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Current Bioactive Compounds

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ISSN (Print): 1573-4072
ISSN (Online): 1875-6646

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Research Article

Gene Expression, Oxidative Stress, and Neurotransmitters in Rotenone-induced Parkinson’s Disease in Rats: Role of Naringin from Citrus aurantium via Blocking Adenosine A2A Receptor

Author(s): Yomna Rashad Ahmed, Asmaa Fathy Aboul Naser, Marwa Mahmoud Elbatanony, Amal Mohamed El-Feky, Wagdy Khalil Bassaly Khalil and Manal Abdel-Aziz Hamed*

Volume 20, Issue 5, 2024

Published on: 10 October, 2023

Article ID: e101023221984 Pages: 16

DOI: 10.2174/0115734072268296231002060839

Price: $65

Abstract

Background: Lack of control in voluntary movements, resting tremor, postural instability, and stiffness are the hallmarks of Parkinson's disease (PD).

Objective: The current work's objective is to assess naringin isolated from Citrus aurantium L. peels as an anti-parkinsonism agent in rats.

Methods: The HPLC and LC-ESI-MS analysis of Citrus aurantium L. peels methanol extract was done. The behavioral, biochemical, genetic, and histopathological analysis were evaluated in parkinsonism rats.

Results: Fourteen phenolics and nine flavonoids were found in the extract, according to the HPLC analysis, while LC-ESI-MS analysis revealed the presence of twenty-six flavonoids. The dominant flavonoid subclasses were 4 aglycones, 11 monoglycosides, 5 diglycosides, and 6 polymethoxy flavonoids, beside 4 coumarines, 4 alkaloids and a limonin triterpene. Adenosine A2A receptor (A2AR) gene expression, malondialdehyde (MDA), interleukin-6 (IL-6), caspase-3 (Cas-3) and DNA fragmentation levels significantly increased in rotenone-induced rats. Dopamine (DA), norepinephrine (NE), serotonin (5-HT), reduced glutathione (GSH), succinate, and lactate dehydrogenase (SDH &LDH) levels all significantly decreased. Treatment with naringin and A2AR antagonists enhanced the animals’ behavior and improved all the selected parameters. The brain hippocampal features confirmed our results.

Conclusion: Naringin could be considered a nutraceutical agent by attenuating the neurodegeneration associated with PD via blocking adenosine A2AR.

