Oral Supplements of Ginkgo biloba Extract Alleviate Neuroinflammation, Oxidative Impairments and Neurotoxicity in Rotenone-Induced Parkinsonian Rats | Bentham Science
Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Oral Supplements of Ginkgo biloba Extract Alleviate Neuroinflammation, Oxidative Impairments and Neurotoxicity in Rotenone-Induced Parkinsonian Rats

Author(s): Nema A. Mohammed, Heba M. Abdou, Mona A. Tass, Manal Alfwuaires, Ashraf M. Abdel-Moneim and Amina E. Essawy*

Volume 21, Issue 12, 2020

Page: [1259 - 1268] Pages: 10

DOI: 10.2174/1389201021666200320135849

Price: $65

Open Access Journals Promotions 2
Abstract

Background: Ginkgo biloba extract (GbE) is known to contain several bioactive compounds and exhibits free radical scavenging activity. Parkinson's Disease (PD) is a neurodegenerative disorder characterized by the loss of dopaminergic neurons and is associated with oxidative stress, neuroinflammation and apoptosis.

Objective: The current study aimed to investigate the neuroprotective effect of GbE in a rat model of PD induced by rotenone (ROT; a neurotoxin).

Methods: Twenty-four male albino rats were randomly divided into four groups of six rats each: normal control, GbE treated, toxin control (ROT treated) and GbE+ROT group.

Results: Oral administration of ROT (2.5 mg/kg b.w.) for 50 days caused an increased generation of lipid peroxidation products and significant depletion of reduced glutathione, total thiol content and activities of enzymatic antioxidants, i.e., superoxide dismutase and glutathione peroxidase in the brains of treated rats. Furthermore, ROT caused an elevation in acetylcholinesterase, interleukin-1β, interleukin- 6 and tumor necrosis factor-α and a significant reduction in dopamine in the stratum and substantia nigra. Immunohistochemical results illustrated that ROT treatment reduced the expression of tyrosine hydroxylase (TH). GbE treatment (150 mg/kg b.w./day) significantly reduced the elevated oxidative stress markers and proinflammatory cytokines and restored the reduced antioxidant enzyme activities, DA level and TH expression. These results were confirmed by histological observations that clearly indicated a neuroprotective effect of GbE against ROT-induced PD.

Conclusion: GbE mitigated ROT-induced PD via the inhibition of free-radical production, scavenging of ROS, and antioxidant enhancement.

Keywords: Ginkgo biloba, neuroprotection, oxidative stress, rotenone, Parkinson's disease, ROT treatment.

