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Review Article

Modelling Parkinson's Disease in C. elegans: Strengths and Limitations

Author(s): Liang Ma, Xi Li, Chengyu Liu, Wanyao Yan, Jinlu Ma, Robert B. Petersen, Anlin Peng* and Kun Huang*

Volume 28, Issue 37, 2022

Published on: 22 September, 2022

Page: [3033 - 3048] Pages: 16

DOI: 10.2174/1381612828666220915103502

Price: $65

Abstract

Parkinson's disease (PD) is a common neurodegenerative disease that affects the motor system and progressively worsens with age. Current treatment options for PD mainly target symptoms, due to our limited understanding of the etiology and pathophysiology of PD. A variety of preclinical models have been developed to study different aspects of the disease. The models have been used to elucidate the pathogenesis and for testing new treatments. These models include cell models, non-mammalian models, rodent models, and non-human primate models. Over the past few decades, Caenorhabditis elegans (C. elegans) has been widely adopted as a model system due to its small size, transparent body, short generation time and life cycle, fully sequenced genome, the tractability of genetic manipulation and suitability for large scale screening for disease modifiers. Here, we review studies using C. elegans as a model for PD and highlight the strengths and limitations of the C. elegans model. Various C. elegans PD models, including neurotoxin-induced models and genetic models, are described in detail. Moreover, methodologies employed to investigate neurodegeneration and phenotypic deficits in C. elegans are summarized.

Keywords: C. elegans, Parkinson’s disease, animal model, neurotoxin-induced models, genetic models, pathological hallmarks, highthroughput screening.

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[1]
Wang H, Naghavi M, Allen C, et al. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: A systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016; 388(10053): 1459-544.
[http://dx.doi.org/10.1016/S0140-6736(16)31012-1] [PMID: 27733281]
[2]
de Lau LML, Breteler MMB. Epidemiology of Parkinson’s disease. Lancet Neurol 2006; 5(6): 525-35.
[http://dx.doi.org/10.1016/S1474-4422(06)70471-9] [PMID: 16713924]
[3]
Goedert M, Compston A. Parkinson’s disease — the story of an eponym. Nat Rev Neurol 2018; 14(1): 57-62.
[http://dx.doi.org/10.1038/nrneurol.2017.165] [PMID: 29217826]
[4]
Jankovic J. Parkinson’s disease: Clinical features and diagnosis. J Neurol Neurosurg Psychiatry 2008; 79(4): 368-76.
[http://dx.doi.org/10.1136/jnnp.2007.131045] [PMID: 18344392]
[5]
Schapira AHV, Chaudhuri KR, Jenner P. Non-motor features of Parkinson disease. Nat Rev Neurosci 2017; 18(7): 435-50.
[http://dx.doi.org/10.1038/nrn.2017.62] [PMID: 28592904]
[6]
Ascherio A, Schwarzschild MA. The epidemiology of Parkinson’s disease: Risk factors and prevention. Lancet Neurol 2016; 15(12): 1257-72.
[http://dx.doi.org/10.1016/S1474-4422(16)30230-7] [PMID: 27751556]
[7]
Corti O, Lesage S, Brice A. What genetics tells us about the causes and mechanisms of Parkinson’s disease. Physiol Rev 2011; 91(4): 1161-218.
[http://dx.doi.org/10.1152/physrev.00022.2010] [PMID: 22013209]
[8]
Shulman JM, De Jager PL, Feany MB. Parkinson’s disease: Genetics and pathogenesis. Annu Rev Pathol 2011; 6(1): 193-222.
[http://dx.doi.org/10.1146/annurev-pathol-011110-130242] [PMID: 21034221]
[9]
Lees AJ, Hardy J, Revesz T. Parkinson’s disease. Lancet 2009; 373(9680): 2055-66.
[http://dx.doi.org/10.1016/S0140-6736(09)60492-X] [PMID: 19524782]
[10]
Alexander AG, Marfil V, Li C. Use of Caenorhabditis elegans as a model to study Alzheimer’s disease and other neurodegenerative diseases. Front Genet 2014; 5: 279.
[http://dx.doi.org/10.3389/fgene.2014.00279] [PMID: 25250042]
[11]
Tieu K. A guide to neurotoxic animal models of Parkinson’s disease. Cold Spring Harb Perspect Med 2011; 1(1): a009316.
[http://dx.doi.org/10.1101/cshperspect.a009316] [PMID: 22229125]
[12]
Dawson TM, Ko HS, Dawson VL. Genetic animal models of Parkinson’s disease. Neuron 2010; 66(5): 646-61.
[http://dx.doi.org/10.1016/j.neuron.2010.04.034] [PMID: 20547124]
[13]
Segura-Aguilar J. The importance of choosing a preclinical model that reflects what happens in Parkinson’s disease. Neurochem Int 2019; 126: 203-9.
[http://dx.doi.org/10.1016/j.neuint.2019.03.016] [PMID: 30922924]
[14]
Falkenburger BH, Saridaki T, Dinter E. Cellular models for Parkinson’s disease. J Neurochem 2016; 139 (Suppl. 1): 121-30.
[http://dx.doi.org/10.1111/jnc.13618] [PMID: 27091001]
[15]
Dung VM, Thao DTP. Parkinson’s disease model. Adv Exp Med Biol 2018; 1076: 41-61.
[http://dx.doi.org/10.1007/978-981-13-0529-0_4] [PMID: 29951814]
[16]
Zhang Y, Zhao Y, Wang Z, et al. Menadione sodium bisulfite inhibits the toxic aggregation of amyloid-beta(1-42). Biochem Biophy J 2018; 1862: 2226-35.
[17]
Ma L, Zhao Y, Chen Y, Cheng B, Peng A, Huang K. Caenorhabditis elegans as a model system for target identification and drug screening against neurodegenerative diseases. Eur J Pharmacol 2018; 819: 169-80.
[http://dx.doi.org/10.1016/j.ejphar.2017.11.051] [PMID: 29208474]
[18]
Ji K, Zhao Y, Yu T, et al. Inhibition effects of tanshinone on the aggregation of α-synuclein. Food Funct 2016; 7(1): 409-16.
[http://dx.doi.org/10.1039/C5FO00664C] [PMID: 26456030]
[19]
Li Y, Yang C, Wang S, et al. Copper and iron ions accelerate the prion-like propagation of α-synuclein: A vicious cycle in Parkinson’s disease. Int J Biol Macromol 2020; 163: 562-73.
[http://dx.doi.org/10.1016/j.ijbiomac.2020.06.274] [PMID: 32629061]
[20]
Cooper JF, Van Raamsdonk JM. Modeling Parkinson’s disease in C. elegans. J Parkinsons Dis 2018; 8(1): 17-32.
[http://dx.doi.org/10.3233/JPD-171258] [PMID: 29480229]
[21]
Martinez BA, Caldwell KA, Caldwell GA. C. elegans as a model system to accelerate discovery for Parkinson disease. Curr Opin Genet Dev 2017; 44: 102-9.
