The DOI matches its Crossref record; 96 of the 97 references it cites were found in a registry or an index.
Autophagy inhibition promotes SNCA/alpha-synuclein release and transfer via extracellular vesicles with a hybrid autophagosome-exosome-like phenotype
Open accessAbstract
The autophagy-lysosome pathway (ALP) regulates intracellular homeostasis of the cytosolic protein SNCA/alpha-synuclein and is impaired in synucleinopathies, including Parkinson disease and dementia with Lewy bodies (DLB). Emerging evidence suggests that ALP influences SNCA release, but the underlying cellular mechanisms are not well understood. Several studies identified SNCA in exosome/extracellular vesicle (EV) fractions. EVs are generated in the multivesicular body compartment and either released upon its fusion with the plasma membrane, or cleared via the ALP. We therefore hypothesized that inhibiting ALP clearance 1) enhances SNCA release via EVs by increasing extracellular shuttling of multivesicular body contents, 2) alters EV biochemical profile, and 3) promotes SNCA cell-to-cell transfer. Indeed, ALP inhibition increased the ratio of extra- to intracellular SNCA and upregulated SNCA association with EVs in neuronal cells. Ultrastructural analysis revealed a widespread, fused multivesicular body-autophagosome compartment. Biochemical characterization revealed the presence of autophagosome-related proteins, such as LC3-II and SQSTM1. This distinct "autophagosome-exosome-like" profile was also identified in human cerebrospinal fluid (CSF) EVs. After a single intracortical injection of SNCA-containing EVs derived from CSF into mice, human SNCA colocalized with endosome and neuronal markers. Prominent SNCA immunoreactivity and a higher number of neuronal SNCA inclusions were observed after DLB patient CSF EV injections. In summary, this study provides compelling evidence that a) ALP inhibition increases SNCA in neuronal EVs, b) distinct ALP components are present in EVs, and c) CSF EVs transfer SNCA from cell to cell in vivo. Thus, macroautophagy/autophagy may regulate EV protein composition and consequently progression in synucleinopathies.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Because TNT formation relies on actin-dependent machinery (e.g., M-Sec/RalA/exocyst) and ciliary Shh signaling regulates neuronal actin dynamics, ciliary dysfunction may promote TNT formation, while impaired autophagy increases EV loading, collectively enhancing α-syn dissemination (Figure 3B) [102,149,150,153,154,155].”
From The Impact of Neurotoxin Proteins Trafficked by Primary Cilia and Extracellular Vesicles in Neurodegenerative Diseases (2025) · cites this paper as [149]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Similar to AD, disruption of cilia–autophagy crosstalk in PD has been shown to cause neurons to redirect α-syn into EVs, increasing its intercellular transfer, while autophagy inhibition further amplifies α-syn-containing EV release and spread [149,150].”
From The Impact of Neurotoxin Proteins Trafficked by Primary Cilia and Extracellular Vesicles in Neurodegenerative Diseases (2025) · cites this paper as [149]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
1 retracted
Crews, L. A., Spencer, B. J., Desplats, P., Patrick, C., Paulino, A., Rockenstein, E. M., Hansen, L. A., Adame, A., Galasko, D. R., & Masliah, E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009313 · Cited by 379
Self-citationRetractedStaging of brain pathology related to sporadic Parkinson’s disease
Braak, H., Tredici, K. D., Rüb, U., de Vos, R. A. I., Jansen Steur, E. N. H., & Braak, E. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00065-9 · Cited by 10,777
Spillantini, M. G., Schmidt, M. L., Lee, V. M.-Y., Trojanowski, J. Q., Jakes, R., & Goedert, M. (1997) · Nature · doi:10.1038/42166 · Cited by 8,382
Extracellular vesicles: Exosomes, microvesicles, and friends
Raposo, G., & Stoorvogel, W. (2013) · Journal of Cell Biology · doi:10.1083/jcb.201211138 · Cited by 8,099
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894
