Involvement of High Mobility Group Box 1 Protein in Optic Nerve Damage in Diabetes

References

• Sayin N, Kara N, Pekel G. Ocular complications of diabetes mellitus. World J Diabetes. 2015;6(1):92–108. doi:10.4239/wjd.v6.i1.92
   PubMed Web of Science ®Google Scholar
• Vieira-Potter VJ, Karamichos D, Lee DJ. Ocular complications of diabetes and therapeutic approaches. Biomed Res Int. 2016;2016:3801570. doi:10.1155/2016/3801570
   PubMed Web of Science ®Google Scholar
• Jeganathan VS, Wang JJ, Wong TY. Ocular associations of diabetes other than diabetic retinopathy. Diabetes Care. 2008;31(9):1905–1912. doi:10.2337/dc08-0342
   PubMed Web of Science ®Google Scholar
• Algan M, Ziegler O, Drouin P.[Optic neuropathy in diabetic subjects]. Diabete Metab. 1993;19(5):395–399. French.
   PubMed Web of Science ®Google Scholar
• Bikbova G, Oshitari T, Baba T, Yamamoto S. Neurotrophic factors for retinal ganglion cell neuropathy - with a special reference to diabetic neuropathy in the retina. Curr Diabetes Rev. 2014;10(3):166–176. doi:10.2174/1573399810666140508121927
   PubMedGoogle Scholar
• Barber AJ, Gardner TW, Abcouwer SF. The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2011;52(2):1156–1163. doi:10.1167/iovs.10-6293
   PubMed Web of Science ®Google Scholar
• Bao YK, Yan Y, Gordon M, McGill JB, Kass M, Rajagopal R. Visual field loss in patients with diabetes in the absence of clinically-detectable vascular retinopathy in a nationally representative survey. Invest Ophthalmol Vis Sci. 2019;60(14):4711–4716. doi:10.1167/iovs.19-28063
   PubMed Web of Science ®Google Scholar
• Montesano G, Ometto G, Higgins BE, et al. Evidence for structural and functional damage of the inner retina in diabetes with no diabetic retinopathy. Invest Ophthalmol Vis Sci. 2021;62(3):35. doi:10.1167/iovs.62.3.35
   PubMed Web of Science ®Google Scholar
• Parisi V, Uccioli L, Monticone G, et al. Electrophysiological assessment of visual function in IDDM patients. Electroencephalogr Clin Neurophysiol. 1997;104(2):171–179. doi:10.1016/S0168-5597(97)96606-5
   PubMedGoogle Scholar
• Sohn EH, van Dijk HW, Jiao C, et al. Retinal neurodegeneration may precede microvascular changes characteristic of diabetic retinopathy in diabetes mellitus. Proc Natl Acad Sci U S A. 2016;113(19):E2655–E2664. doi:10.1073/pnas.1522014113
   PubMed Web of Science ®Google Scholar
• van Dijk HW, Kok PH, Garvin M, et al. Selective loss of inner retinal layer thickness in type 1 diabetic patients with minimal diabetic retinopathy. Invest Ophthalmol Vis Sci. 2009;50(7):3404–3409. doi:10.1167/iovs.08-3143
   PubMed Web of Science ®Google Scholar
• Verrotti A, Lobefalo L, Trotta D, et al. Visual evoked potentials in young persons with newly diagnosed diabetes: a long-term follow-up. Dev Med Child Neurol. 2000;42(4):240–244. doi:10.1017/S0012162200000414
   PubMed Web of Science ®Google Scholar
• Wan ZQ, Gao Y, Cui M, Zhang YJ. Association between risk factors and retinal nerve fiber layer loss in early stages of diabetic retinopathy. Int J Ophthalmol. 2021;14(2):255–262. doi:10.18240/ijo.2021.02.12
   PubMed Web of Science ®Google Scholar
• Zeng Y, Cao D, Yu H, et al. Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy. Br J Ophthalmol. 2019;103(12):1747–1752. doi:10.1136/bjophthalmol-2018-313582
   PubMed Web of Science ®Google Scholar
• Dorfman D, Aranda ML, Rosenstein RE. Enriched environment protects the optic nerve from early diabetes-induced damage in adult rats. PLoS One. 2015;10(8):e0136637. doi:10.1371/journal.pone.0136637
   PubMed Web of Science ®Google Scholar
• Fernandez DC, Pasquini LA, Dorfman D, Aldana Marcos HJ, Rosenstein RE. Early distal axonopathy of the visual pathway in experimental diabetes. Am J Pathol. 2012;180(1):303–313. doi:10.1016/j.ajpath.2011.09.018
   PubMed Web of Science ®Google Scholar
• Pihl-Jensen G, Schmidt MF, Frederiksen JL. Multifocal visual evoked potentials in optic neuritis and multiple sclerosis: a review. Clin Neurophysiol. 2017;128(7):1234–1245. doi:10.1016/j.clinph.2017.03.047
   PubMed Web of Science ®Google Scholar
• Scott TM, Foote J, Peat B, Galway G. Vascular and neural changes in the rat optic nerve following induction of diabetes with streptozotocin. J Anat. 1986;144:145–152.
