

BINDING SITES; BUTYRATES; BUTYRIC ACIDS; CELLS, CULTURED; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-8; INTESTINAL MUCOSA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS (GENETICS); SERUM AMYLOID A PROTEIN; TRANSCRIPTION FACTORS;

EID: 34147120144     PISSN: 10445498     EISSN: None     Source Type: Journal    
DOI: 10.1089/dna.2006.0532     Document Type: Article

References (58)

1. ANDOH, A., FUJIYAMA, Y., ARAKI, K., TAKAYA, Y., SHIMADA, M., AND BAMBA, T. (1999). Counter-regulatory effect of sodium butyrate on tumor necrosis factor-alpha (TNF-alpha)-induced complement C3 and factor B biosynthesis in human intestinal epithelial cells. Clin. Exp. Immunol. 118, 23-29.
2. ANDOH, A., TSUJIKAWA, T., and FUJIYAMA, Y. (2003). Role of dietary fiber and short-chain fatty acids in the colon. Curr. Pharm. Des. 9, 347-358.
3. ARCHER, S., MENG, S., WU, J., JOHNSON, J., TANG R., and HODIN, R. (1998). Butyrate inhibits colon carcinoma cell growth through two distinct pathways. Surgery 124, 248-253.
4. BAGGIOLINI, M., DEWALD, B., and MOSER, B. (1994). Interleukin-8 and related chemotactic cytokines: CXC and CC chemokines. Adv. Immunol. 55, 97-179.
5. BARNARD, J.A., and WARWICK, G. (1997). Butyrate rapidly induces growth inhibition and differentiation in HT-29 cells. Cell. Growth. Differ. 4, 495-501.
6. BLAIS, M., DÉSILETS, A., and ASSELIN, C. (2005). Synergy between deacetylase inhibitors and IL-1beta in activation of the serum amyloid A2 gene promoter. DNA Cell. Biol. 24, 209-217.
7. BLOTTIÈRE, H.M., BUECHER, B., GALMICHE, J.P., and CHERBUT, C. (2003). Molecular analysis of the effect of short-chain fatty acids on intestinal cell proliferation. Proc. Nutr. Soc. 62, 101-106.
8. BOUMA, G., and STROBER, W. (2003). The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3, 521-533.
9. CHEN, L.F., and GREENE, W.C. (2003). Regulation of distinct biological activities of the NF-kappaB transcription factor complex by acetylation. J. Mol. Med. 81, 549-557.
10. CHEN, L.F., and GREENE, W.C. (2004). Shaping the nuclear action of NF-kappaB. Nat. Rev. Mol. Cell Biol. 5, 392-401.
11. COBRIN, G.M., and ABREU, M.T. (2005). Defects in mucosal immunity leading to Cronh's disease. Immunol. Rev. 206, 277-295.
12. DELLA RAGIONE, F., CRINITI, V., DELLA PIETRA, V., BORRIELLO, A., OLIVA, A., INDACO, S., YAMAMOTO, T., and ZAPPIA, V. (2001). Genes modulated by histone acetylation as new effectors of NaBu activity. FEBS Lett. 499, 199-204.
13. DÉSILETS, A., GHEORGHIU, I., YU, S.J., SEIDMAN, E.G., and ASSELIN, C. (2000). Inhibition by deacetylase inhibitors of IL-1-dependent induction of haptoglobin involves CCAAT/Enhancer-binding protein isoforms in intestinal epithelial cells. Biochem. Biophys. Res. Commun. 276, 673-679.
14. DINARELLO, C.A. (1994). The biological properties of interleukin-1. Eur. Cytokine Netw. 5, 517-531.
15. EBERHARTER, A., and BECKER, P.B. (2002). Histone acetylation: A switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep. 3, 224-229.
16. ESCAFFIT, F., PARE, F., GAUTHIER, R., RIVARD, N., BOUDREAU, F., and BEAULIEU, J.F. (2006). Cdx2 modulates proliferation in normal human intestinal epithelial crypt cells. Biochem. Biophys. Res. Commun. 342, 66-72.
17. FUSUNYAN, R.D., QUINN, J.J., FUJIMOTO, M., MACDERMOTT, R.P., and SANDERSON, I.R. (1999). Butyrate switches the pattern of chemokine secretion by intestinal epithelial cells through histone acetylation. Mol. Med. 5, 631-640.
18. GHEORGHIU, I., DESCHÊNES, C., BLAIS, M., BOUDREAU, F., RIVARD, N., and ASSELIN, C. (2001). Role of specific CCAAT/enhancer-binding protein isoforms in intestinal epithelial cells. J. Biol. Chem. 276, 44331-44337.
19. GROSS, V., ANDUS, T., DAIG, R., ASCHENBRENNER, E., SCHOLMERICH, J., and FALK, W. (1995). Regulation of interleukin-8 production in a human colon epithelial cell line (HT-29). Gastroenterology 108, 653-661.
20. HANADA, T., and YOSHIMURA, A. (2002). Regulation of cytokine signaling and inflammation. Cytokine Growth Factor Rev. 13, 413-421.
