Cited by 328Autophagy in Disease and TherapyUbiquitin and proteasome pathwaysGenetics, Aging, and Longevity in Model Organisms

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Autophagy in Neurons

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Stavoe, Andrea K.H., Holzbaur, Erika L.F.·2019·Annual Review of Cell and Developmental Biology

DOI 10.1146/annurev-cellbio-100818-125242PMC PMC6996145

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Abstract

Autophagy is the major cellular pathway to degrade dysfunctional organelles and protein aggregates. Autophagy is particularly important in neurons, which are terminally differentiated cells that must last the lifetime of the organism. There are both constitutive and stress-induced pathways for autophagy in neurons, which catalyze the turnover of aged or damaged mitochondria, endoplasmic reticulum, other cellular organelles, and aggregated proteins. These pathways are required in neurodevelopment as well as in the maintenance of neuronal homeostasis. Here we review the core components of the pathway for autophagosome biogenesis, as well as the cell biology of bulk and selective autophagy in neurons. Finally, we discuss the role of autophagy in neuronal development, homeostasis, and aging and the links between deficits in autophagy and neurodegeneration.

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1 retracted

RETRACTED ARTICLE: Parkin and PINK1 mitigate STING-induced inflammation
Sliter, D. A., Martinez, J., Hao, L., Chen, X., Sun, N., Fischer, T. D., Burman, J. L., Li, Y., Zhang, Z., Narendra, D. P., et al. (2018) · Nature · doi:10.1038/s41586-018-0448-9 · Cited by 1,287 · cited 1×
“The importance of more fully understanding mitochondrial quality control is emphasized by the observation that both PINK1 and Parkin knockout mice are susceptible to stress, and that this in turn leads to inflammation (Sliter et al. 2018).”
Background
Retracted
p62/SQSTM1 Binds Directly to Atg8/LC3 to Facilitate Degradation of Ubiquitinated Protein Aggregates by Autophagy
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Parkin is recruited selectively to impaired mitochondria and promotes their autophagy
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“While many questions remain, the importance of autophagy in neurons is clear, as the neuron-specific ablation of autophagy leads to neurodegeneration (Hara et al. 2006, Komatsu et al. 2006).”
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“While many questions remain, the importance of autophagy in neurons is clear, as the neuron-specific ablation of autophagy leads to neurodegeneration (Hara et al. 2006, Komatsu et al. 2006).”
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p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death
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BackgroundInfluential
PINK1 Is Selectively Stabilized on Impaired Mitochondria to Activate Parkin
Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D.-F., Gautier, C. A., Shen, J., Cookson, M. R., & Youle, R. J. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000298 · Cited by 2,944
The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy
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“Depletion of a single receptor such as OPTN may induce a delay in mitochondrial engulfment (Moore & Holzbaur 2016) but does not block mitophagy completely (Lazarou et al. 2015), indicating some redundancy in the system.”
Background
A ubiquitin-like system mediates protein lipidation
Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M., et al. (2000) · Nature · doi:10.1038/35044114 · Cited by 2,139 · cited 1×
“Elongation of the autophagosome membrane is mediated by the aptly named elongation complex, composed of two ubiquitin-like conjugation complexes (Ichimura et al. 2000, Mizushima et al. 1998).”
Background
Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice.
Komatsu, M., Waguri, S., Koike, M., Sou, Y.-S., Ueno, T., Hara, T., Mizushima, N., Iwata, J.-I., Ezaki, J., Murata, S., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.035 · Cited by 2,124 · cited 3×
“Likewise, conditionally knocking out Atg7 in Purkinje cells using the Pcp2 promoter in mice did not appear to affect dendrites, but did lead to neuronal and axonal dystrophy, degeneration of axon terminals, and eventual neuronal death (Komatsu et al. 2007b).”
Background

