Non-coding RNA interact to regulate neuronal development and function

The human brain is one of the most complex biological systems, and the cognitive abilities have greatly expanded compared to invertebrates without much expansion in the number of protein coding genes. This suggests that gene regulation plays a very important role in the development and function of nervous system, by acting at multiple levels such as transcription and translation. In this article we discuss the regulatory roles of three classes of non-protein coding RNAs (ncRNAs)—microRNAs (miRNAs), piwi-interacting RNA (piRNAs) and long-non-coding RNA (lncRNA), in the process of neurogenesis and nervous function including control of synaptic plasticity and potential roles in neurodegenerative diseases. miRNAs are involved in diverse processes including neurogenesis where they channelize the cellular physiology toward neuronal differentiation. miRNAs can also indirectly influence neurogenesis by regulating the proliferation and self renewal of neural stem cells and are dysregulated in several neurodegenerative diseases. miRNAs are also known to regulate synaptic plasticity and are usually found to be co-expressed with their targets. The dynamics of gene regulation is thus dependent on the local architecture of the gene regulatory network (GRN) around the miRNA and its targets. piRNAs had been classically known to regulate transposons in the germ cells. However, piRNAs have been, recently, found to be expressed in the brain and possibly function by imparting epigenetic changes by DNA methylation. piRNAs are known to be maternally inherited and we assume that they may play a role in early development. We also explore the possible function of piRNAs in regulating the expansion of transposons in the brain. Brain is known to express several lncRNA but functional roles in brain development are attributed to a few lncRNA while functions of most of the them remain unknown. We review the roles of some known lncRNA and explore the other possible functions of lncRNAs including their interaction with miRNAs.

[1]  Y. Goshima,et al.  Identification of axon‐enriched MicroRNAs localized to growth cones of cortical neurons , 2014, Developmental neurobiology.

[2]  J. Flanagan,et al.  MicroRNA-132 Is Enriched in Developing Axons, Locally Regulates Rasa1 mRNA, and Promotes Axon Extension , 2013, The Journal of Neuroscience.

[3]  Di Wu,et al.  MicroRNA-431 regulates axon regeneration in mature sensory neurons by targeting the Wnt antagonist Kremen1 , 2013, Front. Mol. Neurosci..

[4]  L. Stanton,et al.  The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. , 2013, Molecular cell.

[5]  Amar N. Kar,et al.  MicroRNAs in the axon and presynaptic nerve terminal , 2013, Front. Cell. Neurosci..

[6]  Feng-Quan Zhou,et al.  MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. , 2013, Genes & development.

[7]  T. Sun,et al.  MicroRNA cluster miR-17-92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. , 2013, Cell reports.

[8]  Jun S. Song,et al.  Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. , 2013, Cell stem cell.

[9]  E. Lai,et al.  Widespread and extensive lengthening of 3′ UTRs in the mammalian brain , 2013, Genome research.

[10]  D. Tollervey,et al.  Mapping the Human miRNA Interactome by CLASH Reveals Frequent Noncanonical Binding , 2013, Cell.

[11]  Z. Weng,et al.  Transposition-Driven Genomic Heterogeneity in the Drosophila Brain , 2013, Science.

[12]  Di Wu,et al.  Molecular mechanisms of peripheral nerve regeneration: emerging roles of microRNAs , 2013, Front. Physiol..

[13]  Sebastian D. Mackowiak,et al.  Circular RNAs are a large class of animal RNAs with regulatory potency , 2013, Nature.

[14]  J. Kjems,et al.  Natural RNA circles function as efficient microRNA sponges , 2013, Nature.

[15]  M. Siomi,et al.  Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. , 2012, Genes & development.

[16]  Deeksha Bhartiya,et al.  Systematic Transcriptome Wide Analysis of lncRNA-miRNA Interactions , 2012, PloS one.

[17]  Chris Sander,et al.  A Role for Neuronal piRNAs in the Epigenetic Control of Memory-Related Synaptic Plasticity , 2012, Cell.

[18]  F. Guillemot,et al.  microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons , 2012, Nature Neuroscience.

