SULFATE-REDUCING BACTERIA OF THE HUMAN INTESTINE. II. THE ROLE IN THE DEVELOPMENT OF DISEASES

I. V. Kushkevych


DOI: http://dx.doi.org/10.30970/sbi.0602.207

Abstract


The modern literature data about the role of microflora in the diseases of the large intestine of man are summarized. Special attention is paid to the sulfate-reducing bacteria role in ulcerative colitis development. The basic ways of hydrogen metabolism by sulfate-reducing bacteria in the large intestine are characterized. The influence and the action mechanism of the main product of the bacteria metabolism – hydrogen sulphide on cells are described. Antimicrobial drugs that are used during bowel diseases are characterized. The probiotics significance for the intestine diseases prevention and treatment is briefly described.


Keywords


sulfate-reducing bacteria, sulfates, hydrogen sulfide, disease, ulcerative colitis, intestinal microflora

References


1. Асауленко Л.Г., Пуріш Л.М., Козлова І.П. Етапи формування біоплівки сульфатвідновлювальними бактеріями. Мікробіол. журн, 2004; 66(3): 72-79.

2. Кушкевич І.В. Сульфатвідновлювальні бактерії кишечника людини. I. Дисиміляційне відновлення сульфату. Біологічні студії/Studia Biologica, 2012; 6(1): 149-180.
https://doi.org/10.30970/sbi.0601.181

3. Перетятко Т., Галушка А., Гнатуш С. та ін. Використання органічних сполук сульфатвідновлювальними бактеріями роду Desulfovibrio. Наук. вісн. Ужгород. ун-ту. Сер. Біол, 2006; 18: 157-160.

4. Anwar H., Dasgupta M.K., Costerton J.W. Testing the susceptibility of bacteria in biofilms to antibacterial agents. Antimicrob. Ag. Chemother, 1990; 34: 2043-2046.
https://doi.org/10.1128/AAC.34.11.2043
PMid:2073094 PMCid:PMC171995

5. Aslam M., Batten J.J., Florin T.H.J. et al. Hydrogen sulphide induceddamage to the mucosal barrier in the rat. Gut, 1992; 33: 69.

6. Attene-Ramos M.S., Wagner E.D., Gaskins H.R., Plewa M.J. Hydrogen sulfide induces direct radical-associated DNA damage. Mol. Cancer Res, 2007; 5: 455-459.
https://doi.org/10.1158/1541-7786.MCR-06-0439
PMid:17475672

7. Bamba T., Matsuda H., Endo M., Fujiyama Y. The pathogenic role of Bacteroides vulgatus in patients with ulcerative colitis. J. Gastroenterol,1995; 30(8): 45-47.

8. Barton L.L., Hamilton W.A. Sulphate-reducing Bacteria. Environmental and Engineered. Cambridge University Press, 2007; 553 p.
https://doi.org/10.1017/CBO9780511541490

9. Baskar R., Li L., Moore P.K. Hydrogen sulfide-induces DNA damage and changes in apoptotic gene expression in human lung fibroblast cells. FASEB J, 2007; 21: 247-255.
https://doi.org/10.1096/fj.06-6255com
PMid:17116745

10. Breznak J.A., Switzer J.M. Acetate synthesis from H2 plus CO2 by termite microbes. Appl. Environ. Microbiol, 1986; 52: 623-630.

