721
Views
114
CrossRef citations to date
0
Altmetric
Review Article

Oxidative stress in ulcerative colitis: an old concept but a new concern

, &
Pages 1339-1345 | Received 27 Apr 2012, Accepted 30 Jul 2012, Published online: 05 Sep 2012

References

  • Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006;3:390–407.
  • Rodriguez-Bores L, Fonseca GC, Villeda MA, Yamamoto-Furusho JK. Novel genetic markers in inflammatory bowel disease. World J Gastroenterol 2007;13:5560–5570.
  • Abraham C, Cho J. Mechanisms of disease: inflammatory bowel disease. N Engl J Med 2009;361:2066–2078.
  • The Economic Costs of Crohn's Disease and Ulcerative Colitis, 2007 [cited 2007 9th June]. Available from: http://www.crohnsandcolitis.com.au/content/Final_IBD_report_9_June.pdf.
  • Saleh M, Trinchieri G. Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat Rev Immunol 2011;11:9–20.
  • Rezaie A, Parker RD, Abdollahi M. Oxidative stress and pathogenesis of inflammatory bowel disease: an epiphenomenon or the cause?Dig Dis Sci 2007;52:2015–2021.
  • Seril DN, Liao J, Yang GY, Yang CS. Oxidative stress and ulcerative colitis-associated carcinogenesis: studies in humans and animal models. Carcinogenesis 2003;24:353–362.
  • Westbrook AM, Wei B, Braun J, Schiestl RH. Intestinal mucosal inflammation leads to systemic genotoxicity in mice. Cancer Res 2009;69:4827–4834.
  • Westbrook AM, Wei B, Braun J, Schiestl RH. Intestinal inflammation induces genotoxicity to extraintestinal tissues and cell types in mice. Int J Cancer 2011;129:1815–1825.
  • Montrose DC, Horelik NA, Madigan JP, Stoner GD, Wang LS, Bruno RS, . Anti-inflammatory effects of freeze-dried black raspberry powder in ulcerative colitis. Carcinogenesis 2011;32: 343–350.
  • Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007;448:427–434.
  • Rothfuss KS, Stange EF, Herrlinger KR. Extraintestinal manifestations and complications in inflammatory bowel diseases. World J Gastroenterol 2006;12:4819–4831.
  • Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 2001;48:526–535.
  • Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of population-based cohort studies. Clin Gastroenterol Hepatol 2012;10: 639–645.
  • Bernstein CN, Blanchard JF, Kliewer E, Wajda A. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 2001;91:854–862.
  • Xie J, Itzkowitz SH. Cancer in inflammatory bowel disease. World J Gastroenterol 2008;14:378–389.
  • Hamouda HE, Zakaria SS, Ismail SA, Khedr MA, Mayah WW. p53 antibodies, metallothioneins, and oxidative stress markers in chronic ulcerative colitis with dysplasia. World J Gastroenterol 2011;17:2417–2423.
  • Wu CC, Chen JS, Wu WM, Liao TN, Chu P, Lin SH, . Myeloperoxidase serves as a marker of oxidative stress during single haemodialysis session using two different biocompatible dialysis membranes. Nephrol Dial Transplant 2005;20: 1134–1139.
  • Holmes EW, Yong SL, Eiznhamer D, Keshavarzian A. Glutathione content of colonic mucosa (evidence for oxidative damage in active ulcerative colitis). Dig Dis Sci 1998;43:1088–1095.
  • Morgenstern I, Raijmakers MTM, Peters WHM, Hoensch H, Kirch W. Homocysteine, cysteine, and glutathione in human colonic mucosa: elevated levels of homocysteine in patients with inflammatory bowel disease. Dig Dis Sci 2003;48:2083–2090.
  • Bruwer M, Schmid KW, Metz KA, Krieglstein CF, Senninger N, Schurmann G. Increased expression of metallothionein in inflammatory bowel disease. Inflamm Res 2001;50:289–293.
