Advertisement

Digestive Diseases and Sciences

, Volume 56, Issue 3, pp 707–714 | Cite as

The Effect of Exopolysaccharide-Producing Probiotic Strains on Gut Oxidative Damage in Experimental Colitis

  • Neriman Şengül
  • Sevil Işık
  • Belma Aslım
  • Gülberk Uçar
  • Ali Eba Demirbağ
Original Article

Abstract

Background

Oxidative stress plays a role in disease initiation and progression in inflammatory bowel disease (IBD) and manipulation of this pathway may attenuate disease progress. In this study, the effect of exopolysaccharide (EPS)-producing probiotic bacteria on gut oxidative damage was evaluated in a rat model of experimental colitis.

Methods

Colitis was induced by intracolonic administration of acetic acid. Rats were treated daily with two probiotic strains, L. delbrueckii subsp. bulgaricus B3 strain (EPS of 211 mg/l; high-EPS group) or L. delbrueckii subsp. bulgaricus A13 strain (EPS of 27 mg/l; low-EPS group), which were given directly into the stomach. Noncolitis-fed control and preventative groups were only treated with the high-EPS producing strain. Antioxidant enzyme activities (superoxide dismutase, catalase, total glutathione, reduced glutathione, glutathione disulfide) and lipid peroxidation were measured in colonic tissue samples after a treatment period of 7 days.

Results

Significant oxidative damage was associated with a higher level of malondialdehyde (MDA) activity and reduced antioxidant enzyme activities in the colitis model group. All antioxidant enzyme activities were higher in both probiotic-treated groups compared with those of the colitis model group (P < 0.001). Lipid peroxidation was significantly ameliorated in both probiotic groups. The improvement of oxidative stress parameters was significantly more in the high-EPS group than in the low-EPS group (P < 0.001).

Conclusions

EPS-producing probiotic bacteria significantly attenuate oxidative stress in experimental colitis. Increased EPS production gives rise to a better probiotic function. These results suggest that EPS molecules could revaluate probiotic strains and exert their beneficial effects on the host and this may have a therapeutic potential.

