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Journal of Ophthalmology
Volume 2010 (2010), Article ID 746978, 10 pages
NADPH Oxidase versus Mitochondria-Derived ROS in Glucose-Induced Apoptosis of Pericytes in Early Diabetic Retinopathy
1Forest Research Institute Malaysia (FRIM), 52109 Kepong, Selangor Darul Ehsan, Malaysia
2Cardiovascular Division, GKT School of Biomedical & Health Sciences, King's College London, Guy's Campus, London SE1 1UL, UK
3Institute of Biomedical and Clinical Science, Peninsula College of Medicine and Dentistry, Peninsula Medical School, St Luke's Campus, Exeter EX1 2LU, UK
Received 1 January 2010; Revised 29 March 2010; Accepted 23 April 2010
Academic Editor: Renu A. Kowluru
Copyright © 2010 Nik M. Mustapha et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- D. S. Fong, L. P. Aiello, F. L. Ferris III, and R. Klein, “Diabetic retinopathy,” Diabetes Care, vol. 27, no. 10, pp. 2540–2553, 2004.
- M. Mizutani, T. S. Kern, and M. Lorenzi, “Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy,” Journal of Clinical Investigation, vol. 97, no. 12, pp. 2883–2890, 1996.
- T. S. Kern, J. Tang, and J. Tang, “Response of capillary cell death to aminoguanidine predicts the development of retinopathy: comparison of diabetes and galactosemia,” Investigative Ophthalmology and Visual Science, vol. 41, no. 12, pp. 3972–3978, 2000.
- Diabetes Control and Complications Trial Research Group, “The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus,” The New England Journal of Medicine, vol. 329, no. 14, pp. 977–986, 1993.
- UK Prospective Diabetes Study (UKPDS) Group, “Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33),” The Lancet, vol. 352, no. 9131, pp. 837–853, 1998.
- R. A. Kowluru and P.-S. Chan, “Oxidative stress and diabetic retinopathy,” Experimental Diabetes Research, vol. 2007, pp. 1–12, 2007.
- D. M. Niedowicz and D. L. Daleke, “The role of oxidative stress in diabetic complications,” Cell Biochemistry and Biophysics, vol. 43, no. 2, pp. 289–330, 2005.
- T. Nishikawa, D. Edelstein, and D. Edelstein, “Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage,” Nature, vol. 404, no. 6779, pp. 787–790, 2000.
- R. P. Brandes and J. Kreuzer, “Vascular NADPH oxidases: molecular mechanisms of activation,” Cardiovascular Research, vol. 65, no. 1, pp. 16–27, 2005.
- J. Stolk, T. J. Hiltermann, J. H. Dijkman, and A. J. Verhoeven, “Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol,” American Journal of Respiratory Cell and Molecular Biology, vol. 11, no. 1, pp. 95–102, 1994.
- A. M. James, H. M. Cochemé, and M. P. Murphy, “Mitochondria-targeted redox probes as tools in the study of oxidative damage and ageing,” Mechanisms of Ageing and Development, vol. 126, no. 9, pp. 982–986, 2005.
- 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, vol. 40, no. 2, pp. 156–164, 1997.
- V. Gurtu, S. R. Kain, and G. Zhang, “Fluorometric and colorimetric detection of caspase activity associated with apoptosis,” Analytical Biochemistry, vol. 251, no. 1, pp. 98–102, 1997.
- H. Zhao, J. Joseph, H. M. Fales, E. A. Sokoloski, R. L. Levine, J. Vasquez-Vivar, and B. Kalyanaraman, “Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 16, pp. 5727–5732, 2005.
- W. O. Carter, P. K. Narayanan, and J. P. Robinson, “Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells,” Journal of Leukocyte Biology, vol. 55, no. 2, pp. 253–258, 1994.
- R. Chibber, P. A. Molinatti, and E. M. Kohner, “Intracellular protein glycation in cultured retinal capillary pericytes and endothelial cells exposed to high-glucose concentration,” Cellular and Molecular Biology, vol. 45, no. 1, pp. 47–57, 1999.
- E. Beltramo, E. Berrone, S. Buttiglieri, and M. Porta, “Thiamine and benfotiamine prevent increased apoptosis in endothelial cells and pericytes cultured in high glucose,” Diabetes/Metabolism Research and Reviews, vol. 20, no. 4, pp. 330–336, 2004.
- A. Manea, E. Constantinescu, D. Popov, and M. Raicu, “Changes in oxidative balance in rat pericytes exposed to diabetic conditions,” Journal of Cellular and Molecular Medicine, vol. 8, no. 1, pp. 117–126, 2004.
