Extracellular vesicles in neurodegenerative diseases

Molecular Aspects of Medicine

Volumn 60, Issue , 2018, Pages 52-61

  Croese, Tommaso ^a   Furlan, Roberto ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Alzheimer's disease; Amyotrophic lateral sclerosis; Extracellular vesicles; Huntington's disease; Multiple sclerosis; Parkinson's disease

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; BETA 2 MICROGLOBULIN; BETA3 INTEGRIN; CD14 ANTIGEN; CD146 ANTIGEN; CD40 ANTIGEN; GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MICRORNA; MICRORNA 122 5P; MICRORNA 124; MICRORNA 132; MICRORNA 193B; MICRORNA 196B 5P; MICRORNA 219; MICRORNA 301A 3P; MICRORNA 532 5P; PLATELET ENDOTHELIAL CELL ADHESION MOLECULE 1; RECEPTOR TYPE TYROSINE PROTEIN PHOSPHATASE C; TAR DNA BINDING PROTEIN; TAU PROTEIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; BIOLOGICAL MARKER;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; BLOOD BRAIN BARRIER; CELL FUNCTION; COGNITIVE DEFECT; DEGENERATIVE DISEASE; DOWN REGULATION; EXOSOME; HUMAN; HUNTINGTON CHOREA; MULTIPLE SCLEROSIS; NONHUMAN; PARKINSON DISEASE; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; ANIMAL; DISEASE EXACERBATION; GENETICS; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; BIOMARKERS; DISEASE PROGRESSION; EXTRACELLULAR VESICLES; HUMANS; NEURODEGENERATIVE DISEASES;

EID: 85034973870     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2017.11.006     Document Type: Review

References (108)

1. Agosta, F., Dalla Libera, D., Spinelli, E.G., Finardi, A., Canu, E., Bergami, A., Bocchio Chiavetto, L., Baronio, M., Comi, G., Martino, G., Matteoli, M., Magnani, G., Verderio, C., Furlan, R., Myeloid microvesicles in cerebrospinal fluid are associated with myelin damage and neuronal loss in mild cognitive impairment and Alzheimer disease. Ann. Neurol. 76 (2014), 813–825, 10.1002/ana.24235.
2. Alexander, J.S., Chervenak, R., Weinstock-Guttman, B., Tsunoda, I., Ramanathan, M., Martinez, N., Omura, S., Sato, F., Chaitanya, G.V., Minagar, A., McGee, J., Jennings, M.H., Monceaux, C., Becker, F., Cvek, U., Trutschl, M., Zivadinov, R., Blood circulating microparticle species in relapsing-remitting and secondary progressive multiple sclerosis. A case-control, cross sectional study with conventional MRI and advanced iron content imaging outcomes. J. Neurol. Sci. 355 (2015), 84–89, 10.1016/j.jns.2015.05.027.
3. Alvarez-Erviti, L., Seow, Y., Schapira, A.H., Gardiner, C., Sargent, I.L., Wood, M.J.A., Cooper, J.M., Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission. Neurobiol. Dis. 42 (2011), 360–367, 10.1016/j.nbd.2011.01.029.
4. An, K., Klyubin, I., Kim, Y., Jung, J.H., Mably, A.J., O'Dowd, S.T., Lynch, T., Kanmert, D., Lemere, C.A., Finan, G.M., Park, J.W., Kim, T.-W., Walsh, D.M., Rowan, M.J., Kim, J.-H., Exosomes neutralize synaptic-plasticity-disrupting activity of Aβ assemblies in vivo. Mol. Brain, 6, 2013, 47, 10.1186/1756-6606-6-47.
5. Antonucci, F., Turola, E., Riganti, L., Caleo, M., Gabrielli, M., Perrotta, C., Novellino, L., Clementi, E., Giussani, P., Viani, P., Matteoli, M., Verderio, C., Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. EMBO J. 31 (2012), 1231–1240, 10.1038/emboj.2011.489.
6. Asai, H., Ikezu, S., Tsunoda, S., Medalla, M., Luebke, J., Haydar, T., Wolozin, B., Butovsky, O., Kügler, S., Ikezu, T., Depletion of microglia and inhibition of exosome synthesis halt tau propagation. Nat. Neurosci. 18 (2015), 1584–1593, 10.1038/nn.4132.
7. Bonafede, R., Mariotti, R., ALS pathogenesis and therapeutic approaches: the role of mesenchymal stem cells and extracellular vesicles. Front. Cell Neurosci., 11, 2017, 80, 10.3389/fncel.2017.00080.
8. Bonafede, R., Scambi, I., Peroni, D., Potrich, V., Boschi, F., Benati, D., Bonetti, B., Mariotti, R., Exosome derived from murine adipose-derived stromal cells: neuroprotective effect on in vitro model of amyotrophic lateral sclerosis. Exp. Cell Res. 340 (2016), 150–158, 10.1016/j.yexcr.2015.12.009.
