Idebenone Protects against Acute Murine Colitis via Antioxidant and Anti-Inflammatory Mechanisms
Abstract
:1. Introduction
2. Results
2.1. Idebenone Improved the Clinical and Macroscopic Features of Colitis
2.2. Idebenone Reduced the Colon Histopathology in Acute Colitis
2.3. Idebenone Preserved the Intestinal Barrier Integrity and Protected against Goblet Cell Loss in DSS-Induced Colitis
2.4. Idebenone Reduced the Oxidative Stress in DSS-Induced Colitis
2.5. Idebenone Upregulated the Expression of the Phase II Detoxifying Enzyme NQO-1
2.6. Idebenone Reduced the Levels of Pro-Inflammatory Cytokines in Colon Tissue
3. Discussion
4. Material and Methods
4.1. Animals
4.2. Experimental Design and Drug Treatment
4.3. Clinical and Histopathological Evaluations
4.4. Immunohistochemistry
4.5. Western Blotting
4.6. Alcian Blue Staining
4.7. Lipid Peroxidation Assay
4.8. Measurement of SOD Activity and NO Production
4.9. Cytokine Measurement from the Tissue Explant Culture
4.10. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Abraham, C.; Cho, J.H. Inflammatory bowel disease. N. Engl. J. Med. 2009, 361, 2066–2078. [Google Scholar] [CrossRef]
- Biasi, F.; Leonarduzzi, G.; Oteiza, P.I.; Poli, G. Inflammatory bowel disease: Mechanisms, redox considerations, and therapeutic targets. Antioxid. Redox Signal. 2013, 19, 1711–1747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wirtz, S.; Neufert, C.; Weigmann, B.; Neurath, M.F. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2007, 2, 541–546. [Google Scholar] [CrossRef] [PubMed]
- Sann, H.; Erichsen, J.; Hessmann, M.; Pahl, A.; Hoffmeyer, A. Efficacy of drugs used in the treatment of IBD and combinations thereof in acute DSS-induced colitis in mice. Life Sci. 2013, 92, 708–718. [Google Scholar] [CrossRef] [PubMed]
- Chiou, Y.S.; Ma, N.J.; Sang, S.; Ho, C.T.; Wang, Y.J.; Pan, M.H. Peracetylated (-)-epigallocatechin-3-gallate (AcEGCG) potently suppresses dextran sulfate sodium-induced colitis and colon tumorigenesis in mice. J. Agric. Food Chem. 2012, 60, 3441–3451. [Google Scholar] [CrossRef]
- Sanchez-Fidalgo, S.; Cardeno, A.; Sanchez-Hidalgo, M.; Aparicio-Soto, M.; de la Lastra, C.A. Dietary extra virgin olive oil polyphenols supplementation modulates DSS-induced chronic colitis in mice. J. Nutr. Biochem. 2013, 24, 1401–1413. [Google Scholar] [CrossRef]
- Holma, R.; Salmenpera, P.; Virtanen, I.; Vapaatalo, H.; Korpela, R. Prophylactic potential of montelukast against mild colitis induced by dextran sulphate sodium in rats. J. Physiol. Pharmacol. 2007, 58, 455–467. [Google Scholar]
- Okayasu, I.; Hatakeyama, S.; Yamada, M.; Ohkusa, T.; Inagaki, Y.; Nakaya, R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990, 98, 694–702. [Google Scholar] [CrossRef]
- Chassaing, B.; Aitken, J.D.; Malleshappa, M.; Vijay-Kumar, M. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 2014, 104, 15–25. [Google Scholar] [CrossRef]
- Poritz, L.S.; Garver, K.I.; Green, C.; Fitzpatrick, L.; Ruggiero, F.; Koltun, W.A. Loss of the tight junction protein ZO-1 in dextran sulfate sodium induced colitis. J. Surg. Res. 2007, 140, 12–19. [Google Scholar] [CrossRef]
- Perse, M.; Cerar, A. Dextran sodium sulphate colitis mouse model: Traps and tricks. J. Biomed. Biotechnol. 2012, 2012, 718617. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kyoko, O.O.; Kono, H.; Ishimaru, K.; Miyake, K.; Kubota, T.; Ogawa, H.; Okumura, K.; Shibata, S.; Nakao, A. Expressions of tight junction proteins Occludin and Claudin-1 are under the circadian control in the mouse large intestine: Implications in intestinal permeability and susceptibility to colitis. PLoS ONE 2014, 9, e98016. [Google Scholar] [CrossRef]