Iliff, J. J., Wang, M., Liao, Y., Plogg, B. A., Peng, W., Gundersen, G. A., Benveniste, H., Vates, G. E., Deane, R., Goldman, S. A., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003748 · Cited by 5,824
Isolation and Characterization of Exosomes from Cell Culture Supernatants and Biological Fluids
Théry, C., Amigorena, S., Raposo, G., & Clayton, A. (2006) · Current Protocols in Cell Biology · doi:10.1002/0471143030.cb0322s30 · Cited by 5,766
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572
Exosomes: composition, biogenesis and function
Théry, C., Zitvogel, L., & Amigorena, S. (2002) · Nature reviews. Immunology · doi:10.1038/nri855 · Cited by 5,355
Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J.-A., Outzen, H., Øvervatn, A., Bjørkøy, G., & Johansen, T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702824200 · Cited by 4,578
Chronic systemic pesticide exposure reproduces features of Parkinson's disease
Betarbet, R. S., Sherer, T., MacKenzie, G. M., Garcia‐Osuna, M., Panov, A. V., & Greenamyre, J. T. (2000) · Nature Neuroscience · doi:10.1038/81834 · Cited by 3,770
Johnstone, R. M., Adam, M., Hammond, J. R., Orr, L., & Turbide, C. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48095-7 · Cited by 2,931
Trypan Blue Exclusion Test of Cell Viability
Strober, W. (2015) · Current Protocols in Immunology · doi:10.1002/0471142735.ima03bs111 · Cited by 2,631
Impaired Degradation of Mutant α-Synuclein by Chaperone-Mediated Autophagy
Cuervo, A. M., Stefanis, L., Fredenburg, R., Lansbury, P. T., & Sulzer, D. (2004) · Science · doi:10.1126/science.1101738 · Cited by 2,024
Li, J.-Y., Englund, E., Holton, J. L., Soulet, D., Hagell, P., Lees, A. J., Lashley, T., Quinn, N. P., Rehncrona, S., Björklund, A., et al. (2008) · Nature Medicine · doi:10.1038/nm1746 · Cited by 1,845
Bowman, E. J., Siebers, A., & Altendorf, K. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.21.7972 · Cited by 1,801
Fujiki, Y., Hubbard, A. L., Fowler, S., & Lazarow, P. B. (1982) · The Journal of Cell Biology · doi:10.1083/jcb.93.1.97 · Cited by 1,754
Lewy body–like pathology in long-term embryonic nigral transplants in Parkinson's disease
Kordower, J. H., Chu, Y., Hauser, R. A., Freeman, T. B., & Olanow, C. W. (2008) · Nature Medicine · doi:10.1038/nm1747 · Cited by 1,722
In vivo demonstration that α-synuclein oligomers are toxic
Winner, B., Jappelli, R., Maji, S. K., Desplats, P. A., Boyer, L., Aigner, S., Hetzer, C., Loher, T., Vilar, M., Campioni, S., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100976108 · Cited by 1,463
Self-citationLC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation
Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y., & Yoshimori, T. (2004) · Journal of Cell Science · doi:10.1242/jcs.01131 · Cited by 1,394
Trypan Blue Exclusion Test of Cell Viability
Strober, W. (1997) · Current Protocols in Immunology · doi:10.1002/0471142735.ima03bs21 · Cited by 1,349
Yoshimori, T., Yamamoto, A., Moriyama, Y., Futai, M., & Tashiro, Y. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)47429-2 · Cited by 1,334
Yamamoto, A., Tagawa, Y., Yoshimori, T., Moriyama, Y., Masaki, R., & Tashiro, Y. (1998) · Cell Structure and Function · doi:10.1247/csf.23.33 · Cited by 1,312
Emerging regulation and functions of autophagy
Boya, P., Reggiori, F., & Codogno, P. (2013) · Nature Cell Biology · doi:10.1038/ncb2788 · Cited by 1,216
Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S. D., Ntzouni, M., Margaritis, L. H., Stefanis, L., & Vekrellis, K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5699-09.2010 · Cited by 1,115 · cited 3×
“ture medium, including exosomes and other nanovesicles, in several cell line models of SNCA overexpression.(14,17,38) We ini-”
Self-citationExosome: from internal vesicle of the multivesicular body to intercellular signaling device
Denzer, K., Kleijmeer, M. J., Heijnen, H. F. G., Stoorvogel, W., & Geuze, H. J. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.19.3365 · Cited by 1,067
4 Histology and Histopathology
(2015) · Thieme eBooks · doi:10.1055/b-0035-108581 · Cited by 1,052
Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease.
