Progressive neurodegeneration in C. elegans model of tauopathy
Open accessAbstract
Discovery of various mutations in the tau gene among frontotemporal dementia and parkinsonism linked to chromosome 17 (FTDP-17) families suggests gain-of-toxic function of wild-type or mutant tau as the mechanism for extensive neuronal loss. We thus generated transgenic nematode (Caenorhabditis elegans) expressing wild-type or mutant (P301L and R406W) tau in the touch (mechanosensory) neurons. Whereas the worm expressing wild-type tau showed a small decrease in the touch response across the lifespan, the worm expressing mutant tau displayed a large and progressive decrease. When the touch neurons lost their function, neuritic abnormalities were found prominent, and microtubular loss became remarkable in the later stage. A substantial fraction of degenerating neurons developed tau accumulation in the cell body and neuronal processes. This neuronal dysfunction is not related to the apoptotic process because little recovery from touch abnormality was observed in the ced-3 or ced-4-deficient background. Expression of GSK3 brought about slight deterioration in the touch response, while expression of HSP70 led to some improvement.
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Inhibition or genetic reduction of GSK-3β ameliorates tau-related deficits.
“many investigators have shown that either inhibition or genetic reduction of GSK-3β ameliorates tau-related deficits (94–99).”
From Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation (2011) · cites this paper as [96]
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“elegans transgenic model, where human tau is expressed only in mechanosensory neurons, expression of human HSP70 protects against the transgenic tau-induced neuronal dysfunction, a result consistent with our finding that loss of hsp-1 is an enhancer (Table 1) (71).”
ResultTackenberg, C., & Brandt, R. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3590-09.2009 · Cited by 127 · see citing works
“It has been shown that FTDP-17 tau mutants can induce neurodegeneration in vivo (Lewis et al., 2000; Miyasaka et al., 2005; Santacruz et al., 2005).”
BackgroundBrandt, R., Gergou, A., Wacker, I., Fath, T., & Hutter, H. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.05.011 · Cited by 126 · see citing works
Lublin, A. L., & Link, C. D. (2012) · Drug Discovery Today Technologies · doi:10.1016/j.ddtec.2012.02.002 · Cited by 119 · see citing works
Using C. elegans to discover therapeutic compounds for ageing-associated neurodegenerative diseases
Chen, X., Barclay, J. W., Burgoyne, R. D., & Morgan, A. (2015) · Chemistry Central Journal · doi:10.1186/s13065-015-0143-y · Cited by 116 · see citing works
“se l-1 2( ar 13 1) a nd (a r1 71 ) G S1 89 4 Ex hi bi t t he rm ot ax is d ef ec ts [1 34 , 1 35 ]”
BackgroundAmbegaokar, S. S., & Jackson, G. R. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr432 · Cited by 113 · see citing works
Modeling neurodegenerative diseases in Caenorhabditis elegans.
Li, J., & Le, W. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.09.024 · Cited by 113 · see citing works
“When human HSP70 is over-expressed in the mutant tau transgenic worms, it significantly improves touch response (Miyasaka et al., 2005).”
BackgroundNeurodegenerative disorders: insights from the nematode Caenorhabditis elegans
Dimitriadi, M., & Hart, A. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.05.012 · Cited by 107 · see citing works
SUT-2 potentiates tau-induced neurotoxicity in Caenorhabditis elegans.
Guthrie, C. R., Schellenberg, G., & Kraemer, B. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp099 · Cited by 102 · see citing works
“Likewise, insoluble tau protein accumulates in the neurons of tau transgenic worms (15,22,23).”
BackgroundBehavioral Phenotyping and Pathological Indicators of Parkinson's Disease in C. elegans Models
Maulik, M., Mitra, S., Bult-Ito, A., Taylor, B. E., & Vayndorf, E. M. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2017.00077 · Cited by 100 · see citing works
Metal-induced neurodegeneration in C. elegans
Chen, P., Martinez-Finley, E. J., Bornhorst, J., Chakraborty, S., & Aschner, M. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2013.00018 · Cited by 82 · see citing works
“Keywords: neurodegeneration, behavior, metals, C. elegans, neurotransmitters”
BackgroundTeschendorf, D., & Link, C. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-38 · Cited by 75 · see citing works
“elegans by expressing wild type and FTLD-17-mutant tau specifically in touch neurons, using the mec-7 promoter [57].”