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Pragati, Chanu, S., & Sarkar, S. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134622 · Cited by 3
The lncRNA TPT1-AS1 promotes the survival of neuroendocrine prostate cancer cells by facilitating autophagy.
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Molecular switches of SQSTM1: the impact of post-translational modifications on autophagy and neurodegeneration
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The role of energy deficit in autophagy failure in Parkinson’s disease
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“Because neurons cannot dilute damaged cellular components through cell division, eÿcient protein and organelle quality control is essential for neuronal homeostasis and survival (Stavoe and Holzbaur, 2019), while dysfunction of either pathway contributes to neurodegeneration (Passi et al., 2026).”
Neurodegeneration risk variants promote lysosomal TMEM106B fibril accumulationPreprint
Replogle, J. M., Marks, J. D., Fernandez, M. G., Yuan, H., Yu, D., Winters, E., Jawahar, V. M., Deshmukh, R., Sutanto, R., Kowal, I., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.26.714634 · Cited by 6
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Aging-Related Changes in the Injury Response of the Peripheral Nervous System
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“…is a dynamic, lysosome-driven process that supports not only intracellular quality control but also key neuronal activities, including axonal maintenance, synaptic function, neuronal connectivity, and stem cell development (Stavoe and Holzbaur, 2019; Valencia et al., 2021; B et al., 2014).”
Targeting neurodegenerative diseases with bioactive oligosaccharides: Mechanisms and prospects
Ni, Q., Zhang, S., Jia, G., Wang, Y., Guo, Y., & Liu, Y. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.115560 · Cited by 2
Comprehensive Proteomic Analysis of the Differential Expression of 83 Proteins Following Intracortical Microelectrode Implantation
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Spatiotemporal analysis of axonal autophagosome-lysosome dynamics reveals limited fusion events trigger two-step maturationPreprint
Cason, S. E., Mogre, S. S., Holzbaur, E., & Koslover, E. F. (2022) · bioRxiv · doi:10.1101/2022.02.17.480915 · Cited by 2
Self-citation
Autophagy Dysfunction as a Phenotypic Readout in hiPSC-Derived Neuronal Cell Models of Neurodegenerative Diseases
Sun, C., Rosenstock, T. R., Cohen, M. A., & Sarkar, S. (2021) · Methods in molecular biology · doi:10.1007/7651_2021_420 · Cited by 3
Autophagy Flux Is Remodeled Sex‐ and Cell Type‐Specifically During Human Aging, and Is Linked to Reduced Physical Function in Older Adults
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“As long-lived, post-mitotic cells, neurons rely heavily on autophagy to maintain proteostasis, and dysfunctional auto-phagy has been linked to loss of proteostasis and neurodegeneration (Chou et al. 2025; Nixon and Rubinsztein 2024; Stavoe and Holzbaur 2019).”
Mitophagy in neuronal health and disease: from mechanisms to neurodegeneration
Basak, B., Riley, J. F., Nataraj, N. M., & Holzbaur, E. L. F. (2026) · Journal of Clinical Investigation · doi:10.1172/jci199847 · Cited by 1
Self-citation
Metformin Alleviates Cadmium-Induced Autophagic Flux Impairment-Dependent Apoptosis by Activating AMPK in Neuronal Cells
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Copper Dyshomeostasis Affects α-Synuclein Clearance Mechanisms in Parkinson’s Disease: Insights from In Vitro Models and Translational Evidence
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miR-133b-3p Mitigates D-Galactose-Induced Hippocampal Neuron Aging Through Autophagy Regulation via the MAPK/ERK Signaling Pathway
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Differential response of neurons to autophagy modulation in Huntington’s disease
Sharma, A., Rao, S., Manjithaya, R. R., & Sheeba, V. (2025) · Autophagy Reports · doi:10.1080/27694127.2025.2519102 · Cited by 1
TLR3 Knockdown Attenuates Pressure‐Induced Neuronal Damage In Vitro
Lin, L., Lv, Z., Zhou, C., Zhu, T., Hu, Y., Sun, X., Zhou, H., Wang, M., Lin, Y., Gu, G., et al. (2024) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.70276 · Cited by 3
A decrease in Fkbp52 alters autophagosome maturation and A152T-tau clearance in vivo
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BackgroundInfluential
Coenzyme Q10 attenuates neurodegeneration in the cerebellum induced by chronic exposure to tramadol.
Keyhanifard, M., Javan, R., Disfani, R. A., Bahrami, M., Mirzaie, M. S., Taghiloo, S., Mokhtari, H., Nasiry, D., Aghajani, Z. S., & Shooraj, M. (2023) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2023.102367 · Cited by 1
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The G protein-Coupled Metabotropic Glutamate Receptor 1 controls neuronal macroautophagyPreprint
