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Music-performance regulates microRNAs in professional musicians
Musical training and performance require precise integration of multisensory and motor centres of the human brain and can be regarded as an epigenetic modifier of brain functions. Numerous studies have identified structural and functional differences between the brains of musicians and non-musicians...
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| Published in: | PeerJ (San Francisco, CA) CA), 2019-03, Vol.7, p.e6660-e6660, Article e6660 |
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| creator | Nair, Preethy Sasidharan Kuusi, Tuire Ahvenainen, Minna Philips, Anju K Järvelä, Irma |
| description | Musical training and performance require precise integration of multisensory and motor centres of the human brain and can be regarded as an epigenetic modifier of brain functions. Numerous studies have identified structural and functional differences between the brains of musicians and non-musicians and superior cognitive functions in musicians. Recently, music-listening and performance has also been shown to affect the regulation of several genes, many of which were identified in songbird singing. MicroRNAs affect gene regulation and studying their expression may give new insights into the epigenetic effect of music. Here, we studied the effect of 2 hours of classical music-performance on the peripheral blood microRNA expressions in professional musicians with respect to a control activity without music for the same duration. As detecting transcriptomic changes in the functional human brain remains a challenge for geneticists, we used peripheral blood to study music-performance induced microRNA changes and interpreted the results in terms of potential effects on brain function, based on the current knowledge about the microRNA function in blood and brain. We identified significant (FDR |
| doi_str_mv | 10.7717/peerj.6660 |
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Numerous studies have identified structural and functional differences between the brains of musicians and non-musicians and superior cognitive functions in musicians. Recently, music-listening and performance has also been shown to affect the regulation of several genes, many of which were identified in songbird singing. MicroRNAs affect gene regulation and studying their expression may give new insights into the epigenetic effect of music. Here, we studied the effect of 2 hours of classical music-performance on the peripheral blood microRNA expressions in professional musicians with respect to a control activity without music for the same duration. As detecting transcriptomic changes in the functional human brain remains a challenge for geneticists, we used peripheral blood to study music-performance induced microRNA changes and interpreted the results in terms of potential effects on brain function, based on the current knowledge about the microRNA function in blood and brain. We identified significant (FDR <0.05) up-regulation of five microRNAs; hsa-miR-3909, hsa-miR-30d-5p, hsa-miR-92a-3p, hsa-miR-222-3p and hsa-miR-30a-5p; and down-regulation of two microRNAs; hsa-miR-6803-3p and hsa-miR-1249-3p. hsa-miR-222-3p and hsa-miR-92a-3p putatively target FOXP2, which was found down-regulated by microRNA regulation in songbird singing. miR-30d and miR-222 corroborate microRNA response observed in zebra finch song-listening/learning. miR-222 is induced by ERK cascade, which is important for memory formation, motor neuron functions and neuronal plasticity. miR-222 is also activated by FOSL1, an immediate early gene from the FOS family of transcriptional regulators which are activated by auditory-motor stimuli. miR-222 and miR-92 promote neurite outgrowth by negatively regulating the neuronal growth inhibitor, PTEN, and by activating CREB expression and phosphorylation. The up-regulation of microRNAs previously found to be regulators of auditory and nervous system functions (miR-30d, miR-92a and miR-222) is indicative of the sensory perception processes associated with music-performance. Akt signalling pathway which has roles in cell survival, cell differentiation, activation of CREB signalling and dopamine transmission was one of the functions regulated by the up-regulated microRNAs; in accordance with functions identified from songbird learning. The up-regulated microRNAs were also found to be regulators of apoptosis, suggesting repression of apoptotic mechanisms in connection with music-performance. Furthermore, comparative analyses of the target genes of differentially expressed microRNAs with that of the song-responsive microRNAs in songbirds suggest convergent regulatory mechanisms underlying auditory perception.