Acetyl salicylic acid induces damage to intestinal epithelial cells by oxidation-related modifications of ZO-1

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 303, Issue 8, 2012, Pages

  Fukui, Akifumi ^a   Naito, Yuji ^a   Handa, Osamu ^a   Kugai, Munehiro ^a   Tsuji, Toshifumi ^a   Yoriki, Hiroyuki ^a   Qin, Ying ^a   Adachi, Satoko ^a   Higashimura, Yasuki ^a   Mizushima, Katsura ^a   Kamada, Kazuhiro ^a   Katada, Kazuhiro ^a   Uchiyama, Kazuhiko ^a   Ishikawa, Takeshi ^a   Takagi, Tomohisa ^a   Yagi, Nobuaki ^a   Kokura, Satoshi ^a   Yoshikawa, Toshikazu ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Paracellular; Sulfenic acid; Tight junction; Zonula occludens 1

Indexed keywords

ACETYLSALICYLIC ACID; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; PROTEIN ZO1; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL DAMAGE; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CONTROLLED STUDY; ELECTRIC RESISTANCE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; INTESTINE EPITHELIUM; INTESTINE INJURY; OXIDATION; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION;

ASPIRIN; CELL LINE, TUMOR; HUMANS; INTESTINAL MUCOSA; INTESTINE, SMALL; OXIDATIVE STRESS; PERMEABILITY; REACTIVE OXYGEN SPECIES; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84867593217     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00236.2012     Document Type: Article

References (40)

