Role of Glia-Derived Extracellular Vesicles in Neurodegenerative Diseases
Open accessAbstract
Extracellular vesicles (EVs), as nano-sized vesicles secreted by almost all cells, have been recognized as the essential transmitter for cell-to-cell communication and participating in multiple biological processes. Neurodegenerative diseases (ND), such as Alzheimer’s disease, Parkinson’s disease, and amyotrophic lateral sclerosis, share common mechanisms of the aggregation and propagation of distinct pathologic proteins among cells in the nervous systems and neuroinflammatory reactions mediated by glia during the pathogenic process. This feature indicates the vital role of crosstalk between neurons and glia in the pathogenesis of ND. In recent years, glia-derived EVs have been investigated as potential mediators of signals between neurons and glia, which provides a new direction and strategy for understanding ND. By a comprehensive summary, it can be concluded that glia-derived EVs have both a beneficial and/or a detrimental effect in the process of ND. Therefore, this review article conveys the role of glia-derived EVs in the pathogenesis of ND and raises current limitations of their potential application in the diagnosis and treatment of ND.
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In AD, EVs released from brain cells, particularly microglia and astrocytes, have been implicated in exacerbating neuroinflammation, a critical component of AD pathology.
“In AD, EVs released from brain cells, particularly microglia and astrocytes, have been implicated in exacerbating neuroinflammation, a critical component of AD pathology [137, 143].”
From Extracellular vesicles as nanotheranostic platforms for targeted neurological disorder interventions (2024) · cites this paper as [143]
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2 retracted
Zhao, Y., Haney, M. J., Gupta, R., Bohnsack, J. P., He, Z., Kabanov, A. V., & Batrakova, E. V. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106867 · Cited by 144 · see citing works
RetractedHaney, M. J., Zhao, Y., Harrison, E. B., Mahajan, V., Ahmed, S., He, Z., Suresh, P., Hingtgen, S., Klyachko, N. L., Mosley, R. L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061852 · Cited by 143 · see citing works
RetractedShedding light on the cell biology of extracellular vesicles
van Niel, G., D'Angelo, G., & Raposo, G. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.125 · Cited by 8,369 · see citing works
Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes
Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., & Wood, M. J. A. (2011) · Nature Biotechnology · doi:10.1038/nbt.1807 · Cited by 4,930 · see citing works
Mathieu, M., Jaular, L. M., Lavieu, G., & Théry, C. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0250-9 · Cited by 3,776 · see citing works
The neuropathological diagnosis of Alzheimer's disease
DeTure, M. A., & Dickson, D. W. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0333-5 · Cited by 3,329 · cited 2× · see citing works
“A study reported that reducing the secretion of astrocyte-derived EVs by nSMase2 improves pathology and cognition in an AD mouse model (Dinkins et al., 2016).”
BackgroundMicroglia Function in the Central Nervous System During Health and Neurodegeneration
Colonna, M., & Butovsky, O. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-051116-052358 · Cited by 2,894 · see citing works
Differential Roles of M1 and M2 Microglia in Neurodegenerative Diseases
Tang, Y., & Le, W. (2016) · Molecular Neurobiology · doi:10.1007/s12035-014-9070-5 · Cited by 2,190 · see citing works
Self-citationThe Nature and Significance of Platelet Products in Human Plasma
Wolf, P. (1967) · British Journal of Haematology · doi:10.1111/j.1365-2141.1967.tb08741.x · Cited by 1,725 · see citing works
Depletion of microglia and inhibition of exosome synthesis halt tau propagation
Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S., & Ikezu, T. (2015) · Nature Neuroscience · doi:10.1038/nn.4132 · Cited by 1,591 · see citing works
Astrocyte Crosstalk in CNS Inflammation