</description><identifier>ISSN: 2167-8359</identifier><identifier>EISSN: 2167-8359</identifier><identifier>DOI: 10.7717/peerj.6660</identifier><identifier>PMID: 30956902</identifier><language>eng</language><publisher>United States: PeerJ. Ltd</publisher><subject>AKT protein ; Analysis ; Apoptosis ; Auditory perception ; Auditory plasticity ; Axonogenesis ; Binomial distribution ; Bioinformatics ; Brain ; Brain research ; Cell activation ; Cell differentiation ; Cell survival ; Classical music ; Cognition ; Cognitive ability ; Communication ; Cyclic AMP response element-binding protein ; Dopamine ; Epigenetic inheritance ; Ethics ; Foxp2 protein ; Gene expression ; Gene regulation ; Genes ; Genetic regulation ; Genetics ; Genomes ; Genomics ; Hair ; Learning ; Memory ; MicroRNA ; MicroRNAs ; miRNA ; Music-performance ; Musical instruments ; Musical performances ; Musicians ; Musicians & conductors ; Nervous system ; Neurons ; Neurophysiology ; Neuroplasticity ; Neuroscience ; Neurosciences ; Peripheral blood ; Phenols (Class of compounds) ; Phosphorylation ; PTEN protein ; Quality ; Sensory integration ; Sequencing ; Signal transduction ; Statistical analysis ; Structure-function relationships ; Training ; Transcription ; Zebra finch</subject><ispartof>PeerJ (San Francisco, CA), 2019-03, Vol.7, p.e6660-e6660, Article e6660</ispartof><rights>COPYRIGHT 2019 PeerJ. Ltd.</rights><rights>2019 Nair et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 Nair et al. 2019 Nair et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c570t-9a62d11fea5e50ee303b9363a8e93cdc36648c85dbfbdb752c2fddb0cf72d15a3</citedby><cites>FETCH-LOGICAL-c570t-9a62d11fea5e50ee303b9363a8e93cdc36648c85dbfbdb752c2fddb0cf72d15a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2199722894/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2199722894?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768,74869</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30956902$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nair, Preethy Sasidharan</creatorcontrib><creatorcontrib>Kuusi, Tuire</creatorcontrib><creatorcontrib>Ahvenainen, Minna</creatorcontrib><creatorcontrib>Philips, Anju K</creatorcontrib><creatorcontrib>Järvelä, Irma</creatorcontrib><title>Music-performance regulates microRNAs in professional musicians</title><title>PeerJ (San Francisco, CA)</title><addtitle>PeerJ</addtitle><description>Musical training and performance require precise integration of multisensory and motor centres of the human brain and can be regarded as an epigenetic modifier of brain functions. Numerous studies have identified structural and functional differences between the brains of musicians and non-musicians and superior cognitive functions in musicians. Recently, music-listening and performance has also been shown to affect the regulation of several genes, many of which were identified in songbird singing. MicroRNAs affect gene regulation and studying their expression may give new insights into the epigenetic effect of music. Here, we studied the effect of 2 hours of classical music-performance on the peripheral blood microRNA expressions in professional musicians with respect to a control activity without music for the same duration. As detecting transcriptomic changes in the functional human brain remains a challenge for geneticists, we used peripheral blood to study music-performance induced microRNA changes and interpreted the results in terms of potential effects on brain function, based on the current knowledge about the microRNA function in blood and brain. We identified significant (FDR <0.05) up-regulation of five microRNAs; hsa-miR-3909, hsa-miR-30d-5p, hsa-miR-92a-3p, hsa-miR-222-3p and hsa-miR-30a-5p; and down-regulation of two microRNAs; hsa-miR-6803-3p and hsa-miR-1249-3p. hsa-miR-222-3p and hsa-miR-92a-3p putatively target FOXP2, which was found down-regulated by microRNA regulation in songbird singing. miR-30d and miR-222 corroborate microRNA response observed in zebra finch song-listening/learning. miR-222 is induced by ERK cascade, which is important for memory formation, motor neuron functions and neuronal plasticity. miR-222 is also activated by FOSL1, an immediate early gene from the FOS family of transcriptional regulators which are activated by auditory-motor stimuli. miR-222 and miR-92 promote neurite outgrowth by negatively regulating the neuronal growth inhibitor, PTEN, and by activating CREB expression and phosphorylation. The up-regulation of microRNAs previously found to be regulators of auditory and nervous system functions (miR-30d, miR-92a and miR-222) is indicative of the sensory perception processes associated with music-performance. Akt signalling pathway which has roles in cell survival, cell differentiation, activation of CREB signalling and dopamine transmission was one of the functions regulated by the up-regulated microRNAs; in accordance with functions identified from songbird learning. The up-regulated microRNAs were also found to be regulators of apoptosis, suggesting repression of apoptotic mechanisms in connection with music-performance. Furthermore, comparative analyses of the target genes of differentially expressed microRNAs with that of the song-responsive microRNAs in songbirds suggest convergent regulatory mechanisms underlying auditory perception.