Anglade, P., Vyas, S., Javoy-Agid, F., Herrero, M. T., Michel, P. P., Marquez, J., Prigent, A., Ruberg, M., Hirsch, É. C., & Agid, Y. (1997) · PubMed · Cited by 1,045
Production and purification of lentiviral vectors
Tiscórnia, G., Singer, O., & Verma, I. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.37 · Cited by 974
Role for Rab7 in maturation of late autophagic vacuoles
Jäger, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Säftig, P., & Eskelinen, E. (2004) · Journal of Cell Science · doi:10.1242/jcs.01370 · Cited by 970
Autophagy‐based unconventional secretory pathway for extracellular delivery of IL‐1β
Dupont, N., Jiang, S., Pilli, M., Ornatowski, W., Bhattacharya, D., & Deretic, V. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.398 · Cited by 967
Dagda, R. K., Cherra, S. J., Kulich, S. M., Tandon, A., Park, D., & Chu, C. T. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808515200 · Cited by 954
Nalls, M. A. (2011) · The Lancet · doi:10.1016/s0140-6736(10)62345-8 · Cited by 922
Microautophagy of Cytosolic Proteins by Late Endosomes
Sahu, R., Kaushik, S., Clement, C. C., Cannizzo, E. S., Scharf, B., Follenzi, A., Potolicchio, I., Nieves, E., Cuervo, A. M., & Santambrogio, L. (2011) · Developmental Cell · doi:10.1016/j.devcel.2010.12.003 · Cited by 902
Exosomal cell-to-cell transmission of alpha synuclein oligomers
Danzer, K. M., Kranich, L. R., Ruf, W. P., Cagsal‐Getkin, O., Winslow, A. R., Zhu, L., Vanderburg, C. R., & McLean, P. J. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-42 · Cited by 879
Exosome Release Is Regulated by a Calcium-dependent Mechanism in K562 Cells
Savina, A., Furlán, M., Vidal, M., & Colombo, M. I. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301642200 · Cited by 835
Intravesicular Localization and Exocytosis of α-Synuclein and its Aggregates
Lee, H.-J., Patel, S. S., & Lee, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0692-05.2005 · Cited by 826
Biogenesis and Function of Multivesicular Bodies
Piper, R. C., & Katzmann, D. J. (2007) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123319 · Cited by 771
Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission
Alvarez‐Erviti, L., Seow, Y., Schapira, A. H. V., Gardiner, C., Sargent, I. L., Wood, M. J. A., & Cooper, J. A. D. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.01.029 · Cited by 762
Extracellular vesicles round off communication in the nervous system
Budnik, V., Ruiz-Cañada, C., & Wendler, F. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.29 · Cited by 712
El-Agnaf, O. M. A., Salem, S. A., Paleologou, K. E., Cooper, L. J., Fullwood, N. J., Gibson, M. J., Curran, M. D., Court, J. A., Mann, D. M. A., Ikeda, S.-I., et al. (2003) · The FASEB Journal · doi:10.1096/fj.03-0098fje · Cited by 590
Chaperone-Mediated Autophagy Markers in Parkinson Disease Brains
Alvarez‐Erviti, L., Rodríguez-Oroz, M. C., Cooper, J. A. D., Caballero, C., Ferrer, I., Obeso, J. A., & Schapira, A. H. V. (2010) · Archives of Neurology · doi:10.1001/archneurol.2010.198 · Cited by 577
Lysosomes, pH and the Anti-malarial Action of Chloroquine
Homewood, C. A., Warhurst, D. C., Peters, W., & Baggaley, V. C. (1972) · Nature · doi:10.1038/235050a0 · Cited by 530
Identification and proteomic profiling of exosomes in human cerebrospinal fluid
Street, J. M., Barran, P. E., Mackay, C. L., Weidt, S. K., Balmforth, C., Walsh, T. S., Chalmers, R. T. A., Webb, D. J., & Dear, J. W. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-5 · Cited by 508
Autophagy and neurodegeneration: when the cleaning crew goes on strike