Keywords

Inflammatory bowel disease Exopolysaccharides Probiotic Oxidative damage 

References

  1. 1.
    Harris ML, Schiller HJ, Reilly PM, Donowitz M, Grisham MB, Bulkley GB. Free radicals and other reactive oxygen metabolites in inflammatory bowel disease: cause, consequence or epiphenomenon? Pharmacol Ther. 1992;53:375–408.CrossRefPubMedGoogle Scholar
  2. 2.
    Pavlick KP, Laroux FS, Fuseler J, et al. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic Biol Med. 2002;33:311–322.CrossRefPubMedGoogle Scholar
  3. 3.
    Matés JM, Pérez-Gómez C, Núñez de Castro I. Antioxidant enzymes and human diseases. Clin Biochem. 1999;32:595–603.CrossRefPubMedGoogle Scholar
  4. 4.
    Buffinton GD, Doe WF. Depleted mucosal antioxidant defences in inflammatory bowel disease. Free Radic Biol Med. 1995;19:911–918.CrossRefPubMedGoogle Scholar
  5. 5.
    Kruidenier L, Kuiper I, Lamers CB, Verspaget HW. Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol. 2003;201:28–36.CrossRefPubMedGoogle Scholar
  6. 6.
    Kruidenier L, Kuiper I, Van Duijn W, et al. Imbalanced secondary mucosal antioxidant response in inflammatory bowel disease. J Pathol. 2003;201:17–27.CrossRefPubMedGoogle Scholar
  7. 7.
    Sido B, Hack V, Hochlehnert A, Lipps H, Herfarth C, Dröge W. Impairment of intestinal glutathione synthesis in patients with inflammatory bowel disease. Gut. 1998;42:485–492.CrossRefPubMedGoogle Scholar
  8. 8.
    Fioramonti J, Theodorou V, Bueno L. Probiotics: what are they? What are their effects on gut physiology? Best Pract Res Clin Gastroenterol. 2003;17:711–724.CrossRefPubMedGoogle Scholar
  9. 9.
    Rioux KP, Madsen KL, Fedorak RN. The role of enteric microflora in inflammatory bowel disease: human and animal studies with probiotics and prebiotics. Gastroenterol Clin North Am. 2005;34:465–482.CrossRefPubMedGoogle Scholar
  10. 10.
    Prantera C, Scribano ML, Falasco G, Andreoli A, Luzi C. Ineffectiveness of probiotics in preventing recurrence after curative resection for Crohn’s disease: a randomised controlled trial with Lactobacillus GG. Gut. 2002;51:405–409.CrossRefPubMedGoogle Scholar
  11. 11.
    Shibolet O, Karmeli F, Eliakim R, et al. Variable response to probiotics in two models of experimental colitis in rats. Inflamm Bowel Dis. 2002;8:399–406.CrossRefPubMedGoogle Scholar
  12. 12.
    Ito M, Ohishi K, Yoshida Y, Yokoi W, Sawada H. Antioxidative effects of lactic acid bacteria on the colonic mucosa of iron-overloaded mice. J Agric Food Chem. 2003;51:4456–4460.CrossRefPubMedGoogle Scholar
  13. 13.
    Peran L, Camuesco D, Comalada M, et al. Preventative effects of a probiotic, Lactobacillus salivarius ssp. salivarius, in the TNBS model of rat colitis. World J Gastroenterol. 2005;11:5185–5192.PubMedGoogle Scholar
  14. 14.
    Sengül N, Aslim B, Uçar G, et al. Effects of exopolysaccharide-producing probiotic strains on experimental colitis in rats. Dis Colon Rectum. 2006;49:250–258.CrossRefPubMedGoogle Scholar
  15. 15.
    Laws A, Gu Y, Marshall V. Biosynthesis, characterization, and design of bacterial exopolysaccharides from lactic acid bacteria. Biotechnol Adv. 2001;19:597–625.CrossRefPubMedGoogle Scholar
  16. 16.
    Choi SS, Kim Y, Han KS, You S, Oh S, Kim SH. Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett Appl Microbiol. 2006;42:452–458.CrossRefPubMedGoogle Scholar
  17. 17.
    Aslim B, Beyatli Y, Yuksekdag ZN. Productions and monomer compositions of exopolysaccharides by Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus strains isolated from traditional home-made yoghurts and raw milk. Int J Food Sci Technol. 2006;41:973–979.CrossRefGoogle Scholar
  18. 18.
    Draper HH, Hadley M. Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 1990;186:421–431.CrossRefPubMedGoogle Scholar
  19. 19.
    Akerboom TPM, Sies H. Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol. 1981;77:373–382.CrossRefPubMedGoogle Scholar
  20. 20.
    Ueda M, Mozaffar S, Tanaka A. Catalase from Candida boidinii 2201. Methods Enzymol. 1990;188:463–467.CrossRefPubMedGoogle Scholar
  21. 21.
    Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967;70:158–169.PubMedGoogle Scholar
  22. 22.
    Misra HP, Fridovich I. The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247:3170–3175.PubMedGoogle Scholar
  23. 23.