</description><subject>AKT protein</subject><subject>Analysis</subject><subject>Apoptosis</subject><subject>Auditory perception</subject><subject>Auditory plasticity</subject><subject>Axonogenesis</subject><subject>Binomial distribution</subject><subject>Bioinformatics</subject><subject>Brain</subject><subject>Brain research</subject><subject>Cell activation</subject><subject>Cell differentiation</subject><subject>Cell survival</subject><subject>Classical music</subject><subject>Cognition</subject><subject>Cognitive ability</subject><subject>Communication</subject><subject>Cyclic AMP response element-binding protein</subject><subject>Dopamine</subject><subject>Epigenetic inheritance</subject><subject>Ethics</subject><subject>Foxp2 protein</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genetic regulation</subject><subject>Genetics</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Hair</subject><subject>Learning</subject><subject>Memory</subject><subject>MicroRNA</subject><subject>MicroRNAs</subject><subject>miRNA</subject><subject>Music-performance</subject><subject>Musical instruments</subject><subject>Musical performances</subject><subject>Musicians</subject><subject>Musicians & conductors</subject><subject>Nervous system</subject><subject>Neurons</subject><subject>Neurophysiology</subject><subject>Neuroplasticity</subject><subject>Neuroscience</subject><subject>Neurosciences</subject><subject>Peripheral blood</subject><subject>Phenols (Class of compounds)</subject><subject>Phosphorylation</subject><subject>PTEN protein</subject><subject>Quality</subject><subject>Sensory integration</subject><subject>Sequencing</subject><subject>Signal transduction</subject><subject>Statistical analysis</subject><subject>Structure-function relationships</subject><subject>Training</subject><subject>Transcription</subject><subject>Zebra finch</subject><issn>2167-8359</issn><issn>2167-8359</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkl2L1DAUhoMo7rLujT9ACoKI0DEfTZrcKMPix8KqIHod0uRkJkPb1KQV_PdmdtZ1RkwuEpLnfUPOeRF6SvCqbUn7egJIu5UQAj9A55SItpaMq4dH-zN0mfMOlyGpwJI9RmcMKy4Upufo7aclB1tPkHxMgxktVAk2S29myNUQbIpfP69zFcZqStFDziGOpq-GvSqYMT9Bj7zpM1zerRfo-_t3364-1jdfPlxfrW9qy1s818oI6gjxYDhwDMAw6xQTzEhQzDrLhGikldx1vnNdy6ml3rkOW98WHTfsAl0ffF00Oz2lMJj0S0cT9O1BTBtt0hxsD9pSI6UQimDBGqV81wFuZUOw6bwDCsXrzcFrWroBnIVxTqY_MT29GcNWb-JPLZqGKkqLwcs7gxR_LJBnPYRsoe_NCHHJmlLMGyIEJwV9_g-6i0sqJSwUUaqlVKrmL7Ux5QNh9LG8a_emes0lbiSXlBVq9R-qTAelU3EEH8r5ieDFkWALpp-3OfbLXJqYT8FXB7D0O-cE_r4YBOt9zPRtzPQ-ZgV-dly-e_RPqNhvWXTMwg</recordid><startdate>20190329</startdate><enddate>20190329</enddate><creator>Nair, Preethy Sasidharan</creator><creator>Kuusi, Tuire</creator><creator>Ahvenainen, Minna</creator><creator>Philips, Anju K</creator><creator>Järvelä, Irma</creator><general>PeerJ. Ltd</general><general>PeerJ, Inc</general><general>PeerJ Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7XB</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20190329</creationdate><title>Music-performance regulates microRNAs in professional musicians</title><author>Nair, Preethy Sasidharan ; Kuusi, Tuire ; Ahvenainen, Minna ; Philips, Anju K ; Järvelä, Irma</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c570t-9a62d11fea5e50ee303b9363a8e93cdc36648c85dbfbdb752c2fddb0cf72d15a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>AKT protein</topic><topic>Analysis</topic><topic>Apoptosis</topic><topic>Auditory perception</topic><topic>Auditory plasticity</topic><topic>Axonogenesis</topic><topic>Binomial distribution</topic><topic>Bioinformatics</topic><topic>Brain</topic><topic>Brain research</topic><topic>Cell activation</topic><topic>Cell differentiation</topic><topic>Cell survival</topic><topic>Classical music</topic><topic>Cognition</topic><topic>Cognitive ability</topic><topic>Communication</topic><topic>Cyclic AMP response element-binding protein</topic><topic>Dopamine</topic><topic>Epigenetic inheritance</topic><topic>Ethics</topic><topic>Foxp2 protein</topic><topic>Gene expression</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genetic regulation</topic><topic>Genetics</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Hair</topic><topic>Learning</topic><topic>Memory</topic><topic>MicroRNA</topic><topic>MicroRNAs</topic><topic>miRNA</topic><topic>Music-performance</topic><topic>Musical instruments</topic><topic>Musical performances</topic><topic>Musicians</topic><topic>Musicians & conductors</topic><topic>Nervous system</topic><topic>Neurons</topic><topic>Neurophysiology</topic><topic>Neuroplasticity</topic><topic>Neuroscience</topic><topic>Neurosciences</topic><topic>Peripheral blood</topic><topic>Phenols (Class of compounds)</topic><topic>Phosphorylation</topic><topic>PTEN protein</topic><topic>Quality</topic><topic>Sensory integration</topic><topic>Sequencing</topic><topic>Signal transduction</topic><topic>Statistical analysis</topic><topic>Structure-function relationships</topic><topic>Training</topic><topic>Transcription</topic><topic>Zebra finch</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nair, Preethy