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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Autophagosome trafficking along axons was recently described.
“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]
The velocities obtained are in the same order of magnitude as those recently reported for autophagosomes in axons of DRGs from LC3-GFP transgenic mice.
“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]
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.
“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]
Autophagy initiation typically begins outside of the soma, in the distal axon tip.
“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]
Bidirectional movements have been reported for a variety of organelles and vesicles, including mitochondria, autophagosomes, and vesicles during axonal transport.
“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
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InfluentialMechanism and Regulation of Cytoplasmic Dynein
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BORC/kinesin-1 ensemble drives polarized transport of lysosomes into the axon
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“This conclusion is consistent with the notion that fusion of lysosomes with autophagosomes contributes to the dynein-dependent retrograde transport of the resulting autolysosomes, in addition to the degradation of their contents (31, 53).”
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BackgroundInfluentialNeuronal Aggregates: Formation, Clearance, and Spreading
Lim, J., & Yue, Z. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.02.002 · Cited by 221 · see citing works
“Notably, autophagosome initiation is a constitutive and spatially restricted process in the distal ends of cultured dorsal root ganglion (DRG) neurons (Maday et al., 2012; Yue et al., 2008).”
BackgroundAlterations in Mitochondrial Quality Control in Alzheimer’s Disease
Cai, Q., & Tammineni, P. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00024 · Cited by 215 · see citing works
“…mitochondria, predominantly undergo retrograde transport from distal axons to the soma, which allows for autophagosome maturation and subsequent degradation within mature lysosomes in the proximal regions and soma of neurons (Maday and Holzbaur, 2014; Maday et al., 2012; Cheng et al., 2015).”
BackgroundMicrotubule-based transport – basic mechanisms, traffic rules and role in neurological pathogenesis
Franker, M. A. M., & Hoogenraad, C. C. (2013) · Journal of Cell Science · doi:10.1242/jcs.115030 · Cited by 207 · see citing works
“, 2006), autophagosomes (Maday et al., 2012), intermediate filaments (Li et al.”
BackgroundER stress and impaired autophagy flux in neuronal degeneration and brain injury
Yin, Y., Sun, G., Li, E., Kiselyov, K. I., & Sun, D. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.08.008 · Cited by 214 · see citing works
Fu, M., Nirschl, J., & Holzbaur, E. L. F. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.04.015 · Cited by 205 · see citing works
“Autophagosome-enriched fractions were prepared from wild type adult mouse brains following a previously described three-step protocol (Maday et al., 2012; Stromhaug et al., 1998).”
MethodSelf-citationAutophagy and Its Normal and Pathogenic States in the Brain
Yamamoto, A., & Yue, Z. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071013-014149 · Cited by 204 · see citing works
“For neurons, amphisome formation may be especially valid because APs must travel long distances before degradation can occur (Hollenbeck 1993, Larsen et al. 2002, Maday et al. 2012).”
BackgroundTau phosphorylation affects its axonal transport and degradation
Rodríguez-Martín, T., Cuchillo‐Ibáñez, I., Noble, W. J., Nyenya, F., Anderton, B. H., & Hanger, D. P. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.03.015 · Cited by 200 · see citing works
“Autophagosome dynamics in primary neurons has been described by Maday et al. (2012), who found that autophagosome biogenesis occurs distally in the axon.”
BackgroundAutophagy and ALS: mechanistic insights and therapeutic implications
Chua, J. P., De Calbiac, H., Kabashi, E., & Barmada, S. J. (2022) · Autophagy · doi:10.1080/15548627.2021.1926656 · Cited by 189 · see citing works
“neurites to fuse with somatodendritic lysosomes for cargo degradation, with maturation and acidification of the autophagosomal lumen developing en passant [370,372,374].”
BackgroundThe GTPase Rab26 links synaptic vesicles to the autophagy pathway
Binotti, B., Pavlos, N. J., Riedel, D., Wenzel, D., Vorbrüggen, G., Schalk, A. M., Kühnel, K., Boyken, J., Erck, C., Martens, H., et al. (2015) · eLife · doi:10.7554/elife.05597 · Cited by 193 · see citing works
“During their travel they undergo fusion with acidic compartments and finally with the lysosomes (Lee et al., 2011; Maday et al., 2012).”