[19]  C. Wahlestedt,et al.  Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation , 2012, Nature Biotechnology.

[20]  W. Filipowicz,et al.  HuR protein attenuates miRNA-mediated repression by promoting miRISC dissociation from the target RNA , 2012, Nucleic acids research.

[21]  Rory Johnson,et al.  Human long non‐coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors , 2012, The EMBO journal.

[22]  S. Blackshaw,et al.  The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity , 2011, Neural Development.

[23]  D. Zheng,et al.  RNA-Seq of Human Neurons Derived from iPS Cells Reveals Candidate Long Non-Coding RNAs Involved in Neurogenesis and Neuropsychiatric Disorders , 2011, PloS one.

[24]  James B. Uney,et al.  Axotomy-Induced miR-21 Promotes Axon Growth in Adult Dorsal Root Ganglion Neurons , 2011, PloS one.

[25]  Paulo P. Amaral,et al.  The Reality of Pervasive Transcription , 2011, PLoS biology.

[26]  B. S. Manjunath,et al.  Identification of piRNAs in the central nervous system. , 2011, RNA.

[27]  K. Mitsuya,et al.  Role for piRNAs and Noncoding RNA in de Novo DNA Methylation of the Imprinted Mouse Rasgrf1 Locus , 2011, Science.

[28]  M. Furuno,et al.  Competition between a noncoding exon and introns: Gomafu contains tandem UACUAAC repeats and associates with splicing factor-1 , 2011, Genes to cells : devoted to molecular & cellular mechanisms.

[29]  Carla Bosia,et al.  A Curated Database of miRNA Mediated Feed-Forward Loops Involving MYC as Master Regulator , 2011, PloS one.

[30]  S. Hammond,et al.  miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. , 2011, Genes & development.

[31]  S. Mello,et al.  The non-coding RNA BC1 is down-regulated in the hippocampus of Wistar Audiogenic Rat (WAR) strain after audiogenic kindling , 2011, Brain Research.

[32]  A. Fenton,et al.  Regulatory BC1 RNA and the Fragile X Mental Retardation Protein: Convergent Functionality in Brain , 2010, PloS one.

[33]  Michael Q. Zhang,et al.  A long nuclear‐retained non‐coding RNA regulates synaptogenesis by modulating gene expression , 2010, EMBO Journal.

[34]  J. Mattick,et al.  Long non-coding RNAs in nervous system function and disease , 2010, Brain Research.

[35]  Z. Paroo,et al.  Biochemical principles of small RNA pathways. , 2010, Annual review of biochemistry.

[36]  M. Nalls,et al.  Evidence for natural antisense transcript-mediated inhibition of microRNA function , 2010, Genome Biology.

[37]  Carla Bosia,et al.  The Role of Incoherent MicroRNA-Mediated Feedforward Loops in Noise Buffering , 2010, PLoS Comput. Biol..

[38]  J. Mattick,et al.  Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation , 2010, BMC Neuroscience.

[39]  K. Kosik,et al.  A Coordinated Local Translational Control Point at the Synapse Involving Relief from Silencing and MOV10 Degradation , 2009, Neuron.

[40]  Eric T. Wang,et al.  An Abundance of Ubiquitously Expressed Genes Revealed by Tissue Transcriptome Sequence Data , 2009, PLoS Comput. Biol..

[41]  A. Jacquier The complex eukaryotic transcriptome: unexpected pervasive transcription and novel small RNAs , 2009, Nature Reviews Genetics.

[42]  Antonin Morillon,et al.  Pervasive transcription constitutes a new level of eukaryotic genome regulation , 2009, EMBO reports.

[43]  Gene W. Yeo,et al.  L1 retrotransposition in human neural progenitor cells , 2009, Nature.

[44]  A. Fenton,et al.  BC1 Regulation of Metabotropic Glutamate Receptor-Mediated Neuronal Excitability , 2009, The Journal of Neuroscience.

[45]  J. Disterhoft,et al.  Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. , 2009, Nature neuroscience.

