Neurodegeneration and neuroinflammation in diabetic retinopathy: Potential approaches to delay neuronal loss

Current Neuropharmacology

Volumn 14, Issue 8, 2016, Pages 831-839

  Kadłubowska, Joanna ^a   Malaguarnera, Lucia ^b   Wąż, Piotr ^a   Zorena, Katarzyna ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

Diabetic retinopathy; Neurodegeneration of neurons; Neuroinflammation; Neuroprotection

Indexed keywords

ACETYLSALICYLIC ACID; ADVANCED GLYCATION END PRODUCT RECEPTOR; CD14 ANTIGEN; CILOSTAZOL; GLUTAMIC ACID; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HERBACEOUS AGENT; PROPRANOLOL; REACTIVE OXYGEN METABOLITE; ROSIGLITAZONE; SITAGLIPTIN; VASCULOTROPIN; NEUROPROTECTIVE AGENT;

APOPTOSIS; AREA UNDER THE CURVE; CELL DEATH; DIABETIC MICROANGIOPATHY; DIABETIC RETINOPATHY; EXCITOTOXICITY; EXERCISE; EYE FUNDUS; HUMAN; HYPERGLYCEMIA; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RECEIVER OPERATING CHARACTERISTIC; RETINA GANGLION CELL; RETINA NERVE CELL; REVIEW; UMBILICAL CORD BLOOD CELL; ANIMAL; DRUG EFFECTS; INFLAMMATION; PATHOPHYSIOLOGY; PHYSIOLOGY; RETINAL DEGENERATION;

ANIMALS; DIABETIC RETINOPATHY; HUMANS; INFLAMMATION; NEUROPROTECTION; NEUROPROTECTIVE AGENTS; RETINAL DEGENERATION; RETINAL NEURONS;

EID: 85010444981     PISSN: 1570159X     EISSN: 18756190     Source Type: Journal    
DOI: 10.2174/1570159X14666160614095559     Document Type: Review

References (97)

1. Wild, S.; Roglic, G.; Green, A.; Sicree, R.; King, H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care, 2004, 27(5), 1047-1053. [http://dx.doi. org/10.2337/diacare.27.5.1047] [PMID: 15111519]
2. Hartwig, S.; Greiser, K.H.; Medenwald, D.; Tiller, D.; Herzog, B.; Schipf, S.; Ittermann, T.; Volzke, H.; Muller, G.; Haerting, J.; Kluttig, A. Association of Change of Anthropometric Measurements With Incident Type 2 Diabetes Mellitus: A Pooled Analysis of the Prospective Population-Based CARLA and SHIP Cohort Studies. Medicine (Baltimore), 2015, 94(34), e1394. [http://dx.doi.org/10.1097/MD.0000000000001394] [PMID: 26313783]
3. Imperatore, G.; Boyle, J.P.; Thompson, T.J.; Case, D.; Dabelea, D.; Hamman, R.F.; Lawrence, J.M.; Liese, A.D.; Liu, L.L.; Mayer-Davis, E.J.; Rodriguez, B.L.; Standiford, D. Projections of type 1 and type 2 diabetes burden in the U.S. population aged <20 years through 2050: dynamic modeling of incidence, mortality, and population growth. Diabetes Care, 2012, 35(12), 2515-2520. [http://dx.doi.org/10.2337/dc12-0669] [PMID: 23173134]
4. Triolo, T.M.; Chase, H.P.; Barker, J.M. Diabetic subjects diagnosed through the Diabetes Prevention Trial-Type 1 (DPT-1) are often asymptomatic with normal A1C at diabetes onset. Diabetes Care, 2009, 32(5), 769-773. [http://dx.doi.org/10.2337/dc08-1872] [PMID: 19407074]
5. Wierusz-Wysocka, B.; Zozulińska, D.; Knast, B.; Pisarczyk-Wiza, D. [Appearance of undiagnosed diabetes mellitus in the population of professionally active people in the urban areas]. Pol. Arch. Med. Wewn., 2001, 106(3), 815-821. [PMID: 11928591]
6. Pantalone, K.M.; Hobbs, T.M.; Wells, B.J.; Kong, S.X.; Kattan, M.W.; Bouchard, J.; Yu, C.; Sakurada, B.; Milinovich, A.; Weng, W.; Bauman, J.M.; Zimmerman, R.S. Clinical characteristics, complications, comorbidities and treatment patterns among patients with type 2 diabetes mellitus in a large integrated health system. BMJ Open Diabetes Res. Care, 2015, 3(1), e000093. [http://dx.doi. org/10.1136/bmjdrc-2015-000093] [PMID: 26217493]
