Impaired hydrogen sulfide synthesis and IL-10 signaling underlie hyperhomocysteinemia-associated exacerbation of colitis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 37, 2014, Pages 13559-13564

  Flannigan, Kyle L ^a   Agbor, Terence A ^a   Blackler, Rory W ^a   Kim, Janice J ^a   Khan, Waliul I ^a   Verdu, Elena F ^a   Ferraz, Jose G P ^b   Wallace, John L ^c,d  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRAN SULFATE; HYDROGEN SULFIDE; INTERLEUKIN 10; PEROXIDASE; RECOMBINANT PROTEIN;

ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; COLITIS; COLON; COMPLICATION; DEFICIENCY; DIET; DISEASE COURSE; HUMAN; HYPERHOMOCYSTEINEMIA; MALE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; COLITIS; COLON; DEXTRAN SULFATE; DIET; DISEASE PROGRESSION; HUMANS; HYDROGEN SULFIDE; HYPERHOMOCYSTEINEMIA; INTERLEUKIN-10; MALE; MICE, INBRED C57BL; PEROXIDASE; RATS, WISTAR; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84907201013     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1413390111     Document Type: Article

References (55)

1. Oldenburg B, Fijnheer R, van der Griend R, vanBerge-Henegouwen GP, Koningsberger JC (2000) Homocysteine in inflammatory bowel disease: A risk factor for thromboembolic complications?. Am J Gastroenterol 95(10):2825-2830.
2. Vagianos K, Bernstein C.N. (2012) Homocysteinemia and B vitamin status among adult patients with inflammatory bowel disease: A one-year prospective follow-up study. Inflamm Bowel Dis 18(4):718-724.
3. Vagianos K, Bector S, McConnell J., Bernstein C.N. (2007) Nutrition assessment of patients with inflammatory bowel disease. JPEN J Parenter Enteral Nutr 31(4): 311-319.
4. Jacques PF, et al. (1996) Relation between folate status, a common mutation in methylenetetrahydrofolate reductase, and plasma homocysteine concentrations. Circulation 93(1):7-9.
5. den Heijer M, et al. (1996) Hyperhomocysteinemia as a risk factor for deep-vein thrombosis. N Engl J Med 334(12):759-762.
6. Wald DS, Law M, Morris J.K. (2002) Homocysteine and cardiovascular disease: Evidence on causality from a meta-analysis. BMJ 325(7374):1202.
7. Saibeni S, et al. (2003) Low vitamin B(6) plasma levels, a risk factor for thrombosis, in inflammatory bowel disease: Role of inflammation and correlation with acute phase reactants. Am J Gastroenterol 98(1):112-117.
8. Kimura H (2014) Production and physiological effects of hydrogen sulfide. Antioxid Redox Signal 20(5):783-793.
9. Wallace JL, et al. (April 15, 2014) Anti-inflammatory and cytoprotective actions of hydrogen sulfide: Translation to therapeutics. Antioxid Redox Signal, 10.1089/ars.2014.5901.
10. Wallace JL, Dicay M, McKnight W., Martin G.R. (2007) Hydrogen sulfide enhances ulcer healing in rats. FASEB J 21(14):4070-4076.
11. Wallace JL, Vong L, McKnight W., Dicay M, Martin G.R. (2009) Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology 137(2):569-578.e1.
12. Martin GR, et al. (2010) Hydrogen sulphide synthesis in the rat and mouse gastrointestinal tract. Dig Liver Dis 42(2):103-109.
13. Flannigan KL, McCoy KD, Wallace J.L. (2011) Eukaryotic and prokaryotic contributions to colonic hydrogen sulfide synthesis. Am J Physiol Gastrointest Liver Physiol 301(1): G188-G193.
14. Flannigan KL, Ferraz JG, Wang R, Wallace J.L. (2013) Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: A site-specific, proresolution mechanism. PLoS ONE 8(8):e71962.
15. Wallace JL (2010) Physiological and pathophysiological roles of hydrogen sulfide in the gastrointestinal tract. Antioxid Redox Signal 12(9):1125-1133.
16. Yang G, et al. (2008) H2S as a physiologic vasorelaxant: Hypertension in mice with deletion of cystathionine γ-lyase. Science 322(5901):587-590.
17. Kamath AF, et al. (2006) Elevated levels of homocysteine compromise blood-brain barrier integrity in mice. Blood 107(2):591-593.
18. Noguchi E, Homma Y, Kang X., Netea MG, Ma X. (2009) A Crohn's disease-associated NOD2 mutation suppresses transcription of human IL10 by inhibiting activity of the nuclear ribonucleoprotein hnRNP-A1. Nat Immunol 10(5):471-479.
19. Moran CJ, et al. (2013) IL-10R polymorphisms are associated with very-early-onset ulcerative colitis. Inflamm Bowel Dis 19(1):115-123.
20. Cooper HS, Murthy SN, Shah R.S., Sedergran D.J. (1993) Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 69(2):238-249.
21. Watkins D, Rosenblatt D.S. (2011) Inborn errors of cobalamin absorption and metabolism. Am J Med Genet C Semin Med Genet 157C(1):33-44.
22. Niyikiza C, et al. (2002) Homocysteine and methylmalonic acid: Markers to predict and avoid toxicity from pemetrexed therapy. Mol Cancer Ther 1(7):545-552.
23. Cassel S, Robson L, Rosse C. (1978) The effects of vitamin B6 deficiency on the bone marrow of the rat. Anat Rec 191(1):47-53.
24. Duboc H, et al. (2013) Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut 62(4):531-539.
25. Madsen KL (2001) Inflammatory bowel disease: Lessons from the IL-10 gene-deficient mouse. Clin Invest Med 24(5):250-257.
