MicroRNA-101 Modulates Autophagy and Oligodendroglial Alpha-Synuclein Accumulation in Multiple System Atrophy

Alvarez-Erviti, 2013, Influence of microRNA deregulation on chaperone-mediated autophagy and α-synuclein pathology in Parkinson’s disease, Cell Death Dis., 4, e545, 10.1038/cddis.2013.73

Asi, 2014, α-synuclein mRNA expression in oligodendrocytes in MSA, Glia, 62, 964, 10.1002/glia.22653

Banzhaf-Strathmann, 2014, MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer’s disease, EMBO J., 33, 1667, 10.15252/embj.201387576

Barbato, 2014, A lentiviral sponge for miR-101 regulates RanBP9 expression and amyloid precursor protein metabolism in hippocampal neurons, Front. Cell. Neurosci., 8, 37, 10.3389/fncel.2014.00037

Bar-On, 2008, Statins reduce neuronal α-synuclein aggregation in in vitro models of Parkinson’s disease, J. Neurochem., 105, 1656, 10.1111/j.1471-4159.2008.05254.x

Beach, 2015, Arizona study of aging and neurodegenerative disorders and brain and body donation program, Neuropathology, 35, 354, 10.1111/neup.12189

Betel, 2010, Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites, Genome Biol., 11, R90, 10.1186/gb-2010-11-8-r90

Birdsill, 2011, Postmortem interval effect on RNA and gene expression in human brain tissue, Cell Tissue Bank., 12, 311, 10.1007/s10561-010-9210-8

Cardo, 2014, MiRNA profile in the substantia nigra of Parkinson’s disease and healthy subjects, J. Mol. Neurosci., 54, 830, 10.1007/s12031-014-0428-y

Crews, 2010, Selective molecular alterations in the autophagy pathway in patients with Lewy body disease and in models of α-synucleinopathy, PLoS One, 5, e9313, 10.1371/journal.pone.0009313

Cuervo, 2004, Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy, Science, 305, 1292, 10.1126/science.1101738

Denk, 2015, MicroRNA profiling of CSF reveals potential biomarkers to detect Alzheimer’s disease, PLoS One, 10, e0126423, 10.1371/journal.pone.0126423

Desplats, 2009, Inclusion formation and neuronal cell death through neuron-to-neuron transmission of α-synuclein, Proc. Natl. Acad. Sci. U S A, 106, 13010, 10.1073/pnas.0903691106

Desplats, 2012, Combined exposure to Maneb and Paraquat alters transcriptional regulation of neurogenesis-related genes in mice models of Parkinson’s disease, Mol. Neurodegener., 7, 49, 10.1186/1750-1326-7-49

Dickson, , Multiple system atrophy: a sporadic synucleinopathy, Brain Pathol., 9, 721, 10.1111/j.1750-3639.1999.tb00553.x

Dickson, , Widespread alterations of α-synuclein in multiple system atrophy, Am. J. Pathol., 155, 1241, 10.1016/S0002-9440(10)65226-1

Dubinsky, 2014, Let-7 coordinately suppresses components of the amino acid sensing pathway to repress mTORC1 and induce autophagy, Cell Metab., 20, 626, 10.1016/j.cmet.2014.09.001

Fang, 2012, The miR-124 regulates the expression of BACE1/β-secretase correlated with cell death in Alzheimer’s disease, Toxicol. Lett., 209, 94, 10.1016/j.toxlet.2011.11.032

Femminella, 2015, The emerging role of microRNAs in Alzheimer’s disease, Front. Physiol., 6, 40, 10.3389/fphys.2015.00040

Frankel, 2012, MicroRNA regulation of autophagy, Carcinogenesis, 33, 2018, 10.1093/carcin/bgs266

Frankel, 2011, microRNA-101 is a potent inhibitor of autophagy, EMBO J., 30, 4628, 10.1038/emboj.2011.331

Fu, 2012, MicroRNA-modulated autophagic signaling networks in cancer, Int. J. Biochem. Cell Biol., 44, 733, 10.1016/j.biocel.2012.02.004

