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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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InfluentialSelf-citationCoordination of autophagosome–lysosome fusion and transport by a Klp98A–Rab14 complex in Drosophila
Mauvezin, C., Neisch, A. L., Ayala, C. I., Kim, J., Beltrame, A., Braden, C. R., Gardner, M. K., Hays, T. S., & Neufeld, T. P. (2016) · Journal of Cell Science · doi:10.1242/jcs.175224 · Cited by 55
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InfluentialTammineni, P., Jeong, Y. Y., Feng, T., Aikal, D., & Cai, Q. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx321 · Cited by 53
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Autophagy Modulators and Neuroinflammation
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“It cannot be underestimated, however, that this strategy may be beneficial only early in the disease (Majumder et al., 2011), when neuronal loss has not yet occurred.”
BackgroundCombinatorial selective ER-phagy remodels the ER during neurogenesis
Hoyer, M., Capitanio, C., Smith, I. R. L., Paoli, J. C., Bieber, A., Jiang, Y., Paulo, J. A., Gonzalez‐Lozano, M. A., Baumeister, W. P., Wilfling, F., et al. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01356-4 · Cited by 50
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Self-citationTargeting neuronal mitophagy in ischemic stroke: an update
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“In the case of intact neurons, autophagosomes are generated in the axonal tips, transported along with axons and fused with acidic vesicles for maturation [37].”
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“In primary neurons, the LC3 autophagosomes were also maturing during their microtubuledependent transport toward the cell soma (Maday et al., 2012) but LC3 role in the process remained unclear.”
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“Axonal autophagosome biogenesis was first studied in adult mouse DRG neurons (Maday et al., 2012), by imaging GFP-LC3 (an autophagosome marker).”
BackgroundMitophagy in Refractory Temporal Lobe Epilepsy Patients with Hippocampal Sclerosis
Wu, M., Liu, X., Chi, X., Zhang, L., Xiong, W., Chiang, S. M. V., Zhou, D., & Li, J. (2017) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-017-0492-2 · Cited by 41
“Autophagosomes, including those engulfing damaged mitochondria, can be transported retrogradely from distal axons to the soma (Maday et al. 2012).”
BackgroundLi, S., Zhao, H., Wang, Y., Shao, Y., Wang, B., Wang, Y., & Xing, M. (2017) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2017.10.018 · Cited by 41
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Dynamics of Mitochondrial Transport in Axons
Niescier, R. F., Kwak, S. K., Joo, S. H., Chang, K. T., & Min, K. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00123 · Cited by 40
“…we found that none of the retrogradely moving mitochondria originating from the distal axonal area reached the cell body during 2 h of imaging period, which is incompatible to the model that retrogradely moving mitochondria arrive at the cell body for processing and repair (Maday et al., 2012).”
ResultAngular measurements of the dynein ring reveal a stepping mechanism dependent on a flexible stalk
Lippert, L. G., Dadosh, T., Hadden‐Perilla, J. A., Karnawat, V., Diroll, B. T., Murray, C. B., Holzbaur, E. L. F., Schulten, K. J., Reck‐Peterson, S. L., & Goldman, Y. E. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620149114 · Cited by 40
“Axonemal dyneins drive the motility of eukaryotic cilia and flagella, whereas cytoplasmic dynein is responsible for a wide range of functions within eukaryotic cells, including the retrograde transport of cargo such as autophagosomes in neurons (4), alignment of the mitotic spindle (5, 6), and chromosome segregation d…”
BackgroundSelf-citationAutophagy as a Homeostatic Mechanism in Response to Stress Conditions in the Central Nervous System
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“These hybrid structures most likely represent the pre-synaptically formed autophagosomes, whose processing requires retrograde transport along microtubules to the cell soma, where they meet the lysosomes (Maday et al., 2012).”
BackgroundVesicles driven by dynein and kinesin exhibit directional reversals without regulators
D’Souza, A. I., Grover, R., Monzon, G. A., Santen, L., & Diez, S. (2023) · Nature Communications · doi:10.1038/s41467-023-42605-8 · Cited by 41
“Comparing those specific cargos with the observed behaviors in this manuscript is important, since this is a major point.”
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“Multivesicular body (MVB) accommodates targeting of presynaptic proteins to cell body lysosomes/degradative organelles as suggested by recent studies (Uytterhoeven et al. 2011; Maday et al. 2012).”