    Naito Y, Takagi T, Yoshikawa T. Molecular fingerprints of neutrophil-dependent oxidative stress in inflammatory bowel disease. J Gastroenterol. 2007;42:787–798.CrossRefPubMedGoogle Scholar
  24. 24.
    Hirche TO, Gaut JP, Heinecke JW, Belaaouaj A. Myeloperoxidase plays critical roles in killing Klebsiella pneumoniae and inactivating neutrophil elastase: effects on host defense. J Immunol. 2005;174:1557–1565.PubMedGoogle Scholar
  25. 25.
    Arseneau KO, Tamagawa H, Pizarro TT, Cominelli F. Innate and adaptive immune responses related to IBD pathogenesis. Curr Gastroenterol Rep. 2007;9:508–512.CrossRefPubMedGoogle Scholar
  26. 26.
    Williams MS, Kwon J. T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic Biol Med. 2004;37:1144–1151.CrossRefPubMedGoogle Scholar
  27. 27.
    Matthews GM, Butler RN. Cellular mucosal defense during Helicobacter pylori infection: a review of the role of glutathione and the oxidative pentose pathway. Helicobacter. 2005;10:298–306.CrossRefPubMedGoogle Scholar
  28. 28.
    Carrier J, Aghdassi E, Platt I, Cullen J, Allard JP. Effect of oral iron supplementation on oxidative stress and colonic inflammation in rats with induced colitis. Aliment Pharmacol Ther. 2001;15:1989–1999.CrossRefPubMedGoogle Scholar
  29. 29.
    Sartor RB. Pathogenesis and immune mechanisms of chronic inflammatory bowel diseases. Am J Gastroenterol. 1997;92:5S–11S.PubMedGoogle Scholar
  30. 30.
    Amanatidou A, Smid EJ, Bennik MH, Gorris LG. Antioxidative properties of Lactobacillus sake upon exposure to elevated oxygen concentrations. FEMS Microbiol Lett. 2001;203:87–94.CrossRefPubMedGoogle Scholar
  31. 31.
    Virtanen T, Pihlanto A, Akkanen S, Korhonen H. Development of antioxidant activity in milk whey during fermentation with lactic acid bacteria. J Appl Microbiol. 2007;102:106–115.CrossRefPubMedGoogle Scholar
  32. 32.
    Lin MY, Yen CL. Antioxidative ability of lactic acid bacteria. J Agric Food Chem. 1999;47:1460–1466.CrossRefPubMedGoogle Scholar
  33. 33.
    Welman AD, Maddox IS. Exopolysaccharides from lactic acid bacteria: perspectives and challenges. Trends Biotechnol. 2003;21:269–274.CrossRefPubMedGoogle Scholar
  34. 34.
    Lloyd DH, Viac J, Werling D, Rème CA, Gatto H. Role of sugars in surface microbe-host interactions and immune reaction modulation. Vet Dermatol. 2007;18:197–204.CrossRefPubMedGoogle Scholar
  35. 35.
    Kumar AS, Mody K, Jha B. Bacterial exopolysaccharides—a perception. J Basic Microbiol. 2007;47:103–117.CrossRefPubMedGoogle Scholar
  36. 36.
    Choi SS, Kim Y, Han KS, You S, Oh S, Kim SH. Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett Appl Microbiol. 2006;42:452–458.CrossRefPubMedGoogle Scholar
  37. 37.
    Sutherland IW. Microbial polysaccharides from gram negative bacteria. Int Dairy J. 2001;11:663–674.CrossRefGoogle Scholar
  38. 38.
    Sutherland IW. The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol. 2001;9:222–227.CrossRefPubMedGoogle Scholar
  39. 39.
    Jolly L, Stingele F. Molecular organization and functionality of exopolysaccharide gene clusters in lactic acid bacteria. Int Dairy J. 2001;11:733–745.CrossRefGoogle Scholar
  40. 40.
    Corthésy B, Gaskins HR, Mercenier A. Cross-talk between probiotic bacteria and the host immune system. J Nutr. 2007;137:781S–790S.PubMedGoogle Scholar
  41. 41.
    Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R, Eslami-Varzaneh F. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118:229–241.CrossRefPubMedGoogle Scholar
  42. 42.
    Baumgart DC, Carding SR. Inflammatory bowel disease: cause and immunobiology. Lancet. 2007;369:1627–1640.CrossRefPubMedGoogle Scholar
  43. 43.
    Lloyd DH, Viac J, Werling D, Rème CA, Gatto H. Role of sugars in surface microbe-host interactions and immune reaction modulation. Vet Dermatol. 2007;18:197–204.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Neriman Şengül
    • 1
  • Sevil Işık
    • 2
  • Belma Aslım
    • 3
  • Gülberk Uçar
    • 4
  • Ali Eba Demirbağ
    • 5
  1. 1.Department of General Surgery, Faculty of MedicineAbant İzzet Baysal UniversityEmek, AnkaraTurkey
  2. 2.Department of General Surgery, Faculty of MedicineOrdu UniversityOrduTurkey
  3. 3.Department of Biology, Faculty of Science and ArtsGazi UniversityAnkaraTurkey
  4. 4.Department of Biochemistry, Faculty of PharmacyHacettepe UniversityAnkaraTurkey
  5. 5.Department of Gastrointestinal SurgeryTurkey Yuksek Ihtisas HospitalAnkaraTurkey

Personalised recommendations