Linnerbauer, M., Wheeler, M. A., & Quintana, F. J. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.012 · Cited by 989 · see citing works
Lee, H.-J., Suk, J.-E., Patrick, C., Bae, E.-J., Cho, J.-H., Rho, S., Hwang, D., Masliah, E., & Lee, S.-J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.081125 · Cited by 877 · see citing works
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 852 · see citing works
Neurotransmitter-Triggered Transfer of Exosomes Mediates Oligodendrocyte–Neuron Communication
Frühbeis, C., Fröhlich, D., Kuo, W. P., Amphornrat, J., Thilemann, S., Saab, A. S., Kirchhoff, F., Möbius, W., Goebbels, S., Nave, K.-A., et al. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001604 · Cited by 812 · see citing works
Zhang, Y., Chopp, M., Meng, Y., Katakowski, M., Xin, H., Mahmood, A., & Xiong, Y. (2015) · Journal of neurosurgery · doi:10.3171/2014.11.jns14770 · Cited by 737 · see citing works
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 · see citing works
Plasma exosomal α-synuclein is likely CNS-derived and increased in Parkinson’s disease
Shi, M., Liu, C., Cook, T. J., Bullock, K. M., Zhao, Y., Ginghina, C., Li, Y., Aro, P., Dator, R., He, C., et al. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1314-y · Cited by 676 · see citing works
The release and trans-synaptic transmission of Tau via exosomes
Wang, Y., Balaji, V., Kaniyappan, S., Krüger, L., Irsen, S., Tepper, K., Chandupatla, R., Maetzler, W., Schneider, A., Mandelkow, E., et al. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-016-0143-y · Cited by 674 · see citing works
Astrocytes and Glioblastoma cells release exosomes carrying mtDNA
Guescini, M., Genedani, S., Stocchi, V., & Agnati, L. F. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0288-8 · Cited by 662 · see citing works
Protein transmission in neurodegenerative disease
Peng, C., Trojanowski, J. Q., & Lee, V. M.-Y. (2020) · Nature Reviews Neurology · doi:10.1038/s41582-020-0333-7 · Cited by 625 · see citing works
Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes
Katsuda, T., Tsuchiya, R., Kosaka, N., Yoshioka, Y., Takagaki, K., Oki, K., Takeshita, F., Sakai, Y., Kuroda, M., & Ochiya, T. (2013) · Scientific Reports · doi:10.1038/srep01197 · Cited by 565 · see citing works
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 · see citing works
Therapeutic Applications of Extracellular Vesicles: Clinical Promise and Open Questions
György, B., Hung, M. E., Breakefield, X. O., & Leonard, J. N. (2014) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010814-124630 · Cited by 512 · see citing works
Specification and Morphogenesis of Astrocytes
Freeman, M. R. (2010) · Science · doi:10.1126/science.1190928 · Cited by 489 · see citing works
Song, Y., Li, Z., He, T., Qu, M., Jiang, L., Li, W., Shi, X., Pan, J., Zhang, L., Wang, Y., et al. (2019) · Theranostics · doi:10.7150/thno.30879 · Cited by 487 · see citing works
The role of TDP-43 mislocalization in amyotrophic lateral sclerosis
Suk, T. R., & Rousseaux, M. W. C. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00397-1 · Cited by 456 · see citing works
Propagation and spread of pathogenic protein assemblies in neurodegenerative diseases
Jucker, M., & Walker, L. C. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0238-6 · Cited by 450 · see citing works
Alpha-synuclein structure and Parkinson’s disease – lessons and emerging principles
Meade, R. M., Fairlie, D. P., & Mason, J. M. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0329-1 · Cited by 430 · see citing works
HUANG, S. H., Ge, X., Yu, J., Han, Z., Yin, Z., Li, Y., Chen, F., Wang, H., Zhang, J., & Lei, P. (2017) · The FASEB Journal · doi:10.1096/fj.201700673r · Cited by 422 · see citing works
Microglia modulate neurodegeneration in Alzheimer’s and Parkinson’s diseases
Bartels, T., De Schepper, S., & Hong, S. (2020) · Science · doi:10.1126/science.abb8587 · Cited by 412 · see citing works
Cargo proteins of plasma astrocyte‐derived exosomes in Alzheimer's disease
