Oxidative and endoplasmic reticulum stresses mediate apoptosis induced by modified LDL in human retinal Müller cells

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 8, 2012, Pages 4595-4604

  Wu, Mingyuan ^a   Yang, Shihe ^a   Elliott, Michael H ^b   Fu, Dongxu ^a,c   Wilson, Kenneth ^a   Zhang, Jing ^a   Du, Mei ^a   Chen, Junping ^a   Lyons, Timothy ^a  

^a UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHENYLBUTYRIC ACID; 7 OXOCHOLESTEROL; ACETYLCYSTEINE; LOW DENSITY LIPOPROTEIN; REACTIVE OXYGEN METABOLITE; GLYCOSYLATED LIPOPROTEINS, LDL; OXIDIZED LOW DENSITY LIPOPROTEIN;

ADULT; APOPTOSIS; ARTICLE; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; DENSITOMETRY; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMAN; HUMAN CELL; MALE; MUELLER CELL; NICK END LABELING; NORMAL HUMAN; PRIORITY JOURNAL; WESTERN BLOTTING; CELL SURVIVAL; COMPARATIVE STUDY; DIABETIC RETINOPATHY; DRUG EFFECT; ENDOPLASMIC RETICULUM; GLIA; GLYCOSYLATION; METABOLISM; MIDDLE AGED; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOLOGY; RETINA GANGLION CELL;

ADULT; APOPTOSIS; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; DIABETIC RETINOPATHY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FEMALE; GLYCOSYLATION; HUMANS; IN SITU NICK-END LABELING; LIPOPROTEINS, LDL; MALE; MIDDLE AGED; NEUROGLIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; RETINAL GANGLION CELLS; YOUNG ADULT;

EID: 84866954190     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-9910     Document Type: Article

References (61)

