Skip to main content

Advertisement

SpringerLink
Log in

Regulation of gene expression during early neuronal differentiation: evidence for patterns conserved across neuron populations and vertebrate classes

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Analysis of transcription factor function during neurogenesis has provided a huge amount of data on the generation and specification of diverse neuron populations in the central and peripheral nervous systems of vertebrates. However, an understanding of the induction of key neuron functions including electrical information processing and synaptic transmission lags seriously behind. Whereas pan-neuronal markers such as neurofilaments, neuron-specific tubulin and RNA-binding proteins have often been included in developmental analysis, the molecular players underlying electrical activity and transmitter release have been neglected in studies addressing gene expression during neuronal induction. Here, I summarize the evidence for a distinct accumulation pattern of mRNAs for synaptic proteins, a pattern that is delayed compared with pan-neuronal gene expression during neurogenesis. The conservation of this pattern across diverse avian and mammalian neuron populations suggests a common mechanism for the regulation of various sets of neuronal genes during initial neuronal differentiation. The co-regulation of genes coding for synaptic proteins from embryonic to postnatal development indicates that the expression of the players required for synaptic transmission shares common regulatory features. For the ion channels involved in neuronal electrical activity, such as voltage-gated sodium channels, the situation is less clear because of the lack of comparative studies early during neurogenesis. Transcription factors have been characterized that regulate the expression of synaptic proteins in vitro and in vivo. They currently do not explain the co-regulation of these genes across different neuron populations. The neuron-restrictive silencing factor NRSF/REST targets a large gene set, but not all of the genes coding for pan-neuronal, synaptic and ion channel proteins. The discrepancy between NRSF/REST loss-of-function and silencer-to-activator-switch studies leaves the full functional implications of this factor open. Together with microRNAs, splicing regulators, chromatin remodellers and an increasing list of transcriptional regulators, the factor is embedded in feedback circuits with the potential to orchestrate neuronal differentiation. The precise regulation of the coordinated expression of proteins underlying key neuronal functions by these circuits during neuronal induction is a major emerging topic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abrajano JJ, Qureshi IA, Gokhan S, Molero AE, Zheng D, Bergman A, Mehler MF (2010) Corepressor for element-1-silencing transcription factor preferentially mediates gene networks underlying neural stem cell fate decisions. Proc Natl Acad Sci USA 107:16685–16690

    Article  PubMed  CAS  Google Scholar 

  • Abramovitz L, Shapira T, Ben-Dror I, Dror V, Granot L, Rousso T, Landoy E, Blau L, Thiel G, Vardimon L (2008) Dual role of NRSF/REST in activation and repression of the glucocorticoid response. J Biol Chem 283:110–119

    Article  PubMed  CAS  Google Scholar 

  • Albrieux M, Platel JC, Dupuis A, Villaz M, Moody WJ (2004) Early expression of sodium channel transcripts and sodium current by Cajal-Retzius cells in the preplate of the embryonic mouse neocortex. J Neurosci 24:1719–1725

    Article  PubMed  CAS  Google Scholar 

  • Anderson DJ, Axel R (1985) Molecular probes for the development and plasticity of neural crest derivatives. Cell 42:649–662

    Article  PubMed  CAS  Google Scholar 

  • Aoki H, Hara A, Era T, Kunisada T, Yamada Y (2012) Genetic ablation of Rest leads to in vitro-specific derepression of neuronal genes during neurogenesis. Development 139:667–677

    Article  PubMed  CAS  Google Scholar 

  • Balasubramaniyan V, Boddeke E, Bakels R, Küst B, Kooistra S, Veneman A, Copray S (2006) Effects of histone deacetylation inhibition on neuronal differentiation of embryonic mouse neural stem cells. Neuroscience 143:939–951

    Article  PubMed  CAS  Google Scholar 

  • Ballas N, Mandel G (2005) The many faces of REST oversee epigenetic programming of neuronal genes. Curr Opin Neurobiol 15:500

    Article  PubMed  CAS  Google Scholar 

  • Ballas N, Battaglioli E, Atouf F, Andres ME, Chenoweth J, Anderson ME, Burger C, Moniwa M, Davie JR, Bowers WJ, Federoff HJ, Rose DW, Rosenfeld MG, Brehm P, Mandel G (2001) Regulation of neuronal traits by a novel transcriptional complex. Neuron 31:353–365

    Article  PubMed  CAS  Google Scholar 

  • Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121:645–657

    Article  PubMed  CAS  Google Scholar 

  • Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395

    Article  PubMed  CAS  Google Scholar 

  • Barrera LO, Ren B (2006) The transcriptional regulatory code of eukaryotic cells—insights from genome-wide analysis of chromatin organization and transcription factor binding. Curr Opin Cell Biol 18:291–298

    Article  PubMed  CAS  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  PubMed  CAS  Google Scholar 

  • Battaglioli E, Andrés ME, Rose DW, Chenoweth JG, Rosenfeld MG, Anderson ME, Mandel G (2002) REST repression of neuronal genes requires components of the hSWI.SNF complex. J Biol Chem 277:41038–41045

    Article  PubMed  CAS  Google Scholar 

  • Beckh S, Noda M, Lübbert H, Numa S (1989) Differential regulation of three sodium channel messenger RNAs in the rat central nervous system during development. EMBO J 8:3611–3616

    PubMed  CAS  Google Scholar 

  • Belyaev ND, Wood IC, Bruce AW, Street M, Trinh JB, Buckley NJ (2004) Distinct RE-1 silencing transcription factor-containing complexes interact with different target genes. J Biol Chem 279:556–561

