Non-Rodent Genetic Animal Models for Studying Tauopathy: Review of Drosophila, Zebrafish, and C. elegans Models

Heparan Sulfate Glycosaminoglycans: (Un)Expected Allies in Cancer Clinical Management

(2021) Isabel Faria-Ramos et al.   Biomolecules

Seizures are a druggable mechanistic link between TBI and subsequent tauopathy

(2021) Hadeel Alyenbaawi et al.   eLife

Zebrafish disease models in drug discovery: from preclinical modelling to clinical trials

(2021) E. Elizabeth Patton et al.   NATURE REVIEWS DRUG DISCOVERY

UBE4B, a microRNA-9 target gene, promotes autophagy-mediated Tau degradation

(2021) Manivannan Subramanian et al.   Nature Communications

Neuroprotective Brain-Derived Neurotrophic Factor signaling in the TAU-P301L tauopathy zebrafish model

(2020) Clément Barbereau et al.   PHARMACOLOGICAL RESEARCH

Drosophila as a Model System to Investigate the Effects of Mitochondrial Variation on Innate Immunity

(2020) Tiina S. Salminen et al.   Frontiers in Immunology

Automated phenotyping of Caenorhabditis elegans embryos with a high-throughput-screening microfluidic platform

(2020) Huseyin Baris Atakan et al.   Microsystems & Nanoengineering

Pharmacological Treatment of Alzheimer’s Disease: Insights from Drosophila melanogaster

(2020) Xingyi Cheng et al.   INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES

cGMP via PKG activates 26S proteasomes and enhances degradation of proteins, including ones that cause neurodegenerative diseases

(2020) Jordan J. S. VerPlank et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Imaging adult C. elegans live using light‐sheet microscopy

(2020) J. VAN KRUGTEN et al.   JOURNAL OF MICROSCOPY

Live-imaging of astrocyte morphogenesis and function in zebrafish neural circuits

(2020) Jiakun Chen et al.   NATURE NEUROSCIENCE

An evaluation of Drosophila as a model system for studying tauopathies such as Alzheimer’s disease

(2019) Lovesha Sivanantharajah et al.   JOURNAL OF NEUROSCIENCE METHODS

Learning and Memory: Mind over Matter in C. elegans

(2019) Menachem Katz et al.   CURRENT BIOLOGY

Vascular defects of DYRK1A knockouts are ameliorated by modulating calcium signaling in zebrafish

(2019) Hyun-Ju Cho et al.   Disease Models & Mechanisms

Whole-animal connectomes of both Caenorhabditis elegans sexes

(2019) Steven J. Cook et al.   NATURE

Therapeutic targeting of 3′,5′-cyclic nucleotide phosphodiesterases: inhibition and beyond

(2019) George S. Baillie et al.   NATURE REVIEWS DRUG DISCOVERY

Small-molecule drug screening identifies drug Ro 31-8220 that reduces toxic phosphorylated tau in Drosophila melanogaster

(2019) Kyu-Ho Shim et al.   NEUROBIOLOGY OF DISEASE

Neurons Expressing Pathological Tau Protein Trigger Dramatic Changes in Microglial Morphology and Dynamics

(2019) Rahma Hassan-Abdi et al.   Frontiers in Neuroscience

Amentoflavone suppresses amyloid β1–42 neurotoxicity in Alzheimer's disease through the inhibition of pyroptosis

(2019) Ningning Zhao et al.   LIFE SCIENCES

Tau-Cofactor Complexes as Building Blocks of Tau Fibrils

(2019) Yann Fichou et al.   Frontiers in Neuroscience

Magnetic resonance imaging brain atrophy assessment in primary age-related tauopathy (PART)

(2019) Miguel Quintas-Neves et al.   Acta Neuropathologica Communications

Short-term exposure to dim light at night disrupts rhythmic behaviors and causes neurodegeneration in fly models of tauopathy and Alzheimer's disease