11. Brigidi P., Swennen E., Rizzello F. et al. Effects of rifaximin administration on the intestinal microbiotia in patients with ulcerative colitis. J. Chemotherapy, 2002; 14: 290-295.
https://doi.org/10.1179/joc.2002.14.3.290
PMid:12120885

12. Burke D., Axon A. Adhesive E. coli in inflammatory bowel disease and infective diarrhoea. BMJ, 1988; 297: 102-104.
https://doi.org/10.1136/bmj.297.6641.102
PMid:3044496 PMCid:PMC1833778

13. Campieri M., Gionchetti P. Bacteria as the cause of ulcerative colitis. Gut, 2001; 48: 132-135.
https://doi.org/10.1136/gut.48.1.132
PMid:11115835 PMCid:PMC1728175

14. Campieri M., Gionchetti P. Probiotics in inflammatory bowel disease: New insight to pathogenesis or a possible therapeutic alternative? Gastroenterology, 1999; 116: 1246-1260.
https://doi.org/10.1016/S0016-5085(99)70029-6

15. Chadwick V.S. Etiology of chronic ulcerative colitis and Crohn's disease. In: The Large Intestine: Physiology, Pathophysiology and Disease. S.F. Phillips J.H. Pemberton, R.G. Shorter R.G. ed. Raven Press Ltd, New York, 1991; 445-463.

16. Christl S.U., Gibson G.R., Murgatroyd P.R. et al. Impaired H2 metabolism in pneumatosis cystoides intestinalis. Gastroenterology, 1991; 100: 203.

17. Christl S.U., Murgatroyd P.R., Gibson G.R., Cummings J.H. Production, excretion and metabolism of hydrogen in the large intestine. Gastroenterology, 102: 1269-1277.
https://doi.org/10.1016/0016-5085(92)70022-4

18. Cohavy O., Bruckner D., Gordon L.K. et al. Colonic bacteria express an ulcerative colitis pANCA-related protein epitope. Infect. Immun, 2000; 68: 1542-1548.
https://doi.org/10.1128/IAI.68.3.1542-1548.2000
PMid:10678972 PMCid:PMC97313

19. Croucher S.C., Houston A.P., Bayliss C.E., Turner R.J. Bacterial populations associated with different regions of the human colon wall. Appl. Environ. Microbiol, 1983; 45: 1025-1033.

20. Cummings J.H., Macfarlane G.T., Macfarlane S. Intestinal Bacteria and Ulcerative Colitis. Curr. Issues Intest. Microbiol., 2003; 4: 9-20.

21. Deplancke B., Gaskins H.R. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr, 2001; 73: 1131-1141.
https://doi.org/10.1093/ajcn/73.6.1131S
PMid:11393191

22. Duffy M., O'Mahony L., Coffey J.C. et al. Sulfate-reducing bacteria colonize pouches formed for ulcerative colitis but not for familial adenomatous polyposis. Dis. Colon. Rectum, 2002; 45: 384-388.
https://doi.org/10.1007/s10350-004-6187-z
PMid:12068199

23. Fabia R, Ar'Rajab A., Johansson M.-L. et al. Impairment of bacterial flora in human ulcerative colitis and experimental colitis in the rat. Digestion, 1993; 54: 248-255.
https://doi.org/10.1159/000201045
PMid:8243838

24. Farrell R.J., LaMont J.T. Microbial factors in inflammatory bowel disease. Gastroenterol. Clin. North Am, 2002; 31: 41-62.
https://doi.org/10.1016/S0889-8553(01)00004-8

25. Farrell R.J., Peppercorn M.A. Ulcerative colitis. Lancet, 2002; 359: 331-340.
https://doi.org/10.1016/S0140-6736(02)07499-8

26. Finkelstein J.D. Inborn errors of sulfur-containing amino acid metabolism. J. Nutr, 2006; 136: 1750-1754.
https://doi.org/10.1093/jn/136.6.1750S
PMid:16702350

27. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology, 1998; 115: 182-205.
https://doi.org/10.1016/S0016-5085(98)70381-6

28. Fiorucci S., Distrutti E., Cirino G., Wallace J.L. The emerging roles of hydrogen sulfide in the gastrointestinal tract and liver. Gastroenterology, 2006; 131: 259-271.
https://doi.org/10.1053/j.gastro.2006.02.033
PMid:16831608

