Review Article

Exploring the Efficient Natural Products for the Therapy of Parkinson’s Disease via Drosophila Melanogaster (Fruit Fly) Models

Author(s): Wen Zhang, Yingjie Ju, Yunuo Ren, Yaodong Miao and Yiwen Wang*

Volume 25, Issue 2, 2024

Published on: 10 January, 2024

Page: [77 - 93] Pages: 17

DOI: 10.2174/0113894501281402231218071641

Price: $65

conference banner
Abstract

Parkinson's disease (PD) is a severe neurodegenerative disorder, partly attributed to mutations, environmental toxins, oxidative stress, abnormal protein aggregation, and mitochondrial dysfunction. However, the precise pathogenesis of PD and its treatment strategy still require investigation. Fortunately, natural products have demonstrated potential as therapeutic agents for alleviating PD symptoms due to their neuroprotective properties. To identify promising lead compounds from herbal medicines' natural products for PD management and understand their modes of action, suitable animal models are necessary. Drosophila melanogaster (fruit fly) serves as an essential model for studying genetic and cellular pathways in complex biological processes. Diverse Drosophila PD models have been extensively utilized in PD research, particularly for discovering neuroprotective natural products. This review emphasizes the research progress of natural products in PD using the fruit fly PD model, offering valuable insights into utilizing invertebrate models for developing novel anti-PD drugs.

Keywords: Parkinson's disease, Drosophila melanogaster, natural products, chinese medicines, neurodegeneration, herbal medicine, active compounds.

« Previous
Graphical Abstract
[1]
Ortega-Arellano HF, Jimenez-Del-Rio M, Velez-Pardo C. Minocycline protects, rescues and prevents knockdown transgenic parkin Drosophila against paraquat/iron toxicity: Implications for autosomic recessive juvenile parkinsonism. Neurotoxicology 2017; 60: 42-53.
[http://dx.doi.org/10.1016/j.neuro.2017.03.002] [PMID: 28284907]
[2]
Wang H, Sun Z, Rehman R, Wang H, Wang Y, Wang H. Rosemary extract‐mediated lifespan extension and attenuated oxidative damage in drosophila melanogaster fed on high‐fat diet. J Food Sci 2017; 82(4): 1006-11.
[http://dx.doi.org/10.1111/1750-3841.13656] [PMID: 28241105]
[3]
Chambers RP, Call GB, Meyer D, et al. Nicotine increases lifespan and rescues olfactory and motor deficits in a Drosophila model of Parkinson’s disease. Behav Brain Res 2013; 253: 95-102.
[http://dx.doi.org/10.1016/j.bbr.2013.07.020] [PMID: 23871228]
[4]
Forno LS. Neuropathology of Parkinson’s disease. J Neuropathol Exp Neurol 1996; 55(3): 259-72.
[http://dx.doi.org/10.1097/00005072-199603000-00001] [PMID: 8786384]
[5]
Cuervo AM Es, Fau Wong M, Martinez-Vicente M, Martinez-Vicente . Protein degradation, aggregation, and misfolding. Mov Disord 2010; 25 (Suppl 1): 549-54.
[http://dx.doi.org/10.1002/mds.22718]
[6]
Dhanraj V, Karuppaiah J, Balakrishnan R, Elangovan N. Myricetin attenuates neurodegeneration and cognitive impairment in Parkinsonism. Front Biosci 2018; 10(3): 481-94.
[http://dx.doi.org/10.2741/e835]
[7]
Schneider SA, Obeso JA. Clinical and pathological features of Parkinson’s disease.In: Behavioral Neurobiology of Huntington's Disease and Parkinson's Disease. Berlin, Heidelberg: Springer 2014; 22: p. 205-20.
[http://dx.doi.org/10.1007/7854_2014_317]
[8]
Ward CD, Hess WA, Calne DB. Olfactory impairment in Parkinson’s disease. Neurology 1983; 33(7): 943-6.
[http://dx.doi.org/10.1212/WNL.33.7.943] [PMID: 6683381]
[9]
Wszolek ZK, Markopoulou K. Olfactory dysfunction in Parkinson’s disease. Clin Neurosci 1998; 5(2): 94-101.
[PMID: 10785834]
[10]
Takeda A, Kikuchi A, Matsuzaki-Kobayashi M, Sugeno N, Itoyama Y, Eds. Olfactory dysfunction in Parkinson’s disease. Journal of Neurology. 2007; 254: p. (S4)2-7.
[http://dx.doi.org/10.1007/s00415-007-4002-1]
[11]
Diederich NJ, Paolini V. Fau - Vaillant M, Vaillant M. Slow wave sleep and dopaminergic treatment in Parkinson’s disease: A polysomnographic study. Acta Neurol Scand 2009; 120(5): 308-13.
[http://dx.doi.org/10.1111/j.1600-0404.2009.01167.x]
[12]
Sudati JH, Vieira FA, Pavin SS, et al. Valeriana officinalis attenuates the rotenone-induced toxicity in Drosophila melanogaster. Neurotoxicology 2013; 37: 118-26.
[http://dx.doi.org/10.1016/j.neuro.2013.04.006]
[13]
Chittoor-Vinod VG, Villalobos-Cantor S, Roshak H, Shea K, Abalde-Atristain L, Martin I. Dietary amino acids impact lrrk2-induced neurodegeneration in parkinson’s disease models. J Neurosci 2020; 40(32): 6234-49.
