Diabetic retinopathy: Breaking the barrier

Pathophysiology

Volumn 24, Issue 4, 2017, Pages 229-241

  Eshaq, Randa S ^a   Aldalati, Alaa M Z ^a   Alexander, J Steven ^a   Harris, Norman R ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Blood retinal barrier; Diabetes; Oxidative stress; Permeability; Retina

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CD31 ANTIGEN; DNA; GLUCOSE; INTERCELLULAR ADHESION MOLECULE 1; KALLIKREIN; KININ; POLYOL; PROTEIN KINASE C; VASCULOTROPIN;

BIOCHEMISTRY; BLINDNESS; BLOOD RETINA BARRIER; CELL SURFACE; DIABETIC RETINOPATHY; DISEASE COURSE; DNA MODIFICATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; GLYCOCALYX; HUMAN; HYPERGLYCEMIA; INFLAMMATION; INFLAMMATORY CELL; INSULIN DEPENDENT DIABETES MELLITUS; LEUKOCYTE ADHERENCE; MICROANGIOPATHY; MOLECULAR MECHANICS; NERVE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERICYTE; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA BLOOD VESSEL; REVIEW; THROMBOCYTE ADHESION; VASCULAR ENDOTHELIAL CELL;

EID: 85024373116     PISSN: 09284680     EISSN: 1873149X     Source Type: Journal    
DOI: 10.1016/j.pathophys.2017.07.001     Document Type: Review

References (207)

1. Retinal Conditions − Common Eye Disorders|Vision Health Initiative (VHI)|. 2014 [cited; Available from: http://www.cdc.gov/visionhealth/basic_information/eye_disorders_retinal.htm.
2. Yau, J.W., Rogers, S.L., Kawasaki, R., Lamoureux, E.L., Kowalski, J.W., Bek, T., et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 35:March (3) (2012), 556–564.
3. Fowler, M.J., Microvascular and macrovascular complications of diabetes. Clinical Diabetes 26:2 (2008), 77–82.
4. Morello, C.M., Etiology and natural history of diabetic retinopathy: an overview. Am. J. Health. Syst. Pharm. 64:September (17 Suppl 12) (2007), S3–7.
5. Klein, B.E., Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol. 14:July–August (4) (2007), 179–183.
6. Madsen–Bouterse, S.A., Mohammad, G., Kanwar, M., Kowluru, R.A., Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with its progression. Antioxid Redox Signal. 13:6 (2010), 797–805 http://dxdoiorg/101089/ars20092932.
7. Villeneuve, L.M., Natarajan, R., The role of epigenetics in the pathology of diabetic complications. Am. J. Physiol. Renal Physiol. 299:1 (2010), F14–F25.
8. Espaillat, A., Diabetic Eye Disease: A Comprehensive Review. 2012, Slack incorporated, Thorofare, NJ.
9. Jonas, D., Van Scoyoc, E., Gerrald, K., Wines, R., Amick, H., Triplette, M., et al. Drug Class Review: Newer Diabetes Medications, TZDs and Combinations: Final Original Report., 2011 (2011/02).
10. Group TDCaCTEoDIaCR, Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy — NEJM. N. Engl. J. Med. 2000:342 (2000), 381–389.
11. Nathan, D.M., Group ftDER, The diabetes control and complications Trial/Epidemiology of diabetes interventions and complications study at 30 years: overview. Diabetes Care 37:1 (2014), 9–16.
12. White, N.H., Sun, W., Cleary, P.A., Danis, R.P., Davis, M.D., Hainsworth, D.P., et al. Prolonged effect of intensive therapy on the risk of retinopathy complications in patients with type 1 diabetes mellitus: 10 years after the Diabetes Control and Complications Trial. Arch. Ophthalmol. 126:December (12) (2008), 1707–1715.
13. Drzewoski, J., Kasznicki, J., Trojanowski, Z., The role of metabolic memory in the natural history of diabetes mellitus. Pol. Arch. Med. Wewn. 119:July–August (7–8) (2009), 493–500.
14. Ceriello, A., Hypothesis: the metabolic memory, the new challenge of diabetes. Diabetes Res. Clin. Pract. 86:December (Supp l) (2009), S2–6.
15. Ceriello, A., Ihnat, M.A., Thorpe, J.E., Clinical review 2: The metabolic memory: is more than just tight glucose control necessary to prevent diabetic complications?. J. Clin. Endocrinol. Metab. 94:February (2) (2009), 410–415.
16. Chilelli, N.C., Burlina, S., Lapolla, A., AGEs, rather than hyperglycemia, are responsible for microvascular complications in diabetes: a glycoxidation-centric point of view. Nutr. Metab. Cardiovasc. Dis. 23:October (10) (2013), 913–919.
17. Kowluru, R.A., Mitochondria damage in the pathogenesis of diabetic retinopathy and in the metabolic memory associated with its continued progression. Curr. Med. Chem. 20:26 (2013), 3226–3233.
18. Kowluru, R.A., Santos, J.M., Mishra, M., Epigenetic modifications and diabetic retinopathy. BioMed Res. Int., 2013, 2013, 635284.
19. Perrone, L., Matrone, C., Singh, L.P., Epigenetic modifications and potential new treatment targets in diabetic retinopathy. J. Ophthalmol., 2014, 2014, 789120.
20. Hein, T.W., Xu, W., Xu, X., Acute, Kuo L., Chronic hyperglycemia elicit JIP1/JNK-Mediated endothelial vasodilator dysfunction of retinal arterioles. Invest. Ophthalmol. Vis. Sci. 57:August (10) (2016), 4333–4340.
21. Hein, T.W., Potts, L.B., Xu, W., Yuen, J.Z., Kuo, L., Temporal development of retinal arteriolar endothelial dysfunction in porcine type 1 diabetes. Invest. Ophthalmol. Vis. Sci. 53:December (13) (2012), 7943–7949.
22. Nguyen, T.T., Kawasaki, R., Wang, J.J., Kreis, A.J., Shaw, J., Vilser, W., et al. Flicker light-induced retinal vasodilation in diabetes and diabetic retinopathy. Diabetes Care. 32:November (11) (2009), 2075–2080.
23. Fong, D.S., Aiello, L., Gardner, T.W., King, G.L., Blankenship, G., Cavallerano, J.D., et al. Diabetic Retinopathy. 26:1 (2003), 226–229.
24. Van Geest, R.J., Lesnik-Oberstein, S.Y., Tan, H.S., Mura, M., Goldschmeding, R., Van Noorden CJ, et al: a shift in the balance of vascular endothelial growth factor and connective tissue growth factor by bevacizumab causes the angiofibrotic switch in proliferative diabetic retinopathy. Br. J. Ophthalmol. 96:April (4) (2012), 587–590.
25. Gholamhossein, Y., Behrouz, H., Asghar, Z., Diabetic retinopathy risk factors: plasma erythropoietin as a risk factor for proliferative diabetic retinopathy. Korean J. Ophthalmol. 28:October (5) (2014), 373–378.
26. Takagi, H., Watanabe, D., Suzuma, K., Kurimoto, M., Suzuma, I., Ohashi, H., et al. Novel role of erythropoietin in proliferative diabetic retinopathy. Diabetes Res. Clin. Pract. 77:September (Suppl. 1) (2007), S62–64.
27. Wen, C.T., He, T., Xing, Y.Q., Erythropoietin promotes retinal angiogenesis in a mouse model. Mol. Med. Rep. 10:December (6) (2014), 2979–2984.
28. Kalantzis, G., Angelou, M., Poulakou-Rebelakou, E., Diabetic retinopathy: an historical assessment. Hormones (Athens) 5:January–March (1) (2006), 72–75.
29. Joslin, E.P., Apollinaire bouchardat 1806–1886. Diabetes Its Medical and Cultural History, 1989, 359–362.
30. Chast, F., Slama, G., Apollinaire bouchardat and diabetes. Hist. Sci. Med. 41:July–September (3) (2007), 287–301.
31. Fischer, F., The First Case of Diabetic Retinopathy. Diabetes Its Medical and Cultural History, 1989, 363–369.
32. Noyes, H.D., Retinitis in glycosuria. Trans. Am. Ophthalmol. Soc. 1:4–5 (1868), 71–75.
33. Digre, K.B., Practical Viewing of the Optic Disc. 2003, Elsvire Science, Burlington, MA.
34. Fleming, N.B.B., Case of retinitis proliferans without history. Proc. R. Soc. Med. 21:September (11) (1928), 1805–1806.
35. Tattersall, Diabetes: The Biography. 2009, Oxford University Press.
36. Ballantyne, A.J., The ocular manifestations of spontaneous subarachnoid haemorrhage. Br. J. Ophthalmol. 27:September (9) (1943), 383–414.
37. Minagar, A., Alexander, J.S., Blood-brain barrier disruption in multiple sclerosis. Mult. Scler. 9:December (6) (2003), 540–549.
38. Trick, G.L., Berkowtiz, B.A., Retinal oxygenation response and retinopathy. Prog. Retin. Eye Res. 24:2 (2005), 259–274.
39. Purves, D., Augustine, G.J., Fitzpatrick, D., et al. (eds.) Neuroscience, 2nd edition, 2001, Sinauer Associates, Sunderland (MA) The Retina.
40. Saidha, S., Syc, S.B., Ibrahim, M.A., Eckstein, C., Warner, C.V., Farrell, S.K., et al. Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 134:February (Pt 2) (2011), 518–533.
41. Kevil, C.G., Oshima, T., Alexander, B., Coe, L.L., Alexander, J.S., H(2)O(2)-mediated permeability: role of MAPK and occludin. Am. J. Physiol. Cell Physiol. 279:July (1) (2000), C21–30.
42. Blaschuk, O.W., Oshima, T., Gour, B.J., Symonds, J.M., Park, J.H., Kevil, C.G., et al. Identification of an occludin cell adhesion recognition sequence. Inflammation 26:August (4) (2002), 193–198.
43. Dejana, E., Orsenigo, F., Lampugnani, M.G., The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell Sci. 121:July (Pt 13) (2008), 2115–2122.
44. Dejana, E., Endothelial cell–cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5:April (4) (2004), 261–270.
45. Tzima, E., Irani-Tehrani, M., Kiosses, W.B., Dejana, E., Schultz, D.A., Engelhardt, B., et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437:7057 (2005), 426–431.
46. Dejana, E., Bazzoni, G., Lampugnani, M.G., Vascular endothelial (VE)-cadherin: only an intercellular glue?. Exp. Cell Res. 252:October (1) (1999), 13–19.
47. Ilan, N., Mahooti, S., Rimm, D.L., Madri, J.A., PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated beta-catenin. J. Cell Sci. 112:September (Pt 18) (1999), 3005–3014.
48. Ilan, N., Mohsenin, A., Cheung, L., Madri, J.A., PECAM-1 shedding during apoptosis generates a membrane-anchored truncated molecule with unique signaling characteristics. FASEB J. 15:February (2) (2001), 362–372.
49. Newman, P.J., Newman, D.K., Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler Thromb Vasc Biol. United States, 2003, 953–964.
50. Cai, J., Boulton, M., The pathogenesis of diabetic retinopathy: old concepts and new questions. Eye (Lond). 16:May (3) (2002), 242–260.
51. Bergua, A., Kapsreiter, M., Neuhuber, W.L., Reitsamer, H.A., Schrodl, F., Innervation pattern of the preocular human central retinal artery. Exp. Eye Res. 110:May (2013), 142–147.
52. Lorenzi, M., The polyol pathway as a mechanism for diabetic retinopathy: attractive, elusive, and resilient. Exp. Diabetes Res., 2007, 2007, 61038.
53. Safi, S.Z., Qvist, R., Kumar, S., Batumalaie, K., Ismail, I.S., Molecular mechanisms of diabetic retinopathy, general preventive strategies, and novel therapeutic targets. BioMed Res. Int., 2014, 2014, 801269.
54. Gabbay, K.H., The sorbitol pathway and the complications of diabetes. N. Engl. J. Med. 288:April (16) (1973), 831–836.
55. Kitada, M., Zhang, Z., Mima, A., King, G.L., Molecular mechanisms of diabetic vascular complications. J Diabetes Investig. 1:June (3) (2010), 77–89.
56. Tarr, J.M., Kaul, K., Chopra, M., Kohner, E.M., Chibber, R., Pathophysiology of diabetic retinopathy. ISRN Ophthalmol., 2013, 2013, 343560.
57. Hoffmann, E.K., Lambert, I.H., Pedersen, S.F., Physiology of cell volume regulation in vertebrates. Physiol. Rev. 89:1 (2009), 193–277.
58. Burg, M.B., Ferraris, J.D., Dmitrieva, N.I., Cellular response to hyperosmotic stresses. Physiol. Rev. 87:October (4) (2007), 1441–1474.
59. Willermain, F., Department of ophthalmology CS-PaB, brussels, belgium, janssens S, department of ophthalmology CS-PaB, brussels, belgium, arsenijevic T, laboratory of pathophysiological and nutritional biochemistry ULdB, brussels, Belgium, et al osmotic stress decreases aquaporin-4 expression in the human retinal pigment epithelial cell line, ARPE-19. Int. J. Mol. Med. 34:2 (2014), 533–538.
60. Omori, K., Fujiseki, Y., Suzukawa, J., Inagaki, C., Regulation of the expression of lysyl oxidase mRNA in cultured rabbit retinal pigment epithelium cells. Matrix Biol. 21:June (4) (2002), 337–348.
61. Obrosova, I.G., Increased sorbitol pathway activity generates oxidative stress in tissue sites for diabetic complications. Antioxid. Redox Signal. 7:November–December (11k12) (2005), 1543–1552.
62. Obrosova, I.G., Kador, P.F., Aldose reductase/polyol inhibitors for diabetic retinopathy. Curr. Pharm. Biotechnol. 12:March (3) (2011), 373–385.
63. Cheng, H.M., González, R.G., The effect of high glucose and oxidative stress on lens metabolism, aldose reductase, and senile cataractogenesis. Metabolism 35:April (4 Suppl. 1) (1986), 10–14.
64. Suarez, G., Rajaram, R., Oronsky, A.L., Gawinowicz, M.A., Nonenzymatic glycation of bovine serum albumin by fructose (fructation): Comparison with the Maillard reaction initiated by glucose. J. Biol. Chem. 264:March (7) (1989), 3674–3679.
65. Vinores, S.A., Van Niel, E., Swerdloff, J.L., Campochiaro PA. Electron microscopic immunocytochemical demonstration of blood-retinal barrier breakdown in human diabetics and its association with aldose reductase in retinal vascular endothelium and retinal pigment epithelium. Histochem. J. 25:September (9) (1993), 648–663.
66. Barnett, P.A., Gonzalez, R.G., Chylack, L.T. Jr., Cheng, H.M., The effect of oxidation on sorbitol pathway kinetics. Diabetes 35:April (4) (1986), 426–432.
67. Williamson, J.R., Chang, K., Frangos, M., Hasan, K.S., Ido, Y., Kawamura, T., et al. Hyperglycemic pseudohypoxia and diabetic complications. Diabetes 42:June (6) (1993), 801–813.
68. Gomes, A.P., Price, N.L., Ling, A.J., Moslehi, J.J., Montgomery, M.K., Rajman, L., et al. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 155:December (7) (2013), 1624–1638.
69. Singh, V.P., Bali, A., Singh, N., Jaggi, A.S., Advanced glycation end products and diabetic complications. Korean J. Physiol. Pharmacol. 18:February (1) (2014), 1–14.
70. Kandarakis, S.A., Piperi, C., Topouzis, F., Papavassiliou, A.G., Emerging role of advanced glycation-end products (AGEs) in the pathobiology of eye diseases. Prog. Retin. Eye Res. 42:September (2014), 85–102.
71. Alexiou, P., Pegklidou, K., Chatzopoulou, M., Nicolaou, I., Demopoulos, V.J., Aldose reductase enzyme and its implication to major health problems of the 21(st) century. Curr. Med. Chem. 16:6 (2009), 734–752.
72. Kumar, H., Shah, A., Sobhia, M.E., Novel insights into the structural requirements for the design of selective and specific aldose reductase inhibitors. J. Mol. Model. 18:May (5) (2012), 1791–1799.
73. Wermuth, B., Burgisser, H., Bohren K, von Wartburg JP: Purification and characterization of human-brain aldose reductase. Eur. J. Biochem. 127:October (2) (1982), 279–284.
74. Ris, M.M., von Wartburg, J.P., Heterogeneity of NADPH-dependent aldehyde reductase from human and rat brain. Eur. J. Biochem. 37:August (1) (1973), 69–77.
75. Schmidt, A.M., Hori, O., Brett, J., Yan, S.D., Wautier, J.L., Stern, D., Cellular receptors for advanced glycation end products: implications for induction of oxidant stress and cellular dysfunction in the pathogenesis of vascular lesions. Arterioscler. Thromb. 14:October (10) (1994), 1521–1528.
76. Kandarakis, S.A., Piperi, C., Topouzis, F., Papavassiliou, A.G., Emerging role of advanced glycation-end products (AGEs) in the pathobiology of eye diseases. Prog. Retin. Eye Res. 42c:September (2014), 85–102.
77. Brownlee, M., Advanced protein glycosylation in diabetes and aging. Annu. Rev. Med. 46 (1995), 223–234.
78. Schmidt, A.M., Hori, O., Brett, J., Yan, S.D., Wautier, J.L., Stern, D., Cellular receptors for advanced glycation end products. Implications for induction of oxidant stress and cellular dysfunction in the pathogenesis of vascular lesions. Arterioscler Throm 14:10 (1994), 1521–1528.
79. Sharma, S.D., Pandey, B.N., Mishra, K.P., Sivakami, S., Amadori product and age formation during nonenzymatic glycosylation of bovine serum albumin in vitro. J. Biochem. Mol. Biol. Biophys. 6:August (4) (2002), 233–242.
80. Baynes, J.W., Thorpe, S.R., Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48:January (1) (1999), 1–9.
81. Suzuki, D., Miyata, T., Saotome, N., Horie, K., Inagi, R., Yasuda, Y., et al. Immunohistochemical evidence for an increased oxidative stress and carbonyl modification of proteins in diabetic glomerular lesions. J. Am. Soc. Nephrol. 10:April (4) (1999), 822–832.
82. Lo, T.W., Westwood, M.E., McLellan, A.C., Selwood, T., Thornalley, P.J., Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N alpha-acetylarginine, N alpha-acetylcysteine, and N alpha-acetyllysine, and bovine serum albumin. J. Biol. Chem. 269:December (51) (1994), 32299–32305.
83. Frye, E.B., Degenhardt, T.P., Thorpe, S.R., Baynes, J.W., Role of the Maillard reaction in aging of tissue proteins: advanced glycation end product-dependent increase in imidazolium cross-links in human lens proteins. J. Biol. Chem. 273:July (24) (1998), 18714–18719.
84. Ahmed, M.U., Thorpe, S.R., Baynes, J.W., Identification of N epsilon-carboxymethyllysine as a degradation product of fructoselysine in glycated protein. J. Biol. Chem. 261:April (11) (1986), 4889–4894.
85. Schmidt, A.M., Vianna, M., Gerlach, M., Brett, J., Ryan, J., Kao, J., et al. Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J. Biol. Chem. 267:July (21) (1992), 14987–14997.
86. Schmidt, A.M., Yan, S.D., Yan, S.F., Stern, D.M., The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J. Clin. Invest., 2001, 949–955.
87. Maeda, S., Matsui, T., Ojima, A., Takeuchi, M., Yamagishi, S., Sulforaphane inhibits advanced glycation end product-induced pericyte damage by reducing expression of receptor for advanced glycation end products. Nutr. Res. 34:September (9) (2014), 807–813.
88. Choudhuri, S., Dutta, D., Sen, A., Chowdhury, I.H., Mitra, B., Mondal, L.K., et al. Role of N-epsilon- carboxy methyl lysine, advanced glycation end products and reactive oxygen species for the development of nonproliferative and proliferative retinopathy in type 2 diabetes mellitus. Mol. Vis. 19 (2013), 100–113.
89. Lyons, T.J., Basu, A., Biomarkers in diabetes: hemoglobin A1c, vascular and tissue markers. Transl. Res. 159:April (4) (2012), 303–312.
90. Sheikpranbabu, S., Haribalaganesh, R., Gurunathan, S., Pigment epithelium-derived factor inhibits advanced glycation end-products-induced cytotoxicity in retinal pericytes. Diabetes Metab. 37:December (6) (2011), 505–511.
91. Genuth, S., Sun, W., Cleary, P., Sell, D.R., Dahms, W., Malone, J., et al. Glycation and carboxymethyllysine levels in skin collagen predict the risk of future 10-year progression of diabetic retinopathy and nephropathy in the diabetes control and complications trial and epidemiology of diabetes interventions and complications participants with type 1 diabetes. Diabetes 54:November (11) (2005), 3103–3111.
92. Koya, D., King, G.L., Protein kinase C activation and the development of diabetic complications. Diabetes 47:June (6) (1998), 859–866.
93. Newton, A.C., Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem. J 370:March (Pt 2) (2003), 361–371.
94. Nishizuka, Y., The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:August (6184) (1988), 661–665.
95. Huang, Q., Yuan, Y., Interaction of PKC and NOS in signal transduction of microvascular hyperpermeability. Am. J. Physiol. 273:November (5 Pt 2) (1997), H2442–51.
96. Park, J.Y., Takahara, N., Gabriele, A., Chou, E., Naruse, K., Suzuma, K., et al. Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes 49:july (7) (2000), 1239–1248.
97. Williams, B., Gallacher, B., Patel, H., Orme, C., Glucose-induced protein kinase C activation regulates vascular permeability factor mRNA expression and peptide production by human vascular smooth muscle cells in vitro. Diabetes 46:September (9) (1997), 1497–1503.
98. Morita, T., Kurihara, H., Maemura, K., Yoshizumi, M., Nagai, R., Yazaki, Y., Role of Ca2+ and protein kinase C in shear stress-induced actin depolymerization and endothelin 1 gene expression. Circ. Res. 75:October (4) (1994), 630–636.
99. Aiello, L.P., Northrup, J.M., Keyt, B.A., Takagi, H., Iwamoto, M.A., Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch. Ophthalmol. 113:December (12) (1995), 1538–1544.
100. Shiba, T., Inoguchi, T., Sportsman, J.R., Heath, W.F., Bursell, S., King, G.L., Correlation of diacylglycerol level and protein kinase C activity in rat retina to retinal circulation. Am. J. Physiol. 265:November (5 Pt 1) (1993), E783–793.
101. Xia, P., Inoguchi, T., Kern, T.S., Engerman, R.L., Oates, P.J., King, G.L., Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase C pathway in diabetes and hypergalactosemia. Diabetes 43:September (9) (1994), 1122–1129.
102. Sakaguchi, M., Murata, H., Yamamoto, K., Ono, T., Sakaguchi, Y., Motoyama, A., et al. TIRAP, an adaptor protein for TLR2/4, transduces a signal from RAGE phosphorylated upon ligand binding. PLoS One, 6(8), 2011, e23132.
103. Geraldes, P., King, G.L., Activation of protein kinase C isoforms and its impact on diabetic complications. Circ. Res. 106:April (8) (2010), 1319–1331.
104. Kizub, I.V., Klymenko, K.I., Soloviev, A.I., Protein kinase C in enhanced vascular tone in diabetes mellitus. Int. J. Cardiol. 174:June (2) (2014), 230–242.
105. Rask-Madsen, C., King, G.L., Differential regulation of VEGF signaling by PKC-alpha and PKC-epsilon in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28:may (5) (2008), 919–924.
106. Ha, H., Yu, M.R., Lee, H.B., High glucose-induced PKC activation mediates TGF-beta 1 and fibronectin synthesis by peritoneal mesothelial cells. Kidney Int. 59:February (2) (2001), 463–470.
107. Wu, D., Peng, F., Zhang, B., Ingram, A.J., Kelly, D.J., Gilbert, R.E., et al. PKC-beta1 mediates glucose-induced Akt activation and TGF-beta1 upregulation in mesangial cells. J. Am. Soc. Nephrol. 20:March (3) (2009), 554–566.
108. Klaassen, I., Van Noorden, C.J., Schlingemann, R.O., Molecular basis of the inner blood-retinal barrier and its breakdown in diabetic macular edema and other pathological conditions. Prog. Retin. Eye Res. 34:May (2013), 19–48.
109. Titchenell, P.M., Lin, C.M., Keil, J.M., Sundstrom, J.M., Smith, C.D., Antonetti, D.A., Novel atypical PKC inhibitors prevent vascular endothelial growth factor-induced blood-retinal barrier dysfunction. Biochem. J. 446:September (3) (2012), 455–467.
110. Housey, G.M., O'Brian, C.A., Johnson, M.D., Kirschmeier, P., Weinstein, I.B., Isolation of cDNA clones encoding protein kinase C: evidence for a protein kinase C-related gene family. Proc. Natl. Acad. Sci. U. S. A. 84:February (4) (1987), 1065–1069.
111. Steinberg, S.F., Structural basis of protein kinase C isoform function. Physiol. Rev. 88:October (4) (2008), 1341–1378.
112. Corbalán-García, S., Gómez-Fernández, J.C., Protein kinase C regulatory domains: the art of decoding many different signals in membranes. Biochim. Biophys. Acta 1761:july (7) (2006), 633–654.
113. Mukherjee, A., Roy, S., Saha, B., Mukherjee, D., Spatio-Temporal regulation of PKC isoforms imparts signaling specificity. Front. Immunol., 7, 2016, 45.
114. Inoguchi, T., Battan, R., Handler, E., Sportsman, J.R., Heath, W., King, G.L., Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc. Natl. Acad. Sci. U. S. A. 89:Nobember (22) (1992), 11059–11063.
115. Song, H.B., Jun, H.O., Kim, J.H., Yu, Y.S., Kim, K.W., Suppression of protein kinase C-ζ attenuates vascular leakage via prevention of tight junction protein decrease in diabetic retinopathy. Biochem. Biophys. Res. Commun. 444:January (1) (2014), 63–68.
116. Aiello, L.P., Bursell, S.E., Clermont, A., Duh, E., Ishii, H., Takagi, C., et al. Vascular endothelial growth factor-induced retinal permeability is mediated by protein kinase C in vivo and suppressed by an orally effective beta-isoform-selective inhibitor. Diabetes 46:September (9) (1997), 1473–1480.
117. Du, Y., Sarthy, V.P., Kern, T.S., Interaction between NO and COX pathways in retinal cells exposed to elevated glucose and retina of diabetic rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287:October (4) (2004), R735–741.
118. Leal, E.C., Manivannan, A., Hosoya, K., Terasaki, T., Cunha-Vaz, J., Ambrósio, A.F., et al. Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 48:November (11) (2007), 5257–5265.
119. Powell, E.D., Field, R.A., Diabetic retinopathy and rheumatoid arthritis. Lancet 2:July (7349) (1964), 17–18.
120. Bartels, C.M., Wong, J.C., Johnson, S.L., Thorpe, C.T., Barney, N.P., Sheibani, N., et al. Rheumatoid arthritis and the prevalence of diabetic retinopathy. Rheumatology (Oxford). 54:August (8) (2015), 1415–1419.
121. Tikhonenko, M., Lydic, T.A., Wang, Y., Chen, W., Opreanu, M., Sochacki, A., et al. Remodeling of retinal Fatty acids in an animal model of diabetes: a decrease in long-chain polyunsaturated fatty acids is associated with a decrease in fatty acid elongases Elovl2 and Elovl4. Diabetes 59:January (1) (2010), 219–227.
122. Decsi, T., Szabó, E., Burus, I., Marosvölgyi, T., Kozári, A., Erhardt, E., et al. Low contribution of n-3 polyunsaturated fatty acids to plasma and erythrocyte membrane lipids in diabetic young adults. Prostaglandins Leukot. Essent. Fatty Acids 76:March (3) (2007), 159–164.
123. Capozzi, M.E., McCollum, G.W., Cousins, D.B., Penn, J.S., Linoleic acid is a diabetes-relevant stimulator of retinal inflammation in human retinal muller cells and microvascular endothelial cells. J Diabetes Metab., 7(December (12)), 2016.
124. Moore, T.C., Moore, J.E., Kaji, Y., Frizzell, N., Usui, T., Poulaki, V., et al. The role of advanced glycation end products in retinal microvascular leukostasis. Invest. Ophthalmol. Vis. Sci. 44:October (10) (2003), 4457–4464.
125. Inagaki, Y., Yamagishi, S., Okamoto, T., Takeuchi, M., Amano, S., Pigment epithelium-derived factor prevents advanced glycation end products-induced monocyte chemoattractant protein-1 production in microvascular endothelial cells by suppressing intracellular reactive oxygen species generation. Diabetologia 46:February (2) (2003), 284–287.
126. Yoshida, S., Yoshida, A., Ishibashi, T., Induction of IL-8, MCP-1, and bFGF by TNF-alpha in retinal glial cells: implications for retinal neovascularization during post-ischemic inflammation. Graefes Arch. Clin. Exp. Ophthalmol. 242:May (5) (2004), 409–413.
127. Arar, N.H., Freedman, B.I., Adler, S.G., Iyengar, S.K., Chew, E.Y., Davis, M.D., et al. Heritability of the severity of diabetic retinopathy: the FIND-Eye study. Invest. Ophthalmol. Vis. Sci. 49:September (9) (2008), 3839–3845.
128. Looker, H.C., Nelson, R.G., Chew, E., Klein, R., Klein, B.E., Knowler, W.C., et al. Genome-wide linkage analyses to identify Loci for diabetic retinopathy. Diabetes 56:April (4) (2007), 1160–1166.
129. Hallman, D.M., Boerwinkle, E., Gonzalez, V.H., Klein, B.E., Klein, R., Hanis, C.L., A genome-wide linkage scan for diabetic retinopathy susceptibility genes in Mexican Americans with type 2 diabetes from Starr County, Texas. Diabetes 56:April (4) (2007), 1167–1173.
130. Donaghue, K.C., Margan, S.H., Chan, A.K., Holloway, B., Silink, M., Rangel, T., et al. The association of aldose reductase gene (AKR1B1) polymorphisms with diabetic neuropathy in adolescents. Diabet. Med. 22:October (10) (2005), 1315–1320.
131. Abhary, S., Burdon, K.P., Laurie, K.J., Thorpe, S., Landers, J., Goold, L., et al. Aldose reductase gene polymorphisms and diabetic retinopathy susceptibility. Diabetes Care. 33:August (8) (2010), 1834–1836.
132. Syreeni, A., El-Osta, A., Forsblom, C., Sandholm, N., Parkkonen, M., Tarnow, L., et al. Genetic examination of SETD7 and SUV39H1/H2 methyltransferases and the risk of diabetes complications in patients with type 1 diabetes. Diabetes 60:November (11) (2011), 3073–3080.
133. Mishra, M., Zhong, Q., Kowluru, R.A., Epigenetic modifications of Nrf2-mediated glutamate-cysteine ligase: implications for the development of diabetic retinopathy and the metabolic memory phenomenon associated with its continued progression. Free Radic. Biol. Med. 75:October (2014), 129–139.
134. Zhong, Q., Kowluru, R.A., Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation. Invest. Ophthalmol. Vis. Sci. 54:January (1) (2013), 244–250.
135. Silva, V.A., Polesskaya, A., Sousa, T.A., Corrêa, V.M., André, N.D., Reis, R.I., et al. Expression and cellular localization of microRNA-29b and RAX, an activator of the RNA-dependent protein kinase (PKR), in the retina of streptozotocin-induced diabetic rats. Mol. Vis. 17 (2011), 2228–2240.
136. Kowluru, R.A., Koppolu, P., Chakrabarti, S., Chen, S., Diabetes-induced activation of nuclear transcriptional factor in the retina, and its inhibition by antioxidants. Free Radic. Res. 37:November (11) (2003), 1169–1180.
137. Betteridge, D.J., What is oxidative stress?. Metabolism 49:February (2 Suppl 1) (2000), 3–8.
138. Mugge, A., The role of reactive oxygen species in atherosclerosis. Z. Kardiol. 87:November (11) (1998), 851–864.
139. Giacco, F., Brownlee, M., Oxidative stress and diabetic complications. Circ. Res. 107:October (9) (2010), 1058–1070.
140. Hulsmans, M., Van Dooren, E., Holvoet, P., Mitochondrial reactive oxygen species and risk of atherosclerosis. Curr. Atheroscler. Rep. 14:June (3) (2012), 264–276.
141. Dizdaroglu, M., Jaruga, P., Birincioglu, M., Rodriguez, H., Free radical-induced damage to DNA: mechanisms and measurement. Free Radic. Biol. Med. 32:June (11) (2002), 1102–1115.
142. Salvi, A., Carrupt, P., Tillement, J., Testa, B., Structural damage to proteins caused by free radicals: asessment, protection by antioxidants, and influence of protein binding. Biochem. Pharmacol. 61:May (11) (2001), 1237–1242.
143. Du, X., Matsumura, T., Edelstein, D., Rossetti, L., Zsengellér, Z., Szabó, C., et al. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J. Clin. Invest. 112:October (7) (2003), 1049–1057.
144. Zheng, L., Szabó, C., Kern, T.S., Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-kappaB. Diabetes 53:November (11) (2004), 2960–2967.
145. Du, Y., Miller, C.M., Kern, T.S., Hyperglycemia increases mitochondrial superoxide in retina and retinal cells. Free Radic. Biol. Med. 35:December (11) (2003), 1491–1499.
146. Du, Y., Veenstra, A., Palczewski, K., Kern, T.S., Photoreceptor cells are major contributors to diabetes-induced oxidative stress and local inflammation in the retina. Proc. Natl. Acad. Sci. U. S. A. 110:October (41) (2013), 16586–16591.
147. Eshaq, R.S., Wright, W.S., Harris, N.R., Oxygen delivery, consumption, and conversion to reactive oxygen species in experimental models of diabetic retinopathy. Redox Biol., 2014, 661–666.
148. Singh, L.P., Thioredoxin interacting protein (TXNIP) and pathogenesis of diabetic retinopathy. J Clin Exp Ophthalmol., 5(August (4)), 2013.
149. Sasaki, M., Ozawa, Y., Kurihara, T., Kubota, S., Yuki, K., Noda, K., et al. Neurodegenerative influence of oxidative stress in the retina of a murine model of diabetes. Diabetologia 53:May (5) (2010), 971–979.
150. Ozawa, Y., Kurihara, T., Sasaki, M., Ban, N., Yuki, K., Kubota, S., et al. Neural degeneration in the retina of the streptozotocin-induced type 1 diabetes model. Exp. Diabetes Res., 2011, 2011, 108328.
151. Motta, G., Rojkjaer, R., Hasan, A.A., Cines, D.B., Schmaier, A.H., High molecular weight kininogen regulates prekallikrein assembly and activation on endothelial cells: a novel mechanism for contact activation. Blood 91:January (2) (1998), 516–528.
152. Ma, J.X., Song, Q., Hatcher, H.C., Crouch, R.K., Chao, L., Chao, J., Expression and cellular localization of the kallikrein-kinin system in human ocular tissues. Exp. Eye Res. 63:July (1) (1996), 19–26.
153. Pinna, A., Emanueli, C., Dore, S., Salvo, M., Madeddu, P., Carta, F., Levels of human tissue kallikrein in the vitreous fluid of patients with severe proliferative diabetic retinopathy. Ophthalmologica 218:July–August (4) (2004), 260–263.
154. Webb, J.G., The kallikrein/kinin system in ocular function. J. Ocul. Pharmacol. Ther. 27:Dcecember (6) (2011), 539–543.
155. Phipps, J.A., Feener, E.P., The kallikrein-kinin system in diabetic retinopathy: lessons for the kidney. Kidney Int. 73:May (10) (2008), 1114–1119.
156. Phipps, J.A., Jobling, A.I., Greferath, U., Fletcher, E.L., Vessey, K.A., Alternative pathways in the development of diabetic retinopathy: the renin-angiotensin and kallikrein-kinin systems. Clin. Exp. Optom. 95:May (3) (2012), 282–289.
157. Liu, J., Feener, E.P., Plasma kallikrein-kinin system and diabetic retinopathy. Biol. Chem. 394:March (3) (2013), 319–328.
158. Bhat, M., Pouliot, M., Couture, R., Vaucher, E., The kallikrein-kinin system in diabetic retinopathy. Prog. Drug Res. 69 (2014), 111–143.
159. Abdouh, M., Talbot, S., Couture, R., Hassessian, H.M., Retinal plasma extravasation in streptozotocin-diabetic rats mediated by kinin B(1) and B(2) receptors. Br. J. Pharmacol. 154:May (1) (2008), 136–143.
160. Abdouh M, Guy‐Bernier Research Centre MRH, Montréal, PQ Canada H1T 2M4, Ophthalmology Do, Khanjari A, Guy‐Bernier Research Centre MRH, Montréal, PQ Canada H1T 2M4, Sciences B, et al. Early upregulation of kinin B1 receptors in retinal microvessels of the streptozotocin‐diabetic rat. British Journal of Pharmacology. 2003;140(1):33-40.
161. Pruneau, D., Belichard, P., Sahel, J.A., Combal, J.P., Targeting the kallikrein-kinin system as a new therapeutic approach to diabetic retinopathy. Curr. Opin. Investig. Drugs 11:5 (2010), 507–514.
162. Hookes L. Association for Research in Vision and Ophthalmology (ARVO)–2010 Annual Meeting. For Sight: The Future of Eye and Vision Research–part 1. IDrugs. 2010 Jul;13(7):427-9.
163. Catanzaro, O., Labal, E., Andornino, A., Capponi, J.A., Di Martino, I., Sirois, P., Blockade of early and late retinal biochemical alterations associated with diabetes development by the selective bradykinin B1 receptor antagonist R-954. Peptides 34:April (2) (2012), 349–352.
164. Kato, N., Hou, Y., Lu, Z., Lu, C., Nagano, H., Suzuma, K., et al. Kallidinogenase normalizes retinal vasopermeability in streptozotocin-induced diabetic rats: potential roles of vascular endothelial growth factor and nitric oxide. Eur. J. Pharmacol. 606:March (1–3) (2009), 187–190.
165. Nakamura, S., Morimoto, N., Tsuruma, K., Izuta, H., Yasuda, Y., Kato, N., et al. Tissue kallikrein inhibits retinal neovascularization via the cleavage of vascular endothelial growth factor-165. Arterioscler. Thromb. Vasc. Biol. 31:May (5) (2011), 1041–1048.
166. Gao, B.-B., Clermont, A., Rook, S., Fonda, S.J., Srinivasan, V.J., Wojtkowski, M., et al. Extracellular carbonic anhydrase mediates hemorrhagic retinal and cerebral vascular permeability through prekallikrein activation. Nat. Med. 13:2 (2007), 181–188 (2007-01-28).
167. Marti, H.H., Vascular Endothelial Growth Factor. 2000 (2000).
168. Ferrara, N., Gerber, H.P., LeCouter, J., The biology of VEGF and its receptors. Nat. Med. 9:June (6) (2003), 669–676.
169. Dehne, N., Kerkweg, U., Flohe, S.B., Brune, B., Fandrey, J., Activation of hypoxia-inducible factor 1 in skeletal muscle cells after exposure to damaged muscle cell debris. Shock 35:June (6) (2011), 632–638.
170. Dery, M.A., Michaud, M.D., Richard, D.E., Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int. J. Biochem. Cell Biol. 37:March (3) (2005), 535–540.
171. Rudnicki, M., Faine, L.A., Dehne, N., Namgaladze, D., Ferderbar, S., Weinlich, R., et al. Hypoxia inducible factor-dependent regulation of angiogenesis by nitro-fatty acids. Arterioscler. Thromb. Vasc. Biol. 31:June (6) (2011), 1360–1367.
172. Semenza, G.L., HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. (1985) 88:April (4) (2000), 1474–1480.
173. Lee, S.W., Kim, W.J., Choi, Y.K., Song, H.S., Son, M.J., Gelman, I.H., et al. SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier. Nat. Med. 9:july (7) (2003), 900–906.
174. Weidemann, A., Krohne, T.U., Aguilar, E., Kurihara, T., Takeda, N., Dorrell, M.I., et al. Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina. Glia 58:August (10) (2010), 1177–1185.
175. Wang, C., Poon, S., Murali, S., Koo, C.Y., Bell, T.J., Hinkley, S.F., et al. Engineering a vascular endothelial growth factor 165-binding heparan sulfate for vascular therapy. Biomaterials 35:August (25) (2014), 6776–6786.
176. Frey, T., Antonetti, D.A., Alterations to the blood-retinal barrier in diabetes: cytokines and reactive oxygen species. Antioxid. Redox Signal. 15:September (5) (2011), 1271–1284.
177. Esser, S., Lampugnani, M.G., Corada, M., Dejana, E., Risau, W., Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J. Cell Sci. 111:July (Pt 13) (1998), 1853–1865.
178. Murakami, T., Frey, T., Lin, C., Antonetti, D.A., Protein kinase cbeta phosphorylates occludin regulating tight junction trafficking in vascular endothelial growth factor-induced permeability in vivo. Diabetes 61:June (6) (2012), 1573–1583.
179. Maharjan, S., Lee, S., Agrawal, V., Choi, H.J., Maeng, Y.S., Kim, K., et al. Sac-0601 prevents retinal vascular leakage in a mouse model of diabetic retinopathy. Eur. J. Pharmacol. 657:April (1–3) (2011), 35–40.
180. Aveleira, C.A., Lin, C.M., Abcouwer, S.F., Ambrosio, A.F., Antonetti, D.A., TNF-alpha signals through PKCzeta/NF-kappaB to alter the tight junction complex and increase retinal endothelial cell permeability. Diabetes 59:November (11) (2010), 2872–2882.
181. Huang, H., Gandhi, J.K., Zhong, X., Wei, Y., Gong, J., Duh, E.J., et al. TNFalpha is required for late BRB breakdown in diabetic retinopathy, and its inhibition prevents leukostasis and protects vessels and neurons from apoptosis. Invest. Ophthalmol. Vis. Sci. 52:March (3) (2011), 1336–1344.
182. Krady, J.K., Basu, A., Allen, C.M., Xu, Y., LaNoue, K.F., Gardner, T.W., et al. Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy. Diabetes 54:May (5) (2005), 1559–1565.
183. Bamforth, S.D., Lightman, S.L., Greenwood, J., Interleukin-1 beta-induced disruption of the retinal vascular barrier of the central nervous system is mediated through leukocyte recruitment and histamine. Am. J. Pathol. 150:January (1) (1997), 329–340.
184. Ildefonso, C.J., Jaime, H., Rahman, M.M., Li, Q., Boye, S.E., Hauswirth, W.W., et al. Gene delivery of a viral anti-inflammatory protein to combat ocular inflammation. Hum. Gene. Ther., 24(November), 2014.
185. Rangasamy, S., McGuire, P.G., Franco Nitta, C., Monickaraj, F., Oruganti, S.R., Das, A., Chemokine mediated monocyte trafficking into the retina: role of inflammation in alteration of the blood-retinal barrier in diabetic retinopathy. PLoS One, 9(10), 2014, e108508.
186. Capeans, C., De Rojas, M.V., Lojo, S., Salorio, M.S., C–C chemokines in the vitreous of patients with proliferative vitreoretinopathy and proliferative diabetic retinopathy. Retina 18:6 (1998), 546–550.
187. Banerjee, S., Savant, V., Scott, R.A., Curnow, S.J., Wallace, G.R., Murray, P.I., Multiplex bead analysis of vitreous humor of patients with vitreoretinal disorders. Invest Ophthalmol Vis Sci. May 48:May (5) (2007), 2203–2207.
188. Beltramo, E., Porta, M., Pericyte loss in diabetic retinopathy: mechanisms and consequences. Curr. Med. Chem. 20:26 (2013), 3218–3225.
189. Hammes, H.P., Pericytes and the pathogenesis of diabetic retinopathy. Horm. Metab. Res. 37:April (Suppl. 1) (2005), 39–43.
190. Kolar, P., [Patophysiology of diabetic retinopathy]. Vnitr. Lek. 59:March (3) (2013), 173–176.
191. Hu, Y.B., Zhang, J.K., Sun, Z.Y., Yuan, Z.G., Liu, Y.M., Mao, C.J., et al. [Retinal cell apoptosis, microvascular changes and expression of connective tissue growth factor in experimental diabetic rats]. Zhonghua Yan Ke Za Zhi. 47:June (6) (2011), 521–526.
192. Feenstra, D.J., Yego, E.C., Mohr, S., Modes of retinal cell death in diabetic retinopathy. J. Clin. Exp. Ophthalmol., 4(October (5)), 2013, 298.
193. Hammes, H.P., Lin, J., Wagner, P., Feng, Y., Vom Hagen, F., Krzizok, T., et al. Angiopoietin-2 causes pericyte dropout in the normal retina: evidence for involvement in diabetic retinopathy. Diabetes 53:April (4) (2004), 1104–1110.
194. Cogan, D.G., Toussaint, D., Kuwabara, T., Retinal vascular patterns. IV. diabetic retinopathy. Arch. Ophthalmol. 66:September (1961), 366–378.
195. Van Geest, R.J., Leeuwis, J.W., Dendooven, A., Pfister, F., Bosch, K., Hoeben, K.A., et al. Connective tissue growth factor is involved in structural retinal vascular changes in long-term experimental diabetes. J. Histochem. Cytochem. 62:February (2) (2014), 109–118.
196. Nieuwdorp M, Haeften TWv, Gouverneur MCLG, Mooij HL, Lieshout MHPv, Levi M, et al. Loss of Endothelial Glycocalyx During Acute Hyperglycemia Coincides With Endothelial Dysfunction and Coagulation Activation In Vivo. 2006-02-01.
197. Lipowsky, H.H., Gao, L., Lescanic, A., Shedding of the endothelial glycocalyx in arterioles, capillaries, and venules and its effect on capillary hemodynamics during inflammation. Am. J. Physiol. Heart Circ. Physiol. 301:December (6) (2011), H2235–45.
198. Wisniewska-Kruk, J., Klaassen, I., Vogels, I.M., Magno, A.L., Lai, C.M., Van Noorden, C.J., et al. Molecular analysis of blood-retinal barrier loss in the Akimba mouse, a model of advanced diabetic retinopathy. Exp. Eye Res. 122:May (2014), 123–131.
199. Broekhuizen, L.N., Lemkes, B.A., Mooij, H.L., Meuwese, M.C., Verberne, H., Holleman, F., et al. Effect of sulodexide on endothelial glycocalyx and vascular permeability in patients with type 2 diabetes mellitus. Diabetologia 53:December (12) (2010), 2646–2655.
200. Kumase, F., Morizane, Y., Mohri, S., Takasu, I., Ohtsuka, A., Ohtsuki, H., Glycocalyx degradation in retinal and choroidal capillary endothelium in rats with diabetes and hypertension. Acta Med. Okayama 64:October (5) (2010), 277–283.
201. Lopez-Quintero, S.V., Cancel, L.M., Pierides, A., Antonetti, D., Spray, D.C., Tarbell, J.M., High glucose attenuates shear-induced changes in endothelial hydraulic conductivity by degrading the glycocalyx. PLoS One., 8(11), 2013, e78954.
202. Bhattacharjee, P.S., Huq, T.S., Potter, V., Young, A., Davenport, I.R., Graves, R., et al. High-glucose-induced endothelial cell injury is inhibited by a Peptide derived from human apolipoprotein E. PLoS One., 7(12), 2012, e52152.
203. Tarbell, J.M., Shear stress and the endothelial transport barrier. Cardiovasc. Res. 87:July (2) (2010), 320–330.
204. Liu, C.P., Yeh, J.L., Wu, B.N., Chai, C.Y., Chen, I.J., Lai, W.T., KMUP-3 attenuates ventricular remodelling after myocardial infarction through eNOS enhancement and restoration of MMP-9/TIMP-1 balance. Br. J. Pharmacol. 162:January (1) (2011), 126–135.
205. Privratsky, J.R., Newman, D.K., Newman, P.J., PECAM-1: conflicts of interest in inflammation. Life Sci. 87:July (3–4) (2010), 69–82.
206. Cheung, A.K.H., Fung, M.K.L., Lo, A.C.Y., Lam, T.T.L., So, K.F., Chung, S.S.M., et al. Aldose reductase deficiency prevents diabetes-Induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes 54:11 (2005), 3119–3125.
207. Cao, Y., Feng, B., Chen, S., Chu, Y., Chakrabarti, S., Mechanisms of endothelial to mesenchymal transition in the retina in diabetes. Invest. Ophthalmol. Vis. Sci. 55:11 (2014), 7321–7331.