Graphical Abstract

[1]
Rajabally, Y.A; Martey, J Neuropathy in Parkinson disease: Prevalence and determinants. Neurology, 2011, 77(22), 1947-1950.
[http://dx.doi.org/10.1212/WNL.0b013e31823a0ee4] [PMID: 22049200]
[2]
Taylor, T.N; Greene, J.G; Miller, G.W Behavioral phenotyping of mouse models of Parkinson’s disease. Behav. Brain Res., 2010, 211(1), 1-10.
[http://dx.doi.org/10.1016/j.bbr.2010.03.004] [PMID: 20211655]
[3]
Betarbet, R; Sherer, T.B; Greenamyre, J.T Animal models of Parkinson’s disease. BioEssays, 2002, 24(4), 308-318.
[http://dx.doi.org/10.1002/bies.10067] [PMID: 11948617]
[4]
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]
[5]
Abu-Elfotuh, K; Hamdan, A.M.E; Mohammed, A.A; Atwa, A.M; Kozman, M.R; Ibrahim, A.M; Motawea, S.M; Selim, H.M.R.M; Tohamy, S.T.K; Nour El-Din, M.N; Zaghlool, S.S; Gowifel, A.M.H; Awny, M.M Neuroprotective effects of some nutraceuticals against manganese-induced Parkinson’s disease in rats: Possible modulatory effects on TLR4/NLRP3/NF-kB, GSK-3 β, Nrf2/HO-1, and apoptotic pathways. Pharmaceuticals (Basel), 2022, 15(12), 1554.
[http://dx.doi.org/10.3390/ph15121554] [PMID: 36559006]
[6]
Dexter, D.T; Jenner, P Parkinson disease: from pathology to molecular disease mechanisms. Free Radic. Biol. Med., 2013, 62, 132-144.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.01.018] [PMID: 23380027]
[7]
Pardo-Moreno, T; García-Morales, V; Suleiman-Martos, S; Rivas-Domínguez, A; Mohamed-Mohamed, H; Ramos-Rodríguez, J.J; Melguizo-Rodríguez, L; González-Acedo, A Current treatments and new, tentative therapies for Parkinson’s disease. Pharmaceutics, 2023, 15(3), 770.
[http://dx.doi.org/10.3390/pharmaceutics15030770] [PMID: 36986631]
[8]
Mamais, A; Kaganovich, A; Harvey, K Convergence of signalling pathways in innate immune responses and genetic forms of Parkinson’s disease. Neurobiol. Dis., 2022, 169, 105721.
[http://dx.doi.org/10.1016/j.nbd.2022.105721] [PMID: 35405260]
[9]
Sherer, T.B; Betarbet, R; Testa, C.M; Seo, B.B; Richardson, J.R; Kim, J.H; Miller, G.W; Yagi, T; Matsuno-Yagi, A; Greenamyre, J.T Mechanism of toxicity in rotenone models of Parkinson’s disease. J. Neurosci., 2003, 23(34), 10756-10764.
[http://dx.doi.org/10.1523/JNEUROSCI.23-34-10756.2003] [PMID: 14645467]
[10]
Gao, H.M; Liu, B; Hong, J.S Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci., 2003, 23(15), 6181-6187.
[http://dx.doi.org/10.1523/JNEUROSCI.23-15-06181.2003] [PMID: 12867501]
[11]
Freestone, P.S; Chung, K.K.H; Guatteo, E; Mercuri, N.B; Nicholson, L.F.B; Lipski, J Acute action of rotenone on nigral dopaminergic neurons - involvement of reactive oxygen species and disruption of Ca2+ homeostasis. Eur. J. Neurosci., 2009, 30(10), 1849-1859.
[http://dx.doi.org/10.1111/j.1460-9568.2009.06990.x] [PMID: 19912331]
[12]
Ren, Y; Liu, W; Jiang, H; Jiang, Q; Feng, J Selective vulnerability of dopaminergic neurons to microtubule depolymerization. J. Biol. Chem., 2005, 280(40), 34105-34112.
[http://dx.doi.org/10.1074/jbc.M503483200] [PMID: 16091364]
[13]
Mohamed, A.S; Abdel-Fattah, D.S; Abdel-Aleem, G.A; El-Sheikh, T.F; Elbatch, M.M Biochemical study of the effect of mesenchymal stem cells-derived exosome versus l-Dopa in experimentally induced Parkinson’s disease in rats. Mol. Cell. Biochem., 2023.
[http://dx.doi.org/10.1007/s11010-023-04700-8] [PMID: 36966421]
[14]