29. Fite A., Macfarlane G.T., Cummings J.H. et al. Identification and quantitation of mucosal and faecal desulfovibrios using real time polymerase chain reaction. Gut, 2004; 53: 523-529.
https://doi.org/10.1136/gut.2003.031245
PMid:15016746 PMCid:PMC1774019

30. Florin T.H. Hydrogen sulphide and total acid-volatile sulphide in faeces, determined with a direct spectrophotometric method. Clin. Chim. Acta, 1991; 196: 127-134.
https://doi.org/10.1016/0009-8981(91)90065-K

31. Florin T.H.J., Gibson G.R., Neale G., Cummings J.H. A role for sulphate-reducing bacteria in ulcerative colitis? Gastroenterology, 1990; 98: 170.

32. Florin T.H.J., Neale G., Gibson G.R. et al. Metabolism of dietary sulphate: absorption and excretion in humans. Gut, 1991; 32: 766-773.
https://doi.org/10.1136/gut.32.7.766
PMid:1855683 PMCid:PMC1378993

33. Florin T.H.J., Neale G., Goretski S., Cummings J.H. The sulfate content of foods and beverages. J. Food Comp. Analysis, 1993; 6: 140-151.
https://doi.org/10.1006/jfca.1993.1016

34. Fox J.G., Dewhirst F.E., Fraser G.J. et al. Intracellular Campylobacter-like organism from ferrets and hamsters with proliferative bowel disease is a Desulfovibrio sp. J. Clin. Microbiol, 1994; 32: 1229-1237.

35. Gardiner K.R., Halliday M.I., Barclay G.R. et al. Significance of systemic endotoxaemia in inflammatory bowel disease. Gut, 1995; 36: 897-901.
https://doi.org/10.1136/gut.36.6.897
PMid:7615280 PMCid:PMC1382629

36. Ge Y., Konrad M.A., Matherly L.H., Taub J.W. Transcriptional regulation of the human cystathionine beta-synthase-1b basal promoter: synergistic transactivation by transcription factors NF-Y and Sp1/Sp3. Biochem. J, 2001; 357: 97-105.
https://doi.org/10.1042/bj3570097
PMid:11415440 PMCid:PMC1221932

37. Giaffer M.H., Holdsworth C.D., Duerden B.I. The assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. Med. Microbiol, 1991; 35: 238-243.
https://doi.org/10.1099/00222615-35-4-238
PMid:1941994

38. Gibson G.R., Cummings J.H., Macfarlane G.T. Growth and activities of sulphate-reducing bacteria in gut contents of health subjects and patients with ulcerative colitis. FEMS Microbiol. Ecol, 1991; 86: 103-112.
https://doi.org/10.1111/j.1574-6968.1991.tb04799.x

39. Gibson G.R., Macfarlane G.T., Cummings J.H. Sulphate reducing bacteria and hydrogen metabolism in the human large intestine. Gut, 1993; 34: 437-439.
https://doi.org/10.1136/gut.34.4.437
PMid:8491386 PMCid:PMC1374298

40. Gibson G.R., Macfarlane S., Macfarlane G.T. Metabolic interactions involving sulphate-reducing and methanogenic bacteria in the human large intestine. FEMS Microbiol. Ecol, 1993; 12: 117-125.
https://doi.org/10.1111/j.1574-6941.1993.tb00023.x

41. Gilat T., Leichtman G., Delpre G. et al. A comparison of metronidazole and sulfasalazine in the maintenance of remission in patients with ulcerative colitis. J. Clin. Gastroenterol, 1989; 11: 392-395.
https://doi.org/10.1097/00004836-198908000-00008
PMid:2569488

42. Gionchetti P., Rizzello F., Venturi A. et al. Antibiotic combination therapy in patients with chronic, treatment-resistant pouchitis. Aliment. Pharmacol. Ther, 1999; 13: 713-718.
https://doi.org/10.1046/j.1365-2036.1999.00553.x

