The regulation of exosome function in the CNS: implications for neurodegeneration
Abstract
Exosomes are nanovesicles, generally 50 to 90 nm in diameter, that correspond to the intraluminal vesicles of the endosomal multivesicular bodies and are secreted upon fusion of multivesicular bodies with the plasma membrane. Their molecular content is highly selected and includes not only specific proteins and lipids, but also RNA species, such as messenger RNAs (mRNAs) and microRNAs (miRNAs), which are delivered and active in target cells. As they are released in body fluids, exosomes can shuttle molecules for long distances. In the CNS they have been shown to regulate neuronal development and regeneration, and to modulate synaptic functions. In neurodegenerative diseases, they have an important role in propagating neurotoxic misfolded protein from one cell to another and, as recent data show, possibly other molecules contributing to neurotoxicity. Some exosomal lipids such as gangliosides GM1 and GM3 enhance the aggregation of alpha-synuclein, and RNA exosomal cargo is also altered during pathologies such as Alzheimer’s disease, prion diseases and amyotrophic lateral sclerosis. The aim of this review is to focus on the regulation of CNS exosomal function and highlight pathways that might have a role in the neurodegenerative process. The identification of the novel exosomal molecules involved in neurodegenerative diseases could provide important insights into the pathogenesis and contribute to the finding of novel diagnostic biomarkers and therapeutic approaches.
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Previous evidence indicates that miR-146a-5p, miR-181a and miR-223 are dysregulated in patients affected by neuroinflammatory and neurodegenerative diseases.
“Previous evidence indicates that miR-146a-5p, miR-181a and miR-223 are dysregulated in patients affected by neuroinflammatory [36] and neurodegenerative diseases [22, 37, 60], that are characterized by high production of myeloid EVs [38, 78].”
From Glia-to-neuron transfer of miRNAs via extracellular vesicles: a new mechanism underlying inflammation-induced synaptic alterations (2018) · cites this paper as [60]
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Cites
Secretory Mechanisms and Intercellular Transfer of MicroRNAs in Living Cells
Kosaka, N., Iguchi, H., Yoshioka, Y., Takeshita, F., Matsuki, Y., & Ochiya, T. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.107821 · Cited by 1,934 · see citing works
Syndecan–syntenin–ALIX regulates the biogenesis of exosomes
Baietti, M. F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2502 · Cited by 1,899 · see citing works
Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S. D., Ntzouni, M., Margaritis, L. H., Stefanis, L., & Vekrellis, K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5699-09.2010 · Cited by 1,115 · see citing works
A microRNA array reveals extensive regulation of microRNAs during brain development
KRICHEVSKY, A. M., KING, K. S., DONAHUE, C. P., KHRAPKO, K., & KOSIK, K. S. (2003) · RNA · doi:10.1261/rna.5980303 · Cited by 1,040 · see citing works
Saman, S., Kim, W., Raya, M., Visnick, Y., Miro, S., Saman, S., Jackson, B., McKee, A. C., Alvarez, V. E., Lee, N. C. Y., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.277061 · Cited by 985 · see citing works
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., et al. (2015) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2014.06.008 · Cited by 959 · see citing works
Cogswell, J. P., Ward, J., Taylor, I. A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C., et al. (2008) · Journal of Alzheimer s Disease · doi:10.3233/jad-2008-14103 · Cited by 943 · see citing works
Exosomes are released by cultured cortical neurones
Fauré, J., Lachenal, G., Court, M., Hirrlinger, J., Chatellard-Causse, C., Blot, B., Grange, J., Schoehn, G., Goldberg, Y., Boyer, V., et al. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.12.003 · Cited by 896 · see citing works
Ponomarev, E. D., Veremeyko, T., Barteneva, N., Krichevsky, A. M., & Weiner, H. L. (2011) · Nature Medicine · doi:10.1038/nm.2266 · Cited by 787 · see citing works
Urushitani, M., Sik, A., Sakurai, T., Nukina, N., Takahashi, R., & Julien, J.-P. (2006) · Nature Neuroscience · doi:10.1038/nn1603 · Cited by 419 · see citing works
Butovsky, O., Jedrychowski, M. P., Cialic, R., Krasemann, S., Murugaiyan, G., Fanek, Z., Greco, D. J., Wu, P. M., Doykan, C. E., Kiner, O., et al. (2015) · Annals of Neurology · doi:10.1002/ana.24304 · Cited by 358 · see citing works
Emerging roles of exosomes in neuron-glia communication