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“The maturation (Ban et al., 2013; Clark et al., 2018; Shen and Ganetzky, 2009; Stavoe et al., 2016; Stavoe and Holzbaur, 2019) and survival (Hara et al., 2006; Komatsu et al., 2006; Komatsu et al., 2007) of neurons is dependent on autophagy and its dysfunction is linked to neurodegenerative…”
Background
The Role of Panax Notoginseng Saponins on Neuronal Oxidative Stress and Autophagy Response in Craniocerebral Injury Model Rats
Long, L., & Wang, L. (2024) · Journal of Biobased Materials and Bioenergy · doi:10.1166/jbmb.2024.2433 · Cited by 1
Vitamin D binding protein in ventral CA3 of the hippocampus drives stress-induced depression
Kong, Y., Huang, Z., Zeng, C., Xu, Y., & Zhang, Z. (2026) · Science Advances · doi:10.1126/sciadv.aeh9563
Dental Pulp Stem Cell-Derived Small Extracellular Vesicle miR-100-5p Attenuates Neuronal Oxidative Stress via Regulating the mTOR-Autophagy Signaling Axis
Zhou, W.-L., Zhao, Y.-F., Yang, F.-T., Zhang, W.-S., & Zhang, X.-Z. (2026) · Cells · doi:10.3390/cells15201843
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Receptor-specific ER-phagy in neurodegenerative diseases: Molecular mechanisms and emerging therapeutic opportunities
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Penconazole induces developmental neurotoxicity by activating autophagy and neuronal apoptosis in zebrafish.
Jiang, X., Zhang, Z.-K., Gong, Y.-C., Jiang, T., Liu, J., Hu, J., & Zhou, W.-D. (2026) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2026.120858
Neuropeptide Y and brain ageing: an updated scoping review on the role of autophagy
Cheah, S. Y., Kumari, Y., Sahardi, N. F. N. M., Gany, S. L. S., Abdullah, N. A. H., Makpol, S., & Jaafar, F. (2026) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2026.1888512
Manganese Dioxide Nanoparticles Protect PC12 Cells Against H2O2-Induced Oxidative Stress Injury by Regulating PI3K/Akt-Mediated Autophagy
Zeng, W., Zhou, D., Wang, T., Ma‐Högemeier, Z., Cai, S., Liu, B., Song, C., Guo, L., Zhai, R., Song, X., et al. (2026) · Pharmaceutics · doi:10.3390/pharmaceutics18091156
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An Explanation for Dreaming Based on Neuronal MaintenancePreprint
Grinde, B. (2026) · Qeios · doi:10.32388/drh3h4.3
Roles of autophagy in brain homeostasis and disease
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Cell Death in Neurodegenerative Diseases: Molecular Mechanisms and Therapeutic Targets
Li, T., Zhang, Q., Wu, Y., & Huang, R. (2026) · MedComm · doi:10.1002/mco2.70915
Local translation of endosome-associated lc3b mRNA in axons contributes to endosomal clearance
Pappacena, F., Caterino, C., de Pretis, S., Sironi, C., Esposito, A., Cesare, G., Bruni, M., & Cioni, J.-M. (2026) · EMBO Reports · doi:10.1038/s44319-026-00867-5
“Owing to their central and validated functional roles, LC3B and SQSTM1 are widely used as canonical markers for monitoring autophagic activity, including in neurons (Stavoe and Holzbaur, 2019).”
The embedding of stress: mitophagy as a mechanism for the central nervous system (CNS) programming and lifelong disease vulnerability
Wang, M., Zhang, Z., Sha, Z., Zhang, F., & Bao, K. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1808059
“Because neurons are post-mitotic and irreplaceable throughout life, mitophagy is essential for managing proteotoxic stress and maintaining homeostasis in distal compartments (Stavoe and Holzbaur, 2019), and it changes markedly with age.”
Mechanisms of autophagy–lysosome pathway impairment in Alzheimer's disease
Lü, K., Lu, Y., Tang, R., Dong, X., Zhuang, P., Gao, Y., Cheng, M., Wang, Y., & Wang, Y. (2026) · Journal of Alzheimer s Disease · doi:10.1177/13872877261460879
“158 Increasing evidence has shown that neuronal autophagy defects can lead to abnormal axon development and neurodegeneration.”
Impaired Activity-Regulated Proteostasis: A Shared Mechanism in Neurodevelopmental Disorders
Pandey, K. (2026) · Biological Psychiatry · doi:10.1016/j.biopsych.2026.06.032
An ROS-responsive, RGC-targeted nanotherapeutic strategy with a TRPV4 antagonist restores autophagic flux and protects RGCs in a rat model of chronic ocular hypertension
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“Autophagy is an essential degradative pathway that maintains cellular homeostasis and exerts a classical "double-edged sword" effect on neurons [16–18].”
The EMB/ATG7-mediated autophagic process regulates neurite outgrowth and promotes enteric neuronal development
Wu, L., Wang, J., Xiao, J., Meng, X., Wang, J., Mao, H., You, J., Li, Z., Chen, K., Wang, Q., et al. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2601752123
Nicotinamide nucleotide transhydrogenase deficiency impairs neuronal function via energy metabolism dysregulation in Alzheimer's disease
Wan, X., Lu, W., Liu, S., Zhao, Y., Hu, J., Ding, X., Gu, P., Zou, Y., Jiang, B., & Yang, Y. (2026) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2026.05.341
Signaling cross-talk driving neuronal survival, death and inflammation in neurodegeneration
Singh, L. (2026) · Neurophysiology · doi:10.1007/s11062-026-10003-7
