Artículos de revistas
Endocytosis Of Tight Junctions Caveolin Nitrosylation Dependent Is Improved By Cocoa Via Opioid Receptor On Rpe Cells In Diabetic Conditions
Investigative Ophthalmology And Visual Science. Association For Research In Vision And Ophthalmology Inc., v. 55, n. 9, p. 6090 - 6100, 2014.
De Faria J.B.L.
De Faria J.M.L.
PURPOSE. Retinal pigment epithelium cells, along with tight junction (TJ) proteins, constitute the outer blood retinal barrier (BRB). Contradictory findings suggest a role for the outer BRB in the pathogenesis of diabetic retinopathy (DR). The aim of this study was to investigate whether the mechanisms involved in these alterations are sensitive to nitrosative stress, and if cocoa or epicatechin (EC) protects from this damage under diabetic (DM) milieu conditions.METHODS. Cells of a human RPE line (ARPE-19) were exposed to high-glucose (HG) conditions for 24 hours in the presence or absence of cocoa powder containing 0.5% or 60.5% polyphenol (low-polyphenol cocoa [LPC] and high-polyphenol cocoa [HPC], respectively).RESULTS. Exposure to HG decreased claudin-1 and occludin TJ expressions and increased extracellular matrix accumulation (ECM), whereas levels of TNF-α and inducible nitric oxide synthase (iNOS) were upregulated, accompanied by increased nitric oxide levels. This nitrosative stress resulted in S-nitrosylation of caveolin-1 (CAV-1), which in turn increased CAV-1 traffic and its interactions with claudin-1 and occludin. This cascade was inhibited by treatment with HPC or EC through δ-opioid receptor (DOR) binding and stimulation, thereby decreasing TNF-α–induced iNOS upregulation and CAV-1 endocytosis. The TJ functions were restored, leading to prevention of paracellular permeability, restoration of resistance of the ARPE-19 monolayer, and decreased ECM accumulation.CONCLUSIONS. The detrimental effects on TJs in ARPE-19 cells exposed to DM milieu occur through a CAV-1 S-nitrosylation–dependent endocytosis mechanism. High-polyphenol cocoa or EC exerts protective effects through DOR stimulation.55960906100Frank, R.N., Diabetic retinopathy (2004) N Engl J Med, 350, pp. 48-58Simo, R., Villarroel, M., Corraliza, L., Hernandez, C., Garcia-Ramirez, M., The retinal pigment epithelium: Something more than a constituent of the blood retinal barrier—implications for the pathogenesis of diabetic retinopathy (2010) J Biomed Biotechnol, p. 190724. , 2010Xu, H.Z., Le, Y.Z., Significance of outer blood-retina barrier breakdown in diabetes and ischemia (2011) Invest Ophthalmol Vis Sci, 52, pp. 2160-2164Strauss, O., The retinal pigment epithelium in visual function (2005) Physiol Rev, 85, pp. 845-881Eagle, R.C., Jr., Mechanisms of maculopathy (1984) Ophthalmology, 91, pp. 613-625Dorey, C.K., Wu, G., Ebenstein, D., Garsd, A., Weiter, J.J., Cell loss in the aging retina: Relationship to lipofuscin accumulation and macular degeneration (1989) Invest Ophthalmol Vis Sci, 30, pp. 1691-1699Vinores, S.A., Gadegbeku, C., Campochiaro, P.A., Green, W.R., Immunohistochemical localization of blood-retinal barrier breakdown in human diabetics (1989) Am J Pathol, 134, pp. 231-235Hewitt, A.T., Adler, R., (1989) Retina: Basic Science and Inherited Retinal Disease, pp. 58-71. , 1st ed. St. Louis: MosbyPautler, E.L., Ennis, S.R., The effect of induced diabetes on the electroretinogram components of the pigmented rat (1980) Invest Ophthalmol Vis Sci, 19, pp. 702-705Samuels, I.S., Lee, C.A., Petrash, J.M., Peachey, N.S., Kern, T.S., Exclusion of aldose reductase as a mediator of ERG deficits in a mouse model of diabetic eye disease (2012) Vis Neurosci, 29, pp. 267-274Villarroel, M., García-ramírez, M., Corraliza, L., Hernández, C., Simó, R., High glucose concentration leads to