Frühbeis, C., Fröhlich, D., & Krämer-Albers, E.-M. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00119 · Cited by 275 · see citing works
Wang, X., Liu, P., Zhu, H., Xu, Y., Ma, C., Dai, X., Huang, L., Liu, Y., Zhang, L., & Qin, C. (2009) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2009.08.006 · Cited by 271 · see citing works
MicroRNA Profiling of CSF Reveals Potential Biomarkers to Detect Alzheimer`s Disease
Denk, J., Boelmans, K., Siegismund, C., Lassner, D., Arlt, S., & Jahn, H. (2015) · PLOS ONE · doi:10.1371/journal.pone.0126423 · Cited by 236 · see citing works
Circulating miRNAs as Potential Biomarkers in Alzheimer's Disease
Galimberti, D., Villa, C., Fenoglio, C., Serpente, M., Ghezzi, L., Cioffi, S. M. G., Arighi, A., Fumagalli, G., & Scarpini, E. (2014) · Journal of Alzheimer’s Disease · doi:10.3233/jad-140756 · Cited by 222 · see citing works
Serotonin stimulates secretion of exosomes from microglia cells
Glebov, K., Löchner, M., Jabs, R., Lau, T., Merkel, O., Schloss, P., Steinhäuser, C., & Walter, J. (2015) · Glia · doi:10.1002/glia.22772 · Cited by 221 · see citing works
Coleman, B. M., & Hill, A. F. (2015) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2015.02.007 · Cited by 208 · see citing works
Reduced expression of hsa-miR-27a-3p in CSF of patients with Alzheimer disease
Sala Frigerio, C., Lau, P., Salta, E., Tournoy, J., Bossers, K., Vandenberghe, R., Wallin, A., Bjerke, M., Zetterberg, H., Blennow, K., et al. (2013) · Neurology · doi:10.1212/01.wnl.0000437306.37850.22 · Cited by 156 · see citing works
Flagged first, then by citations
Research works printed but not linked: 143
- Cicero A Lo, Stahl PD, Raposo G. Extracellular vesicles shuffling intercellular messages: for good or for bad. Curr Opin Cell Biol. 2015;35:69-77.
- Zocco D, Ferruzzi P, Cappello F, Kuo WP, Fais S. Extracellular vesicles as shuttles of tumor biomarkers and anti-tumor drugs. Front Oncol. 2014;4:267.
- Properzi F, Logozzi M, Fais S. Exosomes: the future of biomarkers in medicine. Biomark Med. 2013;7(5):769-78.
- Kalani A, Tyagi A, Tyagi N. Exosomes: mediators of neurodegen- eration, neuroprotection and therapeutics. Mol Neurobiol. 2014;49(1):590-600.
- Aguzzi A, Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron. 2009;64(6):783-90.
- Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the con- fusion between extracellular vesicles. Trends Cell Biol. 2015;25(6):364-72.
- Gasser O, Hess C, Miot S, Deon C, Sanchez J-C, Schifferli JA. Charac- terisation and properties of ectosomes released by human polymorpho- nuclear neutrophils. Exp Cell Res. 2003;285(2):243-57.
- Andaloussi S EL, Mäger I, Breakefield XO, Wood MJA. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013;12(5):347-57.
- Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183(3):1161-72.
- Logozzi M, De Milito A, Lugini L, Borghi M, Calabrò L, Spada M, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PloS One. 2009;4(4):e5219.
- Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9(6):654-9.
- Llorente A, Skotland T, Sylvänne T, Kauhanen D, Róg T, Orłowski A, et al. Molecular lipidomics of exosomes released by PC-3 prostate can- cer cells. Biochim Biophys Acta. 2013;1831(7):1302-9.
- Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319(5867):1244-7.
- Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ, et al. Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun. 2011;2:282.
- Guo BB, Bellingham SA, Hill AF. The neutral sphingomyelinase path- way regulates packaging of the prion protein into exosomes. J Biol Chem. 2015;290(6):3455-67.
- Katzmann DJ, Stefan CJ, Babst M, Emr SD. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J Cell Biol. 2003;162(3):413-23.
- Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature. 2009;458(7237):445-52.
- Kong SMY, Chan BKK, Park J-S, Hill KJ, Aitken JB, Cottle L, et al. Parkinson's disease-linked human PARK9/ATP13A2 maintains zinc Review article: Medical intelligence homeostasis and promotes α-Synuclein externalization via exosomes. Hum Mol Genet. 2014;23(11):2816-33.
- Tsunemi T, Hamada K, Krainc D. ATP13A2/PARK9 regulates secretion of exosomes and α-synuclein. J Neurosci Off J Soc Neurosci. 2014;34(46):15281-7.
- Géminard C, De Gassart A, Blanc L, Vidal M. Degradation of AP2 during reticulocyte maturation enhances binding of hsc70 and Alix to a common site on TFR for sorting into exosomes. Traffic Cph Den. 2004;5(3):181-93.
- Roucourt B, Meeussen S, Bao J, Zimmermann P, David G. Heparanase activates the syndecan-syntenin-ALIX exosome pathway. Cell Res. 2015;25(4):412-28.
