Molecular mechanism of indomethacin-induced gastropathy

Free Radical Biology and Medicine

Volumn 52, Issue 7, 2012, Pages 1175-1187

  Yadav, Sudhir K ^a   Adhikary, Biplab ^a   Chand, Saswati ^b   Maity, Biswanath ^a   Bandyopadhyay, Sandip K ^a   Chattopadhyay, Subrata ^b  

^a INSTITUTE OF POST GRADUATE MEDICAL EDUCATION AND RESEARCH   (India)

^b BHABHA ATOMIC RESEARCH CENTRE   (India)

Author keywords

Angiogenesis; Free radicals; Gastric ulcer; Indomethacin; Inflammatory modulators; NSAID

Indexed keywords

BLOOD CLOTTING FACTOR 8 PLUS VON WILLEBRAND FACTOR; CELL ADHESION MOLECULE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ENDOSTATIN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOMETACIN; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE; MYELOPEROXIDASE; PROSTAGLANDIN E; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STOMACH DISEASE; STOMACH INJURY; STOMACH ULCER; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CYCLOOXYGENASE 2; ENZYME-LINKED IMMUNOSORBENT ASSAY; GASTRIC MUCOSA; INDOMETHACIN; MALE; MAP KINASE KINASE 4; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STOMACH ULCER; TUMOR NECROSIS FACTOR-ALPHA;

MUS;

EID: 84857920839     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.12.023     Document Type: Article

References (73)

