Protection from diclofenac-induced small intestinal injury by the JNK inhibitor SP600125 in a mouse model of NSAID-associated enteropathy

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 5, 2009, Pages

  Ramirez Alcantara, Veronica ^a   LoGuidice, Amanda ^a   Boelsterli, Urs A ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Mitochondria; Small intestinal ulceration; Villi

Indexed keywords

ALKALINE PHOSPHATASE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BIOLOGICAL MARKER; DICLOFENAC; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; NONSTEROID ANTIINFLAMMATORY AGENT; PROTEIN P46; SOLUTOL HS 15; STRESS ACTIVATED PROTEIN KINASE;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; C57BL 6 MOUSE; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG INDUCED DISEASE; DRUG MECHANISM; ENZYME ACTIVITY; ILEUM; IMMUNOBLOTTING; INTESTINE CELL; INTESTINE INJURY; INTESTINE ULCER; INTESTINE VILLUS; JEJUNUM; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SINGLE DRUG DOSE; WESTERN BLOTTING;

ALKALINE PHOSPHATASE; ANIMALS; ANTHRACENES; APOPTOSIS; BLOOD PROTEINS; DICLOFENAC; INTESTINAL DISEASES; INTESTINAL MUCOSA; INTESTINE, SMALL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MICE; MICE, INBRED C57BL; MICROVILLI; MITOCHONDRIA; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-JUN; TRANSCRIPTION FACTOR CHOP; ULCER;

EID: 72249084181     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00219.2009     Document Type: Article

References (47)

