Advanced glycation end products induce death of retinal neurons via activation of nitric oxide synthase

Experimental Eye Research

Volumn 81, Issue 6, 2005, Pages 647-654

  Kobayashi, Takatoshi ^a   Oku, Hidehiro ^a   Komori, Asako ^a   Okuno, Takashi ^a   Kojima, Shota ^a   Obayashi, Hiroshi ^b   Sugiyama, Tetsuya ^a   Hasegawa, Goji ^c   Fukui, Michiaki ^c   Nakamura, Naoto ^c   Ikeda, Tsunehiko ^a  

^a OSAKA MEDICAL COLLEGE   (Japan)

^b Institute of Bio Response Informatics   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Advanced glycation end products; Cultured retinal neurons; Immunohistochemistry; Nitric oxide synthase; Rat

Indexed keywords

3 NITROTYROSINE; ADVANCED GLYCATION END PRODUCT; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; TRYPAN BLUE;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVATION; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INCUBATION TIME; NEUROTOXICITY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; RETINA AMACRINE CELL; RETINA NERVE CELL;

AMACRINE CELLS; ANIMALS; CASPASE 3; CASPASES; CELL DEATH; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; GLYCOSYLATION END PRODUCTS, ADVANCED; IN SITU NICK-END LABELING; NEURONS; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RATS; RATS, WISTAR; RETINA; TYROSINE;

EID: 29044450538     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2005.04.001     Document Type: Article

References (40)

