Indomethacin-induced small intestinal injury is ameliorated by cilostazol, a specific PDE-3 inhibitor

Scandinavian Journal of Gastroenterology

Volumn 47, Issue 8-9, 2012, Pages 993-1002

  Higashiyama, Masaaki ^a   Hokari, Ryota ^a   Kurihara, Chie ^a   Ueda, Toshihide ^a   Watanabe, Chikako ^a   Tomita, Kengo ^a   Komoto, Shunsuke ^a   Okada, Yoshikiyo ^a   Kawaguchi, Atsushi ^a   Nagao, Shigeaki ^a   Miura, Soichiro ^a  

^a NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

Author keywords

Cilostazol; Nonsteroidal anti inflammatory drugs; Phosphodiesterase inhibitor; Small intestinal lesion

Indexed keywords

CILOSTAZOL; IMMUNOGLOBULIN G ANTIBODY; INDOMETACIN; MYELOPEROXIDASE; PADGEM PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; ERYTHROCYTE; FLOW RATE; HISTOLOGY; INTESTINE INJURY; LEUKOCYTE; LEUKOCYTE MIGRATION; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SHEAR RATE; THROMBOCYTE; THROMBOCYTE FUNCTION;

ANALYSIS OF VARIANCE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BLOOD PLATELETS; CELL COMMUNICATION; CELL MOVEMENT; ILEAL DISEASES; ILEUM; INDOMETHACIN; MALE; MICE; MICE, INBRED C57BL; NEUTROPHILS; PEROXIDASE; PHOSPHODIESTERASE 3 INHIBITORS; STATISTICS, NONPARAMETRIC; TETRAZOLES;

EID: 84865768262     PISSN: 00365521     EISSN: 15027708     Source Type: Journal    
DOI: 10.3109/00365521.2012.690043     Document Type: Article

References (53)