[http://dx.doi.org/10.1016/j.gde.2017.02.011] [PMID: 28242493]
[22]
Harrington AJ, Hamamichi S, Caldwell GA, Caldwell KA. C. elegans as a model organism to investigate molecular pathways involved with Parkinson’s disease. Dev Dyn 2010; 239(5): 1282-95.
[PMID: 20108318]
[23]
Li J, Le W. Modeling neurodegenerative diseases in Caenorhabditis elegans. Exp Neurol 2013; 250: 94-103.
[http://dx.doi.org/10.1016/j.expneurol.2013.09.024] [PMID: 24095843]
[24]
Caldwell KA, Willicott CW, Caldwell GA. Modeling neurodegeneration in Caenorhabditis elegans. Dis Model Mech 2020; 13(10): dmm046110.
[http://dx.doi.org/10.1242/dmm.046110] [PMID: 33106318]
[25]
Chia SJ, Tan EK, Chao YX. Historical perspective: Models of Parkinson’s disease. Int J Mol Sci 2020; 21(7): 2464.
[http://dx.doi.org/10.3390/ijms21072464] [PMID: 32252301]
[26]
Ke M, Chong CM, Zhu Q, et al. Comprehensive perspectives on experimental models for Parkinson’s disease. Aging Dis 2021; 12(1): 223-46.
[http://dx.doi.org/10.14336/AD.2020.0331] [PMID: 33532138]
[27]
Trigo-Damas I, del Rey NLG, Blesa J. Novel models for Parkinson’s disease and their impact on future drug discovery. Expert Opin Drug Discov 2018; 13(3): 229-39.
[http://dx.doi.org/10.1080/17460441.2018.1428556] [PMID: 29363335]
[28]
Chen X, Barclay JW, Burgoyne RD, Morgan A. Using C. elegans to discover therapeutic compounds for ageing-associated neurodegenerative diseases. Chem Cent J 2015; 9(1): 65.
[http://dx.doi.org/10.1186/s13065-015-0143-y] [PMID: 26617668]
[29]
Kwok TCY, Ricker N, Fraser R, et al. A small-molecule screen in C. elegans yields a new calcium channel antagonist. Nature 2006; 441(7089): 91-5.
[http://dx.doi.org/10.1038/nature04657] [PMID: 16672971]
[30]
Youssef K, Tandon A, Rezai P. Studying Parkinson's disease using Caenorhabditis elegans models in microfluidic devices. Integ Biol 2019; 11: 186-207.
[http://dx.doi.org/10.1093/intbio/zyz017]
[31]
Mondal S, Hegarty E, Martin C, Gökçe SK, Ghorashian N, Ben-Yakar A. Large-scale microfluidics providing high-resolution and high-throughput screening of Caenorhabditis elegans poly-glutamine aggregation model. Nat Commun 2016; 7(1): 13023.
[http://dx.doi.org/10.1038/ncomms13023] [PMID: 27725672]
[32]
Petrascheck M, Ye X, Buck LB. An antidepressant that extends lifespan in adult Caenorhabditis elegans. Nature 2007; 450(7169): 553-6.
[http://dx.doi.org/10.1038/nature05991] [PMID: 18033297]
[33]
Braungart E, Gerlach M, Riederer P, Baumeister R, Hoener MC. Caenorhabditis elegans MPP+ model of Parkinson’s disease for high-throughput drug screenings. Neurodegener Dis 2004; 1(4-5): 175-83.
[http://dx.doi.org/10.1159/000080983] [PMID: 16908987]
[34]
Nourse JB Jr, Harshefi G, Marom A, et al. Conserved nicotine-activated neuroprotective pathways involve mitochondrial stress. iScience 2021; 24(3): 102140.
[http://dx.doi.org/10.1016/j.isci.2021.102140] [PMID: 33665559]
[35]
Villafane G, Thiriez C, Audureau E, et al. High-dose transdermal nicotine in Parkinson’s disease patients: A randomized, open-label, blinded-endpoint evaluation phase 2 study. Eur J Neurol 2018; 25(1): 120-7.
[http://dx.doi.org/10.1111/ene.13474] [PMID: 28960663]
[36]
Shen P, Yue Y, Park Y. A living model for obesity and aging research: Caenorhabditis elegans. Crit Rev Food Sci Nutr 2018; 58(5): 741-54.
[http://dx.doi.org/10.1080/10408398.2016.1220914] [PMID: 27575804]
[37]
Gruss M, Corsi AK. Using Caenorhabditis elegans as a model for mechanistic insights of craniofacial. Methods Mol Biol 2022; 2403: 1-18.
[http://dx.doi.org/10.1007/978-1-0716-1847-9_1] [PMID: 34913112]
[38]
Hulme SE, Whitesides GM. Chemistry and the worm: Caenorhabditis elegans as a platform for integrating chemical and biological research. Angew Chem Int Ed 2011; 50(21): 4774-807.
[http://dx.doi.org/10.1002/anie.201005461] [PMID: 21500322]
[39]
Zeng XS, Geng WS, Jia JJ. Neurotoxin-induced animal models of Parkinson disease: Pathogenic mechanism and assessment. ASN Neuro 2018; 10: 1759091418777438.
[http://dx.doi.org/10.1177/1759091418777438] [PMID: 29809058]
[40]
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]
[41]
Simola N, Morelli M, Carta AR. The 6-Hydroxydopamine model of parkinson’s disease. Neurotox Res 2007; 11(3-4): 151-67.
[http://dx.doi.org/10.1007/BF03033565] [PMID: 17449457]
[42]
Blum D, Torch S, Lambeng N, et al. Molecular pathways involved in the neurotoxicity of 6-OHDA, dopamine and MPTP: Contribution to the apoptotic theory in Parkinson’s disease. Prog Neurobiol 2001; 65(2): 135-72.
[http://dx.doi.org/10.1016/S0301-0082(01)00003-X] [PMID: 11403877]
[43]
Marvanova M, Nichols CD. Identification of neuroprotective compounds of Caenorhabditis elegans dopaminergic neurons against 6-OHDA. J Mol Neurosci 2007; 31: 127-37.
[44]
Nass R, Hall DH, Miller DM III, Blakely RD. Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc Natl Acad Sci USA 2002; 99(5): 3264-9.
[http://dx.doi.org/10.1073/pnas.042497999] [PMID: 11867711]
[45]
Nass R, Blakely RD. The Caenorhabditis elegans dopaminergic system: Opportunities for insights into dopamine transport and neurodegeneration. Annu Rev Pharmacol Toxicol 2003; 43(1): 521-44.
