MicroRNA-101 Modulates Autophagy and Oligodendroglial Alpha-Synuclein Accumulation in Multiple System Atrophy
Open accessAbstract
Synucleinopathies, neurodegenerative disorders with alpha-synuclein (α-syn) accumulation, are the second leading cause of neurodegeneration in the elderly, however no effective disease-modifying alternatives exist for these diseases. Multiple system atrophy (MSA) is a fatal synucleinopathy characterized by the accumulation of toxic aggregates of α-syn within oligodendroglial cells, leading to demyelination and neurodegeneration, and the reduction of this accumulation might halt the fast progression of MSA. In this sense, the involvement of microRNAs (miRNAs) in synucleinopathies is yet poorly understood, and the potential of manipulating miRNA levels as a therapeutic tool is underexplored. In this study, we analyzed the levels of miRNAs that regulate the expression of autophagy genes in MSA cases, and investigated the mechanistic correlates of miRNA dysregulation in in vitro models of synucleinopathy. We found that microRNA-101 (miR-101) was significantly increased in the striatum of MSA patients, together with a reduction in the expression of its predicted target gene RAB5A. Overexpression of miR-101 in oligodendroglial cell cultures resulted in a significant increase in α-syn accumulation, along with autophagy deficits. Opposite results were observed upon expression of an antisense construct targeting miR-101. Stereotaxic delivery of a lentiviral construct expressing anti-miR-101 into the striatum of the MBP-α-syn transgenic mouse model of MSA resulted in reduced oligodendroglial α-syn accumulation and improved autophagy. These results suggest that miRNA dysregulation contributes to MSA pathology, with miR-101 alterations potentially mediating autophagy impairments. Therefore, therapies targeting miR-101 may represent promising approaches for MSA and related neuropathologies with autophagy dysfunction.
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Autophagy is regulated by distinct mechanisms in different cell types, and these cell type-specific mechanisms underlie the differential vulnerability of separate tissues to autophagy mutations, resulting in heterogeneous manifestations of disease.
“Furthermore, mounting evidence shows that autophagy is regulated by distinct mechanisms in different cell types [11–26], and these cell type-specific mechanisms underlie the differential vulnerability of separate tissues to autophagy mutations, resulting in heterogenous manifestations of disease.”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [12]
In multiple system atrophy, the pathologic hallmark consists of cytoplasmic SNCA inclusions in oligodendrocytes.
“In multiple system atrophy (MSA), the pathologic hallmark consists of cytoplasmic SNCA inclusions in oligodendrocytes [12],”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [12]
Accumulation of SNCA inclusions in oligodendrocytes is exacerbated by autophagy inhibition, either pharmacologically with chloroquine or genetically by MIR101 overexpression.
“and the accumulation of these inclusions is exacerbated by autophagy inhibition, either pharmacologically with chloroquine or genetically by MIR101 overexpression [12,450,454].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [12]
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2 retracted
Masliah, E., Rockenstein, E. M., Mante, M., Crews, L. A., Spencer, B. J., Adame, A., Patrick, C., Trejo, M., Ubhi, K. K., Rohn, T. T., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019338 · Cited by 422 · see citing works
Self-citationRetractedCrews, L. A., Spencer, B. J., Desplats, P., Patrick, C., Paulino, A., Rockenstein, E. M., Hansen, L. A., Adame, A., Galasko, D. R., & Masliah, E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009313 · Cited by 369 · see citing works
Self-citationRetractedGuidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894 · see citing works
Second consensus statement on the diagnosis of multiple system atrophy
Gilman, S., Wenning, G. K., Low, P. A., Brooks, D. J., Mathias, C. J., Trojanowski, J. Q., Wood, N. W., Colosimo, C., Dürr, A., Fowler, C. J., et al. (2008) · Neurology · doi:10.1212/01.wnl.0000324625.00404.15 · Cited by 3,140 · see citing works
Impaired Degradation of Mutant α-Synuclein by Chaperone-Mediated Autophagy
Cuervo, A. M., Stefanis, L., Fredenburg, R., Lansbury, P. T., & Sulzer, D. (2004) · Science · doi:10.1126/science.1101738 · Cited by 2,024 · cited 3× · see citing works
“…aggregates and organelles in the central nervous system (CNS; Wong and Cuervo, 2010), and it is affected in most diseases that show toxic accumulation of proteins, such as Alzheimer’s disease (AD; Pickford et al., 2008), PD (Cuervo et al., 2004; Crews et al., 2010) and DLB (Crews et al., 2010).”
BackgroundComprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites
Betel, D., Koppal, A., Agius, P., Sander, C., & Leslie, C. (2010) · Genome Biology · doi:10.1186/gb-2010-11-8-r90 · Cited by 1,592 · see citing works
Inclusion formation and neuronal cell death through neuron-to-neuron transmission of α-synuclein
Desplats, P., Lee, H.-J., Bae, E.-J., Patrick, C., Rockenstein, E., Crews, L., Spencer, B., Masliah, E., & Lee, S.-J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903691106 · Cited by 1,485 · see citing works
Self-citationHuman Experimentation: Code of Ethics of W.M.A
RICKHAM, P. P. (1964) · BMJ · doi:10.1136/bmj.2.5402.177 · Cited by 1,457 · see citing works
Pickford, F., Masliah, E., Britschgi, M., Lucin, K. M., Narasimhan, R., Jaeger, P. A., Small, S. A., Spencer, B. J., Rockenstein, E. M., Levine, B., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33585 · Cited by 1,072 · see citing works
Self-citationProduction and purification of lentiviral vectors
Tiscórnia, G., Singer, O., & Verma, I. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.37 · Cited by 974 · see citing works
Autophagy gone awry in neurodegenerative diseases
Wong, E. S. P., & Cuervo, A. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2575 · Cited by 883 · see citing works
Clinical features and natural history of multiple system atrophy
Wenning, G. K., Ben‐Shlomo, Y., Magalhães, M., Danie, S. E., & Quinn, N. P. (1994) · Brain · doi:10.1093/brain/117.4.835 · Cited by 788 · see citing works
Peltier, H. J., & Latham, G. J. (2008) · RNA · doi:10.1261/rna.939908 · Cited by 716 · see citing works
Clonal cell lines from the rat central nervous system
Schubert, D. A., Heinemann, S. F., Carlisle, W., Tarikas, H., Kimes, B. W., Patrick, J. W., Steinbach, J. H., Culp, W., & Brandt, B. L. (1974) · Nature · doi:10.1038/249224a0 · Cited by 713 · see citing works
Evidence for α-synuclein prions causing multiple system atrophy in humans with parkinsonism
Prusiner, S. B., Woerman, A. L., Mordes, D. A., Watts, J. C., Rampersaud, R., Berry, D. B., Patel, S. S., Oehler, A., Lowe, J. K., Kravitz, S. N., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514475112 · Cited by 679 · see citing works
Spencer, B., Potkar, R., Trejo, M., Rockenstein, E., Patrick, C., Gindi, R., Adame, A., Wyss-Coray, T., & Masliah, E. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4390-09.2009 · Cited by 595 · see citing works
Self-citationThe return of the nucleus: transcriptional and epigenetic control of autophagy
Füllgrabe, J., Klionsky, D. J., & Joseph, B. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3716 · Cited by 463 · see citing works
Beach, T. G., Adler, C. H., Sue, L. I., Serrano, G., Shill, H. A., Walker, D. G., Lue, L., Roher, A. E., Dugger, B. N., Maarouf, C., et al. (2015) · Neuropathology · doi:10.1111/neup.12189 · Cited by 460 · see citing works
Self-citationThe Role of Autophagy in Parkinson's DiseasePreprint
Lynch-Day, M. A., Mao, K., Wang, K., Zhao, M., & Klionsky, D. J. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a009357 · Cited by 459 · see citing works
Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells
Hua Zhu, C., Wu, H., Liu, X., Li, B., Chen, Y., Ren, X., Liu, C., & Yang, J. (2009) · Autophagy · doi:10.4161/auto.9064 · Cited by 457 · see citing works
Louis, J., Magal, E., Muir, D., Manthorpe, M., & Varon, S. S. (1992) · Journal of Neuroscience Research · doi:10.1002/jnr.490310125 · Cited by 414 · see citing works
The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila
Liu, N., Landreh, M., Cao, K., Abe, M., Hendriks, G., Kennerdell, J. R., Zhu, Y., Wang, L., & Bonini, N. M. (2012) · Nature · doi:10.1038/nature10810 · Cited by 394 · see citing works
Parkinson's Disease and Alpha Synuclein: Is Parkinson's Disease a Prion‐Like Disorder?