   PubMed Web of Science ®Google Scholar
• Icel E, Icel A, Ucak T, et al. The effects of lycopene on alloxan induced diabetic optic neuropathy. Cutan Ocul Toxicol. 2019;38(1):88–92. doi:10.1080/15569527.2018.1530258
   PubMed Web of Science ®Google Scholar
• Mendonca HR, Carvalho JNA, Abreu CA, et al. Lack of Galectin-3 attenuates neuroinflammation and protects the retina and optic nerve of diabetic mice. Brain Res. 2018;1700:126–137. doi:10.1016/j.brainres.2018.07.018
   PubMed Web of Science ®Google Scholar
• Zhang L, Inoue M, Dong K, Yamamoto M. Alterations in retrograde axonal transport in optic nerve of type I and type II diabetic rats. Kobe J Med Sci. 1998;44(5–6):205–215.
   PubMedGoogle Scholar
• Gong T, Liu L, Jiang W, Zhou R. DAMP-sensing receptors in sterile inflammation and inflammatory diseases. Nat Rev Immunol. 2020;20(2):95–112. doi:10.1038/s41577-019-0215-7
   PubMed Web of Science ®Google Scholar
• Kang R, Chen R, Zhang Q, et al. HMGB1 in health and disease. Mol Aspects Med. 2014;40:1–116. doi:10.1016/j.mam.2014.05.001
   PubMed Web of Science ®Google Scholar
• Yang H, Wang H, Andersson U. Targeting Inflammation Driven by HMGB1. Front Immunol. 2020;11:484. doi:10.3389/fimmu.2020.00484
   PubMed Web of Science ®Google Scholar
• Xue J, Suarez JS, Minaai M, et al. HMGB1 as a therapeutic target in disease. J Cell Physiol. 2021;236(5):3406–3419. doi:10.1002/jcp.30125
   PubMed Web of Science ®Google Scholar
• Liu Y, Zhuang GB, Zhou XZ. HMBG1 as a driver of inflammatory and immune processes in the pathogenesis of ocular diseases. J Ophthalmol. 2018;2018:5195290. doi:10.1155/2018/5195290
   PubMed Web of Science ®Google Scholar
• Mohammad G, Siddiquei MM, Othman A, Al-Shabrawey M, Abu El-Asrar AM. High-mobility group box-1 protein activates inflammatory signaling pathway components and disrupts retinal vascular-barrier in the diabetic retina. Exp Eye Res. 2013;107:101–109. doi:10.1016/j.exer.2012.12.009
   PubMed Web of Science ®Google Scholar
• Abu El-Asrar AM, Alam K, Garcia-Ramirez M, et al. Association of HMGB1 with oxidative stress markers and regulators in PDR. Mol Vis. 2017;23:853–871.