7. Tomić, M.; Ljubić, S.; Kaštelan, S.; Gverović Antunica, A.; Jazbec, A.; Poljičanin, T. Inflammation, haemostatic disturbance, and obesity: possible link to pathogenesis of diabetic retinopathy in type 2 diabetes. Mediators Inflamm., 2013. Article ID 818671
8. Wegner, M.; Araszkiewicz, A.; Piorunska-Stolzmann, M.; Wierusz-Wysocka, B.; Zozulinska-Ziolkiewicz, D. Association between IL-6 concentration and diabetes-related variables in DM1 patients with and without microvascular complications. Inflammation, 2013, 36(3), 723-728. [http://dx.doi.org/10.1007/s10753-013-9598-y] [PMID: 23371411]
9. Zorena, K.; Myśliwska, J.; Myśliwiec, M.; Balcerska, A.; Lipowski, P.; Raczyńska, K. [Interleukin-12, vascular endothelial growth factor and tumor necrosis factor-alpha in the process of neoangiogenesis of diabetic retinopathy in children]. Klin. Oczna, 2007, 109(4-6), 155-159. [PMID: 17725275]
10. Lieth, E.; Barber, A.J.; Xu, B.; Dice, C.; Ratz, M.J.; Tanase, D.; Strother, J.M. Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Diabetes, 1998, 47(5), 815-820. [http://dx.doi.org/10.2337/diabetes.47.5.815] [PMID: 9588455]
11. Howell, S.J.; Mekhail, M.N.; Azem, R.; Ward, N.L.; Kern, T.S. Degeneration of retinal ganglion cells in diabetic dogs and mice: relationship to glycemic control and retinal capillary degeneration. Mol. Vis., 2013, 19, 1413-1421. [PMID: 23825921]
12. Myśliwska, J.; Zorena, K.; Myśliwiec, M.; Malinowska, E.; Raczyńska, K.; Balcerska, A. The -174GG interleukin-6 genotype is protective from retinopathy and nephropathy in juvenile onset type 1 diabetes mellitus. Pediatr. Res., 2009, 66(3), 341-345. [http://dx.doi.org/10.1203/PDR.0b013e3181b1bd05] [PMID: 19542902]
13. Barber, A.J. Diabetic retinopathy: recent advances towards understanding neurodegeneration and vision loss. Sci. China Life Sci., 2015, 58(6), 541-549. [http://dx.doi.org/10.1007/s11427-015-4856-x] [PMID: 25951929]
14. Jindal, V. Neurodegeneration as a primary change and role of neuroprotection in diabetic retinopathy. Mol. Neurobiol., 2015, 51(3), 878-884. [http://dx.doi.org/10.1007/s12035-014-8732-7] [PMID: 24826918]
15. Ola, M.S.; Alhomida, A.S. Neurodegeneration in diabetic retina and its potential drug targets. Curr. Neuropharmacol., 2014, 12(4), 380-386. [http://dx.doi.org/10.2174/1570159X12666140619205024] [PMID: 25342945]
16. Sutter, E.E. Noninvasive Testing Methods: Multifocal Electrophysiology. In: Encyclopedia of the Eye; Dartt, D.A., Ed.; Academic Press: Oxford, 2010; Vol. 3, pp. 142-160. [http://dx.doi.org/10.1016/B978-0-12-374203-2.00226-8]
17. Semeran, K.; Pawłowski, P.; Lisowski, Ł.; Szczepaniak, I.; Wojtowicz, J.; Ławicki, S.; Bakunowicz-Łazarczyk, A.; Bossowski, A. Plasma levels of IL-17, VEGF, and adrenomedullin and S-cone dysfunction of the retina in children and adolescents without signs of retinopathy and with varied duration of diabetes. Mediators Inflamm., 2013, 2013, 274726. [http://dx.doi.org/10.1155/2013/274726] [PMID: 24347823]
18. Lung, J.C.; Swann, P.G.; Wong, D.S.; Chan, H.H. Global flash multifocal electroretinogram: early detection of local functional changes and its correlations with optical coherence tomography and visual field tests in diabetic eyes. Doc. Ophthalmol., 2012, 125(2), 123-135. [http://dx.doi.org/10.1007/s10633-012-9343-0] [PMID: 22828871]
19. Aghdam, S.Y.; Gurel, Z.; Ghaffarieh, A.; Sorenson, C.M.; Sheibani, N. High glucose and diabetes modulate cellular proteasome function: Implications in the pathogenesis of diabetes complications. Biochem. Biophys. Res. Commun., 2013, 432(2), 339-344. [http://dx.doi.org/10.1016/j.bbrc.2013.01.101] [PMID: 23391566]