- R. A. Kowluru and P. Koppolu, “Diabetes-induced activation of caspase-3 in retina: effect of antioxidant therapy,” Free Radical Research, vol. 36, no. 9, pp. 993–999, 2002.
- F. Pomero, A. Allione, and A. Allione, “Effects of protein kinase C inhibition and activation on proliferation and apoptosis of bovine retinal pericytes,” Diabetologia, vol. 46, no. 3, pp. 416–419, 2003.
- A. M. Abu El-Asrar, L. Dralands, L. Missotten, I. A. Al-Jadaan, and K. Geboes, “Expression of apoptosis markers in the retinas of human subjects with diabetes,” Investigative Ophthalmology and Visual Science, vol. 45, no. 8, pp. 2760–2766, 2004.
- S. Mohr, X. Xi, J. Tang, and T. S. Kern, “Caspase activation in retinas of diabetic and galactosemic mice and diabetic patients,” Diabetes, vol. 51, no. 4, pp. 1172–1179, 2002.
- J. M. Cacicedo, S. Benjachareowong, E. Chou, N. B. Ruderman, and Y. Ido, “Palmitate-induced apoptosis in cultured bovine retinal pericytes: roles of NAD(P)H oxidase, oxidant stress, and ceramide,” Diabetes, vol. 54, no. 6, pp. 1838–1845, 2005.
- A. Manea, M. Raicu, and M. Simionescu, “Expression of functionally phagocyte-type NAD(P)H oxidase in pericytes: effect of angiotensin II and high glucose,” Biology of the Cell, vol. 97, no. 9, pp. 723–734, 2005.
- G. Cheng, Z. Cao, X. Xu, E. G. van Meir, and J. D. Lambeth, “Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5,” Gene, vol. 269, no. 1-2, pp. 131–140, 2001.
- U. Bayraktutan, L. Blayney, and A. M. Shah, “Molecular characterization and localization of the NAD(P)H oxidase components gp91-phox and p22-phox in endothelial cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 8, pp. 1903–1911, 2000.
- J.-M. Li and A. M. Shah, “Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells,” Journal of Biological Chemistry, vol. 277, no. 22, pp. 19952–19960, 2002.
- K. Asaba, A. Tojo, M. L. Onozato, A. Goto, M. T. Quinn, T. Fujita, and C. S. Wilcox, “Effects of NADPH oxidase inhibitor in diabetic nephropathy,” Kidney International, vol. 67, no. 5, pp. 1890–1898, 2005.
- T. Etoh, T. Inoguchi, and T. Inoguchi, “Increased expression of NAD(P)H oxidase subunits, NOX4 and p22phox, in the kidney of streptozotocin-induced diabetic rats and its reversibity by interventive insulin treatment,” Diabetologia, vol. 46, no. 10, pp. 1428–1437, 2003.
- T. J. Guzik, N. E. West, E. Black, D. McDonald, C. Ratnatunga, R. Pillai, and K. M. Channon, “Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors,” Circulation Research, vol. 86, no. 9, pp. E85–E90, 2000.
- P. Mohanty, W. Hamouda, R. Garg, A. Aljada, H. Ghanim, and P. Dandona, “Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes,” Journal of Clinical Endocrinology and Metabolism, vol. 85, no. 8, pp. 2970–2973, 2000.
- T. Inoguchi, P. Li, and P. Li, “High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells,” Diabetes, vol. 49, no. 11, pp. 1939–1945, 2000.
- T. E. DeCoursey and E. Ligeti, “Regulation and termination of NADPH oxidase activity,” Cellular and Molecular Life Sciences, vol. 62, no. 19-20, pp. 2173–2193, 2005.
- A. Fontayne, P. M.-C. Dang, M.-A. Gougerot-Pocidalo, and J. El Benna, “Phosphorylation of p47phox sites by PKC α, βII, δ, and ζ: effect on binding to p22phox and on NADPH oxidase activation,” Biochemistry, vol. 41, no. 24, pp. 7743–7750, 2002.
- C.-D. Agardh, B. Hultberg, R. C. Nayak, P. Farthing-Nayak, and E. Agardh, “Bovine retinal pericytes are resistant to glucose-induced oxidative stress in vitro,” Antioxidants and Redox Signaling, vol. 7, no. 11-12, pp. 1486–1493, 2005.
- N. Ouslimani, J. Peynet, D. Bonnefont-Rousselot, P. Thérond, A. Legrand, and J.-L. Beaudeux, “Metformin decreases intracellular production of reactive oxygen species in aortic endothelial cells,” Metabolism, vol. 54, no. 6, pp. 829–834, 2005.