- Grey M, Dunning CJ, Gaspar R, Grey C, Brundin P, Sparr E, et al. Acceleration of α-synuclein aggregation by exosomes. J Biol Chem. 2015;290(5):2969-82.
- Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 2009;284(49):34211-22.
- Fang Y, Wu N, Gan X, Yan W, Morrell JC, Gould SJ. Higher-order oli- gomerization targets plasma membrane proteins and HIV gag to exo- somes. PLoS Biol. 2007;5(6):e158.
- Putz U, Howitt J, Lackovic J, Foot N, Kumar S, Silke J, et al. Nedd4 family-interacting protein 1 (Ndfip1) is required for the exosomal se- cretion of Nedd4 family proteins. J Biol Chem. 2008;283(47):32621-7.
- Moreno-Gonzalo O, Villarroya-Beltri C, Sánchez-Madrid F. Post-trans- lational modifications of exosomal proteins. Front Immunol. 2014;5:383.
- Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F, Pérez- Hernández D, Vázquez J, Martin-Cofreces N, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4:2980.
- Guduric-Fuchs J, O'Connor A, Cullen A, Harwood L, Medina RJ, O'Neill CL, et al. Deep sequencing reveals predominant expression of miR-21 amongst the small non-coding RNAs in retinal microvascular endothelial cells. J Cell Biochem. 2012;113(6):2098-111.
- Zhang J, Li S, Li L, Li M, Guo C, Yao J, et al. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics. 2015;13(1):17-24.
- Koles K, Nunnari J, Korkut C, Barria R, Brewer C, Li Y, et al. Mechan- ism of evenness interrupted (Evi)-exosome release at synaptic boutons. J Biol Chem. 2012;287(20):16820-34.
- Korkut C, Li Y, Koles K, Brewer C, Ashley J, Yoshihara M, et al. Regu- lation of postsynaptic retrograde signaling by presynaptic exosome re- lease. Neuron. 2013;77(6):1039-46.
- Mittelbrunn M, Vicente-Manzanares M, Sánchez-Madrid F. Organizing polarized delivery of exosomes at synapses. Traffic Cph Den. 2015;16(4):327-37.
- Lachenal G, Pernet-Gallay K, Chivet M, Hemming FJ, Belly A, Bodon G, et al. Release of exosomes from differentiated neurons and its reg- ulation by synaptic glutamatergic activity. Mol Cell Neurosci. 2011;46(2):409-18.
- Goldie BJ, Dun MD, Lin M, Smith ND, Verrills NM, Dayas CV, et al. Activity-associated miRNA are packaged in Map1b-enriched exo- somes released from depolarized neurons. Nucleic Acids Res. 2014;42(14):9195-208.
- Chivet M, Javalet C, Laulagnier K, Blot B, Hemming FJ, Sadoul R. Exosomes secreted by cortical neurons upon glutamatergic synapse activation specifically interact with neurons. J Extracell Vesicles. 2014;3:24722.
- Kettenmann H, Verkhratsky A. Neuroglia: the 150 years after. Trends Neurosci. 2008;31(12):653-9.
- Smalheiser NR. Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol Direct. 2007;2:35.
- Robinson MB, Tidwell JL, Gould T, Taylor AR, Newbern JM, Graves J, et al. Extracellular heat shock protein 70: a critical component for motoneuron survival. J Neurosci Off J Soc Neurosci. 2005;25(42):9735-45.
- Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M, Milligan CE. Regulation of heat shock protein 70 release in astrocytes: role of signal- ing kinases. Dev Neurobiol. 2007;67(13):1815-29.
- Wang S, Cesca F, Loers G, Schweizer M, Buck F, Benfenati F, et al. 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. J Neurosci Off J Soc Neurosci. 201;31(20):7275-90.
- Krämer-Albers E-M, Bretz N, Tenzer S, Winterstein C, Möbius W, Ber- ger H, et al. Oligodendrocytes secrete exosomes containing major my- elin and stress-protective proteins: Trophic support for axons? Proteo- mics Clin Appl. 2007;1(11):1446-61.
- Bakhti M, Winter C, Simons M. Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles. J Biol Chem. 2011;286(1):787-96.
- Zhao X, He X, Han X, Yu Y, Ye F, Chen Y, et al. MicroRNA-mediated control of oligodendrocyte differentiation. Neuron. 2010;65(5):612-26.
- Ebrahimi-Barough S, Kouchesfahani HM, Ai J, Massumi M. Differenti- ation of human endometrial stromal cells into oligodendrocyte progen- itor cells (OPCs). J Mol Neurosci MN. 2013;51(2):265-73.