1. Al-Sadi R, Khatib K, Guo S, Ye D, Youssef M, Ma T. Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 300: G1054-G1064, 2011.
2. Anderson JM, Van Itallie CM. Physiology and function of the tight junction (Abstract). Cold Spring Harb Perspect Biol 1: a002584, 2009.
3. Antithrombotic Trialists' Collaboration. Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocar-dial infarction, and stroke in high risk patients. Br Med J 324: 71-86, 2002.
4. Basivireddy J, Vasudevan A, Jacob M, Balasubramanian KA. Indo-methacin-induced mitochondrial dysfunction and oxidative stress in villus enterocytes. Biochem Pharmacol 64: 339-349, 2002.
5. Biteau B, Labarre J, Toledano MB. ATP-dependent reduction of cys-teine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425: 980-984, 2003.
6. Bjarnason I, Hayllar J, MacPherson AJ, Russell AS. Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology 104: 1832-1847, 1993.
7. Bjarnason I, Williams P, So A, Zanelli GD, Levi AJ, Gumpel JM, Peters TJ, Ansell B. Intestinal permeability and inflammation in rheumatoid arthritis: effects of non-steroidal anti-inflammatory drugs. Lancet 2: 1171-1174, 1984.
8. Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J. Restoration of barrier function in injured intestinal mucosa. Physiol Rev 87: 545-564, 2007.
9. Blikslager AT, Roberts MC, Rhoads JM, Argenzio RA. Prostaglandins I2 and E2 have a synergistic role in rescuing epithelial barrier function in porcine ileum. J Clin Invest 100: 1928-1933, 1997.
10. Cardey B, Enescu M. Cysteine oxidation by the superoxide radical: a theoretical study. Chemphyschem 10: 1642-1648, 2009.
11. Claiborne A, Miller H, Parsonage D, Ross RP. Protein-sulfenic acid stabilization and function in enzyme catalysis and gene regulation. FASEB J 7: 1483-1490, 1993.
12. Dorkoosh FA, Setyaningsih D, Borchard G, Rafiee-Tehrani M, Ver-hoef JC, Junginger HE. Effects of superporous hydrogels on paracellular drug permeability and cytotoxicity studies in Caco-2 cell monolayers. Int J Pharm 241: 35-45, 2002.
13. Fiorucci S, de Lima OM Jr, Mencarelli A, Palazzetti B, Distrutti E, McKnight W, Dicay M, Ma L, Romano M, Morelli A, Wallace JL. Cyclooxygenase-2-derived lipoxin A4 increases gastric resistance to aspirin-induced damage. Gastroenterology 123: 1598-1606, 2002.
14. Fogh J, Wright WC, Loveless JD. Absence of HeLa cell contamination in 169 cell lines derived from human tumors. J Natl Cancer Inst 58: 209-214, 1977.
15. Guan Y, Watson AJ, Marchiando AM, Bradford E, Shen L, Turner JR, Montrose MH. Redistribution of the tight junction protein ZO-1 during physiological shedding of mouse intestinal epithelial cells. Am J Physiol Cell Physiol 300: C1404-C1414, 2011.
16. Higuchi K, Umegaki E, Watanabe T, Yoda Y, Morita E, Murano M, Tokioka S, Arakawa T. Present status and strategy of NSAIDs-induced small bowel injury. J Gastroenterol 44: 879-888, 2009.
17. Jahn KA, Biazik JM, Braet F. GM1 expression in caco-2 cells: characterisation of a fundamental passage-dependent transformation of a cell line. J Pharm Sci 100: 3751-3762, 2011.
18. Klann E. Cell-permeable scavengers of superoxide prevent long-term potentiation in hippocampal area CA1. J Neurophysiol 80: 452-457, 1998.
19. Maiden L, Thjodleifsson B, Seigal A, Bjarnason II, Scott D, Birgisson S, Bjarnason I. Long-term effects of nonsteroidal anti-inflammatory drugs and cyclooxygenase-2 selective agents on the small bowel: a cross-sectional capsule enteroscopy study. Clin Gastroenterol Hepatol 5: 1040-1045, 2007.
20. Marchiando AM, Shen L, Graham WV, Edelblum KL, Duckworth CA, Guan Y, Montrose MH, Turner JR, Watson AJ. The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding. Gastroenterology 140: 1208-1218, 2011.
21. Matsumoto T, Kudo T, Esaki M, Yano T, Yamamoto H, Sakamoto C, Goto H, Nakase H, Tanaka S, Matsui T, Sugano K, Iida M. Prevalence of non-steroidal anti-inflammatory drug-induced enteropathy determined by double-balloon endoscopy: a Japanese multicenter study. Scand J Gastroenterol 43: 490-496, 2008.
22. Meunier V, Bourrie M, Berger Y, Fabre G. The human intestinal epithelial cell line Caco-2; pharmacological and pharmacokinetic applications. Cell Biol Toxicol 11: 187-194, 1995.
