About this Journal Submit a Manuscript Table of Contents
Journal of Ophthalmology
Volume 2010 (2010), Article ID 746978, 10 pages
http://dx.doi.org/10.1155/2010/746978
Research Article

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.

Linked References

  1. 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. View at Publisher · View at Google Scholar · View at Scopus
  2. 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. View at Scopus
  3. 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. View at Scopus
  4. 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. View at Publisher · View at Google Scholar · View at Scopus
  5. 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. View at Publisher · View at Google Scholar · View at Scopus
  6. R. A. Kowluru and P.-S. Chan, “Oxidative stress and diabetic retinopathy,” Experimental Diabetes Research, vol. 2007, pp. 1–12, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. R. P. Brandes and J. Kreuzer, “Vascular NADPH oxidases: molecular mechanisms of activation,” Cardiovascular Research, vol. 65, no. 1, pp. 16–27, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. 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. View at Scopus
  11. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. 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. View at Publisher · View at Google Scholar · View at Scopus
  13. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. 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.
  16. 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.
  17. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. 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. View at Scopus
  19. 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. View at Publisher · View at Google Scholar · View at Scopus
  20. 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. View at Scopus
  21. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. 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. View at Scopus
  23. 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. View at Publisher · View at Google Scholar · View at Scopus
  24. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. 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. View at Publisher · View at Google Scholar · View at Scopus
  26. 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. View at Scopus
  27. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. 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. View at Scopus
  31. 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. View at Publisher · View at Google Scholar · View at Scopus
  32. 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. View at Scopus
  33. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. 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. View at Publisher · View at Google Scholar · View at Scopus
  35. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. 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. View at Scopus
  38. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. 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. View at Publisher · View at Google Scholar · View at Scopus
  43. 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. View at Publisher · View at Google Scholar · View at Scopus
  44. 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. View at Publisher · View at Google Scholar · View at Scopus
  45. 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. View at Scopus
  46. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. 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. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Nagai, K. Ikeda, T. Higashi, H. Sano, Y. Jinnouchi, T. Araki, and S. Horiuchi, “Hydroxyl radical mediates Nε-(carboxymethyl)lysine formation from Amadori product,” Biochemical and Biophysical Research Communications, vol. 234, no. 1, pp. 167–172, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. 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. View at Publisher · View at Google Scholar · View at Scopus
  50. 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. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. 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. View at Publisher · View at Google Scholar · View at Scopus
  52. 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. View at Publisher · View at Google Scholar · View at Scopus