{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T15:56:56Z","timestamp":1786982216657,"version":"build-2736575974"},"reference-count":71,"publisher":"Springer Science and Business Media LLC","issue":"5","license":[{"start":{"date-parts":[[2020,1,29]],"date-time":"2020-01-29T00:00:00Z","timestamp":1580256000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,1,29]],"date-time":"2020-01-29T00:00:00Z","timestamp":1580256000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000049","name":"National Institute on Aging","doi-asserted-by":"publisher","award":["R01AG042890"],"award-info":[{"award-number":["R01AG042890"]}],"id":[{"id":"10.13039\/100000049","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000049","name":"National Institute on Aging","doi-asserted-by":"publisher","award":["F31AG057217"],"award-info":[{"award-number":["F31AG057217"]}],"id":[{"id":"10.13039\/100000049","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mol Neurobiol"],"published-print":{"date-parts":[[2020,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Alzheimer\u2019s disease (AD) is marked by synaptic loss (at early stages) and neuronal death (at late stages). Amyloid beta (A\u03b2) and tau oligomers can target and disrupt synapses thus driving cognitive decay. Non-demented individuals with Alzheimer\u2019s neuropathology (NDAN) are capable of withstanding A\u03b2 and tau toxicity, thus remaining cognitively intact despite presence of AD neuropathology. Understanding the involved mechanism(s) would lead to development of novel effective therapeutic strategies aimed at promoting synaptic resilience to amyloid toxicity. NDAN have a unique hippocampal post-synaptic proteome when compared with AD and control individuals. Potential upstream modulators of such unique proteomic profile are miRNA-485, miRNA-4723 and miRNA-149, which we found differentially expressed in AD and NDAN vs. control. We thus hypothesized that these miRNAs play an important role in promoting either synaptic resistance or sensitization to A\u03b2 oligomer binding. Using an in vivo mouse model, we found that administration of these miRNAs affected key synaptic genes and significantly decreased A\u03b2 binding to the synapses. Our findings suggest that miRNA regulation and homeostasis are crucial for A\u03b2 interaction with synaptic terminals and support that a unique miRNA regulation could be driving synaptic resistance to A\u03b2 toxicity in NDAN, thus contributing to their preserved cognitive abilities.<\/jats:p>","DOI":"10.1007\/s12035-020-01868-8","type":"journal-article","created":{"date-parts":[[2020,1,29]],"date-time":"2020-01-29T11:02:53Z","timestamp":1580295773000},"page":"2232-2243","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":30,"title":["Selected microRNAs Increase Synaptic Resilience to the Damaging Binding of the Alzheimer\u2019s Disease Amyloid Beta Oligomers"],"prefix":"10.1007","volume":"57","author":[{"given":"Olga","family":"Zolochevska","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4795-447X","authenticated-orcid":false,"given":"Giulio","family":"Taglialatela","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,1,29]]},"reference":[{"key":"1868_CR1","unstructured":"Alzheimer\u2019s and dementia (2018) Alzheimer\u2019s facts and figures report Alzheimer\u2019s Association. https:\/\/www.alz.org\/alzheimers-dementia\/facts-figures. Accessed 14 Sep 2018"},{"key":"1868_CR2","doi-asserted-by":"publisher","first-page":"108","DOI":"10.5507\/bp.2012.055","volume":"156","author":"J Povova","year":"2012","unstructured":"Povova J, Ambroz P, Bar M et al (2012) Epidemiological of and risk factors for Alzheimer\u2019s disease: a review. Biomed Pap 156:108\u2013114. https:\/\/doi.org\/10.5507\/bp.2012.055","journal-title":"Biomed Pap"},{"key":"1868_CR3","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1007\/s11910-014-0498-9","volume":"14","author":"R