460
Views
14
CrossRef citations to date
0
Altmetric
Original Article

Targeted-mitochondria antioxidants therapeutic implications in inflammatory bowel disease

&
Pages 1-8 | Received 25 Apr 2017, Accepted 03 Jun 2017, Published online: 04 Jul 2017

References

  • Rigoli L, Caruso RA. Inflammatory bowel disease in pediatric and adolescent patients: a biomolecular and histopathological review. World J Gastroenterol. 2014;20:10262–10278.
  • Abdolghaffari AH, Baghaei A, Moayer F, et al. On the benefit of Teucrium in murine colitis through improvement of toxic inflammatory mediators. Hum Exp Toxicol. 2010;29:287–295.
  • Chen Y, Chen Y, Liu WL, et al. Therapeutic effects of rectal administration of muscovite on experimental colitis in rats. J Gastroenterol Hepatol. 2009;24:912–919.
  • Noble CL, Arnott ID. What is the risk that a child will develop inflammatory bowel disease if 1 or both parents have IBD? Inflamm Bowel Dis. 2008;14:S22–S23.
  • Bennett RA, Rubin PH, Present DH. Frequency of inflammatory bowel disease in offspring of couples both presenting with inflammatory bowel disease. Gastroenterology. 1991;100:1638–1643.
  • Dincer Y, Erzin Y, Himmetoglu S, et al. Oxidative DNA damage and antioxidant activity in patients with inflammatory bowel disease. Dig Dis Sci. 2007;52:1636–1641.
  • Pereira C, Grácio D, Teixeira JP, et al. Oxidative stress and DNA damage: implications in inflammatory bowel disease. Inflamm Bowel Dis. 2015;21:2403–2417.
  • Esworthy RS, Aranda R, Martín MG, et al. Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol. 2001;281:G848–G855.
  • Lee I, Huttemann M. Energy crisis: the role of oxidative phosphorylation in acute inflammation and sepsis. Biochim Biophys Acta. 2014;1842:1579–1586.
  • Kruidenier L, Kuiper I, Lamers CB, et al. Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol. 2003;201:28–36.
  • Pravda J. Radical induction theory of ulcerative colitis. World J Gastroenterol. 2005;11:2371–2384.
  • Dashdorj A, Jyothi KR, Lim S, et al. Mitochondria-targeted antioxidant MitoQ ameliorates experimental mouse colitis by suppressing NLRP3 inflammasome-mediated inflammatory cytokines. BMC Med. 2013;11:178.
  • Tait SW, Green DR. Mitochondria and cell signalling. J Cell Sci. 2012;125:807–815.
  • Saitoh T, Fujita N, Jang MH, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature. 2008;456:264–268.
  • de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008;456:605–610.
  • Pfeiffer T, Bonhoeffer S. Cooperation and competition in the evolution of ATP-producing pathways. Science. 2001;292:504–507.
  • Wenz T. Regulation of mitochondrial biogenesis and PGC-1α under cellular stress. Mitochondrion. 2013;13:134–142.
  • Archer SL. Mitochondrial dynamics–mitochondrial fission and fusion in human diseases. N Engl J Med. 2013;369:2236–2251.
  • Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337:1062–1065.
  • Santel A, Fuller MT. Control of mitochondrial morphology by a human mitofusin. J Cell Sci. 2001;114:867–874.
  • Zhao GJ, Yao YM. [Advances in mitochondrial fusion-fission and Ca2+ signaling in mammals]. Sheng Li Ke Xue Jin Zhan. 2010;41:171–176.
  • Cogliati S, Frezza C, Soriano ME, et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell. 2013;155:160–171.
  • Westermann B. Merging mitochondria matters: cellular role and molecular machinery of mitochondrial fusion. EMBO Rep. 2002;3:527–531.
  • Chan DC. Mitochondrial fusion and fission in mammals. Annu Rev Cell Dev Biol. 2006;22:79–99.
  • Friedman JR, Lackner LL, West M, et al. ER tubules mark sites of mitochondrial division. Science. 2011;334:358–362.
  • Sanchis-Gomar F, Derbre F. Mitochondrial fission and fusion in human diseases. N Engl J Med. 2014;370:1073–1074.