    Article  PubMed  CAS  Google Scholar 

  • Benn SC, Costigan M, Tate S, Fitzgerald M, Woolf CJ (2001) Developmental expression of the TTX-resistant voltage-gated sodium channels Nav1.8 (SNS) and Nav1.9 (SNS2) in primary sensory neurons. J Neurosci 21:6077–6085

    PubMed  CAS  Google Scholar 

  • Bennett GS, DiLullo C (1985) Expression of a neurofilament protein by the precursors of a subpopulation of ventral spinal cord neurons. Dev Biol 107:94–106

    Article  PubMed  CAS  Google Scholar 

  • Bernstein BE, Meissner A, Lander ES (2007) The mammalian epigenome. Cell 128:669–681

    Article  PubMed  CAS  Google Scholar 

  • Bonev B, Pisco A, Papalopulu N (2011) MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Dev Cell 20:19–32

    Article  PubMed  CAS  Google Scholar 

  • Broide RS, Redwine JM, Aftahi N, Young W, Bloom FE, Winrow CJ (2007) Distribution of histone deacetylases 1-11 in the rat brain. J Mol Neurosci 31:47–58

    Article  PubMed  CAS  Google Scholar 

  • Bruce AW, Donaldson IJ, Wood IC, Yerbury SA, Sadowski MI, Chapman M, Göttgens B, Buckley NJ (2004) Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes. Proc Natl Acad Sci USA 101:10458–10463

    Article  PubMed  CAS  Google Scholar 

  • Bultman S, Gebuhr T, Yee D, La Mantia C, Nicholson J, Gilliam A, Randazzo F, Metzger D, Chambon P, Crabtree G, Magnuson T (2000) A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6:1287–1295

    Article  PubMed  CAS  Google Scholar 

  • Cao X, Pfaff SL, Gage FH (2007) A functional study of miR-124 in the developing neural tube. Genes Dev 21:531–536

    Article  PubMed  CAS  Google Scholar 

  • Carden MJ, Trojanowski JQ, Schlaepfer WW, Lee VM (1987) Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J Neurosci 7:3489–3504

    PubMed  CAS  Google Scholar 

  • Catterall WA, Goldin AL, Waxman SG (2005) International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397–409

    Article  PubMed  CAS  Google Scholar 

  • Chen ZF, Paquette AJ, Anderson DJ (1998) NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nat Genet 20:136–142

    Article  PubMed  CAS  Google Scholar 

  • Chen CL, Broom DC, Liu Y, Nooij JC de, Li Z, Cen C, Samad OA, Jessell TM, Woolf CJ, Ma Q (2006) Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49:365–377

    Article  PubMed  CAS  Google Scholar 

  • Cheng LC, Pastrana E, Tavazoie M, Doetsch F (2009) miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 12:399–408

    Article  PubMed  CAS  Google Scholar 

  • Chong JA, Tapia-Ramírez J, Kim S, Toledo-Aral JJ, Zheng Y, Boutros MC, Altshuller YM, Frohman MA, Kraner SD, Mandel G (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80:949–957

    Article  PubMed  CAS  Google Scholar 

  • Conaco C, Otto S, Han JJ, Mandel G (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA 103:2422–2427

    Article  PubMed  CAS  Google Scholar 

  • Crandall JE, Jacobson M, Kosik KS (1986) Ontogenesis of microtubule-associated protein 2 (MAP2) in embryonic mouse cortex. Brain Res 393:127–133

    PubMed  CAS  Google Scholar 

  • Curmi PA, Gavet O, Charbaut E, Ozon S, Lachkar-Colmerauer S, Manceau V, Siavoshian S, Maucuer A, Sobel A (1999) Stathmin and its phosphoprotein family: general properties, biochemical and functional interaction with tubulin. Cell Struct Funct 24:345–357

    Article  PubMed  CAS  Google Scholar 

  • Darnell DK, Kaur S, Stanislaw S, Konieczka JH, Yatskievych TA, Antin PB (2006) MicroRNA expression during chick embryo development. Dev Dyn 235:3156–3165

    Article  PubMed  CAS  Google Scholar 

  • Delaloy C, Liu L, Lee JA, Su H, Shen F, Yang GY, Young WL, Ivey KN, Gao FB (2010) MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6:323–335

    Article  PubMed  CAS  Google Scholar 

  • Deschênes-Furry J, Perrone-Bizzozero N, Jasmin BJ (2006) The RNA-binding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. Bioessays 28:822–833

    Article  PubMed  CAS  Google Scholar 

  • Djouhri L, Fang X, Okuse K, Wood JN, Berry CM, Lawson SN (2003) The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol (Lond) 550:739–752

    Article  CAS  Google Scholar 

  • Dráberová E, Del Valle L, Gordon J, Marková V, Smejkalová B, Bertrand L, Chadarévian JP de, Agamanolis DP, Legido A, Khalili K, Dráber P, Katsetos CD (2008) Class III beta-tubulin is constitutively coexpressed with glial fibrillary acidic protein and nestin in midgestational human fetal astrocytes: implications for phenotypic identity. J Neuropathol Exp Neurol 67:341–354

    Article  PubMed  Google Scholar 

  • Drews VL, Lieberman AP, Meisler MH (2005) Multiple transcripts of sodium channel SCN8A (Na(V)1.6) with alternative 5′- and 3′-untranslated regions and initial characterization of the SCN8A promoter. Genomics 85:245–257

    Article  PubMed  CAS  Google Scholar 

  • Drews VL, Shi K, Haan G de, Meisler MH (2007) Identification of evolutionarily conserved, functional noncoding elements in the promoter region of the sodium channel gene SCN8A. Mamm Genome 18:723–731

    Article  PubMed  CAS  Google Scholar 

  • Dykes IM, Lanier J, Eng SR, Turner EE (2010) Brn3a regulates neuronal subtype specification in the trigeminal ganglion by promoting Runx expression during sensory differentiation. Neural Dev 5:3

