Advanced Glycation End Products Induce Human Corneal Epithelial Cells Apoptosis through Generation of Reactive Oxygen Species and Activation of JNK and p38 MAPK Pathways

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Shi, Long ^a   Yu, Xiaoming ^a   Yang, Hongling ^a   Wu, Xinyi ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACETYLCYSTEINE; ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BOVINE SERUM ALBUMIN; CELL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUTRALIZING ANTIBODY; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P47PHOX; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STRESS ACTIVATED PROTEIN KINASE; TELOMERASE; UNCLASSIFIED DRUG; FLUORESCEIN ISOTHIOCYANATE;

APOPTOSIS; ARTICLE; CELL IMMORTALIZATION; CONTROLLED STUDY; CORNEA EPITHELIUM; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; CORNEAL DISEASES; CYTOLOGY; DIABETES MELLITUS; DRUG EFFECTS; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

BOVINAE;

APOPTOSIS; BLOTTING, WESTERN; CORNEAL DISEASES; DIABETES COMPLICATIONS; EPITHELIAL CELLS; EPITHELIUM, CORNEAL; FLUORESCEIN-5-ISOTHIOCYANATE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REACTIVE OXYGEN SPECIES; SERUM ALBUMIN, BOVINE; TELOMERASE;

EID: 84878919999     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066781     Document Type: Article

References (57)

