Neuroprotective Effect of Brazilian Green Propolis on Retinal Ganglion Cells in Ischemic Mouse Retina

References

• Organisciak DT, Darrow RM, Barsalou L, Darrow RA, Kutty RK, Kutty G, Wiggert B. Light history and age-related changes in retinal light damage. Invest Ophthalmol Vis Sci. 1998;39:1107–16.
   PubMed Web of Science ®Google Scholar
• Bhuyan KC, Bhuyan DK. Molecular mechanism of cataractogenesis: III. Toxic metabolites of oxygen as initiators of lipid peroxidation and cataract. Curr Eye Res. 1984;3(1):67–81. doi:10.3109/02713688408997188.
   PubMed Web of Science ®Google Scholar
• Yildirim O, Ates NA, Ercan B, Muşlu N, Unlü A, Tamer L, Atik U, Kanik A. Role of oxidative stress enzymes in open-angle glaucoma. Eye (Lond). 2005;19(5):580–83. doi:10.1038/sj.eye.6701565.
   PubMed Web of Science ®Google Scholar
• Beatty S, Koh H, Phil M, Henson D, Boulton M. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol. 2000;45(2):115–34. doi:10.1016/S0039-6257(00)00140-5.
   PubMed Web of Science ®Google Scholar
• Kanada A, Nishimura Y, Yamaguchi JY, Kobayashi M, Mishima K, Horimoto K, Kanemaru K, Oyama Y. Extract of Ginkgo biloba leaves attenuates kainate-induced increase in intracellular Ca2+ concentration of rat cerebellar granule neurons. Biol Pharm Bull. 2005;28(5):934–36. doi:10.1248/bpb.28.934.
   PubMed Web of Science ®Google Scholar
• Gottlieb M, Leal-Campanario R, Campos-Esparza MR, Sánchez-Gómez MV, Alberdi E, Arranz A, Delgado-García JM, Gruart A, Matute C. Neuroprotection by two polyphenols following excitotoxicity and experimental ischemia. Neurobiol Dis. 2006;23(2):374–86. doi:10.1016/j.nbd.2006.03.017.
   PubMed Web of Science ®Google Scholar
• Ji YS, Park JW, Heo H, Park JS, Park SW. The neuroprotective effect of carnosine (β-Alanyl-l-Histidine) on retinal ganglion cell following ischemia-reperfusion injury. Curr Eye Res. 2014;39(6):634–41. doi:10.3109/02713683.2013.855235.
   PubMed Web of Science ®Google Scholar
• Kim SJ, Sung MS, Heo H, Lee JH, Park SW. Mangiferin protects retinal ganglion cells in ischemic mouse retina via SIRT1. Curr Eye Res. 2016;41(6):844–55. doi:10.3109/02713683.2015.1050736.
   PubMed Web of Science ®Google Scholar
• Park YK, Alencar SM, Aguiar CL. Botanical origin and chemical composition of Brazilian propolis. J Agric Food Chem. 2002;50(9):2502–06. doi:10.1021/jf011432b.
   PubMed Web of Science ®Google Scholar
• Greenaway W, May J, Scaysbrook T, Whatley FR. Identification by gas chromatography-mass spectrometry of 150 compounds in propolis. Zeitschrift Für Naturforschung C. 1991;46(1–2):111–21. doi:10.1515/znc-1991-1-218.
   Google Scholar
• Drago L, Mombelli B, De Vecchi E, Fassina MC, Tocalli L, Gismondo MR. In vitro antimicrobial activity of propolis dry extract. J Chemother. 2000;12(5):390–95. doi:10.1179/joc.2000.12.5.390.
   PubMed Web of Science ®Google Scholar
• Mirzoeva OK, Calder PC. The effect of propolis and its components on eicosanoid production during the inflammatory response. Prostaglandins Leukot Essent FattyAcids. 1996;55(6):441–49. doi:10.1016/S0952-3278(96)90129-5.
   PubMed Web of Science ®Google Scholar
• Pascual C, Gonzalez R, Torricella RG. Scavenging action of propolis extract against oxygen radicals. J Ethnopharmacol. 1994;41(1–2):9–13. doi:10.1016/0378-8741(94)90052-3.
   PubMed Web of Science ®Google Scholar
• Jaiswal AK, Venugopal R, Mucha J, Carothers AM, Grunberger D. Caffeic acid phenethyl ester stimulates human antioxidant response element-mediated expression of the NAD(P)H: quinone oxidoreductase (NQO1) gene. Cancer Res. 1997;57:440–46.