Martínez‐Vicente, M., & Cuervo, A. M. (2007) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70076-5 · Cited by 495
Fader, C. M., Sánchez‐Martínez, D., Furlán, M., & Colombo, M. I. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00677.x · Cited by 490
Autophagy Proteins Regulate the Secretory Component of Osteoclastic Bone Resorption
DeSelm, C. J., Miller, B. C., Zou, W., Beatty, W. L., van Meel, E., Takahata, Y., Klumperman, J., Tooze, S. A., Teitelbaum, S. L., & Virgin, H. W. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.08.016 · Cited by 487
Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease
Goetzl, E. J., Boxer, A., Schwartz, J. B., Abner, E. L., Petersen, R. C., Miller, B. L., & Kapogiannis, D. (2015) · Neurology · doi:10.1212/wnl.0000000000001702 · Cited by 446
Vanlandingham, P. A., & Ceresa, B. P. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m809277200 · Cited by 441
Unconventional secretion of Acb1 is mediated by autophagosomes
Duran, J. M., Anjard, C., Stefan, C., Loomis, W. F., & Malhotra, V. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200911154 · Cited by 433
Stuendl, A., Kunadt, M., Kruse, N., Bartels, C., Moebius, W., Danzer, K. M., Mollenhauer, B., & Schneider, A. (2016) · Brain · doi:10.1093/brain/awv346 · Cited by 428
Self-citationTokuda, T., Salem, S. A., Allsop, D., Mizuno, T., Nakagawa, M., Qureshi, M. M., Locascio, J. J., Schlossmacher, M. G., & El-Agnaf, O. M. A. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.08.024 · Cited by 425
Ebrahimi‐Fakhari, D., Cantuti‐Castelvetri, I., Fan, Z., Rockenstein, E. M., Masliah, E., Hyman, B. T., McLean, P. J., & Unni, V. K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1560-11.2011 · Cited by 387
Self-citationAcceleration of α-Synuclein Aggregation by Exosomes
Grey, M., Dunning, C. J. R., Gaspar, R., Grey, C. E., Brundin, P., Sparr, E., & Linse, S. S. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.585703 · Cited by 383
Xilouri, M., Vogiatzi, T., Vekrellis, K., Park, D. S., & Stefanis, L. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005515 · Cited by 373
Self-citationBalusu, S., Wonterghem, E. V., Rycke, R. M. D., Raemdonck, K., Stremersch, S., Gevaert, K., Brkić, M., Demeestere, D., Vanhooren, V., Hendrix, A., et al. (2016) · EMBO Molecular Medicine · doi:10.15252/emmm.201606271 · Cited by 350
Paleologou, K. E., Oueslati, A., Shakked, G., Rospigliosi, C. C., Kim, H., Lamberto, G. R., Fernández, C. O., Schmid, A. W., Chegini, F., Gai, W., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5922-09.2010 · Cited by 339
Self-citationChoroid plexus transcytosis and exosome shuttling deliver folate into brain parenchyma
Grapp, M., Wrede, A., Schweizer, M., Hüwel, S., Galla, H., Snaidero, N., Simons, M., Bückers, J., Low, P. S., Urlaub, H., et al. (2013) · Nature Communications · doi:10.1038/ncomms3123 · Cited by 338
Early endosomes and endosomal coatomer are required for autophagy
Razi, M., Chan, E. Y. W., & Tooze, S. A. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200810098 · Cited by 298
Functional Consequences of α-Synuclein Tyrosine Nitration
Hodara, R., Norris, E. H., Giasson, B. I., Mishizen-Eberz, A. J., Lynch, D. R., Lee, V. M. ‐., & Ischiropoulos, H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408906200 · Cited by 296
Johnstone, R., Bianchini, A., & Teng, K. (1989) · Blood · doi:10.1182/blood.v74.5.1844.1844 · Cited by 289
Jang, A., Lee, H., Suk, J., Jung, J., Kim, K., & Lee, S. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06695.x · Cited by 281
Proteomic analysis of cerebrospinal fluid extracellular vesicles: A comprehensive dataset
