Calcium dobesilate inhibits the alterations in tight junction proteins and leukocyte adhesion to retinal endothelial cells induced by diabetes

Diabetes

Volumn 59, Issue 10, 2010, Pages 2637-2645

  Leal, Ermelindo C ^a,b,c   Martins, João ^a,b   Voabil, Paula ^a   Liberal, Joana ^a   Chiavaroli, Carlo ^d   Bauer, Jacques ^d   Cunha Vaz, José ^b   Ambrósio, António F ^a,b,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b ASSOCIATION FOR INNOVATION AND BIOMEDICAL RESEARCH ON LIGHT AND IMAGE AIBILI   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d Vifor (International) Inc   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CLAUDIN 5; DOBESILATE CALCIUM; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; OCCLUDIN; PROTEIN ZO1; TYROSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD RETINA BARRIER; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; LEUKOCYTE ADHERENCE; MALE; MOLECULAR MECHANICS; NITRATION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; RETINA; WEIGHT GAIN; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; BLOOD-BRAIN BARRIER; CALCIUM DOBESILATE; CELL ADHESION; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENDOTHELIAL CELLS; ENDOTHELIUM; HEMOSTATICS; LEUKOCYTES; MALE; MEMBRANE PROTEINS; PERMEABILITY; PHOSPHOPROTEINS; RATS; RATS, WISTAR; RETINA; TIGHT JUNCTIONS;

EID: 77957589747     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-1421     Document Type: Article

References (46)