- Tokoi, S.; Ohkusa, T.; Okayasu, I.; Nakamura, K. Population changes in immunoglobulin-containing mononuclear cells in dextran sulfate sodium-induced coltitis. J. Gastroenterol. 1996, 31, 182–188. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.H.; Adam, R.; Colombel, J.F.; Bian, Z.X. A characterization of pro-inflammatory cytokines in dextran sulfate sodium-induced chronic relapsing colitis mice model. Int. Immunopharmacol. 2018, 60, 194–201. [Google Scholar] [CrossRef] [PubMed]
- Damiani, C.R.; Benetton, C.A.F.; Stoffel, C.; Bardini, K.C.; Cardoso, V.H.; Di Giunta, G.; Pinho, R.A.; Dal-Pizzol, F.; Streck, E.L. Oxidative stress and metabolism in animal model of colitis induced by dextran sulfate sodium. J. Gastroenterol. Hepatol. 2007, 22, 1846–1851. [Google Scholar] [CrossRef] [PubMed]
- Tian, T.; Wang, Z.; Zhang, J. Pathomechanisms of Oxidative Stress in Inflammatory Bowel Disease and Potential Antioxidant Therapies. Oxidative Med. Cell. Longev. 2017, 2017, 4535194. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Shen, L.; Luo, H. Luteolin ameliorates dextran sulfate sodium-induced colitis in mice possibly through activation of the Nrf2 signaling pathway. Int. Immunopharmacol. 2016, 40, 24–31. [Google Scholar] [CrossRef]
- Wang, K.; Lv, Q.; Miao, Y.-m.; Qiao, S.-m.; Dai, Y.; Wei, Z.-f. Cardamonin, a natural flavone, alleviates inflammatory bowel disease by the inhibition of NLRP3 inflammasome activation via an AhR/Nrf2/NQO1 pathway. Biochem. Pharmacol. 2018, 155, 494–509. [Google Scholar] [CrossRef]
- Zhou, Y.; Liu, H.; Song, J.; Cao, L.; Tang, L.; Qi, C. Sinomenine alleviates dextran sulfate sodium-induced colitis via the Nrf2/NQO-1 signaling pathway. Mol. Med. Rep. 2018, 18, 3691–3698. [Google Scholar] [CrossRef] [Green Version]
- Beaugerie, L.; Brousse, N.; Bouvier, A.M.; Colombel, J.F.; Lémann, M.; Cosnes, J.; Hébuterne, X.; Cortot, A.; Bouhnik, Y.; Gendre, J.P.; et al. Lymphoproliferative disorders in patients receiving thiopurines for inflammatory bowel disease: A prospective observational cohort study. Lancet 2009, 374, 1617–1625. [Google Scholar] [CrossRef]
- Faubion, W.A.; Loftus, E.V.; Harmsen, W.S.; Zinsmeister, A.R.; Sandborn, W.J. The natural history of corticosteroid therapy for inflammatory bowel disease: A population-based study. Gastroenterology 2001, 121, 255–260. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Govani, S.M.; Higgins, P.D.R. Combination of thiopurines and allopurinol: Adverse events and clinical benefit in IBD. J. Crohn’s Colitis 2010, 4, 444–449. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stallmach, A.; Hagel, S.; Bruns, T. Adverse effects of biologics used for treating IBD. Best Pract. Res. Clin. Gastroenterol. 2010, 24, 167–182. [Google Scholar] [CrossRef] [PubMed]
- Briere, J.J.; Schlemmer, D.; Chretien, D.; Rustin, P. Quinone analogues regulate mitochondrial substrate competitive oxidation. Biochem. Biophys. Res. Commun. 2004, 316, 1138–1142. [Google Scholar] [CrossRef] [PubMed]
- Suno, M.; Nagaoka, A. Inhibition of lipid peroxidation by a novel compound, idebenone (CV-2619). Jpn. J. Pharmacol. 1984, 35, 196–198. [Google Scholar] [CrossRef] [Green Version]
- Becker, C.; Bray-French, K.; Drewe, J. Pharmacokinetic evaluation of idebenone. Expert Opin. Drug Metab. Toxicol. 2010, 6, 1437–1444. [Google Scholar] [CrossRef]
