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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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Citations
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“Since the fusion of AVs with lysosomes during retrograde transport to form mature autolysosomes is an essential step for the degradation of autophagic substrates and thus for the clearance of autophagosomes [4], we wondered if the fusion of AVs and lysosomes is affected after axonal injury.”
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Oettinger, D., & Yamamoto, A. (2025) · Journal of Molecular Biology · doi:10.1016/j.jmb.2025.169219 · Cited by 10
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Disease-causing mutated ATLASTIN 3 is excluded from distal axons and reduces axonal autophagy
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BackgroundSelvarasu, K., Singh, A. K., Dakshinamoorthy, A., Sreenivasmurthy, S. G., Iyaswamy, A., Radhakrishnan, M., Patnaik, S., Huang, J., Williams, L. L., Senapati, S., et al. (2023) · Biomedicines · doi:10.3390/biomedicines12010005 · Cited by 9
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“Atg7, an E1-like ubiquitin activating enzyme that is involved in the conjugation of phosphatidylethanolamine (PE) to Atg8, and formation of the Atg5-Atg12 conjugate, has been shown to suppress the accumulation of ubiquitinated aggregates, thereby contributing to Drosophila adult longevity (Juhasz et al., 2007; Geng an…”
BackgroundInfluentialThe axonal radial contractility: Structural basis underlying a new form of neural plasticity
Pan, X., Zhou, Y., Hotulainen, P., Meunier, F. A., & Wang, T. (2021) · BioEssays · doi:10.1002/bies.202100033 · Cited by 9
“5 μm),[42,43] endosomes (50 nm to 1 μm),[44] and mitochondria (0.”
BackgroundATG2A acts as a tether to regulate autophagosome-lysosome fusion in neural cells
Zheng, Z., Ji, C., Zhao, H., & Zhao, Y. G. (2025) · Autophagy · doi:10.1080/15548627.2025.2479427 · Cited by 9
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Emerging roles for E3 ubiquitin ligases in neural development and disease
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“In neurodegeneration, HAP1 is implicated in retrograde autophagosome transport and subsequent fusion with competent lysosomes (Maday et al., 2012; Wong and Holzbaur, 2014).”
Soma-localized Rab39 inhibits synaptic autophagy by controlling trafficking of Atg9 vesicles
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“Autophagosome precursors are known to form in distal axons and then, during maturation, to move, retrogradely, along the axons, toward the soma [53,54].”
BackgroundMolecular aspects of optic nerve autophagy in glaucoma
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“This requires retrograde transport of autophagosomes, carrying material from the distant cell periphery to the cell body [Maday et al., 2012].”
Gurda, B. L., Bagel, J. H., Fisher, S. J., Schultz, M. L., Lieberman, A. P., Hand, P. J., Vite, C. H., & Swain, G. P. (2018) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlx119 · Cited by 8
Direct observation of aggregate-triggered selective autophagy in human cells
Janssen, A. F. J., Korsten, G., Nijenhuis, W., Katrukha, E. A., & Kapitein, L. C. (2021) · Journal of Cell Science · doi:10.1242/jcs.258824 · Cited by 8
Imaging Intracellular Trafficking in Neurons of C. elegans
Nadiminti, S. S. P., & Koushika, S. P. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-1990-2_27 · Cited by 6
PDZD8 promotes autophagy at ER-Lysosome contact sites to regulate synaptogenesisPreprint
Thakur, R. S., & O’Connor-Giles, K. M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.30.564828 · Cited by 8
Presynapses are mitophagy pit stops that prevent axon degenerationPreprint
Lam, W. K., Lindblom, R. S. J., Milky, B., Mazzachi, P., Hadian-Jazi, M., Küng, C. J., Khuu, G., Uoselis, L., Nguyen, T. N., Skulsuppaisarn, M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.09.611943 · Cited by 10
Autophagy as a new player in the regulation of clock neurons physiology of Drosophila melanogaster
Szypulski, K., Tyszka, A., Pyza, E., & Damulewicz, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-56649-3 · Cited by 9
“Many autophagosomes are formed in the distal part of axons and are retrogradely transported to the soma where they are fused with lysosomes 58 .”
BackgroundFerreira, F. D. S., de Mattos, J. L. A., da Silva, P. H. F., da Costa, C. A., Ognibene, D. T., Resende, Â. C., & de Bem, G. F. (2025) · Plants · doi:10.3390/plants14132010 · Cited by 7
“In addition, there is a small distribution of lysosomes in the distal axons, so autophagosomes must be transported to the cell body [144,145].”
The Emerging Role of Astrocytic Autophagy in Central Nervous System Disorders
Zhou, Z., Zhou, J., Liao, J., Chen, Z., & Zheng, Y. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03714-w · Cited by 7
Nucleus–cytoplasm cross‐talk in the aging brain
Benvegnù, S. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24446 · Cited by 7
Axon terminals control endolysosome diffusion to support synaptic remodelling
Terni, B., & Llobet, A. (2021) · Life Science Alliance · doi:10.26508/lsa.202101105 · Cited by 7
“An example could be the fusion with autophagosomes that are formed in synapses and acidify on their journey to the soma (Maday et al, 2012).”