BackgroundMitochondrial heterogeneity and homeostasis through the lens of a neuron
Pekkurnaz, G., & Wang, X. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00594-w · Cited by 195 · see citing works
Mitochondria as a central sensor for axonal degenerative stimuli
Court, F. A., & Coleman, M. P. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.04.001 · Cited by 193 · see citing works
Bassoon Controls Presynaptic Autophagy through Atg5
Okerlund, N. D., Schneider, K., Leal‐Ortiz, S., Montenegro‐Venegas, C., Kim, S. A., Garner, L. C., Waites, C. L., Gundelfinger, E. D., Reimer, R. J., & Garner, C. C. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.026 · Cited by 189 · see citing works
“Moreover, a number of studies have shown that, while autophagosomes are rather dynamic, they predominantly undergo retrograde transport to the soma (Maday et al., 2012).”
Nirschl, J., Magiera, M. M., Lazarus, J. E., Janke, C., & Holzbaur, E. L. F. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.046 · Cited by 192 · see citing works
Self-citationRudnick, N. D., Griffey, C. J., Guarnieri, P., Gerbino, V., Wang, X., Piersaint, J. A., Tapia, J. C., Rich, M. M., & Maniatis, T. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1704294114 · Cited by 189 · see citing works
“It has been demonstrated that autophagosomes can form distally at the synapse and retrogradely transport cargo for degradation (48).”
Impaired intracellular trafficking defines early Parkinson's disease
Hunn, B. H. M., Cragg, S. J., Bolam, J. P., Spillantini, M., & Wade‐Martins, R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2014.12.009 · Cited by 185 · see citing works
Amyloid assembly and disassembly
Chuang, E., Hori, A. M., Hesketh, C. D., & Shorter, J. (2018) · Journal of Cell Science · doi:10.1242/jcs.189928 · Cited by 182 · see citing works
“3B) (Maday and Holzbaur, 2012, 2014, 2016; Maday et al., 2012).”
Mechanisms Orchestrating Mitochondrial Dynamics for Energy Homeostasis
Yu, S. B., & Pekkurnaz, G. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.07.027 · Cited by 182 · see citing works
“Damaged neuronal mitochondria can be removed by local degradation or shipping of intact or small vesicles containing mitochondrial proteins retrogradely to somatodendritic regions for destruction [64,158,159].”
BackgroundAutophagy and mitophagy in ALS
Evans, C. S., & Holzbaur, E. L. F. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.07.005 · Cited by 178 · see citing works
Self-citationAutophagy induction stabilizes microtubules and promotes axon regeneration after spinal cord injury
He, M., Ding, Y., Chu, C., Tang, J. Y., Xiao, Q., & Luo, Z. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1611282113 · Cited by 177 · see citing works
“Accumulating evidence suggests that MTs play important roles in the regulation of autophagosome formation and transportation in axons (33, 64).”
BackgroundKuijpers, M., Kochlamazashvili, G., Stumpf, A., Puchkov, D., Swaminathan, A., Lucht, M. T., Krause, E., Maritzen, T., Schmitz, D., & Haucke, V. (2021) · Neuron · doi:10.1016/j.neuron.2020.10.005 · Cited by 170 · see citing works
Lewis, T. L., Turi, G. F., Kwon, S., Losonczy, A., & Polleux, F. (2016) · Current Biology · doi:10.1016/j.cub.2016.07.064 · Cited by 167 · see citing works
Tammineni, P., Ye, X., Feng, T., Aikal, D., & Cai, Q. (2017) · eLife · doi:10.7554/elife.21776 · Cited by 169 · see citing works
“Microtubulebased long-distance axonal transport is essential for autophagic clearance because autophagosomes are predominantly generated in distal axons and rely heavily on retrograde transport toward the soma for lysosomal proteolysis (Cheng et al., 2015a, 2015b; Lee et al., 2011a; Maday and Holzbaur, 2016; Maday et…”
BackgroundResultInfluentialAutophagy in the presynaptic compartment in health and disease
Vijayan, V., & Verstreken, P. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201611113 · Cited by 167 · see citing works
“In axons, autophagosomes form continuously at distal tips and contain cargoes derived from synapses (Maday et al., 2012; Maday and Holzbaur, 2014, 2016; Wang et al., 2015).”