26. Koumaki V, et al. (2006) Pro-inflammatory bone marrow milieu in patients with chronic idiopathic neutropenia is associated with impaired local production of in-terleukin-10. Br J Haematol 135(4):570-573.
27. Benchimol EI, et al. (2009) Increasing incidence of paediatric inflammatory bowel disease in Ontario, Canada: Evidence from health administrative data. Gut 58(11): 1490-1497.
28. Molodecky NA, et al. (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142(1): 46-54.e42.
29. Fiorucci S, 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(8):996-1002.
30. Davidson NJ, et al. (1996) T helper cell 1-type CD4+T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J Exp Med 184(1):241-251.
31. Ernest S, Hosack A, O'Brien WE, Rosenblatt DS, Nadeau J.H. (2005) Homocysteine levels in A/J and C57BL/6J mice: Genetic, diet, gender, and parental effects. Physiol Genomics 21(3):404-410.
32. Li T, et al. (2008) Regulatory effects of hydrogen sulfide on IL-6, IL-8 and IL-10 levels in the plasma and pulmonary tissue of rats with acute lung injury. Exp Biol Med (Maywood) 233(9):1081-1087.
33. Tokuda K, et al. (2012) Inhaled hydrogen sulfide prevents endotoxin-induced systemic inflammation and improves survival by altering sulfide metabolism in mice. Antioxid Redox Signal 17(1):11-21.
34. Zeng J, Lin X, Fan H., Li C. (2013) Hydrogen sulfide attenuates the inflammatory response in a mouse burn injury model. Mol Med Rep 8(4):1204-1208.
35. Wu J, et al. (2013) Inhibition of hydrogen sulfide generation contributes to lung injury after experimental orthotopic lung transplantation. J Surg Res 182(1):e25-e33.
36. van der Linde K, et al. (2003) A Gly15Arg mutation in the interleukin-10 gene reduces secretion of interleukin-10 in Crohn disease. Scand J Gastroenterol 38(6):611-617.
37. Franke A, et al.; IBSEN Study Group (2008) Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat Genet 40(11): 1319-1323.
38. Shouval DS, et al. (2014) Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity 40(5):706-719.
39. Holven KB, et al. (2006) Impaired inhibitory effect of interleukin-10 on the balance between matrix metalloproteinase-9 and its inhibitor in mononuclear cells from hy-perhomocysteinemic subjects. Stroke 37(7):1731-1736.
40. Colombel JF, et al. (2001) Interleukin 10 (Tenovil) in the prevention of postoperative recurrence of Crohn's disease. Gut 49(1):42-46.
41. Gunnett CA, Heistad DD, Berg D.J., Faraci F.M. (2000) IL-10 deficiency increases superoxide and endothelial dysfunction during inflammation. Am J Physiol Heart Circ Physiol 279(4):H1555-H1562.
42. Cheng Z, et al. (2011) Hyperhomocysteinemia impairs endothelium-derived hyper-polarizing factor-mediated vasorelaxation in transgenic cystathionine beta synthase-deficient mice. Blood 118(7):1998-2006.
43. Zhao W, Zhang J, Lu Y., Wang R. (2001) The vasorelaxant effect of H(2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 20(21):6008-6016.
44. Ingenbleek Y (2011) The oxidative stress of hyperhomocysteinemia results from reduced bioavailability of sulfur-containing reductants. Open Clin Chem J 4:34-44.
45. Elrod JW, et al. (2007) Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci USA 104(39): 15560-15565.
46. Chang L, et al. (2008) Hydrogen sulfide inhibits myocardial injury induced by homo-cysteine in rats. Amino Acids 34(4):573-585.
47. Yonezawa D, et al. (2007) A protective role of hydrogen sulfide against oxidative stress in rat gastric mucosal epithelium. Toxicology 241(1-2):11-18.
48. Zanardo RC, et al. (2006) Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation. FASEB J 20(12):2118-2120.
49. Troen AM, et al. (2008) B-vitamin deficiency causes hyperhomocysteinemia and vascular cognitive impairment in mice. Proc Natl Acad Sci USA 105(34):12474-12479.
50. Wallace JL, Le T, Carter L., Appleyard CB, Beck P.L. (1995) Hapten-induced chronic colitis in the rat: Alternatives to trinitrobenzene sulfonic acid. J Pharmacol Toxicol Methods 33(4):237-239.
51. Kim JJ, et al. (2013) Targeted inhibition of serotonin type 7 (5-HT7) receptor function modulates immune responses and reduces the severity of intestinal inflammation. J Immunol 190(9):4795-4804.
52. Boughton-Smith NK, Wallace JL, Whittle BJR (1988) Relationship between arachidonic acid metabolism, myeloperoxidase activity and leukocyte infiltration in a rat model of inflammatory bowel disease. Agents Actions 25(1-2):115-123.
53. Mittal R, et al. (2010) IL-10 administration reduces PGE-2 levels and promotes CR3-mediated clearance of Escherichia coli K1 by phagocytes in meningitis. J Exp Med 207(6):1307-1319.
54. Stipanuk MH, Beck P.W. (1982) Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J 206(2):267-277.
55. Chávez-Piña AE, et al. (2008) Lack of effects of acemetacin on signalling pathways for leukocyte adherence may explain its gastrointestinal safety. Br J Pharmacol 155(6): 857-864.