43. Guarner F., Malagelada J.R. Gut flora in health and disease. Lancet, 2003; 361: 512-519.
https://doi.org/10.1016/S0140-6736(03)12489-0

44. Hans A.U., Scholmerich J., Gross V., Falk W. The role of the resident intestinal flora in acute and chronic dextran sulfate sodium-induced colitis in mice. Eur. J. Gastroenterol. Hepatol, 2000; 12: 267-273.
https://doi.org/10.1097/00042737-200012030-00002

45. Hooper L.V., Wong M.H., Thelin A. et al. Molecular analysis of commensal host-microbial relationships in the intestine. Science, 2001; 291: 881-884.
https://doi.org/10.1126/science.291.5505.881
PMid:11157169

46. Jiang Z.D., Ke S., Palazzini E. et al. In vitro activity and fecal concentration of rifaximin after oral administration. Antimicrob. Ag. Chemother, 2000; 44: 2205-2206.
https://doi.org/10.1128/AAC.44.8.2205-2206.2000
PMid:10898704 PMCid:PMC90042

47. Kennedy R.J., Hoper M., Weir H. et al. Probiotic therapy stabilises the gut mucosal barrier in the IL-10 knockout model of mouse colitis. Br. J. Surg, 2000; 87: 669-670.

48. Kleessen B., Kroesen A.J., Buhr H.J., Blaut M. Mucosal and invading bacteria in patients with inflammatory bowel disease compared with controls. Scand. J. Gastroenterol, 2002; 37: 1034-1041.
https://doi.org/10.1080/003655202320378220
PMid:12374228

49. Kraus J.P., Oliveriusova J., Sokolova J. et al. The human cystathionine beta-synthase (CBS) gene: complete sequence, alternative splicing, and polymorphisms. Genomics, 1998; 52: 312-324.
https://doi.org/10.1006/geno.1998.5437
PMid:9790750

50. Kristiansson J.K., Schonheit P., Thauer R.K. Different Ks values for hydrogen of methanogenic bacteria and sulfate reducing bacteria: an explanation for the apparent inhibition of methanogenesis by sulfate. Arch. Microbiol, 1982; 131: 278-282.
https://doi.org/10.1007/BF00405893

51. Kruis W., Schutz E., Fric P. et al. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment. Pharmacol. Ther, 1999; 11: 853-858.
https://doi.org/10.1046/j.1365-2036.1997.00225.x

52. Levitt M.D., Furne J., Springfield J. et al. Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. J. Clin. Invest, 1999; 104: 1107-1114.
https://doi.org/10.1172/JCI7712
PMid:10525049 PMCid:PMC408582

53. Levonen A.L., Lapatto R., Saksela M., Raivio K.O. Human cystathionine gamma-lyase: developmental and in vitro expression of two isoforms. Biochem. J, 2000; 347: 291-295.
https://doi.org/10.1042/bj3470291
PMid:10727430 PMCid:PMC1220959

54. Lewis S., Brazier J., Beard D. et al. Effects of metronidazole and oligofructose on faecal concentrations of sulphate-reducing bacteria and their activity in human volunteers. Scand. J. Gastroenterol, 2005; 40: 1296-1303.
https://doi.org/10.1080/00365520510023585
PMid:16334439

55. Linskens R.K., Huijsdens X.W., Savelkoul P.H.M. et al. The bacterial flora in inflammatory bowel disease: current insights in pathogenesis and the influence of antibiotics and probiotics. Scand. J. Gastroenterol, 2001; 36: 29-40.
https://doi.org/10.1080/003655201753265082

56. Lobo A.J., Burke D.A., Sobala G.M., Axon A.T.R. Oral tobramycin in ulcerative colitis: effect on maintenance of remission. Aliment. Pharmacol. Ther, 1993; 7: 155-158.
https://doi.org/10.1111/j.1365-2036.1993.tb00084.x

57. Loftus E.V., Silverstein M.D., Sandborn W.J. et al. Ulcerative colitis in Olmsted County, Minnesota, 1940- 1993: incidence, prevalence, and survival. Gut, 2000; 46: 336-343.
https://doi.org/10.1136/gut.46.3.336
PMid:10673294 PMCid:PMC1727835

58. Loubinoux J., Mory F., Pereira I.A., Le Faou A.E. Bacteremia caused by a strain of Desulfovibrio related to the provisionally named Desulfovibrio fairfieldensis. J. Clin. Microbiol, 2000; 38: 931-934.