BackgroundSelective motor activation in organelle transport along axons
Cason, S. E., & Holzbaur, E. L. F. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00491-w · Cited by 169 · see citing works
Self-citationBoecker, C. A., Goldsmith, J., Dou, D., Cajka, G. G., & Holzbaur, E. L. F. (2021) · Current Biology · doi:10.1016/j.cub.2021.02.061 · Cited by 166 · see citing works
“LRRK2-G2019S enhances recruitment of JIP4 to the AV membrane and increases kinesin activity Both the anterograde motor kinesin and the retrograde motor dynein are bound to AVs; the opposing activities of these motors are regulated by adaptor proteins that inhibit kinesin and promote dynein activity.(21,43) The observe…”
BackgroundSelf-citationReview: Axon pathology in age‐related neurodegenerative disorders
Adalbert, R., & Coleman, M. P. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01308.x · Cited by 169 · see citing works
Kononenko, N. L., Classen, G. A. E., Kuijpers, M., Puchkov, D., Maritzen, T., Tempes, A., Malik, A. R., Skalecka, A., Bera, S., Jaworski, J., et al. (2017) · Nature Communications · doi:10.1038/ncomms14819 · Cited by 161 · see citing works
Targeting Autophagy for the Treatment of Alzheimer’s Disease: Challenges and Opportunities
Liu, J., & Li, L. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00203 · Cited by 159 · see citing works
Moughamian, A. J., Osborn, G. E., Lazarus, J. E., Maday, S., & Holzbaur, E. L. F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0935-13.2013 · Cited by 161 · see citing works
“1B,C), confirming the uniform plus-end outward polarity of the microtubule cytoskeleton in this cell type (Maday et al., 2012).”
BackgroundInfluentialSelf-citationHung, C. O. Y., & Livesey, F. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.095 · Cited by 159 · see citing works
“Further maturation of lysosomes requires retrograde transport to the cell soma where luminal proteases can be delivered from the trans-Golgi network efficiently (Maday et al., 2012).”
BackgroundCongenital disorders of autophagy: an emerging novel class of inborn errors of neuro-metabolism
Ebrahimi‐Fakhari, D., Saffari, A., Wahlster, L., Lu, J., Byrne, S., Hoffmann, G. F., Jungbluth, H., & Şahin, M. (2015) · Brain · doi:10.1093/brain/awv371 · Cited by 157 · see citing works
The autophagic roles of Rab small GTPases and their upstream regulators
Szatmári, Z., & Sass, M. (2014) · Autophagy · doi:10.4161/auto.29395 · Cited by 152 · see citing works
Davies, A. K., Itzhak, D. N., Edgar, J. R., Archuleta, T. L., Hirst, J., Jackson, L. P., Robinson, M. S., & Borner, G. H. H. (2018) · Nature Communications · doi:10.1038/s41467-018-06172-7 · Cited by 153 · see citing works
The autophagy gene <i>Wdr45/Wipi4</i> regulates learning and memory function and axonal homeostasis
Zhao, Y. G., Sun, L., Miao, G., Ji, C., Zhao, H., Sun, H., Miao, L., Yoshii, S. R., Mizushima, N., Wang, X., et al. (2015) · Autophagy · doi:10.1080/15548627.2015.1047127 · Cited by 148 · see citing works
“Autophagy is required for normal axon terminal membrane trafficking and turnover, and plays an essential role in the maintenance of axonal homeostasis and prevention of axonal degeneration.(20,21) Accumulation of axonal spheroid structures in Wdr45 mice indicates that axoN-terminals are more vulnerable to autophagy im…”
BackgroundThe role of mitophagy in the regulation of mitochondrial energetic status in neurons
Han, S., Zhang, M., Jeong, Y. Y., Margolis, D. J., & Cai, Q. (2021) · Autophagy · doi:10.1080/15548627.2021.1907167 · Cited by 151 · see citing works
Degradation of engulfed mitochondria is rate-limiting in Optineurin-mediated mitophagy in neurons
Evans, C. S., & Holzbaur, E. L. (2020) · eLife · doi:10.7554/elife.50260 · Cited by 137 · see citing works
“Autophagosomes mature during trafficking along the axon to the soma by fusion with lysosomes, which leads to efficient cargo degradation (Cheng et al., 2015; Hollenbeck, 1993; Lee et al., 2011; Maday and Holzbaur, 2014; Maday et al., 2012; Neisch et al., 2017).”
