Indomethacin suppresses LAMP-2 expression and induces lipophagy and lipoapoptosis in rat enterocytes via the ER stress pathway

Journal of Gastroenterology

Volumn 50, Issue 5, 2015, Pages 541-554

  Narabayashi, Ken ^a   Ito, Yuko ^a   Eid, Nabil ^a   Maemura, Kentaro ^a   Inoue, Takuya ^a   Takeuchi, Toshihisa ^a   Otsuki, Yoshinori ^a   Higuchi, Kazuhide ^a  

^a OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

4 Phenylbutyrate; Endoplasmic reticulum stress; Enterocytes; Indomethacin; LAMP 2; LC3 puncta; Lipid droplet; Lipoapoptosis; Lipophagy

Indexed keywords

3 METHYLADENINE; CASPASE 3; CATHEPSIN; FAT DROPLET; INDOMETACIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; NONSTEROID ANTIINFLAMMATORY AGENT;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CELL CULTURE; CELL DEATH; CELL NUCLEUS MEMBRANE; CELL VACUOLE; CELL VIABILITY; CHROMATIN CONDENSATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTESTINE CELL; LIPOAPOPTOSIS; LIPOPHAGOCYTOSIS; LONG TERM EXPOSURE; MALE; MICROSCOPY; MTT ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TUNEL ASSAY; WESTERN BLOTTING; ANIMAL; ANIMAL MODEL; DRUG EFFECTS; ERYTHROCYTE; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; AUTOPHAGY; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; ERYTHROCYTES; GENE EXPRESSION REGULATION; IN VITRO TECHNIQUES; INDOMETHACIN; LIPID METABOLISM; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MALE; MODELS, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84928984957     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-014-0995-2     Document Type: Article

References (68)

1. Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008;9:1004–10.
2. Singh R, Kaushik S, Wang Y, et al. Autophagy regulates lipid metabolism. Nature. 2009;458:1131–5.
3. Ding WX, Li M, Chen X, et al. Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice. Gastroenterology. 2010;139:1740–52.
4. Huang S, Sinicrope FA. Celecoxib-induced apoptosis is enhanced by ABT-737 and by inhibition of autophagy in human colorectal cancer cells. Autophagy. 2010;6:256–69.
5. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280–93.
6. Igusa Y, Yamashina S, Izumi K, et al. Loss of autophagy promotes murine acetaminophen hepatotoxicity. J Gastroenterol. 2012;47:433–43.
7. Eid N, Ito Y, Otsuki Y. The autophagic response to alcohol toxicity: the missing layer. J Hepatol. 2013;59:398.
8. Eid N, Ito Y, Maemura K, et al. Elevated autophagic sequestration of mitochondria and lipid droplets in steatotic hepatocytes of chronic ethanol-treated rats: an immunohistochemical and electron microscopic study. J Mol Histol. 2013;44:311–26.
9. Cazanave SC, Elmi NA, Akazawa Y, et al. CHOP and AP-1 cooperatively mediate PUMA expression during lipoapoptosis. Am J Physiol Gastrointest Liver Physiol. 2010;299:G236–43.
10. Pohle T, Brändlein S, Ruoff N. Lipoptosis: tumor-specific cell death by antibody-induced intracellular lipid accumulation. Cancer Res. 2004;64:3900–6.
11. Garris DR. Diabetes (db/db) mutation-induced endometrial epithelial lipoapoptosis: ultrastructural and cytochemical analysis of reproductive tract atrophy. Reprod Biol Endocrinol. 2005;3:15.
12. Gniuli D, Dalla Libera L, Caristo ME, et al. High saturated-fat diet induces apoptosis in rat enterocytes and blunts GIP and insulin-secretive response to oral glucose load. Int J Obes (Lond). 2008;32:871–4.
13. Koga H, Kaushik S, Cuervo AM, et al. Inhibitory effect of intracellular lipid load on macroautophagy. Autophagy. 2010;6:825–7.
14. Liu K, Czaja MJ. Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ. 2013;20:3–11.
15. Mei S, Ni HM, Manley S, et al. Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. J Pharmacol Exp Ther. 2011;339:487–98.
16. González-Polo RA, Boya P, Pauleau AL, et al. The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J Cell Sci. 2005;118:3091–102.
17. Saftig P, Beertsen W, Eskelinen EL. LAMP-2: a control step for phagosome and autophagosome maturation. Autophagy. 2008;4:510–2.
18. Fortunato F, Bürgers H, Bergmann F, et al. Impaired autolysosome formation correlates with Lamp-2 depletion: role of apoptosis, autophagy, and necrosis in pancreatitis. Gastroenterology. 2009;137:350–60.
19. Otsuki Y, Misaki O, Sugimoto O, et al. Cyclic bcl-2 gene expression in human uterine endometrium during menstrual cycle. Lancet. 1994;344:28–9.
20. Otsuki Y. Tissue specificity of apoptotic signal transduction. Med Electron Microsc. 2004;37(3):163–9.
21. Guimarães EL, Franceschi MF, Andrade CM, et al. Hepatic stellate cell line modulates lipogenic transcription factors. Liver Int. 2007;27:1255–64.
22. Styner M, Sen B, Xie Z, et al. Indomethacin promotes adipogenesis of mesenchymal stem cells through a cyclooxygenase independent mechanism. J Cell Biochem. 2010;111:1042–50.
23. Basivireddy J, Jacob M, Ramamoorthy P, et al. Indomethacin-induced free radical-mediated changes in the intestinal brush border membranes. Biochem Pharmacol. 2003;65:683–95.
24. Levine L. Does the release of arachidonic acid from cells play a role in cancer chemoprevention? FASEB J. 2003;17:800–2.
25. Levine L. Cyclooxygenase expression is not required for release of arachidonic acid from cells by some nonsteroidal anti-inflammatory drugs and cancer preventive agents. BMC Pharmacol. 2006;6:7.
26. Tanaka A, Hase S, Miyazawa T, et al. Role of cyclooxygenase (COX)-1 and COX-2 inhibition in nonsteroidal anti-inflammatory drug-induced intestinal damage in rats: relation to various pathogenic events. J Pharmacol Exp Ther. 2002;303:1248–54.
27. Omatsu T, Naito Y, Handa O, et al. Reactive oxygen species-quenching and anti-apoptotic effect of polaprezinc on indomethacin-induced small intestinal epithelial cell injury. J Gastroenterol. 2010;45:692–702.
28. Fukumoto K, Naito Y, Takagi T, et al. Role of tumor necrosis factor-α in the pathogenesis of indomethacin-induced small intestinal injury in mice. Int J Mol Med. 2011;27:353–9.
29. Fujimori S, Takahashi Y, Gudis K, et al. Rebamipide has the potential to reduce the intensity of NSAID-induced small intestinal injury: a double-blind, randomized, controlled trial evaluated by capsule endoscopy. J Gastroenterol. 2011;46:57–64.
30. Higuchi K, Umegaki E, Watanabe T, et al. Present status and strategy of NSAIDs-induced small bowel injury. J Gastroenterol. 2009;44:879–88.
31. Ito Y, Shibata MA, Eid N, et al. Lymphangiogenesis and axillary lymph node metastases correlated with VEGF-C expression in two immunocompetent mouse mammary carcinoma models. Int J Breast Cancer. 2011. doi:10.4061/2011/867152.
32. Kanthasamy A, Anantharam V, Ali SF, et al. Methamphetamine induces autophagy and apoptosis in a mesencephalic dopaminergic neuronal culture model: role of cathepsin-D in methamphetamine-induced apoptotic cell death. Ann N Y Acad Sci. 2006;1074:234–44.
33. Eid N, Ito Y, Otsuki Y. Enhanced mitophagy in Sertoli cells of ethanol-treated rats: morphological evidence and clinical relevance. J Mol Histol. 2012;43:71–80.
34. Laha D, Pramanik A, Maity J, et al. Interplay between autophagy and apoptosis mediated by copper oxide nanoparticles in human breast cancer cells MCF7. Biochim Biophys Acta. 2014;1840:1–9.
35. Lin CW, Zhang H, Li M, Xiong X, et al. Pharmacological promotion of autophagy alleviates steatosis and injury in alcoholic and non-alcoholic fatty liver conditions in mice. J Hepatol. 2013;58:993–9.