- Pusic AD, Kraig RP. Youth and environmental enrichment generate ser- um exosomes containing miR-219 that promote CNS myelination. Glia. 2014;62(2):284-99.
- Gosselin R-D, Meylan P, Decosterd I. Extracellular microvesicles from astrocytes contain functional glutamate transporters: regulation by pro- tein kinase C and cell activation. Front Cell Neurosci. 2013;7:251.
- Morel L, Regan M, Higashimori H, Ng SK, Esau C, Vidensky S, et al. Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1. J Biol Chem. 2013;288(10):7105-16.
- Pelchen-Matthews A, Raposo G, Marsh M. Endosomes, exosomes and Trojan viruses. Trends Microbiol. 2004;12(7):310-6.
- Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, Verkade P, et al. Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci U S A. 2006;103(30):11172-7.
- Gomes C, Keller S, Altevogt P, Costa J. Evidence for secretion of Cu,Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci Lett. 2007;428(1):43-6.
- Nonaka T, Masuda-Suzukake M, Arai T, Hasegawa Y, Akatsu H, Obi T, et al. Prion-like properties of pathological TDP-43 aggregates from diseased brains. Cell Rep. 2013;4(1):124-34.
- Fevrier B, Vilette D, Archer F, Loew D, Faigle W, Vidal M, et al. Cells release prions in association with exosomes. Proc Natl Acad Sci U S A. 2004;101(26):9683-8.
- McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, et al. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol. 1999;46(6):860-6.
- Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med. 2008;14(8):837-42.
- Selkoe DJ. Soluble oligomers of the amyloid beta-protein impair syn- aptic plasticity and behavior. Behav Brain Res. 2008;192(1):106-13.
- Brouillette J, Caillierez R, Zommer N, Alves-Pires C, Benilova I, Blum D, et al. Neurotoxicity and memory deficits induced by soluble low-molecular-weight amyloid-β1-42 oligomers are revealed in vivo by using a novel animal model. J Neurosci Off J Soc Neurosci. 2012;32(23):7852-61.
- Verderio C. Extracellular membrane microvesicles and nanotubes in the brain: understanding their nature, their function in cell-to-cell commu- nication, their role in transcellular spreading of pathological agents and their therapeutic potential. Front Physiol. 2013;4:163.
- Joshi P, Turola E, Ruiz A, Bergami A, Libera DD, Benussi L, et al. Mi- croglia convert aggregated amyloid-β into neurotoxic forms through the shedding of microvesicles. Cell Death Differ. 2014;21(4):582-93.
- Nielsen HM, Mulder SD, Beliën JAM, Musters RJP, Eikelenboom P, Veerhuis R. Astrocytic A beta 1-42 uptake is determined by A beta-ag- gregation state and the presence of amyloid-associated proteins. Glia. 2010;58(10):1235-46.
- Agosta F, Dalla Libera D, Spinelli EG, Finardi A, Canu E, Bergami A, et al. Myeloid microvesicles in cerebrospinal fluid are associated with myelin damage and neuronal loss in mild cognitive impairment and Alzheimer disease. Ann Neurol. 2014;76(6):813-25.
- Marsh M, van Meer G. Cell biology. No ESCRTs for exosomes. Science. 2008;319(5867):1191-2.
- Yuyama K, Sun H, Mitsutake S, Igarashi Y. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-β by microglia. J Bi- ol Chem. 2012;287(14):10977-89.
- Yuyama K, Sun H, Sakai S, Mitsutake S, Okada M, Tahara H, et al. Decreased amyloid-β pathologies by intracerebral loading of glycosphingolipid-enriched exosomes in Alzheimer model mice. J Biol Chem. 2014;289(35):24488-98.
- Dinkins MB, Dasgupta S, Wang G, Zhu G, Bieberich E. Exosome re- duction in vivo is associated with lower amyloid plaque load in the 5XFAD mouse model of Alzheimer's disease. Neurobiol Aging. 2014;35(8):1792-800.
- Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010;73(10):1907-20.
- Coleman BM, Hanssen E, Lawson VA, Hill AF. Prion-infected cells regulate the release of exosomes with distinct ultrastructural features. FASEB J Off Publ Fed Am Soc Exp Biol. 2012;26(10):4160-73.
- Alais S, Simoes S, Baas D, Lehmann S, Raposo G, Darlix JL, et al. Mouse neuroblastoma cells release prion infectivity associated with exosomal vesicles. Biol Cell Auspices Eur Cell Biol Organ. 2008;100(10):603-15.
- Rajendran L, Bali J, Barr MM, Court FA, Krämer-Albers E-M, Picou F, et al. Emerging roles of extracellular vesicles in the nervous system. J Neurosci Off J Soc Neurosci. 2014;34(46):15482-9.
