Nair Preethy Sasidharan, Kuusi Tuire, Ahvenainen Minna, Philips Anju K, Järvelä Irma
Department of Medical Genetics, University of Helsinki, Helsinki, Finland.
DocMus Doctoral School, Sibelius Academy, University of the Arts, Helsinki, Finland.
PeerJ. 2019 Mar 29;7:e6660. doi: 10.7717/peerj.6660. eCollection 2019.
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.
音乐训练和表演需要人类大脑多感官和运动中枢的精确整合,并且可被视为大脑功能的一种表观遗传修饰因子。众多研究已确定音乐家和非音乐家大脑之间的结构和功能差异,以及音乐家卓越的认知功能。最近,听音乐和表演也被证明会影响多个基因的调控,其中许多基因在鸣禽鸣叫中被识别出来。微小RNA影响基因调控,研究它们的表达可能会为音乐的表观遗传效应提供新的见解。在这里,我们研究了2小时的古典音乐表演对专业音乐家外周血微小RNA表达的影响,并与相同时长的无音乐对照活动进行比较。由于检测人类功能性大脑中的转录组变化对遗传学家来说仍然是一项挑战,我们利用外周血来研究音乐表演诱导的微小RNA变化,并根据目前关于血液和大脑中微小RNA功能的知识,从对大脑功能的潜在影响角度来解释结果。我们鉴定出5种微小RNA有显著上调(FDR<0.05);即hsa-miR-3909、hsa-miR-30d-5p、hsa-miR-92a-3p、hsa-miR-222-3p和hsa-miR-30a-5p;以及2种微小RNA下调;即hsa-miR-6803-3p和hsa-miR-1249-3p。hsa-miR-222-3p和hsa-miR-92a-3p可能靶向FOXP2,在鸣禽鸣叫中发现该基因通过微小RNA调控而下调。miR-30d和miR-222证实了在斑胸草雀听/学歌中观察到的微小RNA反应。miR-222由ERK级联反应诱导,这对记忆形成、运动神经元功能和神经元可塑性很重要。miR-222也被FOSL1激活,FOSL1是转录调节因子FOS家族的一个立即早期基因,被听觉-运动刺激激活。miR-222和miR-92通过负调控神经元生长抑制因子PTEN以及激活CREB表达和磷酸化来促进神经突生长。先前发现的对听觉和神经系统功能起调节作用的微小RNA(miR-30d、miR-92a和miR-222)的上调表明与音乐表演相关的感觉感知过程。在细胞存活、细胞分化、CREB信号激活和多巴胺传递中起作用的Akt信号通路是上调的微小RNA所调控的功能之一;这与从鸣禽学习中确定的功能一致。上调的微小RNA还被发现是细胞凋亡的调节因子,表明与音乐表演相关的凋亡机制受到抑制。此外,对差异表达微小RNA的靶基因与鸣禽中对歌声有反应的微小RNA的靶基因进行比较分析,表明听觉感知存在趋同的调控机制。