Vandenberghe","year":"2014","unstructured":"Vandenberghe R (2014) The relationship between amyloid deposition, neurodegeneration, and cognitive decline in dementia. Curr Neurol Neurosci Rep 14:498. https:\/\/doi.org\/10.1007\/s11910-014-0498-9","journal-title":"Curr Neurol Neurosci Rep"},{"key":"1868_CR4","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1126\/science.1074069","volume":"298","author":"DJ Selkoe","year":"2002","unstructured":"Selkoe DJ (2002) Alzheimer\u2019s disease is a synaptic failure. Science 298:789\u2013791. https:\/\/doi.org\/10.1126\/science.1074069","journal-title":"Science"},{"key":"1868_CR5","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1016\/j.neurobiolaging.2003.09.001","volume":"24","author":"PD Coleman","year":"2003","unstructured":"Coleman PD, Yao PJ (2003) Synaptic slaughter in Alzheimer\u2019s disease. Neurobiol Aging 24:1023\u20131027","journal-title":"Neurobiol Aging"},{"key":"1868_CR6","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1055\/s-2006-956753","volume":"27","author":"R Yaari","year":"2007","unstructured":"Yaari R, Corey-Bloom J (2007) Alzheimer\u2019s disease. Semin Neurol 27:32\u201341. https:\/\/doi.org\/10.1055\/s-2006-956753","journal-title":"Semin Neurol"},{"key":"1868_CR7","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1016\/j.arr.2016.04.005","volume":"28","author":"CM Henstridge","year":"2016","unstructured":"Henstridge CM, Pickett E, Spires-Jones TL (2016) Synaptic pathology: a shared mechanism in neurological disease. Ageing Res Rev 28:72\u201384. https:\/\/doi.org\/10.1016\/j.arr.2016.04.005","journal-title":"Ageing Res Rev"},{"key":"1868_CR8","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/j.ebiom.2016.03.035","volume":"6","author":"U Sengupta","year":"2016","unstructured":"Sengupta U, Nilson AN, Kayed R (2016) The role of amyloid-\u03b2 oligomers in toxicity, propagation, and immunotherapy. EBioMedicine 6:42\u201349. https:\/\/doi.org\/10.1016\/j.ebiom.2016.03.035","journal-title":"EBioMedicine"},{"key":"1868_CR9","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1111\/j.1471-4159.2011.07447.x","volume":"119","author":"LC Reese","year":"2011","unstructured":"Reese LC, Laezza F, Woltjer R, Taglialatela G (2011) Dysregulated phosphorylation of Ca(2+) \/calmodulin-dependent protein kinase II-\u03b1 in the hippocampus of subjects with mild cognitive impairment and Alzheimer\u2019s disease. J Neurochem 119:791\u2013804. https:\/\/doi.org\/10.1111\/j.1471-4159.2011.07447.x","journal-title":"J Neurochem"},{"key":"1868_CR10","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1007\/s00249-007-0237-0","volume":"37","author":"C Aisenbrey","year":"2008","unstructured":"Aisenbrey C, Borowik T, Bystr\u00f6m R et al (2008) How is protein aggregation in amyloidogenic diseases modulated by biological membranes? Eur Biophys J 37:247\u2013255. https:\/\/doi.org\/10.1007\/s00249-007-0237-0","journal-title":"Eur Biophys J"},{"key":"1868_CR11","doi-asserted-by":"publisher","first-page":"1509","DOI":"10.1001\/archneur.65.11.1509","volume":"65","author":"HJ Aizenstein","year":"2008","unstructured":"Aizenstein HJ, Nebes RD, Saxton JA et al (2008) Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch Neurol 65:1509\u20131517. https:\/\/doi.org\/10.1001\/archneur.65.11.1509","journal-title":"Arch Neurol"},{"key":"1868_CR12","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/ana.410410106","volume":"41","author":"T Gomez-Isla","year":"1997","unstructured":"Gomez-Isla T, Hollister R, West H et al (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer\u2019s disease. Ann Neurol 41:17\u201324. https:\/\/doi.org\/10.1002\/ana.410410106","journal-title":"Ann Neurol"},{"key":"1868_CR13","doi-asserted-by":"publisher","first-page":"698","DOI":"10.1038\/nrd3505","volume":"10","author":"E Karran","year":"2011","unstructured":"Karran