Unknotting the Role of circRNAs and IGF2BP3 in Alzheimer’s Disease
Firdous, S. M., Jayathilaka, S. N. S., Marick, S., & Porel, P. (2026) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-026-01724-8
“Another circRNA, circHDAC9, has been reported to be decreased in AD brain tissue and is associated with increased Aβ production through the miR-138/SIRT1 pathway (Stavoe & Holzbaur, 2019).”
Combined Transcriptomic and Proteomic Profiling Uncovers Developmental Dynamics of Autophagy in the Cortex
Nuzzolillo, F., Braccia, C., Andolfo, A., de Pretis, S., & Palmieri, M. (2026) · Biomedicines · doi:10.3390/biomedicines14040812
“It is particularly important in neurons, which are post-mitotic cells, metabolically very active, and highly vulnerable to any loss of cellular homeostasis [2].”
Dysregulation of a novel autophagosome-mitochondria contact contributes to autophagy dysfunction and neurodegeneration in tauopathyPreprint
Jia, N., Guan, H., Zuo, Y., Jeong, Y. Y., Amireddy, N., Rajapaksha, G., Gonzalez, C. U., Jaber, N., Lee, Y.-K., Nissenbaum, M., et al. (2026) · bioRxiv · doi:10.64898/2026.03.23.713823
Developmental Elimination of Electrical Synapses by UNC-51/UNC-76-Mediated Vesicular TransportPreprint
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Lost in translation: absence of KIAA1324/ELAPOR1 protein in pathological TDP-43-affected neurons in ALS/FTD
Cao, M. C., Swanson, M. E. V., Basak, I., McDonald, K., Arnold, F. J., Stockford, C. M., Guo, G., Curtis, M. A., Faull, R. L. M., Hughes, S. M., et al. (2026) · Acta Neuropathologica Communications · doi:10.1186/s40478-026-02237-7
Decoding the brain’s ATG8 paralog code: LC3–GABARAP specialization at synapses and the astrocyte–neuron interface
Choi, H., Lee, S.-M., & Lee, J.-A. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1762891
“Presynaptic autophagosomes typically originate in distal axons and undergo retrograde transport toward the soma for lysosomal clearance, a transport logic shared with mitophagosomes (Maday et al., 2012; Maday and Holzbaur, 2014; Stavoe and Holzbaur, 2019).”
Influential
ALKBH5-mediated autophagic flux impairment is involved in bilirubin neurotoxicity.
Zhou, J.-F., Liao, S.-N., Zhang, C., Li, G.-L., Zheng, F.-L., Yu, G.-X., Hu, H., Shao, W.-Y., Guo, Z.-K., Wu, S.-Y., et al. (2026) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2026.111940
iTBS Improves Behavioral Abnormalities and Synaptic Defects in Fmr1 KO Rats by Regulating the Autophagy Pathway
Deng, Z., Wu, S., Zhao, Y., Song, A., Wu, H., An, Z., Wang, F., & Xu, X. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-05571-4
“This process plays a crucial role in the survival and development of neurons and is closely associated with various neurodegenerative diseases [5, 6] and psychiatric disorders [7–11].”
Protective Effect of SESN2 on Glutamate Neurotoxicity via Keap1‐Nrf2 Pathway‐Mediated Mitophagy
Zhang, X., Li, Y., Zhou, W., & Jiang, Q. (2025) · Journal of biochemical and molecular toxicology · doi:10.1002/jbt.70642
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STED-FCS in subdiffraction limit volumes reveals altered diffusion in live cell applications
Zobiak, B., Andres‐Alonso, M., Wang, Y., Mohammadi, B., Gorzelanny, C., Altmeppen, H., Yin, S.-T., & Failla, A. (2025) · bioRxiv · doi:10.1515/mim-2025-0032
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Sertad1 is elevated and plays a necessary role in neuron loss and cognitive impairment in a mouse model of Alzheimer's disease
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Autophagy Modulation by Antidepressants: Mechanisms and Implications
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“…and aims to restore equilibrium by promoting catabolic processes like autophagy and fatty acid oxidation while suppressing Like other cells, neurons rely on autophagy as a constant cleaning process to eliminate harmful proteins and dam - aged organelles, even in the absence of stress [ 14 ].”
Influential
Bioenergetic and protein processing imbalances in iPSC-dopamine neurons from individuals with idiopathic Parkinson's disease
Bernard, K., Corenblum, M. J., Tonino, P., & Madhavan, L. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.107222
“Specifically, mitochondrial dysfunction is linked to the impairment of autophagy through the accumulation of damaged mitochondria because of defective mitochondrial turnover, as well as through the depletion of functional lysosomes which are core to the autophagy process (Fleming et al., 2022; Palmer et al., 2025).”
circFKBP8(5S,6)-encoded protein promotes stress susceptibility in mice by down-regulating dopamine D3 receptor expression and its downstream AMPK/mTOR/ULK1 autophagy signaling
Xu, D., Huang, Z., Zhang, G., Jiao, J., Cao, Y., Liu, M., Kong, Y., & Zhang, Z. (2025) · Genes & Diseases · doi:10.1016/j.gendis.2025.101718
“43,44 45 — 47 In opposition to this, there is research evidence that inhibition of neuronal autophagy is associated with an increase in synaptic proteins.”