(2018) Mari Kim et al.   BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS

Small Molecule Modulation of Proteasome Assembly

(2018) Evert Njomen et al.   BIOCHEMISTRY

Tau oligomers mediate α-synuclein toxicity and can be targeted by immunotherapy

(2018) Julia E. Gerson et al.   Molecular Neurodegeneration

Pathogenic tau-induced piRNA depletion promotes neuronal death through transposable element dysregulation in neurodegenerative tauopathies

(2018) Wenyan Sun et al.   NATURE NEUROSCIENCE

Tau-targeting therapies for Alzheimer disease

(2018) Erin E. Congdon et al.   Nature Reviews Neurology

Glutamatergic nervous system degeneration in a C. elegans Tau A152T tauopathy model involves pathways of excitotoxicity and Ca 2+ dysregulation

(2018) Bikash Choudhary et al.   NEUROBIOLOGY OF DISEASE

V363I and V363A mutated tau affect aggregation and neuronal dysfunction differently in C. elegans

(2018) Federica Morelli et al.   NEUROBIOLOGY OF DISEASE

Tau Activates Transposable Elements in Alzheimer’s Disease

(2018) Caiwei Guo et al.   Cell Reports

Imbalanced Expression of Tau and Tubulin Induces Neuronal Dysfunction in C. elegans Models of Tauopathy

(2018) Tomohiro Miyasaka et al.   Frontiers in Neuroscience

Surfen and oxalyl surfen decrease tau hyperphosphorylation and mitigate neuron deficits in vivo in a zebrafish model of tauopathy

(2018) Seyedeh Maryam Alavi Naini et al.   Translational Neurodegeneration

Expression of Alzheimer-Like Pathological Human Tau Induces a Behavioral Motor and Olfactory Learning Deficit in Drosophila melanogaster

(2018) Cindy Beharry et al.   JOURNAL OF ALZHEIMERS DISEASE

Regenerating islet-derived 1α (REG-1α) protein increases tau phosphorylation in cell and animal models of tauopathies

(2018) Mireille Moussaed et al.   NEUROBIOLOGY OF DISEASE

The CeNGEN Project: The Complete Gene Expression Map of an Entire Nervous System

(2018) Marc Hammarlund et al.   NEURON

Dihydrolipoamide dehydrogenase suppression induces human tau phosphorylation by increasing whole body glucose levels in a C. elegans model of Alzheimer’s Disease

(2018) Waqar Ahmad   EXPERIMENTAL BRAIN RESEARCH

Molecular Pathogenesis of the Tauopathies

(2018) Jürgen Götz et al.   Annual Review of Pathology-Mechanisms of Disease

Heparan Sulfate Mimetics in Cancer Therapy: The Challenge to Define Structural Determinants and the Relevance of Targets for Optimal Activity

(2018) Cinzia Lanzi et al.   MOLECULES

The therapeutic potential of curcumin: A review of clinical trials

(2018) Bahare Salehi et al.   EUROPEAN JOURNAL OF MEDICINAL CHEMISTRY

An update on the use of C. elegans for preclinical drug discovery: screening and identifying anti-infective drugs

(2017) Wooseong Kim et al.   Expert Opinion on Drug Discovery

Protein Phosphorylation is a Key Mechanism in Alzheimer’s Disease

(2017) Joana Oliveira et al.   JOURNAL OF ALZHEIMERS DISEASE

Role of microtubule-associated protein tau phosphorylation in Alzheimer’s disease

(2017) Rong-hong Ma et al.   Journal of Huazhong University of Science and Technology-Medical Sciences

Survival assays using Caenorhabditis elegans

(2017) Hae-Eun H. Park et al.   MOLECULES AND CELLS

Tau-based therapies in neurodegeneration: opportunities and challenges

(2017) Chuanzhou Li et al.   NATURE REVIEWS DRUG DISCOVERY

Diversification of C. elegans Motor Neuron Identity via Selective Effector Gene Repression

(2017) Sze Yen Kerk et al.   NEURON

Shedding Light on Alzheimer’s β-Amyloidosis: Photosensitized Methylene Blue Inhibits Self-Assembly of β-Amyloid Peptides and Disintegrates Their Aggregates

