Hyperglycemia induces apoptosis via CB 1 activation through the decrease of FAAH 1 in retianl pigment epithelial cells

Journal of Cellular Physiology

Volumn 227, Issue 2, 2012, Pages 569-577

  Lim, Seul Ki ^a   Park, Min Jung ^a   Lim, Jae Cheong ^a   Kim, Jong Choon ^a   Han, Ho Jae ^b   Kim, Gye Yeop ^c   Cravatt, Benjamin F ^d   Woo, Chang Hoon ^e   Ma, Seung Jin ^f   Yoon, Kyung Cheol ^g   Park, Soo Hyun ^a  

^a Chonnam National University   (South Korea)

^b Seoul National University   (South Korea)

^c Dongshin University   (South Korea)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e Yeungnam University College of Medicine   (South Korea)

^f Mokpo National University   (South Korea)

^g Chonnam National University Medical School   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID 1 RECEPTOR; CASPASE 3; CASPASE 9; FATTY ACID AMIDASE; FATTY ACID AMIDASE 1; GLUCOSE; LIPID PEROXIDE; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; DOWN REGULATION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; INTERNALIZATION; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; RECEPTOR BLOCKING; UPREGULATION;

AMIDOHYDROLASES; CELL LINE; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; HYPERGLYCEMIA; REACTIVE OXYGEN SPECIES; RECEPTOR, CANNABINOID, CB1; RETINAL PIGMENT EPITHELIUM; RNA, MESSENGER;

EID: 82155192312     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22756     Document Type: Article

References (48)