  • Hall AR, Hausenloy DJ. Mitochondrial fusion and fission proteins: novel therapeutic targets for combating cardiovascular disease. Br J Pharmacol. 2014;171:1890–1906.
  • Raha S, Robinson BH. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci. 2000;25:502–508.
  • Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life. 2001;52:159–164.
  • Vasquez-Vivar J, Kennedy MC. Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J Biol Chem. 2000;275:14064–14069.
  • Ilangovan G, Kuppusamy P. Heat shock-induced attenuation of hydroxyl radical generation and mitochondrial aconitase activity in cardiac H9c2 cells. Am J Physiol Cell Physiol. 2006;290:C313–C324.
  • Beckman KB, Ames BN. The free radical theory of aging matures. Physiol Rev. 1998;78:547–581.
  • James AM, Murphy MP. How mitochondrial damage affects cell function. J Biomed Sci. 2002;9:475–487.
  • Murphy MP. Nitric oxide and cell death. Biochim Biophys Acta. 1999;1411:401–414.
  • Young IS, Woodside JV. Antioxidants in health and disease. J Clin Pathol. 2001;54:176–186.
  • Willcox JK, Catignani GL. Antioxidants and prevention of chronic disease. Crit Rev Food Sci Nutr. 2004;44:275–295.
  • Kruidenier L, Verspaget HW. Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease-radicals or ridiculous? Aliment Pharmacol Ther. 2002;16:1997–2015.
  • Ramonaite R, Skieceviciene J, Kiudelis G, et al. Influence of NADPH oxidase on inflammatory response in primary intestinal epithelial cells in patients with ulcerative colitis. BMC Gastroenterol. 2013;13:159.
  • Ramonaite R. Protective action of NADPH oxidase inhibitors and role of NADPH oxidase in pathogenesis of colon inflammation in mice. World J Gastroenterol. 2014;20:12533–12541.
  • Buddi R, Brown DJ. Evidence of oxidative stress in human corneal diseases. J Histochem Cytochem. 2002;50:341–351.
  • Oz HS, Chen TS, McClain CJ, et al. Antioxidants as novel therapy in a murine model of colitis. J Nutr Biochem. 2005;16:297–304.
  • Herulf M, Lundberg JO. Increased luminal nitric oxide in inflammatory bowel disease as shown with a novel minimally invasive method. Scand J Gastroenterol. 1998;33:164–169.
  • Eliakim, Karmeli F, Rachmilewitz D, et al. Effect of chronic nicotine administration on trinitrobenzene sulphonic acid-induced colitis. Eur J Gastroenterol Hepatol. 1998;10:1013–1019.
  • Buffinton GD, Doe WF. Depleted mucosal antioxidant defences in inflammatory bowel disease. Free Radic Biol Med. 1995;19:911–918.
  • Ljung T, Hellstrom PM. Increased rectal nitric oxide in children with active inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2002;34:302–306.
  • Esworthy RS, Binder SW, Doroshow JH, et al. Microflora trigger colitis in mice deficient in selenium-dependent glutathione peroxidase and induce Gpx2 gene expression. Biol Chem. 2003;384:597–607.
  • Mulder TP, Verspaget HW, Janssens AR, et al. Decrease in two intestinal copper/zinc containing proteins with antioxidant function in inflammatory bowel disease. Gut. 1991;32:1146–1150.
  • Grisham MB. Oxidants and free radicals in inflammatory bowel disease. Lancet. 1994;344:859–861.
  • Kameyama J, Narui H, Inui M, et al. Energy level in large intestinal mucosa in patients with ulcerative colitis. Tohoku J Exp Med. 1984;143:253–254.
  • Soderholm JD, Tagesson C, Sjodahl R. Augmented increase in tight junction permeability by luminal stimuli in the non-inflamed ileum of Crohn's disease. Gut. 2002;50:307–313.
  • Poulsen NA, Andersen V, Møller JC, et al. Comparative analysis of inflamed and non-inflamed colon biopsies reveals strong proteomic inflammation profile in patients with ulcerative colitis. BMC Gastroenterol. 2012;12:76.
  • Bär F, Bochmann W, Widok A, et al. Mitochondrial gene polymorphisms that protect mice from colitis. Gastroenterology. 2013;145:1055–1063.e3.
  • Man AL, Bertelli E, Rentini S, et al. Age-associated modifications of intestinal permeability and innate immunity in human small intestine. Clin Sci. 2015;129:515–527.