1. Ferrannini E, Cushman WC, (2012) Diabetes and hypertension: the bad companions. Lancet 380: 601-610.
2. Xu KP, Li Y, Ljubimov AV, Yu FS, (2009) High glucose suppresses epidermal growth factor receptor/phosphatidylinositol 3-kinase/Akt signaling pathway and attenuates corneal epithelial wound healing. Diabetes 58: 1077-1085.
3. Yin J, Yu FS, (2010) LL-37 via EGFR transactivation to promote high glucose-attenuated epithelial wound healing in organ-cultured corneas. Invest Ophthalmol Vis Sci 51: 1891-1897.
4. Schulze SD, Sekundo W, Kroll P, (2006) Autologous serum for the treatment of corneal epithelial abrasions in diabetic patients undergoing vitrectomy. Am J Ophthalmol 142: 207-211.
5. Yamagishi S, Matsui T, (2011) Advanced glycation end products (AGEs), oxidative stress and diabetic retinopathy. Curr Pharm Biotechnol 12: 362-368.
6. Yamagishi S, Matsui T, (2010) Advanced glycation end products, oxidative stress and diabetic nephropathy. Oxid Med Cell Longev 3: 101-108.
7. Patel R, Baker SS, Liu W, Desai S, Alkhouri R, et al. (2012) Effect of dietary advanced glycation end products on mouse liver. PLoS One 7: e35143.
8. Prasad A, Bekker P, Tsimikas S, (2012) Advanced glycation end products and diabetic cardiovascular disease. Cardiol Rev 20: 177-183.
9. Xue J, Rai V, Singer D, Chabierski S, Xie J, et al. (2011) Advanced glycation end product recognition by the receptor for AGEs. Structure 19: 722-732.
10. Kaji Y, Usui T, Oshika T, Matsubara M, Yamashita H, et al. (2000) Advanced glycation end products in diabetic corneas. Invest Ophthalmol Vis Sci 41: 362-368.
11. Yucel I, Yucel G, Akar Y, Demir N, Gurbuz N, et al. (2006) Transmission electron microscopy and autofluorescence findings in the cornea of diabetic rats treated with aminoguanidine. Can J Ophthalmol 41: 60-66.
12. Kim J, Kim CS, Sohn E, Jeong IH, Kim H, et al. (2011) Involvement of advanced glycation end products, oxidative stress and nuclear factor-kappaB in the development of diabetic keratopathy. Graefes Arch Clin Exp Ophthalmol 249: 529-536.
13. Kim J, Kim CS, Kim H, Jeong IH, Sohn E, et al. (2011) Protection against advanced glycation end products and oxidative stress during the development of diabetic keratopathy by KIOM-79. J Pharm Pharmacol 63: 524-530.
14. Zou C, Wang S, Huang F, Zhang YA, (2012) Advanced glycation end products and ultrastructural changes in corneas of long-term streptozotocin-induced diabetic monkeys. Cornea 31: 1455-1459.
15. Zhao Z, Liu J, Shi B, He S, Yao X, et al. (2010) Advanced glycation end product (AGE) modified proteins in tears of diabetic patients. Mol Vis 16: 1576-1584.
16. Gul M, Emre S, Esrefoglu M, Vard N, (2008) Protective effects of melatonin and aminoguanidine on the cornea in streptozotocin-induced diabetic rats. Cornea 27: 795-801.
17. Barlovic DP, Soro-Paavonen A, Jandeleit-Dahm KA, (2011) RAGE biology, atherosclerosis and diabetes. Clin Sci (Lond) 121: 43-55.
18. Park S, Yoon SJ, Tae HJ, Shim CY, (2011) RAGE and cardiovascular disease. Front Biosci 16: 486-497.
19. Yan SF, Ramasamy R, Schmidt AM, (2008) Mechanisms of disease: advanced glycation end-products and their receptor in inflammation and diabetes complications. Nat Clin Pract Endocrinol Metab 4: 285-293.
20. Zong H, Ward M, Stitt AW, (2011) AGEs, RAGE, and diabetic retinopathy. Curr Diab Rep 11: 244-252.
21. Alves M, Calegari VC, Cunha DA, Saad MJ, Velloso LA, et al. (2005) Increased expression of advanced glycation end-products and their receptor, and activation of nuclear factor kappa-B in lacrimal glands of diabetic rats. Diabetologia 48: 2675-2681.
22. Liu JP, Feng L, Zhu MM, Wang RS, Zhang MH, et al. (2012) The in vitro protective effects of curcumin and demethoxycurcumin in Curcuma longa extract on advanced glycation end products-induced mesangial cell apoptosis and oxidative stress. Planta Med 78: 1757-1760.
23. Zhan Y, Sun HL, Chen H, Zhang H, Sun J, et al. (2012) Glucagon-like peptide-1 (GLP-1) protects vascular endothelial cells against advanced glycation end products (AGEs)-induced apoptosis. Med Sci Monit 18: BR286-291.
24. Kim J, Kim KM, Kim CS, Sohn E, Lee YM, et al. (2012) Puerarin inhibits the retinal pericyte apoptosis induced by advanced glycation end products in vitro and in vivo by inhibiting NADPH oxidase-related oxidative stress. Free Radic Biol Med 53: 357-365.
25. Xu K, Yu FS, (2011) Impaired epithelial wound healing and EGFR signaling pathways in the corneas of diabetic rats. Invest Ophthalmol Vis Sci 52: 3301-3308.
26. Niiya Y, Abumiya T, Yamagishi S, Takino J, Takeuchi M, (2012) Advanced glycation end products increase permeability of brain microvascular endothelial cells through reactive oxygen species-induced vascular endothelial growth factor expression. J Stroke Cerebrovasc Dis 21: 293-298.
27. Sugamura K, Keaney JF Jr, (2011) Reactive oxygen species in cardiovascular disease. Free Radic Biol Med 51: 978-992.
28. Circu ML, Aw TY, (2010) Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48: 749-762.
29. Yang Q, Chen C, Wu S, Zhang Y, Mao X, et al. (2010) Advanced glycation end products downregulates peroxisome proliferator-activated receptor gamma expression in cultured rabbit chondrocyte through MAPK pathway. Eur J Pharmacol 649: 108-114.
30. Chen L, Hu W, Tan S, Wang M, Ma Z, et al. (2012) Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS One 7: e46744.
31. Alikhani M, Maclellan CM, Raptis M, Vora S, Trackman PC, et al. (2007) Advanced glycation end products induce apoptosis in fibroblasts through activation of ROS, MAP kinases, and the FOXO1 transcription factor. Am J Physiol Cell Physiol 292: C850-856.