Chiasserini, D., van Weering, J. R. T., Piersma, S. R., Pham, T. V., Malekzadeh, A., Teunissen, C. E., de Wit, H., & Jiménez, C. R. (2014) · Journal of Proteomics · doi:10.1016/j.jprot.2014.04.028 · Cited by 269
PIKfyve inhibition increases exosome release and induces secretory autophagy
Hessvik, N. P., Øverbye, A., Brech, A., Torgersen, M. L., Jakobsen, I. S., Sandvig, K., & Llorente, A. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2309-8 · Cited by 269
Ejlerskov, P., Rasmussen, I., Nielsen, T. T., Bergström, A., Tohyama, Y., Jensen, P. H., & Vilhardt, F. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.401174 · Cited by 242
Development of the choroid plexus and blood-CSF barrier
Liddelow, S. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00032 · Cited by 238
Pranke, I. M., Morello, V., Bigay, J., Gibson, K. H., Verbavatz, J., Antonny, B., & Jackson, C. L. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201011118 · Cited by 219
Schmid, G., & Obst, M. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-776-1 · Cited by 217
Boosting chaperone-mediated autophagy in vivo mitigates α-synuclein-induced neurodegeneration
Xilouri, M., Brekk, O. R., Landeck, N., Pitychoutis, P. M., Papasilekas, T., Papadopoulou-Daifoti, Z., Kirik, D., & Stefanis, L. (2013) · Brain · doi:10.1093/brain/awt131 · Cited by 215
Autophagy modulates SNCA/α-synuclein release, thereby generating a hostile microenvironment
Poehler, A.-M., Xiang, W., Spitzer, P., May, V. E. L., Meixner, H., Rockenstein, E., Chutna, O., Outeiro, T. F., Winkler, J., Masliah, E., et al. (2014) · Autophagy · doi:10.4161/auto.36436 · Cited by 212
Self-citationGriffiths, R. E., Kupzig, S., Cogan, N. M., Mankelow, T. J., Betin, V. M. S., Trakarnsanga, K., Massey, E., Lane, J. D., Parsons, S. F., & Anstee, D. J. (2012) · Blood · doi:10.1182/blood-2011-09-376475 · Cited by 182
Extracellular vesicle sorting of α-Synuclein is regulated by sumoylation
Kunadt, M., Eckermann, K., Stuendl, A., Gong, J., Russo, B., Strauss, K., Rai, S., Kügler, S., Falomir‐Lockhart, L. J., Schwalbe, M., et al. (2015) · Acta Neuropathologica · doi:10.1007/s00401-015-1408-1 · Cited by 180
Self-citationATP13A2/PARK9 Regulates Secretion of Exosomes and α-Synuclein
Tsunemi, T., Hamada, K., & Krainc, D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1629-14.2014 · Cited by 172
Unconventional protein secretion: an evolving mechanism
Malhotra, V. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.104 · Cited by 171
Assessment of α-Synuclein Secretion in Mouse and Human Brain Parenchyma
Emmanouilidou, E., Elenis, D., Papasilekas, T., Stranjalis, G., Gerozissis, K., Ioannou, P. C., & Vekrellis, K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022225 · Cited by 163
Self-citationNuber, S., Harmuth, F., Kohl, Z., Adame, A., Trejo, M., Schönig, K., Zimmermann, F., Bauer, C. C., Casadei, N., Giel, C., et al. (2013) · Brain · doi:10.1093/brain/aws358 · Cited by 161
Self-citationAlpha-synuclein aggregation involves a bafilomycin A1-sensitive autophagy pathway
Klucken, J., Poehler, A.-M., Ebrahimi‐Fakhari, D., Schneider, J., Nuber, S., Rockenstein, E. M., Schlötzer-Schrehardt, U. M., Hyman, B. T., McLean, P. J., Masliah, E., et al. (2012) · Autophagy · doi:10.4161/auto.19371 · Cited by 141
Self-citationPérez-Revuelta, B. I., Hettich, M. M., Ciociaro, A., Rotermund, C., Kahle, P. J., Krauss, S., & Di Monte, D. A. (2014) · Cell Death & Disease · doi:10.1038/cddis.2014.175 · Cited by 140
Antagonizing Neuronal Toll-like Receptor 2 Prevents Synucleinopathy by Activating Autophagy