  • Mabbott NA. A breakdown in communication? Understanding the effects of aging on the human small intestine epithelium. Clin Sci. 2015;129:529–531.
  • Bjarnason I, Takeuchi K. Intestinal permeability in the pathogenesis of NSAID-induced enteropathy. J Gastroenterol. 2009;44:23–29.
  • Maiden L. Capsule endoscopic diagnosis of nonsteroidal antiinflammatory drug-induced enteropathy. J Gastroenterol. 2009;44:64–71.
  • Schoultz I, Soderholm JD, McKay DM. Is metabolic stress a common denominator in inflammatory bowel disease? Inflamm Bowel Dis. 2011;17:2008–2018.
  • Lewis K, McKay DM. Metabolic stress evokes decreases in epithelial barrier function. Ann N Y Acad Sci. 2009;1165:327–337.
  • Rodenburg W, Keijer J, R, Kramer E, et al. Impaired barrier function by dietary fructo-oligosaccharides (FOS) in rats is accompanied by increased colonic mitochondrial gene expression. BMC Genomics. 2008;9:144.
  • Nazli A, Yang PC, Jury J, et al. Epithelia under metabolic stress perceive commensal bacteria as a threat. Am J Pathol. 2004;164:947–957.
  • Travassos LH, Carneiro LA, Ramjeet M, et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat Immunol. 2010;11:55–62.
  • Kaser A, Lee AH, Franke A, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell. 2008;134:743–756.
  • Beltrán B, Nos P, Dasí F, et al. Mitochondrial dysfunction, persistent oxidative damage, and catalase inhibition in immune cells of naive and treated Crohn's disease. Inflamm Bowel Dis. 2010;16:76–86.
  • Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol. 2009;9:799–809.
  • Dickman KG, Burakoff R, Shaw RD. Rotavirus alters paracellular permeability and energy metabolism in Caco-2 cells. Am J Physiol Gastrointest Liver Physiol. 2000;279:G757–G766.
  • Davis BK, Philipson C, Allen IC. Emerging significance of NLRs in inflammatory bowel disease. Inflamm Bowel Dis. 2014;20:2412–2432.
  • Van den Bossche J, Baardman J, Otto NA, et al. Mitochondrial dysfunction prevents repolarization of inflammatory macrophages. Cell Rep. 2016;17:684–696.
  • Tschopp J. Mitochondria: Sovereign of inflammation? Eur J Immunol. 2011;41:1196–1202.
  • Zitvogel L, Kepp O, Galluzzi L, et al. Inflammasomes in carcinogenesis and anticancer immune responses. Nat Immunol. 2012;13:343–351.
  • Siegmund B. IL-1 beta-converting enzyme (caspase-1) in intestinal inflammation. Proc Natl Acad Sci U S A. 2001;98:13249–13254.
  • Bauer C, Duewell P, Mayer C, et al. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut. 2010;59:1192–1199.
  • Maguire JJ, Wilson DS, Packer L. Mitochondrial electron transport-linked tocopheroxyl radical reduction. J Biol Chem. 1989;264:21462–21465.
  • Maguire JJ, Kagan VE, Packer L. Electron transport between cytochrome c and alpha tocopherol. Biochem Biophys Res Commun. 1992;188:190–197.
  • Beckman KB, Ames BN. Mitochondrial aging: open questions. Ann N Y Acad Sci. 1998;854:118–127.
  • Mozaffari S, Abdollahi M. Melatonin, a promising supplement in inflammatory bowel disease: a comprehensive review of evidences. Curr Pharm Des. 2011;17:4372–4378.
  • Cui Z, Yin J, Wang L, et al. Effects of pro-inflammatory cytokines and antioxidants expression in the jejunum of mice induced by hydrogen peroxide. Int Immunopharmacol. 2016;31:9–14.
  • Vargas Robles H, Citalan Madrid AF, Schnoor M. Experimental colitis is attenuated by cardioprotective diet supplementation that reduces oxidative stress, inflammation, and mucosal damage. Oxid Med Cell Longev. 2016;2016:8473242.
  • Liu C, Russell RM, Smith DE, et al. The effect of dietary glutathione and coenzyme Q10 on the prevention and treatment of inflammatory bowel disease in mice. Int J Vitam Nutr Res. 2004;74:74–85.