20. Hammes, H.P. Pericytes and the pathogenesis of diabetic retinopathy. Horm. Metab. Res., 2005, 37(Suppl. 1), 39-43. [http://dx.doi.org/10.1055/s-2005-861361] [PMID: 15918109]
21. Simo, R.; Hernandez, C. Neurodegeneration is an early event in diabetic retinopathy: therapeutic implications. Br. J. Ophthalmol., 2012, 96(10), 1285-1290. [http://dx.doi.org/10.1136/bjophthalmol-2012-302005] [PMID: 22887976]
22. Zorena, K.; Raczyńska, D.; Raczyńska, K. Biomarkers in diabetic retinopathy and the therapeutic implications. Mediators Inflamm., 2013, 2013, 193604. [http://dx.doi.org/10.1155/2013/193604] [PMID: 24311895]
23. Mancini, J.E.; Ortiz, G.; Croxatto, J.O.; Gallo, J.E. Retinal upregulation of inflammatory and proangiogenic markers in a model of neonatal diabetic rats fed on a high-fat-diet. BMC Ophthalmol., 2013, 13, 14. [http://dx.doi.org/10.1186/1471-2415-13-14] [PMID: 23587252]
24. Yamagishi, S.; Matsui, T. Soluble form of a receptor for advanced glycation end products (sRAGE) as a biomarker. Front. Biosci. (Elite Ed.), 2010, 2, 1184-1195. [http://dx.doi.org/10.2741/e178] [PMID: 20515790]
25. Beisswenger, P.J. Glycation and biomarkers of vascular complications of diabetes. Amino Acids, 2012, 42(4), 1171-1183. [http://dx.doi.org/10.1007/s00726-010-0784-z] [PMID: 21042818]
26. Yan, S.F.; Yan, S.D.; Ramasamy, R.; Schmidt, A.M. Tempering the wrath of RAGE: an emerging therapeutic strategy against diabetic complications, neurodegeneration, and inflammation. Ann. Med., 2009, 41(6), 408-422. [http://dx.doi.org/10.1080/07853890902806576] [PMID: 19322705]
27. Bharadwaj, A.S.; Appukuttan, B.; Wilmarth, P.A.; Pan, Y.; Stempel, A.J.; Chipps, T.J.; Benedetti, E.E.; Zamora, D.O.; Choi, D.; David, L.L.; Smith, J.R. Role of the retinal vascular endothelial cell in ocular disease. Prog. Retin. Eye Res., 2013, 32, 102-180. [http://dx.doi.org/10.1016/j.preteyeres.2012.08.004] [PMID: 22982179]
28. Fu, S.; Dong, S.; Zhu, M.; Sherry, D.M.; Wang, C.; You, Z.; Haigh, J.J.; Le, Y.Z. Muller glia are a major cellular source of survival signals for retinal neurons in diabetes. Diabetes, 2015, 64(10), 3554-3563. [Epub ahead of print]. [http://dx.doi.org/10.2337/db15-0180] [PMID: 26068541]
29. Zorena, K.; Kula, M.; Malinowska, E.; Raczyńska, D.; Myśliwiec, M.; Raczyńska, K. Threshold serum concentrations of tumour necrosis factor alpha (TNFα) as a potential marker of the presence of microangiopathy in children and adolescents with type 1 diabetes mellitus (T1DM). Hum. Immunol., 2013, 74(1), 75-81. [http://dx.doi.org/10.1016/j.humimm.2012.10.002] [PMID: 23073299]
30. Giacco, F.; Brownlee, M. Oxidative stress and diabetic complications. Circ. Res., 2010, 107(9), 1058-1070. [http://dx.doi. org/10.1161/CIRCRESAHA.110.223545] [PMID: 21030723]
31. Kowluru, R.A.; Chan, P.S. Oxidative stress and diabetic retinopathy. Exp. Diabetes Res., 2007, 2007, 43603. [http://dx.doi.org/10.1155/2007/43603] [PMID: 17641741]
32. Zhang, L.; Yu, C.; Vasquez, F.E.; Galeva, N.; Onyango, I.; Swerdlow, R.H.; Dobrowsky, R.T. Hyperglycemia alters the schwann cell mitochondrial proteome and decreases coupled respiration in the absence of superoxide production. J. Proteome Res., 2010, 9(1), 458-471. [http://dx.doi.org/10.1021/pr900818g] [PMID: 19905032]
33. Herlein, J.A.; Fink, B.D.; Sivitz, W.I. Superoxide production by mitochondria of insulin-sensitive tissues: mechanistic differences and effect of early diabetes. Metabolism, 2010, 59(2), 247-257. [http://dx.doi.org/10.1016/j.metabol.2009.07.021] [PMID: 19765776]
34. Busik, J.V.; Mohr, S.; Grant, M.B. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes, 2008, 57(7), 1952-1965. [http://dx.doi.org/10.2337/db07-1520] [PMID: 18420487]