BackgroundResultSelf-citationFarfel-Becker, T., Roney, J. C., Cheng, X.-T., Li, S., Cuddy, S. R., & Sheng, Z.-H. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.013 · Cited by 152 · see citing works
“Enzymatically Active Degradative Lysosomes Are Positioned in Axons and Distal Tips Although the majority of autophagic and endocytic organelles undergo long-distance retrograde transport fromdistal axons toward the soma, where degradative lysosomes are highly enriched (Cai et al., 2010; Overly et al., 1995; Maday et a…”
InfluentialWang, T., Martin, S., Papadopulos, A., Harper, C. B., Mavlyutov, T. A., Niranjan, D., Glass, N. R., Cooper-White, J. J., Sibarita, J., Choquet, D., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3757-14.2015 · Cited by 151 · see citing works
Endo‐lysosomal and autophagic dysfunction: a driving factor in Alzheimer's disease?
Whyte, L. S., Lau, A. A., Hemsley, K. M., Hopwood, J. J., & Sargeant, T. J. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.13935 · Cited by 150 · see citing works
“…Gowrishankar et al. (2015) described around the plaque on accumulating vesicles is consistent with work showing autophagic vesicles acquire LAMP1 (from fusion with late endosomes and lysosomes) early in their maturation and transport along the axon to the neuronal cell body (Maday et al. 2012).”
BackgroundXie, Y., Zhou, B., Lin, M.-Y., Wang, S., Foust, K. D., & Sheng, Z. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.026 · Cited by 148 · see citing works
“Since neurons are particularly sensitive to the accumulation of misfolded proteins and damaged organelles, newly formed autophagosomes are eliminated quickly by fusing with endolysosomes, thereby avoiding a buildup of AVs (Maday et al., 2012; Cheng et al., 2015).”
BackgroundAutophagy in axonal and dendritic degeneration
Yang, Y., Coleman, M. P., Zhang, L., Zheng, X., & Yue, Z. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.04.001 · Cited by 144 · see citing works
“Once fully acidified in the proximal part of the axons, autophagosomes may switch to bidirectional motility resembling that of lysosomes [30, 34] and initiate the proteolytic clearance of the autophagy substrates [31] (Figure 1a).”
BackgroundInfluentialRocha, E. M., Smith, G. A., Park, E. Y. H., Cao, H., Graham, A.-R., Brown, E., McLean, J. R., Hayes, M. A., Beagan, J. A., Izen, S. C., et al. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6307 · Cited by 144 · see citing works
“Autophagosome biogenesis typically occurs distally at the axon tip and travels to the cell body using retrograde dynein–dynactin transport (33).”
BackgroundGornstein, E. L., & Schwarz, T. L. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.11.015 · Cited by 145 · see citing works
“Furthermore, secondary to a neurite remodeling defect and retraction, disruption of cellular processes at the distal axon, such as autophagosome formation (Maday et al., 2012) and endocytosis of survival factors (Harrington and Ginty, 2013) could contribute to the pathogenesis.”
