156
Views
0
CrossRef citations to date
0
Altmetric
Original Articles

Celecoxib alleviates the DSS-induced ulcerative colitis in mice by enhancing intestinal barrier function, inhibiting ferroptosis and suppressing apoptosis

, , , , , , , , & show all
Pages 240-254 | Received 18 Dec 2022, Accepted 17 Dec 2023, Published online: 18 Jan 2024

References

  • Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 2011;474(7351):298–306. doi: 10.1038/nature10208.
  • Pantavou K, Yiallourou AI, Piovani D, et al. Efficacy and safety of biologic agents and tofacitinib in moderate-to-severe ulcerative colitis: a systematic overview of meta-analyses. United European Gastroenterol J. 2019;7(10):1285–1303. doi: 10.1177/2050640619883566.
  • Zhang ZL, Fan HY, Yang MY, et al. Therapeutic effect of a hydroxynaphthoquinone fraction on dextran sulfate sodium-induced ulcerative colitis. World J Gastroenterol. 2014;20(41):15310–15318. doi: 10.3748/wjg.v20.i41.15310.
  • Wang J, Zhang C, Guo C, et al. Chitosan ameliorates DSS-Induced ulcerative colitis mice by enhancing intestinal barrier function and improving microflora. Int J Mol Sci. 2019;20(22):20.
  • Rogler G. Chronic ulcerative colitis and colorectal cancer. Cancer Lett. 2014;345(2):235–241. doi: 10.1016/j.canlet.2013.07.032.
  • Cui L, Guan X, Ding W, et al. Scutellaria baicalensis georgi polysaccharide ameliorates DSS-induced ulcerative colitis by improving intestinal barrier function and modulating gut microbiota. Int J Biol Macromol. 2021;166:1035–1045. doi: 10.1016/j.ijbiomac.2020.10.259.
  • Chen Y, Zhang P, Chen W, et al. Ferroptosis mediated DSS-induced ulcerative colitis associated with Nrf2/HO-1 signaling pathway. Immunol Lett. 2020;225:9–15. doi: 10.1016/j.imlet.2020.06.005.
  • Huang J, Zhang J, Ma J, et al. Inhibiting ferroptosis: a novel approach for ulcerative colitis therapeutics. Oxid Med Cell Longev. 2022;2022:9678625.
  • Wan Y, Yang L, Jiang S, et al. Excessive apoptosis in ulcerative colitis: crosstalk between apoptosis, ROS, ER stress, and intestinal homeostasis. Inflamm Bowel Dis. 2022;28(4):639–648. doi: 10.1093/ibd/izab277.
  • Shen J, Cheng J, Zhu S, et al. Regulating effect of baicalin on IKK/IKB/NF-kB signaling pathway and apoptosis-related proteins in rats with ulcerative colitis. Int Immunopharmacol. 2019;73:193–200. doi: 10.1016/j.intimp.2019.04.052.
  • Zhang C, Zhu H, Jie H, et al. Arbutin ameliorated ulcerative colitis of mice induced by dextran sodium sulfate (DSS). Bioengineered. 2021;12(2):11707–11715. doi: 10.1080/21655979.2021.2005746.
  • Li H, Ye XF, Su YS, et al. Mechanism of acupuncture and moxibustion on promoting mucosal healing in ulcerative colitis. Chin J Integr Med. 2022;29(9):847–856. doi: 10.1007/s11655-022-3531-x.
  • Wang X, Gao Y, Wang L, et al. Troxerutin improves dextran sulfate sodium-induced ulcerative colitis in mice. J Agric Food Chem. 2021;69(9):2729–2744. doi: 10.1021/acs.jafc.0c06755.
  • Teshima CW, Dieleman LA, Meddings JB. Abnormal intestinal permeability in crohn’s disease pathogenesis. Ann N Y Acad Sci. 2012;1258(1):159–165. doi: 10.1111/j.1749-6632.2012.06612.x.
  • Michielan A, D’Incà R. Intestinal permeability in inflammatory bowel disease: pathogenesis, clinical evaluation, and therapy of leaky gut. Mediators Inflamm. 2015;2015:628157–628110. doi: 10.1155/2015/628157.
  • Yang F, Wang A, Zeng X, et al. Lactobacillus reuteri I5007 modulates tight junction protein expression in IPEC-J2 cells with LPS stimulation and in newborn piglets under normal conditions. BMC Microbiol. 2015;15(1):32. doi: 10.1186/s12866-015-0372-1.