[http://dx.doi.org/10.1523/JNEUROSCI.2809-19.2020] [PMID: 32605938]
[14]
Dorsey ER, Sherer T, Okun MS, Bloem BR. The emerging evidence of the parkinson pandemic. J Parkinsons Dis 2018; 8(s1): S3-8.
[http://dx.doi.org/10.3233/JPD-181474] [PMID: 30584159]
[15]
Musachio EAS, Araujo SM, Bortolotto VC, et al. Bisphenol A exposure is involved in the development of Parkinson like disease in Drosophila melanogaster. Food Chem Toxicol 2020; 137: 111128.
[http://dx.doi.org/10.1016/j.fct.2020.111128]
[16]
Belaidi AA, Bush AI. Iron neurochemistry in Alzheimer’s disease and Parkinson’s disease: Targets for therapeutics. J Neurochem 2016; 139 (Suppl. 1): 179-97.
[http://dx.doi.org/10.1111/jnc.13425]
[17]
Jahromi SR, Haddadi M, Shivanandappa T, Ramesh SR. Attenuation of neuromotor deficits by natural antioxidants of Decalepis hamiltonii in transgenic Drosophila model of Parkinson’s disease. Neuroscience 2015; 293: 136-50.
[http://dx.doi.org/10.1016/j.neuroscience.2015.02.048] [PMID: 25754960]
[18]
Feany MB, Bender WW. A drosophila model of parkinson’s disease. Nature 2000; 404(6776): 394-8.
[http://dx.doi.org/10.1038/35006074] [PMID: 10746727]
[19]
Aryal B, Lee Y. Disease model organism for Parkinson disease: Drosophila melanogaster. BMB Rep 2019; 52(4): 250-8.
[20]
Liu M, Yu S, Wang J, et al. Ginseng protein protects against mitochondrial dysfunction and neurodegeneration by inducing mitochondrial unfolded protein response in Drosophila melanogaster PINK1 model of Parkinson’s disease. J Ethnopharmacol 2020; 247: 112213.
[http://dx.doi.org/10.1016/j.jep.2019.112213] [PMID: 31562951]
[21]
Moisoi N, Fedele V, Edwards J, Martins LM. Loss of PINK1 enhances neurodegeneration in a mouse model of Parkinson’s disease triggered by mitochondrial stress. Neuropharmacology 2014; 77: 350-7.
[http://dx.doi.org/10.1016/j.neuropharm.2013.10.009] [PMID: 24161480]
[22]
Polymeropoulos MH, Lavedan C, Leroy E, et al. Mutation in the α-synuclein gene identified in families with Parkinson’s disease. Science 1997; 276(5321): 2045-7.
[http://dx.doi.org/10.1126/science.276.5321.2045] [PMID: 9197268]
[23]
Wang MS, Boddapati S, Emadi S, Sierks MR. Curcumin reduces α-synuclein induced cytotoxicity in Parkinson’s disease cell model. BMC Neurosci 2010; 11(1): 57.
[http://dx.doi.org/10.1186/1471-2202-11-57] [PMID: 20433710]
[24]
Sultana R, Butterfield DA. Brain protein oxidation and modification for good or for bad in alzheimer’s disease. In: Neurochemical Mechanisms in Disease Advances in Neurobiology. Springer New York 2010; pp. 585-605.
[http://dx.doi.org/10.1007/978-1-4419-7104-3_17]
[25]
Perier C, Vila M. Mitochondrial biology and Parkinson’s disease. Cold Spring Harb Perspect Med 2012; 2(2): a009332.
[http://dx.doi.org/10.1101/cshperspect.a009332] [PMID: 22355801]
[26]
Straka I, Minár M, Gažová A. Valkovič P, Kyselovič J. Clinical aspects of adherence to pharmacotherapy in Parkinson disease: A PRISMA-compliant systematic review. Medicine 2018; 97(23): e10962.
[27]
Aimaiti M, Wumaier A, Aisa Y, et al. Acteoside exerts neuroprotection effects in the model of Parkinson’s disease via inducing autophagy: Network pharmacology and experimental study. Eur J Pharmacol 2021; 903: 174136.
[http://dx.doi.org/10.1016/j.ejphar.2021.174136] [PMID: 33940032]
[28]
Wu Z, Wu A, Dong J, Sigears A, Lu B. Grape skin extract improves muscle function and extends lifespan of a Drosophila model of Parkinson’s disease through activation of mitophagy. Exp Gerontol 2018; 113: 10-7.
[http://dx.doi.org/10.1016/j.exger.2018.09.014] [PMID: 30248358]
[29]
Thao DTP. Ubiquitin carboxyl-terminal hydrolase l1 in parkinson’s disease. In: Ubiquitin Proteasome System - Current Insights into Mechanism Cellular Regulation and Disease. IntechOpen 2019. Available from:
[http://dx.doi.org/10.5772/intechopen.85273]
[30]
Stacy M, Bowron A, Guttman M, et al. Identification of motor and nonmotor wearing‐off in Parkinson’s disease: Comparison of a patient questionnaire versus a clinician assessment. Mov Disord 2005; 20(6): 726-33.
[http://dx.doi.org/10.1002/mds.20383] [PMID: 15719426]
[31]
Pandareesh MD, Shrivash MK, Naveen Kumar HN, Misra K, Srinivas Bharath MM. Curcumin monoglucoside shows improved bioavailability and mitigates rotenone induced neurotoxicity in cell and drosophila models of parkinson’s disease. Neurochem Res 2016; 41(11): 3113-28.