1. A.J. Barber, E. Lieth, S.A. Khin, D.A. Antonetti, A.G. Buchanan, and T.W. Gardner Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin J. Clin. Invest. 102 1998 783 791
2. B. Beltran, A. Mathur, M.R. Duchen, J.D. Erusalimsky, and S. Moncada The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death Proc. Natl Acad. Sci. USA 97 2000 14602 14607
3. V. Borutaite, and G.C. Brown Nitric oxide induces apoptosis via hydrogen peroxide, but necrosis via energy and thiol depletion Free Radic. Biol. Med. 35 2003 1457 1468
4. M. Brownlee Advanced protein glycosylation in diabetes and aging Annu. Rev. Med. 46 1995 223 234
5. S. Cellek, N.A. Foxwell, and S. Moncada Two phases of nitrergic neuropathy in streptozotocin-induced diabetic rats Diabetes 52 2003 2353 2362
6. S. Cellek, W. Qu, A.M. Schmidt, and S. Moncada Synergistic action of advanced glycation end products and endogenous nitric oxide leads to neuronal apoptosis in vitro: a new insight into selective nitrergic neuropathy in diabetes Diabetologia 47 2004 331 339
7. U. Chakravarthy, R.G. Hayes, A.W. Stitt, E. McAuley, and D.B. Archer Constitutive nitric oxide synthase expression in retinal vascular endothelial cells is suppressed by high glucose and advanced glycation end products Diabetes 47 1998 945 952
8. R. Chibber, P.A. Molinatti, N. Rosatto, B. Lambourne, and E.M. Kohner Toxic action of advanced glycation end products on cultured retinal capillary pericytes and endothelial cells: relevance to diabetic retinopathy Diabetologia 40 1997 156 164
9. R.S. Clements Jr, W.G. Robison Jr, and M.P. Cohen Anti-glycated albumin therapy ameliorates early retinal microvascular pathology in db/db mice J. Diabetes Complications 12 1998 28 33
10. U. Denis, M. Lecomte, C. Paget, D. Ruggiero, N. Wiernsperger, and M. Lagarde Advanced glycation end-products induce apoptosis of bovine retinal pericytes in culture: involvement of diacylglycerol/ceramide production and oxidative stress induction Free Radic. Biol. Med. 33 2002 236 247
11. H.P. Hammes, A. Alt, T. Niwa, J.T. Clausen, R.G. Bretzel, M. Brownlee, and E.D. Schleicher Differential accumulation of advanced glycation end products in the course of diabetic retinopathy Diabetologia 42 1999 728 736
12. Y.Y. Hui, W.C. McAmis, J.W. Baynes, R.C. Schaeffer Jr, and M.B. Wolf Effect of advanced glycation end products on oxidative stress in endothelial cells in culture: a warning on the use of cells studied in serum-free media Diabetologia 44 2001 1310 1317
13. S. Kashii, M. Takahashi, M. Mandai, H. Shimizu, Y. Honda, M. Sasa, H. Ujihara, Y. Tamura, T. Yokota, and A. Akaike Protective action of dopamine against glutamate neurotoxicity in the retina Invest. Ophthalmol. Vis. Sci. 35 1994 685 695
14. T.S. Kern, and R.L. Engerman Pharmacological inhibition of diabetic retinopathy: aminoguanidine and aspirin Diabetes 50 2001 1636 1642
15. B.K. Kilhovd, T.J. Berg, K.I. Birkeland, P. Thorsby, and K.F. Hanssen Serum levels of advanced glycation end products are increased in patients with type 2 diabetes and coronary heart disease Diabetes Care 22 1999 1543 1548
16. E.J. Lee, K.Y. Kim, T.H. Gu, J.I. Moon, I.B. Kim, M.Y. Lee, S.J. Oh, and M.H. Chun Neuronal nitric oxide synthase is expressed in the axotomized ganglion cells of the rat retina Brain Res. 986 2003 174 180
17. Q. Li, E. Zemel, B. Miller, and I. Perlman NADPH diaphorase activity in the rat retina during the early stages of experimental diabetes Graefes Arch. Clin. Exp. Ophthalmol. 241 2003 747 756
18. S.A. Lipton, Y.B. Choi, Z.H. Pan, S.Z. Lei, H.S. Chen, N.J. Sucher, J. Loscalzo, D.J. Singel, and J.S. Stamler A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds Nature 364 1993 626 632
19. C. Loske, A. Neumann, A.M. Cunningham, K. Nichol, R. Schinzel, P. Riederer, and G. Munch Cytotoxicity of advanced glycation endproducts is mediated by oxidative stress J. Neural Transm. 105 1998 1005 1015
20. M. Lu, M. Kuroki, S. Amano, M. Tolentino, K. Keough, I. Kim, R. Bucala, and A.P. Adamis Advanced glycation end products increase retinal vascular endothelial growth factor expression J. Clin. Invest. 101 1998 1219 1224
21. L. Ma, R.J. Carter, A.J. Morton, and L.F. Nicholson RAGE is expressed in pyramidal cells of the hippocampus following moderate hypoxic-ischemic brain injury in rats Brain Res. 966 2003 167 174
22. S. Moncada, and J.D. Erusalimsky Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3 2002 214 220