  • Zhu L, Han J, Li L, et al. Claudin family participates in the pathogenesis of inflammatory bowel diseases and colitis-associated colorectal cancer. Front Immunol. 2019;10:1441. doi: 10.3389/fimmu.2019.01441.
  • Capaldo CT, Nusrat A. Claudin switching: physiological plasticity of the tight junction. Semin Cell Dev Biol. 2015;42:22–29. doi: 10.1016/j.semcdb.2015.04.003.
  • Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149(5):1060–1072. doi: 10.1016/j.cell.2012.03.042.
  • Hirschhorn T, Stockwell BR. The development of the concept of ferroptosis. Free Radic Biol Med. 2019;133:130–143. doi: 10.1016/j.freeradbiomed.2018.09.043.
  • Sheng X, Shan C, Liu J, et al. Theoretical insights into the mechanism of ferroptosis suppression via inactivation of a lipid peroxide radical by liproxstatin-1. Phys Chem Chem Phys. 2017;19(20):13153–13159. doi: 10.1039/c7cp00804j.
  • Tsurusaki S, Tsuchiya Y, Koumura T, et al. Hepatic ferroptosis plays an important role as the trigger for initiating inflammation in nonalcoholic steatohepatitis. Cell Death Dis. 2019;10(6):449. doi: 10.1038/s41419-019-1678-y.
  • Li Y, Feng D, Wang Z, et al. Ischemia-induced ACSL4 activation contributes to ferroptosis-mediated tissue injury in intestinal ischemia/reperfusion. Cell Death Differ. 2019;26(11):2284–2299. doi: 10.1038/s41418-019-0299-4.
  • Gao W, Zhang T, Wu H. Emerging pathological engagement of ferroptosis in gut diseases. Oxid Med Cell Longev. 2021;2021:4246255–4246216. doi: 10.1155/2021/4246255.
  • Kobayashi Y, Ohfuji S, Kondo K, et al. Association between dietary iron and zinc intake and development of ulcerative colitis: a case-control study in Japan. J Gastroenterol Hepatol. 2019;34(10):1703–1710. doi: 10.1111/jgh.14642.
  • Triantafillidis J, Vagianos C, Agrogiannis G, et al. Effect of infliximab and adalimumab on experimental colitis following orally supplemented iron. J Invest Surg. 2017;30(1):6–12. doi: 10.1080/08941939.2016.1215574.
  • Xu M, Tao J, Yang Y, et al. Ferroptosis involves in intestinal epithelial cell death in ulcerative colitis. Cell Death Dis. 2020;11(2):86. doi: 10.1038/s41419-020-2299-1.
  • Günther C, Neumann H, Neurath MF, et al. Apoptosis, necrosis and necroptosis: cell death regulation in the intestinal epithelium. Gut. 2013;62(7):1062–1071. doi: 10.1136/gutjnl-2011-301364.
  • Zhang M, Qin X, Zhao Z, et al. A self-amplifying nanodrug to manipulate the janus-faced nature of ferroptosis for tumor therapy. Nanoscale Horiz. 2022;7(2):198–210. doi: 10.1039/d1nh00506e.
  • Chou R, Qaseem A, Snow V, et al. Diagnosis and treatment of low back pain: a joint clinical practice guideline from the American college of physicians and the American pain society. Ann Intern Med. 2007;147(7):478–491. doi: 10.7326/0003-4819-147-7-200710020-00006.
  • Tick H, Nielsen A, Pelletier KR, et al. Evidence-Based nonpharmacologic strategies for comprehensive pain care: the consortium pain task force white paper. Explore (NY). 2018;14(3):177–211. doi: 10.1016/j.explore.2018.02.001.
  • Chou R, Fanciullo GJ, Fine PG, et al. Clinical guidelines for the use of chronic opioid therapy in chronic noncancer pain. J Pain. 2009;10(2):113–130. doi: 10.1016/j.jpain.2008.10.008.
  • Tang C, Shou M, Mei Q, et al. Rodrigues AD: major role of human liver microsomal cytochrome P450 2C9 (CYP2C9) in the oxidative metabolism of celecoxib, a novel cyclooxygenase-II inhibitor. J Pharmacol Exp Ther. 2000;293(2):453–459.