[http://dx.doi.org/10.1146/annurev.pharmtox.43.100901.135934] [PMID: 12415122]
[46]
Nass R, Hahn MK, Jessen T, McDonald PW, Carvelli L, Blakely RD. A genetic screen in Caenorhabditis elegans for dopamine neuron insensitivity to 6-hydroxydopamine identifies dopamine transporter mutants impacting transporter biosynthesis and trafficking. J Neurochem 2005; 94(3): 774-85.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03205.x] [PMID: 15992384]
[47]
Tóth ML, Simon P, Kovács AL, Vellai T. Influence of autophagy genes on ion-channel-dependent neuronal degeneration in Caenorhabditis elegans. J Cell Sci 2007; 120(6): 1134-41.
[http://dx.doi.org/10.1242/jcs.03401] [PMID: 17327275]
[48]
Gerlach M, Riederer P, Przuntek H, Youdim MBH. MPTP mechanisms of neurotoxicity and their implications for Parkinson’s disease. Eur J Pharmacol (Mol Pharmacol Sect) 1991; 208(4): 273-86.
[http://dx.doi.org/10.1016/0922-4106(91)90073-Q] [PMID: 1815982]
[49]
Goetze O, Woitalla D. The role of MPTP in Parkinson’s disease: Connecting brain and gut? Exp Neurol 2008; 210(2): 281-5.
[http://dx.doi.org/10.1016/j.expneurol.2008.01.004] [PMID: 18279853]
[50]
Kopin IJ. MPTP: An industrial chemical and contaminant of illicit narcotics stimulates a new era in research on Parkinson’s disease. Environ Health Perspect 1987; 75: 45-51.
[http://dx.doi.org/10.1289/ehp.877545] [PMID: 3319563]
[51]
Zhang Y, Guo X, Yan W, et al. ANGPTL8 negatively regulates NF-κB activation by facilitating selective autophagic degradation of IKKγ. Nat Commun 2017; 8(1): 2164.
[http://dx.doi.org/10.1038/s41467-017-02355-w] [PMID: 29255244]
[52]
Wang W, Wang Q, Wan D, et al. Histone HIST1H1C/H1.2 regulates autophagy in the development of diabetic retinopathy. Autophagy 2017; 13(5): 941-54.
[http://dx.doi.org/10.1080/15548627.2017.1293768] [PMID: 28409999]
[53]
Murphy D, Patel H, Wimalasena K. Caenorhabditis elegans model studies show MPP+ is a simple member of a large group of related potent dopaminergic toxins. Chem Res Toxicol 2021; 34(5): 1275-85.
[http://dx.doi.org/10.1021/acs.chemrestox.0c00422] [PMID: 33496570]
[54]
Wang YM, Pu P, Le WD. ATP depletion is the major cause of MPP+ induced dopamine neuronal death and worm lethality in α-synuclein transgenic C. elegans. Neurosci Bull 2007; 23(6): 329-35.
[http://dx.doi.org/10.1007/s12264-007-0049-3] [PMID: 18064062]
[55]
Tanner CM, Kamel F, Ross GW, et al. Rotenone, paraquat, and Parkinson’s disease. Environ Health Perspect 2011; 119(6): 866-72.
[http://dx.doi.org/10.1289/ehp.1002839] [PMID: 21269927]
[56]
Berry C, La Vecchia C, Nicotera P. Paraquat and Parkinson’s disease. Cell Death Differ 2010; 17(7): 1115-25.
[http://dx.doi.org/10.1038/cdd.2009.217] [PMID: 20094060]
[57]
Mockett RJ, Bayne ACV, Kwong LK, Orr WC, Sohal RS. Ectopic expression of catalase in Drosophila mitochondria increases stress resistance but not longevity. Free Radic Biol Med 2003; 34(2): 207-17.
[http://dx.doi.org/10.1016/S0891-5849(02)01190-5] [PMID: 12521602]
[58]
Dilberger B, Baumanns S, Schmitt F, et al. Mitochondrial oxidative stress impairs energy metabolism and reduces stress resistance and longevity of C. elegans. Oxid Med Cell Longev 2019; 2019: 1-14.
[http://dx.doi.org/10.1155/2019/6840540] [PMID: 31827694]
[59]
Sampayo JN, Olsen A, Lithgow GJ. Oxidative stress in Caenorhabditis elegans: Protective effects of superoxide dismutase/catalase mimetics. Aging Cell 2003; 2(6): 319-26.
[http://dx.doi.org/10.1046/j.1474-9728.2003.00063.x] [PMID: 14677634]
[60]
Bora S, Vardhan GSH, Deka N, Khataniar L, Gogoi D, Baruah A. Paraquat exposure over generation affects lifespan and reproduction through mitochondrial disruption in C. elegans. Toxicology 2021; 447: 152632.
[http://dx.doi.org/10.1016/j.tox.2020.152632] [PMID: 33197508]
[61]
Wu M, Kang X, Wang Q, Zhou C, Mohan C, Peng A. Regulator of G protein signaling-1 modulates paraquat-induced oxidative stress and longevity via the insulin like signaling pathway in Caenorhabditis elegans. Toxicol Lett 2017; 273: 97-105.
[http://dx.doi.org/10.1016/j.toxlet.2017.03.027] [PMID: 28366735]
[62]
Johnson ME, Bobrovskaya L. An update on the rotenone models of Parkinson’s disease: Their ability to reproduce the features of clinical disease and model gene–environment interactions. Neurotoxicology 2015; 46: 101-16.
[http://dx.doi.org/10.1016/j.neuro.2014.12.002] [PMID: 25514659]
[63]
Gonzalez-Hunt CP, Luz AL, Ryde IT, et al. Multiple metabolic changes mediate the response of Caenorhabditis elegans to the complex I inhibitor rotenone. Toxicology 2021; 447: 152630.
[http://dx.doi.org/10.1016/j.tox.2020.152630] [PMID: 33188857]
[64]
Chikka MR, Anbalagan C, Dvorak K, Dombeck K, Prahlad V. The mitochondria-regulated immune pathway activated in the C. elegans intestine is neuroprotective. Cell Rep 2016; 16(9): 2399-414.
[http://dx.doi.org/10.1016/j.celrep.2016.07.077] [PMID: 27545884]
[65]
Ray A, Martinez BA, Berkowitz LA, Caldwell GA, Caldwell KA. Mitochondrial dysfunction, oxidative stress, and neurodegeneration elicited by a bacterial metabolite in a C. elegans Parkinson’s model. Cell Death Dis 2014; 5(1): e984.
[http://dx.doi.org/10.1038/cddis.2013.513] [PMID: 24407237]
[66]
Aschner M, Erikson K. Manganese. Adv Nutr 2017; 8(3): 520-1.
[http://dx.doi.org/10.3945/an.117.015305] [PMID: 28507016]
[67]
Horning KJ, Caito SW, Tipps KG, Bowman AB, Aschner M. Manganese is essential for neuronal health. Annu Rev Nutr 2015; 35(1): 71-108.
[http://dx.doi.org/10.1146/annurev-nutr-071714-034419] [PMID: 25974698]
[68]
Guilarte TR. Manganese and Parkinson’s disease: A critical review and new findings. Environ Health Perspect 2010; 118(8): 1071-80.