23. Moriscot C, Candel S, Sauret V, Kerr-Conte J, Richard MJ, Favrot MC, Benhamou PY. MnTMPyP, a metalloporphyrin-based superoxide dismutase/catalase mimetic, protects INS-1 cells and human pancreatic islets from an in vitro oxidative challenge. Diabetes Metab 33: 44-53, 2007.
24. Nagano Y, Matsui H, Muramatsu M, Shimokawa O, Shibahara T, Yanaka A, Nakahara A, Matsuzaki Y, Tanaka N, Nakamura Y. Rebamipide significantly inhibits indomethacin-induced mitochondrial damage, lipid peroxidation, and apoptosis in gastric epithelial RGM-1 cells. Dig Dis Sci 50, Suppl 1: S76-S83, 2005.
25. Naito Y, Kajikawa H, Mizushima K, Shimozawa M, Kuroda M, Katada K, Takagi T, Handa O, Kokura S, Ichikawa H, Yoshida N, Matsui H, Yoshikawa T. Rebamipide, a gastro-protective drug, inhibits indomethacin-induced apoptosis in cultured rat gastric mucosal cells: association with the inhibition of growth arrest and DNA damage-induced 45 alpha expression. Dig Dis Sci 50, Suppl 1: S104-S112, 2005.
26. Omatsu T, Naito Y, Handa O, Hayashi N, Mizushima K, Qin Y, Hirata I, Adachi S, Okayama T, Kishimoto E, Takagi T, Kokura S, Ichikawa H, Yoshikawa T. Involvement of reactive oxygen species in indomethacin-induced apoptosis of small intestinal epithelial cells. J Gastroenterol 44, Suppl 19: 30-34, 2009.
27. Pulimeno P, Paschoud S, Citi S. A role for ZO-1 and PLEKHA7 in recruiting paracingulin to tight and adherens junctions of epithelial cells. J Biol Chem 286: 16743-16750, 2011.
28. Qin Y, Naito Y, Handa O, Hayashi N, Kuki A, Mizushima K, Omatsu T, Tanimura Y, Morita M, Adachi S, Fukui A, Hirata I, Kishimoto E, Nishikawa T, Uchiyama K, Ishikawa T, Takagi T, Yagi N, Kokura S, Yoshikawa T. Heat shock protein 70-dependent protective effect of polaprezinc on acetylsalicylic acid-induced apoptosis of rat intestinal epithelial cells. J Clin Biochem Nutr 49: 174-181, 2011.
29. Rao R, Baker RD, Baker SS. Inhibition of oxidant-induced barrier disruption and protein tyrosine phosphorylation in Caco-2 cell monolayers by epidermal growth factor. Biochem Pharmacol 57: 685-695, 1999.
30. Rao RK, Baker RD, Baker SS, Gupta A, Holycross M. Oxidant-induced disruption of intestinal epithelial barrier function: role of protein tyrosine phosphorylation. Am J Physiol Gastrointest Liver Physiol 273: G812-G823, 1997.
31. Rao RK, Basuroy S, Rao VU, Karnaky KJ Jr, Gupta A. Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J 368: 471-481, 2002.
32. Ricchi P, Pignata S, Di Popolo A, Memoli A, Apicella A, Zarrilli R, Acquaviva AM. Effect of aspirin on cell proliferation and differentiation of colon adenocarcinoma Caco-2 cells. Int J Cancer 73: 880-884, 1997.
33. Rousset M. The human colon carcinoma cell lines HT-29 and Caco-2: two in vitro models for the study of intestinal differentiation. Biochimie 68: 1035-1040, 1986.
34. Smecuol E, Pinto Sanchez MI, Suarez A, Argonz JE, Sugai E, Vazquez H, Litwin N, Piazuelo E, Meddings JB, Bai JC, Lanas A. Low-dose aspirin affects the small bowel mucosa: results of a pilot study with a multidimensional assessment. Clin Gastroenterol Hepatol 7: 524-529, 2009.
35. Somasundaram S, Sigthorsson G, Simpson RJ, Watts J, Jacob M, Tavares IA, Rafi S, Roseth A, Foster R, Price AB, Wrigglesworth JM, Bjarnason I. Uncoupling of intestinal mitochondrial oxidative phosphor-ylation and inhibition of cyclooxygenase are required for the development of NSAID-enteropathy in the rat. Aliment Pharmacol Ther 14: 639-650, 2000.
36. Takeuchi K, Miyazawa T, Tanaka A, Kato S, Kunikata T. Pathogenic importance of intestinal hypermotility in NSAID-induced small intestinal damage in rats. Digestion 66: 30-41, 2002.
37. Tomisato W, Tsutsumi S, Rokutan K, Tsuchiya T, Mizushima T. NSAIDs induce both necrosis and apoptosis in guinea pig gastric mucosal cells in primary culture. Am J Physiol Gastrointest Liver Physiol 281: G1092-G1100, 2001.
38. Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol 231: 232-235, 1971.
39. Wang F, Graham WV, Wang Y, Witkowski ED, Schwarz BT, Turner JR. Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am J Pathol 166: 409-419, 2005.
40. Wittchen ES, Haskins J, Stevenson BR. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J Biol Chem 274: 35179-35185, 1999.