    Article  PubMed  CAS  Google Scholar 

  • Ekici M, Hohl M, Schuit F, Martínez-Serrano A, Thiel G (2008) Transcription of genes encoding synaptic vesicle proteins in human neural stem cells: chromatin accessibility, histone methylation pattern, and the essential role of rest. J Biol Chem 283:9257–9268

    Article  PubMed  CAS  Google Scholar 

  • Ekici M, Keim A, Rössler OG, Hohl M, Thiel G (2012) Chromatin structure and expression of the AMPA receptor subunit Glur2 in human glioma cells: major regulatory role of REST and Sp1. J Cell Biochem 113:528–543

    Article  PubMed  CAS  Google Scholar 

  • Elfring LK, Daniel C, Papoulas O, Deuring R, Sarte M, Moseley S, Beek SJ, Waldrip WR, Daubresse G, DePace A, Kennison JA, Tamkun JW (1998) Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2. Genetics 148:251–265

    PubMed  CAS  Google Scholar 

  • Eng SR, Lanier J, Fedtsova N, Turner EE (2004) Coordinated regulation of gene expression by Brn3a in developing sensory ganglia. Development 131:3859–3870

    Article  PubMed  CAS  Google Scholar 

  • Ernsberger U, Patzke H, Tissier-Seta JP, Reh T, Goridis C, Rohrer H (1995) The expression of tyrosine hydroxylase and the transcription factors cPhox-2 and Cash-1: evidence for distinct inductive steps in the differentiation of chick sympathetic precursor cells. Mech Dev 52:125–136

    Article  PubMed  CAS  Google Scholar 

  • Farah MH, Olson JM, Sucic HB, Hume RI, Tapscott SJ, Turner DL (2000) Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127:693–702

    PubMed  CAS  Google Scholar 

  • Ferreira A, Busciglio J, Cáceres A (1987) An immunocytochemical analysis of the ontogeny of the microtubule-associated proteins MAP-2 and Tau in the nervous system of the rat. Dev Brain Res 34:9–31

    Article  CAS  Google Scholar 

  • Gao FB (2010) Context-dependent functions of specific microRNAs in neuronal development. Neural Dev 5:25

    Article  PubMed  CAS  Google Scholar 

  • Gao Z, Ure K, Ding P, Nashaat M, Yuan L, Ma J, Hammer RE, Hsieh J (2011) The master negative regulator REST/NRSF controls adult neurogenesis by restraining the neurogenic program in quiescent stem cells. J Neurosci 31:9772–9786

    Article  PubMed  CAS  Google Scholar 

  • Goedert M, Crowther RA, Garner CC (1991) Molecular characterization of microtubule-associated proteins tau and MAP2. Trends Neurosci 14:193–199

    Article  PubMed  CAS  Google Scholar 

  • Gordon D, Merrick D, Auld V, Dunn R, Goldin AL, Davidson N, Catterall WA (1987) Tissue-specific expression of the RI and RII sodium channel subtypes. Proc Natl Acad Sci USA 84:8682–8686

    Article  PubMed  CAS  Google Scholar 

  • Greenway DJ, Street M, Jeffries A, Buckley NJ (2007) RE1 silencing transcription factor maintains a repressive chromatin environment in embryonic hippocampal neural stem cells. Stem Cells 25:354–363

    Article  PubMed  CAS  Google Scholar 

  • Grenningloh G, Soehrman S, Bondallaz P, Ruchti E, Cadas H (2004) Role of the microtubule destabilizing proteins SCG10 and stathmin in neuronal growth. J Neurobiol 58:60–69

    Article  PubMed  CAS  Google Scholar 

  • Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88

    Article  PubMed  CAS  Google Scholar 

  • Gupta SK, Gressens P, Mani S (2009) NRSF downregulation induces neuronal differentiation in mouse embryonic stem cells. Differentiation 77:19–28

    Article  PubMed  CAS  Google Scholar 

  • Gurrola-Diaz C, Lacroix J, Dihlmann S, Becker CM, Knebel DM von (2003) Reduced expression of the neuron restrictive silencer factor permits transcription of glycine receptor alpha1 subunit in small-cell lung cancer cells. Oncogene 22:5636–5645

    Article  PubMed  CAS  Google Scholar 

  • Hadley D, Murphy T, Valladares O, Hannenhalli S, Ungar L, Kim J, Bućan M (2006) Patterns of sequence conservation in presynaptic neural genes. Genome Biol 7:R105

    Article  PubMed  CAS  Google Scholar 

  • Han X, Wu X, Chung WY, Li T, Nekrutenko A, Altman NS, Chen G, Ma H (2009) Transcriptome of embryonic and neonatal mouse cortex by high-throughput RNA sequencing. Proc Natl Acad Sci USA 106:12741–12746

    Article  PubMed  CAS  Google Scholar 

  • Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39:311–318

    Article  PubMed  CAS  Google Scholar 

  • Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108–112

    Article  PubMed  CAS  Google Scholar 

  • Hirabayashi Y, Gotoh Y (2010) Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 11:377–388

    Article  PubMed  CAS  Google Scholar 

  • Hirabayashi Y, Suzki N, Tsuboi M, Endo TA, Toyoda T, Shinga J, Koseki H, Vidal M, Gotoh Y (2009) Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63:600–613

    Article  PubMed  CAS  Google Scholar 

  • Ho L, Ronan JL, Wu J, Staahl BT, Chen L, Kuo A, Lessard J, Nesvizhskii AI, Ranish J, Crabtree GR (2009) An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci USA 106:5181–5186