Priyanga, S.K VijayaIakshmi, K.; Selvaraj, R. Behavioural studies of Wistar rates in rotenone induce model of Parkinson’s disease. Int. J. Pharm. Pharm. Sci., 2017, 9, 159-164.
[http://dx.doi.org/10.22159/ijpps.2017v9i11.21465]
[15]
Dorszewska, J; Prendecki, M; Lianeri, M; Kozubski, W Molecular effects of L-dopa therapy in Parkinson’s disease. Curr. Genomics, 2014, 15(1), 11-17.
[http://dx.doi.org/10.2174/1389202914666131210213042] [PMID: 24653659]
[16]
Fathalla, A.M; Soliman, A.M; Ali, M.H; Moustafa, A.A Adenosine A2A receptor blockade prevents rotenone-induced motor impairment in a rat model of Parkinsonism. Front. Behav. Neurosci., 2016, 2016, 1-5.
[17]
Aboul Naser, A; Younis, E; El-Feky, A; Elbatanony, M; Hamed, M Management of Citrus sinensis peels for protection and treatment against gastric ulcer induced by ethanol in rats. Biomarkers, 2020, 25(4), 349-359.
[http://dx.doi.org/10.1080/1354750X.2020.1759693] [PMID: 32319821]
[18]
Rafiq, S; Kaul, R; Sofi, S.A; Bashir, N; Nazir, F; Ahmad Nayik, G Citrus peel as a source of functional ingredient: A review. J. Saudi Soc. Agric. Sci., 2018, 17(4), 351-358.
[http://dx.doi.org/10.1016/j.jssas.2016.07.006]
[19]
Liu, S; Lou, Y; Li, Y; Zhang, J; Li, P; Yang, B; Gu, Q Review of phytochemical and nutritional characteristics and food applications of Citrus L. fruits. Front. Nutr., 2022, 9, 968604.
[http://dx.doi.org/10.3389/fnut.2022.968604] [PMID: 35923210]
[20]
Emran, T.B; Islam, F; Nath, N; Sutradhar, H; Das, R; Mitra, S; Alshahrani, M.M; Alhasaniah, A.H; Sharma, R Naringin and naringenin polyphenols in neurological diseases: Understandings from a therapeutic viewpoint. Life (Basel), 2022, 13(1), 99.
[http://dx.doi.org/10.3390/life13010099] [PMID: 36676048]
[21]
Hamed, M; Aboul Naser, A; Elbatanony, M; El-Feky, A; Matloub, A; El-Rigal, N; Khalil, W Therapeutic potential of Citrus sinensis peels against rotenone induced Parkinsonism in rats. Curr. Bioact. Compd., 2021, 17(6), e010621186105.
[http://dx.doi.org/10.2174/1573407216999200918182514]
[22]
Suntar, I; Khan, H; Patel, S; Celano, R; Rastrelli, L An overview on Citrus aurantium L.: Its functions as food ingredient and therapeutic agent. Oxid. Med. Cell. Longev., 2018, 2018, 1-12.
[http://dx.doi.org/10.1155/2018/7864269] [PMID: 29854097]
[23]
Xing, H; Zhang, K; Zhang, R; Shi, H; Bi, K; Chen, X Antidepressant-like effect of the water extract of the fixed combination of Gardenia jasminoides, Citrus aurantium and Magnolia officinalis in a rat model of chronic unpredictable mild stress. Phytomedicine, 2015, 22(13), 1178-1185.
[http://dx.doi.org/10.1016/j.phymed.2015.09.004] [PMID: 26598917]
[24]
Kim, J.A; Park, H.S; Kang, S.R; Park, K.I; Lee, D.H; Nagappan, A; Shin, S.C; Lee, W.S; Kim, E.H; Kim, G.S Suppressive effect of flavonoids from Korean Citrus aurantium L. on the expression of inflammatory mediators in L6 skeletal muscle cells. Phytother. Res., 2012, 26(12), 1904-1912.
[http://dx.doi.org/10.1002/ptr.4666] [PMID: 22431150]
[25]
Nabavi, S.F; Khan, H; D’onofrio, G; Šamec, D; Shirooie, S; Dehpour, A.R; Argüelles, S; Habtemariam, S; Sobarzo-Sanchez, E Apigenin as neuroprotective agent: Of mice and men. Pharmacol. Res., 2018, 128, 359-365.
[http://dx.doi.org/10.1016/j.phrs.2017.10.008] [PMID: 29055745]
[26]
Borai, I.H; Ezz, M.K; Rizk, M.Z; Aly, H.F; El-Sherbiny, M; Matloub, A.A; Fouad, G.I Therapeutic impact of grape leaves polyphenols on certain biochemical and neurological markers in AlCl3-induced Alzheimer’s disease. Biomed. Pharmacother., 2017, 93, 837-851.