Fullgrabe, 2014, The return of the nucleus: transcriptional and epigenetic control of autophagy, Nat. Rev. Mol. Cell Biol., 15, 65, 10.1038/nrm3716

Gascon, 2014, The emerging roles of microRNAs in the pathogenesis of frontotemporal dementia-amyotrophic lateral sclerosis (FTD-ALS) spectrum disorders, J. Neurogenet., 28, 30, 10.3109/01677063.2013.876021

Ghaemi, 2002, Differentiating multiple system atrophy from Parkinson’s disease: contribution of striatal and midbrain MRI volumetry and multi-tracer PET imaging, J. Neurol. Neurosurg. Psychiatry, 73, 517, 10.1136/jnnp.73.5.517

Gilman, 2008, Second consensus statement on the diagnosis of multiple system atrophy, Neurology, 71, 670, 10.1212/01.WNL.0000324625.00404.15

Ham, 2015, let-7b suppresses apoptosis and autophagy of human mesenchymal stem cells transplanted into ischemia/reperfusion injured heart 7by targeting caspase-3, Stem Cell Res. Ther., 6, 147, 10.1186/s13287-015-0134-x

Hoss, 2016, microRNA profiles in Parkinson’s disease prefrontal cortex, Front. Aging Neurosci., 8, 36, 10.3389/fnagi.2016.00036

Huangfu, 2016, miR-183 regulates autophagy and apoptosis in colorectal cancer through targeting of UVRAG, Oncotarget, 7, 4735, 10.18632/oncotarget.6732

Jellinger, 2003, Neuropathological spectrum of synucleinopathies, Mov. Disord., 18, S2, 10.1002/mds.10557

Jellinger, 2012, Neuropathology and pathophysiology of multiple system atrophy, Neuropathol. Appl. Neurobiol., 38, 381, 10.1111/j.1365-2990.2012.01268.x

Jellinger, 2014, Neuropathology of multiple system atrophy: new thoughts about pathogenesis, Mov. Disord., 29, 1720, 10.1002/mds.26052

Jing, 2015, Interaction of autophagy with microRNAs and their potential therapeutic implications in human cancers, Cancer Lett., 356, 332, 10.1016/j.canlet.2014.09.039

Kabaria, 2015, Inhibition of miR-34b and miR-34c enhances α-synuclein expression in Parkinson’s disease, FEBS Lett., 589, 319, 10.1016/j.febslet.2014.12.014

Khoo, 2012, Plasma-based circulating MicroRNA biomarkers for Parkinson’s disease, J. Parkinsons Dis., 2, 321, 10.3233/JPD-012144

Kisos, 2012, Increased neuronal α-synuclein pathology associates with its accumulation in oligodendrocytes in mice modeling α-synucleinopathies, PLoS One, 7, e46817, 10.1371/journal.pone.0046817

Klionsky, 2016, Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition), Autophagy, 12, 1, 10.1080/15548627.2015.1100356

Klucken, 2012, α-synuclein aggregation involves a bafilomycin A 1-sensitive autophagy pathway, Autophagy, 8, 754, 10.4161/auto.19371

Lang, 2012, Genome-wide profiling identified a set of miRNAs that are differentially expressed in glioblastoma stem cells and normal neural stem cells, PLoS One, 7, e36248, 10.1371/journal.pone.0036248

Lantos, 1994, Cellular pathology of multiple system atrophy: a review, J. Neurol. Neurosurg. Psychiatry, 57, 129, 10.1136/jnnp.57.2.129

Lee, 2013, Autophagic failure promotes the exocytosis and intercellular transfer of α-synuclein, Exp. Mol. Med., 45, e22, 10.1038/emm.2013.45

Lee, 2011, Altered microRNA regulation in Huntington’s disease models, Exp. Neurol., 227, 172, 10.1016/j.expneurol.2010.10.012

Lee, 2010, Cell-to-cell transmission of non-prion protein aggregates, Nat. Rev. Neurol., 6, 702, 10.1038/nrneurol.2010.145

Lin, 2010, Unregulated miR-96 induces cell proliferation in human breast cancer by downregulating transcriptional factor FOXO3a, PLoS One, 5, e15797, 10.1371/journal.pone.0015797