Kim, C., Rockenstein, E., Spencer, B., Kim, H.-K., Adame, A., Trejo, M., Stafa, K., Lee, H.-J., Lee, S.-J., & Masliah, E. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.044 · Cited by 135
Self-citationSzatmári, Z., Kis, V., Lippai, M., Hegedűs, K., Faragó, T., Lőrincz, P., Tanaka, T., Juhász, G., & Sass, M. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-10-0574 · Cited by 135
The role of membrane-trafficking small GTPases in the regulation of autophagy
Bento, C. F., Puri, C., Moreau, K., & Rubinsztein, D. C. (2013) · Journal of Cell Science · doi:10.1242/jcs.123075 · Cited by 118
Mollenhauer, B., El‐Agnaf, O. M. A., Marcus, K., Trenkwalder, C., & Schlossmacher, M. G. (2010) · Biomarkers in Medicine · doi:10.2217/bmm.10.90 · Cited by 114
Self-citationLysosomal Network Proteins as Potential Novel CSF Biomarkers for Alzheimer’s Disease
Armstrong, A., Mattsson, N., Appelqvist, H., Janefjord, C., Sandin, L., Agholme, L., Olsson, B., Svensson, S., Blennow, K., Zetterberg, H., et al. (2013) · NeuroMolecular Medicine · doi:10.1007/s12017-013-8269-3 · Cited by 113
Clearance from the mouse brain by convection of interstitial fluid towards the ventricular system
Bedussi, B., van Lier, M. G. J. T. B., Bartstra, J. W., de Vos, J., Siebes, M., VanBavel, E., & Bakker, E. N. T. P. (2015) · Fluids and Barriers of the CNS · doi:10.1186/s12987-015-0019-5 · Cited by 102
Regulation of Membrane Protein Degradation by Starvation‐Response Pathways
Jones, C. B., Ott, E. M., Keener, J., Curtiss, M., Sandrin, V., & Babst, M. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01314.x · Cited by 100
Martin, S., Harper, C. B., May, L. M., Coulson, E. J., Meunier, F. A., & Osborne, S. L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060152 · Cited by 93
Rockenstein, E. M., Schwach, G., Ingolić, E., Adame, A., Crews, L. A., Mante, M., Pfragner, R., Schreiner, E., Windisch, M., & Masliah, E. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20446 · Cited by 90
Self-citationKohl, Z., Abdallah, N. B. B., Vogelgsang, J., Tischer, L., Deusser, J., Amato, D., Anderson, S., Müller, C., Riess, O., Masliah, E., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.10.021 · Cited by 89
Self-citationScotti, E., Calamai, M., Goulbourne, C. N., Zhang, L., Hong, C., Lin, R. R., Choi, J., Pilch, P. F., Fong, L. G., Zou, P., et al. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01716-12 · Cited by 81
Interplay between Sumoylation and Phosphorylation for Protection against α-Synuclein Inclusions
Shahpasandzadeh, H., Popova, B., Kleinknecht, A., Fraser, P. E., Outeiro, T. F., & Braus, G. H. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.559237 · Cited by 81
Sasaki, A., Arawaka, S., Sato, H., & Kato, T. (2015) · Scientific Reports · doi:10.1038/srep14211 · Cited by 79
GABA transmission via ATP-dependent K + channels regulates α-synuclein secretion in mouse striatum
Emmanouilidou, E., Minakaki, G., Keramioti, M. V., Xylaki, M., Balafas, E., Chrysanthou‐Piterou, M., Kloukina, I., & Vekrellis, K. (2016) · Brain · doi:10.1093/brain/awv403 · Cited by 77
Self-citationMenges, S., Minakaki, G., Schaefer, P. M., Meixner, H., Prots, I., Schlötzer-Schrehardt, U., Friedland, K., Winner, B., Outeiro, T., Winklhofer, K., et al. (2017) · Scientific Reports · doi:10.1038/srep42942 · Cited by 74
Self-citationMaerkens, A., Olivé, M., Schreiner, A., Feldkirchner, S., Schessl, J., Uszkoreit, J., Barkovits, K., Güttsches, A., Theis, V., Eisenacher, M., et al. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0280-0 · Cited by 67
Self-citationClinical and biochemical correlates of insoluble α-synuclein in dementia with Lewy bodies
Klucken, J., Ingelsson, M., Shin, Y., Irizarry, M. C., Hedley‐Whyte, E. T., Frosch, M. P., Growdon, J. H., McLean, P. J., & Hyman, B. T. (2006) · Acta Neuropathologica · doi:10.1007/s00401-005-0027-7 · Cited by 60
Self-citationSpencer, B. J., Kim, C., Gonzalez, T., Bisquertt, A., Patrick, C., Rockenstein, E. M., Adame, A., Lee, S., Desplats, P., & Masliah, E. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddv633 · Cited by 59
Self-citation
Cited by
Sorted by citations
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin‐Smith, G. K., et al. (2018) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2018.1535750 · Cited by 11,099
Self-citationDai, E., Han, L., Liu, J., Xie, Y., Kroemer, G., Klionsky, D. J., Zeh, H. J., Kang, R., Wang, J., & Tang, D. (2020) · Autophagy · doi:10.1080/15548627.2020.1714209 · Cited by 613
Microglial exosomes facilitate α-synuclein transmission in Parkinson’s disease
Guo, M., Wang, J., Zhao, Y., Feng, Y., Han, S., Dong, Q., Cui, M., & Tieu, K. (2020) · Brain · doi:10.1093/brain/awaa090 · Cited by 522
Buratta, S., Tancini, B., Sagini, K., Delo, F., Chiaradia, E., Urbanelli, L., & Emiliani, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21072576 · Cited by 446
Therapeutic strategies for Parkinson disease: beyond dopaminergic drugs
Charvin, D., Medori, R., Hauser, R. A., & Rascol, O. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.136 · Cited by 294
Metadata
- Authors
- Minakaki, G., Menges, S., Kittel, A., Emmanouilidou, E., Schaeffner, I., Barkovits, K., Bergmann, A., Rockenstein, E., Adame, A., Marxreiter, F., Mollenhauer, B., Galasko, D., Buzás, E. I., Schlötzer-Schrehardt, U., Marcus, K., Xiang, W., Lie, D. C., Vekrellis, K., Masliah, E., Winkler, J., & Klucken, J.
- Affiliations
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Semmelweis University
- Biomedical Research Foundation of the Academy of Athens (GR)
- Ruhr University Bochum (DE)
- University of California System (US)
- Universitätsmedizin Göttingen (DE)
- Semmelweis University (HU)
- Universitätsklinikum Erlangen (DE)
- Corresponding author
- Klucken, Jochen
- ORCID
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2018-01-02
- Volume
- 14
- Issue
- 1
- Pages
- 98-119
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- PMC
- PMC5846507
- OpenAlex
- W2774564892
- Cited by
- 272
- References
- 97
- Citations by year
- 2026: 32 · 2025: 24 · 2024: 34 · 2023: 26 · 2022: 41 · 2021: 41 · 2020: 38 · 2019: 22 · 2018: 14
- FWCI
- 14.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Autophagy (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Funders
- Interdisciplinary Center of Clinical Research (IZKF) of the University Hospital Erlangen, Germany (IZKF no. E21 and E11)
- deutsche Forschungsgemeinschaft/German Research Foundation (DFG, no. KL1395/8-1)
- Johannes und Frieda Marohn-Stiftung (Alpha-synuclein)
- H2020 project NISCI (GA no. 681094)
- National Institutes of Health (NIH AGO5131 and NIH AG18440)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Keywords
- autophagy inhibition, alpha-synuclein, extracellular vesicles, exosomes, autophagy-lysosome pathway, multivesicular bodies, cell-to-cell transmission, cerebrospinal fluid, dementia with Lewy bodies, Parkinson's disease, synucleinopathies, LC3-II, p62, neuronal inclusions
- MeSH terms
- Autophagosomes, Animals, Autophagy, Cells, Cultured, Chloroquine, Humans, Lysosomes, Neurons, Parkinson Disease, Biomarkers, Rats, Sprague-Dawley, Macrolides, Lewy Body Disease, Protein Transport, Mice, alpha-Synuclein, Exosomes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