35. Cai, R.; Xue, W.; Liu, S.; Petersen, R.B.; Huang, K.; Zheng, L. Overexpression of glyceraldehyde 3-phosphate dehydrogenase prevents neurovascular degeneration after retinal injury. FASEB J., 2015, 29(7), 2749-2758. [http://dx.doi.org/10.1096/fj.14-265801] [PMID: 25805836]
36. Bandyopadhyay, M.; Rohrer, B. Matrix metalloproteinase activity creates pro-angiogenic environment in primary human retinal pigment epithelial cells exposed to complement. Invest. Ophthalmol. Vis. Sci., 2012, 53(4), 1953-1961. [http://dx.doi.org/10.1167/iovs. 11-8638] [PMID: 22408008]
37. Kanwar, M.; Chan, P.S.; Kern, T.S.; Kowluru, R.A. Oxidative damage in the retinal mitochondria of diabetic mice: possible protection by superoxide dismutase. Invest. Ophthalmol. Vis. Sci., 2007, 48(8), 3805-3811. [http://dx.doi.org/10.1167/iovs.06-1280] [PMID: 17652755]
38. Li, X.; Zhang, M.; Zhou, H. The morphological features and mitochondrial oxidative stress mechanism of the retinal neurons apoptosis in early diabetic rats. J. Diabetes Res., 2014, 2014, 678123. [http://dx.doi.org/10.1155/2014/678123] [PMID: 24527463]
39. Jivabhai Patel, S.; Bany-Mohammed, F.; McNally, L.; Valencia, G.B.; Lazzaro, D.R.; Aranda, J.V.; Beharry, K.D. Exogenous Superoxide Dismutase Mimetic Without Scavenging H2O2 Causes Photoreceptor Damage in a Rat Model for Oxygen-Induced Retinopathy. Invest. Ophthalmol. Vis. Sci., 2015, 56(3), 1665-1677. [http://dx.doi.org/10.1167/iovs.14-15321] [PMID: 25670494]
40. Mandal, L.K.; Choudhuri, S.; Dutta, D.; Mitra, B.; Kundu, S.; Chowdhury, I.H.; Sen, A.; Chatterjee, M.; Bhattacharya, B. Oxidative stress-associated neuroretinal dysfunction and nitrosative stress in diabetic retinopathy. Can. J. Diabetes, 2013, 37(6), 401-407. [http://dx.doi.org/10.1016/j.jcjd.2013.05.004] [PMID: 24321721]
41. Lee, J.J.; Hsiao, C.C.; Yang, I.H.; Chou, M.H.; Wu, C.L.; Wei, Y.C.; Chen, C.H.; Chuang, J.H. High-mobility group box 1 protein is implicated in advanced glycation end products-induced vascular endothelial growth factor A production in the rat retinal ganglion cell line RGC-5. Mol. Vis., 2012, 18, 838-850. [PMID: 22511847]
42. Magistretti, P.J. Role of glutamate in neuron-glia metabolic coupling. Am. J. Clin. Nutr., 2009, 90(3), 875S-880S. [http://dx. doi.org/10.3945/ajcn.2009.27462CC] [PMID: 19571222]
43. Orellana, J.A.; Saez, P.J.; Cortes-Campos, C.; Elizondo, R.J.; Shoji, K.F.; Contreras-Duarte, S.; Figueroa, V.; Velarde, V.; Jiang, J.X.; Nualart, F.; Saez, J.C.; Garcia, M.A. Glucose increases intracellular free Ca(2+) in tanycytes via ATP released through connexin 43 hemichannels. Glia, 2012, 60(1), 53-68. [http://dx.doi.org/10.1002/glia.21246] [PMID: 21987367]
44. Wang, L.; Deng, Q.Q.; Wu, X.H.; Yu, J.; Yang, X.L.; Zhong, Y.M. Upregulation of glutamate-aspartate transporter by glial cell linederived neurotrophic factor ameliorates cell apoptosis in neural retina in streptozotocin-induced diabetic rats. CNS Neurosci. Ther., 2013, 19(12), 945-953. [http://dx.doi.org/10.1111/cns.12150] [PMID: 23870489]
45. Al-Shabrawey, M.; Smith, S. Prediction of diabetic retinopathy: role of oxidative stress and relevance of apoptotic biomarkers. EPMA J., 2010, 1(1), 56-72. [http://dx.doi.org/10.1007/s13167-010-0002-9] [PMID: 23199041]
46. Pothecary, C.A.; Thompson, H.; Salt, T.E. Changes in glutamate receptor function in synaptic input to the superficial superior colliculus (SSC) with aging and in retinal degeneration in the Royal College of Surgeons (RCS) rat. Neurobiol. Aging, 2005, 26(6), 965-972. [http://dx.doi.org/10.1016/j.neurobiolaging.2004.07.004] [PMID: 15718056]