« Previous Next »
Graphical Abstract

[1]
Vali, S.; Mythri, R.B.; Jagatha, B.; Padiadpu, J.; Ramanujan, K.S.; Andersen, J.K.; Gorin, F.; Bharath, M.M.S. Integrating glutathione metabolism and mitochondrial dysfunction with implications for Parkinson’s disease: A dynamic model. Neuroscience, 2007, 149(4), 917-930.
[http://dx.doi.org/10.1016/j.neuroscience.2007.08.028 ] [PMID: 17936517]
[2]
Sanders, L.H.; Timothy Greenamyre, J. Oxidative damage to macromolecules in human Parkinson disease and the rotenone model. Free Radic. Biol. Med., 2013, 62, 111-120.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.01.003 ] [PMID: 23328732]
[3]
Naduthota, R.M.; Bharath, R.D.; Jhunjhunwala, K.; Yadav, R.; Saini, J.; Christopher, R.; Pal, P.K. Imaging biomarker correlates with oxidative stress in Parkinson’s disease. Neurol. India, 2017, 65(2), 263-268.
[http://dx.doi.org/10.4103/neuroindia.NI_981_15 ] [PMID: 28290386]
[4]
Spillantini, M.G.; Schmidt, M.L.; Lee, V.M.Y.; Trojanowski, J.Q.; Jakes, R.; Goedert, M. Alpha-synuclein in Lewy bodies. Nature, 1997, 388(6645), 839-840.
[http://dx.doi.org/10.1038/42166 ] [PMID: 9278044]
[5]
Kaur, H.; Chauhan, S.; Sandhir, R. Protective effect of lycopene on oxidative stress and cognitive decline in rotenone induced model of Parkinson’s disease. Neurochem. Res., 2011, 36(8), 1435-1443.
[http://dx.doi.org/10.1007/s11064-011-0469-3 ] [PMID: 21484267]
[6]
Radad, K.; Moldzio, R.; Al-Shraim, M.; Al-Emam, A.; Rausch, W.D. Comparable neuroprotective effect of rapamycin against low and high rotenone concentrations in primary dopaminergic cell culture. J. Appl. Pharm. Sci., 2016, 6(11), 142-146.
[http://dx.doi.org/10.7324/JAPS.2016.601122]
[7]
Sarbishegi, M.; Alhagh Charkhat Gorgich, E.; Khajavi, O. Olive leaves extract improved sperm quality and antioxidant status in the testis of rat exposed to rotenone. Nephrourol. Mon., 2017, 9(3)
[http://dx.doi.org/10.5812/numonthly.47127]
[8]
Liu, J.; Liu, W.; Lu, Y.; Tian, H.; Duan, C.; Lu, L.; Gao, G.; Wu, X.; Wang, X.; Yang, H. Piperlongumine restores the balance of autophagy and apoptosis by increasing BCL2 phosphorylation in rotenone-induced Parkinson disease models. Autophagy, 2018, 14(5), 845-861.
[http://dx.doi.org/10.1080/15548627.2017.1390636 ] [PMID: 29433359]
[9]
Cenini, G.; Lloret, A.; Cascella, R. Oxidative stress in neurodegenerative diseases: From a mitochondrial point of view. Oxid. Med. Cell. Longev., 2019., 20192105607.
[http://dx.doi.org/10.1155/2019/2105607 ] [PMID: 31210837]
[10]
Moustafa, A.A.; Krishna, R.; Frank, M.J.; Eissa, A.M.; Hewedi, D.H. Cognitive correlates of psychosis in patients with Parkinson’s disease. Cogn. Neuropsychiatry, 2014, 19(5), 381-398.
[http://dx.doi.org/10.1080/13546805.2013.877385 ] [PMID: 24446773]
[11]
Ahmad, M.; Saleem, S.; Ahmad, A.S.; Yousuf, S.; Ansari, M.A.; Khan, M.B.; Ishrat, T.; Chaturvedi, R.K.; Agrawal, A.K.; Islam, F. Ginkgo biloba affords dose-dependent protection against 6-hydroxydopamine-induced parkinsonism in rats: Neurobehavioural, neurochemical and immunohistochemical evidences. J. Neurochem., 2005, 93(1), 94-104.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03000.x ] [PMID: 15773909]