BackgroundSegi, N., Ozaki, T., Suzuki, Y., Ouchida, J., Imagama, S., Kadomatsu, K., & Sakamoto, K. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114112 · Cited by 7
Tug-of-War and Coordination in Bidirectional Transport by Molecular Motors
Muñoz, O., & Klumpp, S. (2022) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.2c05194 · Cited by 6
Autophagy in Neurodevelopmental Disorders
Lv, M., & Ma, Q. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-4272-5_11 · Cited by 7
Cytoplasmic dynein dysfunction and neurodegenerative disease
Moughamian, A. J., & Holzbaur, E. L. F. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809470-9.00013-8 · Cited by 7
Self-citationKallergi, E., Daskalaki, A.-D., Ioannou, E., Kolaxi, A., Plataki, M. E., Haberkant, P., Stein, F., Savitski, M. M., Sidiropoulou, K., Dalezios, Y., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.12.983965 · Cited by 7
“…AV biogenesis occurs indiscriminately throughout the cytoplasm, previous work demonstrated that in diverse neuronal populations, including hippocampal pyramidal neurons, biogenesis of AVs is spatially confined to the axon tip under baseline conditions (Maday and Holzbaur, 2016; Maday et al., 2012).”
BackgroundResultInfluentialTRIM16 mediates secretory autophagy in head and neck cancer-associated fibroblasts
Ly, T., Pickard, B., Pandey, A., Yap, M., Opara, J. K., Arnold, L., Martínez-Rivera, N., Rosa‐Molinar, E., New, J., Werner, L. R., et al. (2025) · Autophagy · doi:10.1080/15548627.2025.2508064 · Cited by 6
“Degradative autophagosomes typically mature into autolyso-somes in the perinuclear region [7,23,24].”
The space-time continuum in neurological disorders of the autophagosome-lysosome fusion machinery
Dafsari, H. S., Schuler, J., Schober, E., Möller, B., Antebi, A., Fanto, M., & Jungbluth, H. (2025) · Autophagy Reports · doi:10.1080/27694127.2025.2560903 · Cited by 6
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How does the neuronal proteostasis network react to cellular cues?
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Ariosa, A., & Klionsky, D. J. (2015) · Autophagy · doi:10.1080/15548627.2015.1009790 · Cited by 6
Studying endosomes in cultured neurons by live-cell imaging
Lasiecka, Z. M., & Winckler, B. (2015) · Methods in cell biology · doi:10.1016/bs.mcb.2015.07.002 · Cited by 7
Restoring synaptic function through multimodal therapeutics
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“This centripetal movement of the axonal autophagosome is a microtubule-dependent transport along the axon, driven by kinesin and dynein motors (Maday et al., 2012; Cheng et al., 2015).”
BackgroundTransport-dependent maturation of organelles in neurons
Mathew, A., & Koushika, S. P. (2022) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2022.102121 · Cited by 7
Axon Injury-Induced Autophagy Activation Is Impaired in a C. elegans Model of Tauopathy
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“Autophagic vesicles have been shown to move bidirectionally in axons of primary neurons [39].”
BackgroundProgranulin Protects against Hyperglycemia-Induced Neuronal Dysfunction through GSK3β Signaling
Dedert, C., Salih, L. Y., & Xu, F. (2023) · Cells · doi:10.3390/cells12131803 · Cited by 6
“Since autophagy involves a number of steps, this suggests that GSK3β may be important in the later stages of autophagy, in which autophagosomes tagged with lipidated LC3B travel to the perinuclear region, fuse with lysosomes, and are degraded [63].”
BackgroundWisner, S. R., Chlebowski, M., Mandal, A., Mai, D., Stein, C., Petralia, R. S., Wang, Y., & Drerup, C. M. (2024) · Autophagy · doi:10.1080/15548627.2024.2366122 · Cited by 5
“Previous work has shown a strong correlation between autophagosome acidification, a marker of maturation, and retrograde transport along the axon [3,5,11,12].”
Cytoplasmic Dynein Dysfunction and Neurodegenerative Disease
Moughamian, A. J., & Holzbaur, E. L. F. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-382004-4.10023-8 · Cited by 5
Self-citationNeuronal Mitophagy: Long-Distance Delivery or Eating Locally?
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Kerendi, H., Rahmati, M., Mirnasuri, R., & Kazemi, A. (2019) · Gene · doi:10.1016/j.gene.2019.04.027 · Cited by 5
Metur, S. P., & Klionsky, D. J. (2022) · Autophagy · doi:10.1080/15548627.2022.2071081 · Cited by 5
“components while axons and dendrites serve primarily as platforms for transmitting and receiving electrochemical signals, respectively [3,4].”
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“Evidence supports that autophagy takes place and is regulated locally at the presynaptic compartment, where this process may degrade synaptic vesicles 9,13,26–28 .”
Dynein‐Dependent Endo‐Lysosomal Degradation Drives Lewy Body Disorders Accompanied by Aβ Pathology
Zhou, L., Wang, Y., Liu, Y., Zhu, F., Gao, G., Li, C., Ai, P., Xu, J., Wang, J. J., Guo, L. Z., et al. (2025) · Advanced Science · doi:10.1002/advs.202414860 · Cited by 5
Rasmussen, L. K., Moreira, D. G., Okarmus, J., Simonsen, A., & Meyer, M. (2026) · Autophagy · doi:10.1080/15548627.2026.2711596 · Cited by 4
Role of LRRK2 in axonal transport and Parkinson’s disease
Twellsieck, B., & Boecker, C. A. (2025) · Biochemical Journal · doi:10.1042/bcj20253133 · Cited by 7
“Both the retrograde motor dynein and the anterograde motor kinesin are bound to the autophagosome membrane, but a set of motor adaptor proteins promotes dynein activity while inhibiting kinesin activity to enable processive autophagosome transport in the retrograde direction [108,109,114,115].”
Wang, T., & Meunier, F. A. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2209-4_9 · Cited by 4
Evaluating Autophagy in Preimplantation Embryos
Leung, Z. C. L., Hunter, H., Rafea, B. A., Watson, A. J., & Betts, D. H. (2022) · Autophagy Reports · doi:10.1080/27694127.2022.2101335 · Cited by 4
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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