47. Kannan, K.; Jain, S.K. Oxidative stress and apoptosis. Pathophysiology, 2000, 7(3), 153-163. [http://dx.doi.org/10.1016/S0928-4680(00)00053-5] [PMID: 10996508]
48. Nogueira, T.C.; Paula, F.M.; Villate, O.; Colli, M.L.; Moura, R.F.; Cunha, D.A.; Marselli, L.; Marchetti, P.; Cnop, M.; Julier, C.; Eizirik, D.L. GLIS3, a susceptibility gene for type 1 and type 2 diabetes, modulates pancreatic beta cell apoptosis via regulation of a splice variant of the BH3-only protein Bim. PLoS Genet., 2013, 9(5), e1003532. [http://dx.doi.org/10.1371/journal.pgen.1003532] [PMID: 23737756]
49. Khalfaoui, T.; Basora, N.; Ouertani-Meddeb, A. Apoptotic factors (Bcl-2 and Bax) and diabetic retinopathy in type 2 diabetes. J. Mol. Histol., 2010, 41(2-3), 143-152. [http://dx.doi.org/10.1007/s10735-010-9271-9] [PMID: 20532811]
50. Romeo, G.; Liu, W.H.; Asnaghi, V.; Kern, T.S.; Lorenzi, M. Activation of nuclear factor-kappaB induced by diabetes and high glucose regulates a proapoptotic program in retinal pericytes. Diabetes, 2002, 51(7), 2241-2248. [http://dx.doi.org/10.2337/diabetes.51.7.2241] [PMID: 12086956]
51. Valverde, A.M.; Miranda, S.; Garcia-Ramirez, M.; Gonzalez-Rodriguez, A.; Hernandez, C.; Simo, R. Proapoptotic and survival signaling in the neuroretina at early stages of diabetic retinopathy. Mol. Vis., 2013, 19, 47-53. [PMID: 23335850]
52. Abu El-Asrar, A.M.; Dralands, L.; Missotten, L.; Geboes, K. Expression of antiapoptotic and proapoptotic molecules in diabetic retinas. Eye (Lond.), 2007, 21(2), 238-245. [http://dx.doi.org/10.1038/sj.eye.6702225] [PMID: 16424911]
53. Yang, P.; Peairs, J.J.; Tano, R.; Zhang, N.; Tyrell, J.; Jaffe, G.J. Caspase-8-mediated apoptosis in human RPE cells. Invest. Ophthalmol. Vis. Sci., 2007, 48(7), 3341-3349. [http://dx.doi.org/10.1167/iovs.06-1340] [PMID: 17591907]
54. Bhattacharya, S.; Manna, P.; Gachhui, R.; Sil, P.C. D-saccharic acid-1,4-lactone ameliorates alloxan-induced diabetes mellitus and oxidative stress in rats through inhibiting pancreatic β-cells from apoptosis via mitochondrial dependent pathway. Toxicol. Appl. Pharmacol., 2011, 257(2), 272-283. [http://dx.doi.org/10.1016/j.taap.2011.09.013] [PMID: 21982801]
55. Mohr, S. Caspase-1/interleukin-1beta signaling in diabetic retinopathy. Acta Ophthalmologica, 2008, 86, S243. [http://dx.doi. org/10.1111/j.1755-3768.2008.6114.x]
56. Ortis, F.; Cardozo, A.K.; Crispim, D.; Storling, J.; Mandrup-Poulsen, T.; Eizirik, D.L. Cytokine-induced proapoptotic gene expression in insulin-producing cells is related to rapid, sustained, and nonoscillatory nuclear factor-kappaB activation. Mol. Endocrinol., 2006, 20(8), 1867-1879. [http://dx.doi.org/10.1210/me.2005-0268] [PMID: 16556731]
57. Kern, T.S.; Du, Y.; Miller, C.M.; Hatala, D.A.; Levin, L.A. Overexpression of Bcl-2 in vascular endothelium inhibits the microvascular lesions of diabetic retinopathy. Am. J. Pathol., 2010, 176(5), 2550-2558. [http://dx.doi.org/10.2353/ajpath.2010.091062] [PMID: 20363911]
58. Costa, G.N.; Vindeirinho, J.; Cavadas, C.; Ambrosio, A.F.; Santos, P.F. Contribution of TNF receptor 1 to retinal neural cell death induced by elevated glucose. Mol. Cell. Neurosci., 2012, 50(1), 113-123. [http://dx.doi.org/10.1016/j.mcn.2012.04.003] [PMID: 22522145]
59. Oshitari, T.; Brown, D.; Roy, S. SiRNA strategy against overexpression of extracellular matrix in diabetic retinopathy. Exp. Eye Res., 2005, 81(1), 32-37. [http://dx.doi.org/10.1016/j.exer. 2005.01.006] [PMID: 15978252]