  • Soussi T. p53 Antibodies in the sera of patients with various types of cancer: a review. Cancer Res 2000;60:1777–1788.
  • El-Sayed ZA, Farag DH, Eissa S. Tumor suppressor protein p53 and anti-p53 autoantibodies in pediatric rheumatological diseases. Pedtr Allergy Immunol 2003;14:229–233.
  • Rogler G, Brand K, Vogl D, Page S, Hofmeister R, Andus T, . Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 1998;115: 357–369.
  • Schreiber S, Nikolaus S, Hampe J. Activation of nuclear factor kappa B inflammatory bowel disease. Gut 1998;42:477–484.
  • Andresen L, Jorgensen VL, Perner A, Hansen A, Eugen-Olsen J, Rask-Madsen J. Activation of nuclear factor kappaB in colonic mucosa from patients with collagenous and ulcerative colitis. Gut 2005;54:503–509.
  • Neurath MF, Fuss I, Schürmann G, Pettersson S, Arnold K, Müller-Lobeck H, . Cytokine gene transcription by NF- kappa B family members in patients with inflammatory bowel disease. Ann N Y Acad Sci 1998;859:149–159.
  • Schreiber S, Nikolaus S, Hampe J. Activation of nuclear factor kB in inflammatory bowel disease. Gut 1998;42:477–484.
  • Neurath MF, Pettersson S, Zum Buschenfelde KHM, Strober W. Local administration of antisense phosphorothiate olignucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat Med 1996;2:998–1004.
  • Maccarrone M, Meloni C, Manca-di-Villahermosa S, Cococcetta N, Casciani CU, Finazzi-Agro A, Taccone-Gallucci M. Vitamin E suppresses 5-lipoxygenase-mediated oxidative stress in peripheral blood mononuclear cells of hemodialysis patients regardless of administration route. Am J Kidney Dis 2001;37:964–969.
  • Pathak SK, Sharma RA, Steward WP, Mellon JK, Griffiths TR, Gescher AJ. Oxidative stress and cyclooxygenase activity in prostate carcinogenesis: targets for chemopreventive strategies. Eur J Cancer 2005;41:61–70.
  • Terra VA, Souza-Neto FP, Pereira RC, Da Silva TN, Ramalho LN, Luiz RC, . Nitric oxide is responsible for oxidative skin injury and modulation of cell proliferation after 24h of UVB exposure. Free Radic Res 2012;46:872–882.
  • Khor TO, Huang MT, Kwon KH, Chan JY, Reddy BS, Kong AN. Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res 2006;66:11580–11584.
  • Okada Y, Tsuzuki Y, Miyazaki J, Matsuzaki K, Hokari R, Komoto S, . Propionibacterium freudenreichii component 1.4- dihydroxy-2-naphthoic acid (DHNA) attenuates dextran sodium sulphate induced colitis by modulation of bacterial flora and lymphocyte homing. Gut 2006;:681–688.
  • Turner JR. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am J Pathol 2006;169: 1901–1909.
  • Habtezion A, Toivola DM, Butcher EC, Omary MB. Keratin- 8-deficient mice develop chronic spontaneous Th2 colitis amenable to antibiotic treatment. J Cell Sci 2005;118:1971–1980.
  • Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, . XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008; 134:743–756.
  • Elson CO, Cong Y, McCracken VJ, Dimmitt RA, Lorenz RG, Weaver CT. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev 2005;206:260–276.
  • Ferguson LR. Chronic inflammation and mutagenesis. Mutat Res 2010;690:3–11.
  • Pavlick KP, Laroux FS, Fuseler J, Wolf RE, Gray L, Hoffman J, Grisham MB. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic Biol Med 2002;33: 311–322.
  • Pravda J. Radical induction theory of ulcerative colitis. World J Gastroenterol 2005;11:2371–2384.
  • Grisham MB. Role of reactive oxygen metabolites in inflammatory bowel disease. Curr Opin Gastroenterol 1993;9:971–980.
