Transcriptome sequencing during mouse brain development identifies long non-coding RNAs functionally involved in neurogenic commitment

EMBO Journal

Volumn 32, Issue 24, 2013, Pages 3145-3160

  Aprea, Julieta ^a   Prenninger, Silvia ^a   Dori, Martina ^a   Ghosh, Tanay ^b   Monasor, Laura Sebastian ^a   Wessendorf, Elke ^a   Zocher, Sara ^a   Massalini, Simone ^a   Alexopoulou, Dimitra ^a   Lesche, Mathias ^a   Dahl, Andreas ^a   Groszer, Matthias ^b   Hiller, Michael ^c,d   Calegari, Federico ^a  

^a CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^b INSTITUT DU FER À MOULIN   (France)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^d MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

Author keywords

Cortical development; LncRNAs; Miat; Neurogenesis; Splicing

Indexed keywords

CASPASE 3; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; LONG UNTRANSLATED RNA; MICRORNA; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BRAIN DEVELOPMENT; CELL FATE; CELL POPULATION; CELL SELECTION; CELL SURVIVAL; CHROMOSOME 1; CHROMOSOME 7; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; FLUORESCENCE MICROSCOPY; GENE MAPPING; GENETIC PROCEDURES; IN SITU HYBRIDIZATION; MOUSE; MOUSE EMBRYO; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEWBORN; NONHUMAN; PLEIOTROPY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; START CODON; SYNAPTIC TRANSMISSION;

ALTERNATIVE SPLICING; ANIMALS; BRAIN; CEREBRAL CORTEX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; MICE; MICE, TRANSGENIC; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; PHENOTYPE; PROTEINS; PROTO-ONCOGENE PROTEINS; RNA, LONG NONCODING; WNT PROTEINS;

EID: 84890567188     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.245     Document Type: Article

References (74)

1. Aaker JD, Patineau AL, Yang HJ, Ewart DT, Gong W, Li T, Nakagawa Y, McLoon SC, Koyano-Nakagawa N (2009) Feedback regulation of NEUROG2 activity by MTGR1 is required for progression of neurogenesis. Mol Cell Neurosci 42: 267-277
2. Amaral PP, Clark MB, Gascoigne DK, Dinger ME, Mattick JS (2011) lncRNAdb: a reference database for long noncoding RNAs. Nucleic Acids Res 39: D146-D151
3. Aprea J, Calegari F (2012) Bioelectric state and cell cycle control of Mammalian neural stem cells. Stem Cells Int 2012: 816049
4. Arai Y, Funatsu N, Numayama-Tsuruta K, Nomura T, Nakamura S, Osumi N (2005) Role of Fabp7, a downstream gene of Pax6, in the maintenance of neuroepithelial cells during early embryonic development of the rat cortex. J Neurosci 25: 9752-9761
5. Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB (2011) Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2: 154
6. Artegiani B, Lange C, Calegari F (2012) Expansion of embryonic and adult neural stem cells by in utero electroporation or viral stereotaxic injection. J Vis Exp 68: e4093
7. Artegiani B, Lindemann D, Calegari F (2011) Overexpression of cdk4 and cyclinD1 triggers greater expansion of neural stem cells in the adult mouse brain. J Exp Med 208: 937-948
8. Attardo A, Calegari F, Haubensak W, Wilsch-Brauninger M, Huttner WB (2008) Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS One 3: e2388
9. Attardo A, Fabel K, Krebs J, Haubensak W, Huttner WB, Kempermann G (2010) Tis21 expression marks not only populations of neurogenic precursor cells but also new postmitotic neurons in adult hippocampal neurogenesis. Cereb Cortex 20: 304-314
10. Ayoub AE, Oh S, Xie Y, Leng J, Cotney J, Dominguez MH, Noonan JP, Rakic P (2011) Transcriptional programs in transient embryonic zones of the cerebral cortex defined by high-resolution mRNA sequencing. Proc Natl Acad Sci USA 108: 14950-14955
11. Barry G, Briggs JA, Vanichkina DP, Poth EM, Beveridge NJ, Ratnu VS, Nayler SP, Nones K, Hu J, Bredy TW, Nakagawa S, Rigo F, Taft RJ, Cairns MJ, Blackshaw S, Wolvetang EJ, Mattick JS (2013) The long non-coding RNA Gomafu is acutely regulated in response to neuronal activation and involved in schizophreniaassociated alternative splicing. Mol Psychiatry (advance online publication 30 April 2013; doi:10.1038/mp.2013.45)
12. Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, Hirrlinger J, Haslinger A, Lie DC, Beckers J, Yoder B, Irmler M, Götz M (2010) In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7: 744-758
13. Berghoff EG, Clark MF, Chen S, Cajigas I, Leib DE, Kohtz JD (2013) Evf2 (Dlx6as) lncRNA regulates ultraconserved enhancer methylation and the differential transcriptional control of adjacent genes. Development 140: 4407-4416
14. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J (2006) The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev 20: 3475-3486
15. Blackshaw S, Harpavat S, Trimarchi J, Cai L, Huang H, Kuo WP, Weber G, Lee K, Fraioli RE, Cho SH, Yung R, Asch E, Ohno-Machado L, Wong WH, Cepko CL (2004) Genomic analysis of mouse retinal development. PLoS Biol 2: E247
16. Calegari F, Haubensak W, Haffner C, Huttner WB (2005) Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 25: 6533-6538
17. Camps J, Nguyen QT, Padilla-Nash HM, Knutsen T, McNeil NE, Wangsa D, Hummon AB, Grade M, Ried T, Difilippantonio MJ (2009) Integrative genomics reveals mechanisms of copy number alterations responsible for transcriptional deregulation in colorectal cancer. Genes, Chromosomes Cancer 48: 1002-1017
18. Cappello S, Attardo A, Wu X, Iwasato T, Itohara S, Wilsch-Brauninger M, Eilken HM, Rieger MA, Schroeder TT, Huttner WB, Brakebusch C, Götz M (2006) The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 9: 1099-1107
19. Cappello S, Gray MJ, Badouel C, Lange S, Einsiedler M, Srour M, Chitayat D, Hamdan FF, Jenkins ZA, Morgan T, Preitner N, Uster T, Thomas J, Shannon P, Morrison V, Di Donato N, Van Maldergem L, Neuhann T, Newbury-Ecob R, Swinkells M et al (2013) Mutations in genes encoding the cadherin receptor-ligand pair DCHS1 and FAT4 disrupt cerebral cortical development. Nat Genet 45: 1300-1308
20. Chen LL, Carmichael GG (2010) Decoding the function of nuclear long non-coding RNAs. Curr Opin Cell Biol 22: 357-364
21. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M et al (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22: 1775-1789
22. Diekmann H, Stuermer CA (2009) Zebrafish neurolin-a and -b, orthologs of ALCAM, are involved in retinal ganglion cell differentiation and retinal axon pathfinding. J Comp Neurol 513: 38-50
23. Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, Rozado D, Magen A, Canidio E, Pagani M, Peluso I, Lin-Marq N, Koch M, Bilio M, Cantiello I, Verde R, De Masi C, Bianchi SA