Butyrate Induces Intestinal Sodium Absorption via Sp3-Mediated Transcriptional Up-Regulation of Epithelial Sodium Channels

Gastroenterology

Volumn 132, Issue 1, 2007, Pages 236-248

  Zeissig, Sebastian ^a   Fromm, Anja ^a   Mankertz, Joachim ^a   Weiske, Jörg ^a   Zeitz, Martin ^a   Fromm, Michael ^a   Schulzke, Jörg Dieter ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; BUTYRIC ACID; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; PREGNANCY ASSOCIATED ALPHA2 GLYCOPROTEIN; PROPIONIC ACID; SHORT CHAIN FATTY ACID; SODIUM; SODIUM CHANNEL; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3;

ARTICLE; BINDING AFFINITY; CELL MEMBRANE; CELL STRAIN HT29; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME SYNTHESIS; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INTESTINE ABSORPTION; INTESTINE FLORA; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SODIUM ABSORPTION; SODIUM TRANSPORT; TRANSCRIPTION REGULATION; UPREGULATION;

EID: 33846253247     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2006.10.033     Document Type: Article

References (59)

1. Garty H., and Palmer L.G. Epithelial sodium channels: function, structure, and regulation. Physiol Rev 77 (1997) 359-396
2. Snyder P.M. Minireview: regulation of epithelial Na+ channel trafficking. Endocrinology 146 (2005) 5079-5085
3. Kamynina E., and Staub O. Concerted action of ENaC, Nedd4-2, and Sgk1 in transepithelial Na(+) transport. Am J Physiol Renal Physiol 283 (2002) F377-F387
4. Epple H.J., Amasheh S., Mankertz J., Goltz M., Schulzke J.D., and Fromm M. Early aldosterone effect in distal colon by transcriptional regulation of ENaC subunits. Am J Physiol Gastrointest Liver Physiol 278 (2000) G718-G724
5. Volk K.A., Sigmund R.D., Snyder P.M., McDonald F.J., Welsh M.J., and Stokes J.B. rENaC is the predominant Na+ channel in the apical membrane of the rat renal inner medullary collecting duct. J Clin Invest 96 (1995) 2748-2757
6. Schultheis P.J., Clarke L.L., Meneton P., Miller M.L., Soleimani M., Gawenis L.R., Riddle T.M., Duffy J.J., Doetschman T., Wang T., Giebisch G., Aronson P.S., Lorenz J.N., and Shull G.E. Renal and intestinal absorptive defects in mice lacking the NHE3 Na+/H+ exchanger. Nat Genet 19 (1998) 282-285
7. Amasheh S., Barmeyer C., Koch C.S., Tavalali S., Mankertz J., Epple H.J., Gehring M.M., Florian P., Kroesen A.J., Zeitz M., Fromm M., and Schulzke J.D. Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcerative colitis. Gastroenterology 126 (2004) 1711-1720
8. Young G.P., Hu Y., Le Leu R.K., and Nyskohus L. Dietary fibre and colorectal cancer: a model for environment-gene interactions. Mol Nutr Food Res 49 (2005) 571-584
9. Roediger W.E., Heyworth M., Willoughby P., Piris J., Moore A., and Truelove S.C. Luminal ions and short chain fatty acids as markers of functional activity of the mucosa in ulcerative colitis. J Clin Pathol 35 (1982) 323-326
10. Hague A., Manning A.M., Hanlon K.A., Huschtscha L.I., Hart D., and Paraskeva C. Sodium butyrate induces apoptosis in human colonic tumour cell lines in a p53-independent pathway: implications for the possible role of dietary fibre in the prevention of large-bowel cancer. Int J Cancer 55 (1993) 498-505
11. Heerdt B.G., Houston M.A., and Augenlicht L.H. Potentiation by specific short-chain fatty acids of differentiation and apoptosis in human colonic carcinoma cell lines. Cancer Res 54 (1994) 3288-3293
12. Scheppach W., Sommer H., Kirchner T., Paganelli G.M., Bartram P., Christl S., Richter F., Dusel G., and Kasper H. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103 (1992) 51-56
13. Steinhart A.H., Brzezinski A., and Baker J.P. Treatment of refractory ulcerative proctosigmoiditis with butyrate enemas. Am J Gastroenterol 89 (1994) 179-183
14. Mariadason J.M., Corner G.A., and Augenlicht L.H. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res 60 (2000) 4561-4572
15. Della Ragione F., Criniti V., Della Pietra V., Borriello A., Oliva A., Indaco S., Yamamoto T., and Zappia V. Genes modulated by histone acetylation as new effectors of butyrate activity. FEBS Lett 499 (2001) 199-204
16. Cuff M.A., and Shirazi-Beechey S.P. The importance of butyrate transport to the regulation of gene expression in the colonic epithelium. Biochem Soc Trans 32 (2004) 1100-1102