- Dashdorj, A.; KR, J.; Lim, S.; Jo, A.; Nguyen, M.N.; Ha, J.; Yoon, K.-S.; Kim, H.J.; Park, J.-H.; Murphy, M.P.; et al. Mitochondria-targeted antioxidant MitoQ ameliorates experimental mouse colitis by suppressing NLRP3 inflammasome-mediated inflammatory cytokines. BMC Med. 2013, 11, 178. [Google Scholar] [CrossRef] [Green Version]
- Al-Rasheed, N.M.; Faddah, L.M.; Mohamed, A.M.; Abdel Baky, N.A.; Al-Rasheed, N.M.; Mohammad, R.A. Potential impact of quercetin and idebenone against immuno-inflammatory and oxidative renal damage induced in rats by titanium dioxide nanoparticles toxicity. J. Oleo Sci. 2013, 62, 961–971. [Google Scholar] [CrossRef] [Green Version]
- Yan, A.; Liu, Z.; Song, L.; Wang, X.; Zhang, Y.; Wu, N.; Lin, J.; Liu, Y.; Liu, Z. Idebenone Alleviates Neuroinflammation and Modulates Microglial Polarization in LPS-Stimulated BV2 Cells and MPTP-Induced Parkinson’s Disease Mice. Front. Cell. Neurosci. 2019, 12, 529. [Google Scholar] [CrossRef]
- Mordente, A.; Martorana, G.E.; Minotti, G.; Giardina, B. Antioxidant properties of 2,3-dimethoxy-5-methyl-6-(10-hydroxydecyl)-1,4-benzoquinone (idebenone). Chem. Res. Toxicol. 1998, 11, 54–63. [Google Scholar] [CrossRef]
- Muscoli, C.; Fresta, M.; Cardile, V.; Palumbo, M.; Renis, M.; Puglisi, G.; Paolino, D.; Nistico, S.; Rotiroti, D.; Mollace, V. Ethanol-induced injury in rat primary cortical astrocytes involves oxidative stress: Effect of idebenone. Neurosci. Lett. 2002, 329, 21–24. [Google Scholar] [CrossRef]
- Di Prospero, N.A.; Baker, A.; Jeffries, N.; Fischbeck, K.H. Neurological effects of high-dose idebenone in patients with Friedreich’s ataxia: A randomised, placebo-controlled trial. Lancet. Neurol. 2007, 6, 878–886. [Google Scholar] [CrossRef] [Green Version]
- Yamada, K.; Tanaka, T.; Han, D.; Senzaki, K.; Kameyama, T.; Nabeshima, T. Protective effects of idebenone and alpha-tocopherol on beta-amyloid-(1-42)-induced learning and memory deficits in rats: Implication of oxidative stress in beta-amyloid-induced neurotoxicity in vivo. Eur. J. Neurosci. 1999, 11, 83–90. [Google Scholar] [CrossRef]
- Miyamoto, M.; Coyle, J.T. Idebenone attenuates neuronal degeneration induced by intrastriatal injection of excitotoxins. Exp. Neurol. 1990, 108, 38–45. [Google Scholar] [CrossRef]
- Suno, M.; Nagaoka, A. Inhibition of lipid peroxidation by idebenone in brain mitochondria in the presence of succinate. Arch. Gerontol. Geriatr. 1989, 8, 291–297. [Google Scholar] [CrossRef]
- Giorgio, V.; Petronilli, V.; Ghelli, A.; Carelli, V.; Rugolo, M.; Lenaz, G.; Bernardi, P. The effects of idebenone on mitochondrial bioenergetics. Biochim. Biophys. Acta (BBA) Bioenerg. 2012, 1817, 363–369. [Google Scholar] [CrossRef]
- Rauchová, H.; Vrbacký, M.; Bergamini, C.; Fato, R.; Lenaz, G.; Houštěk, J.; Drahota, Z. Inhibition of glycerophosphate-dependent H2O2 generation in brown fat mitochondria by idebenone. Biochem. Biophys. Res. Commun. 2006, 339, 362–366. [Google Scholar] [CrossRef]
- Haefeli, R.H.; Erb, M.; Gemperli, A.C.; Robay, D.; Courdier Fruh, I.; Anklin, C.; Dallmann, R.; Gueven, N. NQO1-dependent redox cycling of idebenone: Effects on cellular redox potential and energy levels. PLoS ONE 2011, 6, e17963. [Google Scholar] [CrossRef] [Green Version]
- Lind, C.; Hochstein, P.; Ernster, L. DT-diaphorase as a quinone reductase: A cellular control device against semiquinone and superoxide radical formation. Arch. Biochem. Biophys. 1982, 216, 178–185. [Google Scholar] [CrossRef]
- O’Brien, P.J. Molecular mechanisms of quinone cytotoxicity. Chem. Biol. Interact. 1991, 80, 1–41. [Google Scholar] [CrossRef]