Olanow, C. W., & Brundin, P. (2013) · Movement Disorders · doi:10.1002/mds.25373 · Cited by 392 · see citing works
microRNA‐101 is a potent inhibitor of autophagy
Frankel, L. B., Wen, J., Lees, M. J., Høyer-Hansen, M. H., Farkas, T., Krogh, A., Jäättelä, M., & Lund, A. H. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.331 · Cited by 343 · see citing works
Neuropathological spectrum of synucleinopathies
Jellinger, K. A. (2003) · Movement Disorders · doi:10.1002/mds.10557 · Cited by 338 · see citing works
MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer’s disease
Banzhaf‐Strathmann, J., Benito, E., May, S., Arzberger, T., Tahirovic, S., Kretzschmar, H., Fischer, A., & Edbauer, D. (2014) · The EMBO Journal · doi:10.15252/embj.201387576 · Cited by 326 · see citing works
Multiple system atrophy: A primary oligodendrogliopathy
Wenning, G. K., Stefanova, N., Jellinger, K. A., Poewe, W. H., & Schlossmacher, M. G. (2008) · Annals of Neurology · doi:10.1002/ana.21465 · Cited by 320 · see citing works
Cell-to-cell transmission of non-prion protein aggregates
Lee, S., Desplats, P., Sigurdson, C. J., Tsigelny, I. F., & Masliah, E. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2010.145 · Cited by 307 · see citing works
Self-citationWidespread Alterations of α-Synuclein in Multiple System Atrophy
Dickson, D. W., Liu, W.-K., Hardy, J., Farrer, M. J., Mehta, N. D., Uitti, R. J., Mark, M. H., Zimmerman, T., Golbe, L. I., Sage, J., et al. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65226-1 · Cited by 298 · see citing works
Altered microRNA regulation in Huntington's disease models
Lee, S., Chu, K., Im, W., Yoon, H., Im, J.-Y., Park, J.-E., Park, K.-H., Jung, K., Lee, S. K., Kim, M., et al. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.10.012 · Cited by 289 · see citing works
Alpha‐synuclein transfers from neurons to oligodendrocytes
Reyes, J. F., Rey, N. L., Bousset, L., Melki, R., Brundin, P., & Angot, É. (2013) · Glia · doi:10.1002/glia.22611 · Cited by 278 · see citing works
The emerging role of microRNAs in Alzheimer's disease
Femminella, G. D., Ferrara, N., & Rengo, G. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00040 · Cited by 270 · see citing works
MicroRNA regulation of autophagy
Frankel, L. B., & Lund, A. H. (2012) · Carcinogenesis · doi:10.1093/carcin/bgs266 · Cited by 255 · see citing works
Shults, C. W., Rockenstein, E., Crews, L., Adame, A., Mante, M., Larrea, G., Hashimoto, M., Song, D., Iwatsubo, T., Tsuboi, K., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3527-05.2005 · Cited by 254 · see citing works
Self-citationPathological alpha-synuclein propagates through neural networks
Masuda‐Suzukake, M., Nonaka, T., Hosokawa, M., Kubo, M., Shimozawa, A., Akiyama, H., & Hasegawa, M. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0088-8 · Cited by 249 · see citing works
Mellios, N., Huang, H.-S., Grigorenko, A., Rogaev, E., & Akbarian, S. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn201 · Cited by 239 · see citing works
MicroRNA-101 Regulates Amyloid Precursor Protein Expression in Hippocampal Neurons
Vilardo, E., Barbato, C., Ciotti, M., Cogoni, C., & Ruberti, F. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.112664 · Cited by 238 · 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
Ghaemi, M. (2002) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.73.5.517 · Cited by 224 · see citing works
An updated role of microRNA-124 in central nervous system disorders: a review
Sun, Y., Luo, Z.-M., Guo, X.-M., Su, D.-F., & Liu, X. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00193 · Cited by 223 · see citing works
Stefanova, N., Reindl, M., Neumann, M., Kahle, P. J., Poewe, W. H., & Wenning, G. K. (2007) · Movement Disorders · doi:10.1002/mds.21671 · Cited by 217 · see citing works
Genome-Wide Serum microRNA Expression Profiling Identifies Serum Biomarkers for Alzheimer's Disease
Tan, L., Yu, J.-T., Tan, M.-S., Liu, Q.-Y., Wang, H.-F., Zhang, W., Jiang, T., & Tan, L. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-132144 · Cited by 215 · see citing works
Fang, M., Wang, J., Zhang, X., Geng, Y., Hu, Z., Rudd, J. A., Ling, S., Chen, W., & Han, S. (2011) · Toxicology Letters · doi:10.1016/j.toxlet.2011.11.032 · Cited by 215 · see citing works
Multiple System Atrophy: A Sporadic Synucleinopathy
Dickson, D. W., Lin, W.-L., Liu, W.-K., & Yen, S.-H. C. (1999) · Brain Pathology · doi:10.1111/j.1750-3639.1999.tb00553.x · Cited by 210 · see citing works
Alvarez‐Erviti, L., Seow, Y., Schapira, A. H. V., Rodríguez‐Oroz, M., Obeso, J. A., & Cooper, J. A. D. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.73 · Cited by 204 · see citing works
Tong, J., Wong, H., Guttman, M., Ang, L. C., Forno, L. S., Shimadzu, M., Rajput, A. H., Muenter, M. D., Kish, S. J., Hornykiewicz, O., et al. (2009) · Brain · doi:10.1093/brain/awp282 · Cited by 204 · see citing works