17. Bugaut M. Occurrence, absorption and metabolism of short chain fatty acids in the digestive tract of mammals. Comp Biochem Physiol B 86 (1987) 439-472
18. Binder H.J., and Mehta P. Short-chain fatty acids stimulate active sodium and chloride absorption in vitro in the rat distal colon. Gastroenterology 96 (1989) 989-996
19. Musch M.W., Bookstein C., Xie Y., Sellin J.H., and Chang E.B. SCFA increase intestinal Na absorption by induction of NHE3 in rat colon and human intestinal C2/bbe cells. Am J Physiol Gastrointest Liver Physiol 280 (2001) G687-G693
20. Vidyasagar S., and Ramakrishna B.S. Effects of butyrate on active sodium and chloride transport in rat and rabbit distal colon. J Physiol 539 (2002) 163-173
21. Krishnan S., Rajendran V.M., and Binder H.J. Apical NHE isoforms differentially regulate butyrate-stimulated Na absorption in rat distal colon. Am J Physiol Cell Physiol 285 (2003) C1246-C1254
22. Kiela P.R., Hines E.R., Collins J.F., and Ghishan F.K. Regulation of the rat NHE3 gene promoter by sodium butyrate. Am J Physiol Gastrointest Liver Physiol 281 (2001) G947-G956
23. Kunzelmann K., Kathofer S., Hipper A., Gruenert D.C., and Gregner R. Culture-dependent expression of Na+ conductances in airway epithelial cells. Pflugers Arch 431 (1996) 578-586
24. Kreusel K.M., Fromm M., Schulzke J.D., and Hegel U. Cl- secretion in epithelial monolayers of mucus-forming human colon cells (HT-29/B6). Am J Physiol 261 (1991) C574-C582
25. Zeissig S., Fromm A., Mankertz J., Zeitz M., Fromm M., and Schulzke J.D. Restoration of ENaC expression by glucocorticoid receptor transfection in human HT-29/B6 colon cells. Biochem Biophys Res Commun 344 (2006) 1065-1070
26. Thomas C.P., Auerbach S., Stokes J.B., and Volk K.A. 5' heterogeneity in epithelial sodium channel α-subunit mRNA leads to distinct NH2-terminal variant proteins. Am J Physiol 274 (1998) C1312-C1323
27. Auerbach S.D., Loftus R.W., Itani O.A., and Thomas C.P. Human amiloride-sensitive epithelial Na+ channel gamma subunit promoter: functional analysis and identification of a polypurine-polypyrimidine tract with the potential for triplex DNA formation. Biochem J 347 (2000) 105-114
28. Yang J., Kawai Y., Hanson R.W., and Arinze I.J. Sodium butyrate induces transcription from the G α(i2) gene promoter through multiple Sp1 sites in the promoter and by activating the MEK-ERK signal transduction pathway. J Biol Chem 276 (2001) 25742-25752
29. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25 (2001) 402-408
30. Weiske J., and Huber O. The histidine triad protein Hint1 triggers apoptosis independent of its enzymatic activity. J Biol Chem 281 (2006) 27356-27366
31. Grotjohann I., Schulzke J.D., and Fromm M. Electrogenic Na+ transport in rat late distal colon by natural and synthetic glucocorticosteroids. Am J Physiol 276 (1999) G491-G498
32. Barmeyer C., Amasheh S., Tavalali S., Mankertz J., Zeitz M., Fromm M., and Schulzke J.D. IL-1β and TNFα regulate sodium absorption in rat distal colon. Biochem Biophys Res Commun 317 (2004) 500-507
33. Cummings J.H., Pomare E.W., Branch W.J., Naylor C.P., and Macfarlane G.T. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28 (1987) 1221-1227
34. Vernia P., Gnaedinger A., Hauck W., and Breuer R.I. Organic anions and the diarrhea of inflammatory bowel disease. Dig Dis Sci 33 (1988) 1353-1358
35. Kockerling A., Sorgenfrei D., and Fromm M. Electrogenic Na+ absorption of rat distal colon is confined to surface epithelium: a voltage-scanning study. Am J Physiol 264 (1993) C1285-C1293
36. Zweibaum A., Pinto M., Chevalier G., Dussaulx E., Triadou N., Lacroix B., Haffen K., Brun J.L., and Rousset M. Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose. J Cell Physiol 122 (1985) 21-29
37. Rognoni J.B., Pichard V., Honore S., Rigot V., Lehmann M., Roccabianca M., Carles G., Luis J., Marvaldi J., and Briand C. Convergent effects of growth factors, hormones, and fibronectin are necessary for the enterocyte differentiation of a colon adenocarcinoma cell line (HT29-D4). Differentiation 63 (1998) 305-317
38. Wiren M., Magnusson K.E., and Larsson J. The role of glutamine, serum and energy factors in growth of enterocyte-like cell lines. Int J Biochem Cell Biol 30 (1998) 1331-1336