E, Mercken M, De Strooper B (2011) The amyloid cascade hypothesis for Alzheimer\u2019s disease: an appraisal for the development of therapeutics. Nat Rev Drug Discov 10:698\u2013712. https:\/\/doi.org\/10.1038\/nrd3505","journal-title":"Nat Rev Drug Discov"},{"key":"1868_CR14","doi-asserted-by":"publisher","first-page":"e27291","DOI":"10.1371\/journal.pone.0027291","volume":"6","author":"CL Maarouf","year":"2011","unstructured":"Maarouf CL, Daugs ID, Kokjohn TA et al (2011) Alzheimer\u2019s disease and non-demented high pathology control nonagenarians: comparing and contrasting the biochemistry of cognitively successful aging. PLoS One 6:e27291. https:\/\/doi.org\/10.1371\/journal.pone.0027291","journal-title":"PLoS One"},{"key":"1868_CR15","doi-asserted-by":"publisher","unstructured":"Zolochevska O, Taglialatela G (2016) Non-demented individuals with Alzheimer\u2019s disease neuropathology: resistance to cognitive decline may reveal new treatment strategies. Curr Pharm Des:22. https:\/\/doi.org\/10.2174\/1381612822666160518142110","DOI":"10.2174\/1381612822666160518142110"},{"key":"1868_CR16","doi-asserted-by":"publisher","first-page":"1083","DOI":"10.1097\/00005072-199655100-00008","volume":"55","author":"LF Lue","year":"1996","unstructured":"Lue LF, Brachova L, Civin WH, Rogers J (1996) Inflammation, A beta deposition, and neurofibrillary tangle formation as correlates of Alzheimer\u2019s disease neurodegeneration. J Neuropathol Exp Neurol 55:1083\u20131088","journal-title":"J Neuropathol Exp Neurol"},{"key":"1868_CR17","doi-asserted-by":"publisher","unstructured":"Briley D, Ghirardi V, Woltjer R et al (2016) Preserved neurogenesis in non-demented individuals with AD neuropathology. Sci Rep:6. https:\/\/doi.org\/10.1038\/srep27812","DOI":"10.1038\/srep27812"},{"key":"1868_CR18","doi-asserted-by":"publisher","first-page":"659","DOI":"10.3233\/JAD-180179","volume":"65","author":"O Zolochevska","year":"2018","unstructured":"Zolochevska O, Bjorklund N, Woltjer R et al (2018) Postsynaptic proteome of non-demented individuals with Alzheimer\u2019s disease neuropathology. J Alzheimers Dis 65:659\u2013682. https:\/\/doi.org\/10.3233\/JAD-180179","journal-title":"J Alzheimers Dis"},{"key":"1868_CR19","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1186\/1750-1326-7-23","volume":"7","author":"NL Bjorklund","year":"2012","unstructured":"Bjorklund NL, Reese LC, Sadagoparamanujam VM et al (2012) Absence of amyloid \u03b2 oligomers at the postsynapse and regulated synaptic Zn2+ in cognitively intact aged individuals with Alzheimer\u2019s disease neuropathology. Mol Neurodegener 7:23. https:\/\/doi.org\/10.1186\/1750-1326-7-23","journal-title":"Mol Neurodegener"},{"key":"1868_CR20","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/0022-3956(75)90026-6","volume":"12","author":"MF Folstein","year":"1975","unstructured":"Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189\u2013198","journal-title":"J Psychiatr Res"},{"key":"1868_CR21","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1007\/BF00308809","volume":"82","author":"H Braak","year":"1991","unstructured":"Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239\u2013259","journal-title":"Acta Neuropathol"},{"key":"1868_CR22","doi-asserted-by":"publisher","first-page":"2923","DOI":"10.1002\/jnr.22445","volume":"88","author":"KT Dineley","year":"2010","unstructured":"Dineley KT, Kayed R, Neugebauer V et al (2010) Amyloid-beta oligomers impair fear conditioned memory in a calcineurin-dependent fashion in mice. J Neurosci Res 88:2923\u20132932. https:\/\/doi.org\/10.1002\/jnr.22445","journal-title":"J Neurosci Res"},{"key":"1868_CR23","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1152\/jappl.1968.25.3.319","volume":"25","author":"WG Clark","year":"1968","unstructured":"Clark WG, Vivonia CA, Baxter CF (1968) Accurate freehand injection into the lateral