    Article  PubMed  CAS  Google Scholar 

  • Hohl M, Thiel G (2005) Cell type-specific regulation of RE-1 silencing transcription factor (REST) target genes. Eur J Neurosci 22:2216–2230

    Article  PubMed  Google Scholar 

  • Howard PW, Jue SF, Maurer RA (2009) Expression of the synaptotagmin I gene is enhanced by binding of the pituitary-specific transcription factor, POU1F1. Mol Endocrinol 23:1563–1571

    Article  PubMed  CAS  Google Scholar 

  • Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH (2004) Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci USA 101:16659–16664

    Article  PubMed  CAS  Google Scholar 

  • Huang Y, Myers SJ, Dingledine R (1999) Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat Neurosci 2:867–872

    Article  PubMed  CAS  Google Scholar 

  • Iwanaga T, Takahashi Y, Fujita T (1989) Immunohistochemistry of neuron-specific and glia-specific proteins. Arch Histol Cytol 52 (Suppl):13–24

    Article  PubMed  Google Scholar 

  • Johnson DS, Mortazavi A, Myers RM, Wold B (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science 316:1497–1502

    Article  PubMed  CAS  Google Scholar 

  • Johnson R, Teh CH, Kunarso G, Wong KY, Srinivasan G, Cooper ML, Volta M, Chan SS, Lipovich L, Pollard SM, Karuturi RK, Wei CL, Buckley NJ, Stanton LW (2008) REST regulates distinct transcriptional networks in embryonic and neural stem cells. PLoS Biol 6:e256

    Article  PubMed  CAS  Google Scholar 

  • Jørgensen HF, Terry A, Beretta C, Pereira CF, Leleu M, Chen ZF, Kelly C, Merkenschlager M, Fisher AG (2009a) REST selectively represses a subset of RE1-containing neuronal genes in mouse embryonic stem cells. Development 136:715–721

    Article  PubMed  CAS  Google Scholar 

  • Jørgensen HF, Chen ZF, Merkenschlager M, Fisher AG (2009b) Is REST required for ESC pluripotency? Nature 457:E4–E5

    Article  PubMed  CAS  Google Scholar 

  • Juliandi B, Abematsu M, Nakashima K (2010) Chromatin remodeling in neural stem cell differentiation. Curr Opin Neurobiol 20:408–415

    Article  PubMed  CAS  Google Scholar 

  • Kapsimali M, Kloosterman WP, Bruijn E de, Rosa F, Plasterk RH, Wilson SW (2007) MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol 8:R173

    Article  PubMed  CAS  Google Scholar 

  • Kasai N, Fukushima K, Ueki Y, Prasad S, Nosakowski J, Sugata K, Sugata A, Nishizaki K, Meyer NC, Smith RJ (2001) Genomic structures of SCN2A and SCN3A—candidate genes for deafness at the DFNA16 locus. Gene 264:113–122

    Article  PubMed  CAS  Google Scholar 

  • Kim HJ, Rosenfeld MG (2010) Epigenetic control of stem cell fate to neurons and glia. Arch Pharm Res 33:1467–1473

    Article  PubMed  CAS  Google Scholar 

  • Kim JK, Huh SO, Choi H, Lee KS, Shin D, Lee C, Nam JS, Kim H, Chung H, Lee HW, Park SD, Seong RH (2001) Srg3, a mouse homolog of yeast SWI3, is essential for early embryogenesis and involved in brain development. Mol Cell Biol 21:7787–7795

    Article  PubMed  CAS  Google Scholar 

  • Kloosterman WP, Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11:441–450

    Article  PubMed  CAS  Google Scholar 

  • Koizumi K, Higashida H, Yoo S, Islam MS, Ivanov AI, Guo V, Pozzi P, Yu SH, Rovescalli AC, Tang D, Nirenberg M (2007) RNA interference screen to identify genes required for Drosophila embryonic nervous system development. Proc Natl Acad Sci USA 104:5626–5631

    Article  PubMed  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    Article  PubMed  CAS  Google Scholar 

  • Kraner SD, Chong JA, Tsay HJ, Mandel G (1992) Silencing the type II sodium channel gene: a model for neural-specific gene regulation. Neuron 9:37–44

    Article  PubMed  CAS  Google Scholar 

  • Kuwabara T, Hsieh J, Nakashima K, Taira K, Gage FH (2004) A small modulatory dsRNA specifies the fate of adult neural stem cells. Cell 116:779–793

    Article  PubMed  CAS  Google Scholar 

  • Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12:735–739

    Article  PubMed  CAS  Google Scholar 

  • Lamba DA, Hayes S, Karl MO, Reh T (2008) Baf60c is a component of the neural progenitor-specific BAF complex in developing retina. Dev Dyn 237:3016–3023

    Article  PubMed  CAS  Google Scholar 

  • Laneve P, Gioia U, Andriotto A, Moretti F, Bozzoni I, Caffarelli E (2010) A minicircuitry involving REST and CREB controls miR-9-2 expression during human neuronal differentiation. Nucleic Acids Res 38:6895–6905

    Article  PubMed  CAS  Google Scholar 

  • Lanier J, Quina LA, Eng SR, Cox E, Turner EE (2007) Brn3a target gene recognition in embryonic sensory neurons. Dev Biol 302:703–716

    Article  PubMed  CAS  Google Scholar 

  • Lanier J, Dykes IM, Nissen S, Eng SR, Turner EE (2009) Brn3a regulates the transition from neurogenesis to terminal differentiation and represses non-neural gene expression in the trigeminal ganglion. Dev Dyn 238:3065–3079

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Lee SK (2010) Crucial roles of histone-modifying enzymes in mediating neural cell-type specification. Curr Opin Neurobiol 20:29–36

    Article  PubMed  CAS  Google Scholar 

  • Lee MK, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A (1990) The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton 17:118–132