[12]
Alagendran, S.; Rajkumar, R.; Vignesh, S.; Satish, S.S.; Puspha, N.; Arul, D. A randomized controlled trial of Ginkgo biloba for prevention of vascular dementia.Statistical Approaches on Multidisciplinary Research; Vignesh, S.; Philip Arokiadoss, A., Eds.; Surragh Publishers: India, 2017, Vol. I, pp. 95-103.
[13]
Zhang, Z.N.; Zhang, J.S.; Xiang, J.; Yu, Z.H.; Zhang, W.; Cai, M.; Li, X.T.; Wu, T.; Li, W.W.; Cai, D.F. Subcutaneous rotenone rat model of Parkinson’s disease: Dose exploration study. Brain Res., 2017, 1655, 104-113.
[http://dx.doi.org/10.1016/j.brainres.2016.11.020 ] [PMID: 27876560]
[14]
Ude, C.; Schubert-Zsilavecz, M.; Wurglics, M. Ginkgo biloba extracts: A review of the pharmacokinetics of the active ingredients. Clin. Pharmacokinet., 2013, 52(9), 727-749.
[http://dx.doi.org/10.1007/s40262-013-0074-5 ] [PMID: 23703577]
[15]
Ahmed, H.H.; Abdel-Rahman, M.; Ali, R.S.; Moniem, A.E.A. Protective effect of Ginkgo biloba extract and pumpkin seed oil against neurotoxicity of rotenone in adult male rats. J. Appl. Sci. Res., 2009, 5(6), 622-635.
[16]
Inden, M.; Kitamura, Y.; Takeuchi, H.; Yanagida, T.; Takata, K.; Kobayashi, Y.; Taniguchi, T.; Yoshimoto, K.; Kaneko, M.; Okuma, Y.; Taira, T.; Ariga, H.; Shimohama, S. Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. J. Neurochem., 2007, 101(6), 1491-1504.
[http://dx.doi.org/10.1111/j.1471-4159.2006.04440.x ] [PMID: 17459145]
[17]
Paxinos, G.; Watson, C. The rat brain stereotaxic coordinates; Academic Press: Sydney, 1982.
[18]
Tappel, A.L.; Zalkin, H. Inhibition of lipid peroxidation in mitochondria by vitamin E. Arch. Biochem. Biophys., 1959, 80(2), 333-336.
[http://dx.doi.org/10.1016/0003-9861(59)90259-0]
[19]
Jollow, D.J.; Mitchell, J.R.; Zampaglione, N.; Gillette, J.R. Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacology, 1974, 11(3), 151-169.
[http://dx.doi.org/10.1159/000136485 ] [PMID: 4831804]
[20]
Sedlak, J.; Lindsay, R.H. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal. Biochem., 1968, 25(1), 192-205.
[http://dx.doi.org/10.1016/0003-2697(68)90092-4 ] [PMID: 4973948]
[21]
Misra, H.P.; Fridovich, I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem., 1972, 247(10), 3170-3175.
[PMID: 4623845]
[22]
Chiu, D. T. Y.; Stults, F. H.; Tappel, A. L. Purification and properties of rat lung soluble glutathione peroxidase. BBA - Enzymol., 1976, 445(3), 558-566.
[http://dx.doi.org/10.1016/0005-2744(76)90110-8]
[23]
Ellman, G.L.; Courtney, K.D.; Andres, V., Jr; Feather-Stone, R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol., 1961, 7(2), 88-95.
[http://dx.doi.org/10.1016/0006-2952(61)90145-9 ] [PMID: 13726518]
[24]
Lillie, R.D. Histopathologic Technic and Practical Histochemistry, 3rd ed; McGraw Hill Book Co.: New York, 1965.
[25]
Abdel-Salam, O.M.E.; Youness, E.R.; Khadrawy, Y.A.; Mohammed, N.A.; Abdel-Rahman, R.F.; Omara, E.A.; Sleem, A.A. The effect of cannabis on oxidative stress and neurodegeneration induced by intrastriatal rotenone injection in rats. Comp. Clin. Pathol., 2015, 24(2), 359-378.
[http://dx.doi.org/10.1007/s00580-014-1907-9]
[26]