brain ventricle of the conscious mouse. J Appl Physiol 25:319\u2013321","journal-title":"J Appl Physiol"},{"key":"1868_CR24","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1016\/j.jneumeth.2016.01.006","volume":"261","author":"W Franklin","year":"2016","unstructured":"Franklin W, Taglialatela G (2016) A method to determine insulin responsiveness in synaptosomes isolated from frozen brain tissue. J Neurosci Methods 261:128\u2013134. https:\/\/doi.org\/10.1016\/j.jneumeth.2016.01.006","journal-title":"J Neurosci Methods"},{"key":"1868_CR25","doi-asserted-by":"publisher","first-page":"824","DOI":"10.1111\/j.1474-9726.2008.00434.x","volume":"7","author":"LC Reese","year":"2008","unstructured":"Reese LC, Zhang W, Dineley KT et al (2008) Selective induction of calcineurin activity and signaling by oligomeric amyloid beta. Aging Cell 7:824\u2013835. https:\/\/doi.org\/10.1111\/j.1474-9726.2008.00434.x","journal-title":"Aging Cell"},{"key":"1868_CR26","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","volume":"29","author":"A Dobin","year":"2013","unstructured":"Dobin A, Davis CA, Schlesinger F et al (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15\u201321. https:\/\/doi.org\/10.1093\/bioinformatics\/bts635","journal-title":"Bioinformatics"},{"key":"1868_CR27","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https:\/\/doi.org\/10.1186\/s13059-014-0550-8","journal-title":"Genome Biol"},{"key":"1868_CR28","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1002\/path.4078","volume":"229","author":"F Wang","year":"2013","unstructured":"Wang F, Ma YL, Zhang P et al (2013) SP1 mediates the link between methylation of the tumour suppressor miR-149 and outcome in colorectal cancer. J Pathol 229:12\u201324. https:\/\/doi.org\/10.1002\/path.4078","journal-title":"J Pathol"},{"key":"1868_CR29","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.brainresbull.2013.03.005","volume":"95","author":"M Pevida","year":"2013","unstructured":"Pevida M, Lastra A, Hidalgo A et al (2013) Spinal CCL2 and microglial activation are involved in paclitaxel-evoked cold hyperalgesia. Brain Res Bull 95:21\u201327. https:\/\/doi.org\/10.1016\/j.brainresbull.2013.03.005","journal-title":"Brain Res Bull"},{"key":"1868_CR30","doi-asserted-by":"publisher","first-page":"11650","DOI":"10.1073\/pnas.1017576108","volume":"108","author":"JE Cohen","year":"2011","unstructured":"Cohen JE, Lee PR, Chen S et al (2011) MicroRNA regulation of homeostatic synaptic plasticity. Proc Natl Acad Sci U S A 108:11650\u201311655. https:\/\/doi.org\/10.1073\/pnas.1017576108","journal-title":"Proc Natl Acad Sci U S A"},{"key":"1868_CR31","doi-asserted-by":"publisher","unstructured":"Cohen JE, Lee PR, Fields RD (2014) Systematic identification of 3\u2019-UTR regulatory elements in activity-dependent mRNA stability in hippocampal neurons. Philos Trans R Soc L B Biol Sci 369. https:\/\/doi.org\/10.1098\/rstb.2013.0509","DOI":"10.1098\/rstb.2013.0509"},{"key":"1868_CR32","doi-asserted-by":"publisher","first-page":"R56","DOI":"10.1186\/gb-2010-11-5-r56","volume":"11","author":"MA Faghihi","year":"2010","unstructured":"Faghihi MA, Zhang M, Huang J et al (2010) Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol 11:R56. https:\/\/doi.org\/10.1186\/gb-2010-11-5-r56","journal-title":"Genome Biol"},{"key":"1868_CR33","doi-asserted-by":"publisher","first-page":"e78023","DOI":"10.1371\/journal.pone.0078023","volume":"8","author":"S Arora","year":"2013","unstructured":"Arora S, Saini S, Fukuhara S et al (2013) MicroRNA-4723 inhibits prostate cancer growth through inactivation of the Abelson family of nonreceptor protein tyrosine kinases. PLoS One 8:e78023. https:\/\/doi.org\/10.1371\/journal.pone.0078023","journal-title":"PLoS One"},{"key":"1868_CR34","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1016\/j.nbd.2004.06.007","volume":"17","author":"AR