   PubMed Web of Science ®Google Scholar
• Abu El-Asrar AM, Mohammad G, Nawaz MI, Siddiquei MM. High-mobility group box-1 modulates the expression of inflammatory and angiogenic signaling pathways in diabetic retina. Curr Eye Res. 2015;40(11):1141–1152. doi:10.3109/02713683.2014.982829
   PubMed Web of Science ®Google Scholar
• Mohammad G, Abdelaziz GM, Siddiquei MM, Ahmad A, De Hertogh G, Abu El-Asrar AM. Cross-talk between sirtuin 1 and the proinflammatory mediator high-mobility group box-1 in the regulation of blood-retinal barrier breakdown in diabetic retinopathy. Curr Eye Res. 2019;44(10):1133–1143. doi:10.1080/02713683.2019.1625406
   PubMed Web of Science ®Google Scholar
• Mohammad G, Alam K, Nawaz MI, Siddiquei MM, Mousa A, Abu El-Asrar AM. Mutual enhancement between high-mobility group box-1 and NADPH oxidase-derived reactive oxygen species mediates diabetes-induced upregulation of retinal apoptotic markers. J Physiol Biochem. 2015;71(3):359–372. doi:10.1007/s13105-015-0416-x
   PubMed Web of Science ®Google Scholar
• Nawaz MI, Mohammad G. Role of high-mobility group box-1 protein in disruption of vascular barriers and regulation of leukocyte-endothelial interactions. J Recept Signal Transduct Res. 2015;35(4):340–345. doi:10.3109/10799893.2014.984309
   PubMed Web of Science ®Google Scholar
• Liu L, Jiang Y, Steinle JJ. Glycyrrhizin protects the diabetic retina against permeability, neuronal, and vascular damage through anti-inflammatory mechanisms. J Clin Med. 2019;8(7):957. doi:10.3390/jcm8070957
   PubMed Web of Science ®Google Scholar
• Mohammad G, Duraisamy AJ, Kowluru A, Kowluru RA. Functional regulation of an oxidative stress mediator, rac1, in diabetic retinopathy. Mol Neurobiol. 2019;56(12):8643–8655. doi:10.1007/s12035-019-01696-5
   PubMed Web of Science ®Google Scholar
• Mohammad G, Kowluru RA. Diabetic retinopathy and signaling mechanism for activation of matrix metalloproteinase-9. J Cell Physiol. 2012;227(3):1052–1061. doi:10.1002/jcp.22822
   PubMed Web of Science ®Google Scholar
• Mohammad G, Radhakrishnan R, Kowluru RA. Hydrogen sulfide: a potential therapeutic target in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2020;61(14):35. doi:10.1167/iovs.61.14.35
   PubMed Web of Science ®Google Scholar
• Mohammad G, Radhakrishnan R, Kowluru RA. Epigenetic modifications compromise mitochondrial DNA quality control in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2019;60(12):3943–3951. doi:10.1167/iovs.19-27602
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Elsherbiny NM, Abdel-Mottaleb Y, Elkazaz AY, et al. Carbamazepine alleviates retinal and optic nerve neural degeneration in diabetic mice via nerve growth factor-induced PI3K/Akt/mTOR activation. Front Neurosci. 2019;13:1089. doi:10.3389/fnins.2019.01089
   PubMed Web of Science ®Google Scholar
• Visuvanathan S, Baker AN, Lagali PS, et al. XIAP gene therapy effects on retinal ganglion cell structure and function in a mouse model of glaucoma. Gene Ther. 2021;29(3–4):147–156. doi:10.1038/s41434-021-00281-7
   PubMed Web of Science ®Google Scholar
• Rungger-Brandle E, Dosso AA, Leuenberger PM. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2000;41(7):1971–1980.
