Decreased mucosal sulfide detoxification is related to an impaired butyrate oxidation in ulcerative colitis

Inflammatory Bowel Diseases

Volumn 18, Issue 12, 2012, Pages 2371-2380

  De Preter, Vicky ^a   Arijs, Ingrid ^a   Windey, Karen ^a   Vanhove, Wiebe ^a   Vermeire, Severine ^a   Schuit, Frans ^b   Rutgeerts, Paul ^a   Verbeke, Kristin ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

butyrate; gene expression; sulfide; thiosulfate sulfurtransferase; ulcerative colitis

Indexed keywords

BUTYRIC ACID; HYDROGEN SULFIDE; INFLIXIMAB; MESSENGER RNA; THIOSULFATE SULFURTRANSFERASE;

ARTICLE; COLON MUCOSA; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DETOXIFICATION; DISEASE ACTIVITY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; LOADING DRUG DOSE; MAJOR CLINICAL STUDY; MALE; OXIDATION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE DRUG DOSE; SPECTROPHOTOMETRY; ULCERATIVE COLITIS;

ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, MONOCLONAL; BUTYRATES; CASE-CONTROL STUDIES; COLITIS, ULCERATIVE; COLON; FEMALE; GENE EXPRESSION; HUMANS; INTESTINAL MUCOSA; MALE; MIDDLE AGED; OXIDATION-REDUCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SULFIDES; THIOSULFATE SULFURTRANSFERASE;

EID: 84869228196     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.22949     Document Type: Article

References (57)