[http://dx.doi.org/10.1289/ehp.0901748] [PMID: 20403794]
[69]
Mortimer JA, Borenstein AR, Nelson LM. Associations of welding and manganese exposure with Parkinson disease: Review and meta-analysis. Neurology 2012; 79(11): 1174-80.
[http://dx.doi.org/10.1212/WNL.0b013e3182698ced] [PMID: 22965675]
[70]
Ratner MH, Fitzgerald E. Understanding of the role of manganese in parkinsonism and Parkinson disease. Neurology 2017; 88(4): 338-9.
[http://dx.doi.org/10.1212/WNL.0000000000003543] [PMID: 28031391]
[71]
Benedetto A, Au C, Aschner M. Manganese-induced dopaminergic neurodegeneration: Insights into mechanisms and genetics shared with Parkinson’s disease. Chem Rev 2009; 109(10): 4862-84.
[http://dx.doi.org/10.1021/cr800536y] [PMID: 19534496]
[72]
Au C, Benedetto A, Anderson J, et al. SMF-1, SMF-2 and SMF-3 DMT1 orthologues regulate and are regulated differentially by manganese levels in C. elegans. PLoS One 2009; 4(11): e7792.
[http://dx.doi.org/10.1371/journal.pone.0007792] [PMID: 19924247]
[73]
Settivari R, LeVora J, Nass R. The divalent metal transporter homologues SMF-1/2 mediate dopamine neuron sensitivity in Caenorhabditis elegans models of manganism and parkinson disease. J Biol Chem 2009; 284(51): 35758-68.
[http://dx.doi.org/10.1074/jbc.M109.051409] [PMID: 19801673]
[74]
Benedetto A, Au C, Avila DS, Milatovic D, Aschner M. Extracellular dopamine potentiates mn-induced oxidative stress, lifespan reduction, and dopaminergic neurodegeneration in a BLI-3-dependent manner in Caenorhabditis elegans. PLoS Genet 2010; 6(8): e1001084.
[http://dx.doi.org/10.1371/journal.pgen.1001084] [PMID: 20865164]
[75]
Stoker TB, Greenland JC. Parkinson’s disease: Pathogenesis and clinical aspects. Brisbane (AU): Codon Publications 2018.
[76]
Mata IF, Wedemeyer WJ, Farrer MJ, Taylor JP, Gallo KA. LRRK2 in Parkinson’s disease: Protein domains and functional insights. Trends Neurosci 2006; 29(5): 286-93.
[http://dx.doi.org/10.1016/j.tins.2006.03.006] [PMID: 16616379]
[77]
Pickrell AM, Youle RJ. The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson’s disease. Neuron 2015; 85(2): 257-73.
[http://dx.doi.org/10.1016/j.neuron.2014.12.007] [PMID: 25611507]
[78]
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]
[79]
Blauwendraat C, Nalls MA, Singleton AB. The genetic architecture of Parkinson’s disease. Lancet Neurol 2020; 19(2): 170-8.
[http://dx.doi.org/10.1016/S1474-4422(19)30287-X] [PMID: 31521533]
[80]
Kilarski LL, Pearson JP, Newsway V, et al. Systematic review and UK-based study of PARK2 (parkin), PINK1, PARK7 (DJ-1) and LRRK2 in early-onset Parkinson’s disease. Mov Disord 2012; 27(12): 1522-9.
[http://dx.doi.org/10.1002/mds.25132] [PMID: 22956510]
[81]
Bento CF, Ashkenazi A, Jimenez-Sanchez M, Rubinsztein DC. The Parkinson’s disease-associated genes ATP13A2 and SYT11 regulate autophagy via a common pathway. Nat Commun 2016; 7(1): 11803.
[http://dx.doi.org/10.1038/ncomms11803] [PMID: 27278822]
[82]
Lim KL. Non-mammalian animal models of Parkinson’s disease for drug discovery. Expert Opin Drug Discov 2010; 5(2): 165-76.
[http://dx.doi.org/10.1517/17460440903527675] [PMID: 22822916]
[83]
Spillantini MG, Schmidt ML, Lee VMY, Trojanowski JQ, Jakes R, Goedert M. α-Synuclein in Lewy bodies. Nature 1997; 388(6645): 839-40.
[http://dx.doi.org/10.1038/42166] [PMID: 9278044]
[84]
Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci 2001; 2(7): 492-501.
[http://dx.doi.org/10.1038/35081564] [PMID: 11433374]
[85]
Ma L, Yang C, Zhang X, et al. C-terminal truncation exacerbates the aggregation and cytotoxicity of α-Synuclein: A vicious cycle in Parkinson’s disease. Biochim Biophys Acta Mol Basis Dis 2018; 1864(12): 3714-25.
[http://dx.doi.org/10.1016/j.bbadis.2018.10.003] [PMID: 30290273]
[86]
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]
[87]
Ma L, Zheng J, Chen H, et al. A systematic screening of traditional chinese medicine identifies two novel inhibitors against the cytotoxic aggregation of amyloid beta. Front Pharmacol 2021; 12: 637766.
[http://dx.doi.org/10.3389/fphar.2021.637766] [PMID: 33897425]
[88]
Cheng B, Li Y, Ma L, et al. Interaction between amyloidogenic proteins and biomembranes in protein misfolding diseases: Mechanisms, contributors, and therapy. Biochim Biophys Acta Biomembr 2018; 1860(9): 1876-88.
[http://dx.doi.org/10.1016/j.bbamem.2018.02.013] [PMID: 29466701]
[89]
Deng H, Yuan L. Genetic variants and animal models in SNCA and Parkinson disease. Ageing Res Rev 2014; 15: 161-76.
[http://dx.doi.org/10.1016/j.arr.2014.04.002] [PMID: 24768741]
[90]
Ma L, Yang C, Zheng J, Chen Y, Xiao Y, Huang K. Non-polyphenolic natural inhibitors of amyloid aggregation. Eur J Med Chem 2020; 192: 112197.
[http://dx.doi.org/10.1016/j.ejmech.2020.112197] [PMID: 32172082]
[91]
Gómez-Benito M, Granado N, García-Sanz P, Michel A, Dumoulin M, Moratalla R. Modeling Parkinson’s disease with the alpha-synuclein protein. Front Pharmacol 2020; 11: 356.
[http://dx.doi.org/10.3389/fphar.2020.00356] [PMID: 32390826]
[92]
Visanji NP, Brotchie JM, Kalia LV, et al. α-Synuclein-based animal models of parkinson’s disease: challenges and opportunities in a new era. Trends Neurosci 2016; 39(11): 750-62.
[http://dx.doi.org/10.1016/j.tins.2016.09.003] [PMID: 27776749]
[93]
van Ham TJ, Thijssen KL, Breitling R, Hofstra RMW, Plasterk RHA, Nollen EAA. C. elegans model identifies genetic modifiers of alpha-synuclein inclusion formation during aging. PLoS Genet 2008; 4(3): e1000027.