1. Allison M, Howatson A, Torrance C, Lee F, Russell R. Gastrointestinal damage associated with the use of nonsteroidal antiinflammtory drugs. N Engl J Med 327: 749-754, 1992.
2. Assi K, Pillai R, Gomez-Munoz A, Owen D, Salh B. The specific JNK inhibitor SP600125 targets tumour necrosis factor-α production and epithelial cell apoptosis in acute murine colitis. Immunology 118: 112-121, 2006.
3. Atchison CR, West AB, Balakumaran A, Hargus SJ, Pohl LR, Daiker DH, Aronson JF, Hoffmann WE, Shipp BK, Moslen MT. Drug enterocyte adducts: possible causal factors for diclofenac enteropathy in rats. Gastroenterology 119: 1537-1547, 2000. (Pubitemid 32198679)
4. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh J, Bhagwat SS, Manning AM, Anderson DW. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 98: 13681-13686, 2001. (Pubitemid 33115958)
5. Bjarnason I, Hayllar J, McPherson AJ, Russell AS. Side effects of nonsteroidal anti-inflammatory drugs on the small and large intestine in humans. Gastroenterology 104: 1832-1847, 1993.
6. Boelsterli UA. Diclofenac-induced liver injury: a paradigm of idiosyncratic drug toxicity. Toxicol Appl Pharmacol 192: 307-322, 2003.
7. Bogoyevich MA, Arthur PG. Inhibitors of c-Jun N-terminal kinases: JuNK no more? Biochim Biophys Acta 1784: 76-93, 2008.
8. Cano-Gauci DF, Lualdi JC, Ouellette AJ, Brady G, Iscove NN, Buick RN. In vitro cDNA amplification from individual intestinal crypts: a novel approach to the study of differential gene expression along the crypt-villus axis. Exp Cell Res 208: 344-349, 1993. (Pubitemid 23299117)
9. Davies NM, Saleh JY, Skjodt NM. Detection and prevention of NSAID-induced enteropathy. J Pharm Pharm Sci 3: 137-155, 2000.
10. Davis R. Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252, 2000.
11. Fan M, Goodwin M, Vu T, Brantley-Finley C, Gaarde WA, Chambers TC. Vinblastine-induced phosphorylation of Bcl-2 and Bcl-X(L) is mediated by JNK and occurs in parallel with inactivation of the Raf-1/MEK/ ERK cascade. J Biol Chem 275: 29980-29985, 2000. (Pubitemid 30751301)
12. Foletta VC, Segal DH, Cohen DR. Transcriptional regulation in the immune system: all roads lead to AP-1. J Leukoc Biol 63: 139-152, 1998.
13. Fortun PJ, Hawkey CJ. Nonsteroidal antiinflammatory drugs and the small intestine. Curr Opin Gastroenterol 21: 169-175, 2005. (Pubitemid 40316198)
14. Geddes K, Philpot DJ. A new role for intestinal alkaline phosphatase in gut barrier maintenance. Gastroenterology 135: 8-12, 2008. (Pubitemid 351899043)
15. Gunawan B, Liu ZX, Han D, Hanawa N, Gaarde WA, Kaplowitz N. c-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity. Gastroenterology 131: 165-178, 2006. (Pubitemid 44015744)
16. Hanawa N, Shinohara M, Saberi B, Gaarde WA, Han D, Kaplowitz N. Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury. J Biol Chem 283: 13565-13577, 2008.
17. 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.
18. Itoh H, Yagi M, Hasebe K, Fushida S, Tani T, Hashimoto T, Shimizu K, Miwa K. Regeneration of small intestinal mucosa after acute ischemia-reperfusion injury. Dig Dis Sci 47: 2704-2710, 2002. (Pubitemid 35471610)
19. Kim BJ, Ryu SW, Song BJ. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 281: 21256-21265, 2006.
20. Koga H, Matsumoto T, Iida M. Epidemiology, diagnosis and treatments of non-steroidal anti-inflammatory drug-induced enteropathy: a review of the literature. Gastroenterol Endosc 50: 189-198, 2008.
21. Lane ME, Kim MJ. Assessment and prevention of gastrointestinal toxicity of non-steroidal anti-inflammatory drugs. J Pharm Pharmacol 58: 1295-1304, 2006. (Pubitemid 44580559)
22. Latchoumycandane C, Goh CW, Ong MMK, Boelsterli UA. Mitochondrial protection by the JNK inhibitor leflunomide rescues mice from acetaminophen-induced liver injury. Hepatology 45: 412-421, 2007. (Pubitemid 46374598)
23. Li J, Holbrook NJ. Elevated gadd153/chop expression and enhanced c-Jun N-terminal protein kinase activation sensitizes aged cells to ER stress. Exp Gerontol 39: 735-744, 2004. (Pubitemid 38586814)
24. Lim MS, Lim PLK, Gupta R, Boelsterli UA. Critical role of free cytosolic calcium, but not uncoupling, in mitochondrial permeability transition and cell death induced by diclofenac oxidative metabolites in immortalized human hepatocytes. Toxicol Appl Pharmacol 217: 322-331, 2006. (Pubitemid 44855823)
25. Maiden L. Capsule endoscopic diagnosis of nonsteroidal antiinflammatory drug-induced enteropathy. J Gastroenterol 44: 64-71, 2009.
26. Marderstein EL, Bucher B, Guo Z, Feng X, Reid K, Geller DA. Protection of rat hepatocytes from apoptosis by inhibition of c-Jun N-terminal kinase. Surgery 134: 280-284, 2003. (Pubitemid 37070350)
