Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 746415, 10 pages
http://dx.doi.org/10.1155/2014/746415
Research Article

The Proinflammatory Cytokine High-Mobility Group Box-1 Mediates Retinal Neuropathy Induced by Diabetes

1Department of Ophthalmology, College of Medicine, King Saud University, Riyadh, Saudi Arabia
2Department of Ophthalmology, King Abdulaziz University Hospital, Old Airport Road, P.O. Box 245, Riyadh 11411, Saudi Arabia
3Laboratory of Histochemistry and Cytochemistry, University of Leuven, Leuven, Belgium

Received 15 July 2013; Revised 13 January 2014; Accepted 28 January 2014; Published 10 March 2014

Academic Editor: Charles J. Malemud

Copyright © 2014 Ahmed M. Abu El-Asrar 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. 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 Scopus
  5. J. R. Van Beijnum, W. A. Buurman, and A. W. Griffioen, “Convergence and amplification of toll-like receptor (TLR) and receptor for advanced glycation end products (RAGE) signaling pathways via high mobility group B1 (HMGB1),” Angiogenesis, vol. 11, no. 1, pp. 91–99, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. C. J. Treutiger, G. E. Mullins, A.-S. M. Johansson et al., “High mobility group 1 B-box mediates activation of human endothelium,” Journal of Internal Medicine, vol. 254, no. 4, pp. 375–385, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Fiuza, M. Bustin, S. Talwar et al., “Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells,” Blood, vol. 101, no. 7, pp. 2652–2660, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. Z.-G. Luan, H. Zhang, P.-T. Yang, X.-C. Ma, C. Zhang, and R.-X. Guo, “HMGB1 activates nuclear factor-κB signaling by RAGE and increases the production of TNF-α in human umbilical vein endothelial cells,” Immunobiology, vol. 215, no. 12, pp. 956–962, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Takeuchi, J.-I. Takino, and S.-I. Yamagishi, “Involvement of the toxic AGEs (TAGE)-RAGE system in the pathogenesis of diabetic vascular complications: a novel therapeutic strategy,” Current Drug Targets, vol. 11, no. 11, pp. 1468–1482, 2010. View at Google Scholar · View at Scopus
  10. D. Tang, R. Kang, H. J. Zeh 3rd, and M. T. Lotze, “High-mobility group box 1, oxidative stress, and disease,” Antioxidants and Redox Signaling, vol. 14, no. 7, pp. 1315–1335, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. M. Joussen, V. Poulaki, M. L. Le et al., “A central role for inflammation in the pathogenesis of diabetic retinopathy,” The FASEB Journal, vol. 18, no. 12, pp. 1450–1452, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Miyamoto, S. Khosrof, S.-E. Bursell et al., “Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 19, pp. 10836–10841, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. H.-M. Gao, H. Zhou, F. Zhang, B. C. Wilson, W. Kam, and J.-S. Hong, “HMGB1 acts on microglia Mac1 to mediate chronic neuroinflammation that drives progressive neurodegeneration,” Journal of Neuroscience, vol. 31, no. 3, pp. 1081–1092, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. J.-B. Kim, S. C. Joon, Y.-M. Yu et al., “HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain,” Journal of Neuroscience, vol. 26, no. 24, pp. 6413–6421, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Qiu, M. Nishimura, Y. Wang et al., “Early release of HMGB-1 from neurons after the onset of brain ischemia,” Journal of Cerebral Blood Flow and Metabolism, vol. 28, no. 5, pp. 927–938, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. S.-W. Kim, C.-M. Lim, J.