[http://dx.doi.org/10.1371/journal.pgen.1000027] [PMID: 18369446]
[94]
Nagarajan A, Bodhicharla R, Winter J, et al. A fluorescence resonance energy transfer assay for monitoring α- synclein aggregation in a Caenorhabditis elegans model for parkinson’s disease. CNS Neurol Disord Drug Targets 2015; 14(8): 1054-68.
[http://dx.doi.org/10.2174/1871527314666150821110538] [PMID: 26295817]
[95]
Lakso M, Vartiainen S, Moilanen AM, et al. Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human α-synuclein. J Neurochem 2003; 86(1): 165-72.
[http://dx.doi.org/10.1046/j.1471-4159.2003.01809.x] [PMID: 12807436]
[96]
Kuwahara T, Koyama A, Gengyo-Ando K, et al. Familial Parkinson mutant alpha-synuclein causes dopamine neuron dysfunction in transgenic Caenorhabditis elegans. J Biol Chem 2006; 281(1): 334-40.
[http://dx.doi.org/10.1074/jbc.M504860200] [PMID: 16260788]
[97]
Kluss JH, Mamais A, Cookson MR. LRRK2 links genetic and sporadic Parkinson’s disease. Biochem Soc Trans 2019; 47(2): 651-61.
[http://dx.doi.org/10.1042/BST20180462] [PMID: 30837320]
[98]
Tolosa E, Vila M, Klein C, Rascol O. LRRK2 in Parkinson disease: Challenges of clinical trials. Nat Rev Neurol 2020; 16(2): 97-107.
[http://dx.doi.org/10.1038/s41582-019-0301-2] [PMID: 31980808]
[99]
Li J, Huang J, Li JS, Chen H, Huang K, Zheng L. Accumulation of endoplasmic reticulum stress and lipogenesis in the liver through generational effects of high fat diets. J Hepatol 2012; 56(4): 900-7.
[http://dx.doi.org/10.1016/j.jhep.2011.10.018] [PMID: 22173165]
[100]
Sun Y, Wang Q, Zhang Y, et al. Multigenerational maternal obesity increases the incidence of HCC in offspring via miR-27a-3p. J Hepatol 2020; 73(3): 603-15.
[http://dx.doi.org/10.1016/j.jhep.2020.03.050] [PMID: 32593682]
[101]
Vázquez-Vélez GE, Zoghbi HY. Parkinson’s disease genetics and pathophysiology. Annu Rev Neurosci 2021; 44(1): 87-108.
[http://dx.doi.org/10.1146/annurev-neuro-100720-034518] [PMID: 34236893]
[102]
Saha S, Guillily MD, Ferree A, et al. LRRK2 modulates vulnerability to mitochondrial dysfunction in Caenorhabditis elegans. J Neurosci 2009; 29(29): 9210-8.
[http://dx.doi.org/10.1523/JNEUROSCI.2281-09.2009] [PMID: 19625511]
[103]
Yao C, El Khoury R, Wang W, et al. LRRK2-mediated neurodegeneration and dysfunction of dopaminergic neurons in a Caenorhabditis elegans model of Parkinson’s disease. Neurobiol Dis 2010; 40(1): 73-81.
[http://dx.doi.org/10.1016/j.nbd.2010.04.002] [PMID: 20382224]
[104]
Saha S, Liu-Yesucevitz L, Wolozin B. Regulation of Autophagy by LRRK2 in Caenorhabditis elegans. Neurodegener Dis 2014; 13(2-3): 110-3.
[http://dx.doi.org/10.1159/000355654] [PMID: 24192129]
[105]
Sakaguchi-Nakashima A, Meir JY, Jin Y, Matsumoto K, Hisamoto N. LRK-1, a C. elegans PARK8-related kinase, regulates axonal-dendritic polarity of SV proteins. Curr Biol 2007; 17(7): 592-8.
[http://dx.doi.org/10.1016/j.cub.2007.01.074] [PMID: 17346966]
[106]
Fukuzono T, Pastuhov SI, Fukushima O, et al. Chaperone complex BAG2-HSC70 regulates localization of Caenorhabditis elegans leucine-rich repeat kinase LRK-1 to the Golgi. Genes to Cells 2016; 21: 311-24.
[107]
Jeong GR, Lee BD. Pathological Functions of LRRK2 in Parkinson’s disease. Cells 2020; 9(12): 2565.
[http://dx.doi.org/10.3390/cells9122565] [PMID: 33266247]
[108]
Chandler RJ, Cogo S, Lewis PA, Kevei E. Modelling the functional genomics of Parkinson’s disease in Caenorhabditis elegans: LRRK2 and beyond. Biosci Rep 2021; 41(9): BSR20203672.
[http://dx.doi.org/10.1042/BSR20203672] [PMID: 34397087]
[109]
Pilsl A, Winklhofer KF. Parkin, PINK1 and mitochondrial integrity: Emerging concepts of mitochondrial dysfunction in Parkinson’s disease. Acta Neuropathol 2012; 123(2): 173-88.
[http://dx.doi.org/10.1007/s00401-011-0902-3] [PMID: 22057787]
[110]
Arkinson C, Walden H. Parkin function in Parkinson’s disease. Science 2018; 360(6386): 267-8.
[http://dx.doi.org/10.1126/science.aar6606] [PMID: 29674580]
[111]
Chakraborty S, Chen P, Bornhorst J, et al. Loss of pdr-1/parkin influences Mn homeostasis through altered ferroportin expression in C. elegans. Metallomics 2015; 7: 847-56.
[112]
Martinez-Finley EJ, Chakraborty S, Slaughter JC, Aschner M. Early-life exposure to methylmercury in wildtype and pdr-1/parkin knockout C. elegans. Neurochem Res 2013; 38(8): 1543-52.
[http://dx.doi.org/10.1007/s11064-013-1054-8] [PMID: 23609499]
[113]
Ved R, Saha S, Westlund B, et al. Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. J Biol Chem 2005; 280(52): 42655-68.
[http://dx.doi.org/10.1074/jbc.M505910200] [PMID: 16239214]
[114]
Springer W, Hoppe T, Schmidt E, Baumeister R. A Caenorhabditis elegans Parkin mutant with altered solubility couples α-synuclein aggregation to proteotoxic stress. Hum Mol Genet 2005; 14(22): 3407-23.
[http://dx.doi.org/10.1093/hmg/ddi371] [PMID: 16204351]
[115]
Morris HR. Genetics of Parkinson’s disease. Ann Med 2005; 37(2): 86-96.
[http://dx.doi.org/10.1080/07853890510007269] [PMID: 16026116]
[116]
Hauser DN, Hastings TG. Mitochondrial dysfunction and oxidative stress in Parkinson’s disease and monogenic parkinsonism. Neurobiol Dis 2013; 51: 35-42.
[http://dx.doi.org/10.1016/j.nbd.2012.10.011] [PMID: 23064436]
[117]
Fang EF, Hou Y, Palikaras K, et al. Mitophagy inhibits amyloid-β and tau pathology and reverses cognitive deficits in models of Alzheimer’s disease. Nat Neurosci 2019; 22(3): 401-12.
[http://dx.doi.org/10.1038/s41593-018-0332-9] [PMID: 30742114]
[118]
Kane LA, Lazarou M, Fogel AI, et al. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J Cell Biol 2014; 205(2): 143-53.
[http://dx.doi.org/10.1083/jcb.201402104] [PMID: 24751536]
[119]
Kazlauskaite A, Kondapalli C, Gourlay R, et al. Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem J 2014; 460(1): 127-41.
[http://dx.doi.org/10.1042/BJ20140334] [PMID: 24660806]
[120]
Koyano F, Okatsu K, Kosako H, et al. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 2014; 510(7503): 162-6.
[http://dx.doi.org/10.1038/nature13392] [PMID: 24784582]
[121]
Luz AL, Rooney JP, Kubik LL, Gonzalez CP, Song DH, Meyer JN. Mitochondrial morphology and fundamental parameters of the mitochondrial respiratory chain are altered in Caenorhabditis elegans strains deficient in mitochondrial dynamics and homeostasis processes. PLoS One 2015; 10(6): e0130940.
[http://dx.doi.org/10.1371/journal.pone.0130940] [PMID: 26106885]
[122]
Sämann J, Hegermann J, von Gromoff E, Eimer S, Baumeister R, Schmidt E. Caenorhabditits elegans LRK-1 and PINK-1 act antagonistically in stress response and neurite outgrowth. J Biol Chem 2009; 284(24): 16482-91.
[http://dx.doi.org/10.1074/jbc.M808255200] [PMID: 19251702]
[123]
Bastioli G, Regoni M, Cazzaniga F, et al. Animal models of autosomal recessive parkinsonism. Biomedicines 2021; 9(7): 812.
[http://dx.doi.org/10.3390/biomedicines9070812] [PMID: 34356877]
[124]
van der Vlag M, Havekes R, Heckman PRA. The contribution of Parkin, PINK1 and DJ‐1 genes to selective neuronal degeneration in Parkinson’s disease. Eur J Neurosci 2020; 52(4): 3256-68.
[http://dx.doi.org/10.1111/ejn.14689] [PMID: 31991026]
[125]
Mencke P, Boussaad I, Romano CD, Kitami T, Linster CL, Krüger R. The role of dj-1 in cellular metabolism and pathophysiological implications for Parkinson’s disease. Cells 2021; 10(2): 347.
[http://dx.doi.org/10.3390/cells10020347] [PMID: 33562311]
[126]
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]
[127]
Chen P, DeWitt MR, Bornhorst J, et al. Age- and manganese-dependent modulation of dopaminergic phenotypes in a C. elegans DJ-1 genetic model of Parkinson's disease. Metallomics 2015; 7: 289-98.
[128]
Kamal M, D’Amora DR, Kubiseski TJ. Loss of hif-1 promotes resistance to the exogenous mitochondrial stressor ethidium bromide in Caenorhabditis elegans. BMC Cell Biol 2016; 17(1): 34.
[http://dx.doi.org/10.1186/s12860-016-0112-x] [PMID: 27618966]
[129]
Lee J, Kim C, Kim J, Park C. DJR-1.2 of Caenorhabditis elegans is induced by DAF-16 in the dauer state. Gene 2013; 524(2): 373-6.
[http://dx.doi.org/10.1016/j.gene.2013.04.032] [PMID: 23624124]
[130]
Castro CEM, Waak J, Weber SS, et al. Parkinson’s disease-associated DJ-1 modulates innate immunity signaling in Caenorhabditis elegans. J Neural Transm 2010; 117(5): 599-604.
[http://dx.doi.org/10.1007/s00702-010-0397-4] [PMID: 20376509]
[131]
van Veen S. Sørensen DM, Holemans T, Holen HW, Palmgren MG, Vangheluwe P. Cellular function and pathological role of ATP13A2 and related P-type transport ATPases in Parkinson’s disease and other neurological disorders. Front Mol Neurosci 2014; 7: 48.
[http://dx.doi.org/10.3389/fnmol.2014.00048] [PMID: 24904274]
[132]
Park JS, Blair NF, Sue CM. The role of ATP13A2 in Parkinson’s disease: Clinical phenotypes and molecular mechanisms. Mov Disord 2015; 30(6): 770-9.
[http://dx.doi.org/10.1002/mds.26243] [PMID: 25900096]
[133]
Sato S, Li Y, Hattori N. Lysosomal defects in ATP13A2 and GBA associated familial Parkinson’s disease. J Neural Transm 2017; 124(11): 1395-400.
[http://dx.doi.org/10.1007/s00702-017-1779-7] [PMID: 28894968]
[134]
Anand N, Holcom A, Broussalian M, et al. Dysregulated iron metabolism in C. elegans catp-6/ATP13A2 mutant impairs mitochondrial function. Neurobiol Dis 2020; 139: 104786.
[http://dx.doi.org/10.1016/j.nbd.2020.104786] [PMID: 32032734]
[135]
Baesler J, Kopp JF, Pohl G, et al. Zn homeostasis in genetic models of Parkinson's disease in Caenorhabditis elegans. J Trace Elem Med Biol 2019; 55: 44-9.
[http://dx.doi.org/10.1016/j.jtemb.2019.05.005]
[136]
Liang JJH, McKinnon IA, Rankin CH. The contribution of C. elegans neurogenetics to understanding neurodegenerative diseases. J Neurogenet 2020; 34(3-4): 527-48.
[http://dx.doi.org/10.1080/01677063.2020.1803302] [PMID: 32772603]
[137]
Ma L, Yang C, Huang L, et al. Glycated insulin exacerbates the cytotoxicity of human islet amyloid polypeptides: a vicious cycle in type 2 diabetes. ACS Chem Biol 2019; 14(3): 486-96.
[http://dx.doi.org/10.1021/acschembio.8b01128] [PMID: 30715843]
[138]
Guo C, Ma L, Zhao Y, et al. Inhibitory effects of magnolol and honokiol on human calcitonin aggregation. Sci Rep 2015; 5(1): 13556.
[http://dx.doi.org/10.1038/srep13556] [PMID: 26324190]
[139]
Gong H, He Z, Peng A, et al. Effects of several quinones on insulin aggregation. Sci Rep 2015; 4(1): 5648.
[http://dx.doi.org/10.1038/srep05648] [PMID: 25008537]
[140]
Cheng B, Gong H, Xiao H, Petersen RB, Zheng L, Huang K. Inhibiting toxic aggregation of amyloidogenic proteins: A therapeutic strategy for protein misfolding diseases. Biochim Biophys Acta, Gen Subj 2013; 1830(10): 4860-71.
[http://dx.doi.org/10.1016/j.bbagen.2013.06.029] [PMID: 23820032]
[141]
Gong H, Yang X, Zhao Y, et al. Amyloidogenicity of p53: A hidden link between protein misfolding and cancer. Curr Protein Pept Sci 2015; 16(2): 135-46.