9. Burgos, K., Malenica, I., Metpally, R., Courtright, A., Rakela, B., Beach, T., Shill, H., Adler, C., Sabbagh, M., Villa, S., Tembe, W., Craig, D., Van Keuren-Jensen, K., Profiles of extracellular miRNA in cerebrospinal fluid and serum from patients with Alzheimer“s and Parkinson”s diseases correlate with disease status and features of pathology. PLoS One, 9, 2014, e94839, 10.1371/journal.pone.0094839.
10. Chang, C., Lang, H., Geng, N., Wang, J., Li, N., Wang, X., Exosomes of BV-2 cells induced by alpha-synuclein: important mediator of neurodegeneration in PD. Neurosci. Lett. 548 (2013), 190–195, 10.1016/j.neulet.2013.06.009.
11. Chen-Plotkin, A.S., Unger, T.L., Gallagher, M.D., Bill, E., Kwong, L.K., Volpicelli-Daley, L., Busch, J.I., Akle, S., Grossman, M., Van Deerlin, V., Trojanowski, J.Q., Lee, V.M.-Y., TMEM106B, the risk gene for frontotemporal dementia, is regulated by the microRNA-132/212 cluster and affects progranulin pathways. J. Neurosci. 32 (2012), 11213–11227, 10.1523/JNEUROSCI.0521-12.2012.
12. Cheng, L., Doecke, J.D., Sharples, R.A., Villemagne, V.L., Fowler, C.J., Rembach, A., Martins, R.N., Rowe, C.C., Macaulay, S.L., Masters, C.L., Hill, A.F., Australian Imaging, Biomarkers and Lifestyle (AIBL) Research Group. Prognostic serum miRNA biomarkers associated with Alzheimer's disease shows concordance with neuropsychological and neuroimaging assessment. Mol. Psychiatry 20 (2015), 1188–1196, 10.1038/mp.2014.127.
13. Cheng, L., Quek, C.Y.J., Sun, X., Bellingham, S.A., Hill, A.F., The detection of microRNA associated with Alzheimer's disease in biological fluids using next-generation sequencing technologies. Front. Genet., 4, 2013, 150, 10.3389/fgene.2013.00150.
14. Cheng, L., Sharples, R.A., Scicluna, B.J., Hill, A.F., Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J. Extracell. Vesicles, 3, 2014, 10.3402/jev.v3.23743.
15. Chiti, F., Dobson, C.M., Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu. Rev. Biochem. 86 (2017), 27–68, 10.1146/annurev-biochem-061516-045115.
16. Cogswell, J.P., Ward, J., Taylor, I.A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C., Prinjha, R.K., Richardson, J.C., Saunders, A.M., Roses, A.D., Richards, C.A., Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis. 14 (2008), 27–41.
17. Colombo, M., Raposo, G., Théry, C., Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30 (2014), 255–289, 10.1146/annurev-cellbio-101512-122326.
18. Compston, A., Coles, A., Multiple sclerosis. Lancet 372 (2008), 1502–1517, 10.1016/S0140-6736(08)61620-7.
19. Coumans, F.A.W., Brisson, A.R., Buzas, E.I., Dignat-George, F., Drees, E.E.E., El-Andaloussi, S., Emanueli, C., Gasecka, A., Hendrix, A., Hill, A.F., Lacroix, R., Lee, Y., van Leeuwen, T.G., Mackman, N., Mäger, I., Nolan, J.P., van der Pol, E., Pegtel, D.M., Sahoo, S., Siljander, P.R.M., Sturk, G., de Wever, O., Nieuwland, R., Methodological guidelines to study extracellular vesicles. Circ. Res. 120 (2017), 1632–1648, 10.1161/CIRCRESAHA.117.309417.
20. Danzer, K.M., Kranich, L.R., Ruf, W.P., Cagsal-Getkin, O., Winslow, A.R., Zhu, L., Vanderburg, C.R., McLean, P.J., Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol. Neurodegener., 7, 2012, 42, 10.1186/1750-1326-7-42.
21. Dawson, G., Qin, J., Gilenya (FTY720) inhibits acid sphingomyelinase by a mechanism similar to tricyclic antidepressants. Biochem. Biophys. Res. Commun. 404 (2011), 321–323, 10.1016/j.bbrc.2010.11.115.
22. Dendrou, C.A., Fugger, L., Friese, M.A., Immunopathology of multiple sclerosis. Nat. Rev. Immunol. 15 (2015), 545–558, 10.1038/nri3871.
23. Ding, X., Ma, M., Teng, J., Teng, R.K.F., Zhou, S., Yin, J., Fonkem, E., Huang, J.H., Wu, E., Wang, X., Exposure to ALS-FTD-CSF generates TDP-43 aggregates in glioblastoma cells through exosomes and TNTs-like structure. Oncotarget 6 (2015), 24178–24191, 10.18632/oncotarget.4680.