1. P. Brooks, P. Emery, J.F. Evans, H. Fenner, C.J. Hawkey, C. Patrono, J. Smolen, F. Breedveld, R. Day, M. Dougados, E.W. Ehrich, J. Gijon-Banos, T.K. Kvien, M.H. Van Rijswijk, T. Warner, and H. Zeidler Interpreting the clinical significance of the differential inhibition of COX-1 and COX-2 Rheumatology 38 1999 779 788
2. P.A. Gladding, M.W. Webster, H.B. Farrell, I.S. Zeng, R. Park, and N. Ruijne The antiplatelet effect of six non-steroidal anti-inflammatory drugs and their pharmacodynamic interaction with aspirin in healthy volunteers Am. J. Cardiol. 101 2008 1060 1063
3. G.A. Piazza, A.B. Keeton, H.N. Tinsley, J.D. Whitt, B.D. Gary, B. Mathew, R. Singh, W.E. Grizzle, and R.C. Reynolds NSAIDs: old drugs reveal new anticancer targets Pharmaceuticals 3 2010 1652 1667
4. C. Hawkins, and G.W. Hanks The gastroduodenal toxicity of nonsteroidal anti-inflammatory drugs: a review of the literature J. Pain Symptom Manage. 20 2000 140 151
5. A. Lanas, M.A. Perez-Aisa, F. Feu, and J. Ponce A nationwide study of mortality associated with hospital admission due to severe gastrointestinal events and those associated with non-steroidal anti-inflammatory drug use Am. J. Gastroenterol. 100 2005 1685 1693 (Pubitemid 41648418)
6. J.L. Wallace NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies Br. J. Pharmacol. 165 2012 67 74
7. D. Henry, A. Dobson, and C. Turner Variability in the risk of major gastrointestinal complications from nonaspirin nonsteroidal anti-inflammatory drugs Gastroenterology 105 1993 1078 1088 (Pubitemid 23281496)
8. L.A. Garcia-Rodriguez, and H. Jick Risk of upper gastrointestinal bleeding and perforation with individual non-steroidal anti-inflammatory drugs Lancet 343 1994 769 772 (Pubitemid 24098698)
9. R. Langenbach, S.G. Morham, H.F. Tiano, C.D. Loftin, B.I. Ghanayem, P.C. Chulada, J.F. Mahler, C.A. Lee, E.H. Goulding, K.D. Kluckman, H.S. Kim, and O. Smithies Prostaglandin synthase 1 gene disruption in mice reduces arachidonic acid-induced inflammation and indomethacin-induced gastric ulceration Cell 83 1995 483 492
10. A.F. Barrison, and M.M. Wolfe Management of NSAID-related gastrointestinal mucosal injury Inflammopharmacology 7 1999 277 286 (Pubitemid 30007200)
11. F. Halter, A. Schamassman, B.M. Peskar, and A.S. Tarnawski Cyclooxygenase-2 implications on maintenance of gastric mucosal integrity and ulcer healing: controversies and perspectives Gut 49 2001 443 453 (Pubitemid 32802583)
12. T. Yoshikawa, Y. Naito, A. Kishi, T. Tomii, T. Kaneko, S. Iinuma, H. Ichikawa, M. Yasuda, S. Takahashi, and M. Kondo Role of active oxygen, lipid peroxidation, and antioxidants in the pathogenesis of gastric mucosal injury induced by indomethacin in rats Gut 34 1993 732 737 (Pubitemid 23185094)
13. S. Fiorucci, E. Antonelli, and A. Morelli Mechanism of non-steroidal anti-inflammatory drug-gastropathy Dig. Liver Dis. 31 Suppl. 2 2001 S35 S43
14. J.L. Wallace Recent advances in gastric ulcer therapeutics Curr. Opin. Pharmacol. 5 2005 573 577 (Pubitemid 41614454)
15. H. Utsumi, K. Yasukawa, T. Soeda, K.I. Yamada, R. Shigemi, T. Yao, and M. Tsuneyoshi Noninvasive mapping of reactive oxygen species by in vivo electron spin resonance spectroscopy in indomethacin-induced gastric ulcers in rats J. Pharmacol. Exp. Ther. 317 2006 228 235
16. K. Takeuchi, K. Ueshima, Y. Hironaka, Y. Fujioka, J. Matsumoto, and S. Okabe Oxygen free radicals and lipid peroxidation in the pathogenesis of gastric mucosal lesions induced by indomethacin in rats Digestion 49 1991 175 184
17. L. Osborn Leukocyte adhesion to endothelium in inflammation Cell 62 1990 3 6
18. J. Panés, M. Perry, and D.N. Granger Leukocyte-endothelial cell adhesion: avenues for therapeutic intervention Br. J. Pharmacol. 126 1999 537 550 (Pubitemid 29087827)