1. Abu-El-Asrar AM, Dralands L, Missotten L, Al-Jadaan IA, Geboes K. 2004. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest Ophthalmol Vis Sci 45: 2760-2766.
2. Ahn K, Johnson DS, Cravatt BF. 2009. Fatty acid amide hydrolase as a potential therapeutic target for the treatment of pain and CNS disorders. Expert Opin Drug Discov 4: 763-784.
3. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. 1998. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest 102: 783-791.
4. Cai J, Boulton M. 2002. The pathogenesis of diabetic retinopathy: Old concepts and new questions. Eye 16: 242-260.
5. Casson RJ, Chidlow G, Wood JP, Osborne NN. 2004. The effect of hyperglycemia on experimental retinal ischemia. Arch Ophthalmol 122: 361-366.
6. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB. 1996. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384: 83-87.
7. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH. 2001. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci USA 98: 9371-9376.
8. Di Marzo V. 2008. The endocannabinoid system in obesity and type 2 diabetes. Diabetologia 51: 1356-1367.
9. Di Marzo V, Despres JP. 2009. CB1 antagonists for obesity-What lessons have we learned from rimonabant? Nat Rev Endocrinol 5: 633-638.
10. Doonan F, Donovan M, Cotter TG. 2003. Caspase-independent photoreceptor apoptosis in mouse models of retinal degeneration. J Neurosci 23: 5723-5731.
11. Du Y, Miller CM, Kern TS. 2003. Hyperglycemia increases mitochondrial superoxide in retina and retinal cells. Free Radic Biol Med 35: 1491-1499.
12. Durand E, Lecoeur C, Delplanque J, Benzinou M, Degraeve F, Boutin P, Marre M, Balkau B, Charpentier G, Froguel P, Meyre D. 2008. Evaluating the association of FAAH common gene variation with childhood, adult severe obesity and type 2 diabetes in the French population. Obes Facts 1: 305-309.
13. Gao XY, Kuang HY, Zou W, Liu XM, Lin HB, Yang Y. 2009. The timing of re-institution of good blood glucose control affects apoptosis and expression of Bax and Bcl-2 in the retina of diabetic rats. Mol Biol Rep 36: 1977-1982.
14. Hillard CJ, Shi L, Tuniki VR, Falck JR, Campbell WB. 2007. Studies of anandamide accumulation inhibitors in cerebellar granule neurons: Comparison to inhibition of fatty acid amide hydrolase. J Mol Neurosci 33: 18-24.
15. Ikesugi K, Mulhern ML, Madson CJ, Hosoya K, Terasaki T, Kador PF, Shinohara T. 2006. Induction of endoplasmic reticulum stress in retinal pericytes by glucose deprivation. Curr Eye Res 31: 947-953.
16. Johnston TH, Huot P, Fox SH, Wakefield JD, Sykes KA, Bartolini WP, Milne GT, Pearson JP, Brotchie JM. 2011. Fatty acid amide hydrolase (FAAH) inhibition reduces L-DOPA-induced hyperactivity in the MPTP-lesioned non-human primate model of Parkinson's disease. J Pharmacol Exp Ther 336: 423-430.
17. Kern TS, Du Y, Miller CM, Hatala DA, Levin LA. 2010. Overexpression of Bcl-2 in vascular endothelium inhibits the microvascular lesions of diabetic retinopathy. Am J Pathol 176: 2550-2558.
18. Khalfaoui T, Basora N, Ouertani-Meddeb A. 2010. Apoptotic factors (Bcl-2 and Bax) and diabetic retinopathy in type 2 diabetes. J Mol Histol 41: 143-152.
19. Kim DI, Lim SK, Park MJ, Han HJ, Kim GY, Park SH. 2007a. The involvement of phosphatidylinositol 3-kinase/Akt signaling in high glucose-induced downregulation of GLUT-1 expression in ARPE cells. Life Sci 80: 626-632.
20. Kim YS, Jung DH, Kim NH, Lee YM, Kim JS. 2007b. Effect of magnolol on TGF-β1 and fibronectin expression in human retinal epithelial cells under diabetic conditions. Eur J Pharmacol 562: 12-19.
21. Kinsey SG, Long JZ, Cravatt BF, Lichtman AH. 2010. Fatty acid amide hydrolase and monoacylglycerol lipase inhibitors produce anti-allodynic effects in mice through distinct cannabinoid receptor mechanisms. J Pain 11: 1420-1428.
22. Kowluru RA. 2005. Diabetic retinopathy: Mitochondrial dysfunction and retinal capillary cell death. Antioxid Redox Signal 7: 1581-1587.
23. Krügel K, Wurm A, Pannicke T, Hollborn M, Karl A, Wiedemann P, Reichenbach A, Kohen L, Bringmann A. 2011. Involvement of oxidative stress and mitochondrial dysfunction in the osmotic swelling of retinal glial cells from diabetic rats. Exp Eye Res 92: 87-93.
24. Lim SK, Han HJ, Kim KY, Park SH. 2009. Both B1R and B2R act as intermediate signaling molecules in high glucose-induced stimulation of glutamate uptake in ARPE cells. J Cell Physiol 221: 677-687.