[http://dx.doi.org/10.1007/s11064-016-2034-6] [PMID: 27535828]
[32]
Abolaji AO, Adedara AO, Adie MA, Vicente-Crespo M, Farombi EO. Resveratrol prolongs lifespan and improves 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced oxidative damage and behavioural deficits in Drosophila melanogaster. Biochem Biophys Res Commun 2018; 503(2): 1042-8.
[http://dx.doi.org/10.1016/j.bbrc.2018.06.114] [PMID: 29935183]
[33]
Siddique YH, Mujtaba SF, Jyoti S, Naz F. GC–MS analysis of Eucalyptus citriodora leaf extract and its role on the dietary supplementation in transgenic Drosophila model of Parkinson’s disease. Food Chem Toxicol 2013; 55: 29-35.
[http://dx.doi.org/10.1016/j.fct.2012.12.028] [PMID: 23318758]
[34]
Siddique YH, Khan W, Singh BR, Naqvi AH. Synthesis of alginate-curcumin nanocomposite and its protective role in transgenic Drosophila model of Parkinson’s disease. ISRN Pharmacol 2013; 2013: 794582.
[http://dx.doi.org/10.1155/2013/794582]
[35]
Seidl SE, Potashkin JA. The promise of neuroprotective agents in Parkinson’s disease. Front Neurol 2011; 2: 68.
[http://dx.doi.org/10.3389/fneur.2011.00068] [PMID: 22125548]
[36]
de Andrade Teles RB, Diniz TC, Costa Pinto TC, et al. Flavonoids as therapeutic agents in Alzheimer’s and Parkinson’s disease: A systematic review of preclinical evidences. Oxid Med Cell Longev 2018; 2018: 1-21.
[http://dx.doi.org/10.1155/2018/7043213] [PMID: 29861833]
[37]
Akasaka T, Ocorr K. Drug discovery through functional screening in the Drosophila heart. Methods Mol Biol 2009; 577: 235-49.
[http://dx.doi.org/10.1007/978-1-60761-232-2_18] [PMID: 19718521]
[38]
Lopez-Ortiz C, Gracia-Rodriguez C, Belcher S, et al. Drosophila melanogaster as a translational model system to explore the impact of phytochemicals on human health. Int J Mol Sci 2023; 24(17): 13365.
[http://dx.doi.org/10.3390/ijms241713365] [PMID: 37686177]
[39]
Sun S, Yang S, Dai M, et al. The effect of Astragalus polysaccharides on attenuation of diabetic cardiomyopathy through inhibiting the extrinsic and intrinsic apoptotic pathways in high glucose -stimulated H9C2 cells. BMC Complement Altern Med 2017; 17(1): 310.
[http://dx.doi.org/10.1186/s12906-017-1828-7] [PMID: 28610566]
[40]
Pramod Kumar P, Harish Prashanth KV. Diet with low molecular weight chitosan exerts neuromodulation in rotenone induced drosophila model of Parkinson’s disease. Food Chem Toxicol 2020; 146: 111860.
[http://dx.doi.org/10.1016/j.fct.2020.111860] [PMID: 33212211]
[41]
Wu M, Li Y, Miao Y, Qiao H, Wang Y. Exploring the efficient natural products for Alzheimer’s disease therapy viaDrosophila melanogaster (fruit fly) models. J Drug Target 2023; 31(8): 817-31.
[http://dx.doi.org/10.1080/1061186X.2023.2245582] [PMID: 37545435]
[42]
Wang S, Ju Y, Gao L, Miao Y, Qiao H, Wang Y. The fruit fly kidney stone models and their application in drug development. Heliyon 2022; 8(4): e09232.
[http://dx.doi.org/10.1016/j.heliyon.2022.e09232] [PMID: 35399385]
[43]
Meng Q, Xu Y, Li Y, Wang Y. Novel studies on Drosophila melanogaster model reveal the roles of JNK-Jak/STAT axis and intestinal microbiota in insulin resistance. J Drug Target 2023; 31(3): 261-8.
[http://dx.doi.org/10.1080/1061186X.2022.2144869] [PMID: 36343203]
[44]
Weina T, Ying L, Yiwen W, Huan-huan Q. What we have learnt from Drosophila model organism: The coordination between insulin signaling pathway and tumor cells. Heliyon 2022; 8(7): e09957.
[http://dx.doi.org/10.1016/j.heliyon.2022.e09957] [PMID: 35874083]
[45]
Tong Y, Wei Y, Ju Y, et al. Anaerobic purinolytic enzymes enable dietary purine clearance by engineered gut bacteria. Cell Chem Biol 2023; 30(9): 1104-1114.e7.
[http://dx.doi.org/10.1016/j.chembiol.2023.04.008] [PMID: 37164019]
[46]
Ambegaokar SS, Roy B, Jackson GR. Neurodegenerative models in Drosophila: Polyglutamine disorders, Parkinson disease, and amyotrophic lateral sclerosis. Neurobiol Dis 2010; 40(1): 29-39.
[http://dx.doi.org/10.1016/j.nbd.2010.05.026] [PMID: 20561920]
[47]
Lücking CB, Dürr A, Bonifati V, et al. Association between early-onset Parkinson’s disease and mutations in the parkin gene. N Engl J Med 2000; 342(21): 1560-7.
[http://dx.doi.org/10.1056/NEJM200005253422103] [PMID: 10824074]
[48]
Kitada T, Asakawa S, Hattori N, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998; 392(6676): 605-8.