59. Lovley D.R., Klug M.J. Sulfate-reducers can outcompete methanogens at freshwater sulfate concentrations. Appl. Environ. Microbiol, 1983; 45: 187-192.

60. Lukas M., Konecny M., Zboril V. Rifaximin in patients with mild to moderate activity of ulcerative colitis: An open label study. Gastroenterology, 2002; 122: 434.

61. Macfarlane S., Dillon J.F. Microbial biofilms in the human gastrointestinal tract. J. Appl. Microbiol, 2007; 102: 1187-1196.
https://doi.org/10.1111/j.1365-2672.2007.03287.x
PMid:17448154

62. Macfarlane S., Hopkins M.J., Macfarlane G.T. Bacterial growth and metabolism on surfaces in the large intestine. Microb. Ecol. Hlth. Dis, 2000; 2: 64-72.
https://doi.org/10.1080/089106000750060314

63. Macpherson A., Khoo U.Y., Forgacs I. et al. Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria. Gut, 1996; 38: 365-375.
https://doi.org/10.1136/gut.38.3.365
PMid:8675088 PMCid:PMC1383064

64. Madsen K.L., Doyle J.S., Jewell L.D. et al. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology, 1999; 116: 1107-1114.
https://doi.org/10.1016/S0016-5085(99)70013-2

65. Madsen K.L., Doyle J.S., Tavernini M.M. et al. Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology, 2000; 118: 1094-1105.
https://doi.org/10.1016/S0016-5085(00)70362-3

66. Mantzaris G.J., Archavlis E., Christoforidis P. et al. A prospective randomized controlled trial of oral ciprofloxacin in acute ulcerative colitis. Am. J. Gastroenterol, 1997; 92: 454-456.

67. Mantzaris G.J., Petraki K., Archavlis E. et al. A prospective randomised controlled trial of intravenous ciprofloxacin as an adjunct to corticosteroids in acute, severe ulcerative colitis. Scand. J. Gastroenterol, 2001; 36: 971-974.
https://doi.org/10.1080/003655201750305503
PMid:11521989

68. Mao Y., Nobaek S., Kasravi B. et al. The effects of Lactobacillus strains and oat fiber on methotrexateinduced enterocolitis in rats. Gastroenterology, 1996; 111: 334-344.
https://doi.org/10.1053/gast.1996.v111.pm8690198
PMid:8690198

69. Marcus R., Watt J. Ulcerative disease of the colon in laboratory animals induced by pepsin inhibitors. Gastroenterology, 1974; 67: 473-483.
https://doi.org/10.1016/S0016-5085(19)32849-5

70. Matsuda H., Fujiyama Y., Andoh A. et al. Characterization of antibody responses against rectal mucosa-associated bacterial flora in patients with ulcerative colitis. J. Gastroenterol. Hepatol, 2000; 15: 61-68.
https://doi.org/10.1046/j.1440-1746.2000.02045.x
PMid:10719749

71. Moehle C., Ackermann N., Langmann T. et al. Aberrant intestinal expression and allelic variants of mucin genes associated with inflammatory bowel disease. J. Mol. Med, 2006; 84: 1055-1066.
https://doi.org/10.1007/s00109-006-0100-2
PMid:17058067

72. Montgomery S.M., Morris D.L., Thompson N.P. et al. Prevalence of inflammatory bowel disease in British 26 year olds: national longitudinal birth cohort. Br. Med. J, 1998; 316: 1058-1059.
https://doi.org/10.1136/bmj.316.7137.1058
PMid:9552907 PMCid:PMC28509