BackgroundRegulation of mitochondrial dynamics in astrocytes: Mechanisms, consequences, and unknowns
Jackson, J. G., & Robinson, M. B. (2017) · Glia · doi:10.1002/glia.23252 · Cited by 144 · see citing works
“%) of these autophagosomes contain mitochondrial fragments (Maday et al., 2012), suggesting a constitutive, but low level turnover of mitochondria in neuronal processes.”
BackgroundMacroautophagy in CNS health and disease
Griffey, C. J., & Yamamoto, A. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00588-3 · Cited by 144 · see citing works
A role for autophagy in Huntington's disease
Croce, K. R., & Yamamoto, A. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.08.010 · Cited by 139 · see citing works
Niewiadomska, G., Niewiadomski, W., Steczkowska, M., & Gąsiorowska, A. (2021) · Life · doi:10.3390/life11010028 · Cited by 132 · see citing works
Lionaki, E., Markaki, M., Palikaras, K., & Tavernarakis, N. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.04.010 · Cited by 134 · see citing works
“taining dysfunctional or aged mitochondria, has been reported [175].”
BackgroundParkinson's disease: convergence on synaptic homeostasis
Soukup, S., Vanhauwaert, R., & Verstreken, P. (2018) · The EMBO Journal · doi:10.15252/embj.201898960 · Cited by 129 · see citing works
“Autophagy digests parts of the cytoplasm, but at the relatively small presynaptic contacts, where the process is active as well (Maday et al, 2012; Maday & Holzbaur, 2014; Soukup et al, 2016; Oerlundk et al, 2017; Vanhauwaert et al, 2017), it is important to tightly control autophagy as to prevent…”
BackgroundMeasurement of autophagy flux in the nervous system in vivo
Castillo, K., Valenzuela, V, Matus, S., Nassif, M., Oñate, M., Fuentealba, Y., Encina, G., Irrazabal, T., Parsons, G., Court, F. A., et al. (2013) · Cell Death & Disease · doi:10.1038/cddis.2013.421 · Cited by 127 · see citing works
“Autophagosome trafficking along axons was recently described.(31) With this in mind, we monitored the distribution”
BackgroundMethodMechanisms of neuronal homeostasis: Autophagy in the axon
Maday, S. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.047 · Cited by 123 · see citing works
“Retrogradely moving autophagosomes transport engulfed soluble and organelle cargoes such as ubiquitin and mitochondrial fragments (Maday et al., 2012).”
InfluentialSelf-citationImpaired JIP3-dependent axonal lysosome transport promotes amyloid plaque pathology
Gowrishankar, S., Wu, Y., & Ferguson, S. M. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201612148 · Cited by 123 · see citing works
“This interpretation builds on a growing appreciation that there are high rates of autophagy in the distal regions of axons but that such autophagosomes must fuse with endosomes and acquire lysosomal properties such as acidification before undergoing efficient retrograde back toward the cell body for the eventual degra…”
InfluentialBeckers, J., Tharkeshwar, A. K., & Damme, P. V. (2021) · Autophagy · doi:10.1080/15548627.2021.1872189 · Cited by 124 · see citing works
Mitochondrial Morphology Differences and Mitophagy Deficit in Murine Glaucomatous Optic Nerve
Coughlin, L., Morrison, R. S., Horner, P. J., & Inman, D. M. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-16126 · Cited by 124 · see citing works
Neuronal vulnerability in Parkinson disease: Should the focus be on axons and synaptic terminals?
Wong, Y. C., Luk, K. C., Purtell, K., Burke, S., Stoessl, A. J., Trudeau, L., Yue, Z., Krainc, D., Oertel, W. H., Obeso, J. A., et al. (2019) · Movement Disorders · doi:10.1002/mds.27823 · Cited by 123 · see citing works
“to the cell body for degradation through the lysosome.(143,182) Aggregated α-syn impairs macroautophagy(125) as does knockdown of α-syn,(183) which indicates that α-syn”
Background
- 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
- Health Sciences › Medicine › Epidemiology › 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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