- Fadda, L.M.; Hagar, H.; Mohamed, A.M.; Ali, H.M. Quercetin and Idebenone Ameliorate Oxidative Stress, Inflammation, DNA damage, and Apoptosis Induced by Titanium Dioxide Nanoparticles in Rat Liver. Dose Response A Publ. Int. Hormesis Soc. 2018, 16, 1559325818812188. [Google Scholar] [CrossRef] [PubMed]
- Buyse, G.M.; Van der Mieren, G.; Erb, M.; D’Hooge, J.; Herijgers, P.; Verbeken, E.; Jara, A.; Van Den Bergh, A.; Mertens, L.; Courdier-Fruh, I.; et al. Long-term blinded placebo-controlled study of SNT-MC17/idebenone in the dystrophin deficient mdx mouse: Cardiac protection and improved exercise performance. Eur. Heart J. 2009, 30, 116–124. [Google Scholar] [CrossRef] [PubMed]
- Heitz, F.D.; Erb, M.; Anklin, C.; Robay, D.; Pernet, V.; Gueven, N. Idebenone protects against retinal damage and loss of vision in a mouse model of Leber’s hereditary optic neuropathy. PLoS ONE 2012, 7, e45182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nair, A.B.; Jacob, S. A simple practice guide for dose conversion between animals and human. J. Basic Clin. Pharm. 2016, 7, 27–31. [Google Scholar] [CrossRef] [Green Version]
- Di Prospero, N.A.; Sumner, C.J.; Penzak, S.R.; Ravina, B.; Fischbeck, K.H.; Taylor, J.P. Safety, Tolerability, and Pharmacokinetics of High-Dose Idebenone in Patients With Friedreich Ataxia. JAMA Neurol. 2007, 64, 803–808. [Google Scholar] [CrossRef] [PubMed]
- Moura, F.A.; de Andrade, K.Q.; Dos Santos, J.C.F.; Araújo, O.R.P.; Goulart, M.O.F. Antioxidant therapy for treatment of inflammatory bowel disease: Does it work? Redox Biol. 2015, 6, 617–639. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, X.T.; Xu, Y.F.; Huang, Y.F.; Qu, C.; Xu, L.Q.; Su, Z.R.; Zeng, H.F.; Zheng, L.; Yi, T.G.; Li, H.L.; et al. Berberrubine attenuates mucosal lesions and inflammation in dextran sodium sulfate-induced colitis in mice. PLoS ONE 2018, 13, e0194069. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bhattacharyya, A.; Chattopadhyay, R.; Mitra, S.; Crowe, S.E. Oxidative stress: An essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol. Rev. 2014, 94, 329–354. [Google Scholar] [CrossRef] [Green Version]
- Lean, Q.Y.; Eri, R.D.; Randall-Demllo, S.; Sohal, S.S.; Stewart, N.; Peterson, G.M.; Gueven, N.; Patel, R.P. Orally Administered Enoxaparin Ameliorates Acute Colitis by Reducing Macrophage-Associated Inflammatory Responses. PLoS ONE 2015, 10, e0134259. [Google Scholar] [CrossRef] [Green Version]
- Siegel, D.; Gustafson, D.L.; Dehn, D.L.; Han, J.Y.; Boonchoong, P.; Berliner, L.J.; Ross, D. NAD(P)H:quinone oxidoreductase 1: Role as a superoxide scavenger. Mol. Pharmacol. 2004, 65, 1238–1247. [Google Scholar] [CrossRef] [Green Version]
- Zhu, H.; Jia, Z.; Mahaney, J.E.; Ross, D.; Misra, H.P.; Trush, M.A.; Li, Y. The highly expressed and inducible endogenous NAD(P)H:quinone oxidoreductase 1 in cardiovascular cells acts as a potential superoxide scavenger. Cardiovasc. Toxicol. 2007, 7, 202–211. [Google Scholar] [CrossRef] [PubMed]
- Pandurangan, A.K.; Mohebali, N.; Norhaizan, M.E.; Looi, C.Y. Gallic acid attenuates dextran sulfate sodium-induced experimental colitis in BALB/c mice. Drug Des. Dev. Ther. 2015, 9, 3923–3934. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, L.; Yang, Z.-L.; Li, P.; Zhou, Y.-Q. Modulating effect of Hesperidin on experimental murine colitis induced by dextran sulfate sodium. Phytomedicine 2009, 16, 989–995. [Google Scholar] [CrossRef] [PubMed]