73. Okayasu I., Hatakeyama S., Yamada M. et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology, 1990; 98: 694-702.
https://doi.org/10.1016/0016-5085(90)90290-H

74. Onderdonk A.B. Role of the intestinal microflora in ulcerative colitis. In: Human Intestinal Microflora in Health and Disease. D.J. Hentges ed. Academic Press, London, 1983; 481-493.
https://doi.org/10.1016/B978-0-12-341280-5.50024-0

75. Onderdonk A.B., Hermos J.A., Dzink J.L., Bartlett J.G. Protective effect of metronidazole in experimental ulcerative colitis. Gastroenterology, 1978; 74: 521-526.
https://doi.org/10.1016/0016-5085(78)90289-5

76. Pacifici G.M., Romiti P., Santerini S., Giuliani L. S-methyltransferases in human intestine: differential distribution of the microsomal thiol methyltransferase and cytosolic thiopurine methyltransferase along the human bowel. Xenobiotica, 1993; 23: 671-679.
https://doi.org/10.3109/00498259309059404
PMid:8212740

77. Pathmakanthan S., Thornley J.P., Hawkey C.J. Mucosally associated bacterial flora of the human colon: quantitative and species specific differences between normal and inflammed colonic biopsies. Microb. Ecol. Hlth. Dis, 1999; 11: 169-174.
https://doi.org/10.3402/mehd.v11i3.7901

78. Pitcher M.C., Beatty E.R., Cummings J.H. The contribution of sulphate reducing bacteria and 5-aminosalicylic acid to faecal sulphide in patients with ulcerative colitis. Gut, 2000; 46: 64-72.
https://doi.org/10.1136/gut.46.1.64
PMid:10601057 PMCid:PMC1727787

79. Pitcher M.C., Cummings J.H. Hydrogen sulphide: a bacterial toxin in ulcerative colitis? Gut, 1996; 39: 1-4.
https://doi.org/10.1136/gut.39.1.1
PMid:8881797 PMCid:PMC1383219

80. Podolsky D.K. Inflammatory bowel disease. N. Engl. J. Med, 2002; 347: 417-429.
https://doi.org/10.1056/NEJMra020831
PMid:12167685

81. Postgate J.R. The sulfate-reducing bacteria. 2nd ed. Cambridge: Cambridge Univ. Press, 1984; 199 p.

82. Poxton I.R., Brown R., Sawyerr A., Ferguson A. Mucosa-associated bacterial flora of the human colon. J. Med. Microbiol, 1997; 46: 85-91.
https://doi.org/10.1099/00222615-46-1-85
PMid:9003751

83. Prins R.A., Lankhorst A. Synthesis of acetate from CO2 in the cecum of some rodents. FEMS Microbiol. Letts, 1977; 1: 255-258.
https://doi.org/10.1111/j.1574-6968.1977.tb00627.x

84. Qi K., Lu C.D., Owens F.N. Sulfate supplementation of Angora goats: sulfur metabolism and interactions with zinc, copper and molybdenum. Small Ruminant Research, 1993; 11: 209-225.
https://doi.org/10.1016/0921-4488(93)90046-K

85. 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: 288-296.
https://doi.org/10.1152/ajpgi.00324.2005
PMid:16500920

86. Rath H.C., Schultz M., Freitag R. et al. Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice. Infect. Immun, 2001; 69: 227-2285.
https://doi.org/10.1128/IAI.69.4.2277-2285.2001
PMid:11254584 PMCid:PMC98156

87. Rembacken B.J., Snelling A.M., Hawkey P.M. et al. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet, 1999; 354: 636-639.
https://doi.org/10.1016/S0140-6736(98)06343-0