Autophagic failure promotes the exocytosis and intercellular transfer of α-synuclein
Lee, H.-J., Cho, E.-D., Lee, K., Kim, J., Cho, S., & Lee, S. (2013) · Experimental & Molecular Medicine · doi:10.1038/emm.2013.45 · Cited by 199 · see citing works
Yu, Y. H., Yang, L., Zhao, M., Zhu, S., Kang, R., Vernon, P. J., Tang, D., & Cao, L. (2012) · Leukemia · doi:10.1038/leu.2012.65 · Cited by 198 · see citing works
Plasma-Based Circulating MicroRNA Biomarkers for Parkinson's Disease
Khoo, S. K., Petillo, D., Kang, U. J., Resau, J. H., Berryhill, B., Linder, J., Forsgren, L., Neuman, L. A., & Tan, A. C. (2012) · Journal of Parkinson s Disease · doi:10.3233/jpd-012144 · Cited by 198 · see citing works
Alpha‐synuclein mRNA expression in oligodendrocytes in MSA
Asi, Y. T., Simpson, J. E., Heath, P. R., Wharton, S. B., Lees, A. J., Révész, T., Houlden, H., & Holton, J. L. (2014) · Glia · doi:10.1002/glia.22653 · Cited by 191 · see citing works
Lin, H., Dai, T., Xiong, H., Zhao, X., Chen, X., Yu, C., Li, J., Wang, X., & Song, L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015797 · Cited by 184 · see citing works
Neuropathology of multiple system atrophy: New thoughts about pathogenesis
Jellinger, K. A. (2014) · Movement Disorders · doi:10.1002/mds.26052 · Cited by 181 · see citing works
Vallelunga, A., Ragusa, M., Mauro, S. D., Iannitti, T., Pilleri, M., Biundo, R., Weis, L., Pietro, C. D., Iuliis, A. D., Nicoletti, A. S. Q., et al. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00156 · Cited by 175 · see citing works
Inhibition of miR‐34b and miR‐34c enhances α‐synuclein expression in Parkinson's disease
Kabaria, S., Choi, D. C., Chaudhuri, A. D., Mouradian, M. M., & Junn, E. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.12.014 · Cited by 173 · see citing works
Xu, Y.-H., An, Y., Wang, Y., Zhang, C., Zhang, H., Huang, C., Jiang, H., Wang, X., & Li, X. (2013) · Oncology Reports · doi:10.3892/or.2013.2338 · Cited by 169 · see citing works
microRNA Profiles in Parkinson's Disease Prefrontal Cortex
Hoss, A. G., Labadorf, A., Beach, T. G., Latourelle, J. C., & Myers, R. H. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00036 · Cited by 168 · see citing works
Self-citationStatins reduce neuronal α‐synuclein aggregation in in vitro models of Parkinson’s disease
Bar‐On, P., Crews, L. A., Koob, A. O., Mizuno, H., Adame, A., Spencer, B. J., & Masliah, E. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05254.x · Cited by 166 · see citing works
Self-citationMultiple system atrophy: a clinical and neuropathological perspective
Ubhi, K. K., Low, P. A., & Masliah, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.08.003 · Cited by 159 · see citing works
Self-citationMiR-34 modulates Caenorhabditis elegans lifespan via repressing the autophagy gene atg9
Yang, J., Chen, D., He, Y., Meléndez, A., Feng, Z., Hong, Q., Bai, X., Li, Q., Cai, G., Wang, J., et al. (2011) · AGE · doi:10.1007/s11357-011-9324-3 · Cited by 157 · see citing works
Postmortem interval effect on RNA and gene expression in human brain tissue
Birdsill, A. C., Walker, D. G., Lue, L., Sue, L. I., & Beach, T. G. (2010) · Cell and Tissue Banking · doi:10.1007/s10561-010-9210-8 · Cited by 157 · see citing works
Self-citationCellular pathology of multiple system atrophy: a review.
Lantos, P. L., & Papp, M. I. (1994) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.57.2.129 · Cited by 143 · see citing works
MicroRNA-modulated autophagic signaling networks in cancer
Fu, L., Wen, X., Bao, J., & Liu, B. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.02.004 · Cited by 141 · see citing works
Alpha-synuclein aggregation involves a bafilomycin A1-sensitive autophagy pathway
Klucken, J., Poehler, A.-M., Ebrahimi‐Fakhari, D., Schneider, J., Nuber, S., Rockenstein, E. M., Schlötzer-Schrehardt, U. M., Hyman, B. T., McLean, P. J., Masliah, E., et al. (2012) · Autophagy · doi:10.4161/auto.19371 · Cited by 135 · see citing works
Self-citationCauses and Consequences of MicroRNA Dysregulation in Neurodegenerative Diseases
Tan, L., Yu, J.-T., & Tan, L. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8803-9 · Cited by 126 · see citing works
The Parkinson disease protein α-synuclein inhibits autophagy
Winslow, A. R., & Rubinsztein, D. C. (2011) · Autophagy · doi:10.4161/auto.7.4.14393 · Cited by 126 · see citing works
Myelin Degeneration in Multiple System Atrophy Detected by Unique Antibodies
Matsuo, A., Akiguchi, I., Lee, G. C., McGeer, E. G., McGeer, P. L., & Kimura, J. (1998) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65617-9 · Cited by 125 · see citing works
Lang, M., Su, Y., Zhao, C., Sun, G., Murai, K., Wu, X., Wang, J., Gao, H., Brown, C. E., Liu, X., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036248 · Cited by 108 · see citing works
