Mitigation of indomethacin-induced gastrointestinal damages in fat-1 transgenic mice via gate-keeper action of ω-3-polyunsaturated fatty acids

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Han, Young Min ^a   Park, Jong Min ^a   Kang, Jing X ^b   Cha, Ji Young ^c   Lee, Ho Jae ^c   Jeong, Migeyong ^a   Go, Eun Jin ^a   Hahm, Ki Baik ^a,d  

^a Cancer Prevention Research Center   (South Korea)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Gachon University College of Medicine   (South Korea)

^d CHA University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84989260699     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep33992     Document Type: Article

References (45)

1. Vane, J. R. Purity and stability of synthetic peptides such as angiotensins and kinins. Nature 230, 382 (1971).
2. Wallace, J. L. Nonsteroidal anti-inflammatory drugs and gastroenteropathy: the second hundred years. Gastroenterology 112, 1000-1016 (1997).
3. Manrique-Moreno, M., Garidel, P., Suwalsky, M., Howe, J. & Brandenburg, K. The membrane-activity of Ibuprofen, Diclofenac, and Naproxen: a physico-chemical study with lecithin phospholipids. Biochimica et biophysica acta 1788, 1296-1303, doi: 10.1016/j. bbamem.2009.01.016 (2009).
4. Giraud, M. N., Motta, C., Romero, J. J., Bommelaer, G. & Lichtenberger, L. M. Interaction of indomethacin and naproxen with gastric surface-active phospholipids: a possible mechanism for the gastric toxicity of nonsteroidal anti-inflammatory drugs (NSAIDs). Biochemical pharmacology 57, 247-254 (1999).
5. Lichtenberger, L. M. et al. Non-steroidal anti-inflammatory drugs (NSAIDs) associate with zwitterionic phospholipids: insight into the mechanism and reversal of NSAID-induced gastrointestinal injury. Nature medicine 1, 154-158 (1995).
6. Lichtenberger, L. M., Zhou, Y., Dial, E. J. & Raphael, R. M. NSAID injury to the gastrointestinal tract: evidence that NSAIDs interact with phospholipids to weaken the hydrophobic surface barrier and induce the formation of unstable pores in membranes. The Journal of pharmacy and pharmacology 58, 1421-1428, doi: 10.1211/jpp.58.10.0001 (2006).
7. Williams, J. A. et al. Docosahexaenoic and eicosapentaenoic acids segregate differently between raft and nonraft domains. Biophysical journal 103, 228-237, doi: 10.1016/j.bpj.2012.06.016 (2012).
8. Faust, T., Redfern, J. S., Lee, E. & Feldman, M. Effects of fish oil on gastric mucosal 6-keto-PGF1 alpha synthesis and ethanolinduced injury. The American journal of physiology 257, G9-13 (1989).
9. Leung, F. W. Prostaglandins mediate fish oil protection against ethanol-induced gastric mucosal injury in rats. Digestive diseases and sciences 39, 893 (1994).
10. Faust, T. W. et al. Effects of aspirin on gastric mucosal prostaglandin E2 and F2 alpha content and on gastric mucosal injury in humans receiving fish oil or olive oil. Gastroenterology 98, 586-591 (1990).
11. Bhattacharya, A., Ghosal, S. & Bhattacharya, S. K. Effect of fish oil on offensive and defensive factors in gastric ulceration in rats. Prostaglandins, leukotrienes, and essential fatty acids 74, 109-116, doi: 10.1016/j.plefa.2005.11.001 (2006).
12. Guzel, C., Ulak, G., Sermet, A., Cicek, R. & Ulak, M. Effect of fish oil on indometacin-induced gastric lesions in rats. Arzneimittel-Forschung 45, 1172-1173 (1995).
13. Ulak, G. et al. Protective effect of fish oil against stress-induced gastric injury in rats. Arzneimittel-Forschung 45, 1174-1175 (1995).