88. Rizzello F., Gionchetti P., Venturi A. et al. Rifaximin systemic absorption in patients with ulcerative colitis. Eur. J. Clin. Pharmacol, 1998; 54: 91-93.
https://doi.org/10.1007/s002280050426
PMid:9591937

89. Roediger W.E. The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet, 1980; 2: 712-715.
https://doi.org/10.1016/S0140-6736(80)91934-0

90. Roediger W.E.W., Duncan A., Kapaniris O., Millard S. Sulphide impairment of substrate oxidation in rat colonocytes: A biochemical basis for ulcerative colitis? Clin. Sci, 1993; 85: 1-5.
https://doi.org/10.1042/cs0850623
PMid:8287651

91. Roediger W.E.W., Duncan S., Kapaniris O., Millard S. Reducing sulfur compounds of the colon impair colonocyte nutrition: Implications for ulcerative colitis. Gastroenterology, 1993; 104: 802-809.
https://doi.org/10.1016/0016-5085(93)91016-B

92. Rowan F.E., Docherty N.G., Coffey J.C., O'Connell P.R. Sulphate-reducing bacteria and hydrogen sulphide in the aetiology of ulcerative colitis. British Journal of Surgery, 2009; 96: 151-158.
https://doi.org/10.1002/bjs.6454
PMid:19160346

93. Ruseler van Embden J.G.H., Schouten W.R., van Lieshout L.M.C. Pouchitis: result of microbial imbalance? Gut, 1994; 35: 658-664.
https://doi.org/10.1136/gut.35.5.658
PMid:8200561 PMCid:PMC1374752

94. Sadlack B., Merz H., Schorle H. et al. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell, 1993; 75: 253-261.
https://doi.org/10.1016/0092-8674(93)80067-O

95. Saitoh S., Noda S., Aiba Y. et al. Bacteroides ovatus as the predominant commensal intestinal microbe causing a systemic antibody response in inflammatory bowel disease. Clin. Diagnost. Lab. Immunol, 2002; 9: 54-59.
https://doi.org/10.1128/CDLI.9.1.54-59.2002
PMid:11777829 PMCid:PMC119885

96. Sartor R.B., Rath H.C., Sellon H.K. Microbial factors in chronic intestinal inflammation. Curr. Opin. Gastroenterol, 1996; 12: 327-333.
https://doi.org/10.1097/00001574-199607000-00003

97. Satsangi J., Landers C.J., Welsh K.I. et al. The presence of anti neutrophil antibodies reflects clinical and genetic heterogeneity within inflammatory bowel disease. Inflamm. Bowel. Dis, 1998; 4: 18-26.
https://doi.org/10.1097/00054725-199802000-00004
PMid:9552224

98. Schultsz C., Moussa M., van Ketel et al. Frequency of pathogenic and enteroadherent Escherichia coli in patients with inflammatory bowel disease and controls. J. Clin. Pathol, 1997; 50: 573-579.
https://doi.org/10.1136/jcp.50.7.573
PMid:9306938 PMCid:PMC500056

99. Schultz M., Veltkamp C., Dieleman L.A. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel. Dis, 2002; 8: 71-80.
https://doi.org/10.1097/00054725-200203000-00001
PMid:11854603

100. Sekirov I., Russell S.L., Antunes L.C.M., Finlay B.B. Gut Microbiota in Health and Disease. Physiol Rev, 2010; 90: 859-904.
https://doi.org/10.1152/physrev.00045.2009
PMid:20664075

101. Siddiqui A., Ancha H., Tedesco D. et al. Antioxidant therapy with N-acetylcysteine plus mesalamine accelerates mucosal healing in a rodent model of colitis. Dig. Dis. Sci, 2006; 51: 698-705.
https://doi.org/10.1007/s10620-006-3194-z
PMid:16614991

102. Smith L., Kruszyna H., Smith R.P. The effect of methaemoglobin on the inhibition of cytochrome c oxidase by cyanide, sulfide or azide. Biochem. Pharmacol, 1977; 22: 47-50.