24. Dinkins, M.B., Enasko, J., Hernandez, C., Wang, G., Kong, J., Helwa, I., Liu, Y., Terry, A.V., Bieberich, E., Neutral Sphingomyelinase-2 deficiency ameliorates Alzheimer's disease pathology and improves cognition in the 5XFAD mouse. J. Neurosci. 36 (2016), 8653–8667, 10.1523/JNEUROSCI.1429-16.2016.
25. Eitan, E., Hutchison, E.R., Marosi, K., Comotto, J., Mustapic, M., Nigam, S.M., Suire, C., Maharana, C., Jicha, G.A., Liu, D., Machairaki, V., Witwer, K.W., Kapogiannis, D., Mattson, M.P., Extracellular vesicle-associated Aβ mediates trans-neuronal bioenergetic and Ca(2+)-Handling deficits in Alzheimer's disease models. NPJ Aging Mech. Dis., 2, 2016, 10.1038/npjamd.2016.19.
26. Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S.D., Ntzouni, M., Margaritis, L.H., Stefanis, L., Vekrellis, K., Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 30 (2010), 6838–6851, 10.1523/JNEUROSCI.5699-09.2010.
27. Falker, C., Hartmann, A., Guett, I., Dohler, F., Altmeppen, H., Betzel, C., Schubert, R., Thurm, D., Wegwitz, F., Joshi, P., Verderio, C., Krasemann, S., Glatzel, M., Exosomal cellular prion protein drives fibrillization of amyloid beta and counteracts amyloid beta-mediated neurotoxicity. J. Neurochem. 137 (2016), 88–100, 10.1111/jnc.13514.
28. Fernandes, H.J.R., Hartfield, E.M., Christian, H.C., Emmanoulidou, E., Zheng, Y., Booth, H., Bogetofte, H., Lang, C., Ryan, B.J., Sardi, S.P., Badger, J., Vowles, J., Evetts, S., Tofaris, G.K., Vekrellis, K., Talbot, K., Hu, M.T., James, W., Cowley, S.A., Wade-Martins, R., ER stress and autophagic perturbations lead to elevated extracellular α-synuclein in GBA-N370S Parkinson's iPSC-derived dopamine neurons. Stem Cell Rep. 6 (2016), 342–356, 10.1016/j.stemcr.2016.01.013.
29. Fiandaca, M.S., Kapogiannis, D., Mapstone, M., Boxer, A., Eitan, E., Schwartz, J.B., Abner, E.L., Petersen, R.C., Federoff, H.J., Miller, B.L., Goetzl, E.J., Identification of preclinical Alzheimer's disease by a profile of pathogenic proteins in neurally derived blood exosomes: a case-control study. Alzheimers Dement., 11, 2015, 10.1016/j.jalz.2014.06.008 600–607.e1.
30. Fraser, K.B., Moehle, M.S., Daher, J.P.L., Webber, P.J., Williams, J.Y., Stewart, C.A., Yacoubian, T.A., Cowell, R.M., Dokland, T., Ye, T., Chen, D., Siegal, G.P., Galemmo, R.A., Tsika, E., Moore, D.J., Standaert, D.G., Kojima, K., Mobley, J.A., West, A.B., LRRK2 secretion in exosomes is regulated by 14-3-3. Hum. Mol. Genet. 22 (2013), 4988–5000, 10.1093/hmg/ddt346.
31. Fraser, K.B., Rawlins, A.B., Clark, R.G., Alcalay, R.N., Standaert, D.G., Liu, N. Parkinson's Disease Biomarker Program Consortium, West, A.B., Ser(P)-1292 LRRK2 in urinary exosomes is elevated in idiopathic Parkinson's disease. Mov. Disord. 31 (2016), 1543–1550, 10.1002/mds.26686.
32. Gabrielli, M., Battista, N., Riganti, L., Prada, I., Antonucci, F., Cantone, L., Matteoli, M., Maccarrone, M., Verderio, C., Active endocannabinoids are secreted on extracellular membrane vesicles. EMBO Rep. 16 (2015), 213–220, 10.15252/embr.201439668.
33. Galazka, G., Mycko, M.P., Selmaj, I., Raine, C.S., Selmaj, K.W., Multiple sclerosis: serum-derived exosomes express myelin proteins. Mult. Scler., 2017, 10.1177/1352458517696597 1352458517696597.
34. Garbayo, E., Ansorena, E., Lana, H., Carmona-Abellan, M.D.M., Marcilla, I., Lanciego, J.L., Luquin, M.R., Blanco-Prieto, M.J., Brain delivery of microencapsulated GDNF induces functional and structural recovery in parkinsonian monkeys. Biomaterials 110 (2016), 11–23, 10.1016/j.biomaterials.2016.09.015.