-B. Kim et al., “Extracellular HMGB1 released by NMDA treatment confers neuronal apoptosis via RAGE-p38 MAPK/ERK signaling pathway,” Neurotoxicity Research, vol. 20, no. 2, pp. 159–169, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Faraco, S. Fossati, M. E. Bianchi et al., “High mobility group box 1 protein is released by neural cells upon different stresses and worsens ischemic neurodegeneration in vitro and in vivo,” Journal of Neurochemistry, vol. 103, no. 2, pp. 590–603, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Liu, S. Mori, H. K. Takahashi et al., “Anti-high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats,” The FASEB Journal, vol. 21, no. 14, pp. 3904–3916, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Pedrazzi, L. Raiteri, G. Bonanno et al., “Stimulation of excitatory amino acid release from adult mouse brain glia subcellular particles by high mobility group box 1 protein,” Journal of Neurochemistry, vol. 99, no. 3, pp. 827–838, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. A. M. A. El-Asrar, L. Missotten, and K. Geboes, “Expression of high-mobility groups box-1/receptor for advanced glycation end products/osteopontin/early growth response-1 pathway in proliferative vitreoretinal epiretinal membranes,” Molecular Vision, vol. 17, pp. 508–518, 2011. View at Google Scholar · View at Scopus
  21. A. M. A. El-Asrar, M. I. Nawaz, D. Kangave et al., “High-mobility group box-1 and biomarkers of inflammation in the vitreous from patients with proliferative diabetic retinopathy,” Molecular Vision, vol. 17, pp. 1829–1838, 2011. View at Google Scholar · View at Scopus
  22. A. M. Abu El-Asrar, M. I. Nawaz, D. Kangave, M. M. Siddiquei, and K. Geboes, “Osteopontin and other regulators of angiogenesis and fibrogenesis in the vitreous from patients with proliferative vitreoretinal disorders,” Mediators of Inflammation, vol. 2012, Article ID 493043, 8 pages, 2012. View at Publisher · View at Google Scholar
  23. G. Mohammad, M. M. Siddiquei, A. Othman, M. Al-Shabrawey, and A. M. Abu El-Asrar, “High-mobility group box-1 protein activates inflammatory signaling pathway components and disrupts retinal vascular-barrier in the diabetic retina,” Experimental Eye Research, vol. 107, pp. 101–109, 2013. View at Google Scholar
  24. L. Mollica, F. De Marchis, A. Spitaleri et al., “Glycyrrhizin binds to high-mobility group box 1 protein and inhibits its cytokine activities,” Chemistry and Biology, vol. 14, no. 4, pp. 431–441, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. J. Gastinger, R. S. J. Singh, and A. J. Barber, “Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and Ins2Akita-diabetic mouse retinas,” Investigative Ophthalmology and Visual Science, vol. 47, no. 7, pp. 3143–3150, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. R. A. Feit-Leichman, R. Kinouchi, M. Takeda et al., “Vascular damage in a mouse model of diabetic retinopathy: relation to neuronal and glial changes,” Investigative Ophthalmology and Visual Science, vol. 46, no. 11, pp. 4281–4287, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. I. Spiwoks-Becker, L. Vollrath, M. W. Seeliger, G. Jaissle, L. G. Eshkind, and R. E. Leube, “Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice,” Neuroscience, vol. 107, no. 1, pp. 127–142, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. H. D. Vanguilder, R. M. Brucklacher, K. Patel, R. W. Ellis, W. M. Freeman, and A. J. Barber, “Diabetes downregulates presynaptic proteins and reduces basal synapsin i phosphorylation in rat retina,” European Journal of Neuroscience, vol. 28, no. 1, pp. 1–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Kurihara, Y. Ozawa, N. Nagai et al., “Angiotensin II type 1 receptor signaling contributes to synaptophysin degradation and neuronal dysfunction in the diabetic retina,” Diabetes, vol. 57, no. 8, pp. 2191–2198, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. 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, 7 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Szabadfi, T. Atlasz, P. Kiss et al., “Protective effects of the neuropeptide PACAP in diabetic retinopathy,” Cell and Tissue Research, vol. 348, no. 1, pp. 37–46, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Wan, N. N. Liu, L. M. Liu, N. Cai, and L. Chen, “Effect of adenovirus-mediated brain derived neurotrophic factor in early retinal neuropathy of diabetes in rats,” International Journal of Ophthalmology, vol. 3, pp. 145–148, 2010. View at Google Scholar