   PubMed Web of Science ®Google Scholar
• Lieth E, Barber AJ, Xu B, et al. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Penn state retina research group. Diabetes. 1998;47(5):815–820. doi:10.2337/diabetes.47.5.815
   PubMed Web of Science ®Google Scholar
• Horstmann L, Schmid H, Heinen AP, Kurschus FC, Dick HB, Joachim SC. Inflammatory demyelination induces glia alterations and ganglion cell loss in the retina of an experimental autoimmune encephalomyelitis model. J Neuroinflammation. 2013;10(1):120. doi:10.1186/1742-2094-10-120
   PubMed Web of Science ®Google Scholar
• Qu J, Jakobs TC. The time course of gene expression during reactive gliosis in the optic nerve. PLoS One. 2013;8(6):e67094. doi:10.1371/journal.pone.0067094
   PubMed Web of Science ®Google Scholar
• Paudel YN, Angelopoulou E, Semple B, Piperi C, Othman I, Shaikh MF. Potential neuroprotective effect of the HMGB1 inhibitor glycyrrhizin in neurological disorders. ACS Chem Neurosci. 2020;11(4):485–500. doi:10.1021/acschemneuro.9b00640
   PubMed Web of Science ®Google Scholar
• Mollica L, De Marchis F, Spitaleri A, et al. Glycyrrhizin binds to high-mobility group box 1 protein and inhibits its cytokine activities. Chem Biol. 2007;14(4):431–441. doi:10.1016/j.chembiol.2007.03.007
   PubMedGoogle Scholar
• Kim JB, Sig Choi J, Yu YM, et al. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J Neurosci. 2006;26(24):6413–6421. doi:10.1523/JNEUROSCI.3815-05.2006
   PubMed Web of Science ®Google Scholar
• Paudel YN, Shaikh MF, Chakraborti A, et al. HMGB1: a common biomarker and potential target for TBI, neuroinflammation, epilepsy, and cognitive dysfunction. Front Neurosci. 2018;12:628. doi:10.3389/fnins.2018.00628
   PubMed Web of Science ®Google Scholar
• Abu El-Asrar AM, Nawaz MI, Kangave D, Abouammoh M, Mohammad G. High-mobility group box-1 and endothelial cell angiogenic markers in the vitreous from patients with proliferative diabetic retinopathy. Mediators Inflamm. 2012;2012:697489. doi:10.1155/2012/697489
   PubMed Web of Science ®Google Scholar
• El-Asrar AM, Nawaz MI, Kangave D, et al. High-mobility group box-1 and biomarkers of inflammation in the vitreous from patients with proliferative diabetic retinopathy. Mol Vis. 2011;17:1829–1838.
   PubMed Web of Science ®Google Scholar
• Di Leo MA, Caputo S, Falsini B, et al. Nonselective loss of contrast sensitivity in visual system testing in early type I diabetes. Diabetes Care. 1992;15(5):620–625. doi:10.2337/diacare.15.5.620
   PubMed Web of Science ®Google Scholar
• Parisi V, Uccioli L, Parisi L, et al. Neural conduction in visual pathways in newly-diagnosed IDDM patients. Electroencephalogr Clin Neurophysiol. 1998;108(5):490–496. doi:10.1016/S0168-5597(98)00026-4
   PubMedGoogle Scholar
• Lin SC, Singh K, Jampel HD, et al. Optic nerve head and retinal nerve fiber layer analysis: a report by the American Academy of Ophthalmology. Ophthalmology. 2007;114(10):1937–1949. doi:10.1016/j.ophtha.2007.07.005
   PubMed Web of Science ®Google Scholar
• Quigley HA, Miller NR, George T. Clinical evaluation of nerve fiber layer atrophy as an indicator of glaucomatous optic nerve damage. Arch Ophthalmol. 1980;98(9):1564–1571. doi:10.1001/archopht.1980.01020040416003
   PubMedGoogle Scholar
• Soltan-Sanjari M, Parvaresh MM, Maleki A, Ghasemi-Falavarjani K, Bakhtiari P. Correlation between retinal nerve fiber layer thickness by optical coherence tomography and perimetric parameters in optic atrophy. J Ophthalmic Vis Res. 2008;3(2):91–94.
   PubMedGoogle Scholar
• Lopes de Faria JM, Russ H, Costa VP. Retinal nerve fibre layer loss in patients with type 1 diabetes mellitus without retinopathy. Br J Ophthalmol. 2002;86(7):725–728. doi:10.1136/bjo.86.7.725
   PubMed Web of Science ®Google Scholar
• Lutty GA. Effects of diabetes on the eye. Invest Ophthalmol Vis Sci. 2013;54(14):ORSF81–ORSF87. doi:10.1167/iovs.13-12979
   PubMed Web of Science ®Google Scholar
• Rubsam A, Parikh S, Fort PE. Role of inflammation in diabetic retinopathy. Int J Mol Sci. 2018;19(4):942. doi:10.3390/ijms19040942
   PubMed Web of Science ®Google Scholar
• Gerhardinger C, Costa MB, Coulombe MC, Toth I, Hoehn T, Grosu P. Expression of acute-phase response proteins in retinal Muller cells in diabetes. Invest Ophthalmol Vis Sci. 2005;46(1):349–357. doi:10.1167/iovs.04-0860
   PubMed Web of Science ®Google Scholar
• Forrester JV, Kuffova L, Delibegovic M. The role of inflammation in diabetic retinopathy. Front Immunol. 2020;11:583687. doi:10.3389/fimmu.2020.583687
   PubMed Web of Science ®Google Scholar
• Mesquida M, Drawnel F, Fauser S. The role of inflammation in diabetic eye disease. Semin Immunopathol. 2019;41(4):427–445. doi:10.1007/s00281-019-00750-7
   PubMed Web of Science ®Google Scholar
• Selvakumar A, Muthumeena M, Noronha OV, Bapu S. Bilateral optic neuropathy with central diabetes insipidus in a child. Indian J Ophthalmol. 2018;66(11):1642–1644. doi:10.4103/ijo.IJO_281_18
   PubMed Web of Science ®Google Scholar
• Yu Y, Chen H, Su SB. Neuroinflammatory responses in diabetic retinopathy. J Neuroinflammation. 2015;12(1):141. doi:10.1186/s12974-015-0368-7
   PubMed Web of Science ®Google Scholar
• Mendonca HR, Carpi-Santos R, da Costa Calaza K, Blanco martinez AM. Neuroinflammation and oxidative stress act in concert to promote neurodegeneration in the diabetic retina and optic nerve: galectin-3 participation. Neural Regen Res. 2020;15(4):625–635. doi:10.4103/1673-5374.266910
   PubMed Web of Science ®Google Scholar
• Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418(6894):191–195. doi:10.1038/nature00858
   PubMed Web of Science ®Google Scholar
• Yang H, Liu H, Zeng Q, et al. Inhibition of HMGB1/RAGE-mediated endocytosis by HMGB1 antagonist box A, anti-HMGB1 antibodies, and cholinergic agonists suppresses inflammation. Mol Med. 2019;25(1):13. doi:10.1186/s10020-019-0081-6
   PubMed Web of Science ®Google Scholar
• Bucova M, Majernikova B, Durmanova V, et al. HMGB1 as a potential new marker of disease activity in patients with multiple sclerosis. Neurol Sci. 2020;41(3):599–604. doi:10.1007/s10072-019-04136-3
   PubMed Web of Science ®Google Scholar
• Frank MG, Weber MD, Watkins LR, Maier SF. Stress sounds the alarmin: the role of the danger-associated molecular pattern HMGB1 in stress-induced neuroinflammatory priming. Brain Behav Immun. 2015;48:1–7. doi:10.1016/j.bbi.2015.03.010
   PubMed Web of Science ®Google Scholar
• Garcia-Bermudez MY, Freude KK, Mouhammad ZA, van Wijngaarden P, Martin KK, Kolko M. Glial cells in glaucoma: friends, foes, and potential therapeutic targets. Front Neurol. 2021;12:624983. doi:10.3389/fneur.2021.624983
   PubMed Web of Science ®Google Scholar
• Lewis GP, Fisher SK. Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodeling and a comparison to vimentin expression. Int Rev Cytol. 2003;230:263–290.
   PubMed Web of Science ®Google Scholar
• Abu El-Asrar AM, Siddiquei MM, Nawaz MI, Geboes K, Mohammad G. The proinflammatory cytokine high-mobility group box-1 mediates retinal neuropathy induced by diabetes. Mediators Inflamm. 2014;2014:746415. doi:10.1155/2014/746415
   PubMed Web of Science ®Google Scholar
• Liu L, Jiang Y, Steinle JJ. Epac1 and glycyrrhizin both inhibit HMGB1 levels to reduce diabetes-induced neuronal and vascular damage in the mouse retina. J Clin Med. 2019;8(6):772. doi:10.3390/jcm8060772
   PubMed Web of Science ®Google Scholar
• Azeez IA, Olopade F, Laperchia C, et al. Regional myelin and axon damage and neuroinflammation in the adult mouse brain after long-term postnatal vanadium exposure. J Neuropathol Exp Neurol. 2016;75(9):843–854. doi:10.1093/jnen/nlw058
   PubMed Web of Science ®Google Scholar
• Stassart RM, Mobius W, Nave KA, Edgar JM. The axon-myelin unit in development and degenerative disease. Front Neurosci. 2018;12:467. doi:10.3389/fnins.2018.00467
   PubMed Web of Science ®Google Scholar