35. Ghidoni, R., Paterlini, A., Albertini, V., Glionna, M., Monti, E., Schiaffonati, L., Benussi, L., Levy, E., Binetti, G., Cystatin C is released in association with exosomes: a new tool of neuronal communication which is unbalanced in Alzheimer's disease. Neurobiol. Aging 32 (2011), 1435–1442, 10.1016/j.neurobiolaging.2009.08.013.
36. Goetzl, E.J., Boxer, A., Schwartz, J.B., Abner, E.L., Petersen, R.C., Miller, B.L., Kapogiannis, D., Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease. Neurology 85 (2015), 40–47, 10.1212/WNL.0000000000001702.
37. Goetzl, E.J., Kapogiannis, D., Schwartz, J.B., Lobach, I.V., Goetzl, L., Abner, E.L., Jicha, G.A., Karydas, A.M., Boxer, A., Miller, B.L., Decreased synaptic proteins in neuronal exosomes of frontotemporal dementia and Alzheimer's disease. FASEB J. 30 (2016), 4141–4148, 10.1096/fj.201600816R.
38. Gould, S.J., Raposo, G., As we wait: coping with an imperfect nomenclature for extracellular vesicles. J. Extracell. Vesicles, 2, 2013, 10.3402/jev.v2i0.20389.
39. Grey, M., Dunning, C.J., Gaspar, R., Grey, C., Brundin, P., Sparr, E., Linse, S., Acceleration of α-synuclein aggregation by exosomes. J. Biol. Chem. 290 (2015), 2969–2982, 10.1074/jbc.M114.585703.
40. Guerreiro, P.S., Huang, Y., Gysbers, A., Cheng, D., Gai, W.P., Outeiro, T.F., Halliday, G.M., LRRK2 interactions with α-synuclein in Parkinson's disease brains and in cell models. J. Mol. Med. 91 (2013), 513–522, 10.1007/s00109-012-0984-y.
41. Gui, Y., Liu, H., Zhang, L., Lv, W., Hu, X., Altered microRNA profiles in cerebrospinal fluid exosome in Parkinson disease and Alzheimer disease. Oncotarget 6 (2015), 37043–37053, 10.18632/oncotarget.6158.
42. Guo, J.L., Lee, V.M.-Y., Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J. Biol. Chem. 286 (2011), 15317–15331, 10.1074/jbc.M110.209296.
43. Hall, J., Prabhakar, S., Balaj, L., Lai, C.P., Cerione, R.A., Breakefield, X.O., Delivery of therapeutic proteins via extracellular vesicles: review and potential treatments for Parkinson's disease, glioma, and schwannoma. Cell Mol. Neurobiol. 36 (2016), 417–427, 10.1007/s10571-015-0309-0.
44. Haney, M.J., Klyachko, N.L., Zhao, Y., Gupta, R., Plotnikova, E.G., He, Z., Patel, T., Piroyan, A., Sokolsky, M., Kabanov, A.V., Batrakova, E.V., Exosomes as drug delivery vehicles for Parkinson's disease therapy. J. Control Release 207 (2015), 18–30, 10.1016/j.jconrel.2015.03.033.
45. Harischandra, D.S., Ghaisas, S., Rokad, D., Zamanian, M., Jin, H., Anantharam, V., Kimber, M., Kanthasamy, A., Kanthasamy, A.G., Environmental neurotoxicant manganese regulates exosome-mediated extracellular miRNAs in cell culture model of Parkinson's disease: relevance to α-synuclein misfolding in metal neurotoxicity. Neurotoxicology, 2017, 10.1016/j.neuro.2017.04.007.
46. Heneka, M.T., Carson, M.J., Khoury, El, J., Landreth, G.E., Brosseron, F., Feinstein, D.L., Jacobs, A.H., Wyss-Coray, T., Vitorica, J., Ransohoff, R.M., Herrup, K., Frautschy, S.A., Finsen, B., Brown, G.C., Verkhratsky, A., Yamanaka, K., Koistinaho, J., Latz, E., Halle, A., Petzold, G.C., Town, T., Morgan, D., Shinohara, M.L., Perry, V.H., Holmes, C., Bazan, N.G., Brooks, D.J., Hunot, S., Joseph, B., Deigendesch, N., Garaschuk, O., Boddeke, E., Dinarello, C.A., Breitner, J.C., Cole, G.M., Golenbock, D.T., Kummer, M.P., Neuroinflammation in Alzheimer's disease. Lancet neurol. 14 (2015), 388–405, 10.1016/S1474-4422(15)70016-5.
47. Hébert, S.S., Wang, W.-X., Zhu, Q., Nelson, P.T., A study of small RNAs from cerebral neocortex of pathology-verified Alzheimer's disease, dementia with lewy bodies, hippocampal sclerosis, frontotemporal lobar dementia, and non-demented human controls. J. Alzheimers Dis. 35 (2013), 335–348, 10.3233/JAD-122350.