Authors: Stavoe, A. K. H., & Holzbaur, E. L. F.
Affiliations: University of Pennsylvania (US)
ORCID: Stavoe, Andrea K.H.
Holzbaur, Erika L.F.
Venue: Annual Review of Cell and Developmental Biology
Publisher: Annual Reviews
Published: 2019-10-06
Volume: 35
Issue: 1
Pages: 477-500
ISSN: 1081-0706 (ISSN-L)
1530-8995
DOI: 10.1146/annurev-cellbio-100818-125242
PMC: PMC6996145
OpenAlex: W2963539474
Cited by: 328
References: 157
Citations by year: 2026: 41 · 2025: 56 · 2024: 59 · 2023: 61 · 2022: 58 · 2021: 28 · 2020: 21 · 2019: 3
FWCI: 4.01
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Annual Review of Cell and Developmental Biology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute of Neurological Disorders and Stroke (K99NS109286, R37NS060698)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords: autophagy, neurons, autophagosome formation, selective autophagy, bulk autophagy, mitochondrial turnover, protein aggregation, brain development, neuronal homeostasis, aging, neurodegeneration, endoplasmic reticulum, organelle degradation
MeSH terms: Autophagosomes, Animals, Autophagy, Axons, Dendrites, Endoplasmic Reticulum, Homeostasis, Humans, Memory, Mitochondria, Neurons, Synapses, Neurodegenerative Diseases, Proteasome Endopeptidase Complex, Ubiquitination, Unfolded Protein Response

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