Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2013 (2013), Article ID 510451, 10 pages
http://dx.doi.org/10.1155/2013/510451
Research Article

Poly (ADP-Ribose) Polymerase Mediates Diabetes-Induced Retinal Neuropathy

Department of Ophthalmology, College of Medicine, King Saud University, P.O. Box 245, Riyadh 11411, Saudi Arabia

Received 4 August 2013; Revised 30 October 2013; Accepted 3 November 2013

Academic Editor: Dorota Raczynska

Copyright © 2013 Ghulam Mohammad 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. M. Seki, T. Tanaka, H. Nawa et al., “Involvement of brain-derived neurotrophic factor in early retinal neuropathy of streptozotocin-induced diabetes in rats: therapeutic potential of brain-derived neurotrophic factor for dopaminergic amacrine cells,” Diabetes, vol. 53, no. 9, pp. 2412–2419, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. A. J. Barber, “A new view of diabetic retinopathy: a neurodegenerative disease of the eye,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 27, no. 2, pp. 283–290, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Sasaki, Y. Ozawa, T. Kurihara et al., “Neurodegenerative influence of oxidative stress in the retina of a murine model of diabetes,” Diabetologia, vol. 53, no. 5, pp. 971–979, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Simó, C. Hernández, and European consortium for the early treatment of diabetic retinopathy (EUROCONDOR), “Neurodegeneration is an early event in diabetic retinopathy: therapeutic implications,” British Journal of Ophthalmology, vol. 96, no. 10, pp. 1285–1290, 2012. View at Publisher · View at Google Scholar
  5. J. M. Santos, G. Mohammad, Q. Zhong, and R. A. Kowluru, “Diabetic retinopathy, superoxide damage and antioxidants,” Current Pharmaceutical Biotechnology, vol. 12, no. 3, pp. 352–361, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. R. A. Kowluru and M. Kanwar, “Effects of curcumin on retinal oxidative stress and inflammation in diabetes,” Nutrition and Metabolism, vol. 4, article 8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. R. A. Kowluru, B. Menon, and D. L. Gierhart, “Beneficial effect of zeaxanthin on retinal metabolic abnormalities in diabetic rats,” Investigative Ophthalmology and Visual Science, vol. 49, no. 4, pp. 1645–1651, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Mohammad and R. A. Kowluru, “Matrix metalloproteinase-2 in the development of diabetic retinopathy and mitochondrial dysfunction,” Laboratory Investigation, vol. 90, no. 9, pp. 1365–1372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Zong, M. Ward, and A. W. Stitt, “AGEs, RAGE, and diabetic retinopathy,” Current Diabetes Reports, vol. 11, no. 4, pp. 244–252, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. K. C. Silva, M. A. B. Rosales, S. K. Biswas, J. B. L. De Faria, and J. M. L. De Faria, “Diabetic retinal neurodegeneration is associated with mitochondrial oxidative stress and is improved by an angiotensin receptor blocker in a model combining hypertension and diabetes,” Diabetes, vol. 58, no. 6, pp. 1382–1390, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Seki, H. Nawa, T. Fukuchi, H. Abe, and N. Takei, “BDNF is upregulated by postnatal development and visual experience: quantitative and immunohistochemical analyses of BDNF in the rat retina,” Investigative Ophthalmology and Visual Science, vol. 44, no. 7, pp. 3211–3218, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. K. R. G. Martin, H. A. Quigley, D. J. Zack et al., “Gene therapy with brain-derived neurotrophic factor as a protection: retinal ganglion cells in a rat glaucoma model,” Investigative Ophthalmology and Visual Science, vol. 44, no. 10, pp. 4357–4365, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. D. K. Binder and H. E. Scharfman, “Brain-derived neurotrophic factor,” Growth Factors, vol. 22, no. 3, pp. 123–131, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. T. C. Nag and S. Wadhwa, “Differential expression of syntaxin-1 and synaptophysin in the developing and adult human retina,” Journal of Biosciences, vol. 26, no. 2, pp. 179–191, 2001. View at Google Scholar · View at Scopus
  15. T. Kivela, A. Tarkkanen, and I. Virtanen, “Synaptophysin in the human retina and retinoblastoma. An immunohistochemical and Western blotting study,” Investigative Ophthalmology and Visual Science, vol. 30, no. 2, pp. 212–219, 1989. View at Google Scholar · View at Scopus