    Article  PubMed  CAS  Google Scholar 

  • Lessard J, Wu JI, Ranish JA, Wan M, Winslow MM, Staahl BT, Wu H, Aebersold R, Graef IA, Crabtree GR (2007) An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55:201–215

    Article  PubMed  CAS  Google Scholar 

  • Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L (2008) MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci 11:641–648

    Article  PubMed  CAS  Google Scholar 

  • Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769–773

    Article  PubMed  CAS  Google Scholar 

  • Lim DA, Huang YC, Swigut T, Mirick AL, Garcia-Verdugo JM, Wysocka J, Ernst P, Alvarez-Buylla A (2009) Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458:529–533

    Article  PubMed  CAS  Google Scholar 

  • Liu R, Hannenhalli S, Bucan M (2009) Motifs and cis-regulatory modules mediating the expression of genes co-expressed in presynaptic neurons. Genome Biol 10:R72

    Article  PubMed  CAS  Google Scholar 

  • Lunyak VV, Burgess R, Prefontaine GG, Nelson C, Sze SH, Chenoweth J, Schwartz P, Pevzner PA, Glass C, Mandel G, Rosenfeld MG (2002) Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science 298:1747–1752

    Article  PubMed  CAS  Google Scholar 

  • Magin A, Lietz M, Cibelli G, Thiel G (2002) RE-1 silencing transcription factor-4 (REST4) is neither a transcriptional repressor nor a de-repressor. Neurochem Int 40:195–202

    Article  PubMed  CAS  Google Scholar 

  • Maiorano NA, Mallamaci A (2009) Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev 4:40

    Article  PubMed  CAS  Google Scholar 

  • Makeyev EV, Zhang J, Carrasco MA, Maniatis T (2007) The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol Cell 27:435–448

    Article  PubMed  CAS  Google Scholar 

  • Mao CA, Tsai WW, Cho JH, Pan P, Barton MC, Klein WH (2011) Neuronal transcriptional repressor REST suppresses an Atoh7-independent program for initiating retinal ganglion cell development. Dev Biol 349:90–99

    Article  PubMed  CAS  Google Scholar 

  • Marazzi G, Buckley KM (1993) Accumulation of mRNAs encoding synaptic vesicle-specific proteins precedes neurite extension during early neuronal development. Dev Dyn 197:115–124

    Article  PubMed  CAS  Google Scholar 

  • Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343–349

    Article  PubMed  CAS  Google Scholar 

  • Matus A (1988) Microtubule-associated proteins: their potential role in determining neuronal morphology. Annu Rev Neurosci 11:29–44

    Article  PubMed  CAS  Google Scholar 

  • Maue RA, Kraner SD, Goodman RH, Mandel G (1990) Neuron-specific expression of the rat brain type II sodium channel gene is directed by upstream regulatory elements. Neuron 4:223–231

    Article  PubMed  CAS  Google Scholar 

  • McKee AE, Minet E, Stern C, Riahi S, Stiles CD, Silver PA (2005) A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev Biol 5:14

    Article  PubMed  CAS  Google Scholar 

  • Menezes JR, Luskin MB (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 14:5399–5416

    PubMed  CAS  Google Scholar 

  • Messmer K, Shen WB, Remington M, Fishman PS (2011) Induction of neural differentiation by the transcription factor NeuroD2. Int J Dev Neurosci (in press)

  • Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553–560

    Article  PubMed  CAS  Google Scholar 

  • Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schübeler D (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30:755–766

    Article  PubMed  CAS  Google Scholar 

  • Mori N, Morii H (2002) SCG10-related neuronal growth-associated proteins in neural development, plasticity, degeneration, and aging. J Neurosci Res 70:264–273

    Article  PubMed  CAS  Google Scholar 

  • Mori N, Stein R, Sigmund O, Anderson DJ (1990) A cell type-preferred silencer element that controls the neural-specific expression of the SCG10 gene. Neuron 4:583–594

    Article  PubMed  CAS  Google Scholar 

  • Mori N, Schoenherr C, Vandenbergh DJ, Anderson DJ (1992) A common silencer element in the SCG10 and type II Na+ channel genes binds a factor present in nonneuronal cells but not in neuronal cells. Neuron 9:45–54

    Article  PubMed  CAS  Google Scholar 

  • Mortazavi A, Leeper Thompson EC, Garcia ST, Myers RM, Wold B (2006) Comparative genomics modeling of the NRSF/REST repressor network: from single conserved sites to genome-wide repertoire. Genome Res 16:1208–1221

    Article  PubMed  CAS  Google Scholar 

  • Moskowitz PF, Oblinger MM (1995) Transcriptional and post-transcriptional mechanisms regulating neurofilament and tubulin gene expression during normal development of the rat brain. Brain Res Mol Brain Res 30:211–222

    Article  PubMed  CAS  Google Scholar 

  • Müller R, Heinrich M, Heck S, Blohm D, Richter-Landsberg C (1997) Expression of microtubule-associated proteins MAP2 and tau in cultured rat brain oligodendrocytes. Cell Tissue Res 288:239–249

    Article  PubMed  Google Scholar 

  • Olave I, Wang W, Xue Y, Kuo A, Crabtree GR (2002) Identification of a polymorphic, neuron-specific chromatin remodeling complex. Genes Dev 16:2509-2517

    Article  PubMed  CAS  Google Scholar 

  • Ooi L, Belyaev ND, Miyake K, Wood IC, Buckley NJ (2006) BRG1 chromatin remodeling activity is required for efficient chromatin binding by repressor element 1-silencing transcription factor (REST) and facilitates REST-mediated repression. J Biol Chem 281:38974–38980