[http://dx.doi.org/10.1038/33416] [PMID: 9560156]
[49]
Matsumine H, Saito M, Shimoda-Matsubayashi S, et al. Localization of a gene for an autosomal recessive form of juvenile Parkinsonism to chromosome 6q25.2-27. Am J Hum Genet 1997; 60(3): 588-96.
[PMID: 9042918]
[50]
Pienaar IS, Götz J, Feany MB. Parkinson’s disease: Insights from non-traditional model organisms. Prog Neurobiol 2010; 92(4): 558-71.
[http://dx.doi.org/10.1016/j.pneurobio.2010.09.001] [PMID: 20851733]
[51]
Whitworth AJ. Drosophila models of Parkinson’s disease. Adv Genet 2011; 73: 1-50.
[http://dx.doi.org/10.1016/B978-0-12-380860-8.00001-X] [PMID: 21310293]
[52]
Guo M. What have we learned from Drosophila models of Parkinson’s disease? Prog Brain Res. 2010; 184: p. 2-16.
[http://dx.doi.org/10.1016/S0079-6123(10)84001-4] [PMID: 20887867]
[53]
Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci USA 2003; 100(7): 4078-83.
[http://dx.doi.org/10.1073/pnas.0737556100] [PMID: 12642658]
[54]
Park J, Kim SY, Cha GH, Lee SB, Kim S, Chung J. Drosophila DJ-1 mutants show oxidative stress-sensitive locomotive dysfunction. Gene 2005; 361: 133-9.
[http://dx.doi.org/10.1016/j.gene.2005.06.040] [PMID: 16203113]
[55]
Maroteaux L, Campanelli JT, Scheller RH. Synuclein: A neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J Neurosci 1988; 8(8): 2804-15.
[http://dx.doi.org/10.1523/JNEUROSCI.08-08-02804.1988] [PMID: 3411354]
[56]
Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE, Lansbury PT Jr. Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson’s disease: Implications for pathogenesis and therapy. Proc Natl Acad Sci USA 2000; 97(2): 571-6.
[http://dx.doi.org/10.1073/pnas.97.2.571] [PMID: 10639120]
[57]
Siddique YH, Naz F. Rahul, Rashid M, Tajuddin. Effect of Majun Baladur on life span, climbing ability, oxidative stress and dopaminergic neurons in the transgenic Drosophila model of Parkinson’s disease. Heliyon 2019; 5(4): e01483.
[http://dx.doi.org/10.1016/j.heliyon.2019.e01483] [PMID: 31011645]
[58]
Chen AY, Xia S, Wilburn P, Tully T. Olfactory deficits in an alpha-synuclein fly model of Parkinson’s disease. PLoS One 2014; 9(5): e97758.
[http://dx.doi.org/10.1371/journal.pone.0097758] [PMID: 24879013]
[59]
Briffa M, Ghio S, Neuner J, et al. Extracts from two ubiquitous Mediterranean plants ameliorate cellular and animal models of neurodegenerative proteinopathies. Neurosci Lett 2017; 638: 12-20.
[http://dx.doi.org/10.1016/j.neulet.2016.11.058] [PMID: 27919712]
[60]
Schaffner A, Li X, Gomez-Llorente Y, et al. Vitamin B12 modulates Parkinson’s disease LRRK2 kinase activity through allosteric regulation and confers neuroprotection. Cell Res 2019; 29(4): 313-29.
[http://dx.doi.org/10.1038/s41422-019-0153-8] [PMID: 30858560]
[61]
Paisán-Ruíz C, Jain S, Evans EW, et al. Cloning of the gene containing mutations that cause PARK8-linked Parkinson’s disease. Neuron 2004; 44(4): 595-600.
[http://dx.doi.org/10.1016/j.neuron.2004.10.023] [PMID: 15541308]
[62]
Parisiadou L, Yu J, Sgobio C, et al. LRRK2 regulates synaptogenesis and dopamine receptor activation through modulation of PKA activity. Nat Neurosci 2014; 17(3): 367-76.
[http://dx.doi.org/10.1038/nn.3636] [PMID: 24464040]
[63]
Wallings RL, Tansey MG. LRRK2 regulation of immune-pathways and inflammatory disease. Biochem Soc Trans 2019; 47(6): 1581-95.
[http://dx.doi.org/10.1042/BST20180463] [PMID: 31769472]
[64]
Madureira M, Connor-Robson N, Wade-Martins R. LRRK2: Autophagy and lysosomal activity. Front Neurosci 2020; 14: 498.
[http://dx.doi.org/10.3389/fnins.2020.00498] [PMID: 32523507]
[65]
Bardien S, Lesage S, Brice A, Carr J. Genetic characteristics of leucine-rich repeat kinase 2 (LRRK2) associated Parkinson’s disease. Parkinsonism Relat Disord 2011; 17(7): 501-8.
[http://dx.doi.org/10.1016/j.parkreldis.2010.11.008] [PMID: 21641266]
[66]
Orenstein SJ, Kuo SH, Tasset I, et al. Interplay of LRRK2 with chaperone-mediated autophagy. Nat Neurosci 2013; 16(4): 394-406.
[http://dx.doi.org/10.1038/nn.3350] [PMID: 23455607]
[67]
Liu Z, Wang X, Yu Y, et al. A Drosophila model for LRRK2 -linked parkinsonism. Proc Natl Acad Sci USA 2008; 105(7): 2693-8.