21. HASS, R., BUSCHE, R., LUCIANO, L., REALE, E., and ENGELHARDT, W.V. (1997). Lack of butyrate is associated with induction of Bax and subsequent apoptosis in the proximal colon of guinea pig. Gastroenterology 112, 875-881.
22. HUANG, N., KATZ, J.P., MARTIN, D.R., and WU, G.D. (1997). Inhibition of IL-8 gene expression in Caco-2 cells by compounds which induce histone hyperacetylation Cytokine 9, 27-36.
23. IACOMINO, G., TECCE, M.F., GRIMALDI, C., TOSTO, M., and RUSSO, G.L. (2001). Transcriptional response of a human colon adenocarcinoma cell line to sodium NaBu. Biochem. Biophys. Res. Commun. 285, 1280-1289.
24. INAN, M.S., RASOULPOUR, R.J., YIN, L., HUBBARD, A.K., ROSENBERG, D.W., and GIARDINA, C. (2000). The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line. Gastroenterology 118, 724-734.
25. JOBIN, C., HOLT, L., BRADHAM, C.A., STREETZ, K., BRENNER, D.A., and SARTOR, R.B. (1999). TNF receptor-associated factor-2 is involved in both IL-1 beta and TNF-alpha signaling cascades leading to NF-kappa B activation and IL-8 expression in human intestinal epithelial cells. J. Immunol. 162, 4447-4454.
26. KALINA, U., KOYAMA, N., HOSODA, T., NUERNBERGER, H., SATO, K., HOELZER, D., HERWECK, F., MANIGOLD, T., SINGER, M.V., ROSSOLM, S., et al. (2002). Enhanced production of IL-18 in butyrate-treated intestinal epithelium by stimulation of the proximal promoter region. Eur. J. Immunol. 32, 2635-2643.
27. KARANAM, S., and MORENO, C.S. (2004). CONFAC: Automated application of comparative genomic promoter analysis to DNA microarray datasets. Nucleic Acids Res. 32, 475-484.
28. LE, X., SHI, Q., WANG, B., XIONG, Q., QIAN, C., PENG, Z., LI, X.C., TANG, H., ABBRUZZESE, J.L., and XIE, K. (2000). Molecular regulation of constitutive expression of interleukin-8 in human pancreatic adenocarcinoma. J Interferon Cytokine Res. 20, 935-946.
29. LEMISCHKA, I.R., FARMER, S., RACANIELLO, V.R., and SHARP, P.A. (1981). Nucleotide sequence and evolution of a mammalian alpha-tubulin messenger RNA. J. Mol. Biol. 151, 101-120.
30. LEUNG, T.H., HOFFMANN, A., and BALTIMORE, D. (2004). One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimers. Cell 118, 453-464.
31. LUHRS, H., GERKE, T., SCHAUBER, J., DUSEL, G., MELCHER, R., SCHEPPACH, W., and MENZEL, T. (2001). Cytokine-activated degradation of inhibitory kappaB protein alpha is inhibited by the short-chain fatty acid butyrate. Int. J. Colorectal. Dis. 16, 195-201.
32. MARINKOVIC, S., and BAUMANN, H. (1990). Structure, hormonal regulation, and identification of the interleukin-6- and dexamethasone-responsive element of the rat haptoglobin gene. Mol. Cell. Biol. 10, 1573-1583.
33. MCBAIN, J.A., EASTMAN, A., NOBEL, C.S., and MUELLER, G.C. (1997). Apoptotic death in adenocarcinoma cell lines induced by butyrate and other histone deacetylase inhibitors. Biochem. Pharmacol. 53, 1357-1368.
34. MONTOUDIS, A., DELVIN, E., MENARD, D., BEAULIEU, J.F., JEAN, D., TREMBLAY, E., BENDAYAN, M., and LEVY, E. (2006). Intestinal-fatty acid binding protein and lipid transport in human intestinal epithelial cells. Biochem. Biophys. Res. Commun. 339, 248-254.
35. NIEDERAU, C., BACKMERHOFF, F., SCHUMACHER, B., and NIEDERAU, C. (1997). Inflammatory mediators and acute phase proteins in patients with Crohn's disease and ulcerative colitis. Hepatogastroenterology 44, 90-107.
36. OHNO, Y., LEE, J., FUSUNYAN, R.D., MACDERMOTT, R.P., and SANDERSON, I.R. (1997). Macrophage inflammatory protein-2: Chromosomal regulation in rat small intestinal epithelial cells. Proc. Natl. Acad. Sci. USA 94, 10279-10284.
37. PELLETIER, N., BOUDREAU, F., YU, S.J., ZANNONI, S., BOULANGER, V., and ASSELIN, C. (1998). Activation of haptoglobin gene expression by cAMP involves CCAAT/enhancer-binding protein isoforms in intestinal epithelial cells. FEBS Lett. 439, 275-280.
38. PERREAULT, N., and BEAULIEU, J.F. (1996). Use of the dissociating enzyme thermolysin to generate viable human normal intestinal epithelial cell cultures. Exp. Cell. Res. 224, 354-364.