Kisos, H., Pukaß, K., Ben‐Hur, T., Richter‐Landsberg, C., & Sharon, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046817 · Cited by 90 · see citing works
Ham, O., Lee, S.-Y., Lee, C. Y., Park, J., Lee, J., Seo, H., Cha, M., Choi, E., Kim, S., & Hwang, K. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0134-x · Cited by 88 · see citing works
Desplats, P., Patel, P., Kosberg, K. A., Mante, M., Patrick, C., Rockenstein, E. M., Fujita, M., Hashimoto, M., & Masliah, E. (2012) · Molecular Neurodegeneration · doi:10.1186/1750-1326-7-49 · Cited by 87 · see citing works
Self-citationZhao, J., Han, W., Sui, X., Xie, J., & Pan, H. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.09.039 · Cited by 83 · see citing works
Schwarz, L., Goldbaum, O., Bergmann, M., Probst‐Cousin, S., & Richter‐Landsberg, C. (2012) · Journal of Molecular Neuroscience · doi:10.1007/s12031-012-9733-5 · Cited by 82 · see citing works
Dubinsky, A. N., Dastidar, S. G., Hsu, C. L., Zahra, R., Djakovic, S. N., Duarte, S., Esau, C., Spencer, B. J., Ashe, T. D., Fischer, K. M., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.09.001 · Cited by 81 · see citing works
Self-citationValera, E., Ubhi, K. K., Mante, M., Rockenstein, E. M., & Masliah, E. (2013) · Glia · doi:10.1002/glia.22610 · Cited by 78 · see citing works
Self-citationmiR-183 regulates autophagy and apoptosis in colorectal cancer through targeting of UVRAG
Huangfu, L., Liang, H., Wang, G., Su, X., Li, L., Du, Z., Hu, M., Dong, Y., Bai, X., Liu, T., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.6732 · Cited by 77 · see citing works
MiRNA Profile in the Substantia Nigra of Parkinson’s Disease and Healthy Subjects
Cardo, L. F., Coto, E., Ribacoba, R., Menéndez, M., Moris, G., Suárez, E., & Alvarez, V. (2014) · Journal of Molecular Neuroscience · doi:10.1007/s12031-014-0428-y · Cited by 75 · see citing works
Widespread micro-RNA dysregulation in Multiple System Atrophy: disease-related alteration in miR-96
Ubhi, K., Rockenstein, E., Kragh, C., Inglis, C., Spencer, B., Michael, S., Mante, M., Adame, A., Galasko, D., & Masliah, E. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12444 · Cited by 74 · see citing works
Self-citationBiphasic regulation of autophagy by miR-96 in prostate cancer cells under hypoxia
Ma, Y., Yang, H.-Z., Dong, B., Zou, H.-B., Zhou, Y., Kong, X., & Huang, Y.-R. (2014) · OncoTarget · doi:10.18632/oncotarget.2396 · Cited by 72 · see citing works
Spencer, B. J., Desplats, P., Overk, C., Valera, E., Rissman, R. A., Wu, C., Mante, M., Adame, A., Florio, J. B., Rockenstein, E. M., et al. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0775-16.2016 · Cited by 56 · see citing works
Self-citationFOXOphagy path to inducing stress resistance and cell survival
Sandri, M. (2012) · Nature Cell Biology · doi:10.1038/ncb2550 · Cited by 53 · see citing works
Gascon, E., & Gao, F. (2014) · Journal of Neurogenetics · doi:10.3109/01677063.2013.876021 · Cited by 52 · see citing works
Barbato, C., Pezzola, S., Caggiano, C., Antonelli, M., Frisone, P., Ciotti, M. T., & Ruberti, F. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00037 · Cited by 48 · see citing works
Deciphering the Function and Regulation of microRNAs in Alzheimer’s Disease and Parkinson’s Disease
Qiu, L., Zhang, W., Tan, E., & Zeng, L. (2014) · ACS Chemical Neuroscience · doi:10.1021/cn500149w · Cited by 44 · see citing works
Ubhi, K. K., Rockenstein, E. M., Doppler, E., Mante, M., Adame, A., Patrick, C., Trejo, M., Crews, L. A., Paulino, A., Moessler, H., et al. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0505-4 · Cited by 42 · see citing works
Self-citationEffect of microRNA-101 on proliferation and apoptosis of human osteosarcoma cells by targeting mTOR
Lin, S., Shao, N.-N., Fan, L., Ma, X., Pu, F., & Shao, Z. (2014) · Journal of Huazhong University of Science and Technology [Medical Sciences] · doi:10.1007/s11596-014-1369-y · Cited by 38 · see citing works
Wu, D., JIANG, H., Chen, S., & Zhang, H. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3215 · Cited by 30 · see citing works
Wenning, G. K., Seppi, K., Scherfler, C., Stefanova, N., & Puschban, Z. (2001) · Seminars in Neurology · doi:10.1055/s-2001-13117 · Cited by 22 · see citing works
Neuropathology and pathophysiology of multiple system atrophy
Jellinger, K. A. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01268.x · Cited by 18 · see citing works
Activation and alteration of lysosomes in multiple system atrophy
Makioka, K., Yamazaki, T., Takatama, M., Nakazato, Y., & Okamoto, K. (2012) · Neuroreport · doi:10.1097/wnr.0b013e3283503e4f · Cited by 14 · see citing works
Authors response to scientific correspondence
Ahmed, Z., Révész, T., & Holton, J. L. (2012) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01266.x · Cited by 1 · see citing works
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1 of the 91 references couldn’t be matched to a known paper.