[http://dx.doi.org/10.1073/pnas.0708452105] [PMID: 18258746]
[68]
Kahle PJ, Waak J, Gasser T. DJ-1 and prevention of oxidative stress in Parkinson’s disease and other age-related disorders. Free Radic Biol Med 2009; 47(10): 1354-61.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.08.003] [PMID: 19686841]
[69]
Meulener M, Whitworth AJ, Armstrong-Gold CE, et al. Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson’s disease. Curr Biol 2005; 15(17): 1572-7.
[http://dx.doi.org/10.1016/j.cub.2005.07.064] [PMID: 16139213]
[70]
Casani S, Gómez-Pastor R, Matallana E, Paricio N. Antioxidant compound supplementation prevents oxidative damage in a Drosophila model of Parkinson’s disease. Free Radic Biol Med 2013; 61: 151-60.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.03.021] [PMID: 23548634]
[71]
Valente EM, Abou-Sleiman PM, Caputo V, et al. Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 2004; 304(5674): 1158-60.
[http://dx.doi.org/10.1126/science.1096284] [PMID: 15087508]
[72]
Zang LY, Misra HP. Inactivation of acetylcholinesterase by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine hydrochloride. Mol Cell Biochem 2003; 254(1/2): 131-6.
[http://dx.doi.org/10.1023/A:1027376303043] [PMID: 14674691]
[73]
Hu X, Zhang D, Pang H, et al. Macrophage antigen complex-1 mediates reactive microgliosis and progressive dopaminergic neurodegeneration in the MPTP model of Parkinson’s disease. J Immunol 2008; 181(10): 7194-204.
[http://dx.doi.org/10.4049/jimmunol.181.10.7194] [PMID: 18981141]
[74]
Speciale SG. MPTP: Insights into parkinsonian neurodegeneration. Neurotoxicol Teratol 2002; 24(5): 607-20.
[http://dx.doi.org/10.1016/S0892-0362(02)00222-2] [PMID: 12200192]
[75]
Cai Y, Zhang X, Zhou X, et al. Nicotine suppresses the neurotoxicity by MPP +/MPTP through activating α7nAChR/PI3K/Trx-1 and suppressing ER stress. Neurotoxicology 2017; 59: 49-55.
[http://dx.doi.org/10.1016/j.neuro.2017.01.002] [PMID: 28082123]
[76]
Uversky VN. Neurotoxicant-induced animal models of Parkinson?s disease: Understanding the role of rotenone, maneb and paraquat in neurodegeneration. Cell Tissue Res 2004; 318(1): 225-41.
[http://dx.doi.org/10.1007/s00441-004-0937-z] [PMID: 15258850]
[77]
Cannon JR, Greenamyre JT. Neurotoxic in vivo models of Parkinson’s disease. Prog Brain Res. 2010; 184: p. 17-33.
[http://dx.doi.org/10.1016/S0079-6123(10)84002-6] [PMID: 20887868]
[78]
Khadrawy YA, Salem AM, El-Shamy KA, Ahmed EK, Fadl NN, Hosny EN. Neuroprotective and therapeutic effect of caffeine on the rat model of parkinson’s disease induced by rotenone. J Diet Suppl 2017; 14(5): 553-72.
[http://dx.doi.org/10.1080/19390211.2016.1275916] [PMID: 28301304]
[79]
Spivey A. Rotenone and paraquat linked to Parkinson’s disease: Human exposure study supports years of animal studies. Environ Health Perspect 2011; 119(6): A259.
[http://dx.doi.org/10.1289/ehp.119-a259a] [PMID: 21628118]
[80]
Sherer TB, Betarbet R, Testa CM, et al. Mechanism of toxicity in rotenone models of Parkinson’s disease. J Neurosci 2003; 23(34): 10756-64.
[http://dx.doi.org/10.1523/JNEUROSCI.23-34-10756.2003] [PMID: 14645467]
[81]
Hosamani R. Muralidhara. Neuroprotective efficacy of Bacopa monnieri against rotenone induced oxidative stress and neurotoxicity in Drosophila melanogaster. Neurotoxicology 2009; 30(6): 977-85.
[http://dx.doi.org/10.1016/j.neuro.2009.08.012] [PMID: 19744517]
[82]
Dinis-Oliveira RJ, Remião F, Carmo H, et al. Paraquat exposure as an etiological factor of Parkinson’s disease. Neurotoxicology 2006; 27(6): 1110-22.
[http://dx.doi.org/10.1016/j.neuro.2006.05.012] [PMID: 16815551]
[83]
Jahromi SR, Haddadi M, Shivanandappa T, Ramesh SR. Neuroprotective effect of Decalepis hamiltonii in paraquat-induced neurotoxicity in Drosophila melanogaster: Biochemical and behavioral evidences. Neurochem Res 2013; 38(12): 2616-24.
[http://dx.doi.org/10.1007/s11064-013-1179-9] [PMID: 24173775]
[84]
Park JH, Jung JW, Ahn YJ, Kwon HW. Neuroprotective properties of phytochemicals against paraquat-induced oxidative stress and neurotoxicity in Drosophila melanogaster. Pestic Biochem Physiol 2012; 104(2): 118-25.
[http://dx.doi.org/10.1016/j.pestbp.2012.07.006]
[85]
Geens T, Aerts D, Berthot C, et al. A review of dietary and non-dietary exposure to bisphenol-A. Food Chem Toxicol 2012; 50(10): 3725-40.
[http://dx.doi.org/10.1016/j.fct.2012.07.059] [PMID: 22889897]
[86]
Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol 2007; 24(2): 139-77.