  33. F. K. Northington, R. W. Hamill, and S. P. Banerjee, “Dopamine-stimulated adenylate cyclase and tyrosine hydroxylase in diabetic rat retina,” Brain Research, vol. 337, no. 1, pp. 151–154, 1985. View at Publisher · View at Google Scholar · View at Scopus
  34. 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
  35. 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
  36. E. Lieth, A. J. Barber, B. Xu et al., “Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Penn State Retina Research Group,” Diabetes, vol. 47, pp. 815–820, 1998. View at Google Scholar
  37. 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
  38. A. Lecleire-Collet, L. H. Tessier, P. Massin et al., “Advanced glycation end products can induce glial reaction and neuronal degeneration in retinal explants,” British Journal of Ophthalmology, vol. 89, no. 12, pp. 1631–1633, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. J. V. Glenn and A. W. Stitt, “The role of advanced glycation end products in retinal ageing and disease,” Biochimica et Biophysica Acta, vol. 1790, no. 10, pp. 1109–1116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Karachalias, R. Babaei-Jadidi, N. Ahmed, and P. J. Thornalley, “Accumulation of fructosyl-lysine and advanced glycation end products in the kidney, retina and peripheral nerve of streptozotocin-induced diabetic rats,” Biochemical Society Transactions, vol. 31, no. 6, pp. 1423–1425, 2003. View at Google Scholar · View at Scopus
  41. M. Shinohara, P. J. Thornalley, I. Giardino et al., “Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis,” Journal of Clinical Investigation, vol. 101, no. 5, pp. 1142–1147, 1998. View at Google Scholar · View at Scopus
  42. A. G. Miller, G. Tan, K. J. Binger et al., “Candesartan attenuates diabetic retinal vascular pathology by restoring glyoxalase-I function,” Diabetes, vol. 59, no. 12, pp. 3208–3215, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. A. K. Berner, O. Brouwers, R. Pringle et al., “Protection against methylglyoxal-derived AGEs by regulation of glyoxalase 1 prevents retinal neuroglial and vasodegenerative pathology,” Diabetologia, vol. 55, no. 3, pp. 845–854, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. K.-I. Kawahara, K. K. Biswas, M. Unoshima et al., “C-reactive protein induces high-mobility group box-1 protein release through activation of p38MAPK in macrophage RAW264.7 cells,” Cardiovascular Pathology, vol. 17, no. 3, pp. 129–138, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Willenbrock, O. Braun, J. Baumgart et al., “TNF-α induced secretion of HMGB1 from non-immune canine mammary epithelial cells (MTH53A),” Cytokine, vol. 57, no. 2, pp. 210–220, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Hayakawa, K. Arai, and E. H. Lo, “Role of ERK MAP kinase and CRM1 in IL-1β-stimulated release of HMGB1 from cortical astrocytes,” GLIA, vol. 58, no. 8, pp. 1007–1015, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. S.-W. Kim, Y. Jin, J.-H. Shin et al., “Glycyrrhizic acid affords robust neuroprotection in the postischemic brain via anti-inflammatory effect by inhibiting HMGB1 phosphorylation and secretion,” Neurobiology of Disease, vol. 46, no. 1, pp. 147–156, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Ohnishi, H. Katsuki, C. Fukutomi et al., “HMGB1 inhibitor glycyrrhizin attenuates intracerebral hemorrhage-induced injury in rats,” Neuropharmacology, vol. 61, no. 5-6, pp. 975–980, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Gong, L.-B. Yuan, L. Hu et al., “Glycyrrhizin attenuates rat ischemic spinal cord injury by suppressing inflammatory cytokines and HMGB1,” Acta Pharmacologica Sinica, vol. 33, no. 1, pp. 11–18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. F. C. Stormer, R. Reistad, and J. Alexander, “Glycyrrhizic acid in liquorice—evaluation of health hazard,” Food and Chemical Toxicology, vol. 31, no. 4, pp. 303–312, 1993. View at Publisher · View at Google Scholar · View at Scopus
  51. M. M. Celik, A. Karakus, C. Zeren et al., “Licorice induced hypokalemia, edema, and thrombocytopenia,” Human & Experimental Toxicology, vol. 31, pp. 1295–1298, 2012. View at Google Scholar