Protective effect of a GLP-1 analog on ischemia-reperfusion induced blood–retinal barrier breakdown and inflammation

Investigative Ophthalmology and Visual Science

Volumn 57, Issue 6, 2016, Pages 2584-2592

  Gonçalves, Andreia ^a,b,c   Lin, Cheng Mao ^b   Muthusamy, Arivalagan ^b   Fontes Ribeiro, Carlos ^a   Ambrósio, António F ^a,c,d   Abcouwer, Steven F ^b   Fernandes, Rosa ^a,c   Antonetti, David A ^b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d Association for Innovation and Biomedical Research on Light and Image   (Portugal)

Author keywords

Blood brain barrier; Inflammation; Ischemia reperfusion injury; Microglia; Vascular biology

Indexed keywords

EVANS BLUE; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1; PROTECTIVE AGENT; INCRETIN; PEPTIDE; VENOM;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD RETINA BARRIER; CELL FRACTIONATION; CELL LYSATE; CONTROLLED STUDY; CYCLIC AMP BLOOD LEVEL; GENE EXPRESSION REGULATION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTRAOCULAR PRESSURE; LYMPHOCYTIC INFILTRATION; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; STAINING; ANALOGS AND DERIVATIVES; ANIMAL; BOVINE; CELL CULTURE; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ISCHEMIA; LONG EVANS RAT; METABOLISM; RETINAL DISEASES;

ANIMALS; BLOOD-RETINAL BARRIER; CATTLE; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GLUCAGON-LIKE PEPTIDE 1; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INCRETINS; INFLAMMATION; ISCHEMIA; MALE; PEPTIDES; RATS; RATS, LONG-EVANS; REPERFUSION INJURY; RETINAL DISEASES; VENOMS;

EID: 84966340290     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-19006     Document Type: Article

References (32)