[http://dx.doi.org/10.1016/j.reprotox.2007.07.010] [PMID: 17825522]
[87]
Bae B, Jeong JH, Lee SJ. The quantification and characterization of endocrine disruptor bisphenol-A leaching from epoxy resin. Water Sci Technol 2002; 46(11-12): 381-7.
[http://dx.doi.org/10.2166/wst.2002.0766]
[88]
Khan S, Beigh S, Chaudhari BP, et al. Mitochondrial dysfunction induced by Bisphenol A is a factor of its hepatotoxicity in rats. Environ Toxicol 2016; 31(12): 1922-34.
[http://dx.doi.org/10.1002/tox.22193] [PMID: 26450347]
[89]
Jones DC, Miller GW. The effects of environmental neurotoxicants on the dopaminergic system: A possible role in drug addiction. Biochem Pharmacol 2008; 76(5): 569-81.
[http://dx.doi.org/10.1016/j.bcp.2008.05.010] [PMID: 18555207]
[90]
Adedara AO, Babalola AD, Stephano F, et al. An assessment of the rescue action of resveratrol in parkin loss of function-induced oxidative stress in Drosophila melanogaster. Sci Rep 2022; 12(1): 3922.
[http://dx.doi.org/10.1038/s41598-022-07909-7] [PMID: 35273283]
[91]
Jimenez-Del-Rio M, Daza-Restrepo A, Velez-Pardo C. The cannabinoid CP55,940 prolongs survival and improves locomotor activity in Drosophila melanogaster against paraquat: Implications in Parkinson’s disease. Neurosci Res 2008; 61(4): 404-11.
[http://dx.doi.org/10.1016/j.neures.2008.04.011] [PMID: 18538428]
[92]
Farombi EO, Abolaji AO, Farombi TH, Oropo AS, Owoje OA, Awunah MT. Garcinia kola seed biflavonoid fraction (Kolaviron), increases longevity and attenuates rotenone-induced toxicity in Drosophila melanogaster. Pestic Biochem Physiol 2018; 145: 39-45.
[http://dx.doi.org/10.1016/j.pestbp.2018.01.002] [PMID: 29482730]
[93]
Kumar A, Christian PK, Panchal K, Guruprasad BR, Tiwari AK. Supplementation of Spirulina (Arthrospira platensis) improves lifespan and locomotor activity in paraquat-sensitive DJ-1βΔ93 flies, a parkinson’s disease model in drosophila melanogaster. J Diet Suppl 2017; 14(5): 573-88.
[http://dx.doi.org/10.1080/19390211.2016.1275917]
[94]
Manjunath MJ. Muralidhara. Standardized extract of Withania somnifera (Ashwagandha) markedly offsets rotenone-induced locomotor deficits, oxidative impairments and neurotoxicity in Drosophila melanogaster. J Food Sci Technol 2015; 52(4): 1971-81.
[http://dx.doi.org/10.1007/s13197-013-1219-0] [PMID: 25829577]
[95]
Mannett BT, Capt BC, Pearman K, Buhlman LM, VandenBrooks JM, Call GB. Nicotine has a therapeutic window of effectiveness in a drosophila melanogaster model of parkinson’s disease. Parkinsons Dis 2022; 2022: 1-11.
[http://dx.doi.org/10.1155/2022/9291077] [PMID: 35844833]
[96]
He J, Li X, Yang S, et al. Gastrodin extends the lifespan and protects against neurodegeneration in the Drosophila PINK1 model of Parkinson’s disease. Food Funct 2021; 12(17): 7816-24.
[http://dx.doi.org/10.1039/D1FO00847A] [PMID: 34232246]
[97]
Phom L, Achumi B, Alone DP. Muralidhara, Yenisetti SC. Curcumin’s neuroprotective efficacy in Drosophila model of idiopathic Parkinson’s disease is phase specific: Implication of its therapeutic effectiveness. Rejuvenation Res 2014; 17(6): 481-9.
[http://dx.doi.org/10.1089/rej.2014.1591] [PMID: 25238331]
[98]
de Freitas Couto S, Araujo SM, Bortolotto VC, et al. 7-chloro-4-(phenylselanyl) quinoline prevents dopamine depletion in a Drosophila melanogaster model of Parkinson’s-like disease. J Trace Elem Med Biol 2019; 54: 232-43.
[http://dx.doi.org/10.1016/j.jtemb.2018.10.015] [PMID: 30366679]
[99]
Ortega-Arellano HF, Jimenez-Del-Rio M, Velez-Pardo C. Melatonin increases life span, restores the locomotor activity, and reduces lipid peroxidation (LPO) in transgenic knockdown parkin drosophila melanogaster exposed to paraquat or paraquat/Iron. Neurotox Res 2021; 39(5): 1551-63.
[http://dx.doi.org/10.1007/s12640-021-00397-z] [PMID: 34339012]
[100]
Sun X, Ran D, Zhao X, et al. Melatonin attenuates hLRRK2-induced sleep disturbances and synaptic dysfunction in a Drosophila model of Parkinson’s disease. Mol Med Rep 2016; 13(5): 3936-44.
[http://dx.doi.org/10.3892/mmr.2016.4991] [PMID: 26985725]
[101]
Martinez-Perez DA, Jimenez-Del-Rio M, Velez-Pardo C. Epigallocatechin-3-gallate protects and prevents paraquat-induced oxidative stress and neurodegeneration in knockdown dj-1-β drosophila melanogaster. Neurotox Res 2018; 34(3): 401-16.