[http://dx.doi.org/10.1016/j.biopha.2017.07.038] [PMID: 28715867]
[27]
Žilić, S; Serpen, A; Akıllıoğlu, G; Janković, M; Gökmen, V Distributions of phenolic compounds, yellow pigments and oxidative enzymes in wheat grains and their relation to antioxidant capacity of bran and debranned flour. J. Cereal Sci., 2012, 56(3), 652-658.
[http://dx.doi.org/10.1016/j.jcs.2012.07.014]
[28]
El-Feky, A.M; Elbatanony, M.M; Aboul Naser, A.F; Kutkat, O.M; El-Sayed, A.B; Hamed, M.A Phytoconstituents and in vitro antioxidant, antiviral, antihyperlipidemic and anticancer effects of Chlorella vulgaris microalga in normal and stress conditions. Pharma Chem., 2020, 12, 9-20.
[29]
Sudto, K; Pornpakakul, S; Wanichwecharungruang, S An efficient method for the large scale isolation of naringin from pomelo (Citrus grandis) peel. Int. J. Food Sci. Technol., 2009, 44(9), 1737-1742.
[http://dx.doi.org/10.1111/j.1365-2621.2009.01989.x]
[30]
Sharma, P; Pandey, P; Gupta, R Roshan1, S.; Garg, A.; Shulka, A.; Pasi, A. Isolation and characterization of hesperidin from orange peel. J. Pharm. Res., 2013, 3, 3892-3897.
[31]
Gocan, S; Cimpan, G Review of the analysis of medicinal plants by TLC: modern approaches. J. Liq. Chromatogr. Relat. Technol., 2004, 27(7-9), 1377-1411.
[http://dx.doi.org/10.1081/JLC-120030607]
[32]
El Shebiney, S.A; El-Denshary, E.S; Abdel-Salam, O.M.E; Salem, N.A; El-Khyat, Z.A; El Shaffie, N Cannabis resin extract in Parkinson’s disease: Behavioral, neurochemical, and histological evaluation. Cell Biol Res Ther, 2014, 3, 1.
[33]
Alam, M; Schmidt, W.J l-DOPA reverses the hypokinetic behaviour and rigidity in rotenone-treated rats. Behav. Brain Res., 2004, 153(2), 439-446.
[http://dx.doi.org/10.1016/j.bbr.2003.12.021] [PMID: 15265640]
[34]
Perez-Pardo, P; Broersen, L.M; Kliest, T; van Wijk, N; Attali, A; Garssen, J; Kraneveld, A.D Additive effects of levodopa and a neurorestorative diet in a mouse model of Parkinson’s disease. Front. Aging Neurosci., 2018, 10, 237.
[http://dx.doi.org/10.3389/fnagi.2018.00237] [PMID: 30127735]
[35]
Sanberg, P; Martinez, R; Shytle, R; Cahill, D The catalepsy test: Is a standardized method possible? Motor Activity and Movement Disorders; Humana Press: NY, USA, 1996.
[http://dx.doi.org/10.1007/978-1-59259-469-6]
[36]
Buege, J.A; Aust, S.D Microsomal lipid peroxidation. Methods Enzymol., 1978, 52, 302-310.
[http://dx.doi.org/10.1016/S0076-6879(78)52032-6] [PMID: 672633]
[37]
Moron, M; Depierre, J; Mannervik, B Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim. Biophys. Acta, Gen. Subj., 1979, 582(1), 67-78.
[http://dx.doi.org/10.1016/0304-4165(79)90289-7] [PMID: 760819]
[38]
Nishikimi, M; Appaji Rao, N; Yagi, K The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem. Biophys. Res. Commun., 1972, 46(2), 849-854.
[http://dx.doi.org/10.1016/S0006-291X(72)80218-3] [PMID: 4400444]
[39]
Wang, Y; Yang, F; Zhang, H-X; Zi, X-Y; Pan, X-H; Chen, F; Luo, W-D; Li, J-X; Zhu, H-Y; Hu, Y-P Cuprous oxide nanoparticles inhibit the growth and metastasis of melanoma by targeting mitochondria. Cell Death Dis., 2013, 4(8), e783.
[http://dx.doi.org/10.1038/cddis.2013.314] [PMID: 23990023]
[40]
Liu, Y.E; Tong, C.C; Zhang, Y.B; Cong, P.F; Shi, X.Y; Liu, Y; Shi, L; Tong, Z; Jin, H.X; Hou, M.X Chitosan oligosaccharide ameliorates acute lung injury induced by blast injury through the DDAH1/ADMA pathway. PLoS One, 2018, 13(2), e0192135.
