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Neuroprotective Potential of Ginkgo Biloba in Retinal Diseases

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Neuroprotective Potential of Ginkgo Biloba in Retinal Diseases Manuscript submitted to editorial office Neuroprotective potential of Ginkgo biloba in retinal diseases Journal: Planta Medica Manuscript ID PLAMED-2019-03-0258-REV.R1 Manuscript Type: Reviews Date Submitted by the n/a Author:For Peer Review Complete List of Authors: Martínez-Solís, Isabel; Universidad CEU Cardenal Herrera, Farmacia; Universidad CEU Cardenal Herrera, Biomedical Sciences Institute; Universitat de Valencia, Botanical Garden Acero, Nuria; Universidad CEU San Pablo, CC Farmacéuticas y de la Salud Bosch-Morell, Francisco; Universidad CEU Cardenal Herrera, Biomedical Sciences Institute; Universidad CEU Cardenal Herrera, Department of Biomedical Sciences, Faculty of Health Sciences Castillo, Encarna; Universidad CEU Cardenal Herrera, Department of Pharmacy, Faculty of Health Sciences González-Rosende, Maria Eugenia; Universidad CEU Cardenal Herrera, Department of Pharmacy, Faculty of Health Sciences Dolores, Muñoz - Mingarro; Univ. CEU San Pablo, Chemistry Ortega, Teresa; Pharmacy College, Pharmacology; Sanahuja, Maria Amparo; Universidad CEU Cardenal Herrera, Department of Pharmacy, Faculty of Health Sciences Villagrasa, Victoria; Universidad CEU Cardenal Herrera, Department of Pharmacy, Faculty of Health Sciences neurodegeneration, Ginkgo biloba, retinal diseases, age-related macular Keywords: degeneration, diabetic retinopathy, glaucoma, ischaemic retinal disease Georg Thieme Verlag KG, P.O. Box 30 11 20, D-70451 Stuttgart, Germany www.thieme.de/plantamedica Page 1 of 41 Manuscript submitted to editorial office 1 2 3 Neuroprotective potential of Ginkgo biloba in retinal diseases 4 5 6 Isabel Martínez-Solís1,2,3, Nuria Acero4, Francisco Bosch-Morell1,5, Encarna Castillo2, María 7 8 Eugenia González-Rosende2, Dolores Muñoz-Mingarro6, Teresa Ortega7, María Amparo 9 Sanahuja2, Victoria Villagrasa2 10 11 12 1. Biomedical Sciences Institute. Universidad Cardenal Herrera-CEU, CEU Universities. Alfara 13 14 del Patriarca, Valencia (Spain). 15 2. Department of Pharmacy, Faculty of Health Sciences. Universidad Cardenal Herrera-CEU, 16 17 CEU Universities. Alfara del Patriarca, Valencia (Spain). 18 19 3. Botanical Garden. University of Valencia, Valencia (Spain). 20 4. Department of Pharmaceutical and Health Sciences, Faculty of Pharmacy. Universidad San 21 For Peer Review 22 Pablo-CEU, CEU Universities, Madrid (Spain). 23 5. Department of Biomedical Sciences, Faculty of Health Sciences. Universidad Cardenal 24 25 Herrera-CEU, CEU Universities. Alfara del Patriarca, Valencia (Spain). 26 6. Department of Chemistry and Biochemistry, Faculty of Pharmacy. Universidad San Pablo- 27 28 CEU, CEU Universities, Madrid (Spain). 29 30 7. Department of Pharmacology, Pharmacognosy and Botany. Universidad Complutense de 31 Madrid, Madrid (Spain). 32 33 34 Correspondence: Prof. Isabel Martínez-Solís. Department of Pharmacy, Faculty of Health 35 36 Sciences. Universidad Cardenal Herrera-CEU, CEU Universities. C/ Ramón y Cajal s/n. 37 46115 Alfara del Patriarca, Valencia (Spain). Telf. +34 96 136 90 00 | Ext. 64329. E-mail: 38 39 [email protected] 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Georg Thieme Verlag KG, P.O. Box 30 11 20, D-70451 Stuttgart, Germany www.thieme.de/plantamedica Manuscript submitted to editorial office Page 2 of 41 1 2 3 Abstract 4 5 6 Like other tissues of the central nervous system, the retina is susceptible to damage by oxidative 7 8 processes that result in several neurodegenerative disease such as age-related macular 9 degeneration, diabetic retinopathy, glaucoma, ischaemic retinal disease, retinal disease produced 10 11 by light oxidation and detached retina, among other diseases. The use of antioxidant substances 12 is a solution to some health problems caused by oxidative stress, because regulate redox 13 14 homeostasis and reduce oxidative stress. This is important for the neurodegeneration linked to 15 oxidation processes. In line with this, Ginkgo biloba is a medicinal plant with excellent 16 17 antioxidant properties whose effects have been demonstrated in several degenerative processes, 18 19 including retinal diseases associated with neurodegeneration. This review describes the current 20 literature on the role of ginkgo in retinal diseases associated with neurodegeneration. The 21 For Peer Review 22 background leads to the conclusion that G. biloba extracts might be a good option to improve 23 certain neurodegenerative retinal diseases but more research is needed to determine the safety 24 25 and efficacy of G. biloba in these retinal degenerative processes. 