27. Mitsuyama K, Tsuruta O, Matsui Y, Harada K, Tomiyasu N, Suzuki A, Takaki K, Masuda J, Handa K, Satoh Y, Bennett BL, Toyonaga A, Sata M. Activation of c-Jun N-terminal (JNK) signalling in experimentally induced gastric lesions in rats. Clin Exp Immunol 143: 24-29, 2005.
28. Nagai H, Noguchi T, Takeda K, Ichijo H. Pathophysiological roles of ASK1-MAP kinase signaling pathways. J Biochem Mol Biol 40: 1-6, 2007. (Pubitemid 46182728)
29. Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol 20: 7311-7318, 2000.
30. Nieminen R, Lahti A, Jalonen U, Kankaanranta H, Moilanen E. JNK inhibitor SP600125 reduces COX-2 expression by attenuating mRNA in activated murine J774 macrophages. Int Immunopharmacol 6: 987-996, 2006.
31. Noguchi T, Takeda K, Matsutsawa A, Saegusa K, Nakano H, Gohda J, Inoue J, Ichijo H. Recruitment of tumor necrosis factor receptor-associated factor family proteins to apoptosis signal-regulating kinase 1 signalosome is essential for oxidative stress-induced cell death. J Biol Chem 280: 37033-37040, 2005. (Pubitemid 41587787)
32. Omatsu T, Naito Y, Handa O, Hayashi N, Mitsushima K, Qin Y, Hirata I, Adachi S, Okayama T, Kishimoto E, Takagi T, Kokura S, Hchikawa H, Yoshikawa T. Involvement of reactive oxygen species in indomethacin-induced apoptosis of small intestinal epithelial cells. J Gastroenterol 44, Suppl XIX: 30-34, 2009.
33. Papadakis ES, Finegan KG, Wang X, Robinson AC, Guo C, Kayahara M, Tournier C. The regulation of Bax by c-Jun N-terminal protein kinase (JNK) is a prerequisite to the mitochondrial-induced apoptotic pathway. FEBS Lett 580: 1320-1326, 2006. (Pubitemid 43221994)
34. Ramirez-Alcantara V, Castaneda-Hernandez G, Rampy BA, Aronson JF, Treinen-Moslen M. Attenuated gastropathy but not enteropathy of diclofenac-cholestyramine complex in rats. Drug Dev Res 64: 19-27, 2005. (Pubitemid 40605000)
35. Schroeter H, Boyd CS, Ahmed r Spencer JPE, Duncan RF, Rice- Evans C, Cadenas E. c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis. Biochem J 372: 359-369, 2003.
36. Seitz S, Boelsterli UA. Diclofenac acyl glucuronide, a major biliary metabolite, is directly involved in small intestinal injury in rats. Gastroenterology 115: 1476-1482, 1998. (Pubitemid 28545998)
37. Shen HM, Liu ZG. JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radic Biol Med 40: 928-939, 2006.
38. Sigthorsson G, Simpson RJ, Walley M, Anthony A, Foster R, Hotz- Behoftsitz C, Palizban A, Pombo J, Watts J, Morham SG, Bjarnason I. COX-1 and 2, intestinal integrity, and pathogenesis of nonsteroidal anti-inflammatory drug enteropathy in mice. Gastroenterology 122: 1913-1923, 2002.
39. Somasundaram S, Rafi S, Hayllar J, Sigthorsson G, Jacob M, Price AB, Macpherson A, Mahmod T, Scott D, Wrigglesworth JM, Bjarnason I. Mitochondrial damage: a possible mechanism of the "topical" phase of NSAID induced injury to the rat intestine. Gut 41: 344-353, 1997.
40. 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 phosphorylation and inhibition of cyclooxygenase are required for the development of NSAID-enteropathy in the rat. Aliment Pharmacol Ther 14: 639-650, 2000. (Pubitemid 30240758)
41. Tanaka A, Hase S, Miyazawa T, Takeuchi K. Up-regulation of cyclooxygenase- 2 by inhibition of cyclooxygenase-1: a key to nonsteroidal anti-inflammatory drug-induced intestinal damage. J Pharmacol Exp Ther 300: 754-761, 2002. (Pubitemid 34164976)
42. Treinen-Moslen M, Kanz MF. Intestinal tract injury by drugs: importance of metabolite delivery by yellow bile road. Pharmacol Ther 112: 649-667, 2006. (Pubitemid 44596214)
43. Tsutsumi S, Gotoh T, Tomisato W, Mima S, Hoshino T, Hwang HJ, Takenaka H, Tsuchiya T, Mori M, Mizushima T. Endoplasmic reticulum stress response is involved in nonsteroidal anti-inflammatory drug-induced apoptosis. Cell Death Differ 11: 1009-1016, 2004. (Pubitemid 39232360)
44. Ware JA, Graf MLM, Martin BM, Lustberg LR, Pohl LR. Immunochemical detection and identification of protein adducts of diclofenac in the small intestine of rats: possible role in allergic reactions. Chem Res Toxicol 11: 164-171, 1998.
45. Watanabe T, Higuchi K, Kobata A, Nishio H, Tanigawa T, Shiba M, Tominaga K, Fujiwara J, Oshitani N, Asahara T, Nomoto K, Takeuchi K, Arakawa T. Non-steroidal anti-inflammatory drug-induced small intestinal damage is Toll-like receptor 4 dependent. Gut 57: 181-187, 2008. (Pubitemid 351158044)
46. Wolfe MM, Lichtenstein DR, Singh G. Gastrointestinal toxicity of nonsteroidal antiinflammatory drugs. N Engl J Med 340: 1888-1899, 1999.
47. Zou W, Yue P, Khuri FR, Sun SY. Coupling of endoplasmic reticulum stress to CDDO-Me-induced up-regulation of death receptor 5 via a CHOP-dependent mechanism involving JNK activation. Cancer Res 68: 7484-7492, 2008.