Hydrogen sulphide protects against NSAID-enteropathy through modulation of bile and the microbiota

British Journal of Pharmacology

Volumn 172, Issue 4, 2015, Pages 992-1004

  Blackler, Rory W ^a   Motta, Jean Paul ^b   Manko, Anna ^a   Workentine, Matthew ^a   Bercik, Premysl ^a   Surette, Michael G ^a   Wallace, John L ^b,c  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DIALLYL DISULPHIDE; HYDROGEN SULFIDE; NAPROXEN; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTAGLANDIN SYNTHASE; UNCLASSIFIED DRUG; 3-CYANOALANINE; ALANINE; ALLYL COMPOUND; ALLYL SULFIDE; CYCLOOXYGENASE 1; MEMBRANE PROTEIN; PROTECTIVE AGENT; PTGS1 PROTEIN, RAT; SULFIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT DISEASE; CONTROLLED STUDY; DOSE RESPONSE; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; ENTERITIS; ENTEROPATHY; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INTESTINAL BLEEDING; INTESTINE FLORA; INTESTINE ULCER; MICROFLORA; NONHUMAN; RAT; SMALL INTESTINE DISEASE; SPECIES COMPOSITION; STOMACH PROTECTION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BILE; CELL LINE; CHEMICALLY INDUCED; GASTROINTESTINAL HEMORRHAGE; HUMAN; INTESTINAL DISEASES; INTESTINE MUCOSA; JEJUNUM; METABOLISM; MICROBIOLOGY; PATHOLOGY; ULCER; WISTAR RAT;

ALANINE; ALLYL COMPOUNDS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BILE; CELL LINE; CYCLOOXYGENASE 1; GASTROINTESTINAL HEMORRHAGE; HUMANS; HYDROGEN SULFIDE; INTESTINAL DISEASES; INTESTINAL MUCOSA; JEJUNUM; MEMBRANE PROTEINS; MICROBIOTA; NAPROXEN; PROTECTIVE AGENTS; RATS, WISTAR; SULFIDES; ULCER;

EID: 84921760323     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12961     Document Type: Article