1. Maiden L, Thjodleifsson B, Theodors A, Gonzalez J, Bjarnason I. A quantitative analysis of NSAID-induced small bowel pathology by capsule enteroscopy. Gastroenterology 2005;128: 1172-8.
2. Bjarnason I, Hayllar J, Smethurst P, Price A, Gumpel MJ. Metronidazole reduces intestinal inflammation and blood loss in non-steroidal anti-inflammatory drug induced enter-opathy. Gut 1992;33: 1204-8.
3. Shah K, Price AB, Talbot IC, Bardhan KD, Fenn CG, Bjarnason I. Effect of longterm misoprostol coadministration with non-steroidal anti-inflammatory drugs: a histological study. Gut 1995;37: 195-8.
4. Niwa Y, Nakamura M, Ohmiya N, Maeda O, Ando T, Itoh A, et al. Efficacy of rebamipide for diclofenac-induced small-intestinal mucosal injuries in healthy subjects: a prospective, randomized, double-blinded, placebo-controlled, cross-over study. J Gastroenterol 2008;43: 270-6.
5. Robert A. Cytoprotection by prostaglandins. Gastroentero-logy 1979;77: 761-7.
6. Robert A, Asano T. Resistance of germfree rats to indomethacin-induced intestinal lesions. Prostaglandins 1977;14: 333-41.
7. Konaka A, Kato S, Tanaka A, Kunikata T, Korolkiewicz R, Takeuchi K. Roles of enterobacteria, nitric oxide and neutrophil in pathogenesis of indomethacin-induced small intestinal lesions in rats. Pharmacol Res 1999;40: 517-24.
8. Watanabe T, Higuchi K, Kobata A, Nishio H, Tanigawa T, Shiba M, et al. Non-steroidal anti-inflammatory drug-induced small intestinal damage is Toll-like receptor 4 dependent. Gut 2008;57: 181-7.
9. Miura S, Suematsu M, Tanaka S, Nagata H, Houzawa S, Suzuki M, et al. Microcirculatory disturbance in indomethacin-induced intestinal ulcer. Am J Physiol 1991; 261: G213-19.
10. Morise Z, Komatsu S, Fuseler JW, Granger DN, Perry M, Issekutz AC, et al. ICAM-1 and P-selectin expression in a model of NSAID-induced gastropathy. Am J Physiol 1998; 274: G246-52.
11. Ryningen A, Jensen BO, Holmsen H. Role of autocrine stimulation on the effects of cyclic AMP on protein and lipid phosphorylation in collagen-activated and thrombin-activated platelets. Eur J Biochem 1999;260: 87-96.
12. Moore KL, Patel KD, Bruehl RE, Li F, Johnson DA, Lichenstein HS, et al. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol 1995;128: 661-71.
13. Salter JW, Krieglstein CF, Issekutz AC, Granger DN. Platelets modulate ischemia/reperfusion-induced leukocyte recruitment in the mesenteric circulation. Am J Physiol Gastrointest Liver Physiol 2001;281: G1432-9.
14. Inoue T, Tsuzuki Y, Matsuzaki K, Matsunaga H, Miyazaki J, Hokari R, et al. Blockade of PSGL-1 attenuates CD14+ monocytic cell recruitment in intestinal mucosa and ameliorates ileitis in SAMP1/Yit mice. J Leukoc Biol 2005;77: 287-95.
15. Brindis RG, Kloner RA. Sildenafil in patients with cardiovascular disease. Am J Cardiol 2003;92: 26M-36M.
16. Boswell-Smith V, Cazzola M, Page CP. Are phosphodies-terase 4 inhibitors just more theophylline? J Allergy Clin Immunol 2006;117: 1237-43.
17. Dinter H, Tse J, Halks-Miller M, Asarnow D, Onuffer J, Faulds D, et al. The type IV phosphodiesterase specific inhibitor mesopram inhibits experimental autoimmune encephalomyelitis in rodents. J Neuroimmunol 2000;108: 136-46.
18. Schmidt W, Tinelli M, Secchi A, Gebhard MM, Martin E, Schmidt H. Influence of amrinone on intestinal villus blood flow during endotoxemia. J Crit Care 2000;15: 97-102.
19. Gresele P, Momi S, Falcinelli E. Anti-platelet therapy: Phos-phodiesterase inhibitors. Br J Clin Pharmacol 2011;72: 6334-46.
20. Kariyazono H, Nakamura K, Shinkawa T, Yamaguchi T, Sakata R, Yamada K. Inhibition of platelet aggregation and the release of P-selectin from platelets by cilostazol. Thromb Res 2001;101: 445-53.
21. Ito H, Miyakoda G, Mori T. Cilostazol inhibits platelet-leukocyte interaction by suppression of platelet activation. Platelets 2004;15: 293-301.
22. Iba T, Kidokoro A, Fukunaga M, Takuhiro K, Ouchi M, Ito Y. Comparison of the protective effects of type III phosphodiesterase (PDE3) inhibitor (cilostazol) and acetyl-salicylic acid on intestinal microcirculation after ischemia reperfusion injury in mice. Shock 2006;26: 522-6.
23. Higashiyama M, Hokari R, Matsunaga H, Takebayashi K, Watanabe C, Komoto S, et al. P-selectin-dependent mono-cyte recruitment through platelet interaction in intestinal microvessels of LPS-treated mice. Microcirculation 2008; 15: 441-50.
24. Matsunaga H, Hokari R, Higashiyama M, Kurihara C, Okada Y, Watanabe C, et al. Cilostazol, a specific PDE-3 inhibitor, ameliorates chronic ileitis via suppression of interaction of platelets with monocytes. Am J Physiol Gastrointest Liver Physiol 2009;297: G1077-84.
25. Ohba R, Otaka M, Odashima M, Jin M, Komatsu K, Konishi N, et al. Effect of cilostazol, a selective type-III phosphodiesterase inhibitor, on water-immersion stress-induced gastric mucosal injury in rats. J Gastroenterol 2006;41: 34-40.
26. Odashima M, Otaka M, Ohba R, Jin M, Wada I, Horikawa Y, et al. Attenuation of gastric mucosal inflammation induced by aspirin through inhibition of selective type III phospshodiesterase in rats. Dig Dis Sci 2007;52: 1355-9.