60. Oshitari, T.; Yamamoto, S.; Roy, S. Increased expression of c-Fos, c-Jun and c-Jun N-terminal kinase associated with neuronal cell death in retinas of diabetic patients. Curr. Eye Res., 2014, 39(5), 527-531. [http://dx.doi.org/10.3109/02713683.2013.833248] [PMID: 24073601]
61. Rogowicz-Frontczak, A.; Pilacinski, S.; Araszkiewicz, A.; Zozulinska-Ziolkiewicz, D.; Wykretowicz, A.; Wierusz-Wysocka, B. C-Reactive protein and soluble intracellular adhesion molecule-1 are related to pulse wave reflection in type 1 diabetes 1C-1. J. Diabetes, 2014, 6(6), 577-585. [http://dx.doi.org/10.1111/1753-0407.12129] [PMID: 24456036]
62. Yu, Y.; Chen, H.; Su, S.B. Neuroinflammatory responses in diabetic retinopathy. J. Neuroinflammation, 2015, 12, 141. [http://dx.doi.org/10.1186/s12974-015-0368-7] [PMID: 26245868]
63. Abcouwer, S.F.; Gardner, T.W. Diabetic retinopathy: loss of neuroretinal adaptation to the diabetic metabolic environment. Ann. N. Y. Acad. Sci., 2014, 1311, 174-190. [http://dx.doi.org/10.1111/nyas.12412] [PMID: 24673341]
64. Crane, I.J.; Liversidge, J. Mechanisms of leukocyte migration across the blood-retina barrier. Semin. Immunopathol., 2008, 30(2), 165-177. [http://dx.doi.org/10.1007/s00281-008-0106-7] [PMID: 18305941]
65. Cahoon, J.M.; Olson, P.R.; Nielson, S.; Miya, T.R.; Bankhead, P.; McGeown, J.G.; Curtis, T.M.; Ambati, B.K. Acridine orange leukocyte fluorography in mice. Exp. Eye Res., 2014, 120, 15-19. [http://dx.doi.org/10.1016/j.exer.2013.12.002] [PMID: 24333760]
66. Zorena, K.; Malinowska, E.; Raczyńska, D.; Myśliwiec, M.; Raczyńska, K. Serum concentrations of transforming growth factor-Beta 1 in predicting the occurrence of diabetic retinopathy in juvenile patients with type 1 diabetes mellitus. J. Diabetes Res., 2013, 2013, 614908. [http://dx.doi.org/10.1155/2013/614908] [PMID: 23671881]
67. Oh, I.K.; Kim, S.W.; Oh, J.; Lee, T.S.; Huh, K. Inflammatory and angiogenic factors in the aqueous humor and the relationship to diabetic retinopathy. Curr. Eye Res., 2010, 35(12), 1116-1127. [http://dx.doi.org/10.3109/02713683.2010.510257] [PMID: 21121809]
68. 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 of Inflammation, 2012. Article ID 697489, 7 pages, 2012 [http://dx.doi.org/10.1155/2012/697489]
69. Petrovič, M.G.; Korošec, P.; Košnik, M.; Hawlina, M. Vitreous levels of interleukin-8 in patients with proliferative diabetic retinopathy. Am. J. Ophthalmol., 2007, 143(1), 175-176. [http://dx.doi. org/10.1016/j.ajo.2006.07.032] [PMID: 17188064]
70. Hernandez, C.; Fonollosa, A.; Garcia-Ramirez, M.; Higuera, M.; Catalan, R.; Miralles, A.; Garcia-Arumi, J.; Simo, R. Erythropoietin is expressed in the human retina and it is highly elevated in the vitreous fluid of patients with diabetic macular edema. Diabetes Care, 2006, 29(9), 2028-2033. [http://dx.doi.org/10.2337/dc06-0556] [PMID: 16936148]
71. Ersoy, L.; Ristau, T.; Hahn, M.; Karlstetter, M.; Langmann, T.; Droge, K.; Caramoy, A.; den Hollander, A.I.; Fauser, S. Genetic and environmental risk factors for age-related macular degeneration in persons 90 years and older. Invest. Ophthalmol. Vis. Sci., 2014, 55(3), 1842-1847. [http://dx.doi.org/10.1167/iovs.13-13420] [PMID: 24576882]
72. Doria, A. Genetics of diabetes complications. Curr. Diab. Rep., 2010, 10(6), 467-475. [http://dx.doi.org/10.1007/s11892-010-0147- x] [PMID: 20835900]
73. Cilenšek, I.; Hercegovac, A.; Vukojević, K.; Babić, M.S.; Milutinović Živin, A. Polymorphisms of interleukin-4, -10 and 12B genes and diabetic retinopathy. Cent. Eur. J. Biol., 2011, 6, 558-564.