- Yang, N.; Xia, Z.; Shao, N.; Li, B.; Xue, L.; Peng, Y.; Zhi, F.; Yang, Y. Carnosic acid prevents dextran sulfate sodium-induced acute colitis associated with the regulation of the Keap1/Nrf2 pathway. Sci. Rep. 2017, 7, 11036. [Google Scholar] [CrossRef] [PubMed]
- Shafik, N.M.; Gaber, R.A.; Mohamed, D.A.; Ebeid, A.M. Hesperidin modulates dextran sulfate sodium-induced ulcerative colitis in rats: Targeting sphingosine kinase-1-sphingosine 1 phosphate signaling pathway, mitochondrial biogenesis, inflammation, and apoptosis. J. Biochem. Mol. Toxicol. 2019, 33, e22312. [Google Scholar] [CrossRef]
- Nam, S.T.; Hwang, J.H.; Kim, D.H.; Park, M.J.; Lee, I.H.; Nam, H.J.; Kang, J.K.; Kim, S.K.; Hwang, J.S.; Chung, H.K.; et al. Role of NADH: Quinone oxidoreductase-1 in the tight junctions of colonic epithelial cells. BMB Rep. 2014, 47, 494–499. [Google Scholar] [CrossRef] [Green Version]
- Mellors, A.; Tappel, A.L. The inhibition of mitochondrial peroxidation by ubiquinone and ubiquinol. J. Biol. Chem. 1966, 241, 4353–4356. [Google Scholar]
- Tomita, R.; Tanjoh, K. Role of nitric oxide in the colon of patients with ulcerative colitis. World J. Surg. 1998, 22, 88–92. [Google Scholar] [CrossRef]
- Avdagić, N.; Zaćiragić, A.; Babić, N.; Hukić, M.; Seremet, M.; Lepara, O.; Nakaš-Ićindić, E. Nitric oxide as a potential biomarker in inflammatory bowel disease. Bosn. J. Basic Med. Sci. 2013, 13, 5–9. [Google Scholar] [CrossRef] [Green Version]
- Moura, R.M.; Hartmann, R.M.; Licks, F.; Schemitt, E.G.; Colares, J.R.; do Couto Soares, M.; Fillmann, L.S.; Fillmann, H.S.; Marroni, N.P. Antioxidant effect of mesalazine in the experimental colitis model induced by acetic acid. J. Coloproctol. 2016, 36, 139–148. [Google Scholar] [CrossRef] [Green Version]
- Esposti, M.D.; Ngo, A.; Ghelli, A.; Benelli, B.; Carelli, V.; McLennan, H.; Linnane, A.W. The interaction of Q analogs, particularly hydroxydecyl benzoquinone (idebenone), with the respiratory complexes of heart mitochondria. Arch. Biochem. Biophys. 1996, 330, 395–400. [Google Scholar] [CrossRef] [PubMed]
- Gueven, N.; Woolley, K.; Smith, J. Border between natural product and drug: Comparison of the related benzoquinones idebenone and coenzyme Q10. Redox Biol. 2015, 4, 289–295. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rao, R.K.; Basuroy, S.; Rao, V.U.; Karnaky, K.J.; Gupta, A. Tyrosine phosphorylation and dissociation of occludin–ZO-1 and E-cadherin–β-catenin complexes from the cytoskeleton by oxidative stress. Biochem. J. 2002, 368, 471–481. [Google Scholar] [CrossRef] [PubMed]
- Rao, R.K.; Baker, R.D.; Baker, S.S.; Gupta, A.; Holycross, M. Oxidant-induced disruption of intestinal epithelial barrier function: Role of protein tyrosine phosphorylation. Am. J. Physiol. Gastrointest. Liver Physiol. 1997, 273, G812–G823. [Google Scholar] [CrossRef] [PubMed]
- Kevil, C.G.; Oshima, T.; Alexander, B.; Coe, L.L.; Alexander, J.S. H2O2-mediated permeability: Role of MAPK and occludin. Am. J. Physiol. Cell Physiol. 2000, 279, C21–C30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oshima, T.; Sasaki, M.; Kataoka, H.; Miwa, H.; Takeuchi, T.; Joh, T. Wip1 protects hydrogen peroxide-induced colonic epithelial barrier dysfunction. Cell. Mol. Life Sci. 2007, 64, 3139–3147. [Google Scholar] [CrossRef]
- Fink, M.P. Intestinal epithelial hyperpermeability: Update on the pathogenesis of gut mucosal barrier dysfunction in critical illness. Curr. Opin. Crit. Care 2003, 9, 143–151. [Google Scholar] [CrossRef]
- Rao, R. Oxidative stress-induced disruption of epithelial and endothelial tight junctions. Front. Biosci. A J. Virtual Libr. 2008, 13, 7210–7226. [Google Scholar] [CrossRef] [Green Version]