[46]  J. Disterhoft,et al.  Balanced gene regulation by an embryonic brain non-coding RNA is critical for GABA circuitry in adult hippocampus , 2009, Nature Neuroscience.

[47]  A. Mele,et al.  Ago HITS-CLIP decodes miRNA-mRNA interaction maps , 2009, Nature.

[48]  Julius Brennecke,et al.  Specialized piRNA Pathways Act in Germline and Somatic Tissues of the Drosophila Ovary , 2009, Cell.

[49]  Guoqiang Sun,et al.  A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination , 2009, Nature Structural &Molecular Biology.

[50]  J. Mattick,et al.  Long non-coding RNAs: insights into functions , 2009, Nature Reviews Genetics.

[51]  R. Gregory,et al.  Many roads to maturity: microRNA biogenesis pathways and their regulation , 2009, Nature Cell Biology.

[52]  Yi Xing,et al.  The Bifunctional microRNA miR-9/miR-9* Regulates REST and CoREST and Is Downregulated in Huntington's Disease , 2008, The Journal of Neuroscience.

[53]  G. Critchley,et al.  Novel noncoding antisense RNA transcribed from human anti-NOS2A locus is differentially regulated during neuronal differentiation of embryonic stem cells. , 2008, RNA.

[54]  Ravi Sachidanandam,et al.  A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. , 2008, Molecular cell.

[55]  Y. Hayashizaki,et al.  Nkx2.2 antisense RNA overexpression enhanced oligodendrocytic differentiation. , 2008, Biochemical and Biophysical Research Communications - BBRC.

[56]  T. Morgan,et al.  Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of β-secretase , 2008, Nature Medicine.

[57]  Hideaki Ando,et al.  An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP , 2008, Proceedings of the National Academy of Sciences.

[58]  O. Hobert Gene Regulation by Transcription Factors and MicroRNAs , 2008, Science.

[59]  W. Filipowicz,et al.  Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? , 2008, Nature Reviews Genetics.

[60]  S. Sunkin,et al.  Specific expression of long noncoding RNAs in the mouse brain , 2008, Proceedings of the National Academy of Sciences.

[61]  Reuven Agami,et al.  RNA-Binding Protein Dnd1 Inhibits MicroRNA Access to Target mRNA , 2007, Cell.

[62]  T. Maniatis,et al.  The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. , 2007, Molecular cell.

[63]  A. van Oudenaarden,et al.  MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. , 2007, Molecular cell.

[64]  U. Alon Network motifs: theory and experimental approaches , 2007, Nature Reviews Genetics.

[65]  Jae W. Lee,et al.  The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. , 2007, Genes & development.

[66]  F. Gage,et al.  A functional study of miR-124 in the developing neural tube. , 2007, Genes & development.

[67]  D. Haussler,et al.  An RNA gene expressed during cortical development evolved rapidly in humans , 2006, Nature.

[68]  Noam Shomron,et al.  Canalization of development by microRNAs , 2006, Nature Genetics.

[69]  Michael E. Greenberg,et al.  A brain-specific microRNA regulates dendritic spine development , 2006, Nature.

[70]  K. Williams,et al.  Dendritic BC1 RNA in translational control mechanisms , 2005, The Journal of cell biology.

[71]  Fred H. Gage,et al.  Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition , 2005, Nature.

[72]  C. Cepko,et al.  The Noncoding RNA Taurine Upregulated Gene 1 Is Required for Differentiation of the Murine Retina , 2005, Current Biology.

[73]  T. Ludwig,et al.  Role for Akt3/Protein Kinase Bγ in Attainment of Normal Brain Size , 2005, Molecular and Cellular Biology.

[74]  R. Oppenheim,et al.  Role of programmed cell death in normal neuronal development and function , 2004, Anatomical science international.

[75]  U. Alon,et al.  Ordering Genes in a Flagella Pathway by Analysis of Expression Kinetics from Living Bacteria , 2001, Science.

[76]  M. Sur,et al.  miR-132, an experience-dependent microRNA, is essential for visual cortex plasticity. , 2011, Nature neuroscience.