- A. Tawfik, T. Sanders, K. Kahook, S. Akeel, A. Elmarakby, and M. Al-Shabrawey, “Suppression of retinal peroxisome proliferator-activated receptor gamma in experimental diabetes and oxygen-induced retinopathy: role of NADPH oxidase,” Investigative Ophthalmology & Visual Science, vol. 50, no. 2, pp. 878–884, 2009.
- M. Al-Shabrawey, M. Rojas, and M. Rojas, “Role of NADPH oxidase in retinal vascular inflammation,” Investigative Ophthalmology and Visual Science, vol. 49, no. 7, pp. 3239–3244, 2008.
- M. Al-Shabrawey, M. Bartoli, and M. Bartoli, “Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy,” Investigative Ophthalmology and Visual Science, vol. 49, no. 7, pp. 3231–3238, 2008.
- M. Yano, G. Hasegawa, M. Ish II, M. Yamasaki, M. Fukui, N. Nakamura, and T. Yoshikawa, “Short-term exposure of high glucose concentration induces generation of reactive oxygen species in endothelial cells: implication for the oxidative stress associated with postprandial hyperglycemia,” Redox Report, vol. 9, no. 2, pp. 111–116, 2004.
- A. Tojo, K. Asaba, and M. L. Onozato, “Suppressing renal NADPH oxidase to treat diabetic nephropathy,” Expert Opinion on Therapeutic Targets, vol. 11, no. 8, pp. 1011–1018, 2007.
- K. Susztak, A. C. Raff, M. Schiffer, and E. P. Böttinger, “Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy,” Diabetes, vol. 55, no. 1, pp. 225–233, 2006.
- R. M. Kluck, E. Bossy-Wetzel, D. R. Green, and D. D. Newmeyer, “The release of cytochrome c from mitochondria: a primary site for Bcl- 2 regulation of apoptosis,” Science, vol. 275, no. 5303, pp. 1132–1136, 1997.
- M. M. Anderson and J. W. Heinecke, “Production of Nε-(carboxymethyl)lysine is impaired in mice deficient in NADPH oxidase: a role for phagocyte-derived oxidants in the formation of advanced glycation end products during inflammation,” Diabetes, vol. 52, no. 8, pp. 2137–2143, 2003.
- E. D. Schleicher, E. Wagner, and A. G. Nerlich, “Increased accumulation of the glycoxidation product N(ε)- (carboxymethyl)lysine in human tissues in diabetes and aging,” Journal of Clinical Investigation, vol. 99, no. 3, pp. 457–468, 1997.
- E. Berrone, E. Beltramo, C. Solimine, A. U. Ape, and M. Porta, “Regulation of intracellular glucose and polyol pathway by thiamine and benfotiamine in vascular cells cultured in high glucose,” Journal of Biological Chemistry, vol. 281, no. 14, pp. 9307–9313, 2006.
- J.-Z. Zhang, L. Gao, M. Widness, X. Xi, and T. S. Kern, “Captopril inhibits glucose accumulation in retinal cells in diabetes,” Investigative Ophthalmology and Visual Science, vol. 44, no. 9, pp. 4001–4005, 2003.
- R. Nagai, K. Ikeda, T. Higashi, H. Sano, Y. Jinnouchi, T. Araki, and S. Horiuchi, “Hydroxyl radical mediates -(carboxymethyl)lysine formation from Amadori product,” Biochemical and Biophysical Research Communications, vol. 234, no. 1, pp. 167–172, 1997.
- K. J. Wells-Knecht, D. V. Zyzak, J. E. Litchfield, S. R. Thorpe, and J. W. Baynes, “Mechanism of autoxidative glycosylation: identification of glyoxal and arabinose as intermediates in the autoxidative modification of proteins by glucose,” Biochemistry, vol. 34, no. 11, pp. 3702–3709, 1995.
- D. Cervantes-Laurean, M. J. Roberts, E. L. Jacobson, and M. K. Jacobson, “Nuclear proteasome activation and degradation of carboxymethylated histones in human keratinocytes following glyoxal treatment,” Free Radical Biology and Medicine, vol. 38, no. 6, pp. 786–795, 2005.
- 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, vol. 42, no. 6, pp. 728–736, 1999.
- H.-P. Hammes, M. Brownlee, J. Lin, E. Schleicher, and R. G. Bretzel, “Diabetic retinopathy risk correlates with intracellular concentrations of the glycoxidation product Nε-(carboxymethyl) lysine independently of glycohaemoglobin concentrations,” Diabetologia, vol. 42, no. 5, pp. 603–607, 1999.