1. Cunha-Vaz J, Faria de Abreu JR, Campos AJ. Early breakdown of the blood-retinal barrier in diabetes. Br J Ophthalmol 1975;59:649-656
2. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993;329:977-986
3. Antonetti DA, Barber AJ, Hollinger LA, Wolpert EB, Gardner TW. Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occluden 1. A potential mechanism for vascular permeability in diabetic retinopathy and tumors. J Biol Chem 1999;274:23463-23467
4. Antonetti DA, Barber AJ, Khin S, Lieth E, Tarbell JM, Gardner TW. Vascular permeability in experimental diabetes is associated with reduced endothelial occludin content: vascular endothelial growth factor decreases occludin in retinal endothelial cells. Penn State Retina Research Group. Diabetes 1998;47:1953-1959
5. Barber AJ, Antonetti DA. Mapping the blood vessels with paracellular permeability in the retinas of diabetic rats. Invest Ophthalmol Vis Sci 2003;44:5410-5416
6. Barber AJ, Antonetti DA, Gardner TW. Altered expression of retinal occludin and glial fibrillary acidic protein in experimental diabetes. The Penn State Retina Research Group. Invest Ophthalmol Vis Sci 2000;41:3561-3568
7. Harhaj NS, Felinski EA, Wolpert EB, Sundstrom JM, Gardner TW, Antonetti DA. VEGF activation of protein kinase C stimulates occludin phosphorylation and contributes to endothelial permeability. Invest Ophthalmol Vis Sci 2006;47:5106-5115
8. Klaassen I, Hughes JM, Vogels IM, Schalkwijk CG, Van Noorden CJ, Schlingemann RO. Altered expression of genes related to blood-retina barrier disruption in streptozotocin-induced diabetes. Exp Eye Res 2009;89:4-15
9. Fanning AS, Mitic LL, Anderson JM. Transmembrane proteins in the tight junction barrier. J Am Soc Nephrol 1999;10:1337-1345
10. Matter K, Balda MS. Occludin and the functions of tight junctions. Int Rev Cytol 1999;186:117-146
11. Hirase T, Staddon JM, Saitou M, Ando-Akatsuka Y, Itoh M, Furuse M, Fujimoto K, Tsukita S, Rubin LL. Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 1997;110(Pt 14):1603-1613 (Pubitemid 27338748)
12. Turksen K, Troy TC. Barriers built on claudins. J Cell Sci 2004;117:2435-2447
13. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, Furuse M, Tsukita S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 2003;161:653-660
14. Wittchen ES, Haskins J, Stevenson BR. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J Biol Chem 1999;274:35179-35185
15. Adamis AP, Berman AJ. Immunological mechanisms in the pathogenesis of diabetic retinopathy. Semin Immunopathol 2008;30:65-84
16. Kern TS. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007;2007:95103
17. Bucolo C, Ward KW, Mazzon E, Cuzzocrea S, Drago F. Protective effects of a coumarin derivative in diabetic rats. Invest Ophthalmol Vis Sci 2009;50:3846-3852
18. Leal EC, Manivannan A, Hosoya K, Terasaki T, Cunha-Vaz J, Ambrósio AF, Forrester JV. Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy. Invest Ophthalmol Vis Sci 2007;48:5257-5265
19. Miyamoto K, Khosrof S, Bursell SE, Rohan R, Murata T, Clermont AC, Aiello LP, Ogura Y, Adamis AP. Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc Natl Acad Sci U S A 1999;96:10836-10841
20. Joussen AM, Poulaki V, Mitsiades N, Kirchhof B, Koizumi K, Döhmen S, Adamis AP. Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-alpha suppression. FASEB J 2002;16:438-440
21. El-Remessy AB, Al-Shabrawey M, Khalifa Y, Tsai NT, Caldwell RB, Liou GI. Neuroprotective and blood-retinal barrier-preserving effects of cannabidiol in experimental diabetes. Am J Pathol 2006;168:235-244
22. Berthet P, Farine JC, Barras JP. Calcium dobesilate: pharmacological profile related to its use in diabetic retinopathy. Int J Clin Pract 1999;53:631-636
23. Tejerina T, Ruiz E. Calcium dobesilate: pharmacology and future approaches. Gen Pharmacol 1998;31:357-360 (Pubitemid 28398858)
24. Leite EB, Mota MC, de Abreu JR, Cunha-Vaz JG. Effect of calcium dobesilate on the blood-retinal barrier in early diabetic retinopathy. Int Ophthalmol 1990;14:81-88
25. Ribeiro ML, Seres AI, Carneiro AM, Stur M, Zourdani A, Caillon P, Cunha-Vaz JG, DX-Retinopathy Study Group. Effect of calcium dobesilate on progression of early diabetic retinopathy: a randomised double-blind study. Graefes Arch Clin Exp Ophthalmol 2006;244:1591-1600
26. Rota R, Chiavaroli C, Garay RP, Hannaert P. Reduction of retinal albumin leakage by the antioxidant calcium dobesilate in streptozotocin-diabetic rats. Eur J Pharmacol 2004;495:217-224
27. Daubresse JC, Meunier R, Dumont P. A controlled clinical trial of calcium dobesylate in the treatment of diabetic retinopathy. Diabete Metab 1977;3:27-30
28. Larsen HW, Sander E, Hoppe R. The value of calcium dobesilate in the treatment of diabetic retinopathy. A controlled clinical trial. Diabetologia 1977;13:105-109
29. Stamper RL, Smith ME, Aronson SB, Cavender JC, Cleasby GW, Fung WE, Becker B. The effect of calcium dobesilate on nonproliferative diabetic retinopathy: a controlled study. Ophthalmology 1978;85:594-606
30. Haritoglou C, Gerss J, Sauerland C, Kampik A, Ulbig MW, CALDIRET study group. Effect of calcium dobesilate on occurrence of diabetic macular oedema (CALDIRET study): randomised, double-blind, placebo-controlled, multicentre trial. Lancet 2009;373:1364-1371
31. Brunet J, Farine JC, Garay RP, Hannaert P. In vitro antioxidant properties of calcium dobesilate. Fundam Clin Pharmacol 1998;12:205-212
32. Szabo ME, Haines D, Garay E, Chiavaroli C, Farine JC, Hannaert P, Berta A, Garay RP. Antioxidant properties of calcium dobesilate in ischemic/reperfused diabetic rat retina. Eur J Pharmacol 2001;428:277-286
33. Xu Q, Qaum T, Adamis AP. Sensitive blood-retinal barrier breakdown quantitation using Evans blue. Invest Ophthalmol Vis Sci 2001;42:789-794
34. Xu H, Manivannan A, Goatman KA, Liversidge J, Sharp PF, Forrester JV, Crane IJ. Improved leukocyte tracking in mouse retinal and choroidal circulation. Exp Eye Res 2002;74:403-410
35. Abbitt KB, Rainger GE, Nash GB. Effects of fluorescent dyes on selectin and integrin-mediated stages of adhesion and migration of flowing leukocytes. J Immunol Methods 2000;239:109-119
36. Hosoya K, Tomi M, Ohtsuki S, Takanaga H, Ueda M, Yanai N, Obinata M, Terasaki T. Conditionally immortalized retinal capillary endothelial cell lines (TR-iBRB) expressing differentiated endothelial cell functions derived from a transgenic rat. Exp Eye Res 2001;72:163-172
37. Müller SL, Portwich M, Schmidt A, Utepbergenov DI, Huber O, Blasig IE, Krause G. The tight junction protein occludin and the adherens junction protein alpha-catenin share a common interaction mechanism with ZO-1. J Biol Chem 2005;280:3747-3756
38. Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol 2001;158:147-152
39. Joussen AM, Poulaki V, Le ML, Koizumi K, Esser C, Janicki H, Schraermeyer U, Kociok N, Fauser S, Kirchhof B, Kern TS, Adamis AP. A central role for inflammation in the pathogenesis of diabetic retinopathy. Faseb J 2004;18:1450-1452 (Pubitemid 39561611)
40. Joussen AM, Poulaki V, Qin W, Kirchhof B, Mitsiades N, Wiegand SJ, Rudge J, Yancopoulos GD, Adamis AP. Retinal vascular endothelial growth factor induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol 2002;160:501-509
41. Qaum T, Xu Q, Joussen AM, Clemens MW, Qin W, Miyamoto K, Hassessian H, Wiegand SJ, Rudge J, Yancopoulos GD, Adamis AP. VEGF-initiated blood-retinal barrier breakdown in early diabetes. Invest Ophthalmol Vis Sci 2001;42:2408-2413 (Pubitemid 32848873)
42. El-Remessy AB, Behzadian MA, Abou-Mohamed G, Franklin T, Caldwell RW, Caldwell RB. Experimental diabetes causes breakdown of the blood-retina barrier by a mechanism involving tyrosine nitration and increases in expression of vascular endothelial growth factor and urokinase plasminogen activator receptor. Am J Pathol 2003;162:1995-2004
43. Kowluru RA, Koppolu P, Chakrabarti S, Chen S. Diabetes-induced activation of nuclear transcriptional factor in the retina, and its inhibition by antioxidants. Free Radic Res 2003;37:1169-1180
44. Carrozzino F, Pugnale P, Féraille E, Montesano R. Inhibition of basal p38 or JNK activity enhances epithelial barrier function through differential modulation of claudin expression. Am J Physiol Cell Physiol 2009;297:C775-787
45. Shivanna M, Rajashekhar G, Srinivas SP. Barrier dysfunction of the corneal endothelium in response to TNF-alpha: role of p38 MAP kinase. Invest Ophthalmol Vis Sci 2010;51:1575-1582
46. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM. TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 2004;286:G367-376