[http://dx.doi.org/10.1371/journal.pone.0192135] [PMID: 29415054]
[41]
Rice, M.E; Shelton, E Comparison of the reduction of two tetrazolium salts with succinoxidase activity of tissue homogenates. J. Natl. Cancer Inst., 1957, 18(1), 117-125.
[PMID: 13398820]
[42]
Babson, A.L; Babson, S.R Kinetic colorimetric measurement of serum lactate dehydrogenase activity. Clin. Chem., 1973, 19(7), 766-769.
[http://dx.doi.org/10.1093/clinchem/19.7.766] [PMID: 4351362]
[43]
Bradford, M.M A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 1976, 72(1-2), 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[44]
Zagrodzka, J; Romaniuk, A; Wieczorek, M; Boguszewski, P Bicuculline administration into ventromedial hypothalamus: effects on fear and regional brain monoamines and GABA concentrations in rats. Acta Neurobiol. Exp. (Warsz.), 2000, 60(3), 333-343.
[PMID: 11016075]
[45]
Khalil, W; Booles, H Protective role of selenium against over-expression of cancer-related apoptotic genes induced by o-cresol in rats. Arh. Hig. Rada Toksikol., 2011, 62(2), 121-129.
[http://dx.doi.org/10.2478/10004-1254-62-2011-2074] [PMID: 21705299]
[46]
Linjawi, S.A.A; Khalil, W.K.B; Salem, L.M Detoxified Jatropha curcas kernel meal impact against benzene-induce genetic toxicity in male rats. Int. J. Pharm., 2014, 4, 57-66.
[47]
Lu, T; Xu, Y; Mericle, M.T; Mellgren, R.L Participation of the conventional calpains in apoptosis. Biochim. Biophys. Acta Mol. Cell Res., 2002, 1590(1-3), 16-26.
[http://dx.doi.org/10.1016/S0167-4889(02)00193-3] [PMID: 12063165]
[48]
Bancroft, J; Stevens, A Theory and Practice of Histological Techniques, 4th ed; Churchil Livingstone: Edinburgh, Scotland, 1996.
[49]
Jabri karoui, I.; Marzouk, B. Characterization of bioactive compounds in Tunisian bitter orange (Citrus aurantium L.) peel and juice and determination of their antioxidant activities. BioMed Res. Int., 2013, 2013, 1-12.
[http://dx.doi.org/10.1155/2013/345415] [PMID: 23841062]
[50]
Hamdan, D.I; Mahmoud, M.F; Wink, M; El-Shazly, A.M Effect of hesperidin and neohesperidin from bittersweet orange (Citrus aurantium var. bigaradia) peel on indomethacin-induced peptic ulcers in rats. Environ. Toxicol. Pharmacol., 2014, 37(3), 907-915.
[http://dx.doi.org/10.1016/j.etap.2014.03.006] [PMID: 24691249]
[51]
Pellati, F; Benvenuti, S; Melegari, M; Firenzuoli, F Determination of adrenergic agonists from extracts and herbal products of Citrus aurantium L. var. amara by LC. J. Pharm. Biomed. Anal., 2002, 29(6), 1113-1119.
[http://dx.doi.org/10.1016/S0731-7085(02)00153-X] [PMID: 12110397]
[52]
Pellati, F; Benvenuti, S; Melegari, M High-performance liquid chromatography methods for the analysis of adrenergic amines and flavanones in Citrus aurantium L. var.amara. Phytochem. Anal., 2004, 15(4), 220-225.
[http://dx.doi.org/10.1002/pca.771] [PMID: 15311840]
[53]
Yu, L; Chen, M; Liu, J; Huang, X; He, W; Qing, Z; Zeng, J Detection and identification of bioactive ingredients from Citrus aurantium L. var. amara using HPLC-Q-TOF-MS combined with a screening method. Molecules, 2020, 25(2), 357.
[http://dx.doi.org/10.3390/molecules25020357] [PMID: 31952271]
[54]
Ana, C.C; Jesús, P.V; Hugo, E.A; Teresa, A.T; Ulises, G.C; Neith, P Antioxidant capacity and UPLC–PDA ESI–MS polyphenolic profile of Citrus aurantium extracts obtained by ultrasound assisted extraction. J. Food Sci. Technol., 2018, 55(12), 5106-5114.