- Turner, J.R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 2009, 9, 799–809. [Google Scholar] [CrossRef]
- Ischiropoulos, H.; Zhu, L.; Beckman, J.S. Peroxynitrite formation from macrophage-derived nitric oxide. Arch. Biochem. Biophys. 1992, 298, 446–451. [Google Scholar] [CrossRef]
- Sun, Y.N.; Liu, L.B.; Xue, Y.X.; Wang, P. Effects of insulin combined with idebenone on blood-brain barrier permeability in diabetic rats. J. Neurosci. Res. 2015, 93, 666–677. [Google Scholar] [CrossRef] [PubMed]
- Shinde, T.; Perera, A.P.; Vemuri, R.; Gondalia, S.V.; Karpe, A.V.; Beale, D.J.; Shastri, S.; Southam, B.; Eri, R.; Stanley, R. Synbiotic Supplementation Containing Whole Plant Sugar Cane Fibre and Probiotic Spores Potentiates Protective Synergistic Effects in Mouse Model of IBD. Nutrients 2019, 11, 818. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, M.; Wang, B.; Sun, X.; Tang, Y.; Wei, X.; Ge, B.; Tang, Y.; Deng, Y.; He, C.; Yuan, J.; et al. Upregulation of Intestinal Barrier Function in Mice with DSS-Induced Colitis by a Defined Bacterial Consortium Is Associated with Expansion of IL-17A Producing Gamma Delta T Cells. Front. Immunol. 2017, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gersemann, M.; Becker, S.; Kubler, I.; Koslowski, M.; Wang, G.; Herrlinger, K.R.; Griger, J.; Fritz, P.; Fellermann, K.; Schwab, M.; et al. Differences in goblet cell differentiation between Crohn’s disease and ulcerative colitis. Differ. Res. Biol. Divers. 2009, 77, 84–94. [Google Scholar] [CrossRef] [PubMed]
- Strober, W.; Fuss, I.J. Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases. Gastroenterology 2011, 140, 1756–1767. [Google Scholar] [CrossRef] [Green Version]
- Geremia, A.; Biancheri, P.; Allan, P.; Corazza, G.R.; Di Sabatino, A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun. Rev. 2014, 13, 3–10. [Google Scholar] [CrossRef]
- Strober, W.; Fuss, I.J.; Blumberg, R.S. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 2002, 20, 495–549. [Google Scholar] [CrossRef]
- Alex, P.; Zachos, N.C.; Nguyen, T.; Gonzales, L.; Chen, T.E.; Conklin, L.S.; Centola, M.; Li, X. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm. Bowel Dis. 2009, 15, 341–352. [Google Scholar] [CrossRef]
- Neurath, M.F. Cytokines in inflammatory bowel disease. Nat. Rev. Immunol. 2014, 14, 329. [Google Scholar] [CrossRef]
- Yan, Y.; Kolachala, V.; Dalmasso, G.; Nguyen, H.; Laroui, H.; Sitaraman, S.V.; Merlin, D. Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS ONE 2009, 4, e6073. [Google Scholar] [CrossRef]
- Heinsbroek, S.E.; Gordon, S. The role of macrophages in inflammatory bowel diseases. Expert Rev. Mol. Med. 2009, 11, e14. [Google Scholar] [CrossRef] [PubMed]
- Mu, H.X.; Liu, J.; Fatima, S.; Lin, C.Y.; Shi, X.K.; Du, B.; Xiao, H.T.; Fan, B.M.; Bian, Z.X. Anti-inflammatory Actions of (+)-3′alpha-Angeloxy-4′-keto-3′,4′-dihydroseselin (Pd-Ib) against Dextran Sulfate Sodium-Induced Colitis in C57BL/6 Mice. J. Nat. Prod. 2016, 79, 1056–1062. [Google Scholar] [CrossRef] [PubMed]
- Lean, Q.Y.; Eri, R.D.; Fitton, J.H.; Patel, R.P.; Gueven, N. Fucoidan Extracts Ameliorate Acute Colitis. PLoS ONE 2015, 10, e0128453. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Melgar, S.; Yeung, M.M.; Bas, A.; Forsberg, G.; Suhr, O.; Oberg, A.; Hammarstrom, S.; Danielsson, A.; Hammarstrom, M.L. Over-expression of interleukin 10 in mucosal T cells of patients with active ulcerative colitis. Clin. Exp. Immunol. 2003, 134, 127–137. [Google Scholar] [CrossRef] [PubMed]