Essawy, A.E.; Abdou, H.M.; Ibrahim, H.M.; Bouthahab, N.M. Soybean isoflavone ameliorates cognitive impairment, neuroinflammation, and amyloid β accumulation in a rat model of Alzheimer’s disease. Environ. Sci. Pollut. Res. Int., 2019, 26(25), 26060-26070.
[http://dx.doi.org/10.1007/s11356-019-05862-z ] [PMID: 31278647]
[27]
Tešanović, K.; Pejin, B.; Šibul, F.; Matavulj, M.; Rašeta, M.; Janjušević, L.; Karaman, M. A comparative overview of antioxidative properties and phenolic profiles of different fungal origins: fruiting bodies and submerged cultures of Coprinus comatus and Coprinellus truncorum. J. Food Sci. Technol., 2017, 54(2), 430-438.
[http://dx.doi.org/10.1007/s13197-016-2479-2 ] [PMID: 28242942]
[28]
Jeon, W.K.; Kim, M-S.; Lee, J.; Han, J-S. Protective effect of Ginkgo biloba extract (EGB761) against chronic cerebral hypoperfusion by modulating neuroinflammation and the cholinergic system. Alzheimers Dement., 2016, 12(7), 621-P622.
[http://dx.doi.org/10.1016/j.jalz.2016.06.1240]
[29]
Balakrishnan; Tamilselvam, K.; Sulthana, A.; Mohankumar, T.; Manimaran, D.; Elangovan, N. Isolongifolene attenuates oxidative stress and behavioral impairment in rotenone-induced rat model of Parkinson’s disease. Int. J. Nutr. Pharmacol. Neurol. Dis., 2018, 8(2), 53.
[http://dx.doi.org/10.4103/IJNPND.IJNPND_3_18]
[30]
Nandipati, S.; Litvan, I. Environmental exposures and Parkinson’s disease. Int. J. Environ. Res. Public Health, 2016, 13(9), E881.
[http://dx.doi.org/10.3390/ijerph13090881 ] [PMID: 27598189]
[31]
Gopi, M.; Arambakkam Janardhanam, V. Asiaticoside: Attenuation of rotenone induced oxidative burden in a rat model of hemiparkinsonism by maintaining the phosphoinositide-mediated synaptic integrity. Pharmacol. Biochem. Behav., 2017, 155, 1-15.
[http://dx.doi.org/10.1016/j.pbb.2017.02.005 ] [PMID: 28238857]
[32]
Anusha, C.; Sumathi, T.; Joseph, L.D. Protective role of apigenin on rotenone induced rat model of Parkinson’s disease: Suppression of neuroinflammation and oxidative stress mediated apoptosis. Chem. Biol. Interact., 2017, 269, 67-79.
[http://dx.doi.org/10.1016/j.cbi.2017.03.016 ] [PMID: 28389404]
[33]
Zaitone, S.A.; Abo-Elmatty, D.M.; Shaalan, A.A. Acetyl-L-carnitine and α-lipoic acid affect rotenone-induced damage in nigral dopaminergic neurons of rat brain, implication for Parkinson’s disease therapy. Pharmacol. Biochem. Behav., 2012, 100(3), 347-360.
[http://dx.doi.org/10.1016/j.pbb.2011.09.002 ] [PMID: 21958946]
[34]
Venkatesh Gobi, V.; Rajasankar, S.; Ramkumar, M.; Dhanalakshmi, C.; Manivasagam, T.; Justin Thenmozhi, A.; Essa, M.M.; Chidambaram, R.; Kalandar, A. Agaricus blazei extract abrogates rotenone-induced dopamine depletion and motor deficits by its anti-oxidative and anti-inflammatory properties in Parkinsonic mice. Nutr. Neurosci., 2018, 21(9), 657-666.
[http://dx.doi.org/10.1080/1028415X.2017.1337290 ] [PMID: 28628424]
[35]
Xiong, Z.K.; Lang, J.; Xu, G.; Li, H.Y.; Zhang, Y.; Wang, L.; Su, Y.; Sun, A.J. Excessive levels of nitric oxide in rat model of Parkinson’s disease induced by rotenone. Exp. Ther. Med., 2015, 9(2), 553-558.
[http://dx.doi.org/10.3892/etm.2014.2099 ] [PMID: 25574233]