Goetzl, E. J., Mustapić, M., Kapogiannis, D., Eitan, E., Lobach, I. V., Goetzl, L. M., Schwartz, J. B., & Miller, B. L. (2016) · The FASEB Journal · doi:10.1096/fj.201600756r · Cited by 397 · see citing works
High complement levels in astrocyte‐derived exosomes of Alzheimer disease
Goetzl, E. J., Schwartz, J. B., Abner, E. L., Jicha, G. A., & Kapogiannis, D. (2018) · Annals of Neurology · doi:10.1002/ana.25172 · Cited by 369 · see citing works
Long, X., Yao, X., Jiang, Q., Yang, Y., He, X., Tian, W., Zhao, K., & Zhang, H. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01761-0 · Cited by 327 · see citing works
Microglial-derived microparticles mediate neuroinflammation after traumatic brain injury
Kumar, A., Stoica, B. A., Loane, D. J., Yang, M., Abulwerdi, G. A., Khan, N., Kumar, A., Thom, S. R., & Faden, A. I. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0819-4 · Cited by 318 · see citing works
Sun, G., Li, G., Li, D., Huang, W., Zhang, R., Zhang, H., Duan, Y., & Wang, B. (2018) · Materials Science and Engineering C · doi:10.1016/j.msec.2018.04.006 · Cited by 314 · see citing works
Prada, I., Gabrielli, M., Turola, E., Iorio, A., D’Arrigo, G., Parolisi, R., De Luca, M., Pacifici, M., Bastoni, M., Lombardi, M., et al. (2018) · Acta Neuropathologica · doi:10.1007/s00401-017-1803-x · Cited by 312 · see citing works
Basso, M., Pozzi, S., Tortarolo, M., Fiordaliso, F., Bisighini, C., Pasetto, L., Spaltro, G., Lidonnici, D., Gensano, F., Battaglia, E., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.425066 · Cited by 274 · see citing works
Microglia convert aggregated amyloid-β into neurotoxic forms through the shedding of microvesicles
Joshi, P., Turola, E., Ruiz, A., Bergami, A., Libera, D. D., Benussi, L., Giussani, P., Magnani, G., Comı, G., Legname, G., et al. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.180 · Cited by 274 · see citing works
Fröhlich, D., Kuo, W. P., Frühbeis, C., Sun, J.-J., Zehendner, C. M., Luhmann, H. J., Pinto, S., Toedling, J., Trotter, J., & Krämer-Albers, E.-M. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2013.0510 · Cited by 274 · see citing works
Söllvander, S., Nikitidou, E., Brolin, R., Söderberg, L., Sehlin, D., Lannfelt, L., & Erlandsson, A. (2016) · Molecular Neurodegeneration · doi:10.1186/s13024-016-0098-z · Cited by 267 · see citing works
Losurdo, M., Pedrazzoli, M., D’Agostino, C., Elia, C., Massenzio, F., Lonati, E., Mauri, M., Rizzi, L., Molteni, L., Bresciani, E., et al. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0327 · Cited by 265 · see citing works
Regulation of heat shock protein 70 release in astrocytes: Role of signaling kinases
Taylor, A. R., Robinson, M., Gifondorwa, D. J., Tytell, M., & Milligan, C. E. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20559 · Cited by 261 · see citing works
Jarmalavičiūtė, A., Tunaitis, V., Pivoraitė, U., Venalis, A., & Pivoriūnas, A. (2015) · Cytotherapy · doi:10.1016/j.jcyt.2014.07.013 · Cited by 260 · see citing works
Zhang, X., Chen, S., Song, L., Tang, Y., Shen, Y., Li, J. X., & Le, W. (2014) · Autophagy · doi:10.4161/auto.27710 · Cited by 256 · see citing works
Self-citationClayton, K., Delpech, J. C., Herron, S., Iwahara, N., Ericsson, M., Saito, T., Saido, T. C., Ikezu, S., & Ikezu, T. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00440-9 · Cited by 245 · see citing works
Dinkins, M. B., Enasko, J., Hernandez, C. M., Wang, G., Kong, J., Helwa, I., Liu, Y., Terry, A. V., & Bieberich, E. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1429-16.2016 · Cited by 243 · see citing works
Exosomes as a Nanodelivery System: a Key to the Future of Neuromedicine?
Aryani, A., & Denecke, B. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-9054-5 · Cited by 240 · see citing works
Microglia-neuron crosstalk: Signaling mechanism and control of synaptic transmission
Marinelli, S., Basilico, B., Marrone, M. C., & Ragozzino, D. (2019) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2019.05.017 · Cited by 233 · cited 1× · see citing works
“The continuous crosstalk between microglia and neurons is dependent on microglia housekeeping functions and contributes to the homeostasis of CNS (Marinelli et al., 2019).”