differential expression of tight junction proteins in human retinal pigment epithelial cells (2009) Endocrinol Nutr, 56, pp. 53-58Silva, K.C., Rosales, M.A., Hamassaki, D.E., Green tea is neuroprotective in diabetic retinopathy (2013) Invest Ophthalmol Vis Sci, 54, pp. 1325-1336Marchiando, A.M., Shen, L., Graham, W.V., Caveolin-1- dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo (2010) J Cell Biol, 189, pp. 111-126Parton, R.G., Simons, K., The multiple faces of caveolae (2007) Nat Rev Mol Cell Biol, 8, pp. 185-194Feltkamp, C.A., Van Der Waerden, A.W., Junction formation between cultured normal rat hepatocytes. An ultrastructural study on the presence of cholesterol and the structure of developing tight-junction strands (1983) J Cell Sci, 63, pp. 271-286Nusrat, A., Parkos, C.A., Verkade, P., Tight junctions are membrane microdomains (2000) J Cell Sci, 113, pp. 1771-1781Schubert, W., Frank, P.G., Razani, B., Park, D.S., Chow, C.W., Lisanti, M.P., Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo (2001) J Biol Chem, 276, pp. 48619-48622Itallie, C.M., Anderson, J.M., Caveolin binds independently to claudin-2 and occludin (2012) Ann N Y Acad Sci, 1257, pp. 103-107Holtkamp, G.M., Kijlstra, A., Peek, R., De Vos, A.F., Retinal pigment epithelium-immune system interactions: Cytokine production and cytokine-induced changes (2001) Prog Retin Eye Res, 20, pp. 29-48Goureau, O., Lepoivre, M., Becquet, F., Courtois, Y., Differential regulation of inducible nitric oxide synthase by fibroblast growth factors and transforming growth factor b in bovine retinal pigmented epithelial cells: Inverse correlation with cellular proliferation (1993) Proc Natl Acad Sci U S A, 90, pp. 4276-4280Liversidge, J., Grabowski, P., Ralston, S., Benjamin, N., Forrester, J.V., Rats’ retinal pigment epithelial cells express an inducible form of nitric oxide synthase and produce nitric oxide in response to inflammatory cytokines and activated T cells (1994) Immunology, 83, pp. 404-409Yuan, Z., Feng, W., Hong, J., Zheng, Q., Shuai, J., Ge, Y., p38MAPK and ERK promote nitric oxide production in cultured human retinal pigmented epithelial cells induced by high concentration glucose (2009) Nitric Oxide, 20, pp. 9-15Husain, S., Liou, G.I., Crosson, C.E., Opioid-receptor-activation: Suppression of ischemia/reperfusion-induced production of TNF-alpha in the retina (2011) Invest Ophthalmol Vis Sci, 52, pp. 2577-2583Ramiro-Puig, E., Castell, M., Cocoa: Antioxidant and immunomodulator (2009) Br J Nutr, 101, pp. 931-940Katavic, P.L., Lamb, K., Navarro, H., Prisinzano, T.E., Flavonoids as opioid receptor ligands: Identification and preliminary structure- activity relationships (2007) J Nat Prod, 70, pp. 1278-1282Panneerselvam, M., Tsutsumi, Y.M., Bonds, J.A., Dark chocolate receptors: Epicatechin-induced cardiac protection is dependent on delta-opioid receptor stimulation (2010) Am J Physiol Heart Circ Physiol, 299, pp. 1604-1609Heimsath, E.G., Jr., Unda, R., Vidro, E., Muniz, A., Villazana-Espinoza, E.T., Tsin, A., ARPE-19 cell growth and cell functions in euglycemic culture media (2006) Curr Eye Res, 31, pp. 1073-1080Costa, I.S., De Souza, G.F., De Oliveira, M.G., Abrahamsohn Ide, A., Snitrosoglutathione (GSNO) is cytotoxic to intracellular amastigotes and promotes healing of topically treated Leishmania major or Leishmania braziliensis skin lesions (2013) J Antimicrob Chemother, 68, pp. 2561-2568Mosmann, T., Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays (1983) J Immunol Meth, 65, pp. 55-63Garcia-Ramírez, M., Villarroel, M., Corraliza, L., Hernández, C., Simó, R., Measuring permeability in human retinal epithelial cells (ARPE-19): Implications for the study of diabetic retinopathy (2011) Methods Mol Biol, 763, pp. 