  • Sandberg M, Yasar U, Strömberg P, et al. Oxidation of celecoxib by polymorphic cytochrome P450 2C9 and alcohol dehydrogenase. Br J Clin Pharmacol. 2002;54(4):423–429. doi: 10.1046/j.1365-2125.2002.01660.x.
  • Thompson PA, Ashbeck EL, Roe DJ, et al. Celecoxib for the prevention of colorectal adenomas: results of a suspended randomized controlled trial. J Natl Cancer Inst. 2016;108(12):djw151. doi: 10.1093/jnci/djw152.
  • Bertagnolli MM, Eagle CJ, Zauber AG, et al. Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med. 2006;355(9):873–884. doi: 10.1056/NEJMoa061355.
  • Flamiatos JF, Beer TM, Graff JN, et al. Cyclooxygenase-2 (COX-2) inhibition for prostate cancer chemoprevention: double-blind randomised study of pre-prostatectomy celecoxib or placebo. BJU Int. 2017;119(5):709–716. doi: 10.1111/bju.13612.
  • Thompson PA, Martinez JA. The importance of drug concentration at the site of action: celecoxib and colon polyp prevention as a case study. Cancer Prev Res. 2022;15(4):205–208. doi: 10.1158/1940-6207.CAPR-21-0524.
  • Guo J, Li L, Ren Q. Safety evaluation of celecoxib in patients with ulcerative colitis in remission stage with arthritis. Minerva Med. 2021;114(5):758–760. doi: 10.23736/S0026-4806.21.07856-3.
  • Sheta NM, Boshra SA. Fabrication and evaluation of celecoxib oral oleogel to reduce the inflammation of ulcerative colitis. Aaps Pharmscitech. 2021;22(5):180. doi: 10.1208/s12249-021-02042-6.
  • Setia S, Nehru B, Sanyal SN. The PI3K/akt pathway in colitis associated Colon cancer and its chemoprevention with celecoxib, a cox-2 selective inhibitor. Biomed Pharmacother. 2014;68(6):721–727. doi: 10.1016/j.biopha.2014.07.006.
  • Setia S, Nehru B, Sanyal SN. Upregulation of MAPK/erk and PI3K/akt pathways in ulcerative colitis-associated Colon cancer. Biomed Pharmacother. 2014;68(8):1023–1029. doi: 10.1016/j.biopha.2014.09.006.
  • Setia S, Nehru B, Sanyal SN. Celecoxib prevents colitis associated Colon carcinogenesis: an upregulation of apoptosis. Pharmacol Rep. 2014;66(6):1083–1091. doi: 10.1016/j.pharep.2014.07.001.
  • Kamalian A, Sohrabi AM, Dolatshahi M, et al. Interventions of natural and synthetic agents in inflammatory bowel disease, modulation of nitric oxide pathways. World J Gastroenterol. 2020;26(24):3365–3400. doi: 10.3748/wjg.v26.i24.3365.
  • 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(9):1192–1199. doi: 10.1136/gut.2009.197822.
  • Andrés-Manzano MJ, Andrés V, Dorado B. Oil red O and hematoxylin and eosin staining for quantification of atherosclerosis burden in mouse aorta and aortic root. Methods Mol Biol. 2015;1339:85–99. doi: 10.1007/978-1-4939-2929-0_5.
  • Feldman AT, Wolfe D. Tissue processing and hematoxylin and eosin staining. Methods Mol Biol. 2014;1180:31–43. doi: 10.1007/978-1-4939-1050-2_3.
  • Wiesner RJ, Beinbrech B, Rüegg JC. Quantitative PCR. Nature. 1993;366(6454):416–416. doi: 10.1038/366416b0.
  • Siebert PD, Larrick JW. Competitive PCR. Nature. 1992;359(6395):557–558. doi: 10.1038/359557a0.
  • Cheng S, Chang SY, Gravitt P, et al. Long PCR. Nature. 1994;369(6482):684–685. doi: 10.1038/369684a0.
  • Hirano S. Western blot analysis. Methods Mol Biol. 2012;926:87–97. doi: 10.1007/978-1-62703-002-1_6.
  • Hnasko TS, Hnasko RM. The Western blot. Methods Mol Biol. 2015;1318:87–96. doi: 10.1007/978-1-4939-2742-5_9.
  • Abdul KL, Wang P, Chahine J, et al. PD-L1 IHC assays in melanoma. Histopathology. 2017;70(7):1177–1179. doi: 10.1111/his.13174.