39. Siavoshian S., Segain J.P., Kornprobst M., Bonnet C., Cherbut C., Galmiche J.P., and 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
40. Wu J.T., Archer S.Y., Hinnebusch B., Meng S., and Hodin R.A. Transient vs. prolonged histone hyperacetylation: effects on colon cancer cell growth, differentiation, and apoptosis. Am J Physiol Gastrointest Liver Physiol 280 (2001) G482-G490
41. Duan H., Heckman C.A., and Boxer L.M. Histone deacetylase inhibitors down-regulate bcl-2 expression and induce apoptosis in t(14;18) lymphomas. Mol Cell Biol 25 (2005) 1608-1619
42. Gan Y., Shen Y.H., Wang J., Wang X., Utama B., and Wang X.L. Role of histone deacetylation in cell-specific expression of endothelial nitric-oxide synthase. J Biol Chem 280 (2005) 16467-16475
43. Young D.A., Billingham O., Sampieri C.L., Edwards D.R., and Clark I.M. Differential effects of histone deacetylase inhibitors on phorbol ester- and TGF-β1 induced murine tissue inhibitor of metalloproteinases-1 gene expression. FEBS J 272 (2005) 1912-1926
44. Thomas C.P., Doggett N.A., Fisher R., and Stokes J.B. Genomic organization and the 5' flanking region of the γ subunit of the human amiloride-sensitive epithelial sodium channel. J Biol Chem 271 (1996) 26062-26066
45. Binder H.J., McGlone F., and Sandle G.I. Effects of corticosteroid hormones on the electrophysiology of rat distal colon: implications for Na+ and K+ transport. J Physiol 410 (1989) 425-441
46. Firsov D., Schild L., Gautschi I., Merillat A.M., Schneeberger E., and Rossier B.C. Cell surface expression of the epithelial Na channel and a mutant causing Liddle syndrome: a quantitative approach. Proc Natl Acad Sci U S A 93 (1996) 15370-15375
47. Di Gennaro E., Bruzzese F., Caraglia M., Abruzzese A., and Budillon A. Acetylation of proteins as novel target for antitumor therapy: review article. Amino Acids 26 (2004) 435-441
48. Boffa L.C., Mariani M.R., and Parker M.I. Selective hypermethylation of transcribed nucleosomal DNA by sodium butyrate. Exp Cell Res 211 (1994) 420-423
49. Bouwman P., and Philipsen S. Regulation of the activity of Sp1-related transcription factors. Mol Cell Endocrinol 195 (2002) 27-38
50. Thomas C.P., Loftus R.W., Liu K.Z., and Itani O.A. Genomic organization of the 5' end of human β-ENaC and preliminary characterization of its promoter. Am J Physiol Renal Physiol 282 (2002) F898-F909
51. Valentijn J.A., Fyfe G.K., and Canessa C.M. Biosynthesis and processing of epithelial sodium channels in Xenopus oocytes. J Biol Chem 273 (1998) 30344-30351
52. Sauter D., Fernandes S., Goncalves-Mendes N., Boulkroun S., Bankir L., Loffing J., and Bouby N. Long-term effects of vasopressin on the subcellular localization of ENaC in the renal collecting system. Kidney Int 69 (2006) 1024-1032
53. Lambert D.W., Wood I.S., Ellis A., and Shirazi-Beechey S.P. Molecular changes in the expression of human colonic nutrient transporters during the transition from normality to malignancy. Br J Cancer 86 (2002) 1262-1269
54. Gill R.K., Saksena S., Alrefai W.A., Sarwar Z., Goldstein J.L., Carroll R.E., Ramaswamy K., and Dudeja P.K. Expression and membrane localization of MCT isoforms along the length of the human intestine. Am J Physiol Cell Physiol 289 (2005) C846-C852
55. Lombes M., Kenouch S., Souque A., Farman N., and Rafestin-Oblin M.E. The mineralocorticoid receptor discriminates aldosterone from glucocorticoids independently of the 11 β-hydroxysteroid dehydrogenase. Endocrinology 135 (1994) 834-840
56. Vernia P., Cittadini M., Caprilli R., and Torsoli A. Topical treatment of refractory distal ulcerative colitis with 5-ASA and sodium butyrate. Dig Dis Sci 40 (1995) 305-307
57. 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. Butyrate inhibits inflammatory responses through NF-κB inhibition: implications for Crohn's disease. Gut 47 (2000) 397-403
58. Mortensen P.B., and Clausen M.R. Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenterol Suppl 216 (1996) 132-148
59. Sapetschnig A., Koch F., Rischitor G., Mennenga T., and Suske G. Complexity of translationally controlled transcription factor Sp3 isoform expression. J Biol Chem 279 (2004) 42095-42105