- Sharples RA, Vella LJ, Nisbet RM, Naylor R, Perez K, Barnham KJ, et al. Inhibition of gamma-secretase causes increased secretion of amyloid precursor protein C-terminal fragments in association with exosomes. FASEB J Off Publ Fed Am Soc Exp Biol. 2008;22(5):1469-78.
- An K, Klyubin I, Kim Y, Jung JH, Mably AJ, O'Dowd ST, et al. Exo- somes neutralize synaptic-plasticity-disrupting activity of Aβ assem- blies in vivo. Mol Brain. 2013;6:47.
- Yuyama K, Sun H, Usuki S, Sakai S, Hanamatsu H, Mioka T, et al. A potential function for neuronal exosomes: sequestering intracerebral amyloid-β peptide. FEBS Lett. 2015;589(1):84-8.
- Alvarez-Erviti L, Seow Y, Schapira AH, Gardiner C, Sargent IL, Wood MJA, et al. Lysosomal dysfunction increases exosome-mediated alpha- synuclein release and transmission. Neurobiol Dis. 2011;42(3):360-7.
- Desplats P, Lee H-J, Bae E-J, Patrick C, Rockenstein E, Crews L, et al. Inclusion formation and neuronal cell death through neuron-to- neuron transmission of alpha-synuclein. Proc Natl Acad Sci U S A. 2009;106(31):13010-5.
- Bellingham SA, Coleman BM, Hill AF. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion- infected neuronal cells. Nucleic Acids Res. 2012;40(21):10937-49.
- Simón D, García-García E, Gómez-Ramos A, Falcón-Pérez JM, Díaz- Hernández M, Hernández F, et al. Tau overexpression results in its se- cretion via membrane vesicles. Neurodegener Dis. 2012;10(1-4):73-5.
- Danzer KM, Kranich LR, Ruf WP, Cagsal-Getkin O, Winslow AR, Zhu L, et al. Exosomal cell-to-cell transmission of alpha synuclein oli- gomers. Mol Neurodegener. 2012;7:42.
- Sonnino S, Aureli M, Grassi S, Mauri L, Prioni S, Prinetti A. Lipid rafts in neurodegeneration and neuroprotection. Mol Neurobiol. 2014;50(1):130-48.
- Taylor DR, Hooper NM. The prion protein and lipid rafts. Mol Membr Biol. 2006;23(1):89-99.
- Baron GS, Wehrly K, Dorward DW, Chesebro B, Caughey B. Con- version of raft associated prion protein to the protease-resistant state requires insertion of PrP-res (PrP(Sc)) into contiguous membranes. EMBO J. 2002;21(5):1031-40.
- Wang F, Wang X, Ma J. Conversion of bacterially expressed recombin- ant prion protein. Methods San Diego Calif. 2011;53(3):208-13.
- Supattapone S. Synthesis of high titer infectious prions with cofactor molecules. J Biol Chem. 2014;289(29):19850-4.
- Grimm MOW, Grimm HS, Pätzold AJ, Zinser EG, Halonen R, Duering M, et al. Regulation of cholesterol and sphingomyelin metabolism by amyloid-beta and presenilin. Nat Cell Biol. 2005;7(11):1118-23.
- Matsuzaki K, Kato K, Yanagisawa K. Abeta polymerization through interaction with membrane gangliosides. Biochim Biophys Acta. 2010;1801(8):868-77.
- Goetzl EJ, Boxer A, Schwartz JB, Abner EL, Petersen RC, Miller BL, et al. Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease. Neurology. 2015;85(1):40-7.