48. Hunter, M.P., Ismail, N., Zhang, X., Aguda, B.D., Lee, E.J., Yu, L., Xiao, T., Schafer, J., Lee, M.-L.T., Schmittgen, T.D., Nana-Sinkam, S.P., Jarjoura, D., Marsh, C.B., Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE, 3, 2008, e3694, 10.1371/journal.pone.0003694.
49. Hwang, J.-Y., Aromolaran, K.A., Zukin, R.S., The emerging field of epigenetics in neurodegeneration and neuroprotection. Nat. Rev. Neurosci. 18 (2017), 347–361, 10.1038/nrn.2017.46.
50. Iba, M., Guo, J.L., McBride, J.D., Zhang, B., Trojanowski, J.Q., Lee, V.M.-Y., Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J. Neurosci. 33 (2013), 1024–1037, 10.1523/JNEUROSCI.2642-12.2013.
51. Iguchi, Y., Eid, L., Parent, M., Soucy, G., Bareil, C., Riku, Y., Kawai, K., Takagi, S., Yoshida, M., Katsuno, M., Sobue, G., Julien, J.-P., Exosome secretion is a key pathway for clearance of pathological TDP-43. Brain 139 (2016), 3187–3201, 10.1093/brain/aww237.
52. Jimenez, J., Jy, W., Mauro, L.M., Horstman, L.L., Ahn, E.R., Ahn, Y.S., Minagar, A., Elevated endothelial microparticle-monocyte complexes induced by multiple sclerosis plasma and the inhibitory effects of interferon-beta 1b on release of endothelial microparticles, formation and transendothelial migration of monocyte-endothelial microparticle complexes. Mult. Scler. 11 (2005), 310–315, 10.1191/1352458505ms1184oa.
53. Joshi, P., Turola, E., Ruiz, A., Bergami, A., Libera, D.D., Benussi, L., Giussani, P., Magnani, G., Comi, G., Legname, G., Ghidoni, R., Furlan, R., Matteoli, M., Verderio, C., Microglia convert aggregated amyloid. Cell Death Differ., 1–12, 2013, 10.1038/cdd.2013.180.
54. Jy, W., Minagar, A., Jimenez, J.J., Sheremata, W.A., Mauro, L.M., Horstman, L.L., Bidot, C., Ahn, Y.S., Endothelial microparticles (EMP) bind and activate monocytes: elevated EMP-monocyte conjugates in multiple sclerosis. Front. Biosci. 9 (2004), 3137–3144.
55. Kawachi, I., Lassmann, H., Neurodegeneration in multiple sclerosis and neuromyelitis optica. J. Neurol. Neurosurg. Psychiatr. 88 (2017), 137–145, 10.1038/nm.3015.
56. Kong, S.M.Y., Chan, B.K.K., Park, J.-S., Hill, K.J., Aitken, J.B., Cottle, L., Farghaian, H., Cole, A.R., Lay, P.A., Sue, C.M., Cooper, A.A., Parkinson's disease-linked human PARK9/ATP13A2 maintains zinc homeostasis and promotes α-Synuclein externalization via exosomes. Hum. Mol. Genet. 23 (2014), 2816–2833, 10.1093/hmg/ddu099.
57. Lau, P., Frigerio, C.S., De Strooper, B., Variance in the identification of microRNAs deregulated in Alzheimer's disease and possible role of lincRNAs in the pathology: the need of larger datasets. Ageing Res. Rev. 17 (2014), 43–53, 10.1016/j.arr.2014.02.006.
58. Lee, M., Ban, J.-J., Kim, K.Y., Jeon, G.S., Im, W., Sung, J.-J., Kim, M., Adipose-derived stem cell exosomes alleviate pathology of amyotrophic lateral sclerosis in vitro. Biochem. Biophys. Res. Commun. 479 (2016), 434–439, 10.1016/j.bbrc.2016.09.069.
59. Lee, S.-T., Im, W., Ban, J.-J., Lee, M., Jung, K.-H., Lee, S.K., Chu, K., Kim, M., Exosome-based delivery of miR-124 in a Huntington's disease model. J. Mov. Disord. 10 (2017), 45–52, 10.14802/jmd.16054.
60. Lee, Y.J., Jy, W., Horstman, L.L., Janania, J., Reyes, Y., Kelley, R.E., Ahn, Y.S., Elevated platelet microparticles in transient ischemic attacks, lacunar infarcts, and multiinfarct dementias. Thromb. Res. 72 (1993), 295–304.
61. Liu, C.-G., Song, J., Zhang, Y.-Q., Wang, P.-C., 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 (2014), 2395–2400, 10.3892/mmr.2014.2484.
62. Lowery-Nordberg, M., Eaton, E., Gonzalez-Toledo, E., Harris, M.K., Chalamidas, K., McGee-Brown, J., Ganta, C.V., Minagar, A., Cousineau, D., Alexander, J.S., The effects of high dose interferon-β1a on plasma microparticles: correlation with MRI parameters. J. neuroinflammation, 8, 2011, 43, 10.1186/1742-2094-8-43.