27. Gao L, Wang F, Wang B, Gong B, Zhang J, Zhang X, et al. Cilostazol protects diabetic rats from vascular inflammation via nuclear factor-kappa B-dependent down-regulation of vascular cell adhesion molecule-1 expression. J Pharmacol Exp Ther 2006;318: 53-8.
28. Fujita K, Nozaki Y, Wada K, Yoneda M, Endo H, Takahashi H, et al. Effectiveness of antiplatelet drugs against experimental non-alcoholic fatty liver disease. Gut 2008;57: 1583-91.
29. Wang F, Li M, Cheng L, Zhang T, Hu J, Cao M, et al. Intervention with cilostazol attenuates renal inflammation in streptozotocin-induced diabetic rats. Life Sci 2008;83: 828-35.
30. Huang Y, Cheng Y, Wu J, Li Y, Xu E, Hong Z, et al. Cilostazol as an alternative to aspirin after ischaemic stroke: a randomised, double-blind, pilot study. Lancet Neurol 2008;7: 494-9.
31. Hiatt WR, Money SR, Brass EP. Long-term safety of cilos-tazol in patients with peripheral artery disease: the CASTLE study (Cilostazol: A Study in Long-term Effects). J Vasc Surg 2008;47: 330-6.
32. Shinohara Y, Katayama Y, Uchiyama S, Yamaguchi T, Handa S, Matsuoka K, et al. Cilostazol for prevention of secondary stroke (CSPS 2): an aspirin-controlled, double-blind, randomised non-inferiority trial. Lancet Neurol 2010; 9: 959-68.
33. Kim JS, Lee KS, Kim YI, Tamai Y, Nakahata R, Takami H. A randomized crossover comparative study of aspirin, cilos-tazol and clopidogrel in normal controls: analysis with quantitative bleeding time and platelet aggregation test. J Clin Neurosci 2004;11: 600-2.
34. Comerota AJ. Effect on platelet function of cilostazol, clopidogrel, and aspirin, each alone or in combination. Atheroscler Suppl 2005;6: 13-19.
35. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg 1970;101: 478-83.
36. Wu CC, Lu YZ, Wu LL, Yu LC. Role of myosin light chain kinase in intestinal epithelial barrier defects in a rat model of bowel obstruction. BMC Gastroenterol 2010; 10: 39.
37. Bertrand V, Guimbaud R, Tulliez M, Mauprivez C, Sogni P, Couturier D, et al. Increase in tumor necrosis factor-alpha production linked to the toxicity of indomethacin for the rat small intestine. Br J Pharmacol 1998;124: 1385-94.
38. Ishikawa M, Cooper D, Russell J, Salter JW, Zhang JH, Nanda A, et al. Molecular determinants of the prothrom-bogenic and inflammatory phenotype assumed by the postischemic cerebral microcirculation. Stroke 2003;34: 1777-82.
39. Tailor A, Granger DN. Hypercholesterolemia promotes P-selectin-dependent platelet-endothelial cell adhesion in postcapillary venules. Arterioscler Thromb Vasc Biol 2003; 23: 675-80.
40. Ishikawa M, Kusaka G, Yamaguchi N, Sekizuka E, Nakadate H, Minamitani H, et al. Platelet and leukocyte adhesion in the microvasculature at the cerebral surface immediately after subarachnoid hemorrhage. Neurosurgery 2009;64: 546-53.
41. Semple JW, Freedman J. Platelets and innate immunity. Cell Mol Life Sci 2010;67: 499-511.
42. Omi H, Okayama N, Shimizu M, Fukutomi T, Nakamura A, Imaeda K, et al. Cilostazol inhibits high glucose-mediated endothelial-neutrophil adhesion by decreasing adhesion molecule expression via NO production. Microvasc Res 2004;68: 119-25.
43. Iwama D, Miyamoto K, Miyahara S, Tamura H, Tsujikawa A, Yamashiro K, et al. Neuroprotective effect of cilostazol against retinal ischemic damage via inhibition of leukocyte-endothelial cell interactions. J Thromb Haemost 2007;5: 818-25.
44. McEver RP. Adhesive interactions of leukocytes, platelets, and the vessel wall during hemostasis and inflammation. Thromb Haemost 2001;86: 746-56.
45. Rivera-Nieves J, Burcin TL, Olson TS, Morris MA, McDuffie M, Cominelli F, et al. Critical role of endothelial P-selectin glycoprotein ligand 1 in chronic murine ileitis. J Exp Med 2006;203: 907-17.
46. Tailor A, Cooper D, Granger DN. Platelet-vessel wall interactions in the microcirculation. Microcirculation 2005;12: 275-85.
47. Iwai T, Ichikawa T, Goso Y, Ikezawa T, Saegusa Y, Okayasu I, et al. Effects of indomethacin on the rat small intestinal mucosa: immunohistochemical and biochemical studies using anti-mucin monoclonal antibodies. J Gastroenterol 2009;44: 277-84.
48. Satoh H, Hara T, Murakawa D, Matsuura M, Takata K. Soluble dietary fiber protects against nonsteroidal anti-inflammatory drug-induced damage to the small intestine in cats. Dig Dis Sci 2010;55: 1264-71.
49. Hokari R, Lee H, Crawley SC, Yang SC, Gum JR Jr, Miura S, et al. Vasoactive intestinal peptide upregulates MUC2 intestinal mucin via CREB/ATF1. Am J Physiol Gastrointest Liver Physiol 2005;289: G949-59.
50. Kunikata T, Araki H, Takeeda M, Kato S, Takeuchi K. Prostaglandin E prevents indomethacin-induced gastric and intestinal damage through different EP receptor subtypes. J Physiol Paris 2001;95: 157-63.
51. Takeuchi K, Kita K, Hayashi S, Aihara E. Regulatory mechanism of duodenal bicarbonate secretion: roles of endogenous prostaglandins and nitric oxide. Pharmacol Ther 2011; 130: 59-70.
52. -secretion in isolated mouse duodenum in vitro. Biochem Pharmacol 2007;74: 1507-13.
53. Wilhite DB, Comerota AJ, Schmieder FA, Throm RC, Gaughan JP, Rao AK. Managing PAD with multiple platelet inhibitors: the effect of combination therapy on bleeding time. J Vasc Surg 2003;38: 710-13.