[36]
Ismail, A.F.M.; El-Sonbaty, S.M. Fermentation enhances Ginkgo biloba protective role on gamma-irradiation induced neuroinflammatory gene expression and stress hormones in rat brain. J. Photochem. Photobiol. B, 2016, 158, 154-163.
[http://dx.doi.org/10.1016/j.jphotobiol.2016.02.039 ] [PMID: 26974576]
[37]
Wahby, M.M.; Abdallah, Z.M.; Abdou, H.M.; Yousef, M.I.; Newairy, A-S.A. Mitigating potential of Ginkgo biloba extract and melatonin against hepatic and nephrotoxicity induced by bisphenol A in male rats. Egypt. J. Basic Appl. Sci., 2017, 4(4), 350-357.
[http://dx.doi.org/10.1016/j.ejbas.2017.04.004]
[38]
Wei, T.; Ni, Y.; Hou, J.; Chen, C.; Zhao, B.; Xin, W. Hydrogen peroxide-induced oxidative damage and apoptosis in cerebellar granule cells: Protection by Ginkgo biloba extract. Pharmacol. Res., 2000, 41(4), 427-433.
[http://dx.doi.org/10.1006/phrs.1999.0604 ] [PMID: 10704267]
[39]
Qiu, J.; Chen, X.; Netrusov, A.I.; Zhou, Q.; Guo, D.; Liu, X.; He, H.; Xin, X.; Wang, Y.; Chen, L. Screening and identifying antioxidative components in Ginkgo biloba pollen by DPPH-HPLC-PAD coupled with HPLC-ESI-MS2. PLoS One, 2017, 12(1), e0170141.
[http://dx.doi.org/10.1371/journal.pone.0170141 ] [PMID: 28095510]
[40]
Batool, Z.; Sadir, S.; Liaquat, L.; Tabassum, S.; Madiha, S.; Rafiq, S.; Tariq, S.; Batool, T.S.; Saleem, S.; Naqvi, F.; Perveen, T.; Haider, S. Repeated administration of almonds increases brain acetylcholine levels and enhances memory function in healthy rats while attenuates memory deficits in animal model of amnesia. Brain Res. Bull., 2016, 120, 63-74.
[http://dx.doi.org/10.1016/j.brainresbull.2015.11.001 ] [PMID: 26548495]
[41]
Zhang, X.J.; Greenberg, D.S. Acetylcholinesterase involvement in apoptosis. Front. Mol. Neurosci., 2012, 5, 40.
[http://dx.doi.org/10.3389/fnmol.2012.00040 ] [PMID: 22514517]
[42]
Denny Joseph, K.M. Muralidhara. Combined oral supplementation of fish oil and quercetin enhances neuroprotection in a chronic rotenone rat model: Relevance to Parkinson’s disease. Neurochem. Res., 2015, 40(5), 894-905.
[http://dx.doi.org/10.1007/s11064-015-1542-0 ] [PMID: 25687767]
[43]
Denny Joseph, K.M. Muralidhara, Enhanced neuroprotective effect of fish oil in combination with quercetin against 3-nitropropionic acid induced oxidative stress in rat brain. Prog. Neuropsychopharmacol. Biol. Psychiat, 2013, 40(1), 83-92.
[http://dx.doi.org/10.1016/j.pnpbp.2012.08.018 ] [PMID: 22960609]
[44]
Abd-Elhady, R.M.; Elsheikh, A.M.; Khalifa, A.E. Anti-amnestic properties of Ginkgo biloba extract on impaired memory function induced by aluminum in rats. Int. J. Dev. Neurosci., 2013, 31(7), 598-607.
[http://dx.doi.org/10.1016/j.ijdevneu.2013.07.006 ] [PMID: 23933390]
[45]
Tong, Q.; Wu, L.; Gao, Q.; Ou, Z.; Zhu, D.; Zhang, Y. PPARβ/δ Agonist provides neuroprotection by suppression of IRE1α-caspase-12-mediated endoplasmic reticulum stress pathway in the rotenone rat model of Parkinson’s disease. Mol. Neurobiol., 2016, 53(6), 3822-3831.
[http://dx.doi.org/10.1007/s12035-015-9309-9 ] [PMID: 26160761]
[46]