MethodGötz, J., Xia, D., Leinenga, G., Chew, Y. L., & Nicholas, H. (2013) · Frontiers in Neurology · doi:10.3389/fneur.2013.00072 · Cited by 85 · see citing works
“While most studies on TAU use the mouse as a model organism, several wild-type and mutant human TAU transgenic models have been established in the nematode C. elegans (Kraemer et al., 2003; Miyasaka et al., 2005; Brandt et al., 2009; Fatouros et al., 2012).”
BackgroundMa, L., Zhao, Y., Chen, Y., Cheng, B., Peng, A.-L., & Huang, K. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.11.051 · Cited by 72 · see citing works
Colodner, K. J., & Feany, M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2491-10.2010 · Cited by 71 · see citing works
Modeling Alzheimer’s Disease in Caenorhabditis elegans
Alvarez, J., Álvarez-Illera, P., Santo-Domingo, J., Fonteriz, R., & Montero, M. (2022) · Biomedicines · doi:10.3390/biomedicines10020288 · Cited by 70 · see citing works
“Moreover, accumulations of tau in the cell body and neuronal processes were observed in many of the neurons undergoing degeneration [108].”
BackgroundUnderstanding the molecular basis of Alzheimer’s disease using a Caenorhabditis elegans model system
Ewald, C., & Li, C. (2009) · Brain Structure and Function · doi:10.1007/s00429-009-0235-3 · Cited by 68 · see citing works
“…in touch response; neurodegeneration; strong tau accumulation in PLM neuron (as wild-type tau WT4R) tmIs146, tmIs147, tmIs148, tmIs149 Miyasaka et al. (2005) Tau352 (=fetal, 352aa isoform) wild type rgef-1 Constitutively in all neurons Age-dependent progressive uncoordination;…”
BackgroundInfluentialInvertebrate Models of Alzheimer's Disease
Mhatre, S. D., Paddock, B., Saunders, A., & Marenda, D. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2012-121204 · Cited by 67 · see citing works
“elegans hTau (1N4R) and mutants (0N4RV337M, 0N4RP301L) Mechanosensory neurons Impaired touch response, morphological abnormalities in touch neurons, NFTs [128]”
Genetic screens in Caenorhabditis elegans models for neurodegenerative diseases
Sin, O., Michels, H., & Nollen, E. A. A. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.01.015 · Cited by 65 · see citing works
“On the other hand, tau-expressingmodels have been specific to neuronal cells and the phenotype is either worsening of uncoordinatedmovement or insensitivity to the touch response due to transgene expression [75,108,109].”
BackgroundProtein with tau-like repeats regulates neuronal integrity and lifespan inC. elegans
Chew, Y. L., Fan, X., Götz, J., & Nicholas, H. (2013) · Journal of Cell Science · doi:10.1242/jcs.jcs124404 · Cited by 59 · see citing works
“The negative effect of expressing human tau in C. elegans, as also observed in (Kraemer et al., 2003; Miyasaka et al., 2005; Brandt et al., 2009), may either be due to overexpression of any MAP having a detrimental effect, or due to a specific axonal role of tau that evolved with the…”
BackgroundGenetic and Pharmacological Discovery for Alzheimer’s Disease Using Caenorhabditis elegans
Griffin, E. F., Caldwell, K. A., & Caldwell, G. A. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.7b00361 · Cited by 67 · see citing works
Distribution of endogenous normal tau in the mouse brain
Kubo, A., Misonou, H., Matsuyama, M., Nomori, A., Wada‐Kakuda, S., Takashima, A., Kawata, M., Murayama, S., Ihara, Y., & Miyasaka, T. (2019) · Journal of Comparative Neurology · doi:10.1002/cne.24577 · Cited by 57 · see citing works
“and degeneration (Kuchibhotla et al., 2014; Miyasaka et al., 2005; Santacruz et al., 2005) and that the abnormal distribution of pre-”
BackgroundMethodSelf-citationTauopathy models and human neuropathology: similarities and differences
Frank, S., Clavaguera, F., & Tolnay, M. (2007) · Acta Neuropathologica · doi:10.1007/s00401-007-0291-9 · Cited by 51 · see citing works
“To model tauopathy disorders, several transgenic worm models have been generated [10, 46, 61].”
BackgroundMethodGuha, S., Fischer, S., Johnson, G., & Nehrke, K. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00410-7 · Cited by 50 · see citing works
“elegans has been shown to severely impact neuronal morphology and function [31, 40].”