[http://dx.doi.org/10.1007/s13197-018-3451-0] [PMID: 30483007]
[55]
Blanck, H.M; Serdula, M.K; Gillespie, C; Galuska, D.A; Sharpe, P.A; Conway, J.M; Khan, L.K; Ainsworth, B.E Use of nonprescription dietary supplements for weight loss is common among Americans. J. Am. Diet. Assoc., 2007, 107(3), 441-447.
[http://dx.doi.org/10.1016/j.jada.2006.12.009] [PMID: 17324663]
[56]
Peixoto, J.S; Comar, J.F; Moreira, C.T; Soares, A.A; de Oliveira, A.L; Bracht, A; Peralta, R.M Effects of Citrus aurantium (bitter orange) fruit extracts and p-synephrine on metabolic fluxes in the rat liver. Molecules, 2012, 17(5), 5854-5869.
[http://dx.doi.org/10.3390/molecules17055854] [PMID: 22592089]
[57]
Mencherini, T; Campone, L; Piccinelli, A.L; García Mesa, M; Sánchez, D.M; Aquino, R.P; Rastrelli, L HPLC-PDA-MS and NMR characterization of a hydroalcoholic extract of Citrus aurantium L. var. amara peel with antiedematogenic activity. J. Agric. Food Chem., 2013, 61(8), 1686-1693.
[http://dx.doi.org/10.1021/jf302815t] [PMID: 22957519]
[58]
El-Feky, A.M; Elbatanony, M.M; Mounier, M.M Anti-cancer potential of the lipoidal and flavonoidal compounds from Pisum sativum and Vicia faba peels. Egyptian J. Bas. & App. Sci, 2018, 5(4), 258-264.
[http://dx.doi.org/10.1016/j.ejbas.2018.11.001]
[59]
Taetzsch, T; Block, M.L Pesticides, microglial NOX2, and Parkinson’s disease. J. Biochem. Mol. Toxicol., 2013, 27(2), 137-149.
[http://dx.doi.org/10.1002/jbt.21464] [PMID: 23349115]
[60]
Hamed, M.A; Aboul Naser, A.F; Aziz, W.M; Ibrahim, F.M; Ali, S.A; El-Rigal, N.S; Khalil, W.K.B Natural sources, dopaminergic and non-dopaminergic agents for therapeutic assessment of Parkinsonism in rats model. PharmaNutrition, 2020, 11, 100171.
[http://dx.doi.org/10.1016/j.phanu.2019.100171]
[61]
Altharawi, A; Alharthy, K.M; Althurwi, H.N; Albaqami, F.F; Alzarea, S.I; Al-Abbasi, F.A; Nadeem, M.S; Kazmi, I Europinidin inhibits rotenone-activated Parkinson’s disease in rodents by decreasing lipid peroxidation and inflammatory cytokines pathways. Molecules, 2022, 27(21), 7159.
[http://dx.doi.org/10.3390/molecules27217159] [PMID: 36363986]
[62]
Schulz, J.B; Lindenau, J; Seyfried, J; Dichgans, J Glutathione, oxidative stress and neurodegeneration. Eur. J. Biochem., 2000, 267(16), 4904-4911.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01595.x] [PMID: 10931172]
[63]
Magalingam, K.B; Radhakrishnan, A; Haleagrahara, N Protective effects of quercetin glycosides, rutin, and isoquercetrin against 6-hydroxydopamine (6-OHDA)-induced neurotoxicity in rat pheochromocytoma (PC-12) cells. Int. J. Immunopathol. Pharmacol., 2016, 29(1), 30-39.
[http://dx.doi.org/10.1177/0394632015613039] [PMID: 26542606]
[64]
Soto-Otero, R; Méndez-Álvarez, E; Hermida-Ameijeiras, Á; Muñoz-Patiño, A.M; Labandeira-Garcia, J.L Autoxidation and neurotoxicity of 6-hydroxydopamine in the presence of some antioxidants: potential implication in relation to the pathogenesis of Parkinson’s disease. J. Neurochem., 2000, 74(4), 1605-1612.
[http://dx.doi.org/10.1046/j.1471-4159.2000.0741605.x] [PMID: 10737618]
[65]
Glinka, Y.Y; Youdim, M.B Inhibition of mitochondrial complexes I and IV by 6-hydroxydopamine. Eur. J. Pharmacol., 1995, 292(3-4), 329-332.
[PMID: 7796873]
[66]
Walia, V; Kansotia, S Nitic oxide mediated neurodegeneration in Parkinson’s disease. Asian J. Pharm. Clin. Res., 2016, 9(5), 9-13.
[http://dx.doi.org/10.22159/ajpcr.2016.v9i5.11667]
[67]