- Patel N, Hoang D, Miller N, Ansaloni S, Huang Q, Rogers JT, et al. MicroRNAs can regulate human APP levels. Mol Neurodegener. 2008;3:10. 102
- Hébert SS, Horré K, Nicolaï L, Bergmans B, Papadopoulou AS, Delacourte A, et al. MicroRNA regulation of Alzheimer's Amyloid precursor protein expression. Neurobiol Dis. 2009;33(3):422-8. 103
- Absalon S, Kochanek DM, Raghavan V, Krichevsky AM. MiR-26b, upregulated in Alzheimer's disease, activates cell cycle entry, tau- phosphorylation, and apoptosis in postmitotic neurons. J Neurosci Off J Soc Neurosci. 2013;33(37):14645-59. 104
- Jayadev S, Case A, Alajajian B, Eastman AJ, Möller T, Garden GA. Presenilin 2 influences miR146 level and activity in microglia. J Neurochem. 2013;127(5):592-9. 105
- Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, et al. A MicroRNA feedback circuit in midbrain dopamine neurons. Science. 2007;317(5842):1220-4. 106
- Junn E, Lee K-W, Jeong BS, Chan TW, Im J-Y, Mouradian MM. Re- pression of alpha-synuclein expression and toxicity by microRNA-7. Proc Natl Acad Sci U S A. 2009;106(31):13052-7. 107
- Cho HJ, Liu G, Jin SM, Parisiadou L, Xie C, Yu J, et al. Mi- croRNA-205 regulates the expression of Parkinson's disease-related leucine-rich repeat kinase 2 protein. Hum Mol Genet. 2013;22(3):608-20. 108
- Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, et al. MicroRNAs bind to Toll-like receptors to induce prometastatic in- flammatory response. Proc Natl Acad Sci U S A. 2012;109(31):E2110-6. 109
- Simoneau S, Thomzig A, Ruchoux M-M, Vignier N, Daus ML, Po- leggi A, et al. Synthetic scrapie infectivity: interaction between re- combinant PrP and scrapie brain-derived RNA. Virulence. 2015;6(2):132-44. 110
- Ajroud-Driss S, Siddique T. Sporadic and hereditary amyotrophic lat- eral sclerosis (ALS). Biochim Biophys Acta. 2015;1852(4):679-84. 111
- Grad LI, Yerbury JJ, Turner BJ, Guest WC, Pokrishevsky E, O'Neill MA, et al. Intercellular propagated misfolding of wild-type Cu/Zn su- peroxide dismutase occurs via exosome-dependent and -independent mechanisms. Proc Natl Acad Sci U S A. 2014;111(9):3620-5. 113
- Paez-Colasante X, Figueroa-Romero C, Sakowski SA, Goutman SA, Feldman EL. Amyotrophic lateral sclerosis: mechanisms and thera- peutics in the epigenomic era. Nat Rev Neurol. 2015;11(5):266-79. 114
- Campos-Melo D, Droppelmann CA, He Z, Volkening K, Strong MJ. Altered microRNA expression profile in amyotrophic lateral scleros- is: a role in the regulation of NFL mRNA levels. Mol Brain. 2013;6:26. 115
- Parisi C, Arisi I, D'Ambrosi N, Storti AE, Brandi R, D'Onofrio M, et al. Dysregulated microRNAs in amyotrophic lateral sclerosis mi- croglia modulate genes linked to neuroinflammation. Cell Death Dis. 2013;4:e959. 116
- Freischmidt A, Müller K, Ludolph AC, Weishaupt JH. Systemic dys- regulation of TDP-43 binding microRNAs in amyotrophic lateral sclerosis. Acta Neuropathol Commun. 2013;1(1):42. 117
- Williams AH, Valdez G, Moresi V, Qi X, McAnally J, Elliott JL, et al. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science. 2009;326(5959):1549-54. 118
- Toivonen JM, Manzano R, Oliván S, Zaragoza P, García-Redondo A, Osta R. MicroRNA-206: a potential circulating biomarker candidate for amyotrophic lateral sclerosis. PloS One. 2014;9(2):e89065. 119
- Greco S, Perfetti A, Fasanaro P, Cardani R, Capogrossi MC, Meola G, et al. Deregulated microRNAs in myotonic dystrophy type 2. PloS One. 2012;7(6):e39732. 120
- Kong Y, Wu J, Yuan L. MicroRNA expression analysis of adult-onset Drosophila Alzheimer's disease model. Curr Alzheimer Res. 2014;11(9):882-91. 122
- Sethi P, Lukiw WJ. Micro-RNA abundance and stability in human brain: specific alterations in Alzheimer's disease temporal lobe neo- cortex. Neurosci Lett. 2009;459(2):100-4. 123
- Lukiw WJ. Micro-RNA speciation in fetal, adult and Alzheimer's dis- ease hippocampus. Neuroreport. 2007;18(3):297-300. 124
- Shioya M, Obayashi S, Tabunoki H, Arima K, Saito Y, Ishida T, et al. Aberrant microRNA expression in the brains of neurodegenerative diseases: miR-29a decreased in Alzheimer disease brains targets neur- one navigator 3. Neuropathol Appl Neurobiol. 2010;36(4):320-30. 130