  • Fan H, Sun B, Gu Q, Lafond-Walker A, Cao S, Becker LC. Oxygen radicals trigger activation of NF-kappaB and AP-1 and upregulation of ICAM-1 in reperfused canine heart. Am J Physiol Heart Circ Physiol 2002;282:1778–1786.
  • Konishi H, Tanaka M, Takemura Y, Matsuzaki H, Ono Y, Kikkawa U, Nishizuka Y. Activation of protein kinase C by tyrosine phosphorylation in response to H2O2. Proc Natl Acad Sci USA 1997;94:11233–11237.
  • Morel Y, Barouki R. Repression of gene expression by oxidative stress. Biochem J 1999;342:481–496.
  • Schreck R, Albermann K, Baeuerle PA. Nuclear factor kappa B: an oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radic Res Commun 1992;17:221–237.
  • Atreya R, Neurath MF. Involvement of IL-6 in the pathogenesis of inflammatory bowel disease and colon cancer. Clin Rev Allergy Immunol 2005;28:187–196.
  • Libermann TA, Baltimore D. Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol Cell Biol 1990;10:2327–2334.
  • Mudter J, Neurath MF. Il-6 signaling in inflammatory bowel disease: pathophysiological role and clinical relevance. Inflamm Bowel Dis 2007;13:1016–1023.
  • Littman DR, Rudensky AY. Th17 and regulatory T cells in mediating and restraining inflammation. Cell 2010;140:845–858.
  • Ahern PP, Izcue A, Maloy KJ, Powrie F. The interleukin-23 axis in intestinal inflammation. Immunol Rev 2008;226:147–159.
  • Ohshima H, Tatemichi M, Sawa T. Chemical basis of inflammation induced carcinogenesis. Arch Biochem Biophys 2003;417: 3–11.
  • Sawa T, Ohshima H. Nitrative DNA damage in inflammation and its possible role in carcinogenesis. Nitric Oxide 2006;14: 91–100.
  • Kaneko K, Akuta T, Sawa T, Kim HW, Fujii S, Okamoto T, . Mutagenicity of 8-nitroguanosine, a product of nitrative nucleoside modification by reactive nitrogen oxides, in mammalian cells. Cancer Lett 2008;262:239–247.
  • Kondo S, Toyokuni S, Iwasa Y, Tanaka T, Onodera H, Hiai H, Imamura M. Persistent oxidative stress in human colorectal c arcinoma, but not in adenoma. Free Radic Biol Med 1999;27: 401–410.
  • Peluso M, Munnia A, Piro S, Jedpiyawongse A, Sangrajrang S, Giese RW, . Fruit and vegetable and fried food consumption and 3-(2-deoxy-beta-D-erythro-pentafuranosyl)pyrimido[1,2- alpha] purin-10(3H)-one deoxyguanosine adduct formation. Free Radic Res 2012;46:85–92.
  • Gushima M, Hirahashi M, Matsumoto T, Fujita K, Fujisawa R, Mizumoto K, . Altered expression of MUTYH and an increase in 8-hydroxydeoxyguanosine are early events in ulcerative colitis-associated carcinogenesis. J Pathol 2009;219:77–86.
  • Westbrook AM, Wei B, Braun J, Schiestl RH. More damaging than we think: systemic effects of intestinal inflammation. Cell Cycle 2009;8:2482–2483.
  • Memon MI, Memon B, Memon MA. Hepatobiliary manifestations of inflammatory bowel disease. HPB Surg 2000;11: 363–371.
  • Trivedi PP, Jena GB. Dextran sulfate sodium-induced ulcerative colitis leads to increased hematopoiesis and induces both local as well as systemic genotoxicity in mice. Mutat Res 2012;744: 172–183.
  • Verhasselt V, Goldman M, Willems F. Oxidative stress up- regulates IL-8 and TNF-alpha synthesis by human dendritic cells. Eur J Immunol 1998;28:3886–3890.
  • Barrie A, Regueiro M. Biologic therapy in the management of extraintestinal manifestations of inflammatory bowel disease. Inflamm Bowel Dis 2007;13:1424–1429.