Ameen, A.M.; Elkazaz, A.Y.; Mohammad, H.M.F.; Barakat, B.M. Anti-inflammatory and neuroprotective activity of boswellic acids in rotenone parkinsonian rats. Can. J. Physiol. Pharmacol., 2017, 95(7), 819-829.
[http://dx.doi.org/10.1139/cjpp-2016-0158 ] [PMID: 28249117]
[47]
Chompoopong, S.; Jarungjitaree, S.; Punbanlaem, T.; Rungruang, T.; Chongthammakun, S.; Kettawan, A.; Taechowisan, T. Neuroprotective effects of germinated brown rice in rotenone-induced parkinson’s-like disease rats. Neuromolecular Med., 2016, 18(3), 334-346.
[http://dx.doi.org/10.1007/s12017-016-8427-5 ] [PMID: 27430236]
[48]
Darbinyan, L.V.; Hambardzumyan, L.E.; Simonyan, K.V.; Chavushyan, V.A.; Manukyan, L.P.; Sarkisian, V.H. Rotenone impairs hippocampal neuronal activity in a rat model of Parkinson’s disease. Pathophysiology, 2017, 24(1), 23-30.
[http://dx.doi.org/10.1016/j.pathophys.2017.01.001 ] [PMID: 28126254]
[49]
Abdelkader, N.F.; Arafa, N.M.; Attia, A.S.; Ain-Shoka, A.A.; Abdallah, D.M. Pyrrolidinedithio carbamate ameliorates rotenone-induced Parkinson’s disease in rats. Bull. Fac. Pharm. Cairo Univ., 2017, 55, 107-113.
[http://dx.doi.org/10.1016/j.bfopcu.2016.11.003]
[50]
Thakur, P.; Nehru, B. Anti-inflammatory properties rather than anti-oxidant capability is the major mechanism of neuroprotection by sodium salicylate in a chronic rotenone model of Parkinson’s disease. Neuroscience, 2013, 231, 420-431.
[http://dx.doi.org/10.1016/j.neuroscience.2012.11.006 ] [PMID: 23159314]
[51]
Omar, S.H. Ginkgolides and neuroprotective effects. In: Natural Products; Phytochemistry, Botany and Metabolism of Alkaloids, Phenolics and Terpenes, 2013; pp. 3697-3741.
[http://dx.doi.org/10.1007/978-3-642-22144-6_146]
[52]
Abad Martínez, M.J.; Del Olmo, L.M.B.; Benito, P.B. Interactions between natural health products and antiretroviral drugs. In: Studies in Natural Products Chemistry; , 2014; 43, pp. 197-221.
[http://dx.doi.org/10.1016/B978-0-444-63430-6.00006-0]
[53]
Javed, H.; Azimullah, S.; Haque, M.E.; Ojha, S.K. Cannabinoid type 2 (CB2) receptors activation protects against oxidative stress and neuroinflammation associated dopaminergic neurodegeneration in rotenone model of Parkinson’s disease. Front. Neurosci., 2016, 10, 321.
[http://dx.doi.org/10.3389/fnins.2016.00321 ] [PMID: 27531971]
[54]
Niranjan, R. The role of inflammatory and oxidative stress mechanisms in the pathogenesis of Parkinson’s disease: Focus on astrocytes. Mol. Neurobiol., 2014, 49(1), 28-38.
[http://dx.doi.org/10.1007/s12035-013-8483-x ] [PMID: 23783559]
[55]
Lee, C.Y.; Yang, J.J.; Lee, S.S.; Chen, C.J.; Huang, Y.C.; Huang, K.H.; Kuan, Y.H. Protective effect of Ginkgo biloba leaves extract, EGb761, on endotoxin-induced acute lung injury via a JNK- and Akt-dependent NFκB pathway. J. Agric. Food Chem., 2014, 62(27), 6337-6344.
[http://dx.doi.org/10.1021/jf501913b ] [PMID: 24956234]
[56]
Abd-Eldayem, A.; Farghaly, H.M.; Abdel-Zaher, A. The nephroprotective effects of Ginkgo biloba extract (EGb761) against L-N G -nitroarginine methyl ester-induced hypertension in rats: role of oxidative stress and inflammatory markers. J. Curr. Med. Res. Pract., 2016, 1(3), 79.
[http://dx.doi.org/10.4103/2357-0121.199358]