  16. S. C. Massey, “Cell types using glutamate as a neurotransmitter in the vertebrate retina,” Progress in Retinal Research, vol. 9, pp. 399–425, 1990. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Lieth, K. F. LaNoue, D. A. Antonetti, and M. Ratz, “Diabetes reduces glutamate oxidation and glutamine synthesis in the retina,” Experimental Eye Research, vol. 70, no. 6, pp. 723–730, 2000. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Xu-hui, Z. Hong, W. Yu-hong, L. Li-juan, T. Yan, and L. Ping, “Time-dependent reduction of glutamine synthetase in retina of diabetic rats,” Experimental Eye Research, vol. 89, no. 6, pp. 967–971, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Lieth, A. J. Barber, B. Xu et al., “Glial reactivity and impaired glutamate metabolism in short- term experimental diabetic retinopathy,” Diabetes, vol. 47, pp. 815–820, 1998. View at Google Scholar · View at Scopus
  20. R. A. Kowluru, R. L. Engerman, G. L. Case, and T. S. Kern, “Retinal glutamate in diabetes and effect of antioxidants,” Neurochemistry International, vol. 38, no. 5, pp. 385–390, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Ozawa, T. Kurihara, M. Sasaki et al., “Neural degeneration in the retina of the streptozotocin-induced type 1 diabetes model,” Experimental Diabetes Research, vol. 2011, Article ID 108328, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Zheng, C. Szabó, and T. S. Kern, “Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-κB,” Diabetes, vol. 53, no. 11, pp. 2960–2967, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Sugawara, T. Hikichi, N. Kitaya et al., “Peroxynitrite decomposition catalyst, FP15, and poly(ADP-ribose) polymerase inhibitor, PJ34, inhibit leukocyte entrapment in the retinal microcirculation of diabetic rats,” Current Eye Research, vol. 29, no. 1, pp. 11–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. X. Qin, Z. Zhang, H. Xu, and Y. Wu, “Notch signaling protects retina from nuclear factor-κB- and poly-ADP-ribose-polymerase-mediated apoptosis under high-glucose stimulation,” Acta Biochimica et Biophysica Sinica, vol. 43, no. 9, pp. 703–711, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. I. G. Obrosova and U. A. Julius, “Role for poly(ADP-ribose) polymerase activation in diabetic nephropathy, neuropathy and retinopathy,” Current Vascular Pharmacology, vol. 3, no. 3, pp. 267–283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. I. G. Obrosova, V. R. Drel, P. Pacher et al., “Oxidative-nitrosative stress and poly(ADP-ribose) polymerase (PARP) activation in experimental diabetic neuropathy: the relation is revisited,” Diabetes, vol. 54, no. 12, pp. 3435–3441, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Lupachyk, H. Shevalye, Y. Maksimchyk, V. R. Drel, and I. G. Obrosova, “PARP inhibition alleviates diabetes-induced systemic oxidative stress and neural tissue 4-hydroxynonenal adduct accumulation: correlation with peripheral nerve function,” Free Radical Biology and Medicine, vol. 50, no. 10, pp. 1400–1409, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. I. G. Obrosova, A. G. Minchenko, R. N. Frank et al., “Poly(ADP-ribose) polymerase inhibitors counteract diabetes- and hypoxia-induced retinal vascular endothelial growth factor overexpression,” International journal of molecular medicine, vol. 14, no. 1, pp. 55–64, 2004. View at Google Scholar · View at Scopus
  29. B. Dasari, J. R. Prasanthi, G. Marwarha, B. B. Singh, and O. Ghribi, “Cholesterol-enriched diet causes age-related macular degeneration-like pathology in rabbit retina,” BMC Ophthalmology, vol. 11, no. 1, article 22, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Cotter and N. E. Cameron, “Effect of the NAD(P)H oxidase inhibitor, apocynin, on peripheral nerve perfusion and function in diabetic rats,” Life Sciences, vol. 73, no. 14, pp. 1813–1824, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. P. Jagtap and C. Szabo, “Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors,” Nature Reviews Drug Discovery, vol. 4, no. 5, pp. 421–440, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. I. G. Obrosova, V. R. Drel, A. K. Kumagai, C. Szábo, P. Pacher, and M. J. Stevens, “Early diabetes-induced biochemical changes in the retina: comparison of rat and mouse models,” Diabetologia, vol. 49, no. 10, pp. 2525–2533, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. Z. Zheng, H. Chen, H. Wang et al., “Improvement of retinal vascular injury in diabetic rats by statins is associated with the inhibition of mitochondrial reactive oxygen species pathway mediated by peroxisome proliferator-activated