   PubMed Web of Science ®Google Scholar
• Ishihara M, Naoi K, Hashita M, Itoh Y, Suzui M. Growth inhibitory activity of ethanol extracts of Chinese and Brazilian propolis in four human colon carcinoma cell lines. Oncol Rep. 2009;22:349–54.
   PubMed Web of Science ®Google Scholar
• Bazmandegan G, Boroushaki MT, Shamsizadeh A, Ayoobi F, Hakimizadeh E, Allahtavakoli M. Brown propolis attenuates cerebral ischemia-induced oxidative damage via affecting antioxidant enzyme system in mice. Biomed Pharmacother. 2017;85:503–10. doi:10.1016/j.biopha.2016.11.057.
   PubMed Web of Science ®Google Scholar
• Inokuchi Y, Shimazawa M, Nakajima Y, Suemori S, Mishima S, Hara H. Brazilian green propolis protects against retinal damage in vitro and in vivo. Evidence-Based Complement Alternat Med. 2006;3(1):71–77. doi:10.1093/ecam/nek005.
   PubMed Web of Science ®Google Scholar
• Hughes WF. Quantitation of ischemic damage in the rat retina. Exp Eye Res. 1991;53(5):573–82. doi:10.1016/0014-4835(91)90215-Z.
   PubMed Web of Science ®Google Scholar
• Abu-El-Asrar AM, Dralands L, Missotten L, Al-Jadaan IA, Geboes K. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest Ophthalmol Vis Sci. 2004;45(8):2760–66. doi:10.1167/iovs.03-1392.
   PubMed Web of Science ®Google Scholar
• Weinreb RN, Khaw PT. Primary open-angle glaucoma. Lancet. 2004;363(9422):1711–20. doi:10.1016/S0140-6736(04)16257-0.
   PubMed Web of Science ®Google Scholar
• Osborne NN, Ugarte M, Chao M, Chidlow G, Bae JH, Wood JP, Nash MS. Neuroprotection in relation to retinal ischemia and relevance to glaucoma. Surv Ophthalmol. 1999;43:S102–S128. doi:10.1016/S0039-6257(99)00044-2.
   PubMed Web of Science ®Google Scholar
• Wax MB, Tezel G. Neurobiology of glaucomatous optic neuropathy: diverse cellular events in neurodegeneration and neuroprotection. Mol Neurobiol. 2002;26(1):45–55. doi:10.1385/MN:26:1.
   PubMed Web of Science ®Google Scholar
• Neufeld AH, Kawai S, Das S, Vora S, Gachie E, Connor JR, Manning PT. Loss of retinal ganglion cells following retinal ischemia: the role of inducible nitric oxide synthase. Exp Eye Res. 2002;75(5):521–28. doi:10.1006/exer.2002.2042.
   PubMed Web of Science ®Google Scholar
• Vorwerk CK, Hyman BT, Miller JW, Husain D, Zurakowski D, Huang PL, Fishman MC, Dreyer EB. The role of neuronal and endothelial nitric oxide synthase in retinal excitotoxicity. Invest Ophthalmol Vis Sci. 1997;38:2038–44.
   PubMed Web of Science ®Google Scholar
• Büchi ER. Cell death in rat retina after pressure-induced ischaemia-reperfusion insult: electron microscopic study. II. Outer nuclear layer. Jpn J Ophthalmol. 1992;36:62–68.
   PubMed Web of Science ®Google Scholar
• Quigley HA, Nickells RW, Kerrigan LA, Pease ME, Thibault DJ, Zack DJ. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774–86.
   PubMed Web of Science ®Google Scholar
• Nguyen SM, Alexejun CN, Levin LA. Amplification of a reactive oxygen species signal in axotomized retinal ganglion cells. Antioxid Redox Signal. 2003;5(5):629–34. doi:10.1089/152308603770310293.
   PubMed Web of Science ®Google Scholar
• Kanamori A, Catrinescu MM, Kanamori N, Mears KA, Beaubien R, Levin LA. Superoxide is an associated signal for apoptosis in axonal injury. Brain. 2010;133(9):2612–25. doi:10.1093/brain/awq105.
   PubMedGoogle Scholar
• Biermann J, Grieshaber P, Goebel U, Martin G, Thanos S, Di Giovanni S, Lagrèze WA. Valproic acid-mediated neuroprotection and regeneration in injured retinal ganglion cells. Invest Ophthalmol Vis Sci. 2010;51(1):526–34. doi:10.1167/iovs.09-3903.