1. Osborne NN, Casson RJ, Wood JP, Chidlow G, Graham M, Melena J. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog Retin Eye Res. 2004; 23:91-147.
2. Zheng L, Gong B, Hatala DA, Kern TS. Retinal ischemia and reperfusion causes capillary degeneration: similarities to diabetes. Invest Ophthalmol Vis Sci. 2007;48:361-367.
3. 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.
4. Adamiec-Mroczek J, Oficjalska-Mlynczak J. Assessment of selected adhesion molecule and proinflammatory cytokine levels in the vitreous body of patients with type 2 diabetes- role of the inflammatory-immune process in the pathogenesis of proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2008;246:1665-1670.
5. Schwartzman ML, Iserovich P, Gotlinger K, et al. Profile of lipid and protein autacoids in diabetic vitreous correlates with the progression of diabetic retinopathy. Diabetes. 2010;59:1780-1788.
6. Tang J, Kern TS. Inflammation in diabetic retinopathy. Prog Retin Eye Res. 2011;30:343-358.
7. Campbell JE, Drucker DJ. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab. 2013; 17:819-837.
8. Zhang Y, Zhang J, Wang Q, et al. Intravitreal injection of exendin-4 analogue protects retinal cells in early diabetic rats. Invest Ophthalmol Vis Sci. 2011;52:278-285.
9. Goncalves A, Marques C, Leal E, et al. 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;1842:1454-1463.
10. Fan Y, Liu K, Wang Q, Ruan Y, Ye W, Zhang Y. Exendin-4 alleviates retinal vascular leakage by protecting the bloodretinal barrier and reducing retinal vascular permeability in diabetic Goto-Kakizaki rats. Exp Eye Res. 2014;127:104-116.
11. Abcouwer SF, Lin CM, Wolpert EB, et al. Effects of ischemic preconditioning and bevacizumab on apoptosis and vascular permeability following retinal ischemia-reperfusion injury. Invest Ophthalmol Vis Sci. 2010;51:5920-5933.
12. Muthusamy A, Lin CM, Shanmugam S, Lindner HM, Abcouwer SF, Antonetti DA. Ischemia-reperfusion injury induces occludin phosphorylation/ubiquitination and retinal vascular permeability in a VEGFR-2-dependent manner. J Cereb Blood Flow Metab. 2014;34:522-531.
13. Abcouwer SF, Lin CM, Shanmugam S, Muthusamy A, Barber AJ, Antonetti DA. Minocycline prevents retinal inflammation and vascular permeability following ischemia-reperfusion injury. J Neuroinflammation. 2013;10:149.
14. Xu Q, Qaum T, Adamis AP. Sensitive blood-retinal barrier breakdown quantitation using Evans blue. Invest Ophthalmol Vis Sci. 2001;42:789-794.
15. Antonetti DA, Wolpert EB. Isolation and characterization of retinal endothelial cells. Methods Mol Med. 2003;89:365-374.
16. Li AQ, Zhao L, Zhou TF, Zhang MQ, Qin XM. Exendin-4 promotes endothelial barrier enhancement via PKA- and Epac1-dependent Rac1 activation. Am J Physiol Cell Physiol. 2015;308:C164-C175.
17. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol. 1990;27:229-237.
18. Aveleira C, Castilho A, Baptista F, et al. High glucose and interleukin-1beta downregulate interleukin-1 type I receptor (IL-1RI) in retinal endothelial cells by enhancing its degradation by a lysosome-dependent mechanism. Cytokine. 2010;49: 279-286.
19. Madeira MH, Boia R, Santos PF, Ambrosio AF, Santiago AR. Contribution of microglia-mediated neuroinflammation to retinal degenerative diseases. Mediators Inflamm. 2015; 2015:673090.
20. Kastin AJ, Akerstrom V. Entry of exendin-4 into brain is rapid but may be limited at high doses. Int J Obes Relat Metab Disord. 2003;27:313-318.
21. Lee W, Ku SK, Park EJ, Na DH, Kim KM, Bae JS. Exendin-4 inhibits HMGB1-induced inflammatory responses in HUVECs and in murine polymicrobial sepsis. Inflammation. 2014;37: 1876-1888.
22. Dozier KC, Cureton EL, Kwan RO, Curran B, Sadjadi J, Victorino GP. Glucagon-like peptide-1 protects mesenteric endothelium from injury during inflammation. Peptides. 2009; 30:1735-1741.
23. Darsalia V, Hua S, Larsson M, et al. Exendin-4 reduces ischemic brain injury in normal and aged type 2 diabetic mice and promotes microglial M2 polarization. PLoS One. 2014;9: e103114.
24. Kodera R, Shikata K, Kataoka HU, et al. Glucagon-like peptide-1 receptor agonist ameliorates renal injury through its antiinflammatory action without lowering blood glucose level in a rat model of type 1 diabetes. Diabetologia. 2011;54:965-978.
25. Iwai T, Ito S, Tanimitsu K, Udagawa S, Oka J. Glucagon-like peptide-1 inhibits LPS-induced IL-1beta production in cultured rat astrocytes. Neurosci Res. 2006;55:352-360.
26. Arakawa M, Mita T, Azuma K, et al. Inhibition of monocyte adhesion to endothelial cells and attenuation of atherosclerotic lesion by a glucagon-like peptide-1 receptor agonist, exendin-4. Diabetes. 2010;59:1030-1037.
27. Sappington RM, Chan M, Calkins DJ. Interleukin-6 protects retinal ganglion cells from pressure-induced death. Invest Ophthalmol Vis Sci. 2006;47:2932-2942.
28. Sanchez RN, Chan CK, Garg S, et al. Interleukin-6 in retinal ischemia reperfusion injury in rats. Invest Ophthalmol Vis Sci. 2003;44:4006-4011.
29. Lee CH, Yan B, Yoo KY, et al. Ischemia-induced changes in glucagon-like peptide-1 receptor and neuroprotective effect of its agonist, exendin-4, in experimental transient cerebral ischemia. J Neurosci Res. 2011;89:1103-1113.
30. Darsalia V, Mansouri S, Ortsater H, et al. Glucagon-like peptide- 1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats. Clin Sci (Lond). 2012;122:473-483.
31. Kim S, Moon M, Park S. Exendin-4 protects dopaminergic neurons by inhibition of microglial activation and matrix metalloproteinase-3 expression in an animal model of Parkinson’s disease. J Endocrinol. 2009;202:431-439.
32. Parry GC, Mackman N. Role of cyclic AMP response elementbinding protein in cyclic AMP inhibition of NF-kappaBmediated transcription. J Immunol. 1997;159:5450-5456.