Sasidharan</creatorcontrib><creatorcontrib>Kuusi, Tuire</creatorcontrib><creatorcontrib>Ahvenainen, Minna</creatorcontrib><creatorcontrib>Philips, Anju K</creatorcontrib><creatorcontrib>Järvelä, Irma</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>Biological Sciences</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DAOJ: Directory of Open Access Journals</collection><jtitle>PeerJ (San Francisco, CA)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nair, Preethy Sasidharan</au><au>Kuusi, Tuire</au><au>Ahvenainen, Minna</au><au>Philips, Anju K</au><au>Järvelä, Irma</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Music-performance regulates microRNAs in professional musicians</atitle><jtitle>PeerJ (San Francisco, CA)</jtitle><addtitle>PeerJ</addtitle><date>2019-03-29</date><risdate>2019</risdate><volume>7</volume><spage>e6660</spage><epage>e6660</epage><pages>e6660-e6660</pages><artnum>e6660</artnum><issn>2167-8359</issn><eissn>2167-8359</eissn><abstract>Musical training and performance require precise integration of multisensory and motor centres of the human brain and can be regarded as an epigenetic modifier of brain functions. Numerous studies have identified structural and functional differences between the brains of musicians and non-musicians and superior cognitive functions in musicians. Recently, music-listening and performance has also been shown to affect the regulation of several genes, many of which were identified in songbird singing. MicroRNAs affect gene regulation and studying their expression may give new insights into the epigenetic effect of music. Here, we studied the effect of 2 hours of classical music-performance on the peripheral blood microRNA expressions in professional musicians with respect to a control activity without music for the same duration. As detecting transcriptomic changes in the functional human brain remains a challenge for geneticists, we used peripheral blood to study music-performance induced microRNA changes and interpreted the results in terms of potential effects on brain function, based on the current knowledge about the microRNA function in blood and brain. We identified significant (FDR <0.05) up-regulation of five microRNAs; hsa-miR-3909, hsa-miR-30d-5p, hsa-miR-92a-3p, hsa-miR-222-3p and hsa-miR-30a-5p; and down-regulation of two microRNAs; hsa-miR-6803-3p and hsa-miR-1249-3p. hsa-miR-222-3p and hsa-miR-92a-3p putatively target FOXP2, which was found down-regulated by microRNA regulation in songbird singing. miR-30d and miR-222 corroborate microRNA response observed in zebra finch song-listening/learning. miR-222 is induced by ERK cascade, which is important for memory formation, motor neuron functions and neuronal plasticity. miR-222 is also activated by FOSL1, an immediate early gene from the FOS family of transcriptional regulators which are activated by auditory-motor stimuli. miR-222 and miR-92 promote neurite outgrowth by negatively regulating the neuronal growth inhibitor, PTEN, and by activating CREB expression and phosphorylation. The up-regulation of microRNAs previously found to be regulators of auditory and nervous system functions (miR-30d, miR-92a and miR-222) is indicative of the sensory perception processes associated with music-performance. Akt signalling pathway which has roles in cell survival, cell differentiation, activation of CREB signalling and dopamine transmission was one of the functions regulated by the up-regulated microRNAs; in accordance with functions identified from songbird learning. The up-regulated microRNAs were also found to be regulators of apoptosis, suggesting repression of apoptotic mechanisms in connection with music-performance. Furthermore, comparative analyses of the target genes of differentially expressed microRNAs with that of the song-responsive microRNAs in songbirds suggest convergent regulatory mechanisms underlying auditory perception.</abstract><cop>United States</cop><pub>PeerJ. Ltd</pub><pmid>30956902</pmid><doi>10.7717/peerj.6660</doi><oa>free_for_read</oa></addata></record> |
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| subjects | AKT protein Analysis Apoptosis Auditory perception Auditory plasticity Axonogenesis Binomial distribution Bioinformatics Brain Brain research Cell activation Cell differentiation Cell survival Classical music Cognition Cognitive ability Communication Cyclic AMP response element-binding protein Dopamine Epigenetic inheritance Ethics Foxp2 protein Gene expression Gene regulation Genes Genetic regulation Genetics Genomes Genomics Hair Learning Memory MicroRNA MicroRNAs miRNA Music-performance Musical instruments Musical performances Musicians Musicians & conductors Nervous system Neurons Neurophysiology Neuroplasticity Neuroscience Neurosciences Peripheral blood Phenols (Class of compounds) Phosphorylation PTEN protein Quality Sensory integration Sequencing Signal transduction Statistical analysis Structure-function relationships Training Transcription Zebra finch |
| title | Music-performance regulates microRNAs in professional musicians |
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