19. M. Chatterjee, R. Saluja, S. Kanneganti, S. Chinta, and M. Dikshit Biochemical and molecular evaluation of neutrophil NOS in spontaneously hypertensive rats Cell. Mol. Biol. 53 2007 84 92
20. D. Salvemini, G. de Nucci, R.J. Gryglewski, and J.R. Vane Human neutrophils and mononuclear cells inhibit platelet aggregation by releasing a nitric oxide-like factor Proc. Natl. Acad. Sci. U. S. A. 86 1989 6328 6332 (Pubitemid 19210645)
21. B. Kristal, R. Shurtz-Swirski, J. Chezar, J. Manaster, R. Levy, G. Shapiro, I. Weissman, S.M. Shasha, and S. Sela Participation of peripheral polymorphonuclear leukocytes in the oxidative stress and inflammation in patients with essential hypertension Am. J. Hypertens. 11 1998 921 928 (Pubitemid 28378404)
22. J.L. Wallace, K.E. Arfors, and G.W. McKnight A monoclonal antibody against the CD18 leukocyte adhesion molecule prevents indomethacin-induced gastric damage in the rabbit Gastroenterology 100 1991 878 883
23. J.L. Wallace, W. McKnight, M. Miyasaka, T. Tamatani, J. Paulson, D.C. Anderson, D.N. Granger, and P. Kubes Role of endothelial adhesion molecules in NSAID-induced gastric mucosal injury Am. J. Physiol. Gastrointest. Liver Physiol. 265 1993 G993 G998
24. J.S. Pober, M.P. Bevilacqua, D.L. Mendrick, L.A. Lapierre, W. Fiers, and M.A. Gimbrone Jr. Two distinct monokines, interleukin 1 and tumor necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured human vascular endothelial cells J. Immunol. 136 1986 1680 1687 (Pubitemid 16119575)
25. J. Le, and J. Vilcek Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities Lab. Invest. 56 1987 234 248 (Pubitemid 17065343)
26. C.B. Appleyard, D.M. McCafferty, A.W. Tigley, M.G. Swain, and J.L. Wallace Tumor necrosis factor mediation of NSAID-induced gastric damage: role of leukocyte adherence Am. J. Physiol. 270 1996 G42 G48
27. M.H.L.P. Souza, J.M.S.C. Mota, R.B. Oliveira, and F.Q. Cunha Gastric damage induced by different doses of indomethacin in rats is variably affected by inhibiting iNOS or leukocyte infiltration Inflamm. Res. 57 2008 28 33
28. A. Tarnawski, J. Stachura, T.G. Douglass, W.J. Krause, H. Gergely, and I.J. Sarfeh Indomethacin impairs quality of experimental gastric ulcer healing: a quantitative histological and ultrastructural analysis A. Garner, P.E. O'Brien, Mechanisms of Injury, Protection and Repair of the Upper Gastrointestinal Tract 1991 Wiley Chichester 521 531
29. A.S. Tarnawski Cellular and molecular mechanisms of gastrointestinal ulcer healing Dig. Dis. Sci. 50 Suppl. 1 2005 S24 S33
30. P.P. Tak, and G.S. Firestein NF-κB: a key role in inflammatory diseases J. Clin. Invest. 107 2001 7 11 (Pubitemid 32047405)
31. A.S. Baldwin Jr. The NF-κB and I-κB proteins: new discoveries and insights Annu. Rev. Immunol. 14 1996 649 681 (Pubitemid 126664210)
32. C. Scheidereit IκB kinase complexes: gateways to NF-κB activation and transcription Oncogene 25 2006 6685 6705 (Pubitemid 44657846)
33. A.B. Carter, K.L. Knudtson, M.M. Monick, and G.W. Hunninghake The p38 mitogen-activated protein kinase is required for NF-kappa B-dependent gene expression: the role of TATA-binding protein (TBP) J. Biol. Chem. 274 1999 30858 30863
34. G.L. Johnson, and R. Lapadat Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases Science 298 2002 1911 1912 (Pubitemid 35425238)
35. J. Cuschieri, and R.V. Maier Mitogen-activated protein kinase (MAPK) Crit. Care Med. 33 2005 S417 S419
36. D. Dokmeci, M. Akpolat, N. Aydogu, L. Doganay, and F.N. Turan l-Carnitine inhibits ethanol-induced gastric mucosal injury in rats Pharmacol. Rep. 57 2005 481 488 (Pubitemid 41288689)
37. P.P. Bradley, D.A. Priebat, R.D. Christensen, and G. Rothstein Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker J. Invest. Dermatol. 78 1982 206 209 (Pubitemid 12171880)
