Protective factors in diabetic retinopathy: Focus on blood-retinal barrier

Discovery Medicine

Volumn 18, Issue 98, 2014, Pages 105-112

  Zhang, Conghui ^a   Wang, Hao ^a   Nie, Jing ^a   Wang, Fang ^a  

^a TONGJI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; AQUAPORIN 4; BEVACIZUMAB; CADHERIN; CAVEOLIN 1; ERIODICTYOL; ERYTHROPOIETIN; ETHYL PYRUVATE; FENOFIBRIC ACID; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MONOCYTE CHEMOTACTIC PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN; NATRIURETIC PEPTIDE TYPE C; NITRIC OXIDE; PROTEIN KINASE C INHIBITOR; PYRUVIC ACID DERIVATIVE; RUBOXISTAURIN; SITAGLIPTIN; SOMATOMEDIN BINDING PROTEIN 3; TIGHT JUNCTION PROTEIN; TRANSCRIPTION FACTOR NRF2; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN; FENOFIBRATE; IGFBP3 PROTEIN, HUMAN; PYRAZINE DERIVATIVE; TRIAZOLE DERIVATIVE; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ARTICLE; BLOOD RETINA BARRIER; BLOOD VESSEL PERMEABILITY; CLINICAL TRIAL (TOPIC); DIABETIC RETINOPATHY; DISEASE SEVERITY; EYE PROTECTION; HUMAN; HYPERGLYCEMIA; INFLAMMATION; MUELLER CELL; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PIGMENT EPITHELIUM; TIGHT JUNCTION; VITREOUS BODY; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPLICATION; DRUG EFFECTS; MACULAR EDEMA; PATHOLOGY; PHYSIOLOGY; PROTECTION;

ANIMALS; BLOOD-RETINAL BARRIER; DIABETIC RETINOPATHY; ERYTHROPOIETIN; FENOFIBRATE; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; MACULAR EDEMA; PROTECTIVE FACTORS; PYRAZINES; TRIAZOLES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84933041675     PISSN: 15396509     EISSN: 19447930     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Aiello LP, Clermont A, Arora V, Davis MD, Sheetz MJ, Bursell SE. Inhibition of PKC beta by oral administration of ruboxistaurin is well tolerated and ameliorates diabetes-induced retinal hemodynamic abnormalities in patients. Invest Ophthalmol Vis Sci 47(1):86-92, 2006.
2. Aiello LP, Vignati L, Sheetz MJ, Zhi X, Girach A, Davis MD, Wolka AM, Shahri N, Milton RC. PKC-DRS and PKC-DRS2 Study Group. Oral protein kinase c β inhibition using ruboxistaurin: efficacy, safety, and causes of vision loss among 813 patients (1,392 eyes) with diabetic retinopathy in the Protein Kinase C β Inhibitor-Diabetic Retinopathy Study and the Protein Kinase C β Inhibitor-Diabetic Retinopathy Study 2. Retina 31(10):2084-2094, 2011.
3. Amadio M, Bucolo C, Leggio GM, Drago F, Govoni S, Pascale A. The PKCbeta/HuR/VEGF pathway in diabetic retinopathy. Biochem Pharmacol 80(8):1230-1237, 2010.
4. Armaly Z, Assady S, Abassi Z. Corin: a new player in the regulation of salt-water balance and blood pressure. Curr Opin Nephrol Hypertens 22(6):713-722, 2013.
5. Bakri SJ, Kaiser PK. Chapter 21-Diabetic Retinopathy. Retinal Imaging. pp233-240, Mosby, 2006.
6. Bucolo C, Leggio GM, Drago F, Salomone S. Eriodictyol prevents early retinal and plasma abnormalities in streptozotocin-induced diabetic rats. Biochem Pharmacol 84(1):88-92, 2012.
7. Cheema HR, Al Habash A, Al-Askar E. Improvement of visual acuity based on optical coherence tomography patterns following intravitreal bevacizumab treatment in patients with diabetic macular edema. Int J Ophthalmol 7(2):251-255, 2014.
8. Cho S, Szeto HH, Kim E, Kim H, Tolhurst AT, Pinto JT. A novel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36. J Biol Chem 282(7):4634-4642, 2007.