36. Høyer-Hansen M, Jäättelä M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 2007;14:1576–82.
37. Chiribau CB, Gaccioli F, Huang CC, et al. Molecular symbiosis of CHOP and C/EBPβ isoform LIP contributes to endoplasmic reticulum stress-induced apoptosis. Mol Cell Biol. 2010;30:3722–31.
38. Benbrook DM, Long A. Integration of autophagy, proteasomal degradation, unfolded protein response and apoptosis. Exp Oncol. 2012;34:286–9.
39. Yin JJ, Li YB, Wang Y, et al. The role of autophagy in endoplasmic reticulum stress-induced pancreatic β cell death. Autophagy. 2012;8:158–64.
40. Deegan S, Saveljeva S, Gorman AM, et al. Stress-induced self-cannibalism: on the regulation of autophagy by endoplasmic reticulum stress. Cell Mol Life Sci. 2013;70:2425–41.
41. Kim DS, Li B, Oh HW, et al. The regulatory mechanism of 4-phenylbutyric acid against ER stress-induced autophagy in human gingival fibroblasts. Arch Pharm Res. 2012;35:1269–78.
42. Lin CJ, Lee CC, Shih YL, et al. Inhibition of mitochondria- and endoplasmic reticulum stress-mediated autophagy augments temozolomide-induced apoptosis in glioma cells. PLoS One. 2012;7:e38706.
43. Czaja MJ. Autophagy in health and disease. 2. Regulation of lipid metabolism and storage by autophagy: pathophysiological implications. Am J Physiol Cell Physiol. 2010;298:C973–8.
44. Rodriguez-Navarro JA, Cuervo AM. Autophagy and lipids: tightening the knot. Semin Immunopathol. 2010;32:343–53.
45. Kaminskyy V, Zhivotovsky B. Proteases in autophagy. Biochim Biophys Acta. 1824;2012:44–50.
46. Kanamori H, Takemura G, Maruyama R, et al. Functional significance and morphological characterization of starvation-induced autophagy in the adult heart. Am J Pathol. 2009;174:1705–14.
47. Inami Y, Yamashina S, Izumi K, et al. Hepatic steatosis inhibits autophagic proteolysis via impairment of autophagosomal acidification and cathepsin expression. Biochem Biophys Res Commun. 2011;412:618–25.
48. Tatti M, Motta M, Di Bartolomeo S, et al. Reduced cathepsins B and D cause impaired autophagic degradation that can be almost completely restored by overexpression of these two proteases in Sap C-deficient fibroblasts. Hum Mol Genet. 2012;21:5159–73.
49. Basseri S, Austin RC. Endoplasmic reticulum stress and lipid metabolism: mechanisms and therapeutic potential. Biochem Res Int. 2012;2012:841362.
50. Dhaunsi GS, Aulakh BS, Gupta NM, et al. Towards the mechanism of protection against indomethacin induced gastro-intestinal ulceration by naloxone. Biochem Int. 1988;16:511–9.
51. Navarová J, Nosálová V. Effect of H2-receptor antagonists on indomethacin-induced lysosomal enzyme release from rat gastric mucosa. Methods Find Exp Clin Pharmacol. 1994;16:119–24.
52. Rodriguez-Navarro JA, Kaushik S, Koga H, et al. Inhibitory effect of dietary lipids on chaperone mediated autophagy. Proc Natl Acad Sci U S A. 2012;109:E705–14.
53. Quan W, Lim YM, Lee MS. Role of autophagy in diabetes and endoplasmic reticulum stress of pancreatic β-cells. Exp Mol Med. 2012;44:81–8.
54. Ibrahim SH, Kohli R, Gores GJ. Mechanisms of lipotoxicity in NAFLD and clinical implications. J Pediatr Gastroenterol Nutr. 2011;53:131–40.
55. Tsutsumi S, Gotoh T, Tomisato W, et al. Endoplasmic reticulum stress response is involved in nonsteroidal anti-inflammatory drug-induced apoptosis. Cell Death Differ. 2004;11:1009–16.
56. Zhang YJ, Bao YJ, Dai Q, et al. mTOR signaling is involved in indomethacin and nimesulide suppression of colorectal cancer cell growth via a COX-2 independent pathway. Ann Surg Oncol. 2011;18:580–8.
57. Din FV, Valanciute A, Houde VP, et al. Aspirin inhibits mTOR signaling, activates AMP-activated protein kinase, and induces autophagy in colorectal cancer cells. Gastroenterology. 2012;142:1504–15.
58. Drover VA, Ajmal M, Nassir F, et al. CD36 deficiency impairs intestinal lipid secretion and clearance of chylomicrons from the blood. J Clin Investig. 2005;115:1290–7.
59. Orido T, Fujino H, Kawashima T, et al. Decrease in uptake of arachidonic acid by indomethacin in LS174T human colon cancer cells; a novel cyclooxygenase-2-inhibition-independent effect. Arch Biochem Biophys. 2010;494:78–85.
60. Conway KL, Kuballa P, Song JH, et al. Atg16l1 is required for autophagy in intestinal epithelial cells and protection of mice from salmonella infection. Gastroenterology. 2013;145:1347–57.
61. Tanigawa T, Watanabe T, Nadatani Y, et al. Autophagy promotes gastric ulcer healing. Gastroenterology. 2010;138:S-723.
62. Huang KH, Kuo KL, Ho IL, et al. Celecoxib-induced cytotoxic effect is potentiated by inhibition of autophagy in human urothelial carcinoma cells. PLoS One. 2013;8:e82034.
63. Unuma K, Aki T, Funakoshi T, et al. Cobalt protoporphyrin accelerates TFEB activation and lysosome reformation during LPS-induced septic insults in the rat heart. PLoS One. 2013;8:e56526.
64. Saitoh O, Nakagawa K, Asada S, et al. Effects of 16, 16-dimethyl prostaglandin E2 on lysosomal membrane stability in rat stomach. J Gastroenterol. 1994;29:703–9.
65. Naito Y, Kajikawa H, Mizushima K. 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. 2005;50:S104–12.
66. Ishihara T, Tanaka K, Tashiro S, et al. Protective effect of rebamipide against celecoxib-induced gastric mucosal cell apoptosis. Biochem Pharmacol. 2010;79:1622–33.
67. Takeuchi K. Prostaglandin EP receptors and their roles in mucosal protection and ulcer healing in the gastrointestinal tract. Adv Clin Chem. 2010;51:121–44.
68. Handa O, Naito Y, Fukui A, et al. The impact of non-steroidal anti-inflammatory drugs on the small intestinal epithelium. J Clin Biochem Nutr. 2014;54:2–6.