- Hébert SS, Horré K, Nicolaï L, Papadopoulou AS, Mandemakers W, Silahtaroglu AN, et al. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta- secretase expression. Proc Natl Acad Sci U S A. 2008;105(17):6415-20. 131
- Kiko T, Nakagawa K, Tsuduki T, Furukawa K, Arai H, Miyazawa T. MicroRNAs in plasma and cerebrospinal fluid as potential markers for Alzheimer's disease. J Alzheimers Dis JAD. 2014;39(2):253-9. 132
- Lei X, Lei L, Zhang Z, Zhang Z, Cheng Y. Downregulated miR-29c correlates with increased BACE1 expression in sporadic Alzheimer's disease. Int J Clin Exp Pathol. 2015;8(2):1565-74. 133
- Schipper HM, Maes OC, Chertkow HM, Wang E. MicroRNA expres- sion in Alzheimer blood mononuclear cells. Gene Regul Syst Biol. 2007;1:263-74. 135
- Bhatnagar S, Chertkow H, Schipper HM, Yuan Z, Shetty V, Jenkins S, et al. Increased microRNA-34c abundance in Alzheimer's disease cir- culating blood plasma. Front Mol Neurosci. 2014;7:2. 136
- Zovoilis A, Agbemenyah HY, Agis-Balboa RC, Stilling RM, Edbauer D, Rao P, et al. microRNA-34c is a novel target to treat dementias. EMBO J. 2011;30(20):4299-308. 137
- Liu QY, Chang MNV, Lei JX, Koukiekolo R, Smith B, Zhang D, et al. Identification of microRNAs involved in Alzheimer's progression us- ing a rabbit model of the disease. Am J Neurodegener Dis. 2014;3(1):33-44. 138
- Nelson PT, Wang W-X. MiR-107 is reduced in Alzheimer's disease brain neocortex: validation study. J Alzheimers Dis JAD. 2010;21(1):75-9. 140
- Müller M, Kuiperij HB, Claassen JA, Küsters B, Verbeek MM. Mi- croRNAs in Alzheimer's disease: differential expression in hippo- campus and cell-free cerebrospinal fluid. Neurobiol Aging. 2014;35(1):152-8. 141
- Tan L, Yu J-T, Liu Q-Y, Tan M-S, Zhang W, Hu N, et al. Circulating miR-125b as a biomarker of Alzheimer's disease. J Neurol Sci. 2014;336(1-2):52-6. 142
- Culpan D, Kehoe PG, Love S. Tumour necrosis factor-α (TNF-α) and miRNA expression in frontal and temporal neocortex in Alzheimer's disease and the effect of TNF-α on miRNA expression in vitro. Int J Mol Epidemiol Genet. 2011;2(2):156-62. 143
- Liang C, Zhu H, Xu Y, Huang L, Ma C, Deng W, et al. Mi- croRNA-153 negatively regulates the expression of amyloid precurs- or protein and amyloid precursor-like protein 2. Brain Res. 2012;1455:103-13. 145
- Rodriguez-Ortiz CJ, Baglietto-Vargas D, Martinez-Coria H, LaFerla FM, Kitazawa M. Upregulation of miR-181 decreases c-Fos and SIRT-1 in the hippocampus of 3xTg-AD mice. J Alzheimers Dis JAD. 2014;42(4):1229-38. 146
- Schonrock N, Humphreys DT, Preiss T, Götz J. Target gene repression mediated by miRNAs miR-181c and miR-9 both of which are down- regulated by amyloid-β. J Mol Neurosci MN. 2012;46(2):324-35. 147
- Tian N, Cao Z, Zhang Y. MiR-206 decreases brain-derived neuro- trophic factor levels in a transgenic mouse model of Alzheimer's dis- ease. Neurosci Bull. 2014;30(2):191-7. 148
- Lee S-T, Chu K, Jung K-H, Kim JH, Huh J-Y, Yoon H, et al. miR-206 regulates brain-derived neurotrophic factor in Alzheimer disease model. Ann Neurol. 2012;72(2):269-77. 149
- Santa-Maria I, Alaniz ME, Renwick N, Cela C, Fulga TA, Van Vactor D, et al. Dysregulation of microRNA-219 promotes neurodegenera- tion through post-transcriptional regulation of tau. J Clin Invest. 2015;125(2):681-6. 150
- Villa C, Fenoglio C, De Riz M, Clerici F, Marcone A, Benussi L, et al. Role of hnRNP-A1 and miR-590-3p in neuronal death: genetics and expression analysis in patients with Alzheimer disease and frontotem- poral lobar degeneration. Rejuvenation Res. 2011;14(3):275-81. 151
- Margis R, Margis R, Rieder CRM. Identification of blood mi- croRNAs associated to Parkinsonĭs disease. J Biotechnol. 2011;152(3):96-101. 152
- Vallelunga A, Ragusa M, Di Mauro S, Iannitti T, Pilleri M, Biundo R, et al. Identification of circulating microRNAs for the differential dia- gnosis of Parkinson's disease and Multiple System Atrophy. Front Cell Neurosci. 2014;8:156. 153
- Miñones-Moyano E, Porta S, Escaramís G, Rabionet R, Iraola S, Kagerbauer B, et al. MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum Mol Genet. 2011;20(15):3067-78. 154