(2017) Byung Il Lee et al.   Scientific Reports

Studying Autophagy in Zebrafish

(2017) Benan Mathai et al.   Cells

Complex Splicing and Neural Expression of Duplicated Tau Genes in Zebrafish Embryos

(2017) Mengqi Chen et al.   JOURNAL OF ALZHEIMERS DISEASE

Human TAUP301L overexpression results in TAU hyperphosphorylation without neurofibrillary tangles in adult zebrafish brain

(2017) Mehmet I. Cosacak et al.   Scientific Reports

Epicatechin isolated from Tripterygium wilfordii extract reduces tau-GFP-induced neurotoxicity in zebrafish embryo through the activation of Nrf2

(2016) Bo-Kai Wu et al.   BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS

Tau mutant A152T, a risk factor for FTD/PSP, induces neuronal dysfunction and reduced lifespan independently of aggregation in a C. elegans Tauopathy model

(2016) Ghulam Jeelani Pir et al.   Molecular Neurodegeneration

Curcumin improves tau-induced neuronal dysfunction of nematodes

(2016) Tomohiro Miyasaka et al.   NEUROBIOLOGY OF AGING

Reduction of Nuak1 Decreases Tau and Reverses Phenotypes in a Tauopathy Mouse Model

(2016) Cristian A. Lasagna-Reeves et al.   NEURON

Glycogen Synthase Kinase-3 (GSK-3)-Targeted Therapy and Imaging

(2016) Mukesh K. Pandey et al.   Theranostics

Stabilization of Microtubule-Unbound Tau via Tau Phosphorylation at Ser262/356 by Par-1/MARK Contributes to Augmentation of AD-Related Phosphorylation and Aβ42-Induced Tau Toxicity

(2016) Kanae Ando et al.   PLoS Genetics

HS3ST2 expression is critical for the abnormal phosphorylation of tau in Alzheimer’s disease-related tau pathology

(2015) Julia Elisa Sepulveda-Diaz et al.   BRAIN

Ubiquitous L1 Mosaicism in Hippocampal Neurons

(2015) Kyle R. Upton et al.   CELL

Using C. elegans to discover therapeutic compounds for ageing-associated neurodegenerative diseases

(2015) Xi Chen et al.   Chemistry Central Journal

Neuroanatomy: Connectome Connects Fly and Mammalian Brain Networks

(2015) Marcus Kaiser   CURRENT BIOLOGY

C. elegans locomotion: small circuits, complex functions

(2015) Mei Zhen et al.   CURRENT OPINION IN NEUROBIOLOGY

A Transparent Window into Biology: A Primer on Caenorhabditis elegans

(2015) Ann K. Corsi et al.   GENETICS

Tau-driven 26S proteasome impairment and cognitive dysfunction can be prevented early in disease by activating cAMP-PKA signaling

(2015) Natura Myeku et al.   NATURE MEDICINE

Intracerebral injection of preformed synthetic tau fibrils initiates widespread tauopathy and neuronal loss in the brains of tau transgenic mice

(2015) Eve Peeraer et al.   NEUROBIOLOGY OF DISEASE

Invited review: Animal models of tauopathies and their implications for research/translation into the clinic

(2015) Simon Dujardin et al.   NEUROPATHOLOGY AND APPLIED NEUROBIOLOGY

Invited review: Frontotemporal dementia caused bymicrotubule-associated protein taugene (MAPT) mutations: a chameleon for neuropathology and neuroimaging

(2015) Bernardino Ghetti et al.   NEUROPATHOLOGY AND APPLIED NEUROBIOLOGY

A Transparent Window into Biology: A Primer on Caenorhabditis elegans

(2015) Ann K. Corsi et al.   GENETICS

Alzheimer's disease

(2015) Colin L. Masters et al.   Nature Reviews Disease Primers

The Ubiquitin-Proteasome System in Neurodegeneration

(2014) Chris McKinnon et al.   ANTIOXIDANTS & REDOX SIGNALING

Caenorhabditis elegans: A Model System for Anti-Cancer Drug Discovery and Therapeutic Target Identification