179-194Matthews, J.N.S., Altman, D.G., Campbell, M.J., Royston, P., Analysis of serial measurements in medical research (1990) Br Med J, 300, pp. 230-235Bradford, M.M., A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding (1976) Anal Biochem, 72, pp. 248-254Takeuchi, K., Morizane, Y., Kamami-Levy, C., AMP-dependent kinase inhibits oxidative stress-induced caveolin-1 phosphorylation and endocytosis by suppressing the dissociation between c-Abl and Prdx1 proteins in endothelial cells (2013) J Biol Chem, 288, pp. 20581-20591Azad, N., Vallyathan, V., Wang, L., S-nitrosylation of Bcl-2 inhibits its ubiquitin-proteasomal degradation. A novel antiapoptotic mechanism that suppresses apoptosis (2006) J Biol Chem, 281, pp. 34124-34134Flood, M.T., Gouras, P., Kjeldbye, H., Growth characteristics and ultrastructure of human retinal pigment epithelium in vitro (1980) Invest Ophthalmol Vis Sci, 19, pp. 1309-1320Guidry, C., McFarland, R.J., Morris, R., Witherspoon, C.D., Hook, M., Collagen gel contraction by cells associated with proliferative vitreoretinopathy (1992) Invest Ophthalmol Vis Sci, 33, pp. 2429-2435Klettner, A., Roider, J., Comparison of bevacizumab, ranibizumab, and pegaptanib in vitro: Efficiency and possible additional pathways (2008) Invest Ophthalmol Vis Sci, 49, pp. 4523-4527Elner, V.M., Burnstine, M.A., Strieter, R.M., Kunkel, S.L., Elner, S.G., Cell-associated human retinal pigment epithelium interleukin- 8 and monocyte chemotactic protein-1: Immunochemical and in-situ hybridization analyses (1997) Exp Eye Res, 65, pp. 781-789Ivanov, A.I., Nusrat, A., Parkos, C.A., Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment (2004) Mol Biol Cell, 15, pp. 176-188Bruewer, M., Utech, M., Ivanov, A.I., Hopkins, A.M., Parkos, C.A., Nusrat, A., Interferon-gamma induces internalization of epithelial tight junction proteins via a macropinocytosis-like process (2005) FASEB J, 19, pp. 923-933Shen, L., Turner, J.R., Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis (2005) Mol Biol Cell, 16, pp. 3919-3936Marchiando, A.M., Shen, L., Graham, W.V., Caveolin-1- dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo (2010) Cell Biol, 189, pp. 111-126Kirchner, P., Bug, M., Meyer, H., Ubiquitination of the N-terminal region of caveolin-1 regulates endosomal sorting by the VCP/ p97 AAA-ATPase (2013) J Biol Chem, 288, pp. 7363-7372Ban, Y., Rizzolo, L.J., Regulation of glucose transporters during development of the retinal pigment epithelium (2000) Brain Res Dev Brain Res, 121, pp. 89-95Bergersen, L.J., Jóhannsson, E., Veruki, M.L., Cellular and subcellular expression of monocarboxylate transporters in the pigment epithelium and retina of the rat (1999) Neuroscience, 90, pp. 319-331Senanayake, P.D., Calabro, A., Hu, J.G., Glucose utilization by the retinal pigment epithelium: Evidence for rapid uptake and storage in glycogen, followed by glycogen utilization (2006) Exp Eye Res, 83, pp. 235-246Kim, D.I., Lim, S.K., Park, M.J., Han, H.J., Kim, G.Y., Park, S.H., The involvement of phosphatidylinositol 3-kinase/Akt signaling in high glucose-induced downregulation of GLUT-1 expression in ARPE cells (2007) Life Sci, 80, pp. 626-632Salceda, R., Contreras-Cubas, C., Ascorbate uptake in normal and diabetic rat retina and retinal pigment (2007) Comp Biochem Physiol C Toxicol Pharmacol, 146, pp. 175-179Minamizono, A., Tomi, M., Hosoya, K., Inhibition of dehydroascorbic acid transport across the rat blood-retinal and -brain barriers in experimental diabetes (2006) Biol Pharm Bull, 29, pp. 2148-2150Marmorstein, A.D., The polarity of the retinal pigment epithelium (2001) Traffic, 2, pp. 867-872Frambach, D.A., Roy, C.E., Valentine, J.L., Weiter, J.J., Precocious retinal adhesion is affected by furosemide and