[57]
Li, Z.Y.; Chung, Y.H.; Shin, E.J.; Dang, D.K.; Jeong, J.H.; Ko, S.K.; Nah, S.Y.; Baik, T.G.; Jhoo, J.H.; Ong, W.Y.; Nabeshima, T.; Kim, H.C. YY-1224, a terpene trilactone-strengthened Ginkgo biloba, attenuates neurodegenerative changes induced by β-amyloid (1-42) or double transgenic overexpression of APP and PS1 via inhibition of cyclooxygenase-2. J. Neuroinflammation, 2017, 14(1), 94.
[http://dx.doi.org/10.1186/s12974-017-0866-x ] [PMID: 28449688]
[58]
Yang, Y.; Li, Y.; Wang, J.; Sun, K.; Tao, W.; Wang, Z.; Xiao, W.; Pan, Y.; Zhang, S.; Wang, Y. Systematic investigation of Ginkgo biloba leaves for treating cardio-cerebrovascular diseases in an animal model. ACS Chem. Biol., 2017, 12(5), 1363-1372.
[http://dx.doi.org/10.1021/acschembio.6b00762 ] [PMID: 28333443]
[59]
Zhao, H.; Han, H.; Hou, H.; Chen, J.; Lang, X.; Yue, Y.; Gao, H.; Kang, J.; Zhu, Y.; Dun, Z. Effect of Ginkgo biloba extract on splenic immune function of chronic ulcerative colitis in mice. Int. J. Clin. Exp. Med., 2017, 10(5), 7611-7623.
[60]
Khadrawy, Y.A.; Salem, A.M.; El-Shamy, K.A.; Ahmed, E.K.; Fadl, N.N.; Hosny, E.N. neuroprotective and therapeutic effect of caffeine on the rat model of Parkinson’s disease induced by rotenone. J. Diet. Suppl., 2017, 14(5), 553-572.
[http://dx.doi.org/10.1080/19390211.2016.1275916 ] [PMID: 28301304]
[61]
Abdou, H.M.; Yousef, M.I.; El Mekkawy, D.A.; Al-Shami, A.S. Prophylactic neuroprotective efficiency of co-administration of Ginkgo biloba and Trifolium pretense against sodium arsenite-induced neurotoxicity and dementia in different regions of brain and spinal cord of rats. Food Chem. Toxicol., 2016, 94, 112-127.
[http://dx.doi.org/10.1016/j.fct.2016.05.015 ] [PMID: 27234133]
[62]
Cannon, J.R.; Tapias, V.; Na, H.M.; Honick, A.S.; Drolet, R.E.; Greenamyre, J.T. A highly reproducible rotenone model of Parkinson’s disease. Neurobiol. Dis., 2009, 34(2), 279-290.
[http://dx.doi.org/10.1016/j.nbd.2009.01.016 ] [PMID: 19385059]
[63]
Kumar, P.; Pradhan, K.; Karunya, R.; Ambasta, R.K.; Querfurth, H.W. Cross-functional E3 ligases Parkin and C-terminus Hsp70-interacting protein in neurodegenerative disorders. J. Neurochem., 2012, 120(3), 350-370.
[http://dx.doi.org/10.1111/j.1471-4159.2011.07588.x ] [PMID: 22098618]
[64]
Sonia Angeline, M.; Chaterjee, P.; Anand, K.; Ambasta, R.K.; Kumar, P. Rotenone-induced parkinsonism elicits behavioral impairments and differential expression of parkin, heat shock proteins and caspases in the rat. Neuroscience, 2012, 220, 291-301.
[http://dx.doi.org/10.1016/j.neuroscience.2012.06.021 ] [PMID: 22710069]
[65]
Rojas, P.; Serrano-García, N.; Mares-Sámano, J.J.; Medina-Campos, O.N.; Pedraza-Chaverri, J.; Ögren, S.O. EGb761 protects against nigrostriatal dopaminergic neurotoxicity in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinsonism in mice: Role of oxidative stress. Eur. J. Neurosci., 2008, 28(1), 41-50.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06314.x ] [PMID: 18662333]

Rights & Permissions Print Cite
Article Metrics
38
Wayfinder Image
Open Access Journals Promotions
© 2024 Bentham Science Publishers | Privacy Policy