- Asikainen S, Rudgalvyte M, Heikkinen L, Louhiranta K, Lakso M, Wong G, et al. Global microRNA expression profiling of Caenorhab- ditis elegans Parkinson's disease models. J Mol Neurosci MN. 2010;41(1):210-8. 155
- Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, et al. A MicroRNA feedback circuit in midbrain dopamine neurons. Science. 2007;317(5842):1220-4. 156
- Cardo LF, Coto E, de Mena L, Ribacoba R, Moris G, Menéndez M, et al. Profile of microRNAs in the plasma of Parkinson's disease patients and healthy controls. J Neurol. 2013;260(5):1420-2. 157
- Khoo SK, Petillo D, Kang UJ, Resau JH, Berryhill B, Linder J, et al. Plasma-based circulating MicroRNA biomarkers for Parkinson's dis- ease. J Park Dis. 2012;2(4):321-31. 158
- Saba R, Goodman CD, Huzarewich RLCH, Robertson C, Booth SA. A miRNA signature of prion induced neurodegeneration. PloS One. 2008;3(11):e3652. 159 Majer A, Booth SA. Microdissection and transcriptional profiling: a window into the pathobiology of preclinical prion disease. Prion. 201;8(1):67-74. 160
- Lukiw WJ, Dua P, Pogue AI, Eicken C, Hill JM. Upregulation of mi- cro RNA-146a (miRNA-146a), a marker for inflammatory neurode- generation, in sporadic Creutzfeldt-Jakob disease (sCJD) and Gerstmann-Straussler-Scheinker (GSS) syndrome. J Toxicol Environ Health A. 2011;74(22-24):1460-8. 161
- Majer A, Medina SJ, Niu Y, Abrenica B, Manguiat KJ, Frost KL, et al. Early mechanisms of pathobiology are revealed by transcriptional temporal dynamics in hippocampal CA1 neurons of prion infected mice. PLoS Pathog. 2012;8(11):e1003002. 162
- Montag J, Hitt R, Opitz L, Schulz-Schaeffer WJ, Hunsmann G, Motzkus D. Upregulation of miRNA hsa-miR-342-3p in experimental and idiopathic prion disease. Mol Neurodegener. 2009;4:36. 163
- Montag J, Brameier M, Schmädicke A-C, Gilch S, Schätzl HM, Motzkus D. A genome-wide survey for prion-regulated miRNAs as- sociated with cholesterol homeostasis. BMC Genomics. 2012;13:486. 164
- Zhou F, Guan Y, Chen Y, Zhang C, Yu L, Gao H, et al. miRNA-9 ex- pression is upregulated in the spinal cord of G93A-SOD1 transgenic mice. Int J Clin Exp Pathol. 2013;6(9):1826-38. 165
- Marcuzzo S, Bonanno S, Kapetis D, Barzago C, Cavalcante P, D'Alessandro S, et al. Up-regulation of neural and cell cycle-related microRNAs in brain of amyotrophic lateral sclerosis mice at late dis- ease stage. Mol Brain. 2015;8(1):5. 166
- Zhang Z, Almeida S, Lu Y, Nishimura AL, Peng L, Sun D, et al. Downregulation of microRNA-9 in iPSC-derived neurons of FTD/ ALS patients with TDP-43 mutations. PloS One. 2013;8(10):e76055. 167
- Russell AP, Wada S, Vergani L, Hock MB, Lamon S, Léger B, et al. Disruption of skeletal muscle mitochondrial network genes and miRNAs in amyotrophic lateral sclerosis. Neurobiol Dis. 2013;49:107-17. 168
- Nolan K, Mitchem MR, Jimenez-Mateos EM, Henshall DC, Concan- non CG, Prehn JHM. Increased expression of microRNA-29a in ALS mice: functional analysis of its inhibition. J Mol Neurosci MN. 2014;53(2):231-41. 169
- De Felice B, Annunziata A, Fiorentino G, Borra M, Biffali E, Coppola C, et al. miR-338-3p is over-expressed in blood, CFS, serum and spin- al cord from sporadic amyotrophic lateral sclerosis patients. Neuro- genetics. 2014;15(4):243-53. 173
- De Felice B, Guida M, Guida M, Coppola C, De Mieri G, Cotrufo R. A miRNA signature in leukocytes from sporadic amyotrophic lateral sclerosis. Gene. 2012;508(1):35-40. Review article: Medical intelligence
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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
Ananbeh, H., Novak, J., Juhas, S., Juhasova, J., Klempir, J., Doleckova, K., Rysankova, I., Turnovcova, K., Hanus, J., Hansikova, H., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105598 · Cited by 46 · see citing works
- Authors
- Properzi, F., Ferroni, E., Poleggi, A., & Vinci, R.
- Venue
- Swiss Medical Weekly
- Publisher
- SMW Supporting Association
- Published
- 2015-11-01
- Volume
- 145
- Issue
- 4546
- Pages
- w14204
- ISSN
- 1424-3997
- Cited by
- 30
- References
- 18
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