BackgroundExosome-inflammasome crosstalk and their roles in inflammatory responses
Noonin, C., & Thongboonkerd, V. (2021) · Theranostics · doi:10.7150/thno.54004 · Cited by 233 · see citing works
Moving fluid biomarkers for Alzheimer’s disease from research tools to routine clinical diagnostics
Zetterberg, H., & Blennow, K. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00430-x · Cited by 219 · see citing works
Zhong, L., Wang, Z., Wang, D., Wang, Z., Martens, Y. A., Wu, L., Xu, Y., Wang, K., Li, J., Huang, R., et al. (2018) · Molecular Neurodegeneration · doi:10.1186/s13024-018-0247-7 · Cited by 217 · see citing works
de Godoy, M. A., Saraiva, L. M., de Carvalho, L. R. P., Vasconcelos-dos-Santos, A., Beiral, H. J. V., Ramos, A. B., Silva, L. R. D. P., Leal, R. B., Monteiro, V. H. S., Braga, C. V., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.807180 · Cited by 214 · see citing works
Microglia as modulators of exosomal alpha-synuclein transmission
Xia, Y. F., Zhang, G., Han, C., Ma, K., Guo, X., Wan, F. J., Kou, L., Yin, S., Liu, L., Huang, J., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1404-9 · Cited by 208 · see citing works
MicroRNA biomarkers of Parkinson’s disease in serum exosome-like microvesicles
Cao, X., Lu, J., Zhao, Z., Li, M.-C., Lu, T., An, X., & Xue, L. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.02.045 · Cited by 207 · see citing works
Ser(P)‐1292 LRRK2 in urinary exosomes is elevated in idiopathic Parkinson's disease
Fraser, K. B., Rawlins, A. B., Clark, R. G., Alcalay, R. N., Standaert, D. G., Liu, N., & West, A. B. (2016) · Movement Disorders · doi:10.1002/mds.26686 · Cited by 197 · see citing works
Varcianna, A., Myszczynska, M. A., Castelli, L. M., O'Neill, B., Kim, Y., Talbot, J., Nyberg, S., Nyamali, I., Heath, P. R., Stopford, M. J., et al. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2018.11.067 · Cited by 194 · see citing works
Oligodendrocytes support axonal transport and maintenance via exosome secretion
Frühbeis, C., Kuo, W. P., Müller, C., Barth, K., Peris, L., Tenzer, S., Möbius, W., Werner, H. B., Nave, K., Fröhlich, D., et al. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000621 · Cited by 193 · see citing works
Muraoka, S., DeLeo, A. M., Sethi, M. K., Takamatsu-Yukawa, K., Yang, Z., Ko, J., Hogan, J., Ruan, Z., You, Y., Wang, Y., et al. (2020) · Alzheimer s & Dementia · doi:10.1002/alz.12089 · Cited by 189 · see citing works
Lombardi, M., Parolisi, R., Scaroni, F., Bonfanti, E., Gualerzi, A., Gabrielli, M., de Rosbo, N. K., Uccelli, A., Giussani, P., Viani, P., et al. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-02049-1 · Cited by 188 · see citing works
Inflammation leads to distinct populations of extracellular vesicles from microglia
Yang, Y., Boza‐Serrano, A., Dunning, C. J. R., Clausen, B. H., Lambertsen, K. L., & Deierborg, T. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1204-7 · Cited by 186 · see citing works
Chaudhuri, A. D., Dastgheyb, R. M., Yoo, S.-W., Trout, A., Talbot Jr, C. C., Hao, H., Witwer, K. W., & Haughey, N. J. (2018) · Cell Death & Disease · doi:10.1038/s41419-018-0369-4 · Cited by 184 · see citing works
Guitart, K., Loers, G., Buck, F., Bork, U., Schachner, M., & KLEENE, R. B. (2016) · Glia · doi:10.1002/glia.22963 · Cited by 184 · see citing works
Niu, M., Li, Y., Li, G., Zhou, L., Luo, N., Yao, M., Kang, W., & Liu, J. (2020) · European Journal of Neurology · doi:10.1111/ene.14208 · Cited by 178 · see citing works
Zhao, Z., Chen, Z., Zhou, R., Zhang, X., Ye, Q., & Wang, Y. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00438 · Cited by 177 · see citing works
You, Y., Borgmann, K., Edara, V. V., Stacy, S., Ghorpade, A., & Ikezu, T. (2020) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2019.1706801 · Cited by 176 · see citing works
Pascua‐Maestro, R., González, E., Lillo, C., Ganfornina, M. D., Falcón‐Pérez, J. M., & Sánchez, D. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00526 · Cited by 175 · see citing works
Sarkar, S., Rokad, D., Malovic, E., Luo, J., Harischandra, D. S., Jin, H., Anantharam, V., Huang, X., Lewis, M., Kanthasamy, A., et al. (2019) · Science Signaling · doi:10.1126/scisignal.aat9900 · Cited by 171 · see citing works
Silverman, J. M., Christy, D., Shyu, C. C., Moon, K., Fernando, S. M., Gidden, Z., Cowan, C. M., Ban, Y., Stacey, R. G., Grad, L. I., et al. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.004825 · Cited by 166 · see citing works
Biomarkers for Parkinson’s Disease: How Good Are They?