(2014) Robert A. Kobet et al.   Biomolecules & Therapeutics

Loss of tau results in defects in photoreceptor development and progressive neuronal degeneration inDrosophila

(2014) Bonnie J. Bolkan et al.   Developmental Neurobiology

Synaptic abnormalities in a Drosophila model of Alzheimer's disease

(2014) S. D. Mhatre et al.   Disease Models & Mechanisms

Functional screening in Drosophila reveals the conserved role of REEP1 in promoting stress resistance and preventing the formation of Tau aggregates

(2014) Chiara Appocher et al.   HUMAN MOLECULAR GENETICS

Tau Monoclonal Antibody Generation Based on Humanized Yeast Models

(2014) Joëlle Rosseels et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

Oligomer Formation of Tau Protein Hyperphosphorylated in Cells

(2014) Katharina Tepper et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

The C. elegans lifespan assay toolkit

(2014) Francis Raj Gandhi Amrit et al.   METHODS

Cleavage of tau by asparagine endopeptidase mediates the neurofibrillary pathology in Alzheimer's disease

(2014) Zhentao Zhang et al.   NATURE MEDICINE

Immunophilin FKBP52 induces Tau-P301L filamentous assembly in vitro and modulates its activity in a model of tauopathy

(2014) J. Giustiniani et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Zebrafish models of human motor neuron diseases: Advantages and limitations

(2014) Patrick J. Babin et al.   PROGRESS IN NEUROBIOLOGY

A major role for Tau in neuronal DNA and RNA protection in vivo under physiological and hyperthermic conditions

(2014) Marie Violet et al.   Frontiers in Cellular Neuroscience

Barrier mechanisms in the Drosophila blood-brain barrier

(2014) Samantha J. Hindle et al.   Frontiers in Neuroscience

Activating transcription factor 4 is involved in endoplasmic reticulum stress-mediated apoptosis contributing to vascular calcification

(2013) Xiao-Hui Duan et al.   APOPTOSIS

Functional screening in Drosophila identifies Alzheimer's disease susceptibility genes and implicates Tau-mediated mechanisms

(2013) J. M. Shulman et al.   HUMAN MOLECULAR GENETICS

Genomic editing opens new avenues for zebrafish as a model for neurodegeneration

(2013) Bettina Schmid et al.   JOURNAL OF NEUROCHEMISTRY

The zebrafish reference genome sequence and its relationship to the human genome

(2013) Kerstin Howe et al.   NATURE

Transposition-Driven Genomic Heterogeneity in the Drosophila Brain

(2013) P. N. Perrat et al.   SCIENCE

Development and plasticity of the Drosophila larval neuromuscular junction

(2013) Kaushiki P. Menon et al.   Wiley Interdisciplinary Reviews-Developmental Biology

Cognitive defects are reversible in inducible mice expressing pro-aggregant full-length human Tau

(2012) Ann Van der Jeugd et al.   ACTA NEUROPATHOLOGICA

The Synaptic Accumulation of Hyperphosphorylated Tau Oligomers in Alzheimer Disease Is Associated With Dysfunction of the Ubiquitin-Proteasome System

(2012) Hwan-Ching Tai et al.   AMERICAN JOURNAL OF PATHOLOGY

Redox Proteomics Analyses of the Influence of Co-Expression of Wild-Type or Mutated LRRK2 and Tau on C. elegans Protein Expression and Oxidative Modification: Relevance to Parkinson Disease

(2012) Fabio Di Domenico et al.   ANTIOXIDANTS & REDOX SIGNALING

Single-Neuron Sequencing Analysis of L1 Retrotransposition and Somatic Mutation in the Human Brain

(2012) Gilad D. Evrony et al.   CELL

Identification of oligomers at early stages of tau aggregation in Alzheimer's disease

(2012) Cristian A. Lasagna-Reeves et al.   FASEB JOURNAL

Inhibition of tau aggregation in a novel Caenorhabditis elegans model of tauopathy mitigates proteotoxicity