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Autophagy and ALS: mechanistic insights and therapeutic implications
Chua, J. P., De Calbiac, H., Kabashi, E., & Barmada, S. J. (2022) · Autophagy · doi:10.1080/15548627.2021.1926656 · Cited by 189 · see citing works
“Oligodendrocytes Activates [450] Activates [530] MIR101 [12]”
BackgroundUnderstanding the pathogenesis of multiple system atrophy: state of the art and future perspectives
Compagnoni, G. M., & Fonzo, A. D. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0730-6 · Cited by 89 · see citing works
Insights into the pathogenesis of multiple system atrophy: focus on glial cytoplasmic inclusions
Kaji, S., Maki, T., Ishimoto, T., Yamakado, H., & Takahashi, R. (2020) · Translational Neurodegeneration · doi:10.1186/s40035-020-0185-5 · Cited by 68 · see citing works
Herman, S., Djaldetti, R., Mollenhauer, B., & Offen, D. (2023) · Brain · doi:10.1093/brain/awac261 · Cited by 62 · see citing works
Multiple system atrophy: at the crossroads of cellular, molecular and genetic mechanisms
Stefanova, N., & Wenning, G. K. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00697-7 · Cited by 62 · see citing works
MiR-101: a potential therapeutic target of cancers.
Wang, C., Deng, F., Li, H., Wang, D., Zhang, W., Ding, L., & Tang, J. (2018) · Europe PMC (PubMed Central) · Cited by 61 · see citing works
Jellinger, K. A. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02028-6 · Cited by 55 · see citing works
Spencer, B. J., Trinh, I., Rockenstein, E. M., Mante, M., Florio, J. B., Adame, A., El‐Agnaf, O. M. A., Kim, C., Masliah, E., & Rissman, R. A. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.03.001 · Cited by 46 · see citing works
Self-citationTalebian, S., Daghagh, H., Yousefi, B., Özkul, Y., Ilkhani, K., Seif, F., & Alivand, M. R. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111309 · Cited by 42 · see citing works
Shah, S. Z. A., Zhao, D., Hussain, T. A., Sabir, N., & Yang, L. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00139 · Cited by 40 · see citing works
LncRNA-T199678 Mitigates α-Synuclein-Induced Dopaminergic Neuron Injury via miR-101-3p
Bu, L.-L., Xie, Y., Lin, D., Chen, Y., Jing, X., Liang, Y., Peng, S., Huang, K., & Tao, E. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.599246 · Cited by 36 · see citing works
Gao, Y., Wang, C., Jiang, D. M., An, G., Jin, F. J., Zhang, J., Han, G., Cui, C., & Jiang, P. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.994037 · Cited by 37 · see citing works
Autophagy in α-Synucleinopathies—An Overstrained System
Fellner, L., Gabassi, E., Haybaeck, J., & Edenhofer, F. (2021) · Cells · doi:10.3390/cells10113143 · Cited by 33 · see citing works
Mechanism and Therapeutic Prospect of miRNAs in Neurodegenerative Diseases
Ma, Y.-M., & Zhao, L. (2023) · Behavioural Neurology · doi:10.1155/2023/8537296 · Cited by 34 · see citing works
Current Management and Emerging Therapies in Multiple System Atrophy
Burns, M. R., & McFarland, N. R. (2020) · Neurotherapeutics · doi:10.1007/s13311-020-00890-x · Cited by 32 · see citing works
Kim, T., Valera, E., & Desplats, P. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1577-3 · Cited by 30 · see citing works
Self-citationModels of multiple system atrophy
Lee, H.-J., Ricarte, D., Ortiz, D. M., & Lee, S. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0346-8 · Cited by 30 · see citing works
MicroRNAs to differentiate Parkinsonian disorders: Advances in biomarkers and therapeutics
Ramaswamy, P., Christopher, R., Pal, P. K., & Yadav, R. (2018) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2018.08.032 · Cited by 25 · see citing works
Multidimensional biomarkers for multiple system atrophy: an update and future directions
Wan, L., Zhu, S., Chen, Z., Qiu, R., Tang, B., & Jiang, H. F. (2023) · Translational Neurodegeneration · doi:10.1186/s40035-023-00370-0 · Cited by 24 · see citing works
Autophagy in brain tumors: molecular mechanisms, challenges, and therapeutic opportunities
Zhang, J., Jinan, Z., & Chen, Y. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-024-06063-0 · Cited by 22 · see citing works
Multiple system atrophy - a clinicopathological update
