Volume 41 Issue 4
Jul.  2020
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Xiao-Hui Li, Juan Zhang, Ding-Feng Li, Wei Wu, Zhong-Wen Xie, Qiang Liu. Physiological and pathological insights into exosomes in the brain. Zoological Research, 2020, 41(4): 365-372. doi: 10.24272/j.issn.2095-8137.2020.043
Citation: Xiao-Hui Li, Juan Zhang, Ding-Feng Li, Wei Wu, Zhong-Wen Xie, Qiang Liu. Physiological and pathological insights into exosomes in the brain. Zoological Research, 2020, 41(4): 365-372. doi: 10.24272/j.issn.2095-8137.2020.043

Physiological and pathological insights into exosomes in the brain

doi: 10.24272/j.issn.2095-8137.2020.043
Funds:  This research was supported by the National Natural Science Foundation of China (31871082, 91849101, 81601221), The Strategic Priority Research Program of the Chinese Academy of Sciences (XDB39000000), Key Research Program of Frontier Sciences of CAS (QYZDB-SSW-SMC035), the Innovative Program of Development Foundation of Hefei Center for Physical Science and Technology (2018CXFX005), the Fundamental Research Funds for the Central Universities, and China Postdoctoral Science Foundation (2019M662178). The Open Fund of State Key Laboratory of Tea Plant Biology and Utilization (SKLTOF20150101)
More Information
  • Exosomes are small vesicles secreted by all cell types in the brain and play a role in cell-cell communication through the transfer of cargo or encapsulation. Exosomes in the brain have considerable impact on neuronal development, activation, and regeneration. In addition, exosomes are reported to be involved in the onset and propagation of various neurodegenerative diseases. In this review, we discuss the content of exosomes derived from major cell types in the brain, and their function under physiological and pathological conditions.

  • #Authors contributed equally to this work
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  • [1]
    Abels ER, Breakefield XO. 2016. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cellular and Molecular Neurobiology, 36(3): 301−312. doi:  10.1007/s10571-016-0366-z
    [2]
    Alvarez-Erviti L, Seow Y, Yin HF, Betts C, Lakhal S, Wood MJA. 2011. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nature Biotechnology, 29(4): 341−345. doi:  10.1038/nbt.1807
    [3]
    Antonucci F, Turola E, Riganti L, Caleo M, Gabrielli M, Perrotta C, Novellino L, Clementi E, Giussani P, Viani P, Matteoli M, Verderio C. 2012. Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. The EMBO Journal, 31(5): 1231−1240. doi:  10.1038/emboj.2011.489
    [4]
    Bahrini I, Song JH, Diez D, Hanayama R. 2015. Neuronal exosomes facilitate synaptic pruning by up-regulating complement factors in microglia. Scientific Reports, 5: 7989. doi:  10.1038/srep07989
    [5]
    Bakhti M, Winter C, Simons M. 2011. Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles. Journal of Biological Chemistry, 286(1): 787−796. doi:  10.1074/jbc.M110.190009
    [6]
    Bianco F, Perrotta C, Novellino L, Francolini M, Riganti L, Menna E, Saglietti L, Schuchman EH, Furlan R, Clementi E, Matteoli M, Verderio C. 2009. Acid sphingomyelinase activity triggers microparticle release from glial cells. The EMBO Journal, 28(8): 1043−1054. doi:  10.1038/emboj.2009.45
    [7]
    Caruso Bavisotto C, Scalia F, Marino Gammazza A, Carlisi D, Bucchieri F, Conway de Macario E, Macario AJL, Cappello F, Campanella C. 2019. Extracellular vesicle-mediated cell-cell communication in the nervous system: focus on neurological diseases. International Journal of Molecular Sciences, 20(2): 434. doi:  10.3390/ijms20020434
    [8]
    Chang CW, Lang HJ, Geng N, Wang J, Li N, Wang XL. 2013. Exosomes of BV-2 cells induced by alpha-synuclein: important mediator of neurodegeneration in PD. Neuroscience Letters, 548: 190−195. doi:  10.1016/j.neulet.2013.06.009
    [9]
    Chaudhuri AD, Dastgheyb RM, Yoo SW, Trout A, Talbot CC Jr, Hao HP, Witwer KW, Haughey NJ. 2018. TNFα and il-1β modify the miRNA cargo of astrocyte shed extracellular vesicles to regulate neurotrophic signaling in neurons. Cell Death & Disease, 9(3): 363.
    [10]
    Chivet M, Javalet C, Laulagnier K, Blot B, Hemming FJ, Sadoul R. 2014. Exosomes secreted by cortical neurons upon glutamatergic synapse activation specifically interact with neurons. Journal of Extracellular Vesicles, 3(1): 24722. doi:  10.3402/jev.v3.24722
    [11]
    Cocucci E, Meldolesi J. 2015. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends in Cell Biology, 25(6): 364−372. doi:  10.1016/j.tcb.2015.01.004
    [12]
    Colombo M, Raposo G, Théry C. 2014. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annual Review of Cell and Developmental Biology, 30: 255−289. doi:  10.1146/annurev-cellbio-101512-122326
    [13]
    Cummings JL. 2004. Alzheimer's disease. The New England Journal of Medicine, 351(1): 56−67. doi:  10.1056/NEJMra040223
    [14]
    Dinkins MB, Dasgupta S, Wang GH, Zhu G, Bieberich E. 2014. Exosome reduction in vivo is associated with lower amyloid plaque load in the 5XFAD mouse model of Alzheimer's disease. Neurobiology of Aging, 35(8): 1792−1800. doi:  10.1016/j.neurobiolaging.2014.02.012
    [15]
    Dinkins MB, Enasko J, Hernandez C, Wang GH, Kong JN, Helwa I, Liu YT, Terry AV Jr, Bieberich E. 2016. Neutral sphingomyelinase-2 deficiency ameliorates Alzheimer's disease pathology and improves cognition in the 5XFAD mouse. Journal of Neuroscience, 36(33): 8653−8667. doi:  10.1523/JNEUROSCI.1429-16.2016
    [16]
    Emmanouilidou E, Melachroinou K, Roumeliotis T, Garbis SD, Ntzouni M, Margaritis LH, Stefanis L, Vekrellis K. 2010. Cell-produced α-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. Journal of Neuroscience, 30(20): 6838−6851. doi:  10.1523/JNEUROSCI.5699-09.2010
    [17]
    Fauré J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, Blot B, Grange J, Schoehn G, Goldberg Y, Boyer V, Kirchhoff F, Raposo G, Garin J, Sadoul R. 2006. Exosomes are released by cultured cortical neurones. Molecular and Cellular Neuroscience, 31(4): 642−648. doi:  10.1016/j.mcn.2005.12.003
    [18]
    Feiler MS, Strobel B, Freischmidt A, Helferich AM, Kappel J, Brewer BM, Li DY, Thal DR, Walther P, Ludolph AC, Danzer KM, Weishaupt JH. 2015. TDP-43 is intercellularly transmitted across axon terminals. Journal of Cell Biology, 211(4): 897−911. doi:  10.1083/jcb.201504057
    [19]
    Fitzner D, Schnaars M, van Rossum D, Krishnamoorthy G, Dibaj P, Bakhti M, Regen T, Hanisch UK, Simons M. 2011. Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. Journal of Cell Science, 124: 447−458. doi:  10.1242/jcs.074088
    [20]
    Fröhlich D, Kuo WP, Frühbeis C, Sun JJ, Zehendner CM, Luhmann HJ, Pinto S, Toedling J, Trotter J, Krämer-Albers EM. 2014. Multifaceted effects of oligodendroglial exosomes on neurons: impact on neuronal firing rate, signal transduction and gene regulation. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1652): 20130510. doi:  10.1098/rstb.2013.0510
    [21]
    Frühbeis C, Fröhlich D, Kuo WP, Amphornrat J, Thilemann S, Saab AS, Kirchhoff F, Möbius W, Goebbels S, Nave KA, Schneider A, Simons M, Klugmann M, Trotter J, Krämer-Albers EM. 2013a. Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biology, 11(7): e1001604. doi:  10.1371/journal.pbio.1001604
    [22]
    Frühbeis C, Fröhlich D, Kuo WP, Krämer-Albers EM. 2013b. Extracellular vesicles as mediators of neuron-glia communication. Frontiers in Cellular Neuroscience, 7: 182.
    [23]
    Gabrielli M, Battista N, Riganti L, Prada I, Antonucci F, Cantone L, Matteoli M, Maccarrone M, Verderio C. 2015. Active endocannabinoids are secreted on extracellular membrane vesicles. EMBO Reports, 16(2): 213−220. doi:  10.15252/embr.201439668
    [24]
    Goetzl EJ, Kapogiannis D, Schwartz JB, Lobach IV, Goetzl L, Abner EL, Jicha GA, Karydas AM, Boxer A, Miller BL. 2016. Decreased synaptic proteins in neuronal exosomes of frontotemporal dementia and Alzheimer's disease. The FASEB Journal, 30(12): 4141−4148. doi:  10.1096/fj.201600816R
    [25]
    Goldie BJ, Dun MD, Lin MJ, Smith ND, Verrills NM, Dayas CV, Cairns MJ. 2014. Activity-associated miRNA are packaged in map1b-enriched exosomes released from depolarized neurons. Nucleic Acids Research, 42(14): 9195−9208. doi:  10.1093/nar/gku594
    [26]
    Gong JY, Körner R, Gaitanos L, Klein R. 2016. Exosomes mediate cell contact-independent ephrin-Eph signaling during axon guidance. Journal of Cell Biology, 214(1): 35−44. doi:  10.1083/jcb.201601085
    [27]
    Gross JC, Chaudhary V, Bartscherer K, Boutros M. 2012. Active Wnt proteins are secreted on exosomes. Nature Cell Biology, 14(10): 1036−1045. doi:  10.1038/ncb2574
    [28]
    Henderson MX, Cornblath EJ, Darwich A, Zhang B, Brown H, Gathagan RJ, Sandler RM, Bassett DS, Trojanowski JQ, Lee VMY. 2019. Spread of α-synuclein pathology through the brain connectome is modulated by selective vulnerability and predicted by network analysis. Nature Neuroscience, 22(8): 1248−1257. doi:  10.1038/s41593-019-0457-5
    [29]
    Hong Y, Zhao T, Li XJ, Li SH. 2017. Mutant huntingtin inhibits αB-crystallin expression and impairs exosome secretion from astrocytes. Journal of Neuroscience, 37(39): 9550−9563. doi:  10.1523/JNEUROSCI.1418-17.2017
    [30]
    Hu G, Yao H, Chaudhuri AD, Duan M, Yelamanchili SV, Wen H, Cheney PD, Fox HS, Buch S. 2012. Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death & Disease, 3(8): e381.
    [31]
    Huang S, Ge XT, Yu JW, Han ZL, Yin ZY, Li Y, Chen FL, Wang HC, Zhang JN, Lei P. 2018. Increased miR-124-3p in microglial exosomes following traumatic brain injury inhibits neuronal inflammation and contributes to neurite outgrowth via their transfer into neurons. The FASEB Journal, 32(1): 512−528. doi:  10.1096/fj.201700673r
    [32]
    Iguchi Y, Eid L, Parent M, Soucy G, Bareil C, Riku Y, Kawai K, Takagi S, Yoshida M, Katsuno M, Sobue G, Julien JP. 2016. Exosome secretion is a key pathway for clearance of pathological TDP-43. Brain, 139(12): 3187−3201. doi:  10.1093/brain/aww237
    [33]
    Jeon I, Cicchetti F, Cisbani G, Lee S, Li ED, Bae J, Lee N, Li L, Im W, Kim M, Kim HS, Oh SH, Kim TA, Ko JJ, Aubé B, Oueslati A, Kim YJ, Song J. 2016. Human-to-mouse prion-like propagation of mutant huntingtin protein. Acta Neuropathologica, 132(4): 577−592. doi:  10.1007/s00401-016-1582-9
    [34]
    Jia LF, Qiu QQ, Zhang H, Chu L, Du YF, Zhang JW, Zhou CK, Liang FR, Shi SL, Wang S, Qin W, Wang Q, Li FY, Wang QG, Li Y, Shen LX, Wei YP, Jia JP. 2019. Concordance between the assessment of Aβ42, T-tau, and P-T181-tau in peripheral blood neuronal-derived exosomes and cerebrospinal fluid. Alzheimer’s & Dementia, 15(8): 1071−1080.
    [35]
    Kalia LV, Lang AE. 2015. Parkinson's disease. The Lancet, 386(9996): 896−912. doi:  10.1016/S0140-6736(14)61393-3
    [36]
    Kamelgarn M, Chen J, Kuang LS, Arenas A, Zhai JJ, Zhu HN, Gal J. 2016. Proteomic analysis of FUS interacting proteins provides insights into FUS function and its role in ALS. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1862(10): 2004−2014. doi:  10.1016/j.bbadis.2016.07.015
    [37]
    Katsuda T, Tsuchiya R, Kosaka N, Yoshioka Y, Takagaki K, Oki K, Takeshita F, Sakai Y, Kuroda M, Ochiya T. 2013. Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes. Scientific Reports, 3: 1197. doi:  10.1038/srep01197
    [38]
    Klein R, Kania A. 2014. Ephrin signalling in the developing nervous system. Current Opinion in Neurobiology, 27: 16−24. doi:  10.1016/j.conb.2014.02.006
    [39]
    Korkut C, Ataman B, Ramachandran P, Ashley J, Barria R, Gherbesi N, Budnik V. 2009. Trans-synaptic transmission of vesicular Wnt signals through Evi/Wntless. Cell, 139(2): 393−404. doi:  10.1016/j.cell.2009.07.051
    [40]
    Korkut C, Li YH, Koles K, Brewer C, Ashley J, Yoshihara M, Budnik V. 2013. Regulation of postsynaptic retrograde signaling by presynaptic exosome release. Neuron, 77(6): 1039−1046. doi:  10.1016/j.neuron.2013.01.013
    [41]
    Krämer-Albers EM, Bretz N, Tenzer S, Winterstein C, Möbius W, Berger H, Nave KA, Schild H, Trotter J. 2007. Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons?. Proteomics: Clinical Applications, 1(11): 1446−1461. doi:  10.1002/prca.200700522
    [42]
    Kumar A, Stoica BA, Loane DJ, Yang M, Abulwerdi G, Khan N, Kumar A, Thom SR, Faden AI. 2017. Microglial-derived microparticles mediate neuroinflammation after traumatic brain injury. Journal of Neuroinflammation, 14(1): 47. doi:  10.1186/s12974-017-0819-4
    [43]
    Lachenal G, Pernet-Gallay K, Chivet M, Hemming FJ, Belly A, Bodon G, Blot B, Haase G, Goldberg Y, Sadoul R. 2011. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Molecular and Cellular Neuroscience, 46(2): 409−418. doi:  10.1016/j.mcn.2010.11.004
    [44]
    Lee M, Liu T, Im W, Kim M. 2016. Exosomes from adipose-derived stem cells ameliorate phenotype of Huntington's disease in vitro model. European Journal of Neuroscience, 44(4): 2114−2119. doi:  10.1111/ejn.13275
    [45]
    Lee SJ, Desplats P, Lee HJ, Spencer B, Masliah E. 2012. Cell-to-cell transmission of α-synuclein aggregates. In: Sigurdsson EM, Calero M, Gasset M. Amyloid Proteins: Methods and Protocols. USA: Humana Press, 347–359.
    [46]
    Mackenzie IRA, Rademakers R, Neumann M. 2010. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. The Lancet Neurology, 9(10): 995−1007. doi:  10.1016/S1474-4422(10)70195-2
    [47]
    Mao SS, Sun Q, Xiao H, Zhang CY, Li L. 2015. Secreted miR-34a in astrocytic shedding vesicles enhanced the vulnerability of dopaminergic neurons to neurotoxins by targeting Bcl-2. Protein & Cell, 6(7): 529−540.
    [48]
    Men YQ, Yelick J, Jin SJ, Tian Y, Chiang MSR, Higashimori H, Brown E, Jarvis R, Yang YJ. 2019. Exosome reporter mice reveal the involvement of exosomes in mediating neuron to astroglia communication in the CNS. Nature Communications, 10(1): 4136. doi:  10.1038/s41467-019-11534-w
    [49]
    Morel L, Regan M, Higashimori H, Ng SK, Esau C, Vidensky S, Rothstein J, Yang YJ. 2013. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. Journal of Biological Chemistry, 288(10): 7105−7116. doi:  10.1074/jbc.M112.410944
    [50]
    Mustapic M, Eitan E, Werner JK Jr, Berkowitz ST, Lazaropoulos MP, Tran J, Goetzl EJ, Kapogiannis D. 2017. Plasma extracellular vesicles enriched for neuronal origin: a potential window into brain pathologic processes. Frontiers in Neuroscience, 11: 278. doi:  10.3389/fnins.2017.00278
    [51]
    Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, McCluskey LF, Miller BL, Masliah E, Mackenzie IR, Feldman H, Feiden W, Kretzschmar HA, Trojanowski JQ, Lee VMY. 2006. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 314(5796): 130−133. doi:  10.1126/science.1134108
    [52]
    Nixon RA. 2005. Endosome function and dysfunction in Alzheimer's disease and other neurodegenerative diseases. Neurobiology of Aging, 26(3): 373−382. doi:  10.1016/j.neurobiolaging.2004.09.018
    [53]
    Pascua-Maestro R, Gonzalez E, Lillo C, Ganfornina MD, Falcón-Pérez JM, Sanchez D. 2018. Extracellular vesicles secreted by astroglial cells transport apolipoprotein D to neurons and mediate neuronal survival upon oxidative stress. Frontiers in Cellular Neuroscience, 12: 526. doi:  10.3389/fnins.2018.00526
    [54]
    Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV, McCormick J, Yoder N, Belnap DM, Erlendsson S, Morado DR, Briggs JAG, Feschotte C, Shepherd JD. 2018. The neuronal gene Arc encodes a repurposed retrotransposon gag protein that mediates intercellular RNA transfer. Cell, 173(1-2): 275−288.
    [55]
    Peng KY, Pérez-González R, Alldred MJ, Goulbourne CN, Morales-Corraliza J, Saito M, Saito M, Ginsberg SD, Mathews PM, Levy E. 2019. Apolipoprotein E4 genotype compromises brain exosome production. Brain, 142(1): 163−175. doi:  10.1093/brain/awy289
    [56]
    Perez-Gonzalez R, Gauthier SA, Kumar A, Levy E. 2012. The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. Journal of Biological Chemistry, 287(51): 43108−43115. doi:  10.1074/jbc.M112.404467
    [57]
    Polanco JC, Scicluna BJ, Hill AF, Götz J. 2016. Extracellular vesicles isolated from the brains of rtg4510 mice seed tau protein aggregation in a threshold-dependent manner. Journal of Biological Chemistry, 291(24): 12445−12466. doi:  10.1074/jbc.M115.709485
    [58]
    Potolicchio I, Carven GJ, Xu XN, Stipp C, Riese RJ, Stern LJ, Santambrogio L. 2005. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. The Journal of Immunology, 175(4): 2237−2243. doi:  10.4049/jimmunol.175.4.2237
    [59]
    Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, Verkade P, Simons K. 2006. Alzheimer's disease β-amyloid peptides are released in association with exosomes. Proceedings of the National Academy of Sciences of the United States of America, 103(30): 11172−11177. doi:  10.1073/pnas.0603838103
    [60]
    Russo I, Bubacco L, Greggio E. 2012. Exosomes-associated neurodegeneration and progression of Parkinson's disease. American Journal of Neurodegenerative Disease, 1(3): 217−225.
    [61]
    Saman S, Kim WH, Raya M, Visnick Y, Miro S, Saman S, Jackson B, McKee AC, Alvarez VE, Lee NCY, Hall GF. 2012. Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early alzheimer disease. Journal of Biological Chemistry, 287(6): 3842−3849. doi:  10.1074/jbc.M111.277061
    [62]
    Scotter EL, Chen HJ, Shaw CE. 2015. TDP-43 proteinopathy and ALS: insights into disease mechanisms and therapeutic targets. Neurotherapeutics, 12(2): 352−363. doi:  10.1007/s13311-015-0338-x
    [63]
    Sharma P, Mesci P, Carromeu C, McClatchy DR, Schiapparelli L, Yates III JR, Muotri AR, Cline HT. 2019. Exosomes regulate neurogenesis and circuit assembly. Proceedings of the National Academy of Sciences of the United States of America, 116(32): 16086−16094. doi:  10.1073/pnas.1902513116
    [64]
    Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M, Milligan CE. 2007. Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases. Developmental Neurobiology, 67(13): 1815−1829. doi:  10.1002/dneu.20559
    [65]
    Théry C, Zitvogel L, Amigorena S. 2002. Exosomes: composition, biogenesis and function. Nature Reviews Immunology, 2(8): 569−579. doi:  10.1038/nri855
    [66]
    Théry C. 2011. Exosomes: secreted vesicles and intercellular communications. F1000 Biology Reports, 3: 15.
    [67]
    Tkach M, Théry C. 2016. Communication by extracellular vesicles: where we are and where we need to go. Cell, 164(6): 1226−1232. doi:  10.1016/j.cell.2016.01.043
    [68]
    Tomlinson PR, Zheng Y, Fischer R, Heidasch R, Gardiner C, Evetts S, Hu M, Wade-Martins R, Turner MR, Morris J, Talbot K, Kessler BM, Tofaris GK. 2015. Identification of distinct circulating exosomes in Parkinson's disease. Annals of Clinical and Translational Neurology, 2(4): 353−361. doi:  10.1002/acn3.175
    [69]
    Vella LJ, Sharples RA, Nisbet RM, Cappai R, Hill AF. 2008. The role of exosomes in the processing of proteins associated with neurodegenerative diseases. European Biophysics Journal, 37(3): 323−332. doi:  10.1007/s00249-007-0246-z
    [70]
    Verkhratsky A, Matteoli M, Parpura V, Mothet JP, Zorec R. 2016. Astrocytes as secretory cells of the central nervous system: idiosyncrasies of vesicular secretion. The EMBO Journal, 35(3): 239−257. doi:  10.15252/embj.201592705
    [71]
    Vingtdeux V, Hamdane M, Loyens A, Gelé P, Drobeck H, Bégard S, Galas MC, Delacourte A, Beauvillain JC, Buée L, Sergeant N. 2007. Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. Journal of Biological Chemistry, 282(25): 18197−18205. doi:  10.1074/jbc.M609475200
    [72]
    Wang GH, Dinkins M, He Q, Zhu G, Poirier C, Campbell A, Mayer-Proschel M, Bieberich E. 2012. Astrocytes secrete exosomes enriched with proapoptotic ceramide and prostate apoptosis response 4 (PAR-4): potential mechanism of apoptosis induction in alzheimer disease (AD). Journal of Biological Chemistry, 287(25): 21384−21395. doi:  10.1074/jbc.M112.340513
    [73]
    Wang SW, Cesca F, Loers G, Schweizer M, Buck F, Benfenati F, Schachner M, Kleene R. 2011. Synapsin I is an oligomannose-carrying glycoprotein, acts as an oligomannose-binding lectin, and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes. Journal of Neuroscience, 31(20): 7275−7290. doi:  10.1523/JNEUROSCI.6476-10.2011
    [74]
    Westergard T, Jensen BK, Wen XM, Cai JL, Kropf E, Iacovitti L, Pasinelli P, Trotti D. 2016. Cell-to-cell transmission of dipeptide repeat proteins linked to c9orf72-ALS/FTD. Cell Reports, 17(3): 645−652. doi:  10.1016/j.celrep.2016.09.032
    [75]
    Yuyama K, Sun H, Mitsutake S, Igarashi Y. 2012. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia. Journal of Biological Chemistry, 287(14): 10977−10989. doi:  10.1074/jbc.M111.324616
    [76]
    Yuyama K, Sun H, Sakai S, Mitsutake S, Okada M, Tahara H, Furukawa JI, Fujitani N, Shinohara Y, Igarashi Y. 2014. Decreased amyloid-β pathologies by intracerebral loading of glycosphingolipid-enriched exosomes in alzheimer model mice. Journal of Biological Chemistry, 289(35): 24488−24498. doi:  10.1074/jbc.M114.577213
    [77]
    Yuyama K, Yamamoto N, Yanagisawa K. 2008. Accelerated release of exosome-associated GM1 ganglioside (GM1) by endocytic pathway abnormality: another putative pathway for GM1-induced amyloid fibril formation. Journal of Neurochemistry, 105(1): 217−224. doi:  10.1111/j.1471-4159.2007.05128.x
    [78]
    Zappulli V, Friis KP, Fitzpatrick Z, Maguire CA, Breakefield XO. 2016. Extracellular vesicles and intercellular communication within the nervous system. Journal of Clinical Investigation, 126(4): 1198−1207. doi:  10.1172/JCI81134
    [79]
    Zhang DF, Xu M, Bi R, Yao YG. 2019. Genetic analyses of Alzheimer's disease in china: achievements and perspectives. ACS Chemical Neuroscience, 10(2): 890−901. doi:  10.1021/acschemneuro.8b00435
    [80]
    Zhang J, Liu Q. 2015. Cholesterol metabolism and homeostasis in the brain. Protein & Cell, 6(4): 254−264.
    [81]
    Zhang X, Abels ER, Redzic JS, Margulis J, Finkbeiner S, Breakefield XO. 2016. Potential transfer of polyglutamine and CAG-repeat RNA in extracellular vesicles in Huntington's disease: background and evaluation in cell culture. Cellular and Molecular Neurobiology, 36(3): 459−470. doi:  10.1007/s10571-016-0350-7
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