(2012) Chronis Fatouros et al.   HUMAN MOLECULAR GENETICS

Protective Role of Cell Division Cycle 48 (CDC48) Protein against Neurodegeneration via Ubiquitin-Proteasome System Dysfunction during Zebrafish Development

(2012) Shintaro Imamura et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

Tau Oligomers Impair Artificial Membrane Integrity and Cellular Viability

(2012) Katharina Flach et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

In Vivo Imaging of Disease-Related Mitochondrial Dynamics in a Vertebrate Model System

(2012) G. Plucinska et al.   JOURNAL OF NEUROSCIENCE

Automated high-throughput neurophenotyping of zebrafish social behavior

(2012) Jeremy Green et al.   JOURNAL OF NEUROSCIENCE METHODS

Macroautophagy deficiency mediates age-dependent neurodegeneration through a phospho-tau pathway

(2012) Keiichi Inoue et al.   Molecular Neurodegeneration

Trans-Synaptic Spread of Tau Pathology In Vivo

(2012) Li Liu et al.   PLoS One

A Core Metabolic Enzyme Mediates Resistance to Phosphine Gas

(2012) D. I. Schlipalius et al.   SCIENCE

In Vivo labeling of zebrafish motor neurons using an mnx1 enhancer and Gal4/UAS

(2011) Taras A. Zelenchuk et al.   GENESIS

Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation

(2011) Surendra S. Ambegaokar et al.   HUMAN MOLECULAR GENETICS

NMNAT suppresses Tau-induced neurodegeneration by promoting clearance of hyperphosphorylated Tau oligomers in a Drosophila model of tauopathy

(2011) Yousuf O. Ali et al.   HUMAN MOLECULAR GENETICS

Important neuronal toxicity of microtubule-bound Tau in vivo in Drosophila

(2011) Yasmina Talmat-Amar et al.   HUMAN MOLECULAR GENETICS

MSUT2 is a determinant of susceptibility to tau neurotoxicity

(2011) Chris R. Guthrie et al.   HUMAN MOLECULAR GENETICS

Initiation of Locomotion in Adult Zebrafish

(2011) A. Kyriakatos et al.   JOURNAL OF NEUROSCIENCE

Tau-Induced Defects in Synaptic Plasticity, Learning, and Memory Are Reversible in Transgenic Mice after Switching Off the Toxic Tau Mutant

(2011) A. Sydow et al.   JOURNAL OF NEUROSCIENCE

BrainAligner: 3D registration atlases of Drosophila brains

(2011) Hanchuan Peng et al.   NATURE METHODS

Dynamic interactions between transposable elements and their hosts

(2011) Henry L. Levin et al.   NATURE REVIEWS GENETICS

Dynamic association of tau with neuronal membranes is regulated by phosphorylation

(2011) Amy M. Pooler et al.   NEUROBIOLOGY OF AGING

Post-translational modifications of tau protein: Implications for Alzheimer's disease

(2011) Ludovic Martin et al.   NEUROCHEMISTRY INTERNATIONAL

Implicating Calpain in Tau-Mediated Toxicity In Vivo

(2011) James B. Reinecke et al.   PLoS One

Soluble hyper-phosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo

(2010) Catherine M. Cowan et al.   ACTA NEUROPATHOLOGICA

Tau protein degradation is catalyzed by the ATP/ubiquitin-independent 20S proteasome under normal cell conditions

(2010) Tilman Grune et al.   ARCHIVES OF BIOCHEMISTRY AND BIOPHYSICS

Locomotor behaviors in zebrafish (Danio rerio) larvae

(2010) Ruth M. Colwill et al.   BEHAVIOURAL PROCESSES

Dendritic Function of Tau Mediates Amyloid-β Toxicity in Alzheimer's Disease Mouse Models

(2010) Lars M. Ittner et al.   CELL

Live imaging of apoptotic cells in zebrafish

(2010) Tjakko J. van Ham et al.   FASEB JOURNAL

A DNA damage-activated checkpoint kinase phosphorylates tau and enhances tau-induced neurodegeneration