BackgroundThe needs of a synapse—How local organelles serve synaptic proteostasis
Grochowska, K. M., Andres‐Alonso, M., Karpova, A., & Kreutz, M. R. (2022) · The EMBO Journal · doi:10.15252/embj.2021110057 · Cited by 38
“Evidence for a local degradative role of lysosomes in axons is currently scarce (Maday et al , 2012; Farfel-Becker et al , 2019).”
InfluentialRed fluorescent proteins (RFPs) and RFP-based biosensors for neuronal imaging applications
Shen, Y., Lai, T., & Campbell, R. E. (2015) · Neurophotonics · doi:10.1117/1.nph.2.3.031203 · Cited by 39
“Yet other RFPs, many of which are unambiguously monomeric, can form bright puncta in certain cells types due to accumulation in lysosomes or autophagosomes.(50,51)”
BackgroundAutophagy and Autophagy-Related Proteins in CNS Autoimmunity
Keller, C. W., & Lünemann, J. D. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00165 · Cited by 38
“In an antagonistic interplay, the members of the motor protein family dynein/ dynactin complex and kinesin have shown to be involved in guiding autophagosomes alongside microtubules toward lysosomerich areas, a process during which the trafficked vesicles become increasingly acidified as they approach the juxtanuclear…”
BackgroundOrchestrating mitochondria in neurons: Cytoskeleton as the conductor
Cardanho‐Ramos, C., Faria‐Pereira, A., & Morais, V. A. (2019) · Cytoskeleton · doi:10.1002/cm.21585 · Cited by 37
“Accordingly, the formation of autophagosomes incorporating mitochondria has been observed in distal axons (Maday et al., 2012).”
BackgroundAdalbert, R., Kaieda, A., Antoniou, C., Loreto, A., Yang, X., Gilley, J., Hoshino, T., Uga, K., Makhija, M. T., & Coleman, M. P. (2019) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.9b00338 · Cited by 37
Sphingosine kinase 1-associated autophagy differs between neurons and astrocytes
Moruno-Manchon, J. F., Uzor, N.-E., Ambati, C. R., Shetty, V., Putluri, N., Jagannath, C., McCullough, L. D., & Tsvetkov, A. S. (2018) · Cell Death & Disease · doi:10.1038/s41419-018-0599-5 · Cited by 36
Gicking, A. M., Ma, T.-C., Feng, Q., Jiang, R., Badieyan, S., Cianfrocco, M. A., & Hancock, W. O. (2022) · eLife · doi:10.7554/elife.82228 · Cited by 36
“…et al., 2010; Shubeita et al., 2008), as well as characterizing cargo dynamics (Barkus et al., 2008; Kamal et al., 2000; Levi et al., 2006; Maday et al., 2012; Rosa-Ferreira & Munro, 2011; Tanaka et al., 1998), and the codependence of opposite directionality motors (Gross et al., 2002;…”
BackgroundInfluentialDou, D., Smith, E. M., Evans, C. S., Boecker, C. A., & Holzbaur, E. L. F. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112448 · Cited by 36
“The opposing motor kinesin remains bound to AVs during dyneindriven transport but is auto-inhibited under normal conditions (Boecker et al., 2021; Fu and Holzbaur, 2014; Maday et al., 2012).”
BackgroundSelf-citationCell Specific Changes of Autophagy in a Mouse Model of Contusive Spinal Cord Injury
Muñoz‐Galdeano, T., Reigada, D., del Águila, Á., Velez, I., Caballero-López, M. J., Maza, R. M., & Nieto‐Díaz, M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00164 · Cited by 37
Presynaptic Autophagy and the Connection With Neurotransmission
Decet, M., & Verstreken, P. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.790721 · Cited by 34
“Consistent with this hypothesis, several studies performed in cultured neurons showed the presence of ATG8/LC3 positive structures at distal axons, a commonly used marker for autophagosomes, indicating that autophagosome formation occurs at this location (Maday et al., 2012; Wang et al., 2015; Okerlund et al., 2017).”
BackgroundResultGao, Y., Wang, C., Jiang, D. M., An, G., Jin, F. J., Zhang, J., Han, G., Cui, C., & Jiang, P. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.994037 · Cited by 37
“These pathological changes may induce autophagy, enhancing the local biosynthesis of autophagosomes and their accumulation in axons, ultimately leading to cell death (Maday et al., 2012).”