BackgroundCaenorhabditis elegans as a model system for studying aging-associated neurodegenerative diseases
Pelt, K. M. V., & Truttmann, M. C. (2020) · Translational Medicine of Aging · doi:10.1016/j.tma.2020.05.001 · Cited by 60 · see citing works
“corroborating findings of increased severity associated with FTDP-17 tau mutants [97].”
ResultSinnige, T., Yu, A.-A., & Morimoto, R. (2020) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-40204-4_4 · Cited by 47 · see citing works
Curcumin improves tau-induced neuronal dysfunction of nematodes.
Miyasaka, T., Xie, C., Yoshimura, S., Shinzaki, Y., Yoshina, S., Kage-Nakadai, E., Mitani, S., & Ihara, Y. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.11.004 · Cited by 46 · see citing works
“Miyasaka et al. / Neurobiology of Aging 39 (2016) 69e81 70”
Self-citationHegde, R. N., Chiki, A., Petricca, L., Martufi, P., Arbez, N., Mouchiroud, L., Auwerx, J. H., Landles, C., Bates, G. P., Singh‐Bains, M. K., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020104671 · Cited by 48 · see citing works
“…and toxicity, suggesting that targeting TBK1 represents a viable strategy for the treatment of HD. Increasing evidence suggests that dysfunction in autophagy and other protein clearance mechanisms play central roles in the pathogenesis of neurodegenerative diseases, including HD (Nixon, 2013).”
BackgroundMicrotubule destruction induces tau liberation and its subsequent phosphorylation
Miyasaka, T., Sato, S., Tatebayashi, Y., & Takashima, A. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.06.014 · Cited by 41 · see citing works
“This inverse relation can be observed across various animal models for tauopathy [23,24].”
BackgroundSelf-citationAnimal Models for Alzheimer’s Disease and Frontotemporal Dementia: A Perspective
Götz, J., & Götz, N. N. (2009) · ASN NEURO · doi:10.1042/an20090042 · Cited by 37 · see citing works
“Similarly, expression of human tau carrying FTD mutations, but not wild-type tau, in C. elegans results in neurodegeneration with an accumulation of hyperphosphorylated tau and associated uncoordinated locomotion (Unc) (Kraemer et al., 2003; Miyasaka et al., 2005; Brandt et al., 2009).”
BackgroundBessa, C., Maciel, P., & Rodrigues, A. J. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8434-6 · Cited by 50 · see citing works
“These animals presented substantial neurodegeneration, with axonal disruption and presynaptic defects [112, 126].”
BackgroundThe apoptotic engulfment machinery regulates axonal degeneration in C. elegans neurons
Nichols, A. L. A., Meelkop, E., Linton, C., Giordano-Santini, R., Sullivan, R. K. P., Donato, A., Nolan, C., Hall, D. H., Xue, D., Neumann, B., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.050 · Cited by 38 · see citing works
“…neurons have been extensively studied as a model for both neurodegeneration and regeneration, and are among the best-characterized neurons in the nematode nervous system (Chalfie et al., 1985; Huang and Chalfie, 1994; Miyasaka et al., 2005; Neumann et al., 2011, 2015; Zhang et al., 2008).”
TDP-43 promotes tau accumulation and selective neurotoxicity in bigenic Caenorhabditis elegans
Latimer, C., Stair, J. G., Hincks, J. C., Currey, H. N., Bird, T., Keene, C., Kraemer, B., & Liachko, N. F. (2022) · Disease Models & Mechanisms · doi:10.1242/dmm.049323 · Cited by 37 · see citing works
“Mechanosensation assays were adapted from Miyasaka et al. (2005).”
Tien, N.-W., Wu, G.-H., Hsu, C.-C., Chang, C.-Y., & Wagner, O. I. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.04.023 · Cited by 37 · see citing works
Caenorhabditis elegans models of tauopathy
Pir, G. J., Choudhary, B. C., & Mandelkow, E. (2017) · The FASEB Journal · doi:10.1096/fj.201701007 · Cited by 35 · see citing works
The Model Caenorhabditis elegans in Diabetes Mellitus and Alzheimer's Disease
Morcos, M., & Hutter, H. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-0977 · Cited by 35 · see citing works
“elegans [133–135].”
Xie, C., Miyasaka, T., Yoshimura, S., Hatsuta, H., Yoshina, S., Kage-Nakadai, E., Mitani, S., Murayama, S., & Ihara, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089796 · Cited by 28 · see citing works
“elegans were generated as described previously [18,21,22].”
ResultSelf-citationXie, C., Soeda, Y., Shinzaki, Y., In, Y., Tomoo, K., Ihara, Y., & Miyasaka, T. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13228 · Cited by 27 · see citing works
“Thus far, increasing evidence suggests that the mechanisms responsible for neuronal degeneration may not be limited to the formation of inclusions, which is the final step of the pathology (Gomez-Isla et al. 1997; Miyasaka et al. 2005; Santacruz et al. 2005).”
BackgroundSelf-citationAutophagy and cell death in Caenorhabditis elegans.
Samara, C., & Tavernarakis, N. (2008) · Current pharmaceutical design · doi:10.2174/138161208783378770 · Cited by 27 · see citing works
“Nevertheless, it is ameliorated by up-regulation of heat-shock proteins, such as HSP70 [181].”
BackgroundAlzheimer's disease models and functional genomics—How many needles are there in the haystack?
Götz, J., Matamales, M., Götz, N. N., Ittner, L. M., & Eckert, A. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00320 · Cited by 18 · see citing works
“…pathomechanisms in AD and FTLD. Expression of human tau carrying FTLD mutations, but not wild-type tau, results in neurodegeneration with an accumulation of hyperphosphorylated tau and associated uncoordinated locomotion (Unc) (Kraemer et al., 2003; Miyasaka et al., 2005; Brandt et al., 2009).”
BackgroundMiyasaka, T., Shinzaki, Y., Yoshimura, S., Yoshina, S., Kage-Nakadai, E., Mitani, S., & Ihara, Y. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00415 · Cited by 25 · see citing works
Self-citationNon‐apoptotic cell death in Caenorhabditis elegans
Vlachos, M., & Tavernarakis, N. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22230 · Cited by 24 · see citing works
“In the second model of tau-induced pathology, where wild-type or mutant tau is specifically expressed in the 6 touch receptor neurons of the worm, touch responses are weakened particularly in the case of mutant tau expression (Miyasaka et al., 2005).”
BackgroundPharmacological maintenance of protein homeostasis could postpone age‐related disease
Alavez, S., & Lithgow, G. J. (2012) · Aging Cell · doi:10.1111/j.1474-9726.2012.00789.x · Cited by 23 · see citing works
“Models expressing tau protein in neurons (Kraemer et al., 2003; Miyasaka et al., 2005), a-synuclein in different tissues (Lakso et al., 2003; Cao et al., 2005; van Ham et al., 2008; Hamamichi et al., 2008) and mouse prion protein (Park & Li, 2008), among others, have also been generated in C.…”
BackgroundNon-developmentally programmed cell death in Caenorhabditis elegans.
Kourtis, N., & Tavernarakis, N. (2007) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2006.11.004 · Cited by 22 · see citing works
Giong, H.-K., Subramanian, M., Yu, K., & Lee, J.-S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168465 · Cited by 29 · see citing works
Malcolm, J. C., Breuillaud, L., Carmo, S. D., Hall, H., Welikovitch, L. A., Macdonald, J., Goedert, M., & Cuello, A. C. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.03.018 · Cited by 21 · see citing works
Planarian GSK3s are involved in neural regeneration
Adell, T., Marsal, M., & Saló, E. (2008) · Development, Genes and Evolution · doi:10.1007/s00427-007-0199-3 · Cited by 21 · see citing works
“Thus, a key role has been described for GSK3 in neural processes ranging from nervous system development to neurodegeneration (Marcus et al. 1998; Anderton 1999; Miyasaka et al. 2005; Lucas et al. 2001; Chen et al. 2004).”
BackgroundNecrotic cell death in Caenorhabditis elegans.
Nikoletopoulou, V., & Tavernarakis, N. (2014) · Methods in Enzymology · doi:10.1016/b978-0-12-801430-1.00006-8 · Cited by 21 · see citing works
“…the expression of human tau (wild-type tau or tau carrying FTDP-17 mutations) either pan-neuronally, under the control of the aex - 3 promoter (Kraemer et al. 2003 ), or specifi cally in touch receptor neurons of C. elegans , under the control of the mec - 7 promoter (Miyasaka et al. 2005 ).”
BackgroundCaenorhabditis elegans Models to Investigate the Mechanisms Underlying Tau Toxicity in Tauopathies
Natale, C., Barzago, M. M., & Diomede, L. (2020) · Brain Science · doi:10.3390/brainsci10110838 · Cited by 20 · see citing works
“six mechanosensory neurons—a subset of neurons governing the touch response of worms—a decrease in the touch response, accompanied by neuritic abnormalities and microtubular loss, was observed [27] (Table 1).”
BackgroundVayndorf, E. M., Scerbak, C., Hunter, S., Neuswanger, J. R., Toth, M., Parker, J., Néri, C., Driscoll, M., & Taylor, B. E. (2016) · npj Aging and Mechanisms of Disease · doi:10.1038/npjamd.2016.1 · Cited by 20 · see citing works
“Similarly, Miyasaka and colleagues 12 showed that expressing the human mutated tau gene in touch receptor neurons reduced touch sensitivity, increased neuronal abnormalities, and caused the loss of microtubular spindles.”
Wang, C., & Zheng, C. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.875349 · Cited by 22 · see citing works
Simple model systems reveal conserved mechanisms of Alzheimer’s disease and related tauopathies
Jiang, Y.-W., & MacNeil, L. T. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00664-x · Cited by 18 · see citing works
“Expression of these Tau variants in C. elegans induces disease-associated pathologies, including phosphorylation of Tau at disease-relevant sites, accumulation of insoluble Tau aggregates, synaptic loss, decreased neuronal function and neurode-generation [23, 167, 209].”
BackgroundAge-dependent accumulation of tau aggregation in Caenorhabditis elegans
Nunez, W. A., Combs, B., Gamblin, T. C., & Ackley, B. D. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.928574 · Cited by 18 · see citing works
“Other tauopathy models using over-expression of tau have noted cases of neuronal degeneration as well (Miyasaka et al., 2005; Kraemer and Schellenberg, 2007).”
BackgroundNavarro-Hortal, M., Romero-Márquez, J. M., Osta, S., Jiménez-Trigo, V., Muñoz-Ollero, P., & Varela-López, A. (2022) · Diseases · doi:10.3390/diseases10020028 · Cited by 16 · see citing works
“Two of them use pan-neuronal promoters [94,95], while the remaining one expressed tau only in touch cell neurons [96].”
BackgroundEctopic Expression Induces Abnormal Somatodendritic Distribution of Tau in the Mouse Brain
Kubo, A., Ueda, S., Yamane, A., Wada‐Kakuda, S., Narita, M., Matsuyama, M., Nomori, A., Takashima, A., Kato, T., Onodera, O., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2845-18.2019 · Cited by 17 · see citing works
“Cumulative evidence indicates that the formation of NFTs itself might not directly cause neuronal dysfunction and degeneration (Miyasaka et al., 2005a; Santacruz et al., 2005; Kuchibhotla et al., 2014) and that the abnormal distribution of presumably unaggregated tau into dendrites or spines is a…”
BackgroundMethodSelf-citationHess, M., Gomariz, A., Goksel, O., & Ewald, C. (2019) · eNeuro · doi:10.1523/eneuro.0014-19.2019 · Cited by 14 · see citing works
“Expressing human Tau in the six touch receptor neurons results in morphologic abnormalities (Miyasaka et al., 2005).”
BackgroundV363I and V363A mutated tau affect aggregation and neuronal dysfunction differently in C. elegans.
Morelli, F., Romeo, M., Barzago, M. M., Bolis, M., Mattioni, D., Rossi, G., Tagliavini, F., Bastone, A., Salmona, M., & Diomede, L. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.06.018 · Cited by 14 · see citing works
Sinnige, T., Stroobants, K., Dobson, C. M., & Vendruscolo, M. (2020) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583520000025 · Cited by 18 · see citing works
“A study in which the 3R and 4R isoforms of wild-type tau, and the 4R isoforms of P301L and R406W were expressed specifically in the six mechanosensory neurons of C. elegans has largely corroborated these findings (Miyasaka et al., 2005).”
ResultTackling neurodegenerative diseases: animal models of Alzheimer’s disease and Parkinson’s disease
Raslan, A., & Yun, K. (2013) · Genes & Genomics · doi:10.1007/s13258-013-0116-2 · Cited by 13 · see citing works
“Miyasaka et al. (2005) developed another transgenic model in which human wild-type (4R and 3R) or FTDP-17 mutant TAU (P301L and R406W) were overexpressed in the six mechanosensory neurons of the body under the C. elegans mec-7 promoter.”
GLB‐13 is associated with oxidative stress resistance in caenorhabditis elegans
Ren, C.-H., Li, Y., Han, R., Gao, D., Li, W., Shi, J.-P., Hoogewijs, D., Braeckman, B. P., de Henau, S., Lu, Y.-M., et al. (2013) · IUBMB Life - A Journal of the International Union of Biochemistry and Molecular Biology · doi:10.1002/iub.1132 · Cited by 10 · see citing works
“To obtain the expression of hNgb in whole neurons, the coding region of EGFP in the pFX-unc119::EGFP construct (53) was removed by NotI/BglII digestion and then replaced with the hNgb cDNA containing the same restriction sites.”
MethodKraemer, B., & Schellenberg, G. (2007) · International review of neurobiology · doi:10.1016/s0074-7742(06)77007-6 · Cited by 10 · see citing works
Generation and characterization of a tractable C. elegans model of tauopathy
Russell, J., Lei, H., Chaliparambil, R. K., Fish, S., Markiewicz, S. M., Lee, T.-I., Noori, A., & Kaeberlein, M. (2021) · GeroScience · doi:10.1007/s11357-021-00436-9 · Cited by 9 · see citing works
Effects of NAD+ in Caenorhabditis elegans Models of Neuronal Damage
Lee, Y., Jeong, H., Park, K. H., & Kim, K. W. (2020) · Biomolecules · doi:10.3390/biom10070993 · Cited by 8 · see citing works
Tiwari, V., Buvarp, E., Borbolis, F., Puligilla, C., Croteau, D., Palikaras, K., & Bohr, V. A. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae705 · Cited by 8 · see citing works
Proteome-Scale Mapping of Perturbed Proteostasis in Living Cells.Preprint
Lam, I., Hallacli, E., & Khurana, V. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a034124 · Cited by 8 · see citing works
“4 Cite this article as Cold Spring Harb Perspect Biol 2020;12:a034124 α-Synuclein Parkinson’s disease Saccharomyces cerevisiae Outeiro and Lindquist 2003; Willingham et al. 2003; Dixon et al. 2005; Zabrocki et al. 2005; Sharma et al. 2006 Drosophila melanogaster Feany and Bender 2000; Auluck et al. 2002 Caenorhabditis…”
BackgroundAlzheimer’s Disease and Animal Models in Retrospect
Fajemiroye, J. O. (2014) · Medicinal Chemistry · doi:10.4172/2161-0444.1000215 · Cited by 6 · see citing works
“In addition to secretase model, apoE [113-115], axonal transport models [116], studies in fruit flies-Drosophila melanogaster [117,118], studies in nematodes - Caenorhabditis elegans [119,120] among others have been used as animal models of AD.”
MethodMitochondrial Quality Control in Alzheimer’s Disease: Insights from Caenorhabditis elegans Models
Ganguly, U., Carroll, T., Nehrke, K. W., & Johnson, G. V. W. (2024) · Antioxidants · doi:10.3390/antiox13111343 · Cited by 5 · see citing works
“Using metabolomics, Redmann et al. demonstrated that pharmacological molecules that perturb lysosomal activity (bafilomycin, chloroquine) and inhibit autophagy can result in mitochondrial dysfunction in primary cortical neurons by altering mitochondrial respiration, mitochondrial biogenesis, and…”
Caenorhabditis elegans as a model system to evaluate neuroprotective potential of nano formulations
Chauhan, P., Wadhwa, K., & Singh, G. (2022) · Frontiers in Nanotechnology · doi:10.3389/fnano.2022.1018754 · Cited by 6 · see citing works
“Several transgenic worms expressing Tau components have been developed to study the consequences of neuronal Tau expression (Kraemer et al., 2003; Miyasaka et al., 2005; Brandt et al., 2009).”