receptor γ coactivator 1α,” Diabetes, vol. 59, no. 9, pp. 2315–2325, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. Z. H. Wan, W. Z. Li, Y. Z. Li et al., “Poly(ADP-Ribose) polymerase inhibition improves erectile function in diabetic rats,” Journal of Sexual Medicine, vol. 8, no. 4, pp. 1002–1014, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Szabó, A. Biser, R. Benko, E. Böttinger, and K. Suszták, “Poly(ADP-ribose) polymerase inhibitors ameliorate nephropathy of type 2 diabetic Leprdb/db mice,” Diabetes, vol. 55, no. 11, pp. 3004–3012, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. M. S. Ola, M. I. Nawaz, H. A. Khan, and A. S. Alhomida, “Neurodegeneration and neuroprotection in diabetic retinopathy,” International Journal of Molecular Sciences, vol. 14, no. 2, pp. 2559–2572, 2013. View at Publisher · View at Google Scholar
  37. X. Ye, G. Xu, Q. Chang et al., “ERK1/2 signaling pathways involved in VEGF release in diabetic rat retina,” Investigative Ophthalmology and Visual Science, vol. 51, no. 10, pp. 5226–5233, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Mohammad, M. Siddiquei, M. Imtiaz Nawaz, and A. M. Abu El-Asrar, “The ERK1/2 inhibitor U0126 attenuates diabetes-induced upregulation of MMP-9 and biomarkers of inflammation in the retina,” Journal of Diabetes Research, vol. 2013, Article ID 658548, 9 pages, 2013. View at Publisher · View at Google Scholar
  39. M. Domercq, S. Mato, F. N. Soria, M. V. Sánchez-gómez, E. Alberdi, and C. Matute, “Zn2+ -induced ERK activation mediates PARP-1-dependent ischemic-reoxygenation damage to oligodendrocytes,” Glia, vol. 61, no. 3, pp. 383–393, 2013. View at Publisher · View at Google Scholar
  40. T. T. T. Nguyen, E. Tran, T. H. Nguyen, P. T. Do, T. H. Huynh, and H. Huynh, “The role of activated MEK-ERK pathway in quercetin-induced growth inhibition and apoptosis in A549 lung cancer cells,” Carcinogenesis, vol. 25, no. 5, pp. 647–659, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Liu, W. Mao, B. Ding, and C.-S. Liang, “ERKs/p53 signal transduction pathway is involved in doxorubicin-induced apoptosis in H9c2 cells and cardiomyocytes,” The American Journal of Physiology: Heart and Circulatory Physiology, vol. 295, no. 5, pp. H1956–H1965, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Yang, Y. Han, H. Sun et al., “(-)-Epigallocatechin gallate suppresses proliferation of vascular smooth muscle cells induced by high glucose by inhibition of PKC and ERK1/2 signalings,” Journal of Agricultural and Food Chemistry, vol. 59, no. 21, pp. 11483–11490, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Stenberg, M. Kanje, L. Mårtensson, and L. B. Dahlin, “Injury-induced activation of ERK 1/2 in the sciatic nerve of healthy and diabetic rats,” NeuroReport, vol. 22, no. 2, pp. 73–77, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Mohammad and R. A. Kowluru, “Diabetic retinopathy and signaling mechanism for activation of matrix metalloproteinase-9,” Journal of Cellular Physiology, vol. 227, no. 3, pp. 1052–1061, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. B. Veres, B. Radnai, F. Gallyas Jr. et al., “Regulation of kinase cascades and transcription factors by a poly(ADP-ribose) polymerase-1 inhibitor, 4-hydroxyquinazoline, in lipopolysaccharide-induced inflammation in mice,” Journal of Pharmacology and Experimental Therapeutics, vol. 310, no. 1, pp. 247–255, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Éthier, Y. Labelle, and G. G. Poirier, “PARP-1-induced cell death through inhibition of the MEK/ERK pathway in MNNG-treated HeLa cells,” Apoptosis, vol. 12, no. 11, pp. 2037–2049, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Luo and D. B. DeFranco, “Opposing roles for ERK1/2 in neuronal oxidative toxicity: distinct mechanisms of ERK1/2 action at early versus late phases of oxidative stress,” Journal of Biological Chemistry, vol. 281, no. 24, pp. 16436–16442, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. T. P. Rygiel, A. E. Mertens, K. Strumane, R. van der Kammen, and J. G. Collard, “The Rac activator Tiam1 prevents keratinocyte apoptosis by controlling ROS-mediated ERK phosphorylation,” Journal of Cell Science, vol. 121, no. 8, pp. 1183–1192, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. X. Wang, Z. Wang, Y. Yao et al., “Essential role of ERK activation in neurite outgrowth induced by α-lipoic acid,” Biochimica et Biophysica Acta, vol. 1813, no. 5, pp. 827–838, 2011. View at Publisher · View at Google Scholar · View at Scopus