Akyol, O; Zoroglu, S.S; Armutcu, F; Sahin, S; Gurel, A Nitric oxide as a physiopathological factor in neuropsychiatric disorders. In Vivo, 2004, 18(3), 377-390.
[PMID: 15341194]
[68]
Sindhu, K.M; Saravanan, K.S; Mohanakumar, K.P Behavioral differences in a rotenone-induced hemiparkinsonian rat model developed following intranigral or median forebrain bundle infusion. Brain Res., 2005, 1051(1-2), 25-34.
[http://dx.doi.org/10.1016/j.brainres.2005.05.051] [PMID: 15992782]
[69]
Wu, Y.N; Johnson, S.W Dopamine oxidation facilitates rotenone-dependent potentiation of N-methyl-d-aspartate currents in rat substantia nigra dopamine neurons. Neuroscience, 2011, 195, 138-144.
[http://dx.doi.org/10.1016/j.neuroscience.2011.08.041] [PMID: 21884756]
[70]
Gunduluru, S; Wudayagiri, R Protective role of Bacopa monnieri on induced Parkinson’s disease with particular reference to catecholamine system. Int. J. Pharm. Pharm. Sci., 2014, 6, 379-382.
[71]
Nagappan, P; Krishnamurthy, V IC50 value of hesperidin against free radicals: an in vitro study. J Free Radic Antioxid Photon, (214), 271-277.
[72]
Gervais, J; Rouillard, C Dorsal raphe stimulation differentially modulates dopaminergic neurons in the ventral tegmental area and substantia nigra. Synapse, 2000, 35(4), 281-291.
[http://dx.doi.org/10.1002/(SICI)1098-2396(20000315)35:4<281:AID-SYN6>3.0.CO;2-A] [PMID: 10657038]
[73]
Farshbaf, M.J Succinate dehydrogenase in Parkinson’s disease. Front. Biol. (Beijing), 2017, 12(3), 175-182.
[http://dx.doi.org/10.1007/s11515-017-1450-6]
[74]
Quistorff, B; Secher, N.H; Van Lieshout, J.J Lactate fuels the human brain during exercise. FASEB J., 2008, 22(10), 3443-3449.
[http://dx.doi.org/10.1096/fj.08-106104] [PMID: 18653766]
[75]
Ross, J.M; Öberg, J; Brené, S; Coppotelli, G; Terzioglu, M; Pernold, K; Goiny, M; Sitnikov, R; Kehr, J; Trifunovic, A; Larsson, N.G; Hoffer, B.J; Olson, L High brain lactate is a hallmark of aging and caused by a shift in the lactate dehydrogenase A/B ratio. Proc. Natl. Acad. Sci. USA, 2010, 107(46), 20087-20092.
[http://dx.doi.org/10.1073/pnas.1008189107] [PMID: 21041631]
[76]
Imamura, K; Hishikawa, N; Sawada, M; Nagatsu, T; Yoshida, M; Hashizume, Y Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson’s disease brains. Acta Neuropathol., 2003, 106(6), 518-526.
[http://dx.doi.org/10.1007/s00401-003-0766-2] [PMID: 14513261]
[77]
Chen, G; Liu, J; Jiang, L; Ran, X; He, D; Li, Y Galangin reduces the loss of dopaminergic neurons in an LPS-Evoked model of Parkinson’s disease in rats. Int. J. Mol. Sci., 2017, 19(1), 12.
[http://dx.doi.org/10.3390/ijms19010012]
[78]
Mattson, M.P; Duan, W; Pedersen, W.A; Culmsee, C Neurodegenerative disorders and ischemic brain diseases. Apoptosis, 2001, 6(1/2), 69-81.
[http://dx.doi.org/10.1023/A:1009676112184] [PMID: 11321043]
[79]
Jenner, P An overview of adenosine A2A receptor antagonists in Parkinson’s disease. Int. Rev. Neurobiol., 2014, 119, 71-86.
[http://dx.doi.org/10.1016/B978-0-12-801022-8.00003-9] [PMID: 25175961]
[80]
Gyoneva, S; Shapiro, L; Lazo, C; Garnier-Amblard, E; Smith, Y; Miller, G.W; Traynelis, S.F Adenosine A2A receptor antagonism reverses inflammation-induced impairment of microglial process extension in a model of Parkinson’s disease. Neurobiol. Dis., 2014, 67, 191-202.
[http://dx.doi.org/10.1016/j.nbd.2014.03.004] [PMID: 24632419]
[81]