23. T.C. Moore, J.E. Moore, Y. Kaji, N. Frizzell, T. Usui, V. Poulaki, I.L. Campbell, A.W. Stitt, T.A. Gardiner, D.B. Archer, and A.P. Adamis The role of advanced glycation end products in retinal microvascular leukostasis Invest. Ophthalmol. Vis. Sci. 44 2003 4457 4464
24. H. Obayashi, K. Nakano, H. Shigeta, M. Yamaguchi, K. Yoshimori, M. Fukui, M. Fujii, Y. Kitagawa, N. Nakamura, K. Nakamura, Y. Nakazawa, K. Ienaga, M. Ohta, M. Nishimura, I. Fukui, and M. Kondo Formation of crossline as a fluorescent advanced glycation end product in vitro and in vivo Biochem. Biophys. Res. Commun. 226 1996 37 41
25. T.M. Osicka, Y. Yu, V. Lee, S. Panagiotopoulos, B.E. Kemp, and G. Jerums Aminoguanidine and ramipril prevent diabetes-induced increases in protein kinase C activity in glomeruli, retina and mesenteric artery Clin. Sci. (London) 100 2001 249 257
26. M. Palacios-Callender, M. Quintero, V.S. Hollis, R.J. Springett, and S. Moncada Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase Proc. Natl Acad. Sci. USA 101 2004 7630 7635
27. F. Reber, M. Kasper, A. Siegner, E. Kniep, G. Seigel, and R.H. Funk Alteration of the intracellular pH and apoptosis induction in a retinal cell line by the AGE-inducing agent glyoxal Graefes Arch. Clin. Exp. Ophthalmol. 240 2002 1022 1032
28. F. Reber, R. Geffarth, M. Kasper, A. Reichenbach, E.D. Schleicher, A. Siegner, and R.H. Funk Graded sensitiveness of the various retinal neuron populations on the glyoxal-mediated formation of advanced glycation end products and ways of protection Graefes Arch. Clin. Exp. Ophthalmol. 241 2003 213 225
29. G. Sajithlal, H. Huttunen, H. Rauvala, and G. Munch Receptor for advanced glycation end products plays a more important role in cellular survival than in neurite outgrowth during retinoic acid-induced differentiation of neuroblastoma cells J. Biol. Chem. 277 2002 6888 6897
30. R.E. Schmidt, D.A. Dorsey, L.N. Beaudet, K.M. Reiser, J.R. Williamson, and R.G. Tilton Effect of aminoguanidine on the frequency of neuroaxonal dystrophy in the superior mesenteric sympathetic autonomic ganglia of rats with streptozocin-induced diabetes Diabetes 45 1996 284 290
31. M.M. Sousa, S. Du Yan, R. Fernandes, A. Guimaraes, D. Stern, and M.J. Saraiva Familial amyloid polyneuropathy: receptor for advanced glycation end products-dependent triggering of neuronal inflammatory and apoptotic pathways J. Neurosci. 21 2001 7576 7586
32. A.W. Stitt, Y.M. Li, T.A. Gardiner, R. Bucala, D.B. Archer, and H. Vlassara Advanced glycation end products (AGEs) co-localize with AGE receptors in the retinal vasculature of diabetic and of AGE-infused rats Am. J. Pathol. 150 1997 523 531
33. A.W. Stitt, T. Bhaduri, C.B. McMullen, T.A. Gardiner, and D.B. Archer Advanced glycation end products induce blood-retinal barrier dysfunction in normoglycemic rats Mol. Cell Biol. Res. Commun. 3 2000 380 388
34. A.W. Stitt, T.A. Gardiner, N.L. Alderson, P. Canning, N. Frizzell, N. Duffy, C. Boyle, A.S. Januszewski, M. Chachich, J.W. Baynes, and S.R. Thorpe The AGE inhibitor pyridoxamine inhibits development of retinopathy in experimental diabetes Diabetes 51 2002 2826 2832
35. M. Takeuchi, R. Bucala, T. Suzuki, T. Ohkubo, M. Yamazaki, T. Koike, Y. Kameda, and Z. Makita Neurotoxicity of advanced glycation end-products for cultured cortical neurons J. Neuropathol. Exp. Neurol. 59 2000 1094 1105
36. R.G. Tilton, K. Chang, K.S. Hasan, S.R. Smith, J.M. Petrash, T.P. Misko, W.M. Moore, M.G. Currie, J.A. Corbett, and M.L. McDaniel Prevention of diabetic vascular dysfunction by guanidines. Inhibition of nitric oxide synthase versus advanced glycation end-product formation Diabetes 42 1993 221 232
37. C. Treins, S. Giorgetti-Peraldi, J. Murdaca, and E. Van Obberghen Regulation of vascular endothelial growth factor expression by advanced glycation end products J. Biol. Chem. 276 2001 43836 43841
38. S. Yamagishi, S. Amano, Y. Inagaki, T. Okamoto, K. Koga, N. Sasaki, H. Yamamoto, M. Takeuchi, and Z. Makita Advanced glycation end products-induced apoptosis and overexpression of vascular endothelial growth factor in bovine retinal pericytes Biochem. Biophys. Res. Commun. 25 2002 973 978
39. H.W. Yung, A.K. Bal-Price, G.C. Brown, and A.M. Tolkovsky Nitric oxide-induced cell death of cerebrocortical murine astrocytes is mediated through p53- and Bax-dependent pathways J. Neurochem. 89 2004 812 821
40. N. Zamzami, P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S.A. Susin, P.X. Petit, B. Mignotte, and G. Kroemer Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death J. Exp. Med. 182 1995 367 377