1. Gardner TW, Antonetti DA. A prize catch for diabetic retinopathy. Nat Med. 2007;13:131-132.
2. Garner A. Histopathology of diabetic retinopathy in man. Eye (Lond). 1993;7:250-253.
3. Hammes HP, Lin J, Renner O, et al. Pericytes and the pathogenesis of diabetic retinopathy. Diabetes. 2002;51: 3107-3112.
4. Hammes HP. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res. 2005;37:39-43.
5. Canning P, Glenn JV, Hsu DK, Liu FT, Gardiner TA, Stitt AW. Inhibition of advanced glycation and absence of galectin-3 prevent blood-retinal barrier dysfunction during short-term diabetes. Exp Diabetes Res. 2007;2007:51837.
6. Reichenbach A, Stolzenburg JU, Eberhardt W, Chao TI, Dettmer D, Hertz L. What do retinal Muller (glial) cells do for their neuronal 'small siblings'? J Chem Neuroanat. 1993;6: 201-213.
7. Ahmad I, Del Debbio CB, Das AV, Parameswaran S. Müller glia: a promising target for therapeutic regeneration. Invest Ophthalmol Vis Sci. 2011;52:5758-5764.
8. Bringmann A, Francke M, Pannicke T, et al. Human Müller glial cells: altered potassium channel activity in proliferative vitreoretinopathy. Invest Ophthalmol Vis Sci. 1999;40:3316-3323.
9. Xi X, Gao L, Hatala DA, et al. Chronically elevated glucose induced apoptosis is mediated by inactivation of Akt in cultured Müller cells. Biochem Biophys Res Commun. 2005; 326:548-553.
10. Gerhardinger C, Costa MB, Coulombe MC, Toth I, Hoehn T, Grosu P. Expression of acute-phase response proteins in retinal Müller cells in diabetes. Invest Ophthalmol Vis Sci. 2005;46: 349-357.
11. Zong H, Ward M, Madden A, et al. Hyperglycaemia-induced pro-inflammatory responses by retinal Müller glia are regulated by the receptor for advanced glycation end-products (RAGE). Diabetologia. 2010;53:2656-2666.
12. Lyons TJ, Li W, Wells-Knecht MC, Jokl R. Toxicity of mildly modified low-density lipoproteins to cultured retinal capillary endothelial cells and pericytes. Diabetes. 1994;43:1090-1095.
13. Lyons TJ, Jenkins AJ, Zheng D, et al. Diabetic retinopathy and serum lipoprotein subclasses in the DCCT/EDIC cohort. Invest Ophthalmol Vis Sci. 2004;45:910-918.
14. Song W, Barth JL, Lu K, et al. Effects of modified low-density lipoproteins on human retinal pericyte survival. Ann N Y Acad Sci. 2005;1043:390-395.
15. Song W, Barth JL, Yu Y, et al. Effects of oxidized and glycated LDL on gene expression in human retinal capillary pericytes. Invest Ophthalmol Vis Sci. 2005;46:2974-2982.
16. Wu M, Chen Y, Wilson K, et al. Intraretinal leakage and oxidation of LDL in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2008;49:2679-2685.
17. Diffley JM, Wu M, Sohn M, Song W, Hammad SM, Lyons TJ. Apoptosis induction by oxidized glycated LDL in human retinal capillary pericytes is independent of activation of MAPK signaling pathways. Mol Vis. 2009;15:135-145.
18. Zou MH, Li H, He C, Lin M, Lyons TJ, Xie Z. Tyrosine nitration of prostacyclin synthase is associated with enhanced retinal cell apoptosis in diabetes. Am J Pathol. 2011;179:2835-2844.
19. Lloyd CE, Klein R, Maser RE, Kuller LH, Becker DJ, Orchard TJ. The progression of retinopathy over 2 years: the Pittsburgh Epidemiology of Diabetes Complications (EDC) Study. J Diabetes Complications. 1995;9:140-148.
20. van Leiden HA, Dekker JM, Moll AC, et al. Blood pressure, lipids, and obesity are associated with retinopathy: the Hoorn study. Diabetes Care. 2002;25:1320-1325.
21. Chait A, Montes VN. Apolipoproteins and diabetic retinopathy. Diabetes Care. 2011;34:529-531.
22. Yong PH, Zong H, Medina RJ, et al. Evidence supporting a role for N-(3-formyl-3,4-dehydropiperidino)lysine accumulation in Müller glia dysfunction and death in diabetic retinopathy. Mol Vis. 2010;16:2524-2538.
23. Arden GB, Sivaprasad S. Hypoxia and oxidative stress in the causation of diabetic retinopathy. Curr Diabetes Rev. 2011;7: 291-304.
24. Yamagishi S, Matsui T. Advanced glycation end products (AGEs), oxidative stress and diabetic retinopathy. Curr Pharm Biotechnol. 2011;12:362-368.
25. Kowluru RA, Kanwar M. Effects of curcumin on retinal oxidative stress and inflammation in diabetes. Nutr Metab (Lond). 2007;4:8.
26. Kowluru RA, Chan PS. Oxidative stress and diabetic retinopathy. Exp Diabetes Res. 2007;2007:43603.
27. Oshitari T, Hata N, Yamamoto S. Endoplasmic reticulum stress and diabetic retinopathy. Vasc Health Risk Manag. 2008;4: 115-122.
28. Li J, Wang JJ, Yu Q, Wang M, Zhang SX. Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett. 2009;583:1521-1527.
29. Li J, Wang JJ, Yu Q, Chen K, Mahadev K, Zhang SX. Inhibition of reactive oxygen species by Lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4. Diabetes. 2010;59:1528-1538.
30. Jing G, Wang JJ, Zhang SX. ER stress and apoptosis: a new mechanism for retinal cell death. Exp Diabetes Res. 2012; 2012:589.
31. Dong Y, Zhang M, Wang S, et al. Activation of AMP-activated protein kinase inhibits oxidized LDL-triggered endoplasmic reticulum stress in vivo. Diabetes. 2010;59:1386-1396.
32. Jenkins AJ, Velarde V, Klein RL, et al. Native and modified LDL activate extracellular signal-regulated kinases in mesangial cells. Diabetes. 2000;49:2160-2169.