9. Cui B, Sun JH, Xiang FF, Liu L, Li WJ. Aquaporin 4 knockdown exacerbates streptozotocin-induced diabetic retinopathy through aggravating inflammatory response. Exp Eye Res 98:37-43, 2012.
10. Cunha-Vaz J, Bernardes R, Lobo C. Blood-retinal barrier. Eur J Ophthalmol 21(Suppl 6):S3-S9, 2011.
11. Dahrouj M, Alsarraf O, Liu Y, Crosson CE, Ablonczy Z. C-type natriuretic peptide protects the retinal pigment epithelium against advanced glycation end product-induced barrier dysfunction. J Pharmacol Exp Ther 344(1):96-102, 2013.
12. Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, Lin JK, Farzadfar F, Khang YH, Stevens GA, Rao M, Ali MK, Riley LM, Robinson CA, Ezzati M, Global Burden of Metabolic Risk Factors of Chronic Diseases Collaborating Group (Blood Glucose). National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378(9785):31-40, 2011.
13. Deissler HL, Lang GK, Lang GE. Capacity of aflibercept to counteract VEGF-stimulated abnormal behavior of retinal microvascular endothelial cells. Exp Eye Res 122:20-31, 2014.
14. Devi TS, Singh LP, Hosoya K, Terasaki T. GSK-3β/CREB axis mediates IGF-1-induced ECM/adhesion molecule expression, cell cycle progression and monolayer permeability in retinal capillary endothelial cells: Implications for diabetic retinopathy. Biochim Biophys Acta 1812(9):1080-1088, 2011.
15. Do DV, Schmidt-Erfurth U, Gonzalez VH, Gordon CM, Tolentino M, Berliner AJ, Vitti R, Rückert R, Sandbrink R, Stein D, Yang K, Beckmann K, Heier JS. The DA VINCI Study: phase 2 primary results of VEGF Trap-Eye in patients with diabetic macular edema. Ophthalmology 118(9):1819-1826, 2011.
16. Fink MP. Ethyl pyruvate. Curr Opin Anaesthesiol 21(2):160-167, 2008.
17. Funatsu H, Yamashita H, Sakata K, Noma H, Mimura T, Suzuki M, Eguchi S, Hori S. Vitreous levels of vascular endothelial growth factor and intercellular adhesion molecule 1 are related to diabetic macular edema. Ophthalmology 112(5):806-816, 2005.
18. Garcia-Ramírez M, Hernández C, Ruiz-Meana M, Villarroel M, Corraliza L, García-Dorado D, Simó R. Erythropoietin protects retinal pigment epithelial cells against the increase of permeability induced by diabetic conditions: essential role of JAK2/PI3K signaling. Cell Signal 23(10):1596-1602, 2011.
19. Gonçalves A, Leal E, Paiva A, Teixeira Lemos E, Teixeira F, Ribeiro CF, Reis F, Ambrósio AF, 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 14(5):454-463, 2012.
20. Gu X, Fliesler SJ, Zhao YY, Stallcup WB, Cohen AW, Elliott MH. Loss of caveolin-1 causes blood-retinal barrier breakdown, venous enlargement, and mural cell alteration. Am J Pathol 184(2):541-555, 2014.
21. Hammes HP, Alt A, Niwa T, Clausen JT, Bretzel RG, Brownlee M, Schleicher ED. Differential accumulation of advanced glycation end products in the course of diabetic retinopathy. Diabetologia 42(6):728-736, 1999.
22. Hosoya K, Tachikawa M. The inner blood-retinal barrier: molecular structure and transport biology. Adv Exp Med Biol 763:85-104, 2012.
23. Huang H, Gandhi JK, Zhong X, Wei Y, Gong J, Duh EJ, Vinores SA. 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(3):1336-1344, 2011.
24. Jacot JL, Sherris D. Potential therapeutic roles for inhibition of the PI3K/Akt/mTOR pathway in the pathophysiology of diabetic retinopathy. J Ophthalmol 2011:589813, 2011.
25. Jarajapu YP, Cai J, Li YY, Calzi S, Kielczewski JL, Hu P, Shaw LC, Firth SM, Chan-Ling T, Boulton ME, Baxter RC, Grant MB. Protection of blood retinal barrier and systemic vasculature by insulin-like growth factor binding protein-3. PLoS One 7(7):e39398, 2012.