References (58)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M et al. (2013). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
2. Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell S, Patel RP et al. (2007). Hydrogen sulfide mediates the vasoactivity of garlic. Proc Natl Acad Sci U S A 104: 17977-17982.
3. Bjarnason I, Hayllar J, MacPherson AJ, Russell AS (1993). Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology 104: 1832-1847.
4. Blackler R, Syer S, Bolla M, Ongini E, Wallace JL (2012). Gastrointestinal-sparing effects of novel NSAIDs in rats with compromised mucosal defence. PLoS ONE 7: e35196.
5. Boughton-Smith NK, Wallace JL, Whittle BJ (1988). Relationship between arachidonic acid metabolism, myeloperoxidase activity and leukocyte infiltration in a rat model of inflammatory bowel disease. Agents Actions 25: 115-123.
6. Campolo M, Esposito E, Ahmad A, Di Paola R, Wallace JL, Cuzzocrea S (2013). A hydrogen sulfide-releasing cyclooxygenase inhibitor markedly accelerates recovery from experimental spinal cord injury. FASEB J 27: 4489-4499.
7. Dietschy JM (1968). Mechanisms for the intestinal absorption of bile acids. J Lipid Res 9: 297-309.
8. Elliott SN, Buret A, McKnight W, Miller MJ, Wallace JL (1998). Bacteria rapidly colonize and modulate healing of gastric ulcers in rats. Am J Physiol 275: G425-G432.
9. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, Tao L et al. (2007). Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104: 15560-15565.
10. Elsheikh W, Blackler RW, Flannigan KL, Wallace JL (2014). Enhanced chemopreventative effects of a hydrogen sulfide-releasing NSAID (ATB-346) in experimental colorectal cancer. Nitric Oxide 41: 131-137.
11. Fiorucci S, Antonelli E, Distrutti E, Rizzo G, Medcarelli A, Orlandi S et al. (2005). Inhibition of hydrogen sulfide generation contributes to gastric injury caused by anti-inflammatory nonsteroidal drugs. Gastroenterology 129: 1210-1224.
12. Fiorucci S, Orlandi S, Mencarelli A, Caliendo G, Santagada V, Distrutti E et al. (2007). Enhanced activity of a hydrogen sulphide-releasing derivative of mesalamine (ATB-429) in a mouse model of colitis. Br J Pharmacol 150: 996-1002.
13. Flannigan KL, Ferraz JG, Wang R, Wallace JL (2013). Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: a site-specific, pro-resolution mechanism. PLoS ONE 8: e71962.
14. Goubern M, Andriamihaja M, Nubel T, Blachier F, Bouillaud F (2007). Sulfide, the first inorganic substrate for human cells. FASEB J 21: 1699-1706.
15. Hagiwara M, Kataoka K, Arimochi H, Kuwahara T, Ohnishi Y (2004). Role of unbalanced growth of gram-negative bacteria in ileal ulcer formation in rats treated with a nonsteroidal anti-inflammatory drug. J Med Invest 51: 43-51.
16. Hofmann AF (1999). The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med 159: 2647-2658.
17. Jobin C, Morteau O, Hans DS, Sartor RB (1998). Specific NF-kappaB blockade selectively inhibits tumour necrosis factor-alpha-induced COX-2 but not constitutive COX-1 gene expression in HT-29 cells. Immunology 95: 537-543.
18. Kawabata A, Ishiki T, Nagasawa K, Yoshida S, Maeda Y, Takahashi T et al. (2007). Hydrogen sulfide as a novel nociceptive messenger. Pain 132: 74-81.
19. Kent TH, Cardelli RM, Stamler FW (1969). Small intestinal ulcersand intestinal flora in rats given indomethacin. Am J Pathol 54: 237-249.
20. Kimura Y, Goto Y, Kimura H (2010). Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid Redox Signal 12: 1-13.
21. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
22. Lanas A, Garcia-Rodriguez LA, Polo-Tomas M, Ponce M, Alonso-Abreu I, Perez-Aisa MA et al. (2009). Time trends and impact of upper and lower gastrointestinal bleeding and perforation in clinical practice. Am J Gastroenterol 104: 1633-1641.
23. Mard SA, Neisi N, Solgi G, Hassanpour M, Darbor M, Maleki M (2012). Gastroprotective effect of NaHS against mucosal lesions induced by ischemia-reperfusion injury in rat. Dig Dis Sci 57: 1496-1503.
24. Martinez-Augustin O, Sanchez de Medina F (2008). Intestinal bile acid physiology and pathophysiology. World J Gastroenterol 14: 5630-5640.
25. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
26. 2S by differentiated colonic epithelial cells: implication of the sulfide oxidizing unit and of the cell respiratory capacity. Antioxid Redox Signal 17: 1-10.
27. Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P et al. (2013). Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil 25: 733-e575.
28. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledge base of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-1106.
29. Quaroni A, Wands J, Trelstad RL, Isselbacher KJ (1979). Epithelioid cell cultures from rat small intestine. Characterization by morphologic and immunologic criteria. J Cell Biol 80: 248-265.
30. Reuter BK, Davies NM, Wallace JL (1997). Nonsteroidal anti-inflammatory drug enteropathy in rats: role of permeability, bacteria, and enterohepatic circulation. Gastroenterology 112: 109-117.