[http://dx.doi.org/10.1007/s12640-018-9899-x] [PMID: 29667128]
[102]
Rao SV. Muralidhara, Yenisetti SC, Rajini PS. Evidence of neuroprotective effects of saffron and crocin in a Drosophila model of parkinsonism. Neurotoxicology 2016; 52: 230-42.
[http://dx.doi.org/10.1016/j.neuro.2015.12.010] [PMID: 26705857]
[103]
Inoue E, Suzuki T, Shimizu Y, Sudo K, Kawasaki H, Ishida N. Saffron ameliorated motor symptoms, short life span and retinal degeneration in Parkinson’s disease fly models. Gene 2021; 799: 145811.
[http://dx.doi.org/10.1016/j.gene.2021.145811] [PMID: 34224829]
[104]
Gonçalves DF, Senger LR, Foletto JVP, Michelotti P, Soares FAA, Dalla Corte CL. Caffeine improves mitochondrial function in PINK1B9-null mutant Drosophila melanogaster. J Bioenerg Biomembr 2023; 55(1): 1-13.
[http://dx.doi.org/10.1007/s10863-022-09952-5] [PMID: 36494592]
[105]
Tibashailwa N, Stephano F, Shadrack DM, Munissi JJE, Nyandoro SS. Neuroprotective potential of cinnamoyl derivatives against Parkinson’s disease indicators in Drosophila melanogaster and in silico models. Neurotoxicology 2023; 94: 147-57.
[http://dx.doi.org/10.1016/j.neuro.2022.11.010] [PMID: 36410467]
[106]
Chaves NSG, Janner DE, Poetini MR, et al. β-carotene-loaded nanoparticles protect against neuromotor damage, oxidative stress, and dopamine deficits in a model of Parkinson’s disease in Drosophila melanogaster. Comp Biochem Physiol C Toxicol Pharmacol 2023; 268: 109615.
[http://dx.doi.org/10.1016/j.cbpc.2023.109615] [PMID: 36940893]
[107]
Ortega-Arellano HF, Jimenez-Del-Rio M, Velez-Pardo C. Life span and locomotor activity modification by glucose and polyphenols in Drosophila melanogaster chronically exposed to oxidative stress-stimuli: implications in Parkinson’s disease. Neurochem Res 2011; 36(6): 1073-86.
[http://dx.doi.org/10.1007/s11064-011-0451-0] [PMID: 21442225]
[108]
Siima AA, Stephano F, Munissi JJE, Nyandoro SS. Ameliorative effects of flavonoids and polyketides on the rotenone induced Drosophila model of Parkinson’s disease. Neurotoxicology 2020; 81: 209-15.
[http://dx.doi.org/10.1016/j.neuro.2020.09.004] [PMID: 32937168]
[109]
Yang S, Xiu M, Li X, et al. The antioxidant effects of hedysarum polybotrys polysaccharide in extending lifespan and ameliorating aging-related diseases in Drosophila melanogaster. Int J Biol Macromol 2023; 241: 124609.
[http://dx.doi.org/10.1016/j.ijbiomac.2023.124609] [PMID: 37105250]
[110]
Girish C. Muralidhara. Propensity of Selaginella delicatula aqueous extract to offset rotenone-induced oxidative dysfunctions and neurotoxicity in Drosophila melanogaster: Implications for Parkinson’s disease. Neurotoxicology 2012; 33(3): 444-56.
[http://dx.doi.org/10.1016/j.neuro.2012.04.002] [PMID: 22521218]
[111]
Soares JJ, Rodrigues DT, Gonçalves MB, et al. Paraquat exposure-induced Parkinson’s disease-like symptoms and oxidative stress in Drosophila melanogaster: Neuroprotective effect of Bougainvillea glabra Choisy. Biomed Pharmacother 2017; 95: 245-51.
[http://dx.doi.org/10.1016/j.biopha.2017.08.073] [PMID: 28843913]
[112]
Ortega-Arellano HF, Jimenez-Del-Rio M, Velez-Pardo C. Neuroprotective Effects of Methanolic Extract of Avocado Persea americana (var. Colinred) Peel on Paraquat-Induced Locomotor Impairment, Lipid Peroxidation and Shortage of Life Span in Transgenic knockdown Parkin Drosophila melanogaster. Neurochem Res 2019; 44(8): 1986-98.
[http://dx.doi.org/10.1007/s11064-019-02835-z] [PMID: 31309393]
[113]
Bai XL, Luo YJ, Fan WQ, Zhang YM, Liao X. Neuroprotective effects of lycium barbarum fruit extract on Pink1B9Drosophila melanogaster genetic model of parkinson’s disease. Plant Foods Hum Nutr 2023; 78(1): 68-75.
[http://dx.doi.org/10.1007/s11130-022-01016-8] [PMID: 36322321]
[114]
Filaferro M, Codeluppi A, Brighenti V, et al. Disclosing the antioxidant and neuroprotective activity of an anthocyanin-rich extract from sweet cherry (Prunus avium L.) using in vitro and in vivo models. Antioxidants 2022; 11(2): 211.
[http://dx.doi.org/10.3390/antiox11020211] [PMID: 35204092]
[115]
Rosado-Ramos R, Poças GM, Marques D, et al. Genipin prevents alpha-synuclein aggregation and toxicity by affecting endocytosis, metabolism and lipid storage. Nat Commun 2023; 14(1): 1918.