    Article  PubMed  CAS  Google Scholar 

  • Otto SJ, McCorkle SR, Hover J, Conaco C, Han JJ, Impey S, Yochum GS, Dunn JJ, Goodman RH, Mandel G (2007) A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J Neurosci 27:6729–6739

    Article  PubMed  CAS  Google Scholar 

  • Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL (2008) The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J Neurosci 28:14341–14346

    Article  PubMed  CAS  Google Scholar 

  • Palm K, Belluardo N, Metsis M, Timmusk T (1998) Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene. J Neurosci 18:1280–1296

    PubMed  CAS  Google Scholar 

  • Palm K, Metsis M, Timmusk T (1999) Neuron-specific splicing of zinc finger transcription factor REST/NRSF/XBR is frequent in neuroblastomas and conserved in human, mouse and rat. Brain Res Mol Brain Res 72:30–39

    Article  PubMed  CAS  Google Scholar 

  • Pang ZP, Südhof TC (2010) Cell biology of Ca2+-triggered exocytosis. Curr Opin Cell Biol 22:496–505

    Article  PubMed  CAS  Google Scholar 

  • Pang ZP, Yang N, Vierbuchen T, Ostermeier A, Fuentes DR, Yang TQ, Citri A, Sebastiano V, Marro S, Südhof TC, Wernig M (2011) Induction of human neuronal cells by defined transcription factors. Nature 476:220–223

    PubMed  CAS  Google Scholar 

  • Paquette AJ, Perez SE, Anderson DJ (2000) Constitutive expression of the neuron-restrictive silencer factor (NRSF)/REST in differentiating neurons disrupts neuronal gene expression and causes axon pathfinding errors in vivo. Proc Natl Acad Sci USA 97:12318–12323

    Article  PubMed  CAS  Google Scholar 

  • Pascale A, Amadio M, Quattrone A (2008) Defining a neuron: neuronal ELAV proteins. Cell Mol Life Sci 65:128–140

    Article  PubMed  CAS  Google Scholar 

  • Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF (1999) The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:366–370

    Article  PubMed  CAS  Google Scholar 

  • Patzke H, Ernsberger U (2000) Expression of neurexin Ialpha splice variants in sympathetic neurons: selective changes during differentiation and in response to neurotrophins. Mol Cell Neurosci 15:561–572

    Article  PubMed  CAS  Google Scholar 

  • Patzke H, Reissmann E, Stanke M, Bixby JL, Ernsberger U (2001) BMP growth factors and Phox2 transcription factors can induce synaptotagmin I and neurexin I during sympathetic neuron development. Mech Dev 108:149–159

    Article  PubMed  CAS  Google Scholar 

  • Pereira JD, Sansom SN, Smith J, Dobenecker MW, Tarakhovsky A, Livesey FJ (2010) Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc Natl Acad Sci USA 107:15957–15962

    Article  PubMed  CAS  Google Scholar 

  • Plummer NW, McBurney MW, Meisler MH (1997) Alternative splicing of the sodium channel SCN8A predicts a truncated two-domain protein in fetal brain and non-neuronal cells. J Biol Chem 272:24008–24015

    Article  PubMed  CAS  Google Scholar 

  • Puhl HL 3rd, Ikeda SR (2008) Identification of the sensory neuron specific regulatory region for the mouse gene encoding the voltage-gated sodium channel NaV1.8. J Neurochem 106:1209–1224

    Article  PubMed  CAS  Google Scholar 

  • Qureshi IA, Gokhan S, Mehler MF (2010) REST and CoREST are transcriptional and epigenetic regulators of seminal neural fate decisions. Cell Cycle 9:4477–4486

    Article  PubMed  CAS  Google Scholar 

  • Raj B, O'Hanlon D, Vessey JP, Pan Q, Ray D, Buckley NJ, Miller FD, Blencowe BJ (2011) Cross-regulation between an alternative splicing activator and a transcription repressor controls neurogenesis. Mol Cell 43:843–850

    Article  PubMed  CAS  Google Scholar 

  • Randazzo FM, Khavari P, Crabtree G, Tamkun J, Rossant J (1994) brg1: A putative murine homologue of the Drosophila brahma gene, a homeotic gene regulator. Dev Biol 161:229–242

    Article  PubMed  Google Scholar 

  • Ravanpay AC, Hansen SJ, Olson JM (2010) Transcriptional inhibition of REST by NeuroD2 during neuronal differentiation. Mol Cell Neurosci 44:178–189

    Article  PubMed  CAS  Google Scholar 

  • Reyes JC, Barra J, Muchardt C, Camus A, Babinet C, Yaniv M (1998) Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha). EMBO J 17:6979–6991

    Article  PubMed  CAS  Google Scholar 

  • Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38:413–443

    Article  PubMed  CAS  Google Scholar 

  • Román-Trufero M, Méndez-Gómez HR, Pérez C, Hijikata A, Fujimura Y, Endo T, Koseki H, Vicario-Abejón C, Vidal M (2009) Maintenance of undifferentiated state and self-renewal of embryonic neural stem cells by Polycomb protein Ring1B. Stem Cells 27:1559–1570

    Article  PubMed  CAS  Google Scholar 

  • Sanuki R, Onishi A, Koike C, Muramatsu R, Watanabe S, Muranishi Y, Irie S, Uneo S, Koyasu T, Matsui R, Chérasse Y, Urade Y, Watanabe D, Kondo M, Yamashita T, Furukawa T (2011) miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat Neurosci 14:1125–1134

    Article  PubMed  CAS  Google Scholar 

  • Schade SD, Brown GB (2000) Identifying the promoter region of the human brain sodium channel subtype II gene (SCN2A). Brain Res Mol Brain Res 81:187–190