Alvarez","year":"2004","unstructured":"Alvarez AR, Sandoval PC, Leal NR et al (2004) Activation of the neuronal c-Abl tyrosine kinase by amyloid-beta-peptide and reactive oxygen species. Neurobiol Dis 17:326\u2013336. https:\/\/doi.org\/10.1016\/j.nbd.2004.06.007","journal-title":"Neurobiol Dis"},{"key":"1868_CR35","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.molcel.2014.08.013","volume":"56","author":"M Gonzalez-Zu\u00f1iga","year":"2014","unstructured":"Gonzalez-Zu\u00f1iga M, Contreras PS, Estrada LD et al (2014) c-Abl stabilizes HDAC2 levels by tyrosine phosphorylation repressing neuronal gene expression in Alzheimer\u2019s disease. Mol Cell 56:163\u2013173. https:\/\/doi.org\/10.1016\/j.molcel.2014.08.013","journal-title":"Mol Cell"},{"key":"1868_CR36","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1007\/978-1-62703-640-5_2","volume":"1078","author":"J Kovalevich","year":"2013","unstructured":"Kovalevich J, Langford D (2013) Considerations for the use of SH-SY5Y neuroblastoma cells in neurobiology. Methods Mol Biol 1078:9\u201321. https:\/\/doi.org\/10.1007\/978-1-62703-640-5_2","journal-title":"Methods Mol Biol"},{"key":"1868_CR37","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1002\/cyto.a.20031","volume":"60A","author":"KH Gylys","year":"2004","unstructured":"Gylys KH, Fein JA, Yang F, Cole GM (2004) Enrichment of presynaptic and postsynaptic markers by size-based gating analysis of synaptosome preparations from rat and human cortex. Cytometry 60A:90\u201396. https:\/\/doi.org\/10.1002\/cyto.a.20031","journal-title":"Cytometry"},{"key":"1868_CR38","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1002\/1097-4547(20000715)61:2<186::AID-JNR9>3.0.CO;2-X","volume":"61","author":"KH Gylys","year":"2000","unstructured":"Gylys KH, Fein JA, Cole GM (2000) Quantitative characterization of crude synaptosomal fraction (P-2) components by flow cytometry. J Neurosci Res 61:186\u2013192. https:\/\/doi.org\/10.1002\/1097-4547(20000715)61:2<186::AID-JNR9>3.0.CO;2-X","journal-title":"J Neurosci Res"},{"key":"1868_CR39","doi-asserted-by":"publisher","first-page":"756","DOI":"10.1016\/j.neuron.2014.05.004","volume":"82","author":"TL Spires-Jones","year":"2014","unstructured":"Spires-Jones TL, Hyman BT (2014) The intersection of amyloid beta and tau at synapses in Alzheimer\u2019s disease. Neuron 82:756\u2013771. https:\/\/doi.org\/10.1016\/j.neuron.2014.05.004","journal-title":"Neuron"},{"key":"1868_CR40","doi-asserted-by":"publisher","first-page":"464","DOI":"10.3389\/fphys.2012.00464","volume":"3","author":"MC Dinamarca","year":"2012","unstructured":"Dinamarca MC, R\u00edos JA, Inestrosa NC (2012) Postsynaptic receptors for amyloid-\u03b2 oligomers as mediators of neuronal damage in Alzheimer\u2019s disease. Front Physiol 3:464. https:\/\/doi.org\/10.3389\/fphys.2012.00464","journal-title":"Front Physiol"},{"key":"1868_CR41","doi-asserted-by":"publisher","first-page":"27","DOI":"10.3233\/JAD-2008-14103","volume":"14","author":"JP Cogswell","year":"2008","unstructured":"Cogswell JP, Ward J, Taylor IA et al (2008) Identification of miRNA changes in Alzheimer\u2019s disease brain and CSF yields putative biomarkers and insights into disease pathways. J Alzheimers Dis 14:27\u201341","journal-title":"J Alzheimers Dis"},{"key":"1868_CR42","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1097\/WNR.0b013e3280148e8b","volume":"18","author":"WJ Lukiw","year":"2007","unstructured":"Lukiw WJ (2007) Micro-RNA speciation in fetal, adult and Alzheimer\u2019s disease hippocampus. Neuroreport 18:297\u2013300. https:\/\/doi.org\/10.1097\/WNR.0b013e3280148e8b","journal-title":"Neuroreport"},{"key":"1868_CR43","first-page":"263","volume":"1","author":"HM Schipper","year":"2007","unstructured":"Schipper HM, Maes OC, Chertkow HM, Wang E (2007) MicroRNA expression in Alzheimer blood mononuclear cells. Gene Regul Syst Bio 