  • Dechakhamphu S, Yongvanit P, Nair J, Pinlaor S, Sitthithaworn P, Bartsch H. High excretion of etheno adducts in liver fluke-infected patients: protection by praziquantel against DNA damage. Cancer Epidemiol Biomarkers Prev 2008;17:1658–1664.
  • Meerang M, Nair J, Sirankapracha P, Thephinlap C, Srichairatanakool S, Arab K, . Accumulation of lipid peroxidation-derived DNA lesions in iron-overloaded thalassemic mouse livers: comparison with levels in the lymphocytes of thalassemia patients. Int J Cancer 2009;125:759–766.
  • Liao J, Seril DN, Lu GG, Zhang M, Toyokuni S, Yang AL, Yang GY. Increased susceptibility of chronic ulcerative colitis-induced carcinoma development in DNA repair enzyme Ogg1 deficient mice. Mol Carcinog 2008;47:638–646.
  • Hofseth LJ, Khan MA, Ambrose M, Nikolayeva O, Xu-Welliver M, Kartalou M, . The adaptive imbalance in base excision-repair enzymes generates microsatellite instability in chronic inflammation. J Clin Invest 2003;112:1887–1894.
  • Inokuma T, Haraguchi M, Fujita F, Tajima Y, Kanematsu T. Oxidative stress and tumor progression in colorectal cancer. Hepatogastroenterology 2009;56:343–347.
  • Chang D, Wang F, Zhao YS, Pan HZ. Evaluation of oxidative stress in colorectal cancer patients. Biomed Environ Sci 2008;21:286–289.
  • Cerda S, Weitzman SA. Influence of oxygen radical injury on DNA methylation. Mutat Res 1997;386:141–152.
  • Counts JL, McClain RM, Goodman JI. Comparison of effect of tumor promoter treatments on DNA methylation status and gene expression in B6C3F1 and C57BL/6 mouse liver and in B6C3F1 mouse liver tumors. Mol Carcinog 1997;18:97–106.
  • Herman JG, Latif F, Weng Y, Lerman MI, Zbar B, Liu S, . Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci USA 1994;91:9700–9704.
  • Herman JG, Merlo A, Mao L, Lapidus RG, Issa JP, Davidson NE, . Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res 1995;55:4525–4530.
  • Hinoue T, Weisenberger DJ, Lange CP, Shen H, Byun HM, Van Den Berg D, . Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res 2012;22:271–282.
  • Nabilsi NH, Broaddus RR, Loose DS. DNA methylation inhibits p53-mediated survivin repression. Oncogene 2009;28:2046–2050.
  • Ohtani-Fujita N, Fujita T, Aoike A, Osifchin NE, Robbins PD, Sakai T. CpG methylation inactivates the promoter activity of the human retinoblastoma tumor-suppressor gene. Oncogene 1993;8: 1063–1067.
  • Ha PK, Califano JA. Promoter methylation and inactivation of tumour-suppressor genes in oral squamous-cell carcinoma. Lancet Oncol 2006;7:77–82.
  • Lim SO, Gu JM, Kim MS, Kim HS, Park YN, Park CK, . Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter. Gastroenterology 2008;135:2128–2140.
  • Yang B, House MG, Guo M, Herman JG, Clark DP. Promoter methylation profiles of tumor suppressor genes in intrahepatic and extrahepatic cholangiocarcinoma. Mod Pathol 2005;18:412–420.
  • Fagerhol MK. Surrogate markers of intestinal inflammation are predictive of relapse in patients with inflammatory bowel disease. Gastroenterology 2000;119:15–22.
  • Masoodi I, Tijjani BM, Wani H, Hassan NS, Khan AB, Hussain S. Biomarkers in the management of ulcerative colitis: a brief review. Ger Med Sci 2011; Article in press.
  • Bischoff SC, Grabowsky J, Manns MP. Quantification of inflammatory mediators in stool samples of patients with inflammatory bowel disorders and controls. Dig Dis Sci 1997;42:394–403.