    Article  PubMed  CAS  Google Scholar 

  • Schaller KL, Caldwell JH (2000) Developmental and regional expression of sodium channel isoform NaCh6 in the rat central nervous system. J Comp Neurol 420:84–97

    Article  PubMed  CAS  Google Scholar 

  • Schaller KL, Caldwell JH (2003) Expression and distribution of voltage-gated sodium channels in the cerebellum. Cerebellum 2:2–9

    Article  PubMed  CAS  Google Scholar 

  • Schaller KL, Krzemien DM, Yarowsky PJ, Krueger BK, Caldwell JH (1995) A novel, abundant sodium channel expressed in neurons and glia. J Neurosci 15:3231–3242

    PubMed  CAS  Google Scholar 

  • Scheinman RI, Auld VJ, Goldin AL, Davidson N, Dunn RJ, Catterall WA (1989) Developmental regulation of sodium channel expression in the rat forebrain. J Biol Chem 264:10660–10666

    PubMed  CAS  Google Scholar 

  • Schmitz C, Kinge P, Hutter H (2007) Axon guidance genes identified in a large-scale RNAi screen using the RNAi-hypersensitive Caenorhabditis elegans strain nre-1(hd20) lin-15b(hd126). Proc Natl Acad Sci USA 104:834–839

    Article  PubMed  CAS  Google Scholar 

  • Schoenherr CJ, Anderson DJ (1995a) Silencing is golden: negative regulation in the control of neuronal gene transcription. Curr Opin Neurobiol 5:566–571

    Article  PubMed  CAS  Google Scholar 

  • Schoenherr CJ, Anderson DJ (1995b) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267:1360–1363

    Article  PubMed  CAS  Google Scholar 

  • Schratt G (2009) microRNAs at the synapse. Nat Rev Neurosci 10:842–849

    Article  PubMed  CAS  Google Scholar 

  • Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G (2007) Genome regulation by polycomb and trithorax proteins. Cell 128:735–745

    Article  PubMed  CAS  Google Scholar 

  • Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5:R13

    Article  PubMed  Google Scholar 

  • Seo S, Richardson GA, Kroll KL (2005) The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD. Development 132:105–115

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Nakao H, Kiyonari H, Abe T, Aizawa S (2011) MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J Neurosci 31:3407–3422

    Article  PubMed  CAS  Google Scholar 

  • Shimojo M, Paquette AJ, Anderson DJ, Hersh LB (1999) Protein kinase A regulates cholinergic gene expression in PC12 cells: REST4 silences the silencing activity of neuron-restrictive silencer factor/REST. Mol Cell Biol 19:6788–6795

    PubMed  CAS  Google Scholar 

  • Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H, Majumder S (2008) REST maintains self-renewal and pluripotency of embryonic stem cells. Nature 453:223–227

    Article  PubMed  CAS  Google Scholar 

  • Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H, Majumder S (2009) Brief communication arising. Nature 457:E7

    Article  CAS  Google Scholar 

  • Smith MD, Dawson SJ, Latchman DS (1997) The Brn-3a transcription factor induces neuronal process outgrowth and the coordinate expression of genes encoding synaptic proteins. Mol Cell Biol 17:345–354

    PubMed  CAS  Google Scholar 

  • Soldati C, Bithell A, Johnston C, Wong KY, Teng SW, Beglopoulos V, Stanton LW, Buckley NJ (2012) Repressor element 1 silencing transcription factor couples loss of pluripotency with neural induction and neural differentiation. Stem Cells 30:425-434

    Article  PubMed  Google Scholar 

  • Stanke M, Junghans D, Geissen M, Goridis C, Ernsberger U, Rohrer H (1999) The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126:4087–4094

    PubMed  CAS  Google Scholar 

  • Su X, Kameoka S, Lentz S, Majumder S (2004) Activation of REST/NRSF target genes in neural stem cells is sufficient to cause neuronal differentiation. Mol Cell Biol 24:8018–8025

    Article  PubMed  CAS  Google Scholar 

  • Südhof TC (2002) Synaptotagmins: why so many? J Biol Chem 277:7629–7632

    Article  PubMed  CAS  Google Scholar 

  • Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509–547

    Article  PubMed  CAS  Google Scholar 

  • Südhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–477

    Article  PubMed  CAS  Google Scholar 

  • Sullivan KF (1988) Structure and utilization of tubulin isotypes. Annu Rev Cell Biol 4:687–716

    Article  PubMed  CAS  Google Scholar 

  • Sun YM, Greenway DJ, Johnson R, Street M, Belyaev ND, Deuchars J, Bee T, Wilde S, Buckley NJ (2005) Distinct profiles of REST interactions with its target genes at different stages of neuronal development. Mol Biol Cell 16:5630–5638

    Article  PubMed  CAS  Google Scholar 

  • Sun YM, Cooper M, Finch S, Lin HH, Chen ZF, Williams BP, Buckley NJ (2008) Rest-mediated regulation of extracellular matrix is crucial for neural development. PLoS One 3:e3656

    Article  PubMed  CAS  Google Scholar 

  • Szaro BG, Strong MJ (2010) Post-transcriptional control of neurofilaments: new roles in development, regeneration and neurodegenerative disease. Trends Neurosci 33:27–37

    Article  PubMed  CAS  Google Scholar 

  • Tabuchi A, Yamada T, Sasagawa S, Naruse Y, Mori N, Tsuda M (2002) REST4-mediated modulation of REST/NRSF-silencing function during BDNF gene promoter activation. Biochem Biophys Res Commun 290:415–420

    Article  PubMed  CAS  Google Scholar 

  • Trimmer JS, Rhodes KJ (2004) Localization of voltage-gated ion channels in mammalian brain. Annu Rev Physiol 66:477–519