BackgroundRecent insights on principles of synaptic protein degradation
Cohen, L. D., & Ziv, N. E. (2017) · F1000Research · doi:10.12688/f1000research.10599.1 · Cited by 35
Selenium Deficiency Induces Autophagy in Immune Organs of Chickens
Khoso, P. A., Pan, T., Wan, N., Yang, Z., Liu, C., & Li, S. (2016) · Biological Trace Element Research · doi:10.1007/s12011-016-0860-7 · Cited by 35
The axonal endolysosomal and autophagic systems
Kuijpers, M., Tehran, D. A., Haucke, V., & Soykan, T. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15287 · Cited by 38
“…axonal swellings, axonal dystrophy, inflammation, and neurodegeneration (Lee et al., 2011; Nixon et al., 2008; Walkley et al., 2010; Yambire et al., 2019), that is, phenotypes characteristic of lysosomal storage diseases that arise from genetic defects in select lysosomal enzymes (Maegawa, 2019).”
BackgroundPalmitoylation couples the kinases DLK and JNK3 to facilitate prodegenerative axon-to-soma signaling
Niu, J., Holland, S. M., Ketschek, A., Collura, K. M., Hesketh, N., Hayashi, T., Gallo, G., & Thomas, G. M. (2022) · Science Signaling · doi:10.1126/scisignal.abh2674 · Cited by 35
“The CC1 domain of dynactin [generated by polymerase chain reaction (PCR) from a cDNA template provided by Holzbaur and colleagues (29)] was subcloned into FEW- myc-DD upstream of the myc epitope, generating FEW-CC1-mycDD.”
MethodSaito, A., & Cavalli, V. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r115.052753 · Cited by 34
“A key unanswered question remains: why is calcium back propagation on the proximal side not affecting axonal and mitochondria’s health? Perhaps the supply of anterogradely transported healthy mitochondria from the soma can balance the removal of damaged axonal mitochondria mediated by internalization into autophagosom…”
BackgroundPreserve and protect: maintaining axons within functional circuits
Pease-Raissi, S. E., & Segal, R. A. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.07.007 · Cited by 36
Natural products as modulator of autophagy with potential clinical prospects
Wang, P., Zhu, L., Sun, D., Gan, F., Gao, S., Yin, Y., & Chen, L. (2016) · APOPTOSIS · doi:10.1007/s10495-016-1335-1 · Cited by 34
Cao, X., Wang, H., Wang, Z., Wang, Q., Zhang, S., Deng, Y., & Fang, Y. (2017) · Aging Cell · doi:10.1111/acel.12654 · Cited by 36
“It remains debated whether damaged axonal mitochondria are transported back to the soma for turnover (Maday et al., 2012; Maday & Holzbaur, 2014) or are degraded locally in axons by PINK1-Parkin-dependent mitophagy (Ashrafi et al., 2014).”
BackgroundNeuronal endosomes to lysosomes: A journey to the soma
Kulkarni, V. V., & Maday, S. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201806139 · Cited by 33
“Following autophagosome formation in the distal axon, autophagosomes initially fuse with LAMP1-positive late endosomes and undergo retrograde transport to the soma (Maday et al., 2012).”
BackgroundSelf-citationPotential benefits of medium chain fatty acids in aging and neurodegenerative disease
Dunn, E., Zhang, B., Sahota, V. K., & Augustin, H. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1230467 · Cited by 38
“Neuronal cells are especially vulnerable to impaired autophagy—autophagosomes containing cargo to be degraded must be transported along the axon to the cell body to fuse with lysosomes, as lysosomes are rarely found in distal axons (Maday et al., 2012; Cheng et al., 2015).”
BackgroundChowdary, P. D., Che, D. L., Kaplan, L., Chen, O., Pu, K., Bawendi, M. G., & Cui, B. (2015) · Scientific Reports · doi:10.1038/srep18059 · Cited by 34
Modulating Macroautophagy: A Neuronal Perspective
Johnson, C. W., Melia, T. J., & Yamamoto, A. (2012) · Future Medicinal Chemistry · doi:10.4155/fmc.12.112 · Cited by 33
TMEM184b Promotes Axon Degeneration and Neuromuscular Junction Maintenance
Bhattacharya, M. R. C., Geisler, S., Pittman, S. K., Doan, R. A., Weihl, C. C., Milbrandt, J., & DiAntonio, A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2893-15.2016 · Cited by 35
“In neurons, autophagy is a constitutive process (Maday et al., 2012).”
BackgroundLiu, P., Liu, P., Wang, Z., Fang, S., Liu, Y., Wang, J., Liu, W., Wang, N., Chen, L., Wang, J., et al. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000492844 · Cited by 33
Ouyang, C., Mu, J., Lu, Q., Li, J., Zhu, H., Wang, Q., Zou, M., & Xie, Z. (2019) · Autophagy · doi:10.1080/15548627.2019.1707488 · Cited by 32
“Accumulating evidence suggests that microtubules regulate autophagosome formation and transportation in axon [45,46].”