38. J. Crespo, A. Cayon, P. Fernandez-Gil, M. Hernandez-Guerra, M. Mayorga, A. Dominguez-Diez, J.C. Fernandez-Escalante, and F. Pons-Romero Gene expression of tumor necrosis factor and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patients Hepatology 34 2001 1158 1163 (Pubitemid 33096588)
39. K. Nishida, Y. Ohta, T. Kobayashi, and I. Ishiguro Involvement of the xanthine-xanthine oxidase system and neutrophils in the development of acute gastric mucosal lesions in rats with water immersion restraint stress Digestion 58 1997 340 351 (Pubitemid 27368074)
40. Z. Morise, S. Komatsu, J.W. Fuseler, D.N. Granger, M. Perry, A.C. Issekutz, and M.B. Grisham ICAM-1 and P-selectin expression in a model of NSAID-induced gastropathy Am. J. Physiol. 274 1998 G246 G252
41. J.L. Wallace, C.M. Keenan, and D.N. Granger Gastric ulceration induced by nonsteroidal anti-inflammatory drugs is a neutrophil-dependent process Am. J. Physiol. 259 1990 G462 G467
42. H. Fujita, S. Takahashi, and S. Okabe Mechanism by which indomethacin delays the healing of acetic acid-induced ulcer in rats: role of neutrophils antichemotactic and chemotactic activities J. Physiol. Pharmacol. 49 1998 71 82 (Pubitemid 28168393)
43. C.F. Bou-Abboud, H. Wayland, G. Panlsen, and P.H. Guth Microcirculatory stasis precedes tissue necrosis in ethanol-induced gastric mucosal injury in rat Dig. Dis. Sci. 33 1988 872 877
44. Y. Tsukimi, C. Nozue, and S. Okabe Effects of teminoprazole, omeprazole and sucralfate on indomethacin-induced delayed healing of kissing gastric ulcers in rats J. Gastroenterol. Hepatol. 11 1996 335 340 (Pubitemid 26142926)
45. T. Arakawa, K. Higuchi, and F. Takashi Prostaglandins in the stomach: an update J. Clin. Gastroenterol. 27 1998 S1 S11
46. C.C. Wu, J.S. Chen, W.M. Wu, T.N. Liao, P. Chu, S.H. Lin, C.H. Chuang, and Y.F. Lin Myeloperoxidase serves as a marker of oxidative stress during single haemodialysis session using two different biocompatible dialysis membranes Nephrol. Dial. Transplant. 20 2005 1134 1139 (Pubitemid 40862102)
47. V. Loria, I. Dato, F. Graziani, and L.M. Biasucci A new biomarker of inflammation in ischemic heart disease and acute coronary syndromes Mediat. Inflamm. 2008 2008 135625
48. J.E. Krawisz, P. Sharon, and W.F. Stenson Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity Gastroenterology 87 1984 1344 1350
49. M.J. Eppihimer, B. Wolitzky, D.C. Anderson, M.A. Labow, and D.N. Granger Heterogeneity of expression of E- and P-selectins in vivo Circ. Res. 79 1996 560 569 (Pubitemid 26276916)
50. B. Glowinska, M. Urban, J. Peczynska, and B. Florys Soluble adhesion molecules (sICAM-1, sVCAM-1) and selectins (sE selectin, sP selectin, sL selectin) levels in children and adolescents with obesity, hypertension, and diabetes Metabolism 54 2005 1020 1026 (Pubitemid 41033102)
51. M.K. Jones, H. Wang, B.M. Peskar, E. Levin, R.M. Itani, I.J. Sarfeh, and A.S. Tarnawski Inhibition of angiogenesis by nonsteroidal anti-inflammatory drugs: insight into mechanisms and implications for cancer growth and ulcer healing Nat. Med. 5 1999 1418 1423
52. L. Santucci, S. Fiorucci, and F.M. Di Matteo Role of tumor necrosis factor-α release and leukocyte margination in indomethacin induced gastric injury in rats Gastroenterology 108 1995 393 401
53. R.A. Stockston, and B.S. Jacobson Modulation of cell-substrate adhesion by arachidonic acid: lipoxygenase regulates cell spreading and ERK1/2-inducible cyclooxygenase regulates cell migration in NIH-3T3 fibroblasts Mol. Biol. Cell 12 2001 1937 1956 (Pubitemid 33049690)
54. W.A. Mersereau, and E.J. Hinchey Prevention of phenylbutazone ulcer in the rat by glucose: role of a glycoprivic receptor system Am. J. Physiol. 242 1982 G429 G432