  • Negida A, Menshawy A, Rashad Y. Coenzyme Q10 for patients with Parkinson's disease: a systematic review and meta-analysis. CNS Neurol Disord Drug Targets. 2016;15:45–53.
  • Bentinger M, Dallner G, Chojnacki T, et al. Distribution and breakdown of labeled coenzyme Q10 in rat. Free Radic Biol Med. 2003;34:563–575.
  • Murphy MP. Development of lipophilic cations as therapies for disorders due to mitochondrial dysfunction. Expert Opin Biol Ther. 2001;1:753–764.
  • Mollace V, Iannone M, Muscoli C, et al. The role of oxidative stress in paraquat-induced neurotoxicity in rats: protection by non peptidyl superoxide dismutase mimetic. Neurosci Lett. 2003;335:163–166.
  • Peng J, Stevenson FF, Doctrow SR, et al. Superoxide dismutase/catalase mimetics are neuroprotective against selective paraquat-mediated dopaminergic neuron death in the substantial nigra: implications for Parkinson disease. J Biol Chem. 2005;280:29194–29198.
  • Murphy MP. Selective targeting of bioactive compounds to mitochondria. Trends Biotechnol. 1997;15:326–330.
  • Murphy MP, Smith RA. Drug delivery to mitochondria: the key to mitochondrial medicine. Adv Drug Deliv Rev. 2000;41:235–250.
  • Echtay KS, Murphy MP, Smith RA, et al. Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. Studies using targeted antioxidants. J Biol Chem. 2002;277:47129–47135.
  • Kelso GF, Maroz A, Cochemé HM, et al. A mitochondria-targeted macrocyclic Mn(II) superoxide dismutase mimetic. Chem Biol. 2012;19:1237–1246.
  • Kelso GF, Porteous CM, Murphy MP. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J Biol Chem. 2001;276:4588–4596.
  • Jauslin ML, Meier T, Smith RA, et al. Mitochondria-targeted antioxidants protect Friedreich Ataxia fibroblasts from endogenous oxidative stress more effectively than untargeted antioxidants. FASEB J. 2003;17:1972–1974.
  • Asin-Cayuela J, Manas AR, Murphy MP. Fine-tuning the hydrophobicity of a mitochondria-targeted antioxidant. FEBS Lett. 2004;571:9–16.
  • Weissig V. Targeted drug delivery to mammalian mitochondria in living cells. Expert Opin Drug Deliv. 2005;2:89–102.
  • Smith RA, Porteous Murphy MP. Delivery of bioactive molecules to mitochondria in vivo. Proc Natl Acad Sci U S A. 2003;100:5407–5412.
  • Kelso GF, Porteous CM, Hughes G, et al. Prevention of mitochondrial oxidative damage using targeted antioxidants. Ann N Y Acad Sci. 2002;959:263–274.
  • Nussbaumer M, Asara JM, Teplytska L, et al. Selective mitochondrial targeting exerts anxiolytic effects in vivo. Neuropsychopharmacology. 2016;41:1751–1758.
  • Wani WY, Gudup S, Sunkaria A, et al. Protective efficacy of mitochondrial targeted antioxidant MitoQ against dichlorvos induced oxidative stress and cell death in rat brain. Neuropharmacology 2011;61:1193–1201.
  • Ng LF, Gruber J, Cheah IK, et al. The mitochondria-targeted antioxidant MitoQ extends lifespan and improves healthspan of a transgenic Caenorhabditis elegans model of Alzheimer disease. Free Radic Biol Med. 2014;71:390–401.
  • Dhanasekaran A, Kalyanaraman B. Supplementation of endothelial cells with mitochondria-targeted antioxidants inhibit peroxide-induced mitochondrial iron uptake, oxidative damage, and apoptosis. J Biol Chem. 2004;279:37575–37587.
  • Hughes G, Murphy MP, Ledgerwood EC. Mitochondrial reactive oxygen species regulate the temporal activation of nuclear factor kappaB to modulate tumour necrosis factor-induced apoptosis: evidence from mitochondria-targeted antioxidants. Biochem J. 2005;389:83–89.
  • Sheu SS, Nauduri D, Anders MW. Targeting antioxidants to mitochondria: a new therapeutic direction. Biochim Biophys Acta. 2006;1762:256–265.