Pinna, A; Bonaventura, J; Farré, D; Sánchez, M; Simola, N; Mallol, J; Lluís, C; Costa, G; Baqi, Y; Müller, C.E; Cortés, A; McCormick, P; Canela, E.I; Martínez-Pinilla, E; Lanciego, J.L; Casadó, V; Armentero, M.T; Franco, R l-DOPA disrupts adenosine A2A–cannabinoid CB1–dopamine D2 receptor heteromer cross-talk in the striatum of hemiparkinsonian rats: Biochemical and behavioral studies. Exp. Neurol., 2014, 253, 180-191.
[http://dx.doi.org/10.1016/j.expneurol.2013.12.021] [PMID: 24412491]
[82]
Cho, J Antioxidant and neuroprotective effects of hesperidin and its aglycone hesperetin. Arch. Pharm. Res., 2006, 29(8), 699-706.
[http://dx.doi.org/10.1007/BF02968255] [PMID: 16964766]
[83]
Nouri, Z; Fakhri, S; El-Senduny, F.F; Sanadgol, N; Abd-ElGhani, G.E; Farzaei, M.H; Chen, J.T On the neuroprotective effects of naringenin: Pharmacological targets, signaling pathways, molecular mechanisms, and clinical perspective. Biomolecules, 2019, 9(11), 690.
[http://dx.doi.org/10.3390/biom9110690] [PMID: 31684142]
[84]
El Madani, M.A Abd ELSalam, R.M.; Attia, A.S.; El-Shenawy, S.M.; Arbid, M.S. Neuropharmacological effects of naringenin, harmine and adenosine on Parkinsonism induced in rats. Pharm. Lett., 2016, 8, 45-57.
[85]
Cavia-Saiz, M; Busto, M.D; Pilar-Izquierdo, M.C; Ortega, N; Perez-Mateos, M; Muñiz, P Antioxidant properties, radical scavenging activity and biomolecule protection capacity of flavonoid naringenin and its glycoside naringin: a comparative study. J. Sci. Food Agric., 2010, 90(7), 1238-1244.
[http://dx.doi.org/10.1002/jsfa.3959] [PMID: 20394007]
[86]
Manjari, S.K.V; Abraham, S.M; Poornima, R; Chaturvedi, R.K; Maity, S; Komal, P Unprecedented effect of vitamin D3 on T-cell receptor beta subunit and alpha7 nicotinic acetylcholine receptor expression in a 3-nitropropionic acid induced mouse model of Huntington’s disease. IBRO Neuroscience Reports, 2023, 15, 116-125.
[http://dx.doi.org/10.1016/j.ibneur.2023.07.001]
[87]
de Souza, L.G; Rennó, M.N; Figueroa-Villar, J.D Coumarins as cholinesterase inhibitors: A review. Chem. Biol. Interact., 2016, 254, 11-23.
[http://dx.doi.org/10.1016/j.cbi.2016.05.001] [PMID: 27174134]
[88]
Kostova, I; Bhatia, S; Grigorov, P; Balkansky, S; Parmar, V.S; Prasad, A.K; Saso, L Coumarins as antioxidants. Curr. Med. Chem., 2011, 18(25), 3929-3951.
[http://dx.doi.org/10.2174/092986711803414395] [PMID: 21824098]
[89]
Gan, J; Feng, Y; He, Z; Li, X; Zhang, H Correlations between antioxidant activity and alkaloids and phenols of Maca (Lepidium meyenii). J. Food Qual., 2017, 2017, 1-10.
[http://dx.doi.org/10.1155/2017/3185945]
[90]
Omoruyi, S.I; Ibrakaw, A.S; Ekpo, O.E; Boatwright, J.S; Cupido, C.N; Hussein, A.A Neuroprotective activities of Crossyne flava Bulbs and amaryllidaceae alkaloids: Implications for Parkinson’s disease. Molecules, 2021, 26(13), 3990.
[http://dx.doi.org/10.3390/molecules26133990] [PMID: 34208814]
[91]
Piccialli, I; Tedeschi, V; Caputo, L; Amato, G; De Martino, L; De Feo, V; Secondo, A; Pannaccione, A The antioxidant activity of limonene counteracts neurotoxicity triggered by Aβ1-42 oligomers in primary cortical neurons. Antioxidants, 2021, 10(6), 937.
[http://dx.doi.org/10.3390/antiox10060937] [PMID: 34207788]
[92]
Eddin, L.B; Jha, N.K; Meeran, M.F.N; Kesari, K.K; Beiram, R; Ojha, S Neuroprotective potential of limonene and limonene containing Nntural products. Molecules, 2021, 26(15), 4535.
[http://dx.doi.org/10.3390/molecules26154535] [PMID: 34361686]

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