14. Kang, J. X., Wang, J., Wu, L. & Kang, Z. B. Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature 427, 504, doi: 10.1038/427504a (2004).
15. Fiorucci, S. & Antonelli, E. NO-NSAIDs: from inflammatory mediators to clinical readouts. Inflammation & allergy drug targets 5, 121-131 (2006).
16. Lichtenberger, L. M., Barron, M. & Marathi, U. Association of phosphatidylcholine and NSAIDs as a novel strategy to reduce gastrointestinal toxicity. Drugs Today (Barc) 45, 877-890, doi: 1396674/dot.2009.45.12.1441075 (2009).
17. Flannigan, K. L. & Wallace, J. L. Hydrogen sulfide-based anti-inflammatory and chemopreventive therapies: an experimental approach. Current pharmaceutical design 21, 3012-3022 (2015).
18. Lichtenberger, L. M. et al. Insight into NSAID-induced membrane alterations, pathogenesis and therapeutics: characterization of interaction of NSAIDs with phosphatidylcholine. Biochimica et biophysica acta 1821, 994-1002, doi: 10.1016/j.bbalip.2012.04.002 (2012).
19. Alsop, R. J. et al. Aspirin inhibits formation of cholesterol rafts in fluid lipid membranes. Biochimica et biophysica acta 1848, 805-812, doi: 10.1016/j.bbamem.2014.11.023 (2015).
20. Boscher, C. & Nabi, I. R. Caveolin-1: role in cell signaling. Advances in experimental medicine and biology 729, 29-50, doi: 10.1007/978-1-4614-1222-9-3 (2012).
21. Oh, D. Y. et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 142, 687-698, doi: 10.1016/j.cell.2010.07.041 (2010).
22. Park, J. M. et al. S-allyl cysteine alleviates nonsteroidal anti-inflammatory drug-induced gastric mucosal damages by increasing cyclooxygenase-2 inhibition, heme oxygenase-1 induction, and histone deacetylation inhibition. Journal of gastroenterology and hepatology 29 Suppl 4, 80-92, doi: 10.1111/jgh.12730 (2014).
23. Chiou, S. K., Hodges, A. & Hoa, N. Suppression of growth arrest and DNA damage-inducible 45alpha expression confers resistance to sulindac and indomethacin-induced gastric mucosal injury. The Journal of pharmacology and experimental therapeutics 334, 693-702, doi: 10.1124/jpet.110.168153 (2010).
24. Kurata, S. et al. Rebamipide protects small intestinal mucosal injuries caused by indomethacin by modulating intestinal microbiota and the gene expression in intestinal mucosa in a rat model. Journal of clinical biochemistry and nutrition 56, 20-27, doi: 10.3164/ jcbn.14-67 (2015).
25. de Groot, D. J. et al. Indomethacin-induced activation of the death receptor-mediated apoptosis pathway circumvents acquired doxorubicin resistance in SCLC cells. British journal of cancer 92, 1459-1466, doi: 10.1038/sj.bjc.6602516 (2005).
26. Fanning, A. S., Jameson, B. J., Jesaitis, L. A. & Anderson, J. M. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. The Journal of biological chemistry 273, 29745-29753 (1998).
27. Han, Y. M. et al. Endogenous conversion of omega-6 to omega-3 polyunsaturated fatty acids in fat-1 mice attenuated intestinal polyposis by either inhibiting COX-2/beta-catenin signaling or activating 15-PGDH/IL-18. International journal of cancer 138, 2247-2256, doi: 10.1002/ijc.29956 (2016).
28. Wallace, J. L. et al. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology 141, 1314-1322, 1322 e1311-1315, doi: 10.1053/j.gastro.2011.06.075 (2011).
29. Robert, A. Cytoprotection by prostaglandins. Gastroenterology 77, 761-767 (1979).