39. PODOLSKY, D.K. (2002). Inflammatory bowel disease. N. Engl. J. Med. 347, 417-429.
40. POLI, V. (1998). The role of C/EBP isoforms in the control of inflammatory and native immunity functions. J. Biol. Chem. 273, 29279-29282.
41. QUIVY, V., and VAN LINT, C. (2004). Regulation at multiple levels of NF-kappaB-mediated transactivation by protein acetylation. Biochem. Pharmacol. 68, 1221-1229.
42. RUEMMELE, F.M., DIONNE, S., QURESHI, I., SARMA, D.S.R., LEVY, E., and SEIDMAN, E.G. (1999). Butyrate mediates Caco-2 cell apoptosis via upregulation of pro-apoptotic BAK and inducing caspase-3 mediated cleavage of poly- (ADP-ribose) polymerase (PARP). Cell Death Differ. 6, 729-735.
43. SACCANI, S., PANTANO, S., and NATOLI, G. (2001). Two waves of nuclear factor kappaB recruitment to target promoters. J. Exp. Med. 193, 1351-1359.
44. SARTOR, R.B. (2006). Mechanisms of disease: Pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3, 390-407.
45. SCHEPPACH, W., SOMMER, H., KIRCHNER, T., PAGANELLI, G.M., BARTRAM, P., CHRISTL, S., RICHTER, F., DUSEL, G., and KASPER, H. (1992). Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103, 51-56.
46. SCHMITZ, M.L., MATTIOLI, I., BUSS, H., and KRACHT, M. (2004). NF-kappaB: A multifaceted transcription factor regulated at several levels. Chembiochem. 5, 1348-1358.
47. SCHWARTZ, S., BEAULIEU, J.F., and RUEMMELE, F.M. (2005). Interleukin-17 is a potent immuno-modulator and regulator of normal human intestinal epithelial cell growth. Biochem. Biophys. Res. Commun. 337, 505-509.
48. SEGAIN, J.P., RAINGEARD, DE LA BLETIERE, D., BOURREILLE, A., LERAY, V., GERVOIS, N., ROSALES, C., FERRIER, L., BONNET, C., BLOTTIERE, H.M., and GALMICHE, J.P. (2000). Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 47, 397-403.
49. SIAVOSHIAN, S., BLOTTIÈRE, H.M., BENTOUIMOU, N., CHERBUT, C., and GALMICHE, J.P. (1996). Butyrate enhances major histocompatibility complex class I, HLA-DR and ICAM-1 antigen expression on differentiated human intestinal epithelial cells. Eur. J. Clin. Invest. 26, 803-810.
50. STEIN, B., RAHMSDORF, H.J., STEFFEN, A., LITFIN, M., and HERRLICH, P. (1989). UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothionein. Mol. Cell. Biol. 10, 5169-5181.
51. SUZUKI, H., GABRIELSON, E., CHEN, W., ANBAZHAGAN, R., VAN ENGELAND, M., WEIJENBERG, M.P., HERMAN, J.G., and BAYLIN, S.B. (2002). A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat. Genet. 31, 141-149.
52. TABUCHI, Y., ARAI, Y., KONDO, T., TAKEGUCHI, N., and ASANO, S. (2002). Identification of genes responsive to sodium NaBu in colonic epithelial cells. Biochem. Biophys. Res. Commun. 293, 1287-1294.
53. TIAN, B., NOWAK, D.E., and BRASIER, A.R. (2005). A TNF-induced gene expression program under oscillatory NF-kappaB control. BMC Genomics 6, 137.
54. TONG, X., YIN, L., and GIARDINA, C. (2004). Butyrate suppresses Cox-2 activation in colon cancer cells through HDAC inhibition. Biochem. Biophys. Res. Commun. 317, 463-471.
55. UHLAR, C.M., GREHAN, S., STEEL, D.M., STEINKASSERER, A., and WHITEHEAD, A.S. (1997). Use of the acute phase serum amyloid A2 (SAA2) gene promoter in the analysis of pro- and anti-inflammatory mediators: differential kinetics of SAA2 promoter induction by IL-1 beta and TNF-alpha compared to IL-6. J. Immunol. Methods 203, 123-130.
56. VREUGDENHIL, A.C., DENTENER, M.A., SNOEK, A.M., GREVE, J.W., and BUURMAN, W.A. (1999). Lipopolysaccharide binding protein and serum amyloid A secretion by human intestinal epithelial cells during the acute phase response. J. Immunol. 163, 2792-2798.
57. WU, G.D., LAI, E.J., HUANG, N., and WEN, X. (1997). Oct-1 and CCAAT/enhancer-binding protein (C/EBP) bind to overlapping elements within the interleukin-8 promoter. The role of Oct-1 as a transcriptional repressor. J. Biol. Chem. 272, 2396-2403.
58. WU, G.D., HUANG, N., WEN, X., KEILBAUGH, S.A., and YANG, H. (1999). 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, 1049-1056.