Jellinger, K. A. (2020) · Free Neuropathology · doi:10.17879/freeneuropathology-2020-2813 · Cited by 20 · see citing works
MSA: From basic mechanisms to experimental therapeutics
Heras‐Garvin, A., & Stefanova, N. (2020) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2020.01.010 · Cited by 20 · see citing works
Ragni, E., Orfei, C. P., Silini, A. R., Colombini, A., Viganò, M., Parolini, O., & de Girolamo, L. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12040347 · Cited by 20 · see citing works
Emerging urinary alpha-synuclein and miRNA biomarkers in Parkinson’s disease
Giri, B., Seamon, M., Banerjee, A., Chauhan, S., Purohit, S. B., Morgan, J. C., Baban, B., & Wakade, C. G. (2021) · Metabolic Brain Disease · doi:10.1007/s11011-021-00735-2 · Cited by 19 · see citing works
MicroRNA Deregulation in Blood Serum Identifies Multiple System Atrophy Altered Pathways
Pérez‐Soriano, A., Bravo, P., Soto, M., Infante, J., Fernández, M., Valldeoriola, F., Muñoz, E., Compta, Y., Tolosa, E. S., Garrido, A., et al. (2020) · Movement Disorders · doi:10.1002/mds.28143 · Cited by 17 · see citing works
MicroRNA as Candidate Biomarkers in Atypical Parkinsonian Syndromes: Systematic Literature Review
Bougea, A. M. (2022) · Medicina · doi:10.3390/medicina58040483 · Cited by 17 · see citing works
MicroRNAs Dysregulation and Metabolism in Multiple System Atrophy
Xiang, C., Han, S., Nao, J., & Cong, S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01103 · Cited by 16 · see citing works
Song, H., Du, C., Wang, X., Zhang, J., & Shen, Z. (2019) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2019.4077 · Cited by 16 · see citing works
Recent Advances in Clinical Trials in Multiple System Atrophy
Bendetowicz, D., Fabbri, M., Sirna, F., Fernagut, P., Foubert‐Samier, A., Saulnier, T., Traon, A. P., Proust‐Lima, C., Rascol, O., & Meissner, W. G. (2024) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-024-01335-0 · Cited by 14 · see citing works
Taheri, A. T., Golshadi, Z., Zare, H., Alinaghipour, A., Faghihi, Z., Dadgostar, E., Tamtaji, Z., Aschner, M., Mirzaei, H., Tamtaji, O. R., et al. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-024-01461-w · Cited by 14 · see citing works
In vitro models of multiple system atrophy from primary cells to induced pluripotent stem cells
Abati, E., Fonzo, A. D., & Corti, S. P. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13563 · Cited by 14 · see citing works
miR-101a-3p Impairs Synaptic Plasticity and Contributes to Synucleinopathy
Xylaki, M., Paiva, I., Al‐Azzani, M., Gerhardt, E., Jain, G., Islam, R., Vasili, E., Wassouf, Z., Schulze-Hentrich, J. M., Fischer, A., et al. (2023) · Journal of Parkinson s Disease · doi:10.3233/jpd-225055 · Cited by 13 · see citing works
Marmion, D. J., Peelaerts, W., & Kordower, J. H. (2021) · Journal of Neural Transmission · doi:10.1007/s00702-021-02419-8 · Cited by 13 · see citing works
Demiri, S., Veltsista, D., Siokas, V., Spiliopoulos, K. C., Tsika, A., Stamati, P., Chroni, E., Dardiotis, E., & Liampas, I. (2025) · Brain Sciences · doi:10.3390/brainsci15030241 · Cited by 13 · see citing works
Progress in the treatment of Parkinson-Plus syndromes
Olfati, N., Shoeibi, A., & Litvan, I. (2018) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2018.10.006 · Cited by 12 · see citing works
Song, H., Du, C., Wang, X., Zhang, J., & Shen, Z. (2019) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2019.4160 · Cited by 12 · see citing works
Epigenetic regulation of autophagy in coronavirus disease 2019 (COVID-19)
Behrouj, H., Vakili, O., Sadeghdoust, A., Aligolighasemabadi, N., Khalili, P., Zamani, M., & Mokarram, P. (2022) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2022.101264 · Cited by 10 · see citing works
Glutathione Depletion and MicroRNA Dysregulation in Multiple System Atrophy: A Review
Kinoshita, C., Kubota, N., & Aoyama, K. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315076 · Cited by 9 · see citing works
Mini-Review: The MSA transcriptome
Pérez‐Soriano, A., & Martı́, M. J. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135586 · Cited by 9 · see citing works
microRNA and circRNA in Parkinson’s Disease and atypical parkinsonian syndromes