(2010) Kanae Iijima-Ando et al.   HUMAN MOLECULAR GENETICS

Nuclear Tau, a Key Player in Neuronal DNA Protection

(2010) Audrey Sultan et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

Differential Effects of Tau on the Integrity and Function of Neurons Essential for Learning in Drosophila

(2010) S. Kosmidis et al.   JOURNAL OF NEUROSCIENCE

Glial Fibrillary Tangles and JAK/STAT-Mediated Glial and Neuronal Cell Death in a Drosophila Model of Glial Tauopathy

(2010) K. J. Colodner et al.   JOURNAL OF NEUROSCIENCE

Caspase activation precedes and leads to tangles

(2010) Alix de Calignon et al.   NATURE

Regulation of Mammalian Autophagy in Physiology and Pathophysiology

(2010) Brinda Ravikumar et al.   PHYSIOLOGICAL REVIEWS

Lysosomal Dysfunction Promotes Cleavage and Neurotoxicity of Tau In Vivo

(2010) Vikram Khurana et al.   PLoS Genetics

In VivoImaging ofCaenorhabditis elegansGlycans

(2009) Scott T. Laughlin et al.   ACS Chemical Biology

Essential role of tau phosphorylation in adult hippocampal neurogenesis

(2009) Xiao-Ping Hong et al.   HIPPOCAMPUS

SUT-2 potentiates tau-induced neurotoxicity in Caenorhabditis elegans

(2009) Chris R. Guthrie et al.   HUMAN MOLECULAR GENETICS

A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation

(2009) Dominik Paquet et al.   JOURNAL OF CLINICAL INVESTIGATION

Unlocking the secrets of the genome

(2009) Susan E. Celniker et al.   NATURE

Transmission and spreading of tauopathy in transgenic mouse brain

(2009) Florence Clavaguera et al.   NATURE CELL BIOLOGY

Brain-derived neurotrophic factor in neurodegenerative diseases

(2009) Chiara Zuccato et al.   Nature Reviews Neurology

Temporally-Controlled Site-Specific Recombination in Zebrafish

(2009) Stefan Hans et al.   PLoS One

A Tetrahedral Transition State at the Active Sites of the 20S Proteasome Is Coupled to Opening of the α-Ring Channel

(2009) Pawel A. Osmulski et al.   STRUCTURE

Tau phosphorylation: the therapeutic challenge for neurodegenerative disease

(2009) Diane P. Hanger et al.   TRENDS IN MOLECULAR MEDICINE

Deciphering complex mechanisms in neurodegenerative diseases: the advent of systems biology

(2009) Farshid Noorbakhsh et al.   TRENDS IN NEUROSCIENCES

Dissociation of tau toxicity and phosphorylation: role of GSK-3β, MARK and Cdk5 in a Drosophila model

(2008) Shreyasi Chatterjee et al.   HUMAN MOLECULAR GENETICS

Strategies for automated analysis of C. elegans locomotion

(2008) Steven D. Buckingham et al.   INVERTEBRATE NEUROSCIENCE

I PP2A 1 Affects Tau Phosphorylation via Association with the Catalytic Subunit of Protein Phosphatase 2A

(2008) She Chen et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

In Vivo Imaging Reveals Dissociation between Caspase Activation and Acute Neuronal Death in Tangle-Bearing Neurons

(2008) T. L. Spires-Jones et al.   JOURNAL OF NEUROSCIENCE

The amino terminus of tau inhibits kinesin-dependent axonal transport: Implications for filament toxicity

(2008) Nichole E. LaPointe et al.   JOURNAL OF NEUROSCIENCE RESEARCH

Gal4/UAS Transgenic Tools and Their Application to Zebrafish

(2008) Marnie E. Halpern et al.   Zebrafish

Generation of Stable Transgenic C. elegans Using Microinjection

(2008) Laura A. Berkowitz et al.   Jove-Journal of Visualized Experiments

A Caenorhabditis elegans model of tau hyperphosphorylation: Induction of developmental defects by transgenic overexpression of Alzheimer's disease-like modified tau

(2007) Roland Brandt et al.   NEUROBIOLOGY OF AGING