63. Marcos-Ramiro, B., Oliva Nacarino, P., Serrano-Pertierra, E., Blanco-Gelaz, M.A., Weksler, B.B., Romero, I.A., Couraud, P.O., Tuñón, A., López-Larrea, C., Millán, J., Cernuda-Morollón, E., Microparticles in multiple sclerosis and clinically isolated syndrome: effect on endothelial barrier function. BMC Neurosci., 15, 2014, 110, 10.1186/1471-2202-15-110.
64. Medina, M., Avila, J., The role of extracellular Tau in the spreading of neurofibrillary pathology. Front. Cell Neurosci., 8, 2014, 113, 10.3389/fncel.2014.00113.
65. Minagar, A., Jy, W., Jimenez, J.J., Sheremata, W.A., Mauro, L.M., Mao, W.W., Horstman, L.L., Ahn, Y.S., Elevated plasma endothelial microparticles in multiple sclerosis. Neurology 56 (2001), 1319–1324.
66. Moyano, A.L., Li, G., Boullerne, A.I., Feinstein, D.L., Hartman, E., Skias, D., Balavanov, R., van Breemen, R.B., Bongarzone, E.R., Månsson, J.-E., Givogri, M.I., Sulfatides in extracellular vesicles isolated from plasma of multiple sclerosis patients. J. Neurosci. Res. 94 (2016), 1579–1587, 10.1002/jnr.23899.
67. Mullins, R.J., Mustapic, M., Goetzl, E.J., Kapogiannis, D., Exosomal biomarkers of brain insulin resistance associated with regional atrophy in Alzheimer's disease. Hum. Brain Mapp. 38 (2017), 1933–1940, 10.1002/hbm.23494.
68. Mustapic, M., Eitan, E., Werner, J.K. Jr., Berkowitz, S.T., Lazaropoulos, M.P., Tran, J., Goetzl, E.J., Kapogiannis, D., Plasma extracellular vesicles enriched for neuronal origin: a potential window into brain pathologic processes. Front. Neurosci., 11, 2017, 399, 10.1016/j.dadm.2016.04.001.
69. Pant, S., Hilton, H., Burczynski, M.E., The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem. Pharmacol. 83 (2012), 1484–1494, 10.1016/j.bcp.2011.12.037.
70. Perez-Gonzalez, R., Gauthier, S.A., Kumar, A., Levy, E., The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. J. Biol. Chem. 287 (2012), 43108–43115, 10.1074/jbc.M112.404467.
71. Peters, O.M., Ghasemi, M., Brown, R.H., Emerging mechanisms of molecular pathology in ALS. J. Clin. Invest. 125 (2015), 1767–1779, 10.1172/JCI71601.
72. Pinto, S., Cunha, C., Barbosa, M., Vaz, A.R., Brites, D., Exosomes from NSC-34 Cells Transfected with hSOD1-G93A Are Enriched in miR-124 and Drive Alterations in Microglia Phenotype, vol. 11, 2017, 273, 10.3389/fnins.2017.00273.
73. Pusic, A.D., Pusic, K.M., Clayton, B.L.L., Kraig, R.P., IFNγ-stimulated dendritic cell exosomes as a potential therapeutic for remyelination. J. Neuroimmunol. 266 (2014), 12–23, 10.1016/j.jneuroim.2013.10.014.
74. Rajendran, L., Honsho, M., Zahn, T.R., Keller, P., Geiger, K.D., Verkade, P., Simons, K., Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 11172–11177, 10.1073/pnas.0603838103.
75. Richards, R.I., Dynamic mutations: a decade of unstable expanded repeats in human genetic disease. Hum. Mol. Genet. 10 (2001), 2187–2194.
76. Rocha, E.M., De Miranda, B., Sanders, L.H., Alpha-synuclein: pathology, mitochondrial dysfunction and neuroinflammation in Parkinson's disease. Neurobiol. Dis., 2017, 10.1016/j.nbd.2017.04.004.
77. Rocha, N.P., Ribeiro, F.M., Furr-Stimming, E., Teixeira, A.L., Neuroimmunology of Huntington's disease: revisiting evidence from human studies. Mediat. Inflamm., 2016, 2016, 8653132, 10.1155/2016/8653132.
78. Rowland, L.P., How amyotrophic lateral sclerosis got its name: the clinical-pathologic genius of Jean-Martin Charcot. Arch. Neurol. 58:3 (2001), 512–515, 10.1001/archneur.58.3.512.
79. Sanabria-Castro, A., Alvarado-Echeverría, I., Monge-Bonilla, C., Molecular pathogenesis of Alzheimer's disease: an update. Ann. Neurosci. 24 (2017), 46–54, 10.1159/000464422.