1:263\u2013274","journal-title":"Gene Regul Syst Bio"},{"key":"1868_CR44","doi-asserted-by":"publisher","first-page":"87","DOI":"10.3389\/fgene.2015.00087","volume":"6","author":"K Szafranski","year":"2015","unstructured":"Szafranski K, Abraham KJ, Mekhail K (2015) Non-coding RNA in neural function, disease, and aging. Front Genet 6:87. https:\/\/doi.org\/10.3389\/fgene.2015.00087","journal-title":"Front Genet"},{"key":"1868_CR45","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1186\/1755-8794-6-55","volume":"6","author":"W Li","year":"2013","unstructured":"Li W, Chen L, Qu X et al (2013) Unraveling the characteristics of microRNA regulation in the developmental and aging process of the human brain. BMC Med Genet 6:55. https:\/\/doi.org\/10.1186\/1755-8794-6-55","journal-title":"BMC Med Genet"},{"key":"1868_CR46","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1515\/revneuro-2017-0042","volume":"29","author":"R Dehghani","year":"2018","unstructured":"Dehghani R, Rahmani F, Rezaei N (2018) MicroRNA in Alzheimer\u2019s disease revisited: implications for major neuropathological mechanisms. Rev Neurosci 29:161\u2013182. https:\/\/doi.org\/10.1515\/revneuro-2017-0042","journal-title":"Rev Neurosci"},{"key":"1868_CR47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.pneurobio.2017.03.004","volume":"156","author":"MJ Millan","year":"2017","unstructured":"Millan MJ (2017) Linking deregulation of non-coding RNA to the core pathophysiology of Alzheimer\u2019s disease: an integrative review. Prog Neurobiol 156:1\u201368. https:\/\/doi.org\/10.1016\/j.pneurobio.2017.03.004","journal-title":"Prog Neurobiol"},{"key":"1868_CR48","doi-asserted-by":"publisher","first-page":"4282","DOI":"10.1038\/s41598-018-22701-2","volume":"8","author":"A Annese","year":"2018","unstructured":"Annese A, Manzari C, Lionetti C et al (2018) Whole transcriptome profiling of late-onset Alzheimer\u2019s disease patients provides insights into the molecular changes involved in the disease. Sci Rep 8:4282. https:\/\/doi.org\/10.1038\/s41598-018-22701-2","journal-title":"Sci Rep"},{"key":"1868_CR49","doi-asserted-by":"publisher","first-page":"342","DOI":"10.3389\/fneur.2017.00342","volume":"8","author":"J Zhao","year":"2017","unstructured":"Zhao J, Yue D, Zhou Y et al (2017) The role of microRNAs in A\u03b2 deposition and tau phosphorylation in Alzheimer\u2019s disease. Front Neurol 8:342. https:\/\/doi.org\/10.3389\/fneur.2017.00342","journal-title":"Front Neurol"},{"key":"1868_CR50","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1111\/j.1750-3639.2007.00120.x","volume":"18","author":"PT Nelson","year":"2008","unstructured":"Nelson PT, Wang W-X, Rajeev BW (2008) MicroRNAs (miRNAs) in neurodegenerative diseases. Brain Pathol 18:130\u2013138. https:\/\/doi.org\/10.1111\/j.1750-3639.2007.00120.x","journal-title":"Brain Pathol"},{"key":"1868_CR51","doi-asserted-by":"publisher","first-page":"40","DOI":"10.3389\/fphys.2015.00040","volume":"6","author":"GD Femminella","year":"2015","unstructured":"Femminella GD, Ferrara N, Rengo G (2015) The emerging role of microRNAs in Alzheimer\u2019s disease. Front Physiol 6:40. https:\/\/doi.org\/10.3389\/fphys.2015.00040","journal-title":"Front Physiol"},{"key":"1868_CR52","doi-asserted-by":"publisher","first-page":"837","DOI":"10.1038\/nrn2726","volume":"10","author":"SM Eacker","year":"2009","unstructured":"Eacker SM, Dawson TM, Dawson VL (2009) Understanding microRNAs in neurodegeneration. Nat Rev Neurosci 10:837\u2013841. https:\/\/doi.org\/10.1038\/nrn2726","journal-title":"Nat Rev Neurosci"},{"key":"1868_CR53","doi-asserted-by":"publisher","first-page":"741","DOI":"10.3233\/JAD-2010-101020","volume":"22","author":"MS Parihar","year":"2010","unstructured":"Parihar MS, Brewer GJ (2010) Amyloid-\u03b2 as a modulator of synaptic plasticity. J Alzheimers Dis 22:741\u2013763. https:\/\/doi.org\/10.3233\/JAD-2010-101020","journal-title":"J