26. Kim J, Cha YN, Sirh YJ. A protective role of nuclear factor-erythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat Res 690(1-2):12-23, 2010.
27. Kim J, Lee YM, Kim CS, Sohn E, Jo K, Shin SD, Kim JS. Ethyl pyruvate prevents methyglyoxal-induced retinal vascular injury in rats. J Diabetes Res 2013:460820, 2013.
28. Klein R, Klein BEK. Chapter 45-The epidemiology of diabetic retinopathy. RYAN Retina. pp907-924, Saunders, Philadelphia, USA, 2013.
29. Kolár P. Patophysiology of diabetic retinopathy. Vnitr Lek 59(3):173-176, 2013.
30. Koleva-Georgieva DN, Sivkova NP, Terzieva D. Serum inflammatory cytokines IL-1beta, IL-6, TNF-alpha and VEGF have influence on the development of diabetic retinopathy. Folia Med (Plovdiv) 53:44-50, 2011.
31. Kubo Y, Hosoya KI. Inner blood-retinal barrier transporters: relevance to diabetic retinopathy. Diabetic Retinopathy pp92-108. Karger, Basel, Switzerland, 2007.
32. Li J, Chen X, Xiao W, Ma W, Li T, Huang J, Liu X, Liang X, Tang S, Luo Y. Mitochondria-targeted antioxidant peptide SS31 attenuates high glucose-induced injury on human retinal endothelial cells. Biochem Biophys Res Commun 404(1):349-356, 2011.
33. Li X, Mcclellan ME, Tanito M, Garteiser P, Towner R, Bissig D, Berkowitz BA, Fliesler SJ, WoodruffML, Fain GL, Birch DG, Khan MS, Ash JD, Elliott MH. Loss of caveolin-1 impairs retinal function due to disturbance of subretinal microenvironment. J Biol Chem 287(20):16424-16434, 2012.
34. Lu M, Kuroki M, Amano S, Tolentino M, Keough K, Kim I, Bucala R, Adamis AP. Advanced glycation end products increase retinal vascular endothelial growth factor expression. J Clin Invest 101(6):1219-1224, 1998.
35. Maier R, Weger M, Haller-Schober EM, El-Shabrawi Y, Wedrich A, Theisl A, Aigner R, Barth A, Haas A. Multiplex bead analysis of vitreous and serum concentrations of inflammatory and proangiogenic factors in diabetic patients. Mol Vis 14:637-643, 2008.
36. Mamputu JC, Renier G. Advanced glycation end-products increase monocyte adhesion to retinal endothelial cells through vascular endothelial growth factor-induced ICAM-1 expression: inhibitory effect of antioxidants. J Leukoc Biol 75(6):1062-1069., 2004.
37. Mckeage K, Keating GM. Fenofibrate: a review of its use in dyslipidaemia. Drugs 71(14):1917-1946, 2011.
38. Moran EP, Ding L, Wang Z, Cheng R, Chen Q, Moore R, Takahashi Y, Ma JX. Protective and antioxidant effects of PPARα in the ischemic retina. Invest Ophthalmol Vis Sci, 2014.
39. Nakamura N, Hasegawa G, Obayashi H, Yamazaki M, Ogata M, Nakano K, Yoshikawa T, Watanabe A, Kinoshita S, Fujinami A, Ohta M, Imamura Y, Ikeda T. Increased concentration of pentosidine, an advanced glycation end product, and interleukin-6 in the vitreous of patients with proliferative diabetic retinopathy. Diabetes Res Clin Pract 61(2):93-101, 2003.
40. Negre-Salvayre A, Salvayre R, Augé N, Pamplona R, Portero-Otín M. Hyperglycemia and glycation in diabetic complications. Antioxid Redox Signal 11:3071-3109, 2009.
41. Nitoda E, Moschos MM, Mavragani CP, Koutsilieris M. Ocular actions of platelet-activating factor: clinical implications. Expert Opin Ther Targets 16(10):1027-1039, 2012.
42. Otero K, Martínez F, Beltrán A, González D, Herrera B, Quintero G, Delgado R, Rojas A. Albumin-derived advanced glycation end-products trigger the disruption of the vascular endothelial cadherin complex in cultured human and murine endothelial cells. Biochem J 359(Pt 3):567-574, 2001.