Lin, 2014, Effect of microRNA-101 on proliferation and apoptosis of human osteosarcoma cells by targeting mTOR, J. Huazhong Univ. Sci. Technol. Med. Sci., 34, 889, 10.1007/s11596-014-1369-y

Liu, 2012, The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila, Nature, 482, 519, 10.1038/nature10810

Louis, 1992, CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes, Front. Mol. Neurosci., 31, 193, 10.1002/jnr.490310125

Lynch-Day, 2012, The role of autophagy in Parkinson’s disease, Cold Spring Harb. Perspect. Med., 2, a009357, 10.1101/cshperspect.a009357

Ma, 2014, Biphasic regulation of autophagy by miR-96 in prostate cancer cells under hypoxia, Oncotarget, 5, 9169, 10.18632/oncotarget.2396

Makioka, 2012, Activation and alteration of lysosomes in multiple system atrophy, Neuroreport, 23, 270, 10.1097/WNR.0b013e3283503e4f

Masliah, 2011, Passive immunization reduces behavioral and neuropathological deficits in an α-synuclein transgenic model of Lewy body disease, PLoS One, 6, e19338, 10.1371/journal.pone.0019338

Masuda-Suzukake, 2014, Pathological α-synuclein propagates through neural networks, Acta Neuropathol. Commun., 2, 88, 10.1186/s40478-014-0088-8

Matsuo, 1998, Myelin degeneration in multiple system atrophy detected by unique antibodies, Am. J. Pathol., 153, 735, 10.1016/s0002-9440(10)65617-9

Mellios, 2008, A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of BDNF in prefrontal cortex, Hum. Mol. Genet., 17, 3030, 10.1093/hmg/ddn201

Olanow, 2013, Parkinson’s disease and α synuclein: is Parkinson’s disease a prion-like disorder?, Mov. Disord., 28, 31, 10.1002/mds.25373

Peltier, 2008, Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues, RNA, 14, 844, 10.1261/rna.939908

Pickford, 2008, The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid β accumulation in mice, J. Clin. Invest., 118, 2190, 10.1172/JCI33585

Prusiner, 2015, Evidence for α-synuclein prions causing multiple system atrophy in humans with parkinsonism, Proc. Natl. Acad. Sci. U S A, 112, E5308, 10.1073/pnas.1514475112

Qiu, 2014, Deciphering the function and regulation of microRNAs in Alzheimer’s disease and Parkinson’s disease, ACS Chem. Neurosci., 5, 884, 10.1021/cn500149w

Reyes, 2014, α-synuclein transfers from neurons to oligodendrocytes, Glia, 62, 387, 10.1002/glia.22611

Rickham, 1964, Human experimentation. Code of ethics of the world medical association. Declaration of helsinki, Br. Med. J., 2, 177, 10.1136/bmj.2.5402.177

Sandri, 2012, FOXOphagy path to inducing stress resistance and cell survival, Nat. Cell Biol., 14, 786, 10.1038/ncb2550

Schubert, 1974, Clonal cell lines from the rat central nervous system, Nature, 249, 224, 10.1038/249224a0

Schwarz, 2012, Involvement of macroautophagy in multiple system atrophy and protein aggregate formation in oligodendrocytes, J. Mol. Neurosci., 47, 256, 10.1007/s12031-012-9733-5

Shults, 2005, Neurological and neurodegenerative alterations in a transgenic mouse model expressing human α-synuclein under oligodendrocyte promoter: implications for multiple system atrophy, J Neurosci, 25, 10689, 10.1523/JNEUROSCI.3527-05.2005

Spencer, 2016, Reducing endogenous α-synuclein mitigates the degeneration of selective neuronal populations in an Alzheimer’s disease transgenic mouse model, J. Neurosci., 36, 7971, 10.1523/JNEUROSCI.0775-16.2016

Spencer, 2009, Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in α-synuclein models of Parkinson’s and Lewy body diseases, J. Neurosci., 29, 13578, 10.1523/JNEUROSCI.4390-09.2009