[http://dx.doi.org/10.2174/1389203715666141128115649] [PMID: 25692950]
[142]
Li Y, Wang Z, Chen Y, Petersen RB, Zheng L, Huang K. Salvation of the fallen angel: Reactivating mutant p53. Br J Pharmacol 2019; 176(7): 817-31.
[http://dx.doi.org/10.1111/bph.14572] [PMID: 30632144]
[143]
Wang S, Zheng J, Ma L, et al. Inhibiting protein aggregation with nanomaterials: The underlying mechanisms and impact factors. Biochem Biophy J 2022; 1866: 130061.
[144]
Xiong Y, Dawson TM, Dawson VL. Models of LRRK2-associated Parkinson’s disease. Adv Neurobiol 2017; 14: 163-91.
[http://dx.doi.org/10.1007/978-3-319-49969-7_9] [PMID: 28353284]
[145]
Ahier A, Dai CY, Kirmes I, et al. PINK1 and parkin shape the organism-wide distribution of a deleterious mitochondrial genome. Cell Rep 2021; 35(9): 109203.
[http://dx.doi.org/10.1016/j.celrep.2021.109203] [PMID: 34077728]
[146]
Pujols J, Peña-Díaz S, Lázaro DF, et al. Small molecule inhibits α-synuclein aggregation, disrupts amyloid fibrils, and prevents degeneration of dopaminergic neurons. Proc Natl Acad Sci USA 2018; 115(41): 10481-6.
[http://dx.doi.org/10.1073/pnas.1804198115] [PMID: 30249646]
[147]
Laine RF, Sinnige T, Ma KY, et al. Fast fluorescence lifetime imaging reveals the aggregation processes of α-synuclein and polyglutamine in aging Caenorhabditis elegans. ACS Chem Biol 2019; 14(7): 1628-36.
[http://dx.doi.org/10.1021/acschembio.9b00354] [PMID: 31246415]
[148]
Bodhicharla R, Nagarajan A, Winter J, et al. Effects of α-synuclein overexpression in transgenic Caenorhabditis elegans strains. CNS Neurol Disord Drug Targets 2012; 11(8): 965-75.
[http://dx.doi.org/10.2174/1871527311211080005] [PMID: 23244416]
[149]
Bijwadia SR, Morton K, Meyer JN. Quantifying levels of dopaminergic neuron morphological alteration and degeneration in Caenorhabditis elegans. J Vis Exp 2021; (177): 0.3791/62894.
[http://dx.doi.org/10.3791/62894] [PMID: 34866619]
[150]
Smith LL, Ryde IT, Hartman JH, Romersi RF, Markovich Z, Meyer JN. Strengths and limitations of morphological and behavioral analyses in detecting dopaminergic deficiency in Caenorhabditis elegans. Neurotoxicology 2019; 74: 209-20.
[http://dx.doi.org/10.1016/j.neuro.2019.07.002] [PMID: 31323240]
[151]
Huang TT, Matsuyama HJ, Tsukada Y, et al. Age‐dependent changes in response property and morphology of a thermosensory neuron and thermotaxis behavior in Caenorhabditis elegans. Aging Cell 2020; 19(5): e13146.
[http://dx.doi.org/10.1111/acel.13146] [PMID: 32307902]
[152]
Liu Y, Samuel BS, Breen PC, Ruvkun G. Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature 2014; 508(7496): 406-10.
[http://dx.doi.org/10.1038/nature13204] [PMID: 24695221]
[153]
Kaufman DM, Wu X, Scott BA, et al. Ageing and hypoxia cause protein aggregation in mitochondria. Cell Death Differ 2017; 24(10): 1730-8.
[http://dx.doi.org/10.1038/cdd.2017.101] [PMID: 28644434]
[154]
Grad LI, Sayles LC, Lemire BD. Isolation and functional analysis of mitochondria from the nematode Caenorhabditis elegans. Methods Mol Biol 2007; 372: 51-66.
[http://dx.doi.org/10.1007/978-1-59745-365-3_4] [PMID: 18314717]
[155]
Chen LT, Lin CT, Lin LY, Hsu JM, Wu YC, Pan CL. Neuronal mitochondrial dynamics coordinate systemic mitochondrial morphology and stress response to confer pathogen resistance in C. elegans. Dev Cell 2021; 56(12): 1770-1785.e12.
[http://dx.doi.org/10.1016/j.devcel.2021.04.021] [PMID: 33984269]
[156]
Rodríguez-Ramos Á, Gámez-del-Estal MM, Porta-de-la-Riva M, Cerón J, Ruiz-Rubio M. Impaired dopamine-dependent locomotory behavior of C. elegans neuroligin mutants depends on the catechol-O-methyltransferase COMT-4. Behav Genet 2017; 47(6): 596-608.
[http://dx.doi.org/10.1007/s10519-017-9868-9] [PMID: 28879499]
[157]
Peres TV, Arantes LP, Miah MR, et al. Role of Caenorhabditis elegans AKT-1/2 and SGK-1 in manganese toxicity. Neurotox Res 2018; 34(3): 584-96.
[http://dx.doi.org/10.1007/s12640-018-9915-1] [PMID: 29882004]
[158]
Izquierdo PG, Calahorro F, Ruiz-Rubio M. Neuroligin modulates the locomotory dopaminergic and serotonergic neuronal pathways of C. elegans. Neurogenetics 2013; 14(3-4): 233-42.
[http://dx.doi.org/10.1007/s10048-013-0377-6] [PMID: 24100941]
[159]
Maulik M, Mitra S, Bult-Ito A, Taylor BE, Vayndorf EM. Behavioral phenotyping and pathological indicators of Parkinson’s disease in C. elegans models. Front Genet 2017; 8: 77.
[http://dx.doi.org/10.3389/fgene.2017.00077] [PMID: 28659967]
[160]
Gray JM, Hill JJ, Bargmann CI. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci USA 2005; 102(9): 3184-91.
[http://dx.doi.org/10.1073/pnas.0409009101] [PMID: 15689400]
[161]
Hums I, Riedl J, Mende F, et al. Regulation of two motor patterns enables the gradual adjustment of locomotion strategy in Caenorhabditis elegans. eLife 2016; 5: e14116.
[http://dx.doi.org/10.7554/eLife.14116] [PMID: 27222228]
[162]
Ashida K, Kato T, Hotta K, Oka K. Multiple tracking and machine learning reveal dopamine modulation for area-restricted foraging behaviors via velocity change in Caenorhabditis elegans. Neurosci Lett 2019; 706: 68-74.
[http://dx.doi.org/10.1016/j.neulet.2019.05.011] [PMID: 31082452]
[163]
Hills T, Brockie PJ, Maricq AV. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 2004; 24(5): 1217-25.
[http://dx.doi.org/10.1523/JNEUROSCI.1569-03.2004] [PMID: 14762140]
[164]
Liu KS, Sternberg PW. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 1995; 14(1): 79-89.
[http://dx.doi.org/10.1016/0896-6273(95)90242-2] [PMID: 7826644]
[165]
Sugi T, Okumura E, Kiso K, et al. Nanoscale mechanical stimulation method for quantifying C. elegans mechanosensory behavior and memory. Analytical Sciences 2016; 32: 1159-64.
[166]
Sawin ER, Ranganathan R, Horvitz HR. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 2000; 26(3): 619-31.
[http://dx.doi.org/10.1016/S0896-6273(00)81199-X] [PMID: 10896158]
[167]
Baugh LR, Hu PJ. Starvation responses throughout the caenorhabditis elegans life cycle. Genetics 2020; 216(4): 837-78.
[http://dx.doi.org/10.1534/genetics.120.303565] [PMID: 33268389]
[168]
Kaplan REW, Webster AK, Chitrakar R, Dent JA, Baugh LR. Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans. BMC Biol 2018; 16(1): 112.
[http://dx.doi.org/10.1186/s12915-018-0579-3] [PMID: 30296941]
[169]
Fielenbach N, Antebi A C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 2008; 22(16): 2149-65.
[http://dx.doi.org/10.1101/gad.1701508] [PMID: 18708575]
[170]
Gaglia MM, Kenyon C. Stimulation of movement in a quiescent, hibernation-like form of Caenorhabditis elegans by dopamine signaling. J Neurosci 2009; 29(22): 7302-14.
[http://dx.doi.org/10.1523/JNEUROSCI.3429-08.2009] [PMID: 19494152]
[171]
Liu X, Zhou Y, Liu X, et al. MPHOSPH1: A potential therapeutic target for hepatocellular carcinoma. Cancer Res 2014; 74(22): 6623-34.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-1279] [PMID: 25269478]
[172]
Yang C, Zhang Y, Zeng X, et al. Kidney injury molecule-1 is a potential receptor for SARS-CoV-2. J Mol Cell Biol 2021; 13(3): 185-96.
[http://dx.doi.org/10.1093/jmcb/mjab003] [PMID: 33493263]
[173]
Wang C, Xiong M, Yang C, et al. PEGylated and acylated elabela analogues show enhanced receptor binding, prolonged stability, and remedy of acute kidney injury. J Med Chem 2020; 63(24): 16028-42.
[http://dx.doi.org/10.1021/acs.jmedchem.0c01913] [PMID: 33290073]
[174]
Fu RH, Wang YC, Chen CS, et al. Acetylcorynoline attenuates dopaminergic neuron degeneration and α-synuclein aggregation in animal models of Parkinson’s disease. Neuropharmacology 2014; 82: 108-20.
[http://dx.doi.org/10.1016/j.neuropharm.2013.08.007] [PMID: 23973292]
[175]
Pu P, Le W. Dopamine neuron degeneration induced by MPP+ is independent of CED-4 pathway in Caenorhabditis elegans. Cell Res 2008; 18(9): 978-81.
[http://dx.doi.org/10.1038/cr.2008.279] [PMID: 19160545]
[176]
Cao S, Gelwix CC, Caldwell KA, Caldwell GA. Torsin-mediated protection from cellular stress in the dopaminergic neurons of Caenorhabditis elegans. J Neurosci 2005; 25(15): 3801-12.
[http://dx.doi.org/10.1523/JNEUROSCI.5157-04.2005] [PMID: 15829632]
[177]
Cao P, Yuan Y, Pehek EA, et al. Alpha-synuclein disrupted dopamine homeostasis leads to dopaminergic neuron degeneration in Caenorhabditis elegans. PLoS One 2010; 5(2): e9312.
[http://dx.doi.org/10.1371/journal.pone.0009312] [PMID: 20174477]
[178]
Cooper JF, Dues DJ, Spielbauer KK, Machiela E, Senchuk MM, Van Raamsdonk JM. Delaying aging is neuroprotective in Parkinson’s disease: A genetic analysis in C. elegans models. NPJ Parkinsons Dis 2015; 1(1): 15022.
[http://dx.doi.org/10.1038/npjparkd.2015.22] [PMID: 28725688]
[179]
Liu Z, Hamamichi S, Dae Lee B, et al. Inhibitors of LRRK2 kinase attenuate neurodegeneration and Parkinson-like phenotypes in Caenorhabditis elegans and Drosophila Parkinson’s disease models. Hum Mol Genet 2011; 20(20): 3933-42.
[http://dx.doi.org/10.1093/hmg/ddr312] [PMID: 21768216]
[180]
Yao C, Johnson WM, Gao Y, et al. Kinase inhibitors arrest neurodegeneration in cell and C. elegans models of LRRK2 toxicity. Hum Mol Genet 2013; 22(2): 328-44.
[http://dx.doi.org/10.1093/hmg/dds431] [PMID: 23065705]
[181]
Bornhorst J, Chakraborty S, Meyer S, et al. The effects of pdr1, djr1.1 and pink1 loss in manganese-induced toxicity and the role of alpha-synuclein in C. elegans. Metallomics 2014; 6: 476-90.
[182]
Cooper JF, Machiela E, Dues DJ, Spielbauer KK, Senchuk MM, Van Raamsdonk JM. Activation of the mitochondrial unfolded protein response promotes longevity and dopamine neuron survival in Parkinson’s disease models. Sci Rep 2017; 7(1): 16441.
[http://dx.doi.org/10.1038/s41598-017-16637-2] [PMID: 29180793]
[183]
Bess AS, Crocker TL, Ryde IT, Meyer JN. Mitochondrial dynamics and autophagy aid in removal of persistent mitochondrial DNA damage in Caenorhabditis elegans. Nucleic Acids Res 2012; 40(16): 7916-31.
[http://dx.doi.org/10.1093/nar/gks532] [PMID: 22718972]
[184]
Bess AS, Leung MCK, Ryde IT, Rooney JP, Hinton DE, Meyer JN. Effects of mutations in mitochondrial dynamics-related genes on the mitochondrial response to ultraviolet C radiation in developing Caenorhabditis elegans. Worm 2013; 2(1): e23763.
[http://dx.doi.org/10.4161/worm.23763] [PMID: 24058863]
[185]
Lee J, Song J, Kwon K, et al. Human DJ-1 and its homologs are novel glyoxalases. Hum Mol Genet 2012; 21(14): 3215-25.
[http://dx.doi.org/10.1093/hmg/dds155] [PMID: 22523093]
[186]
Gitler AD, Chesi A, Geddie ML, et al. α-Synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat Genet 2009; 41(3): 308-15.
[http://dx.doi.org/10.1038/ng.300] [PMID: 19182805]
[187]
Lambie EJ, Tieu PJ, Lebedeva N, Church DL, Conradt B. CATP-6, a C. elegans ortholog of ATP13A2 PARK9, positively regulates GEM-1, an SLC16A transporter. PLoS One 2013; 8(10): e77202.
[http://dx.doi.org/10.1371/journal.pone.0077202] [PMID: 24130856]

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