- Tsuchiya, K.; Ikeda, T.; Batmunkh, B.; Choijookhuu, N.; Ishizaki, H.; Hotokezaka, M.; Hishikawa, Y.; Nanashima, A. Frequency of CD4 + CD161 + T Cell and Interleukin-10 Expression in Inflammatory Bowel Diseases. Acta Histochem. Cytochem. 2017, 50, 21–28. [Google Scholar] [CrossRef] [Green Version]
- SCHREIBER, S. Interleukin-10 in the intestine. Gut 1997, 41, 274–275. [Google Scholar] [CrossRef] [Green Version]
- Ajuebor, M.N.; Swain, M.G. Role of chemokines and chemokine receptors in the gastrointestinal tract. Immunology 2002, 105, 137–143. [Google Scholar] [CrossRef]
- Banks, C.; Bateman, A.; Payne, R.; Johnson, P.; Sheron, N. Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn’s disease. J. Pathol. 2003, 199, 28–35. [Google Scholar] [CrossRef]
- Adar, T.; Shteingart, S.; Ben-Ya’acov, A.; Shitrit, A.B.; Livovsky, D.M.; Shmorak, S.; Mahamid, M.; Melamud, B.; Vernea, F.; Goldin, E. The Importance of Intestinal Eotaxin-1 in Inflammatory Bowel Disease: New Insights and Possible Therapeutic Implications. Dig. Dis. Sci. 2016, 61, 1915–1924. [Google Scholar] [CrossRef]
- Castaneda, O.A.; Lee, S.-C.; Ho, C.-T.; Huang, T.-C. Macrophages in oxidative stress and models to evaluate the antioxidant function of dietary natural compounds. J. Food Drug Anal. 2017, 25, 111–118. [Google Scholar] [CrossRef] [Green Version]
- Holt, P.R.; Katz, S.; Kirshoff, R. Curcumin therapy in inflammatory bowel disease: A pilot study. Dig. Dis. Sci. 2005, 50, 2191–2193. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barbosa, D.S.; Cecchini, R.; El Kadri, M.Z.; Rodriguez, M.A.; Burini, R.C.; Dichi, I. Decreased oxidative stress in patients with ulcerative colitis supplemented with fish oil omega-3 fatty acids. Nutrition 2003, 19, 837–842. [Google Scholar] [CrossRef]
- Baraniuk, J.N.; El-Amin, S.; Corey, R.; Rayhan, R.; Timbol, C. Carnosine treatment for gulf war illness: A randomized controlled trial. Glob. J. Health Sci. 2013, 5, 69–81. [Google Scholar] [CrossRef]
- Samsami-Kor, M.; Daryani, N.E.; Asl, P.R.; Hekmatdoost, A. Anti-Inflammatory Effects of Resveratrol in Patients with Ulcerative Colitis: A Randomized, Double-Blind, Placebo-controlled Pilot Study. Arch. Med. Res. 2015, 46, 280–285. [Google Scholar] [CrossRef] [PubMed]
- Erichsen, K.; Ulvik, R.J.; Nysaeter, G.; Johansen, J.; Ostborg, J.; Berstad, A.; Berge, R.K.; Hausken, T. Oral ferrous fumarate or intravenous iron sucrose for patients with inflammatory bowel disease. Scand. J. Gastroenterol. 2005, 40, 1058–1065. [Google Scholar] [CrossRef] [PubMed]
- Lang, A.; Salomon, N.; Wu, J.C.; Kopylov, U.; Lahat, A.; Har-Noy, O.; Ching, J.Y.; Cheong, P.K.; Avidan, B.; Gamus, D.; et al. Curcumin in Combination With Mesalamine Induces Remission in Patients With Mild-to-Moderate Ulcerative Colitis in a Randomized Controlled Trial. Clin. Gastroenterol. Hepatol. 2015, 13, 1444–1449.e1. [Google Scholar] [CrossRef] [PubMed]
- Hoentjen, F.; Seinen, M.L.; Hanauer, S.B.; de Boer, N.K.; Rubin, D.T.; Bouma, G.; Harrell, L.E.; van Bodegraven, A.A. Safety and effectiveness of long-term allopurinol-thiopurine maintenance treatment in inflammatory bowel disease. Inflamm. Bowel Dis. 2013, 19, 363–369. [Google Scholar] [CrossRef]
- Seril, D.N.; Liao, J.; Yang, G.-Y.; Yang, C.S. Oxidative stress and ulcerative colitis-associated carcinogenesis: Studies in humans and animal models. Carcinogenesis 2003, 24, 353–362. [Google Scholar] [CrossRef] [Green Version]
- Oz, H.S.; Chen, T.; de Villiers, W.J. Green Tea Polyphenols and Sulfasalazine have Parallel Anti-Inflammatory Properties in Colitis Models. Front. Immunol. 2013, 4, 132. [Google Scholar] [CrossRef] [Green Version]