74. Petrovič, D. Candidate genes for proliferative diabetic retinopathy. BioMed Res. Int., 2013, 2013, 540416. [http://dx.doi.org/10.1155/2013/540416] [PMID: 24066292]
75. Awata, T.; Inoue, K.; Kurihara, S.; Ohkubo, T.; Watanabe, M.; Inukai, K.; Inoue, I.; Katayama, S. A common polymorphism in the 5′-untranslated region of the VEGF gene is associated with diabetic retinopathy in type 2 diabetes. Diabetes, 2002, 51(5), 1635-1639. [http://dx.doi.org/10.2337/diabetes.51.5.1635] [PMID: 11978667]
76. Choudhuri, S.; Chowdhury, I.H.; Das, S.; Dutta, D.; Saha, A.; Sarkar, R.; Mandal, L.K.; Mukherjee, S.; Bhattacharya, B. Role of NF-κB activation and VEGF gene polymorphisms in VEGF up regulation in non-proliferative and proliferative diabetic retinopathy. Mol. Cell. Biochem., 2015, 405(1-2), 265-279. [http://dx.doi.org/10.1007/s11010-015-2417-z] [PMID: 25956512]
77. Barengo, N.C.; Tuomilehto, J.O. Blood pressure treatment target in patients with diabetes mellitus-current evidence. Ann. Med., 2012, 44(Suppl. 1), S36-S42. [http://dx.doi.org/10.3109/07853890.2012. 679961] [PMID: 22713147]
78. Izzo, R.; de Simone, G.; Trimarco, V.; Gerdts, E.; Giudice, R.; Vaccaro, O.; De Luca, N.; Trimarco, B. Hypertensive target organ damage predicts incident diabetes mellitus. Eur. Heart J., 2013, 34(44), 3419-3426. [http://dx.doi.org/10.1093/eurheartj/eht281] [PMID: 23882068]
79. Zorena, K.; Myśliwska, J.; Myśliwiec, M.; Rybarczyk-Kapturska, K.; Malinowska, E.; Wiśniewski, P.; Raczyńska, K. Association between vascular endothelial growth factor and hypertension in children and adolescents type I diabetes mellitus. J. Hum. Hypertens., 2010, 24(11), 755-762. [http://dx.doi.org/10.1038/jhh.2010.7] [PMID: 20164848]
80. Pons, M.; Marin-Castano, M.E. Cigarette smoke-related hydroquinone dysregulates MCP-1, VEGF and PEDF expression in retinal pigment epithelium in vitro and in vivo. PLoS One, 2011, 6(2), e16722. [http://dx.doi.org/10.1371/journal.pone.0016722] [PMID: 21386905]
81. Csiszar, A.; Gautam, T.; Sosnowska, D.; Tarantini, S.; Banki, E.; Tucsek, Z.; Toth, P.; Losonczy, G.; Koller, A.; Reglodi, D.; Giles, C.B.; Wren, J.D.; Sonntag, W.E.; Ungvari, Z. Caloric restriction confers persistent anti-oxidative, pro-angiogenic, and antiinflammatory effects and promotes anti-aging miRNA expression profile in cerebromicrovascular endothelial cells of aged rats. Am. J. Physiol. Heart Circ. Physiol., 2014, 307(3), H292-H306. [http://dx.doi.org/10.1152/ajpheart.00307.2014] [PMID: 24906921]
82. Uruska, A.; Araszkiewicz, A.; Uruski, P.; Zozulinska-Ziolkiewicz, D. Higher risk of microvascular complications in smokers with type 1 diabetes despite intensive insulin therapy. Microvasc. Res., 2014, 92, 79-84. [http://dx.doi.org/10.1016/j.mvr.2014.01.002] [PMID: 24423616]
83. Lieth, E.; Gardner, T.W.; Barber, A.J.; Antonetti, D.A. Retinal neurodegeneration: early pathology in diabetes. Clin. Experiment. Ophthalmol., 2000, 28(1), 3-8. [http://dx.doi.org/10.1046/j.1442-9071.2000.00222.x] [PMID: 11345341]
84. Kim, D.Y.; Jung, S.Y.; Kim, C.J.; Sung, Y.H.; Kim, J.D. Treadmill exercise ameliorates apoptotic cell death in the retinas of diabetic rats. Mol. Med. Rep., 2013, 7(6), 1745-1750. [PMID: 23620139]
85. Ji, E.S.; Ko, I.G.; Cho, J.W.; Davis, R.W.; Hwang, G.Y.; Jee, Y.S.; Lim, B.V. Treadmill exercise inhibits apoptotic neuronal cell death with suppressed vascular endothelial growth factor expression in the retinas of the diabetic rats. J. Exerc. Rehabil., 2013, 9(3), 348-353. [http://dx.doi.org/10.12965/jer.130043] [PMID: 24278883]