Alzheimers Dis"},{"key":"1868_CR54","doi-asserted-by":"publisher","unstructured":"Aksoy-Aksel A, Zampa F, Schratt G (2014) MicroRNAs and synaptic plasticity--a mutual relationship. Philos Trans R Soc L B Biol Sci 369. https:\/\/doi.org\/10.1098\/rstb.2013.0515","DOI":"10.1098\/rstb.2013.0515"},{"key":"1868_CR55","doi-asserted-by":"publisher","first-page":"136","DOI":"10.3389\/fncel.2013.00136","volume":"7","author":"SM Eacker","year":"2013","unstructured":"Eacker SM, Dawson TM, Dawson VL (2013) The interplay of microRNA and neuronal activity in health and disease. Front Cell Neurosci 7:136. https:\/\/doi.org\/10.3389\/fncel.2013.00136","journal-title":"Front Cell Neurosci"},{"key":"1868_CR56","doi-asserted-by":"publisher","first-page":"4959523","DOI":"10.1155\/2016\/4959523","volume":"2016","author":"Y Ye","year":"2016","unstructured":"Ye Y, Xu H, Su X, He X (2016) Role of microRNA in governing synaptic plasticity. Neural Plast 2016:4959523. https:\/\/doi.org\/10.1155\/2016\/4959523","journal-title":"Neural Plast"},{"key":"1868_CR57","doi-asserted-by":"publisher","first-page":"260","DOI":"10.2174\/1570159X14666160709001441","volume":"15","author":"WD Nadim","year":"2017","unstructured":"Nadim WD, Simion V, Benedetti H et al (2017) MicroRNAs in neurocognitive dysfunctions: new molecular targets for pharmacological treatments? Curr Neuropharmacol 15:260\u2013275. https:\/\/doi.org\/10.2174\/1570159X14666160709001441","journal-title":"Curr Neuropharmacol"},{"key":"1868_CR58","doi-asserted-by":"publisher","first-page":"e11070","DOI":"10.1371\/journal.pone.0011070","volume":"5","author":"N Schonrock","year":"2010","unstructured":"Schonrock N, Ke YD, Humphreys D et al (2010) Neuronal microRNA deregulation in response to Alzheimer\u2019s disease amyloid-beta. PLoS One 5:e11070. https:\/\/doi.org\/10.1371\/journal.pone.0011070","journal-title":"PLoS One"},{"key":"1868_CR59","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1038\/nrn2754","volume":"11","author":"E Jazin","year":"2010","unstructured":"Jazin E, Cahill L (2010) Sex differences in molecular neuroscience: from fruit flies to humans. Nat Rev Neurosci 11:9\u201317. https:\/\/doi.org\/10.1038\/nrn2754","journal-title":"Nat Rev Neurosci"},{"key":"1868_CR60","doi-asserted-by":"publisher","first-page":"e1000100","DOI":"10.1371\/journal.pgen.1000100","volume":"4","author":"B Reinius","year":"2008","unstructured":"Reinius B, Saetre P, Leonard JA et al (2008) An evolutionarily conserved sexual signature in the primate brain. PLoS Genet 4:e1000100. https:\/\/doi.org\/10.1371\/journal.pgen.1000100","journal-title":"PLoS Genet"},{"key":"1868_CR61","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1016\/S0169-328X(03)00339-5","volume":"118","author":"P Dewing","year":"2003","unstructured":"Dewing P, Shi T, Horvath S, Vilain E (2003) Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res Mol Brain Res 118:82\u201390","journal-title":"Brain Res Mol Brain Res"},{"key":"1868_CR62","doi-asserted-by":"publisher","first-page":"4767","DOI":"10.1038\/s41598-018-20959-0","volume":"8","author":"S Moradifard","year":"2018","unstructured":"Moradifard S, Hoseinbeyki M, Ganji SM, Minuchehr Z (2018) Analysis of microRNA and gene expression profiles in Alzheimer\u2019s disease: a meta-analysis approach. Sci Rep 8:4767. https:\/\/doi.org\/10.1038\/s41598-018-20959-0","journal-title":"Sci Rep"},{"key":"1868_CR63","doi-asserted-by":"publisher","first-page":"3184","DOI":"10.1038\/s41598-018-21596-3","volume":"8","author":"F Biundo","year":"2018","unstructured":"Biundo F, Del Prete D, Zhang H et al (2018) A role for tau in learning, memory and synaptic plasticity. Sci Rep 8:3184. https:\/\/doi.org\/10.1038\/s41598-018-21596-3","journal-title":"Sci Rep"},{"key":"1868_CR64","doi-asserted-by":"publisher","first-page":"7","DOI":"10.3389\/fnsyn.2016.00007","volume":"8","author":"F