103. Steffen R. Rifaximin: A nonabsorbed antimicrobial as a new tool for treatment of travelers' diarrhea. J. Travel Med, 2001; 8: 34-39.
https://doi.org/10.1111/j.1708-8305.2001.tb00545.x
PMid:12186672

104. Stein J., Schroder O., Milovic V., Caspary W. Mercaptoproprionate inhibits butyrate uptake in isolated apical membrane vesicles of the rat distal colon. Gastroenterology, 1995; 108: 673-679.
https://doi.org/10.1016/0016-5085(95)90438-7

105. Strocchi A., Ellis C.J., Fume J.K., Levitt M.D. Study of constancy of hydrogen-consuming flora of human colon. Dig. Dis. Sci, 1994; 39: 494-497.
https://doi.org/10.1007/BF02088333
PMid:8131685

106. Takeuchi H., Setoguchi T., Machigashira M. et al. Hydrogen sulfide inhibits cell proliferation and induces cell cycle arrest via an elevated p21 Cip1 level in Ca9-22 cells. J. Periodontal Res, 2008; 43: 90-95.
https://doi.org/10.1111/j.1600-0765.2007.00999.x
PMid:18086166

107. Truelove S.C., Jewell D.P. Intensive intravenous regimen for severe attacks of ulcerative colitis. Lancet, 1974; 1: 1067-1070.
https://doi.org/10.1016/S0140-6736(74)90552-2

108. Turunen U.M., Saarinen M., Farkkila M.A. et al. Antibody responses to Escherichia coli, Proteus mirabilis and Klebsiella, Pneumoniae in ulcerative colitis during ciprofloxacin treatment. Gastroenterology, 1999; 116: 834.

109. Venturi A., Gionchetti P. Rizzello F. et al. Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment. Pharmacol. Ther, 1999; 13: 1103-1108.
https://doi.org/10.1046/j.1365-2036.1999.00560.x

110. Wallace J.L., Dicay M., McKnight W., Martin G.R. Hydrogen sulfide enhances ulcer healing in rats. FASEB J, 2007; 21: 4070-4076.
https://doi.org/10.1096/fj.07-8669com
PMid:17634391

111. Walmsey R.S., Anthony A., Slim R. et al. Absence of Escherichia coli, Listeria monocytogenes, and Klebsiella pneumoniae antigens within inflammatory bowel disease tissues. J. Clin. Pathol, 1998; 51: 657-661.
https://doi.org/10.1136/jcp.51.9.657
PMid:9930068 PMCid:PMC500901

112. Wang R. Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J, 2002; 16: 1792-1798.
https://doi.org/10.1096/fj.02-0211hyp
PMid:12409322

113. Wilson K., Mudra M., Furne J., Levitt M. 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.
https://doi.org/10.1007/s10620-007-9854-9
PMid:17551834

114. Yang G., Cao K., Wu L., Wang R. Cystathionine gamma-lyase overexpression inhibits cell proliferation via a H2S-dependent modulation of ERK1/2 phosphorylation and p21Cip/WAK-1. J. Biol. Chem, 2004; 279: 49199-49205.
https://doi.org/10.1074/jbc.M408997200
PMid:15347670

115. Zinkevich V.V., Beech I.B. Screening of sulfate-reducing bacteria in colonoscopy samples from healthy and colitic human gut mucosa. FEMS Microbiol. Ecol, 2000; 34: 147-155.
https://doi.org/10.1016/S0168-6496(00)00086-6

116. Zoetendal E.G., VonWright A., Vilpponen-Salmela T. et al. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl. Environ. Microbiol, 2002; 68: 3401-3407.
https://doi.org/10.1128/AEM.68.7.3401-3407.2002
PMid:12089021 PMCid:PMC126800


Refbacks

  • There are currently no refbacks.


Copyright (c) 2012 Studia biologica

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.