Expression of WIPI2B counteracts age-related decline in autophagosome biogenesis in neurons
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Abstract
Autophagy defects are implicated in multiple late-onset neurodegenerative diseases including Amyotrophic Lateral Sclerosis (ALS) and Alzheimer’s, Huntington’s, and Parkinson’s diseases. Since aging is the most common shared risk factor in neurodegeneration, we assessed rates of autophagy in mammalian neurons during aging. We identified a significant decrease in the rate of constitutive autophagosome biogenesis during aging and observed pronounced morphological defects in autophagosomes in neurons from aged mice. While early stages of autophagosome formation were unaffected, we detected the frequent production of stalled LC3B-negative isolation membranes in neurons from aged mice. These stalled structures recruited the majority of the autophagy machinery, but failed to develop into LC3B-positive autophagosomes. Importantly, ectopically expressing WIPI2B effectively restored autophagosome biogenesis in aged neurons. This rescue is dependent on the phosphorylation state of WIPI2B at the isolation membrane, suggesting a novel therapeutic target in age-associated neurodegeneration.
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With increasing age, basal autophagy and the capacity for efficient autophagosome maturation progressively deteriorate in neurons, leading to accumulation of malformed and immature autophagic vesicles, implying reduced proteostatic reserve over time.
“With increasing age, basal autophagy and the capacity for efficient autophagosome maturation progressively deteriorate in neurons, leading to accumulation of malformed and immature autophagic vesicles, implying reduced proteostatic reserve over time [382].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [382]
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Transcriptional Reprogramming of Distinct Peripheral Sensory Neuron Subtypes after Axonal Injury
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BackgroundAutophagy, aging, and age-related neurodegeneration
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Self-citationMacroautophagy and aging: The impact of cellular recycling on health and longevity
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Autophagy within the mushroom body protects from synapse aging in a non-cell autonomous manner
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Structural basis for membrane recruitment of ATG16L1 by WIPI2 in autophagy
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Self-citationSpermidine protects from age-related synaptic alterations at hippocampal mossy fiber-CA3 synapses
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Molecular Mechanisms of Autophagy Decline during Aging
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Autophagy-Lysosomal Pathway as Potential Therapeutic Target in Parkinson’s Disease
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WIPI2 positively regulates mitophagy by promoting mitochondrial recruitment of VCP
Lu, G. X., Tan, H. W. S., Schmauck‐Medina, T., Wang, L., Chen, J., Cho, Y.-L., Chen, K., Zhang, J., He, W., Wu, Y., et al. (2022) · Autophagy · doi:10.1080/15548627.2022.2052461 · Cited by 53 · see citing works
Neuronal Senescence in the Aged Brain
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Profiling of purified autophagic vesicle degradome in the maturing and aging brain
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Neuronal Autophagy: Regulations and Implications in Health and Disease
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Neuronal autophagy in the control of synapse function
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Organization of the autophagy pathway in neurons
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Olfactory dysfunction and its related molecular mechanisms in Parkinson’s disease
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The axonal endolysosomal and autophagic systems
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Self-citationNeuronal autophagy declines substantially with age and is rescued by overexpression of WIPI2
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Self-citationAging Differentially Affects Axonal Autophagosome Formation and Maturation
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Autophagy and Redox Homeostasis in Parkinson’s: A Crucial Balancing Act
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The Role of LRRK2 in Intracellular Organelle Dynamics
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Keeping synapses in shape: degradation pathways in the healthy and aging brain
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ULK3-dependent activation of GLI1 promotes DNMT3A expression upon autophagy induction
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Horizons in Human Aging Neuroscience: From Normal Neural Aging to Mental (Fr)Agility
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The Role of WIPI2, ATG16L1 and ATG12-ATG5 in Selective and Nonselective Autophagy
Campisi, D., Hawkins, N., Bonjour, K., & Wollert, T. (2025) · Journal of Molecular Biology · doi:10.1016/j.jmb.2025.169138 · Cited by 20 · see citing works
Development of small fluorescent probes for the analysis of autophagy kinetics
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Human WIPI β‐propeller function in autophagy and neurodegeneration
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Organization of Presynaptic Autophagy-Related Processes
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WIPI2b recruitment to phagophores and ATG16L1 binding are regulated by ULK1 phosphorylation
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MicroRNAs regulating autophagy: opportunities in treating neurodegenerative diseases
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Monitoring Autophagy in Human Aging: Key Cell Models and Insights
Moreno, T. M., Nieto-Torres, J. L., & Kumsta, C. (2025) · Frontiers in Bioscience-Landmark · doi:10.31083/fbl27091 · Cited by 8 · see citing works
Macroautophagy and normal aging of the nervous system: Lessons from animal models
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Maintenance and Decline of Neuronal Lysosomal Function in Aging
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Impact of Obesity and Age on Mouse Corneal Innervation at the Epithelial-Stromal Interface
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Multiple phosphatidylinositol(3)phosphate roles in retinal pigment epithelium membrane recyclingPreprint
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Hitchhiking on vesicles: a way to harness age‐related proteopathies?