31. Robert A, Asano T (1977). Resistance of germfree rats to indomethacin-induced intestinal lesions. Prostaglandins 14: 333-341.
32. Saitta KS, Zhang C, Lee KK, Fujimoto K, Redinbo MR, Boelsterli UA (2014). Bacterial β-glucuronidase inhibition protects mice against enteropathy induced by indomethacin, ketoprofen or diclofenac: mode of action and pharmacokinetics. Xenobiotica 44: 28-35.
33. Satoh H, Amagase K, Takeuchi K (2012). Exacerbation of nonsteroidal anti-inflammatory drug-induced small intestinal lesions by antisecretory drugs in rats: the role of intestinal motility. J Pharmacol Exp Ther 343: 270-277.
34. Scheiman JM, Yeomans ND, Talley NJ, Vakil N, Chan FK, Tulassay Z (2006). Prevention of ulcers by esomeprazole in at-risk patients using non-selective NSAIDs and COX-2 inhibitors. Am J Gastroenterol 101: 701-710.
35. Seitz S, Boelsterli UA (1998). Diclofenac acyl glucuronide, a major biliary metabolite, is directly involved in small intestinal injury in rats. Gastroenterology 115: 1476-1482.
36. Somasundaram S, Rafi S, Hayllar J, Sigthorsson G, Jacob M, Price AB et al. (1997). Mitochondrial damage: a possible mechanism of the 'topical' phase of NSAID induced injury to the rat intestine. Gut 41: 344-353.
37. Uejima M, Kinouchi T, Kataoka K, Hiraoka I, Ohnishi Y (1996). Role of intestinal bacteria in ileal ulcer formation in rats treated with a nonsteroidal antiinflammatory drug. Microbiol Immunol 40: 553-560.
38. Wallace JL (2008). Prostaglandins, NSAIDs, and gastric mucosal protection; why doesn't the stomach digest itself? Physiol Rev 88: 1547-1565.
39. Wallace JL (2010). Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract. Antioxid Redox Signal 12: 1125-1133.
40. Wallace JL (2012). NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies. Br J Pharmacol 165: 67-74.
41. Wallace JL (2013a). Mechanisms, prevention and clinical implications of nonsteroidal anti-inflammatoty drug-enteropathy. World J Gastroenterol 19: 1861-1876.
42. Wallace JL (2013b). Polypharmacy of osteoarthritis: the perfect intestinal storm. Dig Dis Sci 58: 3088-3093.
43. Wallace JL, Keenan CM, Granger DN (1990). Gastric ulceration induced by nonsteroidal anti-inflammatory drugs is a neutrophil-dependent process. Am J Physiol 259: 462-467.
44. Wallace JL, Bak A, McKnight W, Asfaha S, Sharkey KA, MacNaughton WK (1998). Cyclooxygenase 1 contributes to inflammatory responses in rats and mice: implications for gastrointestinal toxicity. Gastroenterology 115: 101-109.
45. Wallace JL, McKnight W, Reuter BK, Vergnolle N (2000). NSAID-induced gastric damage in rats: requirement for inhibition of both cyclooxygenase 1 and 2. Gastroenterology 119: 706-714.
46. Wallace JL, Caliendo G, Santagada V, Cirino G, Fiorucci S (2007a). Gastrointestinal safety and anti-inflammatory effects of a hydrogen sulfide-releasing diclofenac derivative in the rat. Gastroenterology 132: 261-271.
47. Wallace JL, Dicay M, McKnight W, Martin GR (2007b). Hydrogen sulfide enhances ulcer healing. FASEB J 21: 4070-4076.
48. Wallace JL, Vong L, McKnight W, Dicay M, Martin GR (2009). Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology 137: 569-578.
49. Wallace JL, Caliendo G, Santagada V, Cirino G (2010). Markedly reduced toxicity of a hydrogen sulphide-releasing derivative of naproxen (ATB-346). Br J Pharmacol 159: 1236-1246.
50. Wallace JL, Syer S, Denou E, de Palma G, Vong L, McKnight W et al. (2011). Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology 141: 1314-1322.
51. Wallace JL, Ferraz JG, Muscara MN (2012). Hydrogen sulfide: an endogenous mediator of resolution of inflammation and injury. Antioxid Redox Signal 17: 58-67.
52. Wallace JL, Blackler RW, Chan MV, Da Silva GJ, Elsheikh W, Flannigan KL et al. (2014). Anti-inflammatory and cytoprotective actions of hydrogen sulfide: translation to theapeutics. Antioxid Redox Signal. Epub ahead of print.
53. Watanabe T, Higuchi K, Kobata A, Nishio H, Tanigawa T, Shiba M et al. (2008). Non-steroidal anti-inflammatory drug-induced small intestinal damage is Toll-like receptor 4 dependent. Gut 57: 181-187.
54. Watanabe T, Tanigawa T, Nadatani Y, Nagami Y, Sugimori S, Okazaki H et al. (2013). Risk factors for severe nonsteroidal anti-inflammatory drug-induced small intestinal damage. Dig Liver Dis 45: 390-395.
55. Wax J, Clinger WA, Varner P, Bass P, Winder CV (1970). Relationship of the enterohepatic cycle to ulcerogenesis in the rat small bowel with flufenamic acid. Gastroenterology 58: 772-780.
56. Yamada T, Deitch E, Specian RD, Perry MA, Sartor RB, Grisham MB (1993). Mechanisms of acute and chronic intestinal inflammation induced by indomethacin. Inflammation 17: 641-662.
57. Zanardo RC, Brancaleone V, Distrutti E, Fiorucci S, Cirino G, Wallace JL (2006). Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20: 2118-2120.
58. Zhao Y, Encinosa W (2008). Hospitalizations for gastrointestinal bleeding in 1998 and 2006: Statistical brief #65. Health Care Cost and Utilization Project (HCUP) Statistical Briefs. Agency for Health Care Policy and Research.