26 27 28 29 30 Key words: Ginkgo biloba, Ginkgoaceae, neurodegeneration, retinal diseases, age-related 31 32 macular degeneration, diabetic retinopathy, glaucoma, ischaemic retinal disease 33 34 35 36 37 38 Abbreviations 39 40 ARMD: age-related macular degeneration 41 42 43 BD: Behcet's disease 44 45 CNV: choroidal neovascularisation 46 47 DR: diabetic retinopathy 48 49 GBE: Ginkgo biloba extracts 50 51 52 NTG: normal-tension glaucoma 53 54 IOP: intraocular pressure 55 56 NO: nitric oxide 57 58 NOX: NADPH oxidase 59 60 Georg Thieme Verlag KG, P.O. Box 30 11 20, D-70451 Stuttgart, Germany www.thieme.de/plantamedica Page 3 of 41 Manuscript submitted to editorial office 1 2 3 POAG: primary open-angle glaucoma 4 5 PUFAs: polyunsaturated fatty acids 6 7 8 RCT: randomised controlled trials 9 10 RD: retinal detachment 11 12 ROS: reactive oxygen species 13 14 RP: retinitis pigmentosa 15 16 17 RPE: retinal pigment epithelium 18 19 TM: trabecular meshwork 20 21 VEGF: vascular endothelialFor growth Peer factors Review 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Georg Thieme Verlag KG, P.O. Box 30 11 20, D-70451 Stuttgart, Germany www.thieme.de/plantamedica Manuscript submitted to editorial office Page 4 of 41 1 2 3 Introduction 4 5 6 The degeneration of retinal ganglion cells is involved in several optic neuropathies. These cells 7 8 are neuronal retinal cells that project their axons to the brain by forming the optic nerve [1]. The 9 long axons of these cells make them more vulnerable to hypoxia, exposure to free radicals, 10 11 mechanical compression or photo-oxidative damage [2]. Some retinal diseases are directly 12 related to oxidative stress, especially in aging eyes [3]. Like other neuronal cells, retinal 13 14 ganglion cells have poor antioxidant capacities and insufficient nucleic acid repair mechanisms 15 (mainly in mitochondria) [4]. Reactive oxygen species (ROS) are involved in the progression of 16 17 retina disorders, including aging, apoptosis and post-ischaemic cellular injuries [5]. Glaucoma 18 19 [6, 7], diabetic retinopathy (DR) [8-10], age-related macular degeneration (ARMD) [11, 12], 20 ischaemic retinal injuries [13] are examples of ROS and retina disease relationship. In addition, 21 For Peer Review 22 excessive ROS generation and the consequent induction of oxidative stress are some factors that 23 trigger the cellular response to retinal detachment (RD), and are also a major cytotoxic factor for 24 25 photoreceptor apoptosis [14]. Indeed antioxidants protect against oxidative stress, prevent ROS 26 27 production and they should act as neuroprotectants with therapeutic options for retinal diseases. 28 29 Ginkgo biloba L. (Ginkgoaceae), commonly known as ginkgo, is a living fossil as it is one of 30 31 the most ancient living trees that has existed for more than 250 million years. The therapeutic 32 benefits of ginkgo leaf extracts have long since been well-known, proven by the fact that they 33 34 were used in traditional Chinese medicine 5000 years ago [15]. Dr. Willmar Schwabe 35 36 introduced ginkgo leaf extract as medication in 1965 [16]. Many types of G. biloba extracts 37 (GBE) can be found on the market nowadays, but preclinical and clinical studies have been 38 39 performed mainly using EGb 761 and LI 1370 [17], especially the former. EGb 761 is one of 40 the best characterised herbal extracts containing two major groups of active principles: 41 42 flavonoids (24 %) and terpene lactones (6%). Quercetin, kaempferol, iso-rhamnetin, myricetin, 43 44 laricitrin, mearnsetin and apigenin glycosides have been identified as the main flavonoids, 45 together with biflavonoids like ginkgetin, isoginkgetin [18]. Ginkgolides A, B, C and J 46 47 (diterpene lactones) and bilobalide (sesquiterpene lactones) are the most important components 48 of the terpene fraction [19]. Another important aspect of this extract is that ginkgolic acids 49 50 appear in concentrations below 0.0005%. Ginkgolic acids exert allergenic and genotoxic effects, 51 with neurotoxic results. It has been proven that ginkgolic acids-induced death is mediated by 52 53 both apoptosis and necrosis [20]. In fact due to low concentrations of this type of compounds in 54 55 EGb 761, toxic effects in humans are not expected. EGb 761 and other ginkgo leaf extracts have 56 been widely used to treat and prevent several disorders like Alzheimer´s disease, dementia, 57 58 multiple sclerosis, asthma, vertigo, fatigue, tinnitus or circulatory problems [21-23]. The 59 neuroprotective effect of this plant has been demonstrated both in vitro and in vivo. The 60 Georg Thieme Verlag KG, P.O. Box 30 11 20, D-70451 Stuttgart, Germany www.thieme.de/plantamedica Page 5 of 41 Manuscript submitted to editorial office 1 2 3 terpenoid and flavonoid fractions of GBE protect neurons against necrosis and apoptosis 4 2+ 5 induced by ROS, Ca overload, nitric oxide (NO), or β-amyloid induced toxicity [16]. The 6 antioxidant capacity of the extract can be explained by its ability to act as a free radical 7 8 scavenger of nearly all ROS types, and can inhibit lipid peroxidation. Furthermore, antioxidant 9 properties of ginkgo are particularly interesting given the ability of its active principles, mainly 10 11 the flavonoid fraction, to act at the mitochondrial level unlike other antioxidants [17]. GBE 12 13 maintains ATP content thanks to mitochondrial respiration protection, and also to oxidative 14 phosphorylation preservation.
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