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Self-citationSex does not influence neuronal autophagosome biogenesis throughout aging in mice
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Self-citationMechanisms of autophagy: the machinery of macroautophagy and points of control
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Systematic Analysis of Autophagy Identifies Atg9 Vesicles as the Origin of the PhagophorePreprint
Broadbent, D. G., Barnaba, C., & Schmidt, J. C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.03.502680 · Cited by 2 · see citing works
ATG-18 drives longevity in an HLH-30—dependent mannerPreprint
Schmauck‐Medina, T., Anisimov, A. S., Meyer, D. H., Hu, Y., Huang, Z., Wu, Y., Taylor, S. J., Takla, M., MacArthur, M. R., Mitchell, S. J., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.27.701268 · Cited by 2 · see citing works
Preservation of Autophagy May Be a Mechanism Behind Healthy Aging
Bektas, A., Schurman, S. H., Candia, J., Santiago‐Fernández, O., Kaushik, S., Cuervo, A. M., & Ferrucci, L. (2025) · Aging Cell · doi:10.1111/acel.70246 · Cited by 2 · see citing works
Lipid dysregulation as a convergent pathway linking environmental exposures to stroke
Santerre, M., Shcherbik, N., & Sawaya, B. E. (2026) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2026.1815998 · Cited by 1 · see citing works
Local autophagy impairment triggers brain-wide presynaptic remodeling and resilience
Toppe, D., Huang, S., Lützkendorf, J., Jiang, P., Suárez-Grimalt, R., Neumann, A., Zhao, Z., Lőrincz, P., Scheunemann, L., Juhász, G., et al. (2026) · The EMBO Journal · doi:10.1038/s44318-026-00847-4 · Cited by 1 · see citing works
Tsong, H., Waxham, M. N., & Stavoe, A. K. (2026) · iScience · doi:10.1016/j.isci.2026.117518 · Cited by 1 · see citing works
Self-citationLive Imaging of Autophagosome Biogenesis and Maturation in Primary Neurons
Stavoe, A. K., & Holzbaur, E. L. F. (2021) · Neuromethods · doi:10.1007/978-1-0716-1589-8_3 · Cited by 1 · see citing works
Self-citationAging Differentially Affects Axonal Autophagosome Formation and MaturationPreprint
Tsong, H., Holzbaur, E. L. F., & Stavoe, A. K. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.27.505553 · Cited by 1 · see citing works
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Green, J. R., Ojo, A. E., Gooden, M. K., Papell, L. D., Kalejaiye, T. D., & Evans, C. S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.16.700014 · Cited by 1 · see citing works
Sex does not Influence Neuronal Autophagy throughout Aging in MicePreprint
Rodruiguez, M. N., & Stavoe, A. K. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.16.633428
Self-citationAutophagy and Neurodegenerative Diseases
Barbosa, A. D., Palmer, J. E., Li, X., & Rubinsztein, D. C. (2025) · Learning materials in biosciences · doi:10.1007/978-3-031-88121-3_6
Autophagy-driven Presynaptic Reorganization as a Molecular Signature of Brain ResiliencePreprint
Toppe, D., Huang, S., Lützkendorf, J., Liu, F., Maglione, M., & Sigrist, S. J. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.09.663822
Choi, H., Lee, S.-M., & Lee, J.-A. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1762891
Autophagy mediates the hormonal regulation of neuronal homeostasis and brain aging
Rivagorda, M. (2021) · theses.fr (ABES) · doi:10.70675/e4cd7313zfed5z4ebezb547z9b4557da55e6
Interaction entre autophagie et exosomes au niveau synaptique dans la maladie de Parkinson
Sanchez-Mirasierra, I. (2023) · theses.fr (ABES) · doi:10.70675/7104d6d5z945ez494eza917zda9e6be1eea6
KIF1A-mediated trafficking is required for neuronal autophagy in human neuronsPreprint
Borland, C. T., Popolow, J., & Holzbaur, E. L. F. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.22.740140
Self-citationDifferent forms of autophagy restrict neurite outgrowth in disparate compartments in a single neuronPreprint
Mukherjee, S., Cuentas-Condori, A., Colón‐Ramos, D. A., & Stavoe, A. K. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.24.746867
Self-citation
- Authors
- Stavoe, A. K., Gopal, P. P., Gubas, A., Tooze, S. A., & Holzbaur, E. L.
- Affiliations
- University of Pennsylvania (US)
- Molecular Cell Biology of Autophagy Laboratory, The Francis Crick Institute, London, United Kingdom
- The Francis Crick Institute (GB)
- Corresponding author
- Holzbaur, Erika LF
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2019-07-16
- Volume
- 8
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6634969
- OpenAlex
- W2958740406
- Cited by
- 82
- References
- 127
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 8 · 2023: 10 · 2022: 14 · 2021: 12 · 2020: 10 · 2019: 6
- FWCI
- 7.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- The Francis Crick Institute (cc-by)
- Funders
- National Institutes of Health (R37 NS060698, F32 NS100348-01, K99 NS109286-01)
- Cancer Research UK (FC001187)
- Medical Research Council (FC001187)
- Wellcome Trust (FC001187)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- autophagosome formation, aging, neurons, autophagy, isolation membrane, LC3B, autophagy defects, age-related neurodegeneration, neurodegenerative diseases, protein phosphorylation, therapeutic target
- MeSH terms
- Autophagosomes, Autophagy-Related Proteins, Aging, Animals, Autophagy, Neurons, Gene Expression, Phosphate-Binding Proteins, Mice
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