86. Marchetti, V.; Yanes, O.; Aguilar, E.; Wang, M.; Friedlander, D.; Moreno, S.; Storm, K.; Zhan, M.; Naccache, S.; Nemerow, G.; Siuzdak, G.; Friedlander, M. Differential macrophage polarization promotes tissue remodeling and repair in a model of ischemic retinopathy. Sci. Rep., 2011, 1, 76. [http://dx.doi.org/10.1038/srep00076] [PMID: 22355595]
87. Li, P.; Xu, X.; Zheng, Z.; Zhu, B.; Shi, Y.; Liu, K. Protective effects of rosiglitazone on retinal neuronal damage in diabetic rats. Curr. Eye Res., 2011, 36(7), 673-679. [http://dx.doi.org/10.3109/02713683.2011.572220] [PMID: 21599458]
88. Nissen, S.E.; Wolski, K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N. Engl. J. Med., 2007, 356(24), 2457-2471. [http://dx.doi.org/10.1056/NEJMoa072761] [PMID: 17517853]
89. Goncalves, A.; Leal, E.; Paiva, A.; Teixeira Lemos, E.; Teixeira, F.; Ribeiro, C.F.; Reis, F.; Ambrosio, A.F.; Fernandes, R. Protective effects of the dipeptidyl peptidase IV inhibitor sitagliptin in the blood-retinal barrier in a type 2 diabetes animal model. Diabetes Obes. Metab., 2012, 14(5), 454-463. [http://dx.doi.org/10.1111/j.1463-1326.2011.01548.x] [PMID: 22151893]
90. Goncalves, A.; Marques, C.; Leal, E.; Ribeiro, C.F.; Reis, F.; Ambrosio, A.F.; Fernandes, R. Dipeptidyl peptidase-IV inhibition prevents blood-retinal barrier breakdown, inflammation and neuronal cell death in the retina of type 1 diabetic rats. Biochim. Biophys. Acta, 2014, 1842(9), 1454-1463. [http://dx.doi.org/10.1016/j.bbadis.2014.04.013] [PMID: 24769045]
91. Jung, K.I.; Kim, J.H.; Park, H.Y.; Park, C.K. Neuroprotective effects of cilostazol on retinal ganglion cell damage in diabetic rats. J. Pharmacol. Exp. Ther., 2013, 345(3), 457-463. [http://dx.doi. org/10.1124/jpet.113.203067] [PMID: 23536314]
92. Sun, W.; Gerhardinger, C.; Dagher, Z.; Hoehn, T.; Lorenzi, M. Aspirin at low-intermediate concentrations protects retinal vessels in experimental diabetic retinopathy through non-platelet-mediated effects. Diabetes, 2005, 54(12), 3418-3426. [http://dx.doi.org/10.2337/diabetes.54.12.3418] [PMID: 16306357]
93. El-Remessy, A.B.; Al-Shabrawey, M.; Khalifa, Y.; Tsai, N.T.; Caldwell, R.B.; Liou, G.I. Neuroprotective and blood-retinal barrier-preserving effects of cannabidiol in experimental diabetes. Am. J. Pathol., 2006, 168(1), 235-244. [http://dx.doi.org/10.2353/ajpath.2006.050500] [PMID: 16400026]
94. Casini, G.; Dal Monte, M.; Fornaciari, I.; Filippi, L.; Bagnoli, P. The β-adrenergic system as a possible new target for pharmacologic treatment of neovascular retinal diseases. Prog. Retin. Eye Res., 2014, 42, 103-129. [http://dx.doi.org/10.1016/j.preteyeres. 2014.06.001] [PMID: 24933041]
95. Sohn, E.J.; Kim, Y.S.; Kim, C.S.; Lee, Y.M.; Kim, J.S. KIOM-79 prevents apoptotic cell death and AGEs accumulation in retinas of diabetic db/db mice. J. Ethnopharmacol., 2009, 121(1), 171-174. [http://dx.doi.org/10.1016/j.jep.2008.09.036] [PMID: 19013511]
96. Dong, Z.; Tao, X.; Fu, X.; Wang, H.; Wang, D.; Zhang, T. Protective effects of Purendan superfine powder on retinal neuron apoptosis in a rat model of type 2 diabetes mellitus. Neural Regen. Res., 2012, 7(3), 202-206. [PMID: 25767500]
97. Kim, J.; Kim, C.S.; Lee, Y.M.; Sohn, E.; Jo, K.; Kim, J.S. Litsea japonica extract inhibits neuronal apoptosis and the accumulation of advanced glycation end products in the diabetic mouse retina. Mol. Med. Rep., 2015, 12(1), 1075-1081. [PMID: 25815519]