  • Victor VM, Espulgues JV, Hernández-Mijares A, et al. Oxidative stress and mitochondrial dysfunction in sepsis: a potential therapy with mitochondria-targeted antioxidants. Infect Disord Drug Targets. 2009;9:376–389.
  • Du G, Mouithys-Mickalad A, Sluse FE. Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radic Biol Med. 1998;25:1066–1074.
  • Soderholm JD, Olaison G, Sjodahl R. Different intestinal permeability patterns in relatives and spouses of patients with Crohn's disease: an inherited defect in mucosal defence? Gut. 1999;44:96–100.
  • Hsieh SY, Shih TC, Yeh CY, et al. Comparative proteomic studies on the pathogenesis of human ulcerative colitis. Proteomics. 2006;6:5322–5331.
  • Fukushima K, Fiocchi C. Paradoxical decrease of mitochondrial DNA deletions in epithelial cells of active ulcerative colitis patients. Am J Physiol Gastrointest Liver Physiol. 2004;286:G804–G813.
  • Delpre G, Avidor I, Steinherz R, et al. Ultrastructural abnormalities in endoscopically and histologically normal and involved colon in ulcerative colitis. Am J Gastroenterol. 1989;84:1038–1046.
  • Schoultz I, Verma D, Halfvarsson J, et al. Combined polymorphisms in genes encoding the inflammasome components NALP3 and CARD8 confer susceptibility to Crohn's disease in Swedish men. Am J Gastroenterol. 2009;104:1180–1188.
  • Roediger WE. The colonic epithelium in ulcerative colitis: an energy-deficiency disease? Lancet. 1980;2:712–715.
  • Barrett JC, Hansoul S, Nicolae DL, et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet. 2008;40:955–962.
  • Rezaie A, Ghorbani F, Eshghtork A, et al. Alterations in salivary antioxidants, nitric oxide, and transforming growth factor-beta 1 in relation to disease activity in Crohn’s disease patients. Ann N Y Acad Sci. 2006;1091:110–122.
  • Tham DM, Whitin JC, Cohen HJ. Increased expression of extracellular glutathione peroxidase in mice with dextran sodium sulfate-induced experimental colitis. Pediatr Res. 2002;51:641–646.
  • Narushima S, Spitz DR, Oberley LW, et al. Evidence for oxidative stress in NSAID-induced colitis in IL10-/- mice. Free Radic Biol Med. 2003;34:1153–1166.
  • Sundaram U, Hassanain H, Christofi FL. Rabbit chronic ileitis leads to up-regulation of adenosine A1/A3 gene products, oxidative stress, and immune modulation. Biochem Pharmacol. 2003;65:1529–1538.
  • Siddiqui A, Ancha H, Harty RF. Antioxidant therapy with N-acetylcysteine plus mesalamine accelerates mucosal healing in a rodent model of colitis. Dig Dis Sci. 2006;51:698–705.
  • dos Reis SB, de Oliveira CC, Acedo SC, et al. Attenuation of colitis injury in rats using Garcinia cambogia extract. Phytother Res. 2009;23:324–329.
  • Yao J, Wang JY, Wang LS. Anti-oxidant effects of resveratrol on mice with DSS-induced ulcerative colitis. Arch Med Res. 2010;41:288–294.
  • Lenoir L, Rossary A, Joubert-Zakeyh J, et al. Lemon verbena infusion consumption attenuates oxidative stress in dextran sulfate sodium-induced colitis in the rat. Dig Dis Sci. 2011;56:3534–3545.
  • Sengül N, Isik S, Aslim B, et al. The effect of exopolysaccharide-producing probiotic strains on gut oxidative damage in experimental colitis. Dig Dis Sci. 2011;56:707–714.
  • Borrelli F, Fasolino I, Romano B, et al. Beneficial effect of the non-psychotropic plant cannabinoid cannabigerol on experimental inflammatory bowel disease. Biochem Pharmacol. 2013;85:1306–1316.
  • Zielinska-Przyjemska M, Olejnik A, Dobrowolska-Zachwieja A,, et al. DNA damage and apoptosis in blood neutrophils of inflammatory bowel disease patients and in Caco-2 cells in vitro exposed to betanin. Postepy Hig Med Dosw. 2016;70:265–271.

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.