Antonucci","year":"2016","unstructured":"Antonucci F, Corradini I, Fossati G et al (2016) SNAP-25, a known presynaptic protein with emerging postsynaptic functions. Front Synaptic Neurosci 8:7. https:\/\/doi.org\/10.3389\/fnsyn.2016.00007","journal-title":"Front Synaptic Neurosci"},{"key":"1868_CR65","doi-asserted-by":"publisher","first-page":"699","DOI":"10.3233\/JPD-150642","volume":"5","author":"J Burr\u00e9","year":"2015","unstructured":"Burr\u00e9 J (2015) The synaptic function of \u03b1-synuclein. J Park Dis 5:699\u2013713. https:\/\/doi.org\/10.3233\/JPD-150642","journal-title":"J Park Dis"},{"key":"1868_CR66","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1016\/j.jbi.2011.05.002","volume":"44","author":"H Dweep","year":"2011","unstructured":"Dweep H, Sticht C, Pandey P, Gretz N (2011) miRWalk--database: prediction of possible miRNA binding sites by \u201cwalking\u201d the genes of three genomes. J Biomed Inform 44:839\u2013847. https:\/\/doi.org\/10.1016\/j.jbi.2011.05.002","journal-title":"J Biomed Inform"},{"key":"1868_CR67","doi-asserted-by":"publisher","first-page":"697","DOI":"10.1038\/nmeth.3485","volume":"12","author":"H Dweep","year":"2015","unstructured":"Dweep H, Gretz N (2015) miRWalk2.0: a comprehensive atlas of microRNA-target interactions. Nat Methods 12:697\u2013697. https:\/\/doi.org\/10.1038\/nmeth.3485","journal-title":"Nat Methods"},{"key":"1868_CR68","doi-asserted-by":"publisher","unstructured":"Catalanotto C, Cogoni C, Zardo G (2016) MicroRNA in control of gene expression: an overview of nuclear functions. Int J Mol Sci 17. https:\/\/doi.org\/10.3390\/ijms17101712","DOI":"10.3390\/ijms17101712"},{"key":"1868_CR69","unstructured":"Oliveros JC (2015) Venny. An interactive tool for comparing lists with Venn\u2019s diagrams."},{"key":"1868_CR70","doi-asserted-by":"publisher","first-page":"D284","DOI":"10.1093\/nar\/gki078","volume":"33","author":"H Mi","year":"2005","unstructured":"Mi H, Lazareva-Ulitsky B, Loo R et al (2005) The PANTHER database of protein families, subfamilies, functions and pathways. Nucleic Acids Res 33:D284\u2013D288. https:\/\/doi.org\/10.1093\/nar\/gki078","journal-title":"Nucleic Acids Res"},{"key":"1868_CR71","doi-asserted-by":"publisher","first-page":"2129","DOI":"10.1101\/gr.772403","volume":"13","author":"PD Thomas","year":"2003","unstructured":"Thomas PD, Campbell MJ, Kejariwal A et al (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13:2129\u20132141. https:\/\/doi.org\/10.1101\/gr.772403","journal-title":"Genome Res"}],"container-title":["Molecular Neurobiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s12035-020-01868-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s12035-020-01868-8\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s12035-020-01868-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,27]],"date-time":"2021-01-27T19:29:45Z","timestamp":1611775785000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s12035-020-01868-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,29]]},"references-count":71,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2020,5]]}},"alternative-id":["1868"],"URL":"https:\/\/doi.org\/10.1007\/s12035-020-01868-8","relation":{},"ISSN":["0893-7648","1559-1182"],"issn-type":[{"value":"0893-7648","type":"print"},{"value":"1559-1182","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,29]]},"assertion":[{"value":"15 September 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 January 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 January 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with Ethical Standards"}},{"value":"All applicable international, national, and\/or institutional guidelines for the care and use of animals were followed.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical Approval"}},{"value":"The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Disclaimer"}}]}}