   PubMed Web of Science ®Google Scholar
• Fan J, Alsarraf O, Dahrouj M, Platt KA, Chou CJ, Rice DS, Crosson CE. Inhibition of HDAC2 protects the retina from ischemic injury. Investig Ophthalmol Vis Sci. 2013;54(6):4072–80. doi:10.1167/iovs.12-11529.
   PubMed Web of Science ®Google Scholar
• Schmitt HM, Schlamp CL, Nickells RW. Role of HDACs in optic nerve damage-induced nuclear atrophy of retinal ganglion cells. Neurosci Lett. 2016;625:11–15. doi:10.1016/j.neulet.2015.12.012.
   PubMed Web of Science ®Google Scholar
• López BG, Schmidt EM, Eberlin MN, Sawaya AC. Phytochemical markers of different types of red propolis. Food Chem. 2014;146:174–80. doi:10.1016/j.foodchem.2013.09.063.
   PubMed Web of Science ®Google Scholar
• Akyol S, Ozturk G, Ginis Z, Armutcu F, Yigitoglu MR, Akyol O. In vivo and in vitro antineoplastic actions of Caffeic acid phenethyl ester (CAPE): therapeutic perspectives. Nutr Cancer. 2013;65(4):515–26. doi:10.1080/01635581.2013.776693.
   PubMed Web of Science ®Google Scholar
• Zhang ZZ, Gong YY, Shi YH, Zhang W, Qin XH, Wu XW. Valproate promotes survival of retinal ganglion cells in a rat model of optic nerve crush. Neuroscience. 2012;224:282–93. doi:10.1016/j.neuroscience.2012.07.056.
   PubMed Web of Science ®Google Scholar
• Araújo AS, da Rocha LL, Tomazela DM, Sawaya AC, Almeida RR, Catharino RR, Eberlin MN. Electrospray ionization mass spectrometry fingerprinting of beer. Analyst. 2005;130(6):884–89. doi:10.1039/b415252b.
   PubMed Web of Science ®Google Scholar
• Kakoolaki S, Talas ZS, Cakir O, Ciftci O, Ozdemir I. Role of propolis on oxidative stress in fish brain. Basic Clin Neurosci. 2013;4:153–58.
   PubMedGoogle Scholar
• Shimazawa M, Chikamatsu S, Morimoto N, Mishima S, Nagai H, Hara H. Neuroprotection by Brazilian green propolis against in vitro and in vivo ischemic neuronal damage. Evid Based Complement Alternat Med. 2005;2(2):201–07. doi:10.1093/ecam/neh078.
   PubMed Web of Science ®Google Scholar
• Righi AA, Alves TR, Negri G, Marques LM, Breyer H, Salatino A. Brazilian red propolis: unreported substances, antioxidant and antimicrobial activities. J Sci Food Agric. 2001;91(13):2363–70. doi:10.1002/jsfa.4468.
   Google Scholar
• Hata T, Tazawa S, Ohta S, Rhyu MR, Misaka T, Ichihara K, Artepillin C. A major ingredient of Brazilian propolis, induces a pungent taste by activating TRPA1 channels. PLoS One. 2012;7(11):e48072. doi:10.1371/journal.pone.0048072.
   PubMed Web of Science ®Google Scholar
• Farooqui T, Farooqui AA. Beneficial effects of propolis on human health and neurological diseases. Front Biosci(Elite Ed). 2012;4:779–93. doi:10.2741/e418.
   PubMedGoogle Scholar
• Punithavathi VR, Prince PS, Kumar R, Selvakumari J. Antihyperglycaemic, antilipid peroxidative and antioxidant effects of gallic acid on streptozotocin induced diabetic Wistar rats. Eur J Pharmacol. 2011;650(1):465–71. doi:10.1016/j.ejphar.2010.08.059.
   PubMed Web of Science ®Google Scholar
• Zhao L, Pu L, Wei J, Li J, Wu J, Xin Z, Gao W, Guo C. Brazilian green propolis improves antioxidant function in patients with type 2 diabetes mellitus. Int J Environ Res Public Health. 2016;13:5. doi:10.3390/ijerph13050498.
   Web of Science ®Google Scholar
• Ueda T, Inden M, Shirai K, Sekine SI, Masaki Y, Kurita H, Ichihara K, Inuzuka T, Hozumi I. The effects of Brazilian green propolis that contains flavonols against mutant copper-zinc superoxide dismutase-mediated toxicity. Sci Rep. 2017;7(1):2882. doi:10.1038/s41598-017-03115-y.