25. Lim JC, Lim SK, Han HJ, Park SH. 2010. Cannabinoid receptor 1 mediates palmitic acid-induced apoptosis via endoplasmic reticulum stress in human renal proximal tubular cells. J Cell Physiol 225: 654-663.
26. López EM, Tagliaferro P, Onaivi ES, López-Costa JJ. 2011. Distribution of CB2 cannabinoid receptor in adult rat retina. Synapse 65: 388-392.
27. Malfait M, Gomez P, van Veen TA, Parys JB, De Smedt H, Vereecke J, Himpens B. 2001. Effects of hyperglycemia and protein kinase C on connexin 43 expression in cultured rat retinal pigment epithelial cells. J Membr Biol 181: 31-40.
28. Matias I, Gonthier MP, Orlando P, Martiadis V, De Petrocellis L, Cervino C, Petrosino S, Hoareau L, Festy F, Pasquali R, Roche R, Maj M, Pagotto U, Monteleone P, Di Marzo V. 2006. Regulation, function, and dysregulation of endocannabinoids in models of adipose and beta-pancreatic cells and in obesity and hyperglycemia. J Clin Endocrinol Metab 91: 3171-3180.
29. Matias I, Petrosino S, Racioppi A, Capasso R, Izzo AA, Di Marzo V. 2008. Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: Effect of high fat diets. Mol Cell Endocrinol 286: S66-S78.
30. Matsuda S, Kanemitsu N, Nakamura A, Mimura Y, Ueda N, Kurahashi Y, Yamamoto S. 1997. Metabolism of anandamide, an endogenous cannabinoid receptor ligand, in porcine ocular tissues. Exp Eye Res 64: 707-711.
31. Mechoulam R, Fride E, Di Marzo V. 1998. Endocannabinoids. Eur J Pharmacol 359: 1-18.
32. Mechoulam R, Panikashvili D, Shohami E. 2002. Cannabinoids and brain injury: Therapeutic implications. Trends Mol Med 8: 58-61.
33. Mousavi SH, Tayarani NZ, Parsaee H. 2010. Protective effect of saffron extract and crocin on reactive oxygen species-mediated high glucose-induced toxicity in PC12 cells. Cell Mol Neurobiol 30: 185-191.
34. Nishikawa T, Araki E. 2007. Impact of mitochondrial ROS production in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 9: 343-353.
35. Nucci C, Gasperi V, Tartaglione R, Cerulli A, Terrinoni A, Bari M, De Simone C, Agrò AF, Morrone LA, Corasaniti MT, Bagetta G, Maccarrone M. 2007. Involvement of the endocannabinoid system in retinal damage after high intraocular pressure-induced ischemia in rats. Invest Ophthalmol Vis Sci 48: 2997-3004.
36. Ohkawa H, Ohishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95: 351-358.
37. Oshitari T, Yamamoto S, Hata N, Roy S. 2008. Mitochondria- and caspase-dependent cell death pathway involved in neuronal degeneration in diabetic retinopathy. Br J Ophthalmol 92: 552-556.
38. Pasquariello N, Catanzaro G, Marzano V, Amadio D, Barcaroli D, Oddi S, Federici G, Urbani A, Finazzi Agrò A, Maccarrone M. 2009. Characterization of the endocannabinoid system in human neuronal cells and proteomic analysis of anandamide-induced apoptosis. J Biol Chem 284: 29413-29426.
39. Trudeau K, Molina AJ, Guo W, Roy S. 2010. High glucose disrupts mitochondrial morphology in retinal endothelial cells: Implications for diabetic retinopathy. Am J Pathol 177: 447-455.
40. Ueda N. 2002. Endocannabinoid hydrolases. Prostaglandins Other Lipid Mediat 68-69: 521-534.
41. Villarroel M, García-Ramírez M, Corraliza L, Hernández C, Simó R. 2009. High glucose concentration leads to differential expression of tight junction proteins in human retinal pigment epithelial cells. Endocrinol Nutr 56: 53-58.
42. Wei Y, Wang X, Wang L. 2009. Presence and regulation of cannabinoid receptors in human retinal pigment epithelial cells. Mol Vis 15: 1243-1251.
43. Wu DF, Yang LQ, Goschke A, Stumm R, Brandenburg LO, Liang YJ, Hollt V, Koch T. 2008. Role of receptor internalization in the agonist-induced desensitization of cannabinoid type 1 receptors. J Neurochem 104: 1132-1143.
44. Xie L, Zhu X, Hu Y, Li T, Gao Y, Shi Y, Tang S. 2008. Mitochondrial DNA oxidative damage triggering mitochondrial dysfunction and apoptosis in high glucose-induced HRECs. Invest Ophthalmol Vis Sci 49: 4203-4209.
45. Yazulla S. 2008. Endocannabinoids in the retina: From marijuana to neuroprotection. Prog Retin Eye Res 27: 501-526.
46. Yazulla S, Studholme KM, McIntosh HH, Deutsch DG. 1999. Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina. J Comp Neurol 415: 80-90.
47. Yuan Z, Feng W, Hong J, Zheng Q, Shuai J, Ge Y. 2009. p38MAPK and ERK promote nitric oxide production in cultured human retinal pigmented epithelial cells induced by high concentration glucose. Nitric Oxide 20: 9-15.
48. Zheng L, Kern TS. 2009. Role of nitric oxide, superoxide, peroxynitrite and PARP in diabetic retinopathy. Front Biosci 14: 3974-3987.