Stefanova, 2007, Microglial activation mediates neurodegeneration related to oligodendroglial α-synucleinopathy: implications for multiple system atrophy, Mov. Disord., 22, 2196, 10.1002/mds.21671

Sun, 2015, An updated role of microRNA-124 in central nervous system disorders: a review, Front. Cell. Neurosci., 9, 193, 10.3389/fncel.2015.00193

Tan, 2015, Causes and consequences of microRNA dysregulation in neurodegenerative diseases, Mol. Neurobiol., 51, 1249, 10.1007/s12035-014-8803-9

Tan, 2014, Genome-wide serum microRNA expression profiling identifies serum biomarkers for Alzheimer’s disease, J. Alzheimers Dis., 40, 1017, 10.3233/JAD-132144

Tiscornia, 2006, Production and purification of lentiviral vectors, Nat. Protoc., 1, 241, 10.1038/nprot.2006.37

Tong, 2010, Brain α-synuclein accumulation in multiple system atrophy, Parkinson’s disease and progressive supranuclear palsy: a comparative investigation, Brain, 133, 172, 10.1093/brain/awp282

Ubhi, 2011, Multiple system atrophy: a clinical and neuropathological perspective, Trends Neurosci., 34, 581, 10.1016/j.tins.2011.08.003

Ubhi, 2009, Neurofibrillary and neurodegenerative pathology in APP-transgenic mice injected with AAV2-mutant TAU: neuroprotective effects of Cerebrolysin, Acta Neuropathol., 117, 699, 10.1007/s00401-009-0505-4

Ubhi, 2014, Widespread microRNA dysregulation in multiple system atrophy—disease-related alteration in miR-96, Eur. J. Neurosci., 39, 1026, 10.1111/ejn.12444

Valera, 2014, Antidepressants reduce neuroinflammatory responses and astroglial α-synuclein accumulation in a transgenic mouse model of multiple system atrophy, Glia, 62, 317, 10.1002/glia.22610

Vallelunga, 2014, Identification of circulating microRNAs for the differential diagnosis of Parkinson’s disease and Multiple System Atrophy, Front. Cell. Neurosci., 8, 156, 10.3389/fncel.2014.00156

Vilardo, 2010, MicroRNA-101 regulates amyloid precursor protein expression in hippocampal neurons, J. Biol. Chem., 285, 18344, 10.1074/jbc.M110.112664

Wenning, 1994, Clinical features and natural history of multiple system atrophy. An analysis of 100 cases, Brain, 117, 835, 10.1093/brain/117.4.835

Wenning, 2001, Multiple system atrophy, Semin. Neurol., 21, 33, 10.1055/s-2001-13117

Wenning, 2008, Multiple system atrophy: a primary oligodendrogliopathy, Ann. Neurol., 64, 239, 10.1002/ana.21465

Winslow, 2011, The Parkinson disease protein α-synuclein inhibits autophagy, Autophagy, 7, 429, 10.4161/auto.7.4.14393

Wong, 2010, Autophagy gone awry in neurodegenerative diseases, Nat. Neurosci., 13, 805, 10.1038/nn.2575

Wu, 2015, Inhibition of microRNA-101 attenuates hypoxia/reoxygenationinduced apoptosis through induction of autophagy in H9c2 cardiomyocytes, Mol. Med. Rep., 11, 3988, 10.3892/mmr.2015.3215

Xu, 2013, miR-101 inhibits autophagy and enhances cisplatin-induced apoptosis in hepatocellular carcinoma cells, Oncol. Rep., 29, 2019, 10.3892/or.2013.2338

Yang, 2013, MiR-34 modulates Caenorhabditis elegans lifespan via repressing the autophagy gene atg9, Age (Dordr), 35, 11, 10.1007/s11357-011-9324-3

Yu, 2012, Targeting microRNA-30a-mediated autophagy enhances imatinib activity against human chronic myeloid leukemia cells, Leukemia, 26, 1752, 10.1038/leu.2012.65

Zhu, 2009, Regulation of autophagy by a beclin 1-targeted microRNA, miR-30a, in cancer cells, Autophagy, 5, 816, 10.4161/auto.9064