43. Patel N. Targeting leukostasis for the treatment of early diabetic retinopathy. Cardiovasc Hematol Disord Drug Targets 9(3):222-229, 2009.
44. Pinazo-Durán MD, Gallego-Pinazo R, García-Medina JJ, Zanón-Moreno V, Nucci C, Dolz-Marco R, Martínez-Castillo S, Galbis-Estrada C, Marco-Ramírez C, López-Gálvez MI, Galarreta DJ, Díaz-Llópis M. Oxidative stress and its downstream signaling in aging eyes. Clin Interv Aging 9:637-652, 2014.
45. Rangasamy S, Srinivasan R, Maestas J, McGuire PG, Das A. A potential role for angiopoietin 2 in the regulation of the blood-retinal barrier in diabetic retinopathy. Invest Ophthalmol Vis Sci 52(6):3784-3791, 2011.
46. Sanlioglu AD, Karacay B, Balci MK, Griffith TS, Sanlioglu S. Therapeutic potential of VIP vs. PACAP in diabetes. J Mol Endocrinol 49(3):R157-R167, 2012.
47. Scuderi S, D'amico AG, Castorina A, Imbesi R, Carnazza ML, D'agata V. Ameliorative effect of PACAP and VIP against increased permeability in a model of outer blood retinal barrier dysfunction. Peptides 39:119-124, 2013.
48. Sharom FJ. Complex interplay between the P-glycoprotein multidrug efflux pump and the membrane: its role in modulating protein function. Front Oncol 4:41, 2014.
49. Silva PAS, Cavallerano JD, Sun JK, Blodi BA, Davis MD, Aiello LM, Aiello LP. Chapter 48-Proliferative diabetic retinopathy. RYAN Retina. pp969-1000. Saunders, Philadelphia, USA, 2013.
50. Syvänen S, Eriksson J. Advances in PET imaging of P-glycoprotein function at the blood-brain barrier. ACS Chem Neurosci 4(2):225-237, 2013.
51. Titchenell PM, Lin CM, Keil JM, Sundstrom JM, Smith CD, Antonetti DA. Novel atypical PKC inhibitors prevent vascular endothelial growth factor-induced blood-retinal barrier dysfunction. Biochem J 446(3):455-467, 2012.
52. Toda N, Nakanishi-Toda M. Nitric oxide: ocular blood flow, glaucoma, and diabetic retinopathy. Prog Retin Eye Res 26(3):205-238, 2007.
53. Toth PP. Clinical insights from the Fenofibrate Intervention and Event Lowering in Diabetes study: a community practice perspective. Int J Clin Pract 63(6):903-911, 2009.
54. Trudeau K, Roy S, Guo W, Hernández C, Villarroel M, Simó R, Roy S. Fenofibric acid reduces fibronectin and collagen type IV overexpression in human retinal pigment epithelial cells grown in conditions mimicking the diabetic milieu: functional implications in retinal permeability. Invest Ophthalmol Vis Sci 52(9):6348-6354, 2011.
55. World Health Organization. Global data on visual impairments 2010. Geneva, Switzerland, 2012.
56. Xu H, Zhang L, Gu L, Lu L, Gao G, Li W, Xu G, Wang J, Gao F, Xu Jy, Yao J, Wang F, Zhang J, Xu GT. Subretinal delivery of AAV2-mediated human erythropoietin gene is protective and safe in experimental diabetic retinopathy. Invest Ophthalmol Vis Sci 55(3):1519-1530, 2014.
57. Xu Z, Wei Y, Gong J, Cho H, Park JK, Sung ER, Huang H, Wu L, Eberhart C, Handa JT, Du Y, Kern TS, Thimmulappa R, Barber AJ, Biswal S, Duh EJ. NRF2 plays a protective role in diabetic retinopathy in mice. Diabetologia 57(1):204-213, 2014.
58. Zhang Y, Li C, Sun X, Kuang X, Ruan X. High glucose decreases expression and activity of p-glycoprotein in cultured human retinal pigment epithelium possibly through iNOS induction. PLoS One 7(2):e31631, 2012.
59. Zhong Q, Mishra M, Kowluru RA. Transcription factor Nrf2-mediated antioxidant defense system in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci 54(6):3941-3948, 2013.