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Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons
Open accessAbstract
Autophagy is an essential cellular degradation pathway in neurons; defects in autophagy are sufficient to induce neurodegeneration. In this paper, we investigate autophagosome dynamics in primary dorsal root ganglion neurons. Autophagosome biogenesis occurs distally in a constitutive process at the neurite tip. Autophagosomes initially move bidirectionally and then switch to unidirectional, processive movement toward the cell soma driven by dynein. Autophagosomes copurify with anterograde and retrograde motors, suggesting that the activity of bound kinesin motors is effectively down-regulated to yield robust retrograde motility driven by dynein. Both organelle and soluble cargoes are internalized into autophagosomes, including mitochondria and ubiquitin. As autophagosomes move distally to proximally, they undergo maturation and become increasingly acidified, consistent with the formation of an autolysosomal compartment that may more efficiently degrade cargo. This maturation is accompanied by a switch to bidirectional motility characteristic of lysosomes. Together, autophagosome biogenesis and maturation in primary neurons is a constitutive process that is spatially and temporally regulated along the axon.
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“Lysosomes fuse with autophagosome in the distal axon, and they mature on the way back to the soma (Maday et al., 2012).”
From TMEM55B promotes anterograde transport and distal axonal distribution of LAMP1-positive organelles (2026) · cites this paper as Maday et al., 2012
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Autophagosome trafficking along axons was recently described.31”
From Measurement of autophagy flux in the nervous system in vivo (2013) · cites this paper as [31]
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In the citing paper
“Remarkably, the velocities obtained were in the same order of magnitude to the ones recently reported for autophagosomes in axons of DRGs obtained from LC3-GFP transgenic mice.31”
From Measurement of autophagy flux in the nervous system in vivo (2013) · cites this paper as [31]
In the citing paper
“Newly-formed autophagosomes in neuronal processes undergo retrograde transport to the soma and proximal segments of neurites to fuse with somatodendritic lysosomes for cargo degradation, with maturation and acidification of the autophagosomal lumen developing en passant [370,372,374].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [372]
In the citing paper
“Autophagy initiation typically begins outside of the soma, in the distal axon tip [370,372,373].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [372]
In the citing paper
“Bidirectional movements have been reported for a variety of organelles and vesicles (Welte, 2004), including even those that move persistently in one direction, such as mitochondria (Saxton and Hollenbeck, 2012), autophagosomes (Maday et al., 2012), and vesicles (Encalada et al., 2011), as they undergo axonal transport.”
From Microtubule motors transport phagosomes in the RPE, and lack of KLC1 leads to AMD-like pathogenesis (2015) · cites this paper as Maday et al., 2012
In the citing paper
“puncta may be numerous in neurites, especially within dystrophic swellings and, in many cases, these vacuoles are amphisomes or autolysosomes, reflecting the delayed or inhibited degradation of LC3 despite the presence of abundant hydrolase activity [77,84].”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [84]
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Sidibe, D. K., Kulkarni, V. V., Dong, A., Herr, J. B., & Maday, S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.08.503181 · Cited by 3
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BackgroundInfluentialSelf-citationA retrograde transit filter mediated by optineurin controls mitostasis in distal axonsPreprint
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“…of dorsal root ganglion neurons with mCherry-EGFP-LC3 plasmid showed a reducing gradient of autophagosomes positive for both mCherry and EGFP between distal and proximal axon regions, implying that autophagosomes are transported to proximal axons become fully acidified (Maday et al., 2012).”
BackgroundInfluentialAxonal transport proteins: What they are and how they relate to depressive behaviors
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“…of survival signals from the synapse to the cell body, and in the transport mechanisms that remove misfolded proteins and cellular debris from the axon (Okada et al., 1995; Bhattacharyya et al., 2002; Delcroix et al., 2003; Klopfenstein and Vale, 2004; Pack-Chung et al., 2007; Maday et al., 2012).”
BackgroundRoşianu, F., Mihaylov, S. R., Eder, N., Martiniuc, A., Claxton, S., Flynn, H. R., Jalal, S., Domart, M., Collinson, L., Skehel, M. J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.28.486054 · Cited by 1
“It is also known that autophagosomes formed at axons and presynaptic boutons travel to neuronal cell bodies for lysosomal fusion and degradation (Maday & Holzbaur, 2016; Maday et al, 2012).”
BackgroundResultAging 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
Self-citationCombinatorial selective ER-phagy remodels the ER during neurogenesis v3Preprint
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Autophagic enhancer rescues Tau accumulation in a stem cell model of frontotemporal dementiaPreprint
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“Late endosomes predominantly undergo long-range retrograde transport while simultaneously acidifying and maturing into lysosomes, and ultimately fusing with mature lysosomes enriched in the cell body 62 .”
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“…an important role in clearing damaged organelles and old proteins from axons, engage with endolysosomes and undergo retrograde transport so that cargo can be degraded in the highly acidic lysosomes in the soma (Cheng et al., 2015a; Kuijpers et al., 2021; Maday et al., 2012; Maday & Holzbaur, 2014).”
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“Autophagosomes form at the terminus of neurites (the axon and dendrites) or along their length, and transport towards the cell body collecting debris for breakdown (Maday, Wallace and Holzbaur, 2012).”
Winter, J., Landoni, J. C., Holt, K. B., Nejma, S. B., Durmus, E. B., Kleele, T., Koslover, E. F., & Manley, S. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.08.692722 · Cited by 1
Local ROS and inefficient autophagosome formation limit Optineurin-mediated mitophagy in neuronsPreprint
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Microglia extract neuronal proteolytic organelles via skoupocytosisPreprint
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“Eventually, they fuse with lysosomes, which are enriched in the proximal axon and the cell soma 9–12 .”
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“In C. elegans, as in vertebrate neurons, retrograde transport of autophagosomes depends on the dynein complex (Cheng et al., 2015; Ikenaka et al., 2013; Katsumata et al., 2010; Maday et al., 2012) (Figures 3A-3C).”
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“However, as autophagosomes are highly mobile (Cheng et al., 2015b; Maday et al., 2012), it remains unclear whether they arise within boutons or simply accumulate there.”
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“These observations underscore the notion that autophagy biogenesis in neurons occurs distally in axons with retrograde transport of autophagosomes to the soma where lysis occurs (Maday et al., 2012).”
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Metadata
- Authors
- Maday, S., Wallace, K. E., & Holzbaur, E. L. F.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Maday, Sandra
- Holzbaur, Erika L.F.
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2012-02-13
- Volume
- 196
- Issue
- 4
- Pages
- 407-417
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC3283992
- OpenAlex
- W2137686667
- Cited by
- 681
- References
- 30
- Citations by year
- 2026: 34 · 2025: 45 · 2024: 56 · 2023: 37 · 2022: 66 · 2021: 65 · 2020: 52 · 2019: 55 · 2018: 53 · 2017: 39 · 2016: 47 · 2015: 52 · 2014: 38 · 2013: 27 · 2012: 13
- FWCI
- 31.13
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R37NS060698, NS060698, R01NS060698)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- autophagosomes, autophagy, dorsal root ganglion neurons, axonal transport, dynein, kinesin, retrograde transport, autophagosome maturation, autolysosomes, lysosomes, mitochondria, ubiquitin, neurodegeneration
- MeSH terms
- Superoxide Dismutase-1, Animals, Autophagy, Axons, Biological Transport, Cell Compartmentation, Dyneins, Fluorescent Antibody Technique, Image Processing, Computer-Assisted, Mice, Transgenic, Neurons, Phagosomes, Superoxide Dismutase, Green Fluorescent Proteins, Mice
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