   PubMedGoogle Scholar
• Gao W, Wu J, Wei J, Pu L, Guo C, Yang J, Yang M, Luo H. Brazilian green propolis improves immune function in aged mice. J Clin Biochem Nutr. 2014;55(1):7–10. doi:10.3164/jcbn.13-70.
   PubMed Web of Science ®Google Scholar
• Semenza GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol. 1999;15:551–78. doi:10.1146/annurev.cellbio.15.1.551.
   PubMed Web of Science ®Google Scholar
• Lee JW, Bae SH, Jeong JW, Kim SH, Kim KW. Hypoxia-inducible factor (HIF-1) alpha: its protein stability and biological functions. Exp Mol Med. 2004;36(1):1–12. doi:10.1038/emm.2004.1.
   PubMed Web of Science ®Google Scholar
• Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, et al. Role of HIF-1alpha in hypoxia- mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 1998;394(6692):485–90. doi:10.1038/28867.
   PubMed Web of Science ®Google Scholar
• Halterman MW, Miller CC, Federoff HJ. Hypoxia-inducible factor-1alpha mediates hypoxia-induced delayed neuronal death that involves p53. J Neurosci. 1999;19(16):6818–24. doi:10.1523/JNEUROSCI.19-16-06818.1999.
   PubMed Web of Science ®Google Scholar
• Zhang H, Bosch-Marce M, Shimoda LA. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008;283:10892–903.
   PubMed Web of Science ®Google Scholar
• Chang Y, Hsieh CY, Peng ZA, Yen TL, Hsiao G, Chou DS, Chen CM, Sheu JR. Neuroprotective mechanisms of puerarin in middle cerebral artery occlusion-induced brain infarction in rats. J Biomed Sci. 2009;16:9. doi:10.1186/1423-0127-16-9.
   PubMed Web of Science ®Google Scholar
• Mellor HR, Harris AL. The role of the hypoxia-inducible BH3-only proteins BNIP3 and BNIP3L in cancer. Cancer Metastasis Rev. 2007;26(3–4):553–66. doi:10.1007/s10555-007-9080-0.
   PubMed Web of Science ®Google Scholar
• Woldemussie E, Wijono M, Ruiz G. Müller cell response to laser-induced increase in intraocular pressure in rats. Glia. 2004;47(2):109–19. doi:10.1002/glia.v47:2.
   PubMed Web of Science ®Google Scholar
• Crosson CE, Mani SK, Husain S, Alsarraf O, Menick DR. Inhibition of histone deacetylase protects the retina from ischemic injury. Invest Ophthalmol Vis Sci. 2010;51(7):3639–45. doi:10.1167/iovs.09-4538.
   PubMed Web of Science ®Google Scholar
• Saha RN, Pahan K. HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis. Cell Death Differ. 2006;13(4):539–50. doi:10.1038/sj.cdd.4401769.
   PubMed Web of Science ®Google Scholar
• Pelzel HR, Schlamp CL, Nickells RW. Histone H4 deacetylation plays a critical role in early gene silencing during neuronal apoptosis. BMC Neurosci. 2010;11:62. doi:10.1186/1471-2202-11-62.
   PubMed Web of Science ®Google Scholar
• Alsarraf O, Fan J, Dahrouj M, Chou CJ, Menick DR, Crosson CE. Acetylation: a lysine modification with neuroprotective effects in ischemic retinal degeneration. Exp Eye Res. 2014;127:124–31. doi:10.1016/j.exer.2014.07.012.
   PubMed Web of Science ®Google Scholar
• Alsarraf O, Fan J, Dahrouj M, Chou CJ, Yates PW, Crosson CE. Acetylation preserves retinal ganglion cell structure and function in a chronic model of ocular hypertension. Invest Ophthalmol Vis Sci. 2014;55(111):7486–93. doi:10.1167/iovs.14-14792.
   PubMedGoogle Scholar
• Ishiai S, Tahara W, Yamamoto E, Yamamoto R, Nagai K. Histone deacetylase inhibitory effect of Brazilian propolis and its association with the antitumor effect in Neuro2a cells. Food Sci Nutr. 2014;2(5):565–70. doi:10.1002/fsn3.2014.2.issue-5.
   PubMedGoogle Scholar
• Ko LJ, Prives C. p53: puzzle and paradigm. Genes Dev. 1996;10(9):1054–72. doi:10.1101/gad.10.9.1054.
   PubMed Web of Science ®Google Scholar
• Momand J, Zambetti GP, Olson DC, George D, Levine AJ. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell. 1992;69(7):1237–45. doi:10.1016/0092-8674(92)90644-R.