  • Sugi K, Saitoh O, Hirata I, Katsu K. Fecal lactoferrin as a marker for disease activity in inflammatory bowel disease: comparison with other neutrophil-derived proteins. Am J Gastroenterol 1996;91:927–934.
  • Erbayrak M, Turkay C, Eraslan E, Cetinkaya H, Kasapoglu B, Bektas M. The role of fecal calprotectin in investigating inflammatory bowel diseases. Clinics 2009;64:421–425.
  • Golikov P. A novel biomarker for diagnosis of ulcerative colitis and colon cancer, [cited 2003]. Available from: www.umdnj.edu/resrhweb/patents/for_licensing/diagnostics/01-08-Das-A_b_Colitis.pdf.
  • Bousvaros A, Sylvester F, Kugathasan S, Szigethy E, Fiocchi C, Colletti R, . Challenges in pediatric inflammatory bowel disease. Inflamm Bowel Dis 2006;12:885–913.
  • Dong WG, Mei Q, Yu JP, Xu JM, Xiang L, Xu Y. Effects of melatonin on the expression of iNOS and COX-2 in rat models of colitis. World J Gastroenterol 2003;9:1307–1311.
  • Kolgazi M, Jahovic N, Yuksel M, Ercan F, Alican I. Alpha-lipoic acid modulates gut inflammation induced by trinitrobenzene sulfonic acid in rats. J Gastroenterol Hepatol 2007;22: 1859–1865.
  • Mirbagheri SA, Nezami BG, Assa S, Hajimahmoodi M. Rectal administration of d-alpha tocopherol for active ulcerative colitis: a preliminary report. World J Gastroenterol 2008;14: 5990–5995.
  • Trivedi PP, Kushwaha S, Tripathi DN, Jena GB. Cardioprotective effects of hesperetin against doxorubicin-induced oxidative stress and DNA damage in rat. Cardiovasc Toxicol 2011;11:215–225.
  • Trivedi PP, Tripathi DN, Jena GB. Hesperetin protects testicular toxicity of doxorubicin in rat: role of NFkappaB, p38 and caspase-3. Food Chem Toxicol 2011;49:838–847.
  • Dave M, Loftus EV Jr. Mucosal healing in inflammatory bowel disease-a true paradigm of success?Gastroenterol Hepatol (NY) 2012;8:29–38.
  • Loguercio C, D’Argenio G, Delle Cave M, Cosenza V, Della Valle N, Mazzacca G, Del Vecchio Blanco C. Glutathione supplementation improves oxidative damage in experimental colitis. Dig Liver Dis 2003;35:635–641.
  • Arafa HM, Hemeida RA, El-Bahrawy AI, Hamada FM. Prophylactic role of curcumin in dextran sulfate sodium (DSS)-induced ulcerative colitis murine model. Food Chem Toxicol 2009;47:1311–1317.
  • Yao J, Wang JY, Liu L, Li YX, Xun AY, Zeng WS, . Anti-oxidant effects of resveratrol on mice with DSS-induced ulcerative colitis. Arch Med Res 2010;41:288–294.
  • Chojnacki C, Wisniewska-Jarosinska M, Walecka-Kapica E, Klupinska G, Jaworek J, Chojnacki J. Evaluation of melatonin effectiveness in the adjuvant treatment of ulcerative colitis. J Physiol Pharmacol 2011;62:327–334.
  • Hanai H, Iida T, Takeuchi K, Watanabe F, Maruyama Y, Andoh A, . Curcumin maintenance therapy for ulcerative colitis: randomized, multicenter, double-blind, placebo-controlled trial. Clin Gastroenterol Hepatol 2006;4:1502–1506.
  • Meira LB, Bugni JM, Green SL, Lee CW, Pang B, Borenshtein D, . DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice. J Clin Invest 2008;118: 2516–2525.
  • Grimble RF. Nutritional antioxidants and the modulation of inflammation: theory and practice. New Horiz 1994;2:175–185.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.