Generic placeholder image

CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Review Article

Modeling Parkinson’s Disease in Zebrafish

Author(s): Nor H.M. Najib, Yong H. Nies, Syarifah A.S. Abd Halim, Mohamad F. Yahaya, Srijit Das, Wei L. Lim and Seong L. Teoh*

Volume 19, Issue 5, 2020

Page: [386 - 399] Pages: 14

DOI: 10.2174/1871527319666200708124117

Price: $65

Abstract

Parkinson’s Disease (PD) is one of the most common neurodegenerative disorders that affects the motor system, and includes cardinal motor symptoms such as resting tremor, cogwheel rigidity, bradykinesia and postural instability. Its prevalence is increasing worldwide due to the increase in life span. Although, two centuries since the first description of the disease, no proper cure with regard to treatment strategies and control of symptoms could be reached. One of the major challenges faced by the researchers is to have a suitable research model. Rodents are the most common PD models used, but no single model can replicate the true nature of PD. In this review, we aim to discuss another animal model, the zebrafish (Danio rerio), which is gaining popularity. Zebrafish brain has all the major structures found in the mammalian brain, with neurotransmitter systems, and it also possesses a functional blood-brain barrier similar to humans. From the perspective of PD research, the zebrafish possesses the ventral diencephalon, which is thought to be homologous to the mammalian substantia nigra. We summarize the various zebrafish models available to study PD, namely chemical-induced and genetic models. The zebrafish can complement the use of other animal models for the mechanistic study of PD and help in the screening of new potential therapeutic compounds.

Keywords: Neurodegenerative disease, disease models, neurotoxins, transgenic, Danio rerio, Parkinson’s Disease (PD).

« Previous
Graphical Abstract

[1]
Poewe W, Seppi K, Tanner CM, et al. Parkinson disease. Nat Rev Dis Primers 2017; 3: 17013.
[http://dx.doi.org/10.1038/nrdp.2017.13] [PMID: 28332488]
[2]
Parkinson J. An essay on the shaking palsy. J Neuropsychiatry Clin Neurosci 2002; 14(2): 223-36.
[http://dx.doi.org/10.1176/jnp.14.2.223] [PMID: 11983801]
[3]
McDonald C, Gordon G, Hand A, Walker RW, Fisher JM. 200 Years of Parkinson’s disease: What have we learnt from James Parkinson? Age Ageing 2018; 47(2): 209-14.
[http://dx.doi.org/10.1093/ageing/afx196] [PMID: 29315364]
[4]
DeMaagd G, Philip A. Parkinson’s disease and its management: Part 1: Disease entity, risk factors, pathophysiology, clinical presentation, and diagnosis. P&T 2015; 40(8): 504-32.
[PMID: 26236139]
[5]
Marques de Sousa S, Massano J. Motor complications in Parkinson’s disease: A comprehensive review of emergent management strategies. CNS Neurol Disord Drug Targets 2013; 12(7): 1017-49.
[http://dx.doi.org/10.2174/18715273113129990086] [PMID: 23844692]
[6]
Pfeiffer RF. Non-motor symptoms in Parkinson’s disease. Parkinsonism Relat Disord 2016; 22(Suppl. 1): S119-22.
[http://dx.doi.org/10.1016/j.parkreldis.2015.09.004] [PMID: 26372623]
[7]
Weerkamp NJ, Tissingh G, Poels PJ, et al. Nonmotor symptoms in nursing home residents with Parkinson’s disease: Prevalence and effect on quality of life. J Am Geriatr Soc 2013; 61(10): 1714-21.
[http://dx.doi.org/10.1111/jgs.12458] [PMID: 24117286]
[8]
Azmin S, Khairul AAM, Tan HJ, et al. Nonmotor symptoms in a malaysian Parkinson’s disease population. Parkinsons Dis 2014; 2014472157
[http://dx.doi.org/10.1155/2014/472157] [PMID: 24800102]
[9]
GBD 2015 Neurological Disorders Collaborator Group. Global, regional, and national burden of neurological disorders during 1990-2015: A systematic analysis for the Global Burden of Disease Study 2015. Lancet Neurol 2017; 16(11): 877-97.
[http://dx.doi.org/10.1016/S1474-4422(17)30299-5] [PMID: 28931491]
[10]
GBD 2016 Parkinson’s Disease Collaborators. Global, regional, and national burden of Parkinson’s disease, 1990-2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 2018; 17(11): 939-53.
[http://dx.doi.org/10.1016/S1474-4422(18)30295-3] [PMID: 30287051]
[11]
Dehay B, Bourdenx M, Gorry P, et al. Targeting α-synuclein for treatment of Parkinson’s disease: Mechanistic and therapeutic considerations. Lancet Neurol 2015; 14(8): 855-66.
[http://dx.doi.org/10.1016/S1474-4422(15)00006-X] [PMID: 26050140]
[12]
Savica R, Grossardt BR, Bower JH, et al. Survival and causes of death among people with clinically diagnosed synucleinopathies with parkinsonism: A population-based study. JAMA Neurol 2017; 74(7): 839-46.
[http://dx.doi.org/10.1001/jamaneurol.2017.0603] [PMID: 28505261]
[13]
Darweesh SKL, Raphael KG, Brundin P, et al. Parkinson Matters. J Parkinsons Dis 2018; 8(4): 495-8.
[http://dx.doi.org/10.3233/JPD-181374] [PMID: 30149463]
[14]
Cicchetti F, David LS, Siddu A, Denis HL. Cysteamine as a novel disease-modifying compound for Parkinson’s disease: Over a decade of research supporting a clinical trial. Neurobiol Dis 2019; 130104530
[http://dx.doi.org/10.1016/j.nbd.2019.104530] [PMID: 31301344]
[15]
Li B, Jiang Y, Xu Y, Li Y, Li B. Identification of miRNA-7 as a regulator of brain-derived neurotrophic factor/α-synuclein axis in atrazine-induced Parkinson’s disease by peripheral blood and brain microRNA profiling. Chemosphere 2019; 233: 542-8.
[http://dx.doi.org/10.1016/j.chemosphere.2019.05.064] [PMID: 31185338]
[16]
Gad ESA, Ghanem AA, Abdelghaffar H, El Dakroury S, Salama MM. Parkinson’s disease: Is it a toxic syndrome? Neurol Res Int 2010; 2010103094
[http://dx.doi.org/10.1155/2010/103094] [PMID: 21152209]
[17]
Deng H, Wang P, Jankovic J. The genetics of Parkinson disease. Ageing Res Rev 2018; 42: 72-85.
[http://dx.doi.org/10.1016/j.arr.2017.12.007] [PMID: 29288112]
[18]
Bekris LM, Mata IF, Zabetian CP. The genetics of Parkinson disease. J Geriatr Psychiatry Neurol 2010; 23(4): 228-42.
[http://dx.doi.org/10.1177/0891988710383572] [PMID: 20938043]
[19]
Abdel-Salam OM. The paths to neurodegeneration in genetic Parkinson’s disease. CNS Neurol Disord Drug Targets 2014; 13(9): 1485-512.
[http://dx.doi.org/10.2174/1871527313666140806142955] [PMID: 25106632]
[20]
Mastrangelo L. The genetics of Parkinson disease. Adv Genet 2017; 98: 43-62.
[http://dx.doi.org/10.1016/bs.adgen.2017.08.001] [PMID: 28942794]
[21]
Dave KD, De Silva S, Sheth NP, et al. Phenotypic characterization of recessive gene knockout rat models of Parkinson’s disease. Neurobiol Dis 2014; 70: 190-203.
[http://dx.doi.org/10.1016/j.nbd.2014.06.009] [PMID: 24969022]
[22]
Chen H, Ritz B. The search for environmental causes of Parkinson’s disease: Moving forward. J Parkinsons Dis 2018; 8(s1): S9-S17.
[http://dx.doi.org/10.3233/JPD-181493] [PMID: 30584168]
[23]
Pezzoli G, Cereda E. Exposure to pesticides or solvents and risk of Parkinson disease. Neurology 2013; 80(22): 2035-41.
[http://dx.doi.org/10.1212/WNL.0b013e318294b3c8] [PMID: 23713084]
[24]
Elbaz A, Carcaillon L, Kab S, Moisan F. Epidemiology of Parkinson’s disease. Rev Neurol 2016; 172(1): 14-26.
[http://dx.doi.org/10.1016/j.neurol.2015.09.012] [PMID: 26718594]
[25]
Yaribeygi H, Panahi Y, Javadi B, Sahebkar A. The underlying role of oxidative stress in neurodegeneration: A mechanistic review. CNS Neurol Disord Drug Targets 2018; 17(3): 207-15.
[http://dx.doi.org/10.2174/1871527317666180425122557] [PMID: 29692267]
[26]
Mule NK, Singh JN. Diabetes mellitus to neurodegenerative disorders: Is oxidative stress fueling the flame? CNS Neurol Disord Drug Targets 2018; 17(9): 644-53.
[http://dx.doi.org/10.2174/1871527317666180809092359] [PMID: 30091419]
[27]
Modi P, Mohamad A, Phom L, et al. Understanding pathophysiology of sporadic Parkinson’s disease in Drosophila model: Potential opportunities and notable limitations Challenges in Parkinson’s disease. Croatia: Ed. In Tech 2016; pp. 217-44.
[http://dx.doi.org/10.5772/63767]
[28]
Chung SY, Kishinevsky S, Mazzulli JR, et al. Parkin and PINK1 patient iPSC-derived midbrain dopamine neurons exhibit mitochondrial dysfunction and a-synuclein accumulation. Stem Cell Reports 2016; 7(4): 664-77.
[http://dx.doi.org/10.1016/j.stemcr.2016.08.012] [PMID: 27641647]
[29]
Hirsch EC, Jenner P, Przedborski S. Pathogenesis of Parkinson’s disease. Mov Disord 2013; 28(1): 24-30.
[http://dx.doi.org/10.1002/mds.25032] [PMID: 22927094]
[30]
Kumar A, Dhawan A, Kadam A, Shinde A. Autophagy and mitochondria: Targets in neurodegenerative disorders. CNS Neurol Disord Drug Targets 2018; 17(9): 696-705.
[http://dx.doi.org/10.2174/1871527317666180816100203] [PMID: 30113005]
[31]
Chai C, Lim KL. Genetic insights into sporadic Parkinson’s disease pathogenesis. Curr Genomics 2013; 14(8): 486-501.
[http://dx.doi.org/10.2174/1389202914666131210195808] [PMID: 24532982]
[32]
Tan JM, Wong ES, Lim KL. Protein misfolding and aggregation in Parkinson’s disease. Antioxid Redox Signal 2009; 11(9): 2119-34.
[http://dx.doi.org/10.1089/ars.2009.2490] [PMID: 19243238]
[33]
Goedert M, Jakes R, Spillantini MG. The synucleinopathies: Twenty years on. J Parkinsons Dis 2017; 7(s1): S51-69.
[http://dx.doi.org/10.3233/JPD-179005] [PMID: 28282814]
[34]
Davis AA, Andruska KM, Benitez BA, Racette BA, Perlmutter JS, Cruchaga C. Variants in GBA, SNCA, and MAPT influence Parkinson disease risk, age at onset, and progression. Neurobiol Aging 2016; 37: 209.
[35]
Pihlstrøm L, Blauwendraat C, Cappelletti C, et al. International Parkinson disease genomics consortium; North American brain expression consortium. A comprehensive analysis of SNCA-related genetic risk in sporadic parkinson disease. Ann Neurol 2018; 84(1): 117-29.
[http://dx.doi.org/10.1002/ana.25274] [PMID: 30146727]
[36]
Cooper CA, Jain N, Gallagher MD, et al. Common variant rs356182 near SNCA defines a Parkinson’s disease endophenotype. Ann Clin Transl Neurol 2016; 4(1): 15-25.
[http://dx.doi.org/10.1002/acn3.371] [PMID: 28078311]
[37]
Deas E, Cremades N, Angelova PR, et al. Alpha-synuclein oligomers interact with metal ions to induce oxidative stress and neuronal death in Parkinson’s disease. Antioxid Redox Signal 2016; 24(7): 376-91.
[http://dx.doi.org/10.1089/ars.2015.6343] [PMID: 26564470]
[38]
Terada T, Yokokura M, Yoshikawa E, et al. Extrastriatal spreading of microglial activation in Parkinson’s disease: A positron emission tomography study. Ann Nucl Med 2016; 30(8): 579-87.
[http://dx.doi.org/10.1007/s12149-016-1099-2] [PMID: 27299437]
[39]
Ouchi Y, Yoshikawa E, Sekine Y, et al. Microglial activation and dopamine terminal loss in early Parkinson’s disease. Ann Neurol 2005; 57(2): 168-75.
[http://dx.doi.org/10.1002/ana.20338] [PMID: 15668962]
[40]
Macchi B, Di Paola R, Marino-Merlo F, Felice MR, Cuzzocrea S, Mastino A. Inflammatory and cell death pathways in brain and peripheral blood in Parkinson’s disease. CNS Neurol Disord Drug Targets 2015; 14(3): 313-24.
[http://dx.doi.org/10.2174/1871527314666150225124928] [PMID: 25714978]
[41]
Venkateshappa C, Harish G, Mythri RB, Mahadevan A, Bharath MM, Shankar SK. Increased oxidative damage and decreased antioxidant function in aging human substantia nigra compared to striatum: Implications for Parkinson’s disease. Neurochem Res 2012; 37(2): 358-69.
[http://dx.doi.org/10.1007/s11064-011-0619-7] [PMID: 21971758]
[42]
Ikawa M, Okazawa H, Kudo T, Kuriyama M, Fujibayashi Y, Yoneda M. Evaluation of striatal oxidative stress in patients with Parkinson’s disease using [62Cu]ATSM PET. Nucl Med Biol 2011; 38(7): 945-51.
[http://dx.doi.org/10.1016/j.nucmedbio.2011.02.016] [PMID: 21982566]
[43]
Blandini F, Armentero MT. Animal models of Parkinson’s disease. FEBS J 2012; 279(7): 1156-66.
[http://dx.doi.org/10.1111/j.1742-4658.2012.08491.x] [PMID: 22251459]
[44]
Patil DA, Patil VA, Bari SB, Surana SJ, Patil PO. Animal models for Parkinson’s disease. CNS Neurol Disord Drug Targets 2014; 13(9): 1580-94.
[http://dx.doi.org/10.2174/1871527313666140806144425] [PMID: 25106631]
[45]
Fatima A, Jyoti S, Siddique YH. Models of Parkinson’s disease with special emphasis on Drosophila melanogaster. CNS Neurol Disord Drug Targets 2018; 17(10): 757-66.
[http://dx.doi.org/10.2174/1871527317666180820164250] [PMID: 30129420]
[46]
Bombardi DAC, Santana MG, di Camilo OG, de Oliveira CTP, Priolli DG. Literature evidence and ARRIVE assessment on neuroprotective effects of flavonols in neurodegenerative diseases’ models. CNS Neurol Disord Drug Targets 2018; 17(1): 34-42.
[http://dx.doi.org/10.2174/1871527317666171221110139] [PMID: 29268692]
[47]
Javed H, Kamal MA, Ojha S. An overview on the role of a-synuclein in experimental models of Parkinson’s disease from pathogenesis to therapeutics. CNS Neurol Disord Drug Targets 2016; 15(10): 1240-52.
[http://dx.doi.org/10.2174/1871527315666160920160512] [PMID: 27658511]
[48]
Lawrence C. The husbandry of zebrafish (Danio rerio): A review. Aquaculture 2007; 269: 1-20.
[http://dx.doi.org/10.1016/j.aquaculture.2007.04.077]
[49]
Singh AP, Nüsslein-Volhard C. Zebrafish stripes as a model for vertebrate colour pattern formation. Curr Biol 2015; 25(2): R81-92.
[http://dx.doi.org/10.1016/j.cub.2014.11.013] [PMID: 25602311]
[50]
Stewart AM, Braubach O, Spitsbergen J, Gerlai R, Kalueff AV. Zebrafish models for translational neuroscience research: From tank to bedside. Trends Neurosci 2014; 37(5): 264-78.
[http://dx.doi.org/10.1016/j.tins.2014.02.011] [PMID: 24726051]
[51]
Kalueff AV, Echevarria DJ, Stewart AM. Gaining translational momentum: More zebrafish models for neuroscience research. Prog Neuropsychopharmacol Biol Psychiatry 2014; 55: 1-6.
[http://dx.doi.org/10.1016/j.pnpbp.2014.01.022] [PMID: 24593944]
[52]
Howe K, Clark MD, Torroja CF, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496(7446): 498-503.
[http://dx.doi.org/10.1038/nature12111] [PMID: 23594743]
[53]
Gerhard GS, Kauffman EJ, Wang X, et al. Life spans and senescent phenotypes in two strains of Zebrafish (Danio rerio). Exp Gerontol 2002; 37(8-9): 1055-68.
[http://dx.doi.org/10.1016/S0531-5565(02)00088-8] [PMID: 12213556]
[54]
Westerfield M. The zebrafish book: A guide for the laboratory use of zebrafish (Danio rerio). 4th Edition ed. Eugene: University of Oregon Press 2000
[55]
Panula P, Chen YC, Priyadarshini M, et al. The comparative neuroanatomy and neurochemistry of zebrafish CNS systems of relevance to human neuropsychiatric diseases. Neurobiol Dis 2010; 40(1): 46-57.
[http://dx.doi.org/10.1016/j.nbd.2010.05.010] [PMID: 20472064]
[56]
Kim SS, Im SH, Yang JY, et al. Zebrafish as a screening model for testing the permeability of blood-brain barrier to small molecules. Zebrafish 2017; 14(4): 322-30.
[http://dx.doi.org/10.1089/zeb.2016.1392] [PMID: 28488933]
[57]
Du Y, Guo Q, Shan M, et al. Spatial and temporal distribution of dopaminergic neurons during development in zebrafish. Front Neuroanat 2016; 10: 115.
[http://dx.doi.org/10.3389/fnana.2016.00115] [PMID: 27965546]
[58]
Zhu Y, Zhang J, Zeng Y. Overview of tyrosine hydroxylase in Parkinson’s disease. CNS Neurol Disord Drug Targets 2012; 11(4): 350-8.
[http://dx.doi.org/10.2174/187152712800792901] [PMID: 22483316]
[59]
Chen YC, Priyadarshini M, Panula P. Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem Cell Biol 2009; 132(4): 375-81.
[http://dx.doi.org/10.1007/s00418-009-0619-8] [PMID: 19603179]
[60]
Yamamoto K, Ruuskanen JO, Wullimann MF, Vernier P. Two tyrosine hydroxylase genes in vertebrates new dopaminergic territories revealed in the zebrafish brain. Mol Cell Neurosci 2010; 43(4): 394-402.
[http://dx.doi.org/10.1016/j.mcn.2010.01.006] [PMID: 20123022]
[61]
Ek F, Malo M, Åberg AM, et al. Behavioral analysis of dopaminergic activation in zebrafish and rats reveals similar phenotypes. ACS Chem Neurosci 2016; 7(5): 633-46.
[http://dx.doi.org/10.1021/acschemneuro.6b00014] [PMID: 26947759]
[62]
Olmedo-Díaz S, Estévez-Silva H, Orädd G, Bjerkén AFS, Marcellino D, Virel A. An altered blood-brain barrier contributes to brain iron accumulation and neuroinflammation in the 6-OHDA rat model of Parkinson’s disease. Neuroscience 2017; 362: 141-51.
[http://dx.doi.org/10.1016/j.neuroscience.2017.08.023] [PMID: 28842186]
[63]
Ren M, Han M, Wei X, et al. FTY720 attenuates 6-OHDA-associated dopaminergic degeneration in cellular and mouse Parkinsonian models. Neurochem Res 2017; 42(2): 686-96.
[http://dx.doi.org/10.1007/s11064-016-2125-4] [PMID: 27943027]
[64]
Vijayanathan Y, Lim FT, Lim SM, et al. 6-OHDA-lesioned adult zebrafish as a useful Parkinson’s disease model for dopaminergic neuroregeneration. Neurotox Res 2017; 32(3): 496-508.
[http://dx.doi.org/10.1007/s12640-017-9778-x] [PMID: 28707266]
[65]
Anichtchik OV, Kaslin J, Peitsaro N, Scheinin M, Panula P. Neurochemical and behavioural changes in zebrafish Danio rerio after systemic administration of 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J Neurochem 2004; 88(2): 443-53.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02190.x] [PMID: 14690532]
[66]
Feng CW, Wen ZH, Huang SY, et al. Effects of 6-hydroxy-dopamine exposure on motor activity and biochemical expression in zebrafish (Danio rerio) larvae. Zebrafish 2014; 11(3): 227-39.
[http://dx.doi.org/10.1089/zeb.2013.0950] [PMID: 24720843]
[67]
Benvenutti R, Marcon M, Reis CG, et al. N-acetylcysteine protects against motor, optomotor and morphological deficits induced by 6-OHDA in zebrafish larvae. PeerJ 2018; 6e4957
[http://dx.doi.org/10.7717/peerj.4957] [PMID: 29868300]
[68]
Li M, Zhou F, Xu T, Song H, Lu B. Acteoside protects against 6-OHDA-induced dopaminergic neuron damage via Nrf2-ARE signaling pathway. Food Chem Toxicol 2018; 119: 6-13.
[http://dx.doi.org/10.1016/j.fct.2018.06.018] [PMID: 29906474]
[69]
Wang M, Zhang Z, Cheang LC, Lin Z, Lee SM. Eriocaulon buergerianum extract protects PC12 cells and neurons in zebrafish against 6-hydroxydopamine-induced damage. Chin Med 2011; 6: 16.
[http://dx.doi.org/10.1186/1749-8546-6-16] [PMID: 21527031]
[70]
Zhang LQ, Sa F, Chong CM, et al. Schisantherin A protects against 6-OHDA-induced dopaminergic neuron damage in zebrafish and cytotoxicity in SH-SY5Y cells through the ROS/NO and AKT/GSK3β pathways. J Ethnopharmacol 2015; 170: 8-15.
[http://dx.doi.org/10.1016/j.jep.2015.04.040] [PMID: 25934514]
[71]
Cronin A, Grealy M. Neuroprotective and neuro-restorative effects of minocycline and rasagiline in a zebrafish 6-hydroxydopamine model of Parkinson’s disease. Neuroscience 2017; 367: 34-46.
[http://dx.doi.org/10.1016/j.neuroscience.2017.10.018] [PMID: 29079063]
[72]
Langston JW. The MPTP story. J Parkinsons Dis 2017; 7: S11-9.
[http://dx.doi.org/10.3233/JPD-179006]
[73]
Ballard PA, Tetrud JW, Langston JW. Permanent human parkinsonism due to 1‐methy 1-4‐phenyl‐1, 2, 3, 6‐tetrahydropyridine (MPTP): Seven cases. Neurology 1985; 35: 949.
[74]
Langston JW, Ballard P, Tetrud JW, Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis 1983; 219: 979-80.
[http://dx.doi.org/10.1126/science.6823561]
[75]
Ramsay RR, Dadgar J, Trevor A, Singer TP. Energy-driven uptake of N-methyl-4-phenylpyridine by brain mitochondria mediates the neurotoxicity of MPTP. Life Sci 1986; 39: 581-8.
[http://dx.doi.org/10.1016/0024-3205(86)90037-8]
[76]
Colpo GD, Ribeiro FM, Rocha NP, Teixeira AL. Study of Human Disease Animal Models for the Study of Human Neurodegenerative DiseasesAnimal Models for the Study of Human Disease. Elsevier 2017; pp. 1109-29.
[http://dx.doi.org/10.1016/B978-0-12-809468-6.00042-5]
[77]
Javitch JA, D’Amato RJ, Strittmatter SM, Snyder SH. Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-1, 2, 3, 6-tetrahydro-pyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. Proc Natl Acad Sci USA 1985; 82: 2173-7.
[78]
Speciale SG. MPTP: Insights into parkinsonian neurodegeneration. Neurotoxicol Teratol 2002; 24: 607-20.
[79]
Przedborski S, Jackson-Lewis V. Mechanisms of MPTP toxicity. Mov Disord 1998; 13: 35-8.
[80]
Dutta D, Kundu M, Mondal S, et al. RANTES-induced invasion of Th17 cells into substantia nigra potentiates dopaminergic cell loss in MPTP mouse model of Parkinson’s disease. Neurobiol Dis 2019; 132104575
[http://dx.doi.org/10.1016/j.nbd.2019.104575] [PMID: 31445159]
[81]
Zheng M, Liu C, Fan Y, Yan P, Shi D, Zhang Y. Neuroprotection by Paeoniflorin in the MPTP mouse model of Parkinson’s disease. Neuropharmacology 2017; 116: 412-20.
[http://dx.doi.org/10.1016/j.neuropharm.2017.01.009] [PMID: 28093210]
[82]
Chen X, Liu Z, Cao BB, Qiu YH, Peng YP. TGF-b1 neuroprotection via inhibition of microglial activation in a rat model of Parkinson’s disease. J Neuroimmune Pharmacol 2017; 12(3): 433-46.
[http://dx.doi.org/10.1007/s11481-017-9732-y] [PMID: 28429275]
[83]
Sarath BN, Murthy CHL, Kakara S, Sharma R, Brahmendra SCV, Idris MM. 1-Methyl-4-phenyl-1,2,3,6-tetrahydro-pyridine induced Parkinson’s disease in zebrafish. Proteomics 2016; 16(9): 1407-20.
[http://dx.doi.org/10.1002/pmic.201500291] [PMID: 26959078]
[84]
Nellore J, Pauline C, Amarnath K. Bacopa monnieri phytochemicals mediated synthesis of platinum nanoparticles and its neurorescue effect on 1-methyl 4-phenyl 1,2,3,6 tetrahydropyridine-induced experimental Parkinsonism in zebrafish. J Neurodegener Dis 2013; 2013972391
[http://dx.doi.org/10.1155/2013/972391] [PMID: 26317003]
[85]
Sallinen V, Torkko V, Sundvik M, et al. MPTP and MPP+ target specific aminergic cell populations in larval zebrafish. J Neurochem 2009; 108(3): 719-31.
[http://dx.doi.org/10.1111/j.1471-4159.2008.05793.x] [PMID: 19046410]
[86]
Liu JC, Koppula S, Huh SJ, et al. Necrosis inhibitor-5 (NecroX-5), attenuates MPTP-induced motor deficits in a zebrafish model of Parkinson’s disease. Genes Genomics 2015; 37: 1073-9.
[http://dx.doi.org/10.1007/s13258-015-0364-4]
[87]
Chong CM, Ma D, Zhao C, et al. Discovery of a novel neuroprotectant, BHDPC, that protects against MPP+/MPTP-induced neuronal death in multiple experimental models. Free Radic Biol Med 2015; 89: 1057-66.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.08.013] [PMID: 26415025]
[88]
Yao L, Peng SX, Xu YD, et al. Unexpected neuroprotective effects of loganin on 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity and cell death in zebrafish. J Cell Biochem 2017; 118(3): 615-28.
[http://dx.doi.org/10.1002/jcb.25749] [PMID: 27662601]
[89]
Pinho BR, Reis SD, Guedes-Dias P, et al. Pharmacological modulation of HDAC1 and HDAC6 in vivo in a zebrafish model: Therapeutic implications for Parkinson’s disease. Pharmacol Res 2016; 103: 328-39.
[http://dx.doi.org/10.1016/j.phrs.2015.11.024] [PMID: 26657418]
[90]
Huang CL, Chao CC, Lee YC, et al. Paraquat induces cell death through impairing mitochondrial membrane permeability. Mol Neurobiol 2016; 53(4): 2169-88.
[http://dx.doi.org/10.1007/s12035-015-9198-y] [PMID: 25947082]
[91]
Cristóvão AC, Campos FL, Je G, et al. Characterization of a Parkinson’s disease rat model using an upgraded paraquat exposure paradigm. Eur J Neurosci 2020; 52(4): 3242-55.
[http://dx.doi.org/10.1111/ejn.14683] [PMID: 31958881]
[92]
Manning-Bog AB, McCormack AL, Purisai MG, Bolin LM, Di Monte DA. Alpha-synuclein overexpression protects against paraquat-induced neurodegeneration. J Neurosci 2003; 23(8): 3095-9.
[http://dx.doi.org/10.1523/JNEUROSCI.23-08-03095.2003] [PMID: 12716914]
[93]
Niso-Santano M, González-Polo RA, Bravo-San PJM, et al. Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED). Activation of apoptosis signal-regulating kinase 1 is a key factor in paraquat-induced cell death: modulation by the Nrf2/Trx axis. Free Radic Biol Med 2010; 48(10): 1370-81.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.02.024] [PMID: 20202476]
[94]
Bortolotto JW, Cognato GP, Christoff RR, et al. Long-term exposure to paraquat alters behavioral parameters and dopamine levels in adult zebrafish (Danio rerio). Zebrafish 2014; 11(2): 142-53.
[http://dx.doi.org/10.1089/zeb.2013.0923] [PMID: 24568596]
[95]
Nellore JPN. Paraquat exposure induces behavioral deficits in larval zebrafish during the window of dopamine neurogenesis. Toxicol Rep 2015; 2: 950-6.
[http://dx.doi.org/10.1016/j.toxrep.2015.06.007] [PMID: 28962434]
[96]
Müller TE, Nunes ME, Menezes CC, et al. Sodium selenite prevents paraquat-induced neurotoxicity in zebrafish. Mol Neurobiol 2018; 55(3): 1928-41.
[http://dx.doi.org/10.1007/s12035-017-0441-6] [PMID: 28244005]
[97]
Wang XH, Souders CL, Zhao YH, Martyniuk CJ. Paraquat affects mitochondrial bioenergetics, dopamine system expression, and locomotor activity in zebrafish (Danio rerio). Chemosphere 2018; 191: 106-17.
[http://dx.doi.org/10.1016/j.chemosphere.2017.10.032] [PMID: 29031050]
[98]
Bretaud S, Lee S, Guo S. Sensitivity of zebrafish to environmental toxins implicated in Parkinson’s disease. Neurotoxicol Teratol 2004; 26(6): 857-64.
[http://dx.doi.org/10.1016/j.ntt.2004.06.014] [PMID: 15451049]
[99]
Nunes ME, Muller TE, Braga MM, et al. Chronic treatment with paraquat induces brain injury, changes in antioxidant defenses system, and modulates behavioral functions in zebrafish. Mol Neurobiol 2017; 54(6): 3925-34.
[http://dx.doi.org/10.1007/s12035-016-9919-x] [PMID: 27229491]
[100]
Horst CH, Schlemmer F, de Aguiar MN, et al. Signature of aberrantly expressed microRNAs in the striatum of rotenone-induced Parkinsonian rats. Neurochem Res 2018; 43(11): 2132-40.
[http://dx.doi.org/10.1007/s11064-018-2638-0] [PMID: 30267378]
[101]
Khotimah H, Sumitro SB, Aris WM. Zebrafish Parkinson’s model: Rotenone decrease motility, dopamine, and increase α-synuclein aggregation and apoptosis of zebrafish brain. Int J Pharm Tech Res 2015; 8: 614-21.
[102]
Abdul wahid AI, Ahmad KH. Environmental toxins and Parkinson’s disease: Putative roles of impaired electron transport chain and oxidative stress. Toxicol Ind Health 2010; 26(2): 121-8.
[http://dx.doi.org/10.1177/0748233710362382] [PMID: 20207656]
[103]
Jiang X, Tang PC, Chen Q, et al. Cordycepin exerts neuroprotective effects via an anti-apoptotic mechanism based on the mitochondrial pathway in a rotenone-induced parkinsonism rat model. CNS Neurol Disord Drug Targets 2019; 18(8): 609-20.
[http://dx.doi.org/10.2174/1871527318666190905152138] [PMID: 31486758]
[104]
Askar MH, Hussein AM, Al-Basiony SF, et al. Effects of exercise and ferulic acid on alpha synuclein and neuroprotective heat shock protein 70 in an experimental model of Parkinsonism disease. CNS Neurol Disord Drug Targets 2019; 18(2): 156-69.
[http://dx.doi.org/10.2174/1871527317666180816095707] [PMID: 30113007]
[105]
Tapias V, McCoy JL, Greenamyre JT. Phenothiazine normalizes the NADH/NAD+ ratio, maintains mitochondrial integrity and protects the nigrostriatal dopamine system in a chronic rotenone model of Parkinson’s disease. Redox Biol 2019; 24101164
[http://dx.doi.org/10.1016/j.redox.2019.101164] [PMID: 30925294]
[106]
Wang Y, Liu W, Yang J, et al. Parkinson’s disease-like motor and non-motor symptoms in rotenone-treated zebrafish. Neurotoxicology 2017; 58: 103-9.
[http://dx.doi.org/10.1016/j.neuro.2016.11.006] [PMID: 27866991]
[107]
Martel S, Keow JY, Ekker M. Rotenone neurotoxicity causes dopamine neuron loss in zebrafish. Univ Ottawa J Med 2015; 5: 16-21.
[http://dx.doi.org/10.18192/uojm.v5i2.1413]
[108]
Melo KM, Oliveira R, Grisolia CK, et al. Short-term exposure to low doses of rotenone induces developmental, biochemical, behavioral, and histological changes in fish. Environ Sci Pollut Res Int 2015; 22(18): 13926-38.
[http://dx.doi.org/10.1007/s11356-015-4596-2] [PMID: 25948382]
[109]
Khotimah H, Darwitri D, Yuliyani T, et al. Centella asiatica increased the body length through the modulation of antioxidant in rotenone-induced zebrafish larvae. Biomed Pharmacol J 2018; 11: 827-33.
[http://dx.doi.org/10.13005/bpj/1438]
[110]
Nasevicius A, Ekker SC. Effective targeted gene ‘knockdown’ in zebrafish. Nat Genet 2000; 26(2): 216-20.
[http://dx.doi.org/10.1038/79951] [PMID: 11017081]
[111]
Hwang WY, Fu Y, Reyon D, et al. Heritable and precise zebrafish genome editing using a CRISPR-Cas system. PLoS One 2013; 8(7)e68708
[http://dx.doi.org/10.1371/journal.pone.0068708] [PMID: 23874735]
[112]
Pinto M, Nissanka N, Moraes CT. Lack of Parkin anticipates the phenotype and affects mitochondrial morphology and mtDNA levels in a mouse model of Parkinson’s disease. J Neurosci 2018; 38(4): 1042-53.
[http://dx.doi.org/10.1523/JNEUROSCI.1384-17.2017] [PMID: 29222404]
[113]
Noda S, Sato S, Fukuda T, et al. Loss of Parkin contributes to mitochondrial turnover and dopaminergic neuronal loss in aged mice. Neurobiol Dis 2020; 136104717
[http://dx.doi.org/10.1016/j.nbd.2019.104717] [PMID: 31846738]
[114]
Fett ME, Pilsl A, Paquet D, et al. Parkin is protective against proteotoxic stress in a transgenic zebrafish model. PLoS One 2010; 5(7)e11783
[http://dx.doi.org/10.1371/journal.pone.0011783] [PMID: 20689587]
[115]
Maynard ME, Redell JB, Kobori N, et al. Loss of PTEN-induced kinase 1 (Pink1) reduces hippocampal tyrosine hydroxylase and impairs learning and memory. Exp Neurol 2020; 323113081
[http://dx.doi.org/10.1016/j.expneurol.2019.113081] [PMID: 31655049]
[116]
Kelm-Nelson CA, Brauer AFL, Barth KJ, et al. Characterization of early-onset motor deficits in the Pink1-/- mouse model of Parkinson disease. Brain Res 2018; 1680: 1-12.
[http://dx.doi.org/10.1016/j.brainres.2017.12.002] [PMID: 29229503]
[117]
Priyadarshini M, Orosco LA, Panula PJ. Oxidative stress and regulation of Pink1 in zebrafish (Danio rerio). PLoS One 2013; 8(11)e81851
[http://dx.doi.org/10.1371/journal.pone.0081851] [PMID: 24324558]
[118]
Sallinen V, Kolehmainen J, Priyadarshini M, Toleikyte G, Chen YC, Panula P. Dopaminergic cell damage and vulnerability to MPTP in Pink1 knockdown zebrafish. Neurobiol Dis 2010; 40(1): 93-101.
[http://dx.doi.org/10.1016/j.nbd.2010.06.001] [PMID: 20600915]
[119]
Xi Y, Ryan J, Noble S, Yu M, Yilbas AE, Ekker M. Impaired dopaminergic neuron development and locomotor function in zebrafish with loss of pink1 function. Eur J Neurosci 2010; 31(4): 623-33.
[http://dx.doi.org/10.1111/j.1460-9568.2010.07091.x] [PMID: 20141529]
[120]
Flinn LJ, Keatinge M, Bretaud S, et al. TigarB causes mitochondrial dysfunction and neuronal loss in PINK1 deficiency. Ann Neurol 2013; 74(6): 837-47.
[http://dx.doi.org/10.1002/ana.23999] [PMID: 24027110]
[121]
Soman S, Keatinge M, Moein M, et al. Inhibition of the mitochondrial calcium uniporter rescues dopaminergic neurons in pink1-/- zebrafish. Eur J Neurosci 2017; 45(4): 528-35.
[http://dx.doi.org/10.1111/ejn.13473] [PMID: 27859782]
[122]
Dolgacheva LP, Berezhnov AV, Fedotova EI, Zinchenko VP, Abramov AY. Role of DJ-1 in the mechanism of pathogenesis of Parkinson’s disease. J Bioenerg Biomembr 2019; 51(3): 175-88.
[http://dx.doi.org/10.1007/s10863-019-09798-4] [PMID: 31054074]
[123]
Pham TT, Giesert F, Röthig A, et al. DJ-1-deficient mice show less TH-positive neurons in the ventral tegmental area and exhibit non-motoric behavioural impairments. Genes Brain Behav 2010; 9(3): 305-17.
[http://dx.doi.org/10.1111/j.1601-183X.2009.00559.x] [PMID: 20039949]
[124]
Giangrasso DM, Furlong TM, Keefe KA. Characterization of striatum-mediated behavior and neurochemistry in the DJ-1 knock-out rat model of Parkinson’s disease. Neurobiol Dis 2020; 134104673
[http://dx.doi.org/10.1016/j.nbd.2019.104673] [PMID: 31734455]
[125]
Bai Q, Mullett SJ, Garver JA, Hinkle DA, Burton EA. Zebrafish DJ-1 is evolutionarily conserved and expressed in dopaminergic neurons. Brain Res 2006; 1113(1): 33-44.
[http://dx.doi.org/10.1016/j.brainres.2006.07.057] [PMID: 16942755]
[126]
Bretaud S, Allen C, Ingham PW, Bandmann O. p53-dependent neuronal cell death in a DJ-1-deficient zebrafish model of Parkinson’s disease. J Neurochem 2007; 100(6): 1626-35.
[127]
Edson AJ, Hushagen HA, Frøyset AK, et al. Dysregulation in the brain protein profile of zebrafish lacking the Parkinson’s disease-related protein dj-1. Mol Neurobiol 2019; 56(12): 8306-22.
[http://dx.doi.org/10.1007/s12035-019-01667-w] [PMID: 31218647]
[128]
Sloan M, Alegre-Abarrategui J, Wade-Martins R. Insights into LRRK2 function and dysfunction from transgenic and knockout rodent models. Biochem Soc Trans 2012; 40(5): 1080-5.
[http://dx.doi.org/10.1042/BST20120151] [PMID: 22988869]
[129]
Hinkle KM, Yue M, Behrouz B, et al. LRRK2 knockout mice have an intact dopaminergic system but display alterations in exploratory and motor co-ordination behaviors. Mol Neurodegener 2012; 7: 25.
[http://dx.doi.org/10.1186/1750-1326-7-25] [PMID: 22647713]
[130]
Sheng D, Qu D, Kwok KH, et al. Deletion of the WD40 domain of LRRK2 in Zebrafish causes Parkinsonism-like loss of neurons and locomotive defect. PLoS Genet 2010; 6(4)e1000914
[http://dx.doi.org/10.1371/journal.pgen.1000914] [PMID: 20421934]
[131]
Prabhudesai S, Bensabeur FZ, Abdullah R, et al. LRRK2 knockdown in zebrafish causes developmental defects, neuronal loss, and synuclein aggregation. J Neurosci Res 2016; 94(8): 717-35.
[http://dx.doi.org/10.1002/jnr.23754] [PMID: 27265751]
[132]
Schober A. Classic toxin-induced animal models of Parkinson’s disease: 6-OHDA and MPTP. Cell Tissue Res 2004; 318(1): 215-24.
[http://dx.doi.org/10.1007/s00441-004-0938-y] [PMID: 15503155]
[133]
Radad K, Moldzio R, Al-Shraim M, Kranner B, Krewenka C, Rausch WD. Recent advances on the role of neurogenesis in the adult brain: Therapeutic potential in Parkinson’s and Alzheimer’s diseases. CNS Neurol Disord Drug Targets 2017; 16(7): 740-8.
[http://dx.doi.org/10.2174/1871527316666170623094728] [PMID: 28641510]
[134]
Antinucci P, Hindges R. A crystal-clear zebrafish for in vivo imaging. Sci Rep 2016; 6: 29490.
[http://dx.doi.org/10.1038/srep29490] [PMID: 27381182]
[135]
MacRae CA, Peterson RT. Zebrafish as tools for drug discovery. Nat Rev Drug Discov 2015; 14(10): 721-31.
[http://dx.doi.org/10.1038/nrd4627] [PMID: 26361349]
[136]
Sun Y, Dong Z, Khodabakhsh H, Chatterjee S, Guo S. Zebrafish chemical screening reveals the impairment of dopaminergic neuronal survival by cardiac glycosides. PLoS One 2012; 7(4)e35645
[http://dx.doi.org/10.1371/journal.pone.0035645] [PMID: 22563390]
[137]
Vaz RL, Sousa S, Chapela D, et al. Identification of antiparkinsonian drugs in the 6-hydroxydopamine zebrafish model. Pharmacol Biochem Behav 2020; 189172828
[http://dx.doi.org/10.1016/j.pbb.2019.172828] [PMID: 31785245]
[138]
Zhang ZJ, Cheang LC, Wang MW, et al. Ethanolic extract of fructus Alpinia oxyphylla protects against 6-hydroxydopamine-induced damage of PC12 cells in vitro and dopaminergic neurons in zebrafish. Cell Mol Neurobiol 2012; 32(1): 27-40.
[http://dx.doi.org/10.1007/s10571-011-9731-0] [PMID: 21744117]
[139]
Chong CM, Zhou ZY, Razmovski-Naumovski V, et al. Danshensu protects against 6-hydroxydopamine-induced damage of PC12 cells in vitro and dopaminergic neurons in zebrafish. Neurosci Lett 2013; 543: 121-5.
[http://dx.doi.org/10.1016/j.neulet.2013.02.069] [PMID: 23562886]
[140]
Kabashi E, Brustein E, Champagne N, Drapeau P. Zebrafish models for the functional genomics of neurogenetic disorders. Biochim Biophys Acta 2011; 1812(3): 335-45.
[http://dx.doi.org/10.1016/j.bbadis.2010.09.011] [PMID: 20887784]
[141]
Wang K, Huang Z, Zhao L, et al. Large-scale forward genetic screening analysis of development of hematopoiesis in zebrafish. J Genet Genomics 2012; 39(9): 473-80.
[http://dx.doi.org/10.1016/j.jgg.2012.07.008] [PMID: 23021547]
[142]
Huang P, Zhu Z, Lin S, Zhang B. Reverse genetic approaches in zebrafish. J Genet Genomics 2012; 39(9): 421-33.
[http://dx.doi.org/10.1016/j.jgg.2012.07.004] [PMID: 23021542]
[143]
Shah AN, Davey CF, Whitebirch AC, Miller AC, Moens CB. Rapid reverse genetic screening using CRISPR in zebrafish. Nat Methods 2015; 12(6): 535-40.
[http://dx.doi.org/10.1038/nmeth.3360] [PMID: 25867848]
[144]
Chakraborty C, Teoh SL, Das S. The smart programmable CRISPR technology: A next generation genome editing tool for investigators. Curr Drug Targets 2017; 18(14): 1653-63.
[http://dx.doi.org/10.2174/1389450117666160527142321] [PMID: 27231109]
[145]
Pankratz N, Nichols WC, Uniacke SK, et al. Parkinson Study Group- Significant linkage of Parkinson disease to chromosome 2q36-37. Am J Hum Genet 2003; 72(4): 1053-7.
[http://dx.doi.org/10.1086/374383] [PMID: 12638082]
[146]
Lautier C, Goldwurm S, Dürr A, et al. Mutations in the GIGYF2 (TNRC15) gene at the PARK11 locus in familial Parkinson disease. Am J Hum Genet 2008; 82(4): 822-33.
[http://dx.doi.org/10.1016/j.ajhg.2008.01.015] [PMID: 18358451]
[147]
Guella I, Pistocchi A, Asselta R, et al. Mutational screening and zebrafish functional analysis of GIGYF2 as a Parkinson-disease gene. Neurobiol Aging 2011; 32(11): 1994-2005.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.12.016] [PMID: 20060621 ]

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