Polyphenol-enriched cocoa protects the diabetic retina from glial reaction through the sirtuin pathway

Journal of Nutritional Biochemistry

Volumn 26, Issue 1, 2015, Pages 64-74

  Duarte, Diego A ^a   Rosales, Mariana Ap B ^a   Papadimitriou, Alexandros ^a   Silva, Kamila C ^a   Amancio, Vitor Hugo O ^a   Mendonça, Jacqueline N ^b   Lopes, Norberto P ^b   Lopes de Faria, José B ^a   Lopes de Faria, Jacqueline M ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cocoa; Diabetic retinopathy; GFAP; NAD^{+< sup>; Neurodegeneration; NF kB; SIRT1}

Indexed keywords

EPICATECHIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; HYDROGEN PEROXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLYPHENOL; REACTIVE OXYGEN METABOLITE; SIRTUIN 1; SMALL INTERFERING RNA; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR RELA; ANTIOXIDANT; CATECHIN; PROTECTIVE AGENT; RELA PROTEIN, RAT; SIRT1 PROTEIN, RAT; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CACAO; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIABETIC RETINOPATHY; DOSE RESPONSE; DOWN REGULATION; DRUG EFFICACY; ELECTRORETINOGRAM; GENE SILENCING; INTRACELLULAR SPACE; MALE; MUELLER CELL; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PROTEIN ACETYLATION; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UPREGULATION; ANIMAL; BLOOD; CHEMISTRY; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; GENETICS; GLIA; LIQUID CHROMATOGRAPHY; METABOLISM; OXIDATIVE STRESS; RETINA; SPONTANEOUSLY HYPERTENSIVE RAT; TANDEM MASS SPECTROMETRY;

ANIMALIA; RATTUS; THEOBROMA CACAO;

ANIMALS; ANTIOXIDANTS; CACAO; CATECHIN; CHROMATOGRAPHY, LIQUID; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; DOSE-RESPONSE RELATIONSHIP, DRUG; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; HYDROGEN PEROXIDE; MALE; NEUROGLIA; OXIDATIVE STRESS; POLYPHENOLS; PROTECTIVE AGENTS; RATS; RATS, INBRED SHR; REACTIVE OXYGEN SPECIES; RETINA; SIGNAL TRANSDUCTION; SIRTUIN 1; STREPTOZOCIN; TANDEM MASS SPECTROMETRY; TRANSCRIPTION FACTOR RELA;

EID: 84926249778     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.09.003     Document Type: Article

References (49)

1. Klein R., Klein B.E., Moss S.E., Wong T.Y. The relationship of retinopathy in persons without diabetes to the 15-year incidence of diabetes and hypertension: Beaver Dam Eye Study. Trans Am Ophthalmol Soc 2006, 104:98-107.
2. Asnaghi V., Gerhardinger C., Hoehn T., Adeboje A., Lorenzi M. A role for the polyol pathway in the early neuroretinal apoptosis and glial changes induced by diabetes in the rat. Diabetes 2003, 52:506-511.
3. Duarte D.A., Silva K.C., Rosales M.A., Lopes de Faria J.B., Lopes de Faria J.M. The concomitance of hypertension and diabetes exacerbating retinopathy: the role of inflammation and oxidative stress. Curr Clin Pharmacol 2013, 8:266-277.
4. Barber A.J., Lieth E., Khin S.A., Antonetti D.A., Buchanan A.G., Gardner T.W. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest 1998, 102:783-791.
5. Bringmann A., Iandiev I., Pannicke T., Wurm A., Hollborn M., Wiedemann P., et al. Cellular signaling and factors involved in Müller cell gliosis: neuroprotective and detrimental effects. Prog Retin Eye Res 2009, 28:423-451.
6. Vincent J.A., Mohr S. Inhibition of caspase-1/interleukin-1β signaling prevents degeneration of retinal capillaries in diabetes and galactosemia. Diabetes 2007, 56:224-230.
7. Nagai N., Izumi-Nagai K., Oike Y., Koto T., Satofuka S., Ozawa Y., et al. Suppression of diabetesinduced retinal inflammation by blocking the angiotensin II type 1 receptor or its downstream nuclear factor-kappaB pathway. Invest Ophthalmol Vis Sci 2007, 48:4342-4350.
8. Rine J., Strathern J.N., Hicks J.B., Herskowitz I. A suppressor of mating-type locus mutations in Saccharomyces cerevisiae: evidence for and identification of cryptic mating-type loci. Genetics 1979, 93:877-901.
9. Kaeberlein M., McVey M., Guarente L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev 1999, 13:2570-2580.
10. Lin S.J., Defossez P.A., Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 2000, 289:2126-2128.
11. Chung S., Yao H., Caito S., Hwang J.W., Arunachalam G., Rahman I. Regulation of SIRT1 incellular functions: role of polyphenols. Arch Biochem Biophys 2010, 501:79-90.
12. Rahman I., Kinnula V.L., Gorbunova V., Yao H. SIRT1 as atherapeutic target in inflammaging of the pulmonary disease. Prev Med 2012, 54:S20-S28.
13. Yao H., Rahman I. Perspectives on translational and therapeutic spects of SIRT1 in inflammaging and senescence. Biochem Pharmacol 2012, 84:1332-1339.
14. Yao H., Chung S., Hwang J.W., Rajendrasozhan S., Sundar I.K., Dean D.A., et al. SIRT1 protects against emphysema via FOXO3-mediated reduction of pre-mature senescence in mice. J Clin Invest 2012, 122:2032-2045.
15. Dioum E.M., Chen R., Alexander M.S., Zhang Q., Hogg R.T., Gerard R.D., et al. Regulation of hypoxia-inducible factor 2 alpha signaling by the stress-responsive deacetylase sirtuin1. Science 2009, 324:1289-1293.
16. Bordone L., Guarente L. Calorie restriction, SIRT1and metabolism: understanding longevity. Nat Rev Mol Cell Biol 2005, 6:298-305.
17. Toledano M.B., Leonard W.J. Modulation of transcription factor NF-kappa B binding activity by oxidation-reduction in vitro. Proc Natl Acad Sci 1991, 88:4328-4332.
18. Chen L.F., Williams S.A., Mu Y., Nakano H., Duerr J.M., Buckbinder L., et al. NF-kappaB RelA phosphorylation regulates RelA acetylation. Mol Cell Biol 2005, 25:7966-797.
19. Chen L.F., Mu Y., Greene W.C. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J 2002, 21:6539-6548.
20. Lanzillotta A., Sarnico I., Ingrassia R., Boroni F., Branca C., Benarese M., et al. The acetylation of RelA in Lys310 dictates the NF-kappaB-dependent response in post-ischemic injury. Cell Death Dis 2010, 1:e107.
21. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye R.A., et al. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 2004, 23:2369-2380.
22. Grassi D., Necozione S., Lippi C., Croce G., Valeri L., Pasqualetti P., et al. Cocoa reduces blood pressure and insulin resistance and improves endothelium-dependent vasodilation in hypertensives. Hypertension 2005, 46:398-405.
23. Taubert D., Roesen R., Lehmann C., Jung N., Schömig E. Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide: a randomized controlled trial. JAMA 2007, 298:49-60.
24. Desch S., Schmidt J., Kobler D., Sonnabend M., Eitel I., Sareban M., et al. Effect of cocoa products on blood pressure: systematic review and meta-analysis. Am J Hypertens 2010, 23:97-103.
25. Rimbach G., Melchin M., Moehring J., Wagner A.E. Polyphenols from cocoa and vascular health: a critical review. Int J Mol Sci 2009, 10:4290-4309.
26. Siddique H.R., Liao D.J., Mishra S.K., Schuster T., Wang L., Matter B., et al. Epicatechin-rich cocoa polyphenol inhibits kras-activated pancreatic ductal carcinoma cell growth in vitro and in a mouse model. Int J Cancer 2012, 131:1720-1731.
27. Ejaz Ahmed M., Khan M.M., Javed H., Vaibhav K., Khan A., Tabassum R., et al. Amelioration of cognitive impairment and neurodegeneration by catechin hydrate in rat model of streptozotocin-induced experimental dementia of Alzheimer's type. Neurochem Int 2013, 62:492-501.
28. Kang K.S., Yamabe N., Wen Y., Fukui M., Zhu B.T. Beneficial effects of natural phenolics on levodopa methylation and oxidative neurodegeneration. Brain Res 2013, 1497:1-14.
29. Al-Gayyar M.M., Matragoon S., Pillai B.A., Ali T.K., Abdelsaid M.A., El-Remessy A.B. Epicatechin blocks pro-nerve growth factor (proNGF)-mediated retinal neurodegeneration via inhibition of p75 neurotrophin receptor expression in a rat model of diabetes. Diabetologia 2011, 54:669-680.
30. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63.
31. Xu Y., Nie L., Yin Y.G., Tang J.L., Zhou J.Y., Li D.D., et al. Resveratrol protects against hyperglycemia-induced oxidative damage to mitochondria by activating SIRT-1 in rat mesangial cells. Toxicol Appl Pharmacol 2012, 259:395-401.
32. Silva K.C., Rosales M.A., Hamassaki D.E., Saito K.C., Faria A.M., Ribeiro P.A., et al. Green tea is neuroprotective in diabetic retinopathy. Invest Ophthalmol Vis Sci 2013, 54:1325-1336.
33. Amadio M., Scapagnini G., Laforenza U., Intrieri M., Romeo L., Govoni S., et al. Post-transcriptional regulation of HSP70 expression following oxidative stress in SH-SY5Y cells: the potential involvement of the RNA-binding protein HuR. Curr Pharm Des 2008, 14:2651-2658.
34. Goto T., Yoshida Y., Kiso M., Nagashima H. Simultaneous analysis of individual catechins and caffeine in green tea. J Chromatogr 1996, 749:295-299.
35. Bui B.V., Armitage J.A., Tolcos M., Cooper M.E., Vingrys A.J. ACE inhibition salvages the visual loss caused by diabetes. Diabetologia 2003, 46:401-408.
36. Paudel L., Wyzgoski F.J., Scheerens J.C., Chanon A.M., Reese R.N., Smiljanic D., et al. Nonanthocyanin secondary metabolites of black raspberry (Rubus occidentalis L.) fruits: identification by HPLC-DAD, NMR, HPLC-ESI-MS, and ESI-MS/MS analyses. J Agric Food Chem 2013, 61:12032-12043.
37. Qiao Shi, Shi Rui, Liu Man, Zhang Chong, Yang Wei, Shi Xiaowei, et al. Simultaneous quantification of flavonoids and phenolic acids in Herba Scutellariae barbatae and its confused plants by high performance liquid chromatographytandem mass spectrometry. Food Chem 2011, 129:1297-1304.
38. KolthurSeetharam U., Dantzer F., McBurney M.W., de Murcia G., Sassone-Corsi P. Control of AIF-mediated cell death by the functional inter play of SIRT1 and PARP-1 inresponse to DNA damage. Cell Cycle 2006, 5:873-877.
39. Madison D.L., Stauffer D., Lundblad J.R. The PARP inhibitor PJ34 causes a PARP1-independent, p21 dependent mitotic arrest. DNA Repair (Amst) 2011, 10:1003-1013.
40. Rothgiesser K.M., Erener S., Waibel S., Lüscher B., Hottiger M.O. SIRT2 regulates NF-κB dependent gene expression through deacetylation of p65 Lys310. J Cell Sci 2010, 123:4251-4258.
41. Dai Y., Rahmani M., Dent P., Grant S. Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-κB activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Mol Cell Biol 2005, 25:5429-5444.
42. Bisson J.F., Hidalgo S., Rozan P., Messaoudi M. Preventive effects of ACTICOA powder, a cocoa polyphenolic extract, on experimentally induced prostate hyperplasia in Wistar-Unilever rats. J Med Food 2007, 10:622-627.
43. Chen L.F. Duration of nuclear NF-κB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
44. Kiernan R., Brès V., Ng R.W., Coudart M.P., El Messaoudi S., Sardet C., et al. Post-activation turn-off of NF-κB-dependent transcription is regulated by acetylation of p65. J Biol Chem 2003, 278:2758-2766.
45. Chen L.F., Fischle W., Verdin E., Greene W.C. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
46. Martínez-Balbás M.A., Bauer U.M., Nielsen S.J., Brehm A., Kouzarides T. Regulation of E2F1 activity by acetylation. EMBO J 2000, 19:662-671.
47. Gu W., Roeder R.G. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997, 90:595-606.
48. Brunet A., Sweeney L.B., Sturgill J.F., Chua K.F., Greer P.L., Lin Y., et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004, 26:2011-2015.
49. Zheng Z., Chen H., Li J., Li T., Zheng B., Zheng Y., et al. Sirtuin 1-mediated cellular metabolic memory of high glucose via the LKB1/AMPK/ROS pathway and therapeutic effects of metformin. Diabetes 2012, 61:217-228.