Bougea, A. M., & Stefanis, L. (2023) · Advances in clinical chemistry · doi:10.1016/bs.acc.2023.03.002 · Cited by 9 · see citing works
Shin, J. H., Ruhno, K. E., Shin, C., Kim, H. J., Nam, S. J., Chung, S. J., Moon, J. H., & Kim, H. (2025) · Acta Neuropathologica Communications · doi:10.1186/s40478-025-02107-8 · Cited by 7 · see citing works
Duan, R., Shi, L., Deng, Y., Wu, J., Wang, S., Peng, Q., Li, Z., Xu, Z., Wang, F., Xue, X., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-76058-w · Cited by 5 · see citing works
Fluid biomarkers in atypical Parkinsonism: current state and future perspectives
Bougea, A. M., Colosimo, C., Falup‐Pecurariu, C., Palermo, G., & Değirmenci, Y. (2025) · Journal of Neural Transmission · doi:10.1007/s00702-025-02930-2 · Cited by 5 · see citing works
LncRNA NEAT1 and miRNA 101 as potential diagnostic biomarkers in patients with alopecia areata
Erfan, R., Shaker, O. G., Khalil, M. A. F., Hassan, A. R., Abu-El-Azayem, A. K., Samy, A., Abdelhamid, H., Awaji, A. A., Sayed, H. S. E., & Mohammed, A. (2024) · Non-coding RNA Research · doi:10.1016/j.ncrna.2024.08.005 · Cited by 5 · see citing works
Functional roles of non-coding RNAs in atrophy
Ghafouri‐Fard, S., Abak, A., Khademi, S., Shoorei, H., Bahroudi, Z., Taheri, M. N., & Dilmaghani, N. A. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111820 · Cited by 5 · see citing works
Harada, M., Masaki, K., Tanaka, T., Sekiya, H., Matsuse, D., Yamaguchi, H., Nishimura, Y., Takase, E. O., Tanaka, E., Kira, Y., et al. (2025) · Acta Neuropathologica Communications · doi:10.1186/s40478-025-02116-7 · Cited by 3 · see citing works
Seeing Neurodegeneration in a New Light Using Genetically Encoded Fluorescent Biosensors and iPSCs
Stellon, D., Talbot, J., Hewitt, A. W., King, A. E., & Cook, A. L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021766 · Cited by 3 · see citing works
Commentary: LncRNA-T199678 Mitigates α-Synuclein-Induced Dopaminergic Neuron Injury via miR-101-3p
Wang, Y., Zhang, X., Chen, F., Chen, L., & Xie, J. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.650840 · Cited by 3 · see citing works
Autophagy–Lysosome Pathway in Multiple System Atrophy Pathogenesis: The Best Is Yet to Come
Mavroeidi, P., & Xilouri, M. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262010204 · Cited by 2 · see citing works
Li, Y., Wu, J., Zhang, X., Liu, W., Shi, L., Xu, F., Wang, J., & Xiong, Y. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.116551 · Cited by 2 · see citing works
RetractedNdayisaba, A., Herrera-Vaquero, M., Wenning, G. K., & Stefanova, N. (2019) · Clinical Autonomic Research · doi:10.1007/s10286-019-00614-y · Cited by 3 · see citing works
MicroRNAs Regulating Autophagy in Neurodegeneration
Lai, Q., Kovzel, N., Konovalov, R., & Vinnikov, I. A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-981-16-2830-6_11 · Cited by 1 · see citing works
Widyarti, S., Wibowo, S., Sabarudin, A., Abhirama, I., & Sumitro, S. B. (2023) · Preprints.org · doi:10.20944/preprints202301.0220.v1 · Cited by 1 · see citing works
- Authors
- Valera, E., Spencer, B., Mott, J., Trejo, M., Adame, A., Mante, M., Rockenstein, E., Troncoso, J. C., Beach, T. G., Masliah, E., & Desplats, P.
- Affiliations
- University of California San Diego (US)
- Johns Hopkins University (US)
- Banner Sun Health Research Institute (US)
- Corresponding author
- Desplats, Paula
- ORCID
- Venue
- Frontiers in Molecular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2017-10-17
- Volume
- 10
- Pages
- 329-329
- ISSN
- 1662-5099 (ISSN-L)
- PMC
- PMC5650998
- OpenAlex
- W2766187488
- Cited by
- 55
- References
- 91
- Citations by year
- 2025: 6 · 2024: 4 · 2023: 7 · 2022: 6 · 2021: 7 · 2020: 9 · 2019: 10 · 2018: 6
- FWCI
- 4.76
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Molecular Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (AG18440, AG022074, NS044233, NS092803)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- microRNA-101, multiple system atrophy, alpha-synuclein accumulation, autophagy, oligodendroglial cells, synucleinopathies, Rab5a, microRNA dysregulation, lentiviral gene delivery, striatum, demyelination, neurodegeneration, therapeutic target
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