  • Liu M, Zhao SQ, Yang L, et al. A direct immunohistochemistry (IHC) method improves the intraoperative diagnosis of breast papillary lesions including breast cancer. Discov Med. 2019;28:29–37.
  • Le Berre M, Gerlach JQ, Dziembala I, et al. Calculating half maximal inhibitory concentration (IC(50)) values from glycomics microarray data using GraphPad prism. Methods Mol Biol. 2022;2460:89–111.
  • Mitteer DR, Greer BD. Using GraphPad prism’s heat maps for efficient, fine-grained analyses of single-case data. Behav Anal Pract. 2022;15(2):505–514. doi: 10.1007/s40617-021-00664-7.
  • Kucharzik T, Koletzko S, Kannengiesser K, et al. Ulcerative colitis-diagnostic and therapeutic algorithms. Dtsch Arztebl Int. 2020;117(33-34):564–574. doi: 10.3238/arztebl.2020.0564.
  • Du L, Ha C. Epidemiology and pathogenesis of ulcerative colitis. Gastroenterol Clin North Am. 2020;49(4):643–654. doi: 10.1016/j.gtc.2020.07.005.
  • Sandborn WJ, Feagan BG, D’Haens G, et al. Ozanimod as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2021;385(14):1280–1291. doi: 10.1056/NEJMoa2033617.
  • Kobayashi T, Siegmund B, Le Berre C, et al. Ulcerative colitis. Nat Rev Dis Primers. 2020;6(1):74. doi: 10.1038/s41572-020-0205-x.
  • Segal JP, LeBlanc JF, Hart AL. Ulcerative colitis: an update. Clin Med. 2021;21(2):135–139. doi: 10.7861/clinmed.2021-0080.
  • Dignass A, Lindsay JO, Sturm A, et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 2: current management. J Crohns Colitis. 2012;6(10):991–1030. doi: 10.1016/j.crohns.2012.09.002.
  • Mishra RK, Ahmad A, Kumar A, et al. Lipid-based nanocarrier-mediated targeted delivery of celecoxib attenuate severity of ulcerative colitis. Mater Sci Eng C Mater Biol Appl. 2020;116:111103. doi: 10.1016/j.msec.2020.111103.
  • Parikh K, Antanaviciute A, Fawkner-Corbett D, et al. Colonic epithelial cell diversity in health and inflammatory bowel disease. Nature. 2019;567(7746):49–55. doi: 10.1038/s41586-019-0992-y.
  • Chelakkot C, Ghim J, Ryu SH. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med. 2018;50(8):1–9. doi: 10.1038/s12276-018-0126-x.
  • Ozaki H, Ishii K, Horiuchi H, et al. Cutting edge: combined treatment of TNF-alpha and IFN-gamma causes redistribution of junctional adhesion molecule in human endothelial cells. J Immunol. 1999;163(2):553–557.
  • Ye D, Ma I, Ma TY. Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol. 2006;290(3):G496–G504. doi: 10.1152/ajpgi.00318.2005.
  • Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol. 1963;17(2):375–412. doi: 10.1083/jcb.17.2.375.
  • Feldman GJ, Mullin JM, Ryan MP. Occludin: structure, function and regulation. Adv Drug Deliv Rev. 2005;57(6):883–917. doi: 10.1016/j.addr.2005.01.009.
  • Li X, Wang Q, Xu H, et al. Somatostatin regulates tight junction proteins expression in colitis mice. Int J Clin Exp Pathol. 2014;7:2153–2162.
  • Nighot P, Al-Sadi R, Rawat M, et al. Matrix metalloproteinase 9-induced increase in intestinal epithelial tight junction permeability contributes to the severity of experimental DSS colitis. Am J Physiol Gastrointest Liver Physiol. 2015;309(12):G988–G997. doi: 10.1152/ajpgi.00256.2015.
  • Tsukita S, Furuse M. Occludin and claudins in tight-junction strands: leading or supporting players? Trends Cell Biol. 1999;9(7):268–273. doi: 10.1016/s0962-8924(99)01578-0.
  • Zeissig S, Bürgel N, Günzel D, et al. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn’s disease. Gut. 2007;56(1):61–72. doi: 10.1136/gut.2006.094375.