33. Limb GA, Salt TE, Munro PM, Moss SE, Khaw PT. In vitro characterization of a spontaneously immortalized human Müller cell line (MIO-M1). Invest Ophthalmol Vis Sci. 2002; 43:864-869.
34. Lawrence JM, Singhal S, Bhatia B, et al. MIO-M1 cells and similar Muller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells. 2007;25: 2033-2043.
35. Dong Y, Wu Y, Wu M, et al. Activation of protease calpain by oxidized and glycated LDL increases the degradation of endothelial nitric oxide synthase. J Cell Mol Med. 2009;13: 2899-2910.
36. Galle J, Schneider R, Winner B, et al. Glyc-oxidized LDL impair endothelial function more potently than oxidized LDL: role of enhanced oxidative stress. Atherosclerosis. 1998;138:65-77.
37. Lam MC, Tan KC, Lam KS. Glycoxidized low-density lipoprotein regulates the expression of scavenger receptors in THP-1 macrophages. Atherosclerosis. 2004;177:313-320.
38. Calzada C, Coulon L, Halimi D, et al. In vitro glycoxidized lowdensity lipoproteins and low-density lipoproteins isolated from type 2 diabetic patients activate platelets via p38 mitogen-activated protein kinase. J Clin Endocrinol Metab. 2007;92:1961-1964.
39. Zhou T, Zhou KK, Lee K, et al. The role of lipid peroxidation products and oxidative stress in activation of the canonical wingless-type MMTV integration site (WNT) pathway in a rat model of diabetic retinopathy. Diabetologia. 2010;54:459-468.
40. Zhang SX, Wang JJ, Dashti A, et al. Pigment epithelium-derived factor mitigates inflammation and oxidative stress in retinal pericytes exposed to oxidized low-density lipoprotein. J Mol Endocrinol. 2008;41:135-143.
41. Bringmann A, Pannicke T, Grosche J, et al. Müller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25:397-424.
42. Puro DG. Diabetes-induced dysfunction of retinal Müller cells. Trans Am Ophthalmol Soc. 2002;100:339-352.
43. Mizutani M, Gerhardinger C, Lorenzi M. Müller cell changes in human diabetic retinopathy. Diabetes. 1998;47:445-449.
44. Lieth E, Barber AJ, Xu B, et al. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Penn State Retina Research Group. Diabetes. 1998;47:815-820.
45. Lieth E, Gardner TW, Barber AJ, Antonetti DA. Retinal neurodegeneration: early pathology in diabetes. Clin Experiment Ophthalmol. 2000;28:3-8.
46. Barber AJ, Antonetti DA, Gardner TW. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. The Penn State Retina Research Group. Invest Ophthalmol Vis Sci. 2000;41:3561-3568.
47. Basuroy S, Tcheranova D, Bhattacharya S, Leffler CW, Parfenova H. Nox4 NADPH oxidase-derived reactive oxygen species, via endogenous carbon monoxide, promote survival of brain endothelial cells during TNF-alpha-induced apoptosis. Am J Physiol Cell Physiol. 2011;300:C256-265.
48. Tout S, Chan-Ling T, Hollander H, Stone J. The role of Müller cells in the formation of the blood-retinal barrier. Neuroscience. 1993;55:291-301.
49. Curtis TM, Hamilton R, Yong PH, et al. Müller glial dysfunction during diabetic retinopathy in rats is linked to accumulation of advanced glycation end-products and advanced lipoxidation end-products. Diabetologia. 2010;54:690-698.
50. Li Q, Puro DG. Diabetes-induced dysfunction of the glutamate transporter in retinal Müller cells. Invest Ophthalmol Vis Sci. 2002;43:3109-3116.
51. Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A. 1995;92:905-909.
52. Wang J, Xu X, Elliott MH, Zhu M, Le YZ. Müller cell-derived VEGF is essential for diabetes-induced retinal inflammation and vascular leakage. Diabetes. 2010;59:2297-2305.
53. Amin RH, Frank RN, Kennedy A, Eliott D, Puklin JE, Abrams GW. Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci. 1997;38:36-47.
54. Lyons TJ, Baynes JW, Patrick JS, Colwell JA, Lopes-Virella MF. Glycation of low density lipoprotein in patients with Type I diabetes: correlations with other parameters of glycaemic control. Diabetologia. 1986;29:685-689.
55. Baydas G, Tuzcu M, Yasar A, Baydas B. Early changes in glial reactivity and lipid peroxidation in diabetic rat retina: effects of melatonin. Acta Diabetol. 2004;41:123-128.
56. Kanwar M, Chan PS, Kern TS, Kowluru RA. Oxidative damage in the retinal mitochondria of diabetic mice: possible protection by superoxide dismutase. Invest Ophthalmol Vis Sci. 2007;48:3805-3811.
57. Mattson MP. Roles of the lipid peroxidation product 4-hydroxynonenal in obesity, the metabolic syndrome, and associated vascular and neurodegenerative disorders. Exp Gerontol. 2009;44:625-633.
58. Martinet W, De Bie M, Schrijvers DM, De Meyer GR, Herman AG, Kockx MM. 7-ketocholesterol induces protein ubiquitination, myelin figure formation, and light chain 3 processing in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2004;24:2296-2301.
59. Martinet W, De Meyer GR. Autophagy in atherosclerosis: a cell survival and death phenomenon with therapeutic potential. Circ Res. 2009;104:304-317.
60. Rodriguez IR, Alam S, Lee JW. Cytotoxicity of oxidized low density lipoprotein in cultured RPE cells is dependent on the formation of 7-ketocholesterol. Invest Ophthalmol Vis Sci. 2004;45:2830-2837.
61. Yang Y, Sharma R, Sharma A, Awasthi S, Awasthi YC. Lipid peroxidation and cell cycle signaling: 4-hydroxynonenal, a key molecule in stress mediated signaling. Acta Biochim Pol. 2003;50:319-336.