32. Alikhani M, Alikhani Z, Boyd C, MacLellan CM, Raptis M, et al. (2007) Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 40: 345-353.
33. Liu Y, Ma Y, Wang R, Xia C, Zhang R, et al. (2011) Advanced glycation end products accelerate ischemia/reperfusion injury through receptor of advanced end product/nitrative thioredoxin inactivation in cardiac microvascular endothelial cells. Antioxid Redox Signal 15: 1769-1778.
34. Busch M, Franke S, Wolf G, Brandstadt A, Ott U, et al. (2006) The advanced glycation end product N(epsilon)-carboxymethyllysine is not a predictor of cardiovascular events and renal outcomes in patients with type 2 diabetic kidney disease and hypertension. Am J Kidney Dis 48: 571-579.
35. Busch M, Franke S, Wolf G, Rohde RD, Stein G, (2008) Serum levels of the advanced glycation end products Nepsilon-carboxymethyllysine and pentosidine are not influenced by treatment with the angiotensin receptor II type 1 blocker irbesartan in patients with type 2 diabetic nephropathy and hypertension. Nephron Clin Pract 108: c291-297.
36. Kumar A, Zhang J, Yu FS, (2006) Toll-like receptor 2-mediated expression of beta-defensin-2 in human corneal epithelial cells. Microbes Infect 8: 380-389.
37. Shi L, Chang Y, Yang Y, Zhang Y, Yu FS, et al. (2012) Activation of JNK signaling mediates connective tissue growth factor expression and scar formation in corneal wound healing. PLoS One 7: e32128.
38. Guimaraes EL, Empsen C, Geerts A, van Grunsven LA, (2010) Advanced glycation end products induce production of reactive oxygen species via the activation of NADPH oxidase in murine hepatic stellate cells. J Hepatol 52: 389-397.
39. Yamagishi S, Nakamura K, Matsui T, Inagaki Y, Takenaka K, et al. (2006) Pigment epithelium-derived factor inhibits advanced glycation end product-induced retinal vascular hyperpermeability by blocking reactive oxygen species-mediated vascular endothelial growth factor expression. J Biol Chem 281: 20213-20220.
40. Yuan H, Zhang X, Huang X, Lu Y, Tang W, et al. (2010) NADPH oxidase 2-derived reactive oxygen species mediate FFAs-induced dysfunction and apoptosis of beta-cells via JNK, p38 MAPK and p53 pathways. PLoS One 5: e15726.
41. Klenovics KS, Boor P, Somoza V, Celec P, Fogliano V, et al. (2013) Advanced glycation end products in infant formulas do not contribute to insulin resistance associated with their consumption. PLoS One 8: e53056.
42. Sheikpranbabu S, Haribalaganesh R, Gurunathan S, (2011) Pigment epithelium-derived factor inhibits advanced glycation end-products-induced cytotoxicity in retinal pericytes. Diabetes Metab 37: 505-511.
43. Guo W, Liu W, Hong S, Liu H, Qian C, et al. (2012) Mitochondria-dependent apoptosis of con A-activated T lymphocytes induced by asiatic acid for preventing murine fulminant hepatitis. PLoS One 7: e46018.
44. Malla R, Gopinath S, Alapati K, Gondi CS, Gujrati M, et al. (2010) Downregulation of uPAR and cathepsin B induces apoptosis via regulation of Bcl-2 and Bax and inhibition of the PI3K/Akt pathway in gliomas. PLoS One 5: e13731.
45. Sorci G, Riuzzi F, Giambanco I, Donato R, (2013) RAGE in tissue homeostasis, repair and regeneration. Biochim Biophys Acta 1833: 101-109.
46. Sukkar MB, Ullah MA, Gan WJ, Wark PA, Chung KF, et al. (2012) RAGE: a new frontier in chronic airways disease. Br J Pharmacol 167: 1161-1176.
47. Ramasamy R, Yan SF, Schmidt AM, (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243: 88-102.
48. van Zoelen MA, Achouiti A, van der Poll T, (2011) RAGE during infectious diseases. Front Biosci (Schol Ed) 3: 1119-1132.
49. Ishibashi Y, Yamagishi S, Matsui T, Ohta K, Tanoue R, et al. (2012) Pravastatin inhibits advanced glycation end products (AGEs)-induced proximal tubular cell apoptosis and injury by reducing receptor for AGEs (RAGE) level. Metabolism 61: 1067-1072.
50. Basta G, Lazzerini G, Del Turco S, Ratto GM, Schmidt AM, et al. (2005) At least 2 distinct pathways generating reactive oxygen species mediate vascular cell adhesion molecule-1 induction by advanced glycation end products. Arterioscler Thromb Vasc Biol 25: 1401-1407.
51. Jendrysik MA, Vasilevsky S, Yi L, Wood A, Zhu N, et al. (2011) NADPH oxidase-2 derived ROS dictates murine DC cytokine-mediated cell fate decisions during CD4 T helper-cell commitment. PLoS One 6: e28198.
52. Huo Y, Qiu WY, Pan Q, Yao YF, Xing K, et al. (2009) Reactive oxygen species (ROS) are essential mediators in epidermal growth factor (EGF)-stimulated corneal epithelial cell proliferation, adhesion, migration, and wound healing. Exp Eye Res 89: 876-886.
53. Octavia Y, Brunner-La Rocca HP, Moens AL, (2012) NADPH oxidase-dependent oxidative stress in the failing heart: From pathogenic roles to therapeutic approach. Free Radic Biol Med 52: 291-297.
54. Belambri SA, Hurtado-Nedelec M, Senator A, Makni-Maalej K, Fay M, et al. (2012) Phosphorylation of p47phox is required for receptor-mediated NADPH oxidase/NOX2 activation in Epstein-Barr virus-transformed human B lymphocytes. Am J Blood Res 2: 187-193.
55. Al-Azayzih A, Gao F, Goc A, Somanath PR, (2012) TGFbeta1 induces apoptosis in invasive prostate cancer and bladder cancer cells via Akt-independent, p38 MAPK and JNK/SAPK-mediated activation of caspases. Biochem Biophys Res Commun 427: 165-170.
56. Riemann A, Schneider B, Ihling A, Nowak M, Sauvant C, et al. (2011) Acidic environment leads to ROS-induced MAPK signaling in cancer cells. PLoS One 6: e22445.
57. Hsu WH, Hsieh YS, Kuo HC, Teng CY, Huang HI, et al. (2007) Berberine induces apoptosis in SW620 human colonic carcinoma cells through generation of reactive oxygen species and activation of JNK/p38 MAPK and FasL. Arch Toxicol 81: 719-728.