30. Biondo, P. D., Brindley, D. N., Sawyer, M. B. & Field, C. J. The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy. The Journal of nutritional biochemistry 19, 787-796, doi: 10.1016/j.jnutbio.2008.02.003 (2008).
31. Fetterman, J. W., Jr. & Zdanowicz, M. M. Therapeutic potential of n-3 polyunsaturated fatty acids in disease. American journal of health-system pharmacy: AJHP: official journal of the American Society of Health-System Pharmacists 66, 1169-1179, doi: 10.2146/ ajhp080411 (2009).
32. Calder, P. C. Long-chain fatty acids and inflammation. The Proceedings of the Nutrition Society 71, 284-289, doi: 10.1017/ S0029665112000067 (2012).
33. Park, J. M. et al. Omega-3 polyunsaturated fatty acids as an angelus custos to rescue patients from NSAID-induced gastroduodenal damage. Journal of gastroenterology 50, 614-625, doi: 10.1007/s00535-014-1034-z (2015).
34. Wassall, S. R. et al. Order from disorder, corralling cholesterol with chaotic lipids. The role of polyunsaturated lipids in membrane raft formation. Chemistry and physics of lipids 132, 79-88, doi: 10.1016/j.chemphyslip.2004.09.007 (2004).
35. Hou, T. Y., McMurray, D. N. & Chapkin, R. S. Omega-3 fatty acids, lipid rafts, and T cell signaling. European journal of pharmacology, doi: 10.1016/j.ejphar.2015.03.091 (2015).
36. Yaqoob, P. The nutritional significance of lipid rafts. Annual review of nutrition 29, 257-282, doi: 10.1146/annurev-nutr-080508-141205 (2009).
37. Shaikh, S. R., Kinnun, J. J., Leng, X., Williams, J. A. & Wassall, S. R. How polyunsaturated fatty acids modify molecular organization in membranes: insight from NMR studies of model systems. Biochimica et biophysica acta 1848, 211-219, doi: 10.1016/j. bbamem.2014.04.020 (2015).
38. Mollinedo, F. & Gajate, C. Lipid rafts as major platforms for signaling regulation in cancer. Advances in biological regulation 57, 130-146, doi: 10.1016/j.jbior.2014.10.003 (2015).
39. Shaikh, S. R., Wassall, S. R., Brown, D. A. & Kosaraju, R. N-3 Polyunsaturated Fatty Acids, Lipid Microclusters, and Vitamin E. Current topics in membranes 75, 209-231, doi: 10.1016/bs.ctm.2015.03.003 (2015).
40. Shaikh, S. R. Biophysical and biochemical mechanisms by which dietary N-3 polyunsaturated fatty acids from fish oil disrupt membrane lipid rafts. The Journal of nutritional biochemistry 23, 101-105, doi: 10.1016/j.jnutbio.2011.07.001 (2012).
41. George, K. S. & Wu, S. Lipid raft: A floating island of death or survival. Toxicology and applied pharmacology 259, 311-319, doi: 10.1016/j.taap.2012.01.007 (2012).
42. Calder, P. C. Polyunsaturated fatty acids and inflammation. Prostaglandins, leukotrienes, and essential fatty acids 75, 197-202, doi: 10.1016/j.plefa.2006.05.012 (2006).
43. Fredriksson, R., Hoglund, P. J., Gloriam, D. E., Lagerstrom, M. C. & Schioth, H. B. Seven evolutionarily conserved human rhodopsin G protein-coupled receptors lacking close relatives. FEBS letters 554, 381-388 (2003).
44. Barnett, J. V., Segal, D. S. & Kuczenski, R. Repeated amphetamine pretreatment alters the responsiveness of striatal dopaminestimulated adenylate cyclase to amphetamine-induced desensitization. The Journal of pharmacology and experimental therapeutics 242, 40-47 (1987).
45. Patel, H. H. & Insel, P. A. Lipid rafts and caveolae and their role in compartmentation of redox signaling. Antioxidants & redox signaling 11, 1357-1372, doi: 10.1089/ARS.2008.2365 (2009).