55. K. Takeuchi, Y. Ishihara, M. Okada, H. Niida, and S. Okabe A continuous monitoring of mucosal integrity and secretory activity in rat stomach: a preparation using a Lucite chamber Jpn. J. Pharmacol. 49 1989 235 244 (Pubitemid 19064603)
56. M. Shibuya, and L. Claesson-Welsh Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis Exp. Cell Res. 312 2006 549 560 (Pubitemid 43290332)
57. N. Rahimi VEGFR-1 and VEGFR-2: two non-identical twins with a unique physiognomy Front. Biosci. 11 2006 818 829 (Pubitemid 43262905)
58. M.S. O'Reilly, T. Boehm, Y. Shing, N. Fukai, G. Vasios, W.S. Lane, E. Flynn, J.R. Birkhead, B.R. Olsen, and J. Folkman Endostatin: an endogenous inhibitor of angiogenesis and tumour growth Cell 88 1997 277 285 (Pubitemid 28015876)
59. E. Dejana, M.G. Lampugnani, M. Giorgi, M. Gaboli, A.B. Federici, Z.M. Ruggeri, and P.C. Marchisio von Willebrand factor promotes endothelial cell adhesion via an Arg-Gly-Asp-dependent mechanism J. Cell Biol. 109 1989 367 375 (Pubitemid 19180143)
60. A.W.Y. Hoa, C.K. Wonga, and C.W.K. Lama Tumor necrosis factor-α up-regulates the expression of CCL2 and adhesion molecules of human proximal tubular epithelial cells through MAPK signaling pathways Immunobiology 213 2008 533 544
61. E. Kopp, and S. Ghosh Inhibition of NF-kappa B by sodium salicylate and aspirin Science 265 1994 956 959
62. H.C. Ledebur, and T.P. Parks Transcriptional regulation of the intercellular adhesion molecule-1 gene by inflammatory cytokines in human endothelial cells: essential roles of a variant NF-κB site and P65 homodimers J. Biol. Chem. 270 1995 933 943
63. M.F. Iademarco, J.J. McQuillan, G.D. Rosen, and D.C. Dean Characterization of the promoter for vascular cell adhesion molecule-1 (VCAM-1) J. Biol. Chem. 267 1992 16323 16329
64. J.M. Kyriakis, and J. Avruch Sounding the alarm: protein kinase cascades activated by stress and inflammation J. Biol. Chem. 271 1996 24313 24316 (Pubitemid 26333156)
65. V. Ramirez-Alcantara, A. LoGuidice, and U.A. Boelsterli Protection from diclofenac-induced small intestinal injury by the JNK inhibitor SP600125 in a mouse model of NSAID-associated enteropathy Am. J. Physiol. Gastrointest. Liver Physiol. 297 2009 G990 G998
66. R. Pai, M. Ohta, R.M. Itani, I.J. Sarfeh, and A.S. Tarnawski Induction of mitogen-activated protein kinase signal transduction pathway during gastric ulcer healing in rats Gastroenterology 114 1998 706 713 (Pubitemid 28160405)
67. J.W. Kim, C.O. Joe, and E.J. Choi Role of receptor-interacting protein in tumor necrosis factor-α-dependent MEKK1 activation J. Biol. Chem. 276 2001 27064 27070
68. 2-terminal kinase regulation but does not cause a measurable defect in NF-κB activation Proc. Natl. Acad. Sci. U. S. A. 97 2000 7272 7277 (Pubitemid 30431453)
69. L.P. Ngoc, D.R. Gold, A.O. Tzianabos, S.T. Weiss, and J.C. Celedon Cytokines, allergy, and asthma Curr. Opin. Allergy Clin. Immunol. 5 2005 161 166 (Pubitemid 40434466)
70. Y. Yamaoka, M. Kita, T. Kodama, N. Sawai, K. Kashima, and J. Imanishi Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains Gut 41 1997 442 451
71. M.H.L.P. Souza, H.P. Lemos, R.B. Oliveira, and F.Q. Cunha Gastric damage and granulocyte infiltration induced by indomethacin in tumour necrosis factor receptor 1 (TNF-R1) or inducible nitric oxide synthase (iNOS) deficient mice Gut 53 2004 791 796 (Pubitemid 38662127)
72. K. Fukumoto, Y. Naito, T. Takagi, S. Yamada, R. Horie, K. Inoue, A. Harusato, I. Hirata, T. Omatsu, K. Mizushima, Y. Hirai, N. Yoshida, K. Uchiyama, T. Ishikawa, O. Handa, H. Konishi, N. Wakabayashi, N. Yagi, S. Kokura, H. Ichikawa, M. Kita, and T. Yoshikawa Role of tumor necrosis factor-α in the pathogenesis of indomethacin-induced small intestinal injury in mice Int. J. Mol. Med. 27 2011 353 359
73. G. Alvan, M. Orme, L. Bertilsson, R. Ekstrand, and L. Palmer Pharmokinetics of indomethacin Clin. Pharmacol. Ther. 18 1975 364 373