BackgroundAxonal Organelles as Molecular Platforms for Axon Growth and Regeneration after Injury
Petrova, V., Nieuwenhuis, B., Fawcett, J. W., & Eva, R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041798 · Cited by 35
Selvarasu, K., Singh, A. K., Iyaswamy, A., Sreenivasmurthy, S. G., Krishnamoorthi, S., Bera, A. K., Huang, J., & Durairajan, S. S. K. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.1050768 · Cited by 33
“Although autophagosomes in cortical neurons are known to undergo dynein-dependent unidirectional retrograde transport along the axon (Lee et al., 2011; Maday et al., 2012), Maday et al.”
BackgroundThe evolution of the axonal transport toolkit
Surana, S., Villarroel‐Campos, D., Lazo, O. M., Moretto, E., Tosolini, A. P., Rhymes, E. R., Richter, S., Sleigh, J. N., & Schiavo, G. (2019) · Traffic · doi:10.1111/tra.12710 · Cited by 31
Autophagy in the presynaptic compartment
Lüningschrör, P., & Sendtner, M. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.023 · Cited by 32
FYCO1 mediates clearance of α‐synuclein aggregates through a Rab7‐dependent mechanism
Saridaki, T., Nippold, M., Dinter, E., Roos, A., Diederichs, L., Fensky, L., Schulz, J. B., & Falkenburger, B. H. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14461 · Cited by 33
“Dynein is a protein complex mediating transport along microtubules towards their minus end, which is located at the perinuclear microtubuleorganizing centre (MTOC).”
BackgroundInfluentialAutophagy and lysosomal pathways in nervous system disorders
Bingol, B. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.04.009 · Cited by 32
Mattera, R., Williamson, C. D., Ren, X., & Bonifacino, J. S. (2020) · Molecular Biology of the Cell · doi:10.1091/mbc.e19-11-0658 · Cited by 31
“This could be due to a role of Hook proteins in coupling of autophagosomes to dynein–dynactin (Ravikumar et al., 2005; Kimura et al., 2008; Maday et al., 2012; Reck-Peterson et al., 2018).”
BackgroundBalancing the Opposing Principles That Govern Peroxisome Homeostasis
Mahalingam, S. S., Shukla, N., Farré, J., Zientara‐Rytter, K., & Subramani, S. E. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.09.006 · Cited by 31
“In mammalian cells, the retrograde movement of autophagosomes is dependent on microtubules and dynein/ dynactin for retrograde motility [64–66], whereas the anterograde movement is dependent on kinesin motors [67].”
BackgroundCason, S. E., Mogre, S. S., Holzbaur, E. L. F., & Koslover, E. F. (2022) · Molecular Biology of the Cell · doi:10.1091/mbc.e22-03-0111 · Cited by 33
“Neuronal AVs form constitutively at presynaptic sites including the distal tip of the axon (Figure 1b), where they clear aged proteins and organelles (Maday et al., 2012; Goldsmith et al., 2022).”
BackgroundResultInfluentialSelf-citationZaninello, M., & Bean, C. (2023) · Biomolecules · doi:10.3390/biom13060938 · Cited by 34
“It is under debate where autophagy occurs, if it involves the transport of mitochondria to the soma or if it happens in distal axons [94,95].”
BackgroundATG9 resides on a unique population of small vesicles in presynaptic nerve terminals
Binotti, B., Ninov, M., Cepeda, A. P., Ganzella, M., Matti, U., Riedel, D., Urlaub, H., Sambandan, S., & Jahn, R. (2023) · Autophagy · doi:10.1080/15548627.2023.2274204 · Cited by 32
“They are mainly initiated in distal nerve endings and then mature during transport back toward the cell body [71] but the details of initial formation and growth are still unclear.”
BackgroundCadmium neurotoxicity and therapeutic strategies
Wen, S., & Wang, L. (2024) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.23670 · Cited by 29
Clarke, J.-P. W. E., & Mearow, K. M. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23733 · Cited by 30
“…protein 1A/1B light chain 3B (LC3B) to study autophagy within axons; previous studies have employed GFP–LC3B transgenic mice and have elucidated constitutive autophagy and formation of autophagosomes in DRG neurons (Mizushima et al., 2004; Maday et al., 2012; Maday and Holzbaur, 2014).”
BackgroundInfluential
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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