   PubMed Web of Science ®Google Scholar
• Prives C, Hall PA. The p53 pathway. J Pathol. 1999;187(1):112–26. doi:10.1002/(ISSN)1096-9896.
   PubMed Web of Science ®Google Scholar
• Joo CK, Choi JS, Ko HW, Park KY, Sohn S, Chun MH, Oh YJ, Gwag BJ. Necrosis and apoptosis after retinal ischemia: involvement of NMDA-mediated excitotoxicity and p53. Invest Ophthalmol Vis Sci. 1999;40:713–20.
   PubMed Web of Science ®Google Scholar
• Rosenbaum DM, Rosenbaum PS, Gupta H, Singh M, Aggarwal A, Hall DH, Roth S, Kessler JA. The role of the p53 protein in the selective vulnerability of the inner retina to transient ischemia. Invest Ophthalmol Vis Sci. 1998;39:2132–39.
   PubMed Web of Science ®Google Scholar
• Westlund BS, Cai B, Zhou J, Sparrow JR. Involvement of c-Abl, p53 and the MAP kinase JNK in the cell death program initiated in A2E-laden ARPE-19 cells by exposure to blue light. Apoptosis. 2009;14(1):31–41. doi:10.1007/s10495-008-0285-7.
   PubMed Web of Science ®Google Scholar
• Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 1995;80(2):293–99. doi:10.1016/0092-8674(95)90412-3.
   PubMed Web of Science ®Google Scholar
• Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell. 2001;7(3):683–94. doi:10.1016/S1097-2765(01)00214-3.
   PubMed Web of Science ®Google Scholar
• Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM. p53 has a direct apoptogenic role at the mitochondria. Mol Cell. 2003;11(3):577–90. doi:10.1016/S1097-2765(03)00050-9.
   PubMed Web of Science ®Google Scholar
• Hong LZ, Zhao XY, Zhang HL. p53-mediated neuronal cell death in ischemic brain injury. Neurosci Bull. 2010;26(3):232–40. doi:10.1007/s12264-010-1111-0.
   PubMed Web of Science ®Google Scholar
• Wilson AM, Chiodo VA, Boye SL, Brecha NC, Hauswirth WW, Di Polo A. Inhibitor of apoptosis stimulating protein of p53 (iASPP) is required for neuronal survival after axonal injury. PLoS One. 2014;9:e94175.
   PubMed Web of Science ®Google Scholar
• Wilson AM, Morquette B, Abdouh M, Unsain N, Barker PA, Feinstein E, Bernier G, Di Polo A. ASPP1/2 regulate p53-dependent death of retinal ganglion cells through PUMA and Fas/CD95 activation in vivo. Journal of Neuroscience. 2013;33(5):2205–16. doi:10.1523/JNEUROSCI.2635-12.2013.
   PubMed Web of Science ®Google Scholar
• Lebrun-Julien F, Suter U. Combined HDAC1 and HDAC2 depletion promotes retinal ganglion cell survival after injury through reduction of p53 target gene expression. ASN Neuro. 2015;7(3). doi:10.1177/1759091415593066.
   PubMed Web of Science ®Google Scholar
• Berthiaume M, Boufaied N, Moisan A, Gaudreau L. High levels of oxidative stress globally inhibit gene transcription and histone acetylation. DNA Cell Biol. 2006;25(2):124–34. doi:10.1089/dna.2006.25.124.
   PubMed Web of Science ®Google Scholar
• Tzeng TF, Liu WY, Liou SS, Hong TY, Liu IM. Antioxidant-rich extract from plantaginis semen ameliorates diabetic retinal injury in a streptozotocin-induced diabetic rat model. Nutrients. 2016;8(9). doi:10.3390/nu8090572.
   Web of Science ®Google Scholar
• Oliveira WH, Nunes AK, França ME, Santos LA, Lós DB, Rocha SW, Barbosa KP, Rodrigues GB, Peixoto CA. Effects of metformin on inflammation and short-term memory in streptozotocin-induced diabetic mice. Brain Res. 2016;1644:149–60. doi:10.1016/j.brainres.2016.05.013.
   PubMed Web of Science ®Google Scholar
• Wardyn JD, Ponsford AH, Sanderson CM. Dissecting molecular cross-talk between Nrf2 and NF-κB response pathways. Biochem Soc Trans. 2015;43(4):621–26. doi:10.1042/BST20150014.
   PubMed Web of Science ®Google Scholar