ouabain (1989) Curr Eye Res, 8, pp. 553-556Crider, J.Y., Yorio, T., Sharif, N.A., Griffin, B.W., The effects of elevated glucose on Naþ/Kþ-ATPpase of cultured bovine retinal pigment epithelial cells measured by a new nonradioactive rubidium uptake assay (1997) J Ocul Pharmacol Ther, 13, pp. 337-352Villarroel, M., Garcia-Ramirez, M., Corraliza, L., Hernandez, C., Simo, R., Effects of high glucose concentration on the barrier function and the expression of tight junction proteins in human retinal pigment epithelial cells (2009) Exp Eye Res, 89, pp. 913-920Trudeau, K., Roy, S., Guo, W., 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 (2011) Invest Ophthalmol Vis Sci, 52, pp. 6348-6354Yoshikawa, T., Ogata, N., Izuta, H., Shimazawa, M., Hara, H., Takahashi, K., Increased expression of tight junctions in ARPE-19 cells under endoplasmic reticulum stress (2011) Curr Eye Res, 36, pp. 1153-1163Zheng, L., Du, Y., Miller, C., Role of inducible nitric oxide synthase in degeneration of retinal capillaries in mice with streptozotocin-induced diabetes (2007) Diabetologia, 50, pp. 1987-1996Kronstein, R., Seebach, J., Grossklaus, S., Caveolin-1 opens endothelial cell junctions by targeting catenins (2012) Cardiovasc Res, 93, pp. 130-140Klaassen, I., Hughes, J.M., Vogels, I.M.C., Schalkwijk, C.G., Van Noorden, C.J.F., Schlingemann, R.O., Altered expression of genes related to blood–retina barrier disruption in streptozotocin induced diabetes (2009) Exp Eye Res, 89, pp. 4-15Mora, R.C., Bonilha, V.L., Shin, B.C., Bipolar assembly of caveolae in retinal pigment epithelium (2006) Am J Physiol Cell Physiol, 290, pp. 832-843Li, X., McClellan, M.E., Tanito, M., Loss of caveolin-1 impairs retinal function due to disturbance of subretinal microenvironment (2012) J Biol Chem, 287, pp. 16424-16434Kirchner, P., Bug, M., Meyer, H., Ubiquitination of the N-terminal region of caveolin-1 regulates endosomal sorting by the VCP/ p97 AAA-ATPase (2013) J Biol Chem, 288, pp. 7363-7372Pradhan, A.A., Befort, K., Nozaki, C., Gaveriaux-Ruff, C., Kieffer, B.L., The delta opioid receptor: An evolving target for the treatment of brain disorders (2011) Trends Pharmacol Sci, 32, pp. 581-590Engler, M.B., Engler, M.M., The emerging role of flavonoid-rich cocoa and chocolate in cardiovascular health and disease (2006) Nutr Rev, 64, pp. 109-118Ramiro-Puig, E., Castell, M., Cocoa: Antioxidant and immunomodulator (2009) Br J Nutr, 101, pp. 931-940Steffen, Y., Schewe, T., Sies, H., Myeloperoxidase-mediated LDL oxidation and endothelial cell toxicity of oxidized LDL: Attenuation by (-)-epicatechin (2006) Free Radic Res, 40, pp. 1076-1085Granier, S., Manglik, A., Kruse, A.C., Structure of the d-opioid receptor bound to naltrindole (2012) Nature, 485, pp. 400-404Panneerselvam, M., Ali, S.S., Finley, J.C., Epicatechin regulation of mitochondrial structure and function is opioid receptor dependent (2013) Mol Nutr Food Res, 57, pp. 1007-1014Yu, S., Fan, J., Liu, L., Zhang, L., Wang, S., Zhang, J., Caveolin-1 upregulates integrin a2,6-sialylation to promote integrin a5b1- dependent hepatocarcinoma cell adhesion (2013) FEBS Lett, 587, pp. 782-787Rodriguez-Feo, J.A., Hellings, W.E., Moll, F.L., Caveolin-1 influences vascular protease activity and is a potential stabilizing factor in human atherosclerotic disease (2008) PLoS One, e2612, p. 3Cassuto, J., Dou, H., Czikora, I., Peroxynitrite disrupts endothelial caveolae leading to eNOS uncoupling and diminished flow-mediated dilation in coronary arterioles of diabetic patients (2014) Diabetes, 63, pp. 1381-1393Wang, Y., Wang, X., Lau, W.B., Adiponectin inhibits TNF-ainduced vascular inflammatory response via caveolin-mediated ceramidase recruitment and activation (2014) Circ Res, 28, pp. 792-805