- Arab, H.H.; Al-Shorbagy, M.Y.; Abdallah, D.M.; Nassar, N.N. Telmisartan attenuates colon inflammation, oxidative perturbations and apoptosis in a rat model of experimental inflammatory bowel disease. PLoS ONE 2014, 9, e97193. [Google Scholar] [CrossRef] [Green Version]
- El Morsy, E.M.; Kamel, R.; Ahmed, M.A. Attenuating effects of coenzyme Q10 and amlodipine in ulcerative colitis model in rats. Immunopharmacol. Immunotoxicol. 2015, 37, 244–251. [Google Scholar] [CrossRef] [PubMed]
- Youn, J.; Lee, J.S.; Na, H.K.; Kundu, J.K.; Surh, Y.J. Resveratrol and piceatannol inhibit iNOS expression and NF-kappaB activation in dextran sulfate sodium-induced mouse colitis. Nutr. Cancer 2009, 61, 847–854. [Google Scholar] [CrossRef] [PubMed]
- Murthy, S.N.; Cooper, H.S.; Shim, H.; Shah, R.S.; Ibrahim, S.A.; Sedergran, D.J. Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin. Dig. Dis. Sci. 1993, 38, 1722–1734. [Google Scholar] [CrossRef] [PubMed]
- Koelink, P.J.; Wildenberg, M.E.; Stitt, L.W.; Feagan, B.G.; Koldijk, M.; van’t Wout, A.B.; Atreya, R.; Vieth, M.; Brandse, J.F.; Duijst, S.; et al. Development of Reliable, Valid and Responsive Scoring Systems for Endoscopy and Histology in Animal Models for Inflammatory Bowel Disease. J. Crohn’s Colitis 2018, 12, 794–803. [Google Scholar] [CrossRef] [Green Version]
- Sovran, B.; Lu, P.; Loonen, L.M.; Hugenholtz, F.; Belzer, C.; Stolte, E.H.; Boekschoten, M.V.; van Baarlen, P.; Smidt, H.; Kleerebezem, M.; et al. Identification of Commensal Species Positively Correlated with Early Stress Responses to a Compromised Mucus Barrier. Inflamm. Bowel Dis. 2016, 22, 826–840. [Google Scholar] [CrossRef] [Green Version]
- Das, A.; Durrant, D.; Koka, S.; Salloum, F.N.; Xi, L.; Kukreja, R.C. Mammalian target of rapamycin (mTOR) inhibition with rapamycin improves cardiac function in type 2 diabetic mice: Potential role of attenuated oxidative stress and altered contractile protein expression. J. Biol. Chem. 2014, 289, 4145–4160. [Google Scholar] [CrossRef] [Green Version]
- Ojalvo, A.G.; Acosta, J.B.; Mari, Y.M.; Mayola, M.F.; Perez, C.V.; Gutierrez, W.S.; Marichal, I.I.; Seijas, E.A.; Kautzman, A.M.; Pacheco, A.E.; et al. Healing enhancement of diabetic wounds by locally infiltrated epidermal growth factor is associated with systemic oxidative stress reduction. Int. Wound J. 2017, 14, 214–225. [Google Scholar] [CrossRef]
- Waitumbi, J.; Warburg, A. Phlebotomus papatasi saliva inhibits protein phosphatase activity and nitric oxide production by murine macrophages. Infect. Immun. 1998, 66, 1534–1537. [Google Scholar] [CrossRef] [Green Version]
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Shastri, S.; Shinde, T.; Sohal, S.S.; Gueven, N.; Eri, R. Idebenone Protects against Acute Murine Colitis via Antioxidant and Anti-Inflammatory Mechanisms. Int. J. Mol. Sci. 2020, 21, 484. https://doi.org/10.3390/ijms21020484
Shastri S, Shinde T, Sohal SS, Gueven N, Eri R. Idebenone Protects against Acute Murine Colitis via Antioxidant and Anti-Inflammatory Mechanisms. International Journal of Molecular Sciences. 2020; 21(2):484. https://doi.org/10.3390/ijms21020484
Chicago/Turabian StyleShastri, Sonia, Tanvi Shinde, Sukhwinder Singh Sohal, Nuri Gueven, and Rajaraman Eri. 2020. "Idebenone Protects against Acute Murine Colitis via Antioxidant and Anti-Inflammatory Mechanisms" International Journal of Molecular Sciences 21, no. 2: 484. https://doi.org/10.3390/ijms21020484