[http://dx.doi.org/10.1038/s41467-023-37561-2] [PMID: 37024503]
[116]
Cicchetti F, Drouin-Ouellet J, Gross RE. Environmental toxins and Parkinson’s disease: what have we learned from pesticide-induced animal models? Trends Pharmacol Sci 2009; 30(9): 475-83.
[http://dx.doi.org/10.1016/j.tips.2009.06.005] [PMID: 19729209]
[117]
Zhang X, Lu L, Liu S, Ye W, Wu J, Zhang X. Acetylcholinesterase deficiency decreases apoptosis in dopaminergic neurons in the neurotoxin model of Parkinson’s disease. Int J Biochem Cell Biol 2013; 45(2): 265-72.
[http://dx.doi.org/10.1016/j.biocel.2012.11.015] [PMID: 23201480]
[118]
Bhusal CK, Uti DE, Mukherjee D, et al. Unveiling Nature’s potential: Promising natural compounds in Parkinson’s disease management. Parkinsonism Relat Disord 2023; 115: 105799.
[http://dx.doi.org/10.1016/j.parkreldis.2023.105799] [PMID: 37633805]
[119]
Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 2007; 6(4): 304-12.
[http://dx.doi.org/10.1038/nrd2272] [PMID: 17396135]
[120]
Jahan I, Ahmad A, Deep S. Effect of flavonoids on the destabilization of α-synuclein fibrils and their conversion to amorphous aggregate: A molecular dynamics simulation and experimental study. Biochim Biophys Acta Proteins Proteomics 2023; 1871(6): 140951.
[http://dx.doi.org/10.1016/j.bbapap.2023.140951] [PMID: 37574034]
[121]
Glover V, Sandler M. Neurotoxins and Monoamine Oxidase B Inhibitors: Possible Mechanisms for the Neuroprotective Effect of (—)-Deprenyl. Inhibitors of Monoamine Oxidase B 1993; 169-81.
[http://dx.doi.org/10.1007/978-3-0348-6348-3_8]
[122]
Halliwell B. Oxidative stress and neurodegeneration: Where are we now? J Neurochem 2006; 97(6): 1634-58.
[http://dx.doi.org/10.1111/j.1471-4159.2006.03907.x] [PMID: 16805774]
[123]
Razani E, Pourbagheri-Sigaroodi A, Safaroghli-Azar A, Zoghi A, Shanaki-Bavarsad M, Bashash D. The PI3K/Akt signaling axis in Alzheimer’s disease: A valuable target to stimulate or suppress? Cell Stress Chaperones 2021; 26(6): 871-87.
[http://dx.doi.org/10.1007/s12192-021-01231-3] [PMID: 34386944]
[124]
Akiyama H, Barger S, Barnum S, et al. Inflammation and Alzheimer’s disease. Neurobiol Aging 2000; 21(3): 383-421.
[http://dx.doi.org/10.1016/S0197-4580(00)00124-X] [PMID: 10858586]
[125]
Mikhed Y, Daiber A, Steven S. Mitochondrial oxidative stress, mitochondrial dna damage and their role in age-related vascular dysfunction. Int J Mol Sci 2015; 16(7): 15918-53.
[http://dx.doi.org/10.3390/ijms160715918] [PMID: 26184181]
[126]
Madiha S, Batool Z, Shahzad S, et al. Naringenin, a functional food component, improves motor and non-motor symptoms in animal model of parkinsonism induced by rotenone. Plant Foods Hum Nutr 2023.
[http://dx.doi.org/10.1007/s11130-023-01103-4] [PMID: 37796415]
[127]
Meng HW, Shen ZB, Meng XS, et al. Novel flavonoid 1,3,4-oxadiazole derivatives ameliorate MPTP-induced Parkinson’s disease via Nrf2/NF-κB signaling pathway. Bioorg Chem 2023; 138: 106654.
[http://dx.doi.org/10.1016/j.bioorg.2023.106654] [PMID: 37300959]
[128]
Su KY, Yu CY, Chen YW, et al. Rutin, a flavonoid and principal component of saussurea involucrata, attenuates physical fatigue in a forced swimming mouse model. Int J Med Sci 2014; 11(5): 528-37.
[http://dx.doi.org/10.7150/ijms.8220] [PMID: 24693223]
[129]
Rios-Barrera LD, Riesgo-Escovar JR. Regulating cell morphogenesis: The Drosophila Jun N-terminal kinase pathway. Genesis 2013; 51(3): 147-62.
[http://dx.doi.org/10.1002/dvg.22354]
[130]
Pimenta de Castro I, Costa AC, Lam D, et al. Genetic analysis of mitochondrial protein misfolding in Drosophila melanogaster. Cell Death Differ 2012; 19(8): 1308-16.
[http://dx.doi.org/10.1038/cdd.2012.5] [PMID: 22301916]
[131]
Kaplan Algin A, Tomruk C, Gözde Aslan Ç, et al. Effects of ozone treatment to the levels of neurodegeneration biomarkers after rotenone induced rat model of Parkinson’s disease. Neurosci Lett 2023; 814: 137448.
[http://dx.doi.org/10.1016/j.neulet.2023.137448] [PMID: 37597740]
[132]
Deepika NP, Rahman MH, Chipurupalli S, Shilpa TN, Duraiswamy B. The emerging role of marine natural products for the treatment of parkinson’s disease. CNS Neurol Disord Drug Targets 2023; 22(6): 801-16.
[http://dx.doi.org/10.2174/1871527321666220511205231] [PMID: 35546747]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy