Extracellular vesicles in neurodegenerative diseases: Insights and new perspectives

Grey, 2015, Acceleration of alpha-synuclein aggregation by exosomes, J Biol Chem, 290, 2969, 10.1074/jbc.M114.585703 Silverman, 2019, CNS-derived extracellular vesicles from superoxide dismutase 1 (SOD1)(G93A) ALS mice originate from astrocytes and neurons and carry misfolded SOD1, J Biol Chem, 294, 3744, 10.1074/jbc.RA118.004825 You, 2019, Emerging roles of extracellular vesicles in neurodegenerative disorders, Neurobiol Dis, 130, e104512, 10.1016/j.nbd.2019.104512 Rufino-Ramos, 2017, Extracellular vesicles: novel promising delivery systems for therapy of brain diseases, J Control Release, 262, 247, 10.1016/j.jconrel.2017.07.001 Liew, 2017, Mesenchymal stem cell-derived extracellular vesicles: a glimmer of hope in treating Alzheimer's disease, Int Immunol, 29, 11, 10.1093/intimm/dxx002 Szatanek, 2017, The methods of choice for extracellular vesicles (EVs) characterization, Int J Mol Sci, 18, e1153, 10.3390/ijms18061153 Mathieu, 2019, Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication, Nat Cell Biol, 21, 9, 10.1038/s41556-018-0250-9 Das, 2019, The extracellular RNA communication consortium: establishing foundational knowledge and technologies for extracellular RNA research, Cell, 177, 231, 10.1016/j.cell.2019.03.023 Srinivasan, 2019, Small RNA sequencing across diverse biofluids identifies optimal methods for exRNA isolation, Cell, 177, 446, 10.1016/j.cell.2019.03.024 Thery, 2018, Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines, J Extracell Vesicles, 7, e1535750, 10.1080/20013078.2018.1535750 van Niel, 2018, Shedding light on the cell biology of extracellular vesicles, Nat Rev Mol Cell Biol, 19, 213, 10.1038/nrm.2017.125 Chaput, 2011, Exosomes: immune properties and potential clinical implementations, Semin Immunopathol, 33, 419, 10.1007/s00281-010-0233-9 Bobrie, 2011, Exosome secretion: molecular mechanisms and roles in immune responses, Traffic, 12, 1659, 10.1111/j.1600-0854.2011.01225.x Thery, 2009, Membrane vesicles as conveyors of immune responses, Nat Rev Immunol, 9, 581, 10.1038/nri2567 Ratajczak, 2012, Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies?, Leukemia, 26, 1166, 10.1038/leu.2011.389 Colombo, 2014, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles, Annu Rev Cell Dev Biol, 30, 255, 10.1146/annurev-cellbio-101512-122326 Iranifar, 2019, Exosomes and microRNAs: new potential therapeutic candidates in Alzheimer disease therapy, J Cell Physiol, 234, 2296, 10.1002/jcp.27214 Wu, 2017, Exosomes in Parkinson's disease, Neurosci Bull, 33, 331, 10.1007/s12264-016-0092-z Skog, 2008, Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers, Nat Cell Biol, 10, 1470, 10.1038/ncb1800 Alvarez-Erviti, 2011, Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes, Nat Biotechnol, 29, 341, 10.1038/nbt.1807 Wang, 2019, Curcumin-primed exosomes potently ameliorate cognitive function in AD mice by inhibiting hyperphosphorylation of the Tau protein through the AKT/GSK-3beta pathway, Nanoscale, 11, 7481, 10.1039/C9NR01255A Mrowczynski, 2019, Exosomes and their implications in central nervous system tumor biology, Prog Neurobiol, 172, 71, 10.1016/j.pneurobio.2018.06.006 Holm, 2018, Extracellular vesicles: multimodal envoys in neural maintenance and repair, Trends Neurosci, 41, 360, 10.1016/j.tins.2018.03.006 Prada, 2018, Glia-to-neuron transfer of miRNAs via extracellular vesicles: a new mechanism underlying inflammation-induced synaptic alterations, Acta Neuropathol, 135, 529, 10.1007/s00401-017-1803-x Fruhbeis, 2013, Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication, PLoS Biol, 11, 10.1371/journal.pbio.1001604 Frohlich, 2014, Multifaceted effects of oligodendroglial exosomes on neurons: impact on neuronal firing rate, signal transduction and gene regulation, Philos Trans R Soc Lond B Biol Sci, 369, 10.1098/rstb.2013.0510 Xu, 2017, Neurons secrete miR-132-containing exosomes to regulate brain vascular integrity, Cell Res, 27, 882, 10.1038/cr.2017.62 Perez-Gonzalez, 2019, Neuroprotection mediated by cystatin C-loaded extracellular vesicles, Sci Rep, 9, e11104, 10.1038/s41598-019-47524-7 Trotta, 2018, Microglia-derived extracellular vesicles in Alzheimer's Disease: a double-edged sword, Biochem Pharmacol, 148, 184, 10.1016/j.bcp.2017.12.020 Antonucci, 2012, Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism, EMBO J, 31, 1231, 10.1038/emboj.2011.489 Gabrielli, 2015, Active endocannabinoids are secreted on extracellular membrane vesicles, EMBO Rep, 16, 213, 10.15252/embr.201439668 Riganti, 2016, Sphingosine-1-Phosphate (S1P) impacts presynaptic functions by regulating synapsin I localization in the presynaptic compartment, J Neurosci, 36, 4624, 10.1523/JNEUROSCI.3588-15.2016 Yuyama, 2017, Exosomes as carriers of Alzheimer's amyloid-ss, Front Neurosci, 11, e229, 10.3389/fnins.2017.00229 Quek, 2017, The role of extracellular vesicles in neurodegenerative diseases, Biochem Biophys Res Commun, 483, 1178, 10.1016/j.bbrc.2016.09.090 Zheng, 2017, Plasma exosomes spread and cluster Around beta-amyloid plaques in an animal model of Alzheimer's disease, Front Aging Neurosci, 9, e12, 10.3389/fnagi.2017.00012 Asai, 2015, Depletion of microglia and inhibition of exosome synthesis halt tau propagation, Nat Neurosci, 18, 1584, 10.1038/nn.4132 Wang, 2012, Astrocytes secrete exosomes enriched with proapoptotic ceramide and prostate apoptosis response 4 (PAR-4): potential mechanism of apoptosis induction in Alzheimer disease (AD), J Biol Chem, 287, 21384, 10.1074/jbc.M112.340513 Eitan, 2016, Extracellular vesicle-associated abeta mediates trans-neuronal bioenergetic and Ca(2+)-handling deficits in Alzheimer's disease models, NPJ Aging Mech Dis, 2, 10.1038/npjamd.2016.19 Yuyama, 2015, A potential function for neuronal exosomes: sequestering intracerebral amyloid-beta peptide, FEBS Lett, 589, 84, 10.1016/j.febslet.2014.11.027 Ghidoni, 2011, Cystatin C is released in association with exosomes: a new tool of neuronal communication which is unbalanced in Alzheimer's disease, Neurobiol Aging, 32, 1435, 10.1016/j.neurobiolaging.2009.08.013 Chistiakov, 2017, alpha-Synuclein-carrying extracellular vesicles in Parkinson's disease: deadly transmitters, Acta Neurol Belg, 117, 43, 10.1007/s13760-016-0679-1 Soria, 2017, Exosomes, an unmasked culprit in neurodegenerative diseases, Front Neurosci, 11, e26, 10.3389/fnins.2017.00026 Tofaris, 2017, A critical assessment of exosomes in the pathogenesis and stratification of Parkinson's disease, J Parkinson's Dis, 7, 569, 10.3233/JPD-171176 Chang, 2013, Exosomes of BV-2 cells induced by alpha-synuclein: important mediator of neurodegeneration in PD, Neurosci Lett, 548, 190, 10.1016/j.neulet.2013.06.009 Zhang, 2016, Potential transfer of polyglutamine and CAG-repeat RNA in extracellular vesicles in Huntington's disease: background and evaluation in cell culture, Cell Mol Neurobiol, 36, 459, 10.1007/s10571-016-0350-7 Bonafede, 2017, ALS pathogenesis and therapeutic approaches: the role of mesenchymal stem cells and extracellular vesicles, Front Cell Neurosci, 11, e80, 10.3389/fncel.2017.00080 Fyfe, 2017, Motor neuron disease: proinflammatory monocytes might contribute to ALS progression, Nat Rev Neurol, 13, e385 Zondler, 2017, Impaired activation of ALS monocytes by exosomes, Immunol Cell Biol, 95, 207, 10.1038/icb.2016.89 Sproviero, 2018, Pathological proteins are transported by extracellular vesicles of sporadic amyotrophic lateral sclerosis patients, Front Neurosci, 12, e487, 10.3389/fnins.2018.00487 Fiandaca, 2015, Identification of preclinical Alzheimer's disease by a profile of pathogenic proteins in neurally derived blood exosomes: a case-control study, Alzheimers Dement, 11, 600, 10.1016/j.jalz.2014.06.008 Winston, 2016, Prediction of conversion from mild cognitive impairment to dementia with neuronally derived blood exosome protein profile, Alzheimers Dement, 3, 63 Kapogiannis, 2015, Dysfunctionally phosphorylated type 1 insulin receptor substrate in neural-derived blood exosomes of preclinical Alzheimer's disease, FASEB J, 29, 589, 10.1096/fj.14-262048 Goetzl, 2015, Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease, Neurology, 85, 40, 10.1212/WNL.0000000000001702 Goetzl, 2018, Declining levels of functionally specialized synaptic proteins in plasma neuronal exosomes with progression of Alzheimer's disease, FASEB J, 32, 888, 10.1096/fj.201700731R Liu, 2014, MicroRNA-193b is a regulator of amyloid precursor protein in the blood and cerebrospinal fluid derived exosomal microRNA-193b is a biomarker of Alzheimer's disease, Mol Med Rep, 10, 2395, 10.3892/mmr.2014.2484 Lugli, 2015, Plasma exosomal miRNAs in persons with and without alzheimer disease: altered expression and prospects for biomarkers, PLoS One, 10, 10.1371/journal.pone.0139233 Wang, 2017, Elevated LRRK2 autophosphorylation in brain-derived and peripheral exosomes in LRRK2 mutation carriers, Acta Neuropathol Commun, 6, e86, 10.1186/s40478-017-0492-y Stuendl, 2016, Induction of alpha-synuclein aggregate formation by CSF exosomes from patients with Parkinson's disease and dementia with Lewy bodies, Brain, 139, 481, 10.1093/brain/awv346 Barbour, 2008, Red blood cells are the major source of alpha-synuclein in blood, Neurodegener Dis, 5, 55, 10.1159/000112832 Shi, 2010, Significance and confounders of peripheral DJ-1 and alpha-synuclein in Parkinson's disease, Neurosci Lett, 480, 78, 10.1016/j.neulet.2010.06.009 Cerri, 2018, The exosomal/total alpha-synuclein ratio in plasma is associated with glucocerebrosidase activity and correlates with measures of disease severity in PD patients, Front Cell Neurosci, 12, e125, 10.3389/fncel.2018.00125 Shi, 2014, Plasma exosomal alpha-synuclein is likely CNS-derived and increased in Parkinson's disease, Acta Neuropathol, 128, 639, 10.1007/s00401-014-1314-y Shi, 2016, CNS tau efflux via exosomes is likely increased in Parkinson's disease but not in Alzheimer's disease, Alzheimers Dement, 12, 1125, 10.1016/j.jalz.2016.04.003 Cao, 2019, alpha-Synuclein in salivary extracellular vesicles as a potential biomarker of Parkinson's disease, Neurosci Lett, 696, 114, 10.1016/j.neulet.2018.12.030 Ho, 2014, Increased DJ-1 in urine exosome of Korean males with Parkinson's disease, BioMed Res Int, 2014, 10.1155/2014/704678 Fraser, 2016, Ser(P)-1292 LRRK2 in urinary exosomes is elevated in idiopathic Parkinson's disease, Mov Disord, 31, 1543, 10.1002/mds.26686 Fraser, 2016, Urinary LRRK2 phosphorylation predicts parkinsonian phenotypes in G2019S LRRK2 carriers, Neurology, 86, 994, 10.1212/WNL.0000000000002436 Gui, 2015, Altered microRNA profiles in cerebrospinal fluid exosome in Parkinson disease and Alzheimer disease, Oncotarget, 6, 37043, 10.18632/oncotarget.6158 Cao, 2017, MicroRNA biomarkers of Parkinson's disease in serum exosome-like microvesicles, Neurosci Lett, 644, 94, 10.1016/j.neulet.2017.02.045 Doxakis, 2010, Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153, J Biol Chem, 285, 12726, 10.1074/jbc.M109.086827 Junn, 2009, Repression of alpha-synuclein expression and toxicity by microRNA-7, Proc Natl Acad Sci U S A, 106, 13052, 10.1073/pnas.0906277106 Denis, 2019, Platelet abnormalities in Huntington's disease, J Neurol Neurosurg Psychiatry, 90, 272, 10.1136/jnnp-2018-318854 Denis, 2018, Platelet-derived extracellular vesicles in Huntington's disease, J Neurol, 265, 2704, 10.1007/s00415-018-9022-5 Xu, 2018, Comparison of the extraction and determination of serum exosome and miRNA in serum and the detection of miR-27a-3p in serum exosome of ALS patients, Intractable Rare Dis Res, 7, 13, 10.5582/irdr.2017.01091 Otake, 2019, Identification of biomarkers for amyotrophic lateral sclerosis by comprehensive analysis of exosomal mRNAs in human cerebrospinal fluid, BMC Med Genomics, 12, e7, 10.1186/s12920-019-0473-z Li, 2019, In Vitro and in vivo RNA inhibition by CD9-HuR functionalized exosomes encapsulated with miRNA or CRISPR/dCas9, Nano Lett, 19, 19, 10.1021/acs.nanolett.8b02689 Hall, 2016, Delivery of therapeutic proteins via extracellular vesicles: review and potential treatments for Parkinson's disease, glioma, and schwannoma, Cell Mol Neurobiol, 36, 417, 10.1007/s10571-015-0309-0 Garbayo, 2016, Brain delivery of microencapsulated GDNF induces functional and structural recovery in parkinsonian monkeys, Biomaterials, 110, 11, 10.1016/j.biomaterials.2016.09.015 Lee, 2016, Exosomes from adipose-derived stem cells ameliorate phenotype of Huntington's disease in vitro model, Eur J Neurosci, 44, 2114, 10.1111/ejn.13275 Didiot, 2016, Exosome-mediated delivery of hydrophobically modified siRNA for Huntingtin mRNA silencing, Mol Ther, 24, 1836, 10.1038/mt.2016.126 Lee, 2017, Exosome-based delivery of miR-124 in a Huntington's disease model, J Mov Disord, 10, 45, 10.14802/jmd.16054 Lee, 2016, Adipose-derived stem cell exosomes alleviate pathology of amyotrophic lateral sclerosis in vitro, Biochem Biophys Res Commun, 479, 434, 10.1016/j.bbrc.2016.09.069 Bonafede, 2016, Exosome derived from murine adipose-derived stromal cells: neuroprotective effect on in vitro model of amyotrophic lateral sclerosis, Exp Cell Res, 340, 150, 10.1016/j.yexcr.2015.12.009