    Article  PubMed  CAS  Google Scholar 

  • Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC, Wernig M (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463:1035–1041

    Article  PubMed  CAS  Google Scholar 

  • Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin EM, Pennacchio LA (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457:854–858

    Article  PubMed  CAS  Google Scholar 

  • Visvanathan J, Lee S, Lee B, Lee JW, Lee SK (2007) The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21:744–749

    Article  PubMed  CAS  Google Scholar 

  • Watanabe Y, Kameoka S, Gopalakrishnan V, Aldape KD, Pan ZZ, Lang FF, Majumder S (2004) Conversion of myoblasts to physiologically active neuronal phenotype. Genes Dev 18:889–900

    Article  PubMed  CAS  Google Scholar 

  • Watanabe H, Mizutani T, Haraguchi T, Yamamichi N, Minoguchi S, Yamamichi-Nishina M, Mori N, Kameda T, Sugiyama T, Iba H (2006) SWI/SNF complex is essential for NRSF-mediated suppression of neuronal genes in human nonsmall cell lung carcinoma cell lines. Oncogene 25:470–479

    PubMed  CAS  Google Scholar 

  • Westbrook TF, Hu G, Ang XL, Mulligan P, Pavlova NN, Liang A, Leng Y, Maehr R, Shi Y, Harper JW, Elledge SJ (2008) SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 452:370–374

    Article  PubMed  CAS  Google Scholar 

  • Westerlund N, Zdrojewska J, Padzik A, Komulainen E, Björkblom B, Rannikko E, Tararuk T, Garcia-Frigola C, Sandholm J, Nguyen L, Kallunki T, Courtney MJ, Coffey ET (2011) Phosphorylation of SCG10/stathmin-2 determines multipolar stage exit and neuronal migration rate. Nat Neurosci 14:305–313

    Article  PubMed  CAS  Google Scholar 

  • Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, Bruijn E de, Horvitz HR, Kauppinen S, Plasterk RH (2005) MicroRNA expression in zebrafish embryonic development. Science 309:310–311

    Article  PubMed  CAS  Google Scholar 

  • Williams RR, Azuara V, Perry P, Sauer S, Dvorkina M, Jørgensen H, Roix J, McQueen P, Misteli T, Merkenschlager M, Fisher AG (2006) Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J Cell Sci 119:132–140

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Xie X (2006) Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression. Genome Biol 7:R85

    Article  PubMed  CAS  Google Scholar 

  • Wu JI, Lessard J, Olave IA, Qiu Z, Ghosh A, Graef IA, Crabtree GR (2007) Regulation of dendritic development by neuron-specific chromatin remodeling complexes. Neuron 56:94–108

    Article  PubMed  CAS  Google Scholar 

  • Wu JI, Lessard J, Crabtree GR (2009) Understanding the words of chromatin regulation. Cell 136:200–206

    Article  PubMed  CAS  Google Scholar 

  • Yamada Y, Aoki H, Kunisada T, Hara A (2010) Rest promotes the early differentiation of mouse ESCs but is not required for their maintenance. Cell Stem Cell 6:10–15

    Article  PubMed  CAS  Google Scholar 

  • Yoo AS, Crabtree GR (2009) ATP-dependent chromatin remodeling in neural development. Curr Opin Neurobiol 19:120–126

    Article  PubMed  CAS  Google Scholar 

  • Yoo AS, Staahl BT, Chen L, Crabtree GR (2009) MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460:642–646

    PubMed  CAS  Google Scholar 

  • Yoo AS, Sun AX, Li L, Shcheglovitov A, Portmann T, Li Y, Lee-Messer C, Dolmetsch RE, Tsien RW, Crabtree GR (2011) MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476:228–231

    Article  PubMed  CAS  Google Scholar 

  • Yu JY, Chung KH, Deo M, Thompson RC, Turner DL (2008) MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp Cell Res 314:2618–2633

    Article  PubMed  CAS  Google Scholar 

  • Yuva-Aydemir Y, Simkin A, Gascon E, Gao FB (2011) MicroRNA-9: functional evolution of a conserved small regulatory RNA. RNA Biol 8:557–564

    Article  PubMed  CAS  Google Scholar 

  • Zhao C, Sun G, Li S, Shi Y (2009) A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 16:365–371

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

I wish to thank Hermann Rohrer for generously providing access to laboratory space and facilities and for his critical comments on the manuscript. Andreas Schober, Sandra Partimo and Ingid Stenull provided excellent assistance in the generation of the ISH figures. Ute Tönchen-Wagner provided invaluable support. Joachim Häfele, Jurka Herrnkind, Rosa-Maria Alvarez Pérez, Ursula Halm-Leihs and the Caritas Nordend-Ost team in Frankfurt a.M., Nicole Richter and the BEK-GEK team, the Neurologische Klinik at the J.-W. Goethe-Universität in Frankfurt a.M., the Quellenhof Neurologisches Rehabilitationszentrum in Bad Wildbad, and the efforts of the City of Frankfurt a.M. to provide accessible transportation all contributed to keeping things moving.

Author information

Authors and Affiliations

  1. Max Planck Institute for Brain Research, Deutschordenstrasse 46, 60528, Frankfurt, Germany

    Uwe Ernsberger

Authors
  1. Uwe Ernsberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Uwe Ernsberger.

Additional information

Support from the Gemeinnützige Hertie-Stiftung, Frankfurt a.M., Germany, is gratefully acknowledged.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Table 1

(DOC 88 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ernsberger, U. Regulation of gene expression during early neuronal differentiation: evidence for patterns conserved across neuron populations and vertebrate classes. Cell Tissue Res 348, 1–27 (2012). https://doi.org/10.1007/s00441-012-1367-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-012-1367-y

Keywords

Search

Navigation