1. Topping DL, Clifton PM,. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001; 81: 1031-1064.
2. Roediger WEW,. The colonic epithelium in ulcerative-colitis - an energy-deficiency disease. Lancet. 1980; 2: 712-715.
3. Roediger WE, Moore J, Babidge W,. Colonic sulfide in pathogenesis and treatment of ulcerative colitis. Dig Dis Sci. 1997; 42: 1571-1579.
4. Babidge W, Millard S, Roediger W,. Sulfides impair short chain fatty acid beta-oxidation at acyl-CoA dehydrogenase level in colonocytes: implications for ulcerative colitis. Mol Cell Biochem. 1998; 181: 117-124.
5. Leschelle X, Goubern M, Andriamihaja M, et al. Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide. Biochim Biophys Acta Gen Subj. 2005; 1725: 201-212.
6. Den Hond E, Hiele M, Evenepoel P, et al. In vivo butyrate metabolism and colonic permeability in extensive ulcerative colitis. Gastroenterology. 1998; 115: 584-590.
7. Kato K, Ishii Y, Mizuno S, et al. Usefulness of rectally administering [1(13)C]-butyrate for breath test in patients with active and quiescent ulcerative colitis. Scand J Gastroenterol. 2007; 42: 207-214.
8. Chapman MAS, Grahn MF, Boyle MA, et al. Butyrate oxidation is impaired in the colonic mucosa of sufferers of quiescent ulcerative-colitis. Gut. 1994; 35: 73-76.
9. Duffy MM, Regan MC, Ravichandran P, et al. Mucosal metabolism in ulcerative colitis and Crohn's disease. Dis Colon Rectum. 1998; 41: 1399-1405.
10. De Preter V, Bulteel V, Suenaert P, et al. Pouchitis, similar to active ulcerative colitis, is associated with impaired butyrate oxidation by intestinal mucosa. Inflamm Bowel Dis. 2009; 15: 335-340.
11. De Preter V, Arijs I, Windey K, et al. Impaired butyrate oxidation in ulcerative colitis is due to decreased butyrate uptake and a defect in the oxidation pathway. Inflamm Bowel Dis. 2011 [Epub ahead of print].
12. Packey CD, Sartor RB,. Commensal bacteria, traditional and opportunistic pathogens, dysbiosis and bacterial killing in inflammatory bowel diseases. Curr Opin Infect Dis. 2009; 22: 292-301.
13. Sands BE,. Inflammatory bowel disease: past, present, and future. J Gastroenterol. 2007; 42: 16-25.
14. Roediger WEW, Duncan A, Kapaniris O, et al. Reducing sulfur-compounds of the colon impair colonocyte nutrition - implications for ulcerative-colitis. Gastroenterology. 1993; 104: 802-809.
15. Roediger WEW, Duncan A, Kapaniris O, et al. Sulfide impairment of substrate oxidation in rat colonocytes - a biochemical basis for ulcerative-colitis. Clin Sci. 1993; 85: 623-627.
16. Medani M, Collins D, Docherty NG, et al. Emerging role of hydrogen sulfide in colonic physiology and pathophysiology. Inflamm Bowel Dis. 2011; 17: 1620-1625.
17. Hulin SJ, Singh S, Chapman MAS, et al. Sulphide-induced energy deficiency in colonic cells is prevented by glucose but not by butyrate. Aliment Pharmacol Ther. 2002; 16: 325-331.
18. Moore JWE, Babidge W, Millard S, et al. Effect of sulphide on short chain acyl-CoA metabolism in rat colonocytes. Gut. 1997; 41: 77-81.
19. Blachier F, Davila AM, Mimoun S, et al. Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids. 2010; 39: 335-347.
20. Florin T, Neale G, Gibson GR, et al. Metabolism of dietary sulphate: absorption and excretion in humans. Gut. 1991; 32: 766-773.
21. Roediger WE, Moore J, Babidge W,. Colonic sulfide in pathogenesis and treatment of ulcerative colitis. Dig Dis Sci. 1997; 42: 1571-1579.
22. Florin THJ,. Hydrogen-sulfide and total acid-volatile sulfide in feces, determined with a direct spectrophotometric method. Clin Chim Acta. 1991; 196: 127-134.
23. Levine J, Ellis CJ, Furne JK, et al. Fecal hydrogen sulfide production in ulcerative colitis. Am J Gastroenterol. 1998; 93: 83-87.
24. Pitcher MCL, Cummings JH,. Hydrogen sulphide: a bacterial toxin in ulcerative colitis? Gut. 1996; 39: 1-4.
25. Moore J, Babidge W, Millard S, et al. Colonic luminal hydrogen sulfide is not elevated in ulcerative colitis. Dig Dis Sci. 1998; 43: 162-165.
26. Roediger WE, Babidge WJ,. Thiol methyltransferase activity in inflammatory bowel disease. Gut. 2000; 47: 206-210.
27. Levitt MD, Furne J, Springfield J, et al. Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J Clin Invest. 1999; 104: 1107-1114.
28. Schroeder KW, Tremaine WJ, Ilstrup DM,. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative-colitis - a randomized study. N Engl J Med. 1987; 317: 1625-1629.
29. Kight CE, Fleming SE,. Nutrient oxidation by rat intestinal epithelial cells is concentration dependent. J Nutr. 1993; 123: 876-882.
30. Rutgeerts P, Sandborn WJ, Feagan BG, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005; 353: 2462-2476.
31. Geboes K, Riddell R, Ost A, et al. A reproducible grading scale for histological assessment of inflammation in ulcerative colitis. Gut. 2000; 47: 404-409.
32. Arijs I, Li K, Toedter G, et al. Mucosal gene signatures to predict response to infliximab in patients with ulcerative colitis. Gut. 2009; 58: 1612-1619.
33. Aminlari M, Gilanpour H,. Comparative studies on the distribution of rhodanese in different tissues of domestic animals. Comp Biochem Physiol B. 1991; 99: 673-677.
34. Zilbauer M, Jenke A, Wenzel G, et al. Intestinal alpha-defensin expression in pediatric inflammatory bowel disease. Inflamm Bowel Dis. 2011; 17: 2076-2086.
35. Pfaffl MW,. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29: e45.
36. Cooper CE, Brown GC,. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr. 2008; 40: 533-539.
37. Attene-Ramos MS, Wagner ED, Plewa MJ, et al. Evidence that hydrogen sulfide is a genotoxic agent. Mol Cancer Res. 2006; 4: 9-14.
38. Elson CO, Sartor RB, Tennyson GS, et al. Experimental models of inflammatory bowel disease. Gastroenterology. 1995; 109: 1344-1367.
39. Sartor RB,. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008; 134: 577-594.
40. Gibson GR, Macfarlane GT, Cummings JH,. Sulfate reducing bacteria and hydrogen metabolism in the human large-intestine. Gut. 1993; 34: 437-439.
41. Zinkevich V, Beech IB,. Screening of sulfate-reducing bacteria in colonoscopy samples from healthy and colitic human gut mucosa. FEMS Microbiol Ecol. 2000; 34: 147-155.
42. Marchesi JR, Holmes E, Khan F, et al. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res. 2007; 6: 546-551.
43. Jorgensen J, Mortensen PB,. Hydrogen sulfide and colonic epithelial metabolism - implications for ulcerative colitis. Dig Dis Sci. 2001; 46: 1722-1732.
44. Wallace JL, Vong L, McKnight W, et al. Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology. 2009; 137: 569-578.
45. Suarez F, Furne J, Springfield J, et al. Production and elimination of sulfur-containing gases in the rat colon. Am J Physiol. 1998; 274: G727-G733.
46. Levitt MD, Furne J, Springfield J, et al. Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J Clin Invest. 1999; 104: 1107-1114.
47. Wilson K, Mudra M, Furne J, et al. Differentiation of the roles of sulfide oxidase and rhodanese in the detoxification of sulfide by the colonic mucosa. Dig Dis Sci. 2008; 53: 277-283.
48. Hildebrandt TM, Grieshaber MK,. Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J. 2008; 275: 3352-3361.
49. Goubern M, Andriamihaja M, Nubel T, et al. Sulfide, the first inorganic substrate for human cells. FASEB J. 2007; 21: 1699-1706.
50. Ramasamy S, Singh S, Taniere P, et al. Sulfide-detoxifying enzymes in the human colon are decreased in cancer and upregulated in differentiation. Am J Physiol Gastrointest Liver Physiol. 2006; 291: G288-G296.
51. Picton R, Eggo MC, Langman MJS, et al. Impaired detoxication of hydrogen sulfide in ulcerative colitis? Dig Dis Sci. 2007; 52: 373-378.
52. Taniguchi E, Matsunami M, Kimura T, et al. Rhodanese, but not cystathionine-gamma-lyase, is associated with dextran sulfate sodium-evoked colitis in mice: a sign of impaired colonic sulfide detoxification? Toxicology. 2009; 264: 96-103.
53. Cao Q, Zhang L, Yang G, et al. Butyrate-stimulated H2S production in colon cancer cells. Antioxid Redox Signal. 2010; 12: 1101-1109.
54. Macfarlane GT, Gibson GR, Cummings JH,. Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol. 1992; 72: 57-64.
55. Danese S,. Mechanisms of action of infliximab in inflammatory bowel disease: an anti-inflammatory multitasker. Dig Liver Dis. 2008; 40 (Suppl 2): S225-S228.
56. Billaut-Laden I, Allorge D, Crunelle-Thibaut A, et al. Evidence for a functional genetic polymorphism of the human thiosulfate sulfurtransferase (Rhodanese), a cyanide and H2S detoxification enzyme. Toxicology. 2006; 225: 1-11.
57. Zanardo RC, Brancaleone V, Distrutti E, et al. Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J. 2006; 20: 2118-2120.