BackgroundCaenorhabditis elegans as a model to assess reproductive and developmental toxicity
Ávila, D., Adams, M., Chakraborty, S., & Aschner, M. (2011) · doi:10.1016/b978-0-12-382032-7.10016-5 · Cited by 6
Kanaan, N. M., Himmelstein, D. S., Ward, S., Combs, B., & Binder, L. I. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405195-9.00056-1 · Cited by 9 · see citing works
Ladagu, A., Olopade, F., Chazot, P., Elufioye, T., Luong, T., Fuller, M., Halprin, E., Mckay, J., Ates-Alagoz, Z., Gilbert, T. T., et al. (2024) · BMC Neuroscience · doi:10.1186/s12868-024-00902-y · Cited by 4 · see citing works
“…neuronal degeneration, impaired synaptic transmission, altered morphology, disrupted neuronal activity, and functional impairments in locomotion and behavior which ultimately leads to abnormal movement patterns, paralysis, or altered behavioral responses as observed in our behavioural assays [95].”
BackgroundUnraveling Molecular Targets for Neurodegenerative Diseases Through Caenorhabditis elegans Models
Xu, R., Kang, Q., Yang, X.-F., Yi, P., & Zhang, R.-Y. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26073030 · Cited by 3 · see citing works
“Mutated tau forms linked to insoluble phosphorylated aggregates and motor deficits have been explored [34,35].”
Guha, S., Fischer, S., Johnson, G., & Nehrke, K. (2020) · bioRxiv · doi:10.1101/2020.02.12.946004 · Cited by 3
“been shown to severely impact neuronal morphology and function (30).”
BackgroundChen, X., Reichert, M., & Gan, L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802851-3.00005-x · Cited by 3 · see citing works
Joshi, M., van Falier, S., & Sinnige, T. (2025) · bioRxiv · doi:10.1101/2025.08.01.668095 · Cited by 2 · see citing works
“…reported functional defects accompanied by damage to neuronal structures (Brandt et al., 2009; Fatouros et al., 2012; Kraemer et al., 2003; Miyasaka et al., 2005; Pir et al., 2016) In some cases, insoluble tau was found to accumulate (Aquino Nunez et al., 2022; Fatouros et al., 2012;…”
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“It was previously shown that transgenic overexpression of human kinases in C. elegans could be used to determine their effects on pathogenic disease mechanisms (Branco-Santos et al., 2017; Miyasaka et al., 2005).”
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Caenorhabditis elegans as a model organism for protein homeostasis diseases
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“Previously published C. elegans Tau models relied mainly on the expression of untagged Tau or used a stoichiometric GFP-Tau fusion (Kraemer et al., 2003; Aquino Nunez et al., 2022; Fatouros et al., 2012; Morelli et al., 2018; Pir et al., 2016; Miyasaka et al., 2005).”
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- Authors
- Miyasaka, T., Ding, Z., Gengyo-Ando, K., Oue, M., Yamaguchi, H., Mitani, S., & Ihara, Y.
- Affiliations
- The University of Tokyo (JP)
- Tokyo Women's Medical University (JP)
- Gunma University (JP)
- Corresponding author
- Ihara, Yasuo
- Venue
- Neurobiology of Disease
- Publisher
- Elsevier BV
- Published
- 2005-11
- Volume
- 20
- Issue
- 2
- Pages
- 372-383
- ISSN
- 0969-9961 (ISSN-L)
- OpenAlex
- W2050553218
- Cited by
- 115
- References
- 61
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 2 · 2022: 8 · 2021: 2 · 2020: 16 · 2019: 5 · 2018: 6 · 2017: 5 · 2016: 3 · 2015: 3 · 2014: 8 · 2013: 11 · 2012: 5
- FWCI
- 2.40
- Type
- journal article
- Language
- en
- Open access
- green
- doaj.org
- Licence
- Locations
- Neurobiology of Disease (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- National Center for Research Resources
- Japan Society for the Promotion of Science
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Keywords
- tauopathy, tau protein, FTDP-17, Caenorhabditis elegans, touch neurons, mechanosensory neurons, P301L tau, gain of toxic function, neurodegeneration, glycogen synthase kinase-3, HSP70, apoptosis, CED-3, CED-4, transgenic nematodes
- MeSH terms
- Glycogen Synthase Kinase 3 beta, Animals, Disease Models, Animal, Immunohistochemistry, Mechanoreceptors, Microtubules, Mutation, Nerve Degeneration, Nervous System, Neurons, Touch, Neurites, tau Proteins, Caenorhabditis elegans, Oxidative Stress, HSP70 Heat-Shock Proteins, Somatosensory Disorders, Tauopathies, Animals, Genetically Modified, Glycogen Synthase Kinase 3, Microscopy, Electron, Transmission
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