  • D’Incà R, Di Leo V, Corrao G, et al. Intestinal permeability test as a predictor of clinical course in Crohn’s disease. Am J Gastroenterol. 1999;94(10):2956–2960. doi: 10.1111/j.1572-0241.1999.01444.x.
  • Arnott ID, Kingstone K, Ghosh S. Abnormal intestinal permeability predicts relapse in inactive Crohn disease. Scand J Gastroenterol. 2000;35(11):1163–1169. doi: 10.1080/003655200750056637.
  • Chen X, Li J, Kang R, et al. Ferroptosis: machinery and regulation. Autophagy. 2021;17(9):2054–2081. doi: 10.1080/15548627.2020.1810918.
  • Badgley MA, Kremer DM, Maurer HC, et al. Cysteine depletion induces pancreatic tumor ferroptosis in mice. Science. 2020;368(6486):85–89. doi: 10.1126/science.aaw9872.
  • Wang H, An P, Xie E, et al. Characterization of ferroptosis in murine models of hemochromatosis. Hepatology. 2017;66(2):449–465. doi: 10.1002/hep.29117.
  • Wu Z, Geng Y, Lu X, et al. Chaperone-mediated autophagy is involved in the execution of ferroptosis. Proc Natl Acad Sci U S A. 2019;116(8):2996–3005. doi: 10.1073/pnas.1819728116.
  • Dai E, Han L, Liu J, et al. Autophagy-dependent ferroptosis drives tumor-associated macrophage polarization via release and uptake of oncogenic KRAS protein. Autophagy. 2020;16(11):2069–2083. doi: 10.1080/15548627.2020.1714209.
  • Xue Q, Yan D, Chen X, et al. Copper-dependent autophagic degradation of GPX4 drives ferroptosis. Autophagy. 2023;19(7):1982–1996. doi: 10.1080/15548627.2023.2165323.
  • Cui DJ, Chen C, Yuan WQ, et al. Integrative analysis of ferroptosis-related genes in ulcerative colitis. J Int Med Res. 2021;49(9):3000605211042975. doi: 10.1177/03000605211042975.
  • Szeto CC, Sugano K, Wang JG, et al. Non-steroidal anti-inflammatory drug (NSAID) therapy in patients with hypertension, cardiovascular, renal or gastrointestinal comorbidities: joint APAGE/APLAR/APSDE/APSH/APSN/PoA recommendations. Gut. 2020;69(4):617–629. doi: 10.1136/gutjnl-2019-319300.
  • García-Rayado G, Navarro M, Lanas A. NSAID induced gastrointestinal damage and designing GI-sparing NSAIDs. Expert Rev Clin Pharmacol. 2018;11(10):1031–1043. doi: 10.1080/17512433.2018.1516143.
  • Tan T, Fu X, Qu J, et al. 2,5-dimethyl celecoxib induces apoptosis and autophagy via activation of ROS/JNK axis in nasopharyngeal carcinoma cells. Aging. 2021;13(17):21483–21496. doi: 10.18632/aging.203488.
  • Zhu J, May S, Ulrich C, et al. High ROS production by celecoxib and enhanced sensitivity for death Ligand-Induced apoptosis in cutaneous SCC cell lines. Int J Mol Sci. 2021;22(7):22. doi: 10.3390/ijms22073622.
  • Liu M, Li CM, Chen ZF, et al. Celecoxib regulates apoptosis and autophagy via the PI3K/akt signaling pathway in SGC-7901 gastric cancer cells. Int J Mol Med. 2014;33(6):1451–1458. doi: 10.3892/ijmm.2014.1713.
  • Liu DB, Hu GY, Long GX, et al. Celecoxib induces apoptosis and cell-cycle arrest in nasopharyngeal carcinoma cell lines via inhibition of STAT3 phosphorylation. Acta Pharmacol Sin. 2012;33(5):682–690. doi: 10.1038/aps.2012.18.
  • Jia Z, Zhang H, Ma C, et al. Celecoxib enhances apoptosis of the liver cancer cells via regulating ERK/JNK/P38 pathway. J Buon. 2021;26:875–881.
  • Li Y, Cao Y, Xiao J, et al. Inhibitor of apoptosis-stimulating protein of p53 inhibits ferroptosis and alleviates intestinal ischemia/reperfusion-induced acute lung injury. Cell Death Differ. 2020;27(9):2635–2650. doi: 10.1038/s41418-020-0528-x.

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.