Li, T., & Le, W. (2019) · Neuroscience Bulletin · doi:10.1007/s12264-019-00433-1 · Cited by 164 · see citing works
Self-citationGlial phagocytic clearance in Parkinson’s disease
Tremblay, M., Cookson, M., & Civiero, L. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0314-8 · Cited by 159 · see citing works
Muraoka, S., Jedrychowski, M. P., Yanamandra, K., Ikezu, S., Gygi, S. P., & Ikezu, T. (2020) · Cells · doi:10.3390/cells9091959 · Cited by 157 · see citing works
Exosomes of BV-2 cells induced by alpha-synuclein: Important mediator of neurodegeneration in PD
Chang, C., Lang, H., Geng, N., Wang, J., Li, N., & Wang, X. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.06.009 · Cited by 156 · see citing works
Narbute, K., Piļipenko, V., Pupure, J., Dzirkale, Z., Jonavičė, U., Tunaitis, V., Kriaučiūnaitė, K., Jarmalavičiūtė, A., Jansone, B., Kluša, V., et al. (2019) · Stem Cells Translational Medicine · doi:10.1002/sctm.18-0162 · Cited by 150 · see citing works
P2RX7 inhibitor suppresses exosome secretion and disease phenotype in P301S tau transgenic mice
Ruan, Z., Delpech, J.-C., Venkatesan Kalavai, S., Van Enoo, A. A., Hu, J., Ikezu, S., & Ikezu, T. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00396-2 · Cited by 150 · see citing works
Proteomic analysis of urinary extracellular vesicles reveal biomarkers for neurologic disease
Wang, S., Kojima, K., Mobley, J. A., & West, A. B. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.06.021 · Cited by 145 · see citing works
Chaudhuri, A. D., Dastgheyb, R. M., Devine, L. R., Bi, H., Cole, R. N., & Haughey, N. J. (2019) · Glia · doi:10.1002/glia.23708 · Cited by 130 · see citing works
Zhang, F., Zhong, R., Li, S., Fu, Z., Cheng, C., Cai, H., & Le, W. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00282 · Cited by 125 · see citing works
Self-citationOhmichi, T., Mitsuhashi, M., Tatebe, H., Kasai, T., El‐Agnaf, O. M. A., & Tokuda, T. (2018) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2018.11.021 · Cited by 125 · see citing works
Biomarkers of neurodegenerative disorders: How good are they?
Rachakonda, V., Pan, T. H., & Le, W. D. (2004) · Cell Research · doi:10.1038/sj.cr.7290235 · Cited by 116 · see citing works
Self-citationSi, X., Tian, J., Chen, Y., Yan, Y., Pu, J., & Zhang, B. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.05.015 · Cited by 111 · see citing works
Circulating exosomal miRNAs as diagnostic biomarkers in Parkinson's disease.
Yf, Y., Mw, Q., Gc, L., Fb, Z., & Hc, R. (2018) · PubMed · doi:10.26355/eurrev_201808_15727 · Cited by 111 · see citing works
Chiarini, A., Armato, U., Gardenal, E., Gui, L., & Prà, I. D. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00217 · Cited by 102 · see citing works
Xu, L., Cao, H., Xie, Y., Zhang, Y., Du, M., Xu, X., Ye, R., & Liu, X. (2019) · Brain Research · doi:10.1016/j.brainres.2019.04.009 · Cited by 102 · see citing works
Wnt3a induces exosome secretion from primary cultured rat microglia
Hooper, C., Sáinz‐Fuertes, R., Lynham, S., Hye, A., Killick, R., Warley, A., Bolondi, C., Pocock, J. M., & Lovestone, S. (2012) · BMC Neuroscience · doi:10.1186/1471-2202-13-144 · Cited by 100 · see citing works
Fernandes, A., Ribeiro, A. R., Monteiro, M., Garcia, G., Vaz, A. R., & Brites, D. (2018) · Biochimie · doi:10.1016/j.biochi.2018.05.015 · Cited by 93 · see citing works
Chen, Y., Xia, K., Chen, L., & Fan, D. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00574 · Cited by 91 · see citing works
Therapeutic Advances of Stem Cell-Derived Extracellular Vesicles in Regenerative Medicine
Yin, L., Liu, X., Shi, Y., Ocansey, D. K. W., Hu, Y., Li, X., Zhang, C., Xu, W., & Qian, H. (2020) · Cells · doi:10.3390/cells9030707 · Cited by 90 · see citing works
Pei, X., Li, Y., Zhu, L., & Zhou, Z.-L. (2020) · Cell Cycle · doi:10.1080/15384101.2020.1731649 · Cited by 88 · see citing works
Vinuesa, Á., Bentivegna, M., Calfa, G. D., Filipello, F., Pomilio, C. J., Bonaventura, M. M., Lux-Lantos, V. A., Matzkin, M. E., Gregosa, A., Presa, J., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1435-8 · Cited by 84 · see citing works
Willis, C. M., Nicaise, A. M., Bongarzone, E. R., Givogri, M., Reiter, C. R., Heintz, O., Jellison, E. R., Sutter, P. A., TeHennepe, G., Ananda, G., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-57663-x · Cited by 76 · see citing works
Shakespear, N., Ogura, M., Yamaki, J., & Homma, Y. (2020) · Neurochemical Research · doi:10.1007/s11064-020-02977-5 · Cited by 72 · see citing works
Nikitidou, E., Khoonsari, P. E., Shevchenko, G., Ingelsson, M., Kultima, K., & Erlandsson, A. (2017) · Journal of Alzheimer's Disease · doi:10.3233/jad-170278 · Cited by 68 · see citing works
Mao, S., Sun, Q., Xiao, H., Zhang, C., & Li, L. (2015) · Protein & Cell · doi:10.1007/s13238-015-0168-y · Cited by 66 · see citing works
Isolation of microglia-derived extracellular vesicles: towards miRNA signatures and neuroprotection
Lemaire, Q., Raffo‐Romero, A., Arab, T., Camp, C. V., Drago, F., Forte, S., Gimeno, J., Bégard, S., Colin, M., Vizioli, J., et al. (2019) · Journal of Nanobiotechnology · doi:10.1186/s12951-019-0551-6 · Cited by 66 · see citing works
Microglia-Derived Microvesicles Affect Microglia Phenotype in Glioma
Grimaldi, A., Serpe, C., Chece, G., Nigro, V., Sarra, A., Ruzicka, B., Relucenti, M., Familiari, G., Ruocco, G., Pascucci, G. R., et al. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00041 · Cited by 65 · see citing works
Fan, R. Z., Guo, M. A., Luo, S., Cui, M., & Tieu, K. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0821-4 · Cited by 63 · see citing works
Luarte, A., Henzi, R., Fernández, A., Gaete, D., Cisternas, P., Pizarro, M., Bátiz, L. F., Villalobos, I., Masalleras, M., Vergara, R. C., et al. (2020) · Cells · doi:10.3390/cells9040930 · Cited by 63 · see citing works
Muraoka, S., Jedrychowski, M. P., Iwahara, N., Abdullah, M., Onos, K. D., Keezer, K. J., Hu, J., Ikezu, S., Howell, G. R., Gygi, S. P., et al. (2021) · Journal of Proteome Research · doi:10.1021/acs.jproteome.0c00934 · Cited by 61 · see citing works
Decoding distinctive features of plasma extracellular vesicles in amyotrophic lateral sclerosis
Pasetto, L., Callegaro, S., Corbelli, A., Fiordaliso, F., Ferrara, D., Brunelli, L., Sestito, G., Pastorelli, R., Bianchi, E., Cretich, M., et al. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00470-3 · Cited by 57 · see citing works
Extracellular Vesicles in Regenerative Medicine: Potentials and Challenges
Lee, J. Y., & Kim, H.-S. (2021) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-021-00365-w · Cited by 53 · see citing works
Adolf, A., Rohrbeck, A., Münster‐Wandowski, A., Johansson, M., Kuhn, H. G., Kopp, M. A., Brommer, B., Schwab, J. M., Just, I., Ahnert‐Hilger, G., et al. (2018) · Glia · doi:10.1002/glia.23566 · Cited by 44 · see citing works
Glia-derived extracellular vesicles in parkinson’s disease.
Marchetti, B., Leggio, L., L’Episcopo, F., Vivarelli, S., Tirolo, C., Paternò, G., Giachino, C., Caniglia, S., Serapide, M. F., & Iraci, N. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9061941 · Cited by 38 · see citing works
Extracellular vesicles in the oligodendrocyte microenvironment
Krämer‐Albers, E. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.134915 · Cited by 36 · see citing works
Dong, J., Liu, X., Wang, Y. Y., Cai, H., & Le, W. (2020) · Glia · doi:10.1002/glia.23826 · Cited by 22 · see citing works
Self-citationLi, N., Wu, Y., Zhu, L., Huang, Y. X. R., Liu, Z., Shi, M. Y., Soltys, D., Zhang, J., & Chang, Q. (2019) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2019.07.084 · Cited by 17 · see citing works
Clayton, K. A., Delpech, J.-C., Herron, S., Iwahara, N., Ericsson, M., Saito, T., Saido, T. C., Ikezu, S., & Ikezu, T. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00447-2 · Cited by 15 · see citing works
Biomarker Discovery in Parkinson’s Disease: Present Challenges and Future Opportunities
Li, S., & Le, W. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0184-4 · Cited by 15 · see citing works
Self-citationWolters, E. C., Strekalova, T. V., de Munter, J., & Kramer, B. W. W. (2021) · Ageing and Neurodegenerative Diseases · doi:10.20517/and.2021.04 · Cited by 6 · see citing works
Wang, Q., Song, S., Jiang, L., & Hon, J.-S. (2021) · Ageing and Neurodegenerative Diseases · doi:10.20517/and.2021.06 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Zhao, Y., Liu, B., Xu, L., Yu, S., Fu, J., Wang, J., Yan, X., & Su, J. (2021) · Antioxidants · doi:10.3390/antiox10121917 · Cited by 114 · see citing works
Recommendations for reproducibility of cerebrospinal fluid extracellular vesicle studies
Sandau, U. S., Magaña, S. M., Costa, J., Nolan, J. P., Ikezu, T., Vella, L. J., Jackson, H. K., Moreira, L. R., Palacio, P. L., Hill, A. F., et al. (2023) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12397 · Cited by 59 · see citing works
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Cabrera‐Pastor, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25137041 · Cited by 58 · see citing works
Brain incoming call from glia during neuroinflammation: Roles of extracellular vesicles
D’Egidio, F., Castelli, V., d’Angelo, M., Ammannito, F., Quintiliani, M., & Cimini, A. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106663 · Cited by 39 · see citing works
Sex-dependent factors of alcohol and neuroimmune mechanisms
Cruz, B., Borgonetti, V., Bajo, M., & Roberto, M. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100562 · Cited by 37 · see citing works
Mavroeidi, P., Vetsi, M., Dionysopoulou, D., & Xilouri, M. (2022) · Biomolecules · doi:10.3390/biom12070957 · Cited by 31 · see citing works
Sattarov, R., Havers, M., Orbjörn, C., Stomrud, E., Janelidze, S., Laurell, T., & Mattsson, N. (2024) · Scientific Reports · doi:10.1038/s41598-024-75406-0 · Cited by 27 · see citing works
Zhou, Q., Luo, J., Chai, X., Yang, J., Zhong, S., Zhang, Z., Chang, X., & Wang, H. (2025) · International Immunopharmacology · doi:10.1016/j.intimp.2025.114679 · Cited by 28 · see citing works
Extracellular vesicles as nanotheranostic platforms for targeted neurological disorder interventions
Choi, H. K., Chen, M., Goldston, L. L., & Lee, K.-B. (2024) · Nano Convergence · doi:10.1186/s40580-024-00426-5 · Cited by 26 · see citing works
Li, T., Tan, X., Tian, L., Jia, C., Cheng, C., Chen, X., Wei, M., Wang, Y., Hu, Y., Jia, Q., et al. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02956-x · Cited by 25 · see citing works
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Magni, G., Riboldi, B., & Ceruti, S. (2024) · Cells · doi:10.3390/cells13070606 · Cited by 25 · see citing works
Virtuoso, A., D’Amico, G., Scalia, F., Luca, C. D., Papa, M., Maugeri, G., D’Agata, V., Bavisotto, C. C., & D’Amico, A. G. (2024) · Brain Sciences · doi:10.3390/brainsci14040331 · Cited by 23 · see citing works
Neuron-derived extracellular vesicle-based diagnostics for Tau and Alzheimer’s disease
Chinnathambi, S., Kumarappan, M., Malik, S., Velmurugan, G., & Chandrashekar, M. (2025) · Brain Network Disorders · doi:10.1016/j.bnd.2024.12.006 · Cited by 21 · see citing works
From Neuron‐Centric to Glia‐Centric: How Aging Glial Networks Drive Neurodegenerative Disease
Hayashide, L. D. S., Pessoa, B., Dias, G. R., Pontes, B., Pinto, R. S., & Diniz, L. P. (2026) · Journal of Neurochemistry · doi:10.1111/jnc.70361 · Cited by 19 · see citing works
Glial Cells in the Early Stages of Neurodegeneration: Pathogenesis and Therapeutic Targets
Ahremenko, E. A., Andreev, A., Apushkin, D., & Korkotian, E. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262411995 · Cited by 16 · see citing works
Song, J.-J., Zhao, Y., Shan, X., Luo, Y., Hao, N., & Zhao, L. (2023) · Brain Research · doi:10.1016/j.brainres.2023.148603 · Cited by 13 · see citing works
Balbi, M., Bonanno, G., Bonifacino, T., & Milanese, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065240 · Cited by 14 · see citing works
Metabolic and inflammatory roles of glial cells in neurodegenerative and cerebrovascular diseases
OGUNLEYE, F. A., Zhou, Y., Yan, L., Abhulimen, P. O., Xu, Y., Lai, M. K. P., Okunowo, W. O., Sethi, G., Fang, C., & Ma, Y. (2026) · Ageing Research Reviews · doi:10.1016/j.arr.2026.103120 · Cited by 10 · see citing works
Tunset, M. E., Haslene‐Hox, H., Bossche, T. V. D., Maleki, S., Vaaler, A., & Kondziella, D. (2023) · Nordic Journal of Psychiatry · doi:10.1080/08039488.2023.2223572 · Cited by 9 · see citing works
Gao, S., Bai, L., Jia, S., & Meng, C. (2022) · Genes · doi:10.3390/genes13091603 · Cited by 9 · see citing works
Negah, S. S., Moradi, H. R., Forouzanfar, F., Sahraian, M. A., & Faraji, M. (2025) · Neurochemical Research · doi:10.1007/s11064-025-04344-8 · Cited by 8 · see citing works
Emerging Roles of Neuronal Extracellular Vesicles at the Synapse
Mason, A. J., Deppmann, C. D., & Winckler, B. (2023) · The Neuroscientist · doi:10.1177/10738584231160521 · Cited by 7 · see citing works
Forró, T., Manu, D. R., Barbu–Tudoran, L., & Bălașa, R. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252212471 · Cited by 6 · see citing works
Exosomes in epilepsy: bridging neuroinflammation, diagnosis, and therapeutic delivery
Li, B., Zhu, Y., Chen, L., Cui, J., & Zhang, Z. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1667122 · Cited by 5 · see citing works
Kajitani, G. S., Xavier, G., Villena-Rueda, B. E., Karia, B. T. R., & Santoro, M. L. (2024) · Current topics in membranes · doi:10.1016/bs.ctm.2024.06.002 · Cited by 4 · see citing works
Dual role of extracellular vesicles in neurodegenerative diseases
Scuteri, A., & Donzelli, E. (2024) · World Journal of Stem Cells · doi:10.4252/wjsc.v16.i12.1002 · Cited by 4 · see citing works
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Barathan, M., & Abdullah, N. A. H. (2025) · Biology · doi:10.3390/biology14101349 · Cited by 2 · see citing works
Reyes-Ábalos, A. L., Álvarez-Zabaleta, M., Olivera‐Bravo, S., & Tomaso, M. V. D. (2024) · International Journal of Cell Biology · doi:10.1155/2024/5524487 · Cited by 1 · see citing works
Song, J.-J., Zhao, Y., Shan, X., Luo, Y., Hao, N., & Zhao, L. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4523046
Role of extracellular vesicles in neurodegenerative diseases
Pahwa, H., Mukherjee, A. G., Gopalakrishnan, A. V., Vyas, N., Pandey, V., & Wanjari, U. R. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-23891-8.00016-0
Li, T., Tan, X., Tian, L., Jia, C., Cheng, C., Chen, X., Wei, M., Wang, Y., Hu, Y., Jia, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24603498
Self-citationMirzaahmadi, B., Shafaie, H., Mahmoodi, J., Haddadi, P., Hassanzadeh, A., Reiter, R. J., Fazli, F., Karimipour, M., & Rahbarghazi, R. (2026) · Journal of Translational Medicine · doi:10.1186/s12967-026-07709-x
Lekshmi, S. S. A., Palathingal, M., Manikkath, J., Sarath Chandran, C., & Nampoothiri, M. (2026) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2026.109009
- Authors
- Li, T., Tan, X., Li, S., Al-Nusaif, M., & Le, W.
- Affiliations
- Dalian Medical University (CN)
- Corresponding author
- Le, Weidong
- Venue
- Frontiers in Aging Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2021-10-20
- Volume
- 13
- Pages
- 765395-765395
- ISSN
- 1663-4365 (ISSN-L)
- PMC
- PMC8563578
- OpenAlex
- W3205360394
- Cited by
- 33
- References
- 109
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 10 · 2023: 9 · 2022: 2 · 2021: 1
- FWCI
- 0.58
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Aging Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (81771521, 82001483)
- National Key Research and Development Program of China (2016YFC1306600)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- neurodegenerative diseases, Alzheimer's disease, Parkinson's disease, amyotrophic lateral sclerosis, neuroinflammation, neuron-glia crosstalk, cell-to-cell communication, pathogenesis, diagnosis and treatment
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