80. Santa-Maria, I., Alaniz, M.E., Renwick, N., Cela, C., Fulga, T.A., Van Vactor, D., Tuschl, T., Clark, L.N., Shelanski, M.L., McCabe, B.D., Crary, J.F., Dysregulation of microRNA-219 promotes neurodegeneration through post-transcriptional regulation of tau. J. Clin. Invest. 125 (2015), 681–686, 10.1172/JCI78421.
81. Saudou, F., Humbert, S., The biology of huntingtin. Neuron 89 (2016), 910–926, 10.1016/j.neuron.2016.02.003.
82. Sáenz-Cuesta, M., Irizar, H., Castillo-Triviño, T., Muñoz-Culla, M., Osorio-Querejeta, I., Prada, A., Sepúlveda, L., López-Mato, M.P., López de Munain, A., Comabella, M., Villar, L.M., Olascoaga, J., Otaegui, D., Circulating microparticles reflect treatment effects and clinical status in multiple sclerosis. Biomark. Med. 8 (2014), 653–661, 10.2217/bmm.14.9.
83. Sáenz-Cuesta, M., Osorio-Querejeta, I., Otaegui, D., Extracellular vesicles in multiple sclerosis: what are they telling us?. Front. Cell Neurosci., 8, 2014, 100, 10.3389/fncel.2014.00100.
84. Scolding, N.J., Morgan, B.P., Houston, W.A., Linington, C., Campbell, A.K., Compston, D.A., Vesicular removal by oligodendrocytes of membrane attack complexes formed by activated complement. Nature 339 (1989), 620–622, 10.1038/339620a0.
85. Selmaj, I., Cichalewska, M., Namiecinska, M., Galazka, G., Horzelski, W., Selmaj, K.W., Mycko, M.P., Global exosome transcriptome profiling reveals biomarkers for multiple sclerosis. Ann. Neurol. 81 (2017), 703–717, 10.1002/ana.24931.
86. Sharples, R.A., Vella, L.J., Nisbet, R.M., Naylor, R., Perez, K., Barnham, K.J., Masters, C.L., Hill, A.F., Inhibition of gamma-secretase causes increased secretion of amyloid precursor protein C-terminal fragments in association with exosomes. FASEB J. 22 (2008), 1469–1478, 10.1096/fj.07-9357com.
87. Sheremata, W.A., Jy, W., Horstman, L.L., Ahn, Y.S., Alexander, J.S., Minagar, A., Evidence of platelet activation in multiple sclerosis. J. neuroinflammation, 5, 2008, 27, 10.1186/1742-2094-5-27.
88. Shi, M., Liu, C., Cook, T.J., Bullock, K.M., Zhao, Y., Ginghina, C., Li, Y., Aro, P., Dator, R., He, C., Hipp, M.J., Zabetian, C.P., Peskind, E.R., Hu, S.-C., Quinn, J.F., Galasko, D.R., Banks, W.A., Zhang, J., Plasma exosomal α-synuclein is likely CNS-derived and increased in Parkinson's disease. Acta Neuropathol. 128 (2014), 639–650, 10.1007/s00401-014-1314-y.
89. Shrivastava, A.N., Aperia, A., Melki, R., Triller, A., Physico-pathologic mechanisms involved in neurodegeneration: misfolded protein-plasma membrane interactions. Neuron 95 (2017), 33–50, 10.1016/j.neuron.2017.05.026.
90. Silverman, J.M., Fernando, S.M., Grad, L.I., Hill, A.F., Turner, B.J., Yerbury, J.J., Cashman, N.R., Disease mechanisms in ALS: misfolded SOD1 transferred through exosome-dependent and exosome-independent pathways. Cell Mol. Neurobiol. 36 (2016), 377–381, 10.1007/s10571-015-0294-3.
91. Stenovec, M., Trkov, S., Lasič, E., Terzieva, S., Kreft, M., Rodríguez Arellano, J.J., Parpura, V., Verkhratsky, A., Zorec, R., Expression of familial Alzheimer disease presenilin 1 gene attenuates vesicle traffic and reduces peptide secretion in cultured astrocytes devoid of pathologic tissue environment. Glia 64 (2016), 317–329, 10.1002/glia.22931.
92. Stuendl, A., Kunadt, M., Kruse, N., Bartels, C., Moebius, W., Danzer, K.M., Mollenhauer, B., Schneider, A., Induction of α-synuclein aggregate formation by CSF exosomes from patients with Parkinson's disease and dementia with Lewy bodies. Brain 139 (2016), 481–494, 10.1093/brain/awv346.
93. Taylor, J.P., Brown, R.H., Cleveland, D.W., Decoding ALS: from genes to mechanism. Nature 539 (2016), 197–206, 10.1038/nature20413.
94. Théry, C., Ostrowski, M., Segura, E., Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9 (2009), 581–593, 10.1038/nri2567.
95. Tomlinson, P.R., Zheng, Y., Fischer, R., Heidasch, R., Gardiner, C., Evetts, S., Hu, M., Wade-Martins, R., Turner, M.R., Morris, J., Talbot, K., Kessler, B.M., Tofaris, G.K., Identification of distinct circulating exosomes in Parkinson's disease. Ann. Clin. Transl. Neurol. 2 (2015), 353–361, 10.1002/acn3.175.
96. Verderio, C., Muzio, L., Turola, E., Bergami, A., Novellino, L., Ruffini, F., Riganti, L., Corradini, I., Francolini, M., Garzetti, L., Maiorino, C., Servida, F., Vercelli, A., Rocca, M., Dalla Libera, D., Martinelli, V., Comi, G., Martino, G., Matteoli, M., Furlan, R., Myeloid microvesicles are a marker and therapeutic target for neuroinflammation. Ann. Neurol. 72 (2012), 610–624, 10.1002/ana.23627.
97. Vingtdeux, V., Hamdane, M., Loyens, A., Gelé, P., Drobeck, H., Bégard, S., Galas, M.-C., Delacourte, A., Beauvillain, J.-C., Buée, L., Sergeant, N., Alkalizing drugs induce accumulation of amyloid precursor protein by-products in luminal vesicles of multivesicular bodies. J. Biol. Chem. 282 (2007), 18197–18205, 10.1074/jbc.M609475200.
98. Wheway, J., Latham, S.L., Combes, V., Grau, G.E.R., Endothelial microparticles interact with and support the proliferation of T cells. J. Immunol. 193 (2014), 3378–3387, 10.4049/jimmunol.1303431.
99. Witwer, K.W., Buzas, E.I., Bemis, L.T., Bora, A., Lässer, C., Lötvall, J., Nolte-'t Hoen, E.N., Piper, M.G., Sivaraman, S., Skog, J., Théry, C., Wauben, M.H., Hochberg, F., Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J. Extracell. Vesicles, 2, 2013, 10.3402/jev.v2i0.20360.
100. Wong, H.-K.A., Veremeyko, T., Patel, N., Lemere, C.A., Walsh, D.M., Esau, C., Vanderburg, C., Krichevsky, A.M., De-repression of FOXO3a death axis by microRNA-132 and -212 causes neuronal apoptosis in Alzheimer's disease. Hum. Mol. Genet. 22 (2013), 3077–3092, 10.1093/hmg/ddt164.
101. Xiao, T., Zhang, W., Jiao, B., Pan, C.-Z., Liu, X., Shen, L., The role of exosomes in the pathogenesis of Alzheimer' disease. Transl. Neurodegener., 6, 2017, 3, 10.1186/s40035-017-0072-x.
102. Yuyama, K., Igarashi, Y., Exosomes as Carriers of Alzheimer's Amyloid-ß, vol. 11, 2017, 229, 10.3389/fnins.2017.00229.
103. Yuyama, K., Sun, H., Sakai, S., Mitsutake, S., Okada, M., Tahara, H., Furukawa, J.-I., Fujitani, N., Shinohara, Y., Igarashi, Y., Decreased amyloid-β pathologies by intracerebral loading of glycosphingolipid-enriched exosomes in Alzheimer model mice. J. Biol. Chem. 289 (2014), 24488–24498, 10.1074/jbc.M114.577213.
104. Yuyama, K., Sun, H., Usuki, S., Sakai, S., Hanamatsu, H., Mioka, T., Kimura, N., Okada, M., Tahara, H., Furukawa, J.-I., Fujitani, N., Shinohara, Y., Igarashi, Y., A potential function for neuronal exosomes: sequestering intracerebral amyloid-β peptide. FEBS Lett. 589 (2015), 84–88, 10.1016/j.febslet.2014.11.027.
105. Zachau, A., Landén, M., Mobarrez, F., Nybom, R., Wallén, H., Wetterberg, L., Leukocyte-derived microparticles and scanning electron microscopic structures in two fractions of fresh cerebrospinal fluid in amyotrophic lateral sclerosis: a case report. J. Med. case Rep., 6, 2012, 274.
106. Zhang, X., Abels, E.R., Redzic, J.S., Margulis, J., Finkbeiner, S., Breakefield, X.O., 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 (2016), 459–470, 10.1007/s10571-016-0350-7.
107. Zinger, A., Latham, S.L., Combes, V., Byrne, S., Barnett, M.H., Hawke, S., Grau, G.E., Plasma levels of endothelial and B-cell-derived microparticles are restored by fingolimod treatment in multiple sclerosis patients. Mult. Scler. 22 (2016), 1883–1887, 10.1177/1352458516636959.
108. Zondler, L., Feiler, M.S., Freischmidt, A., Ruf, W.P., Ludolph, A.C., Danzer, K.M., Weishaupt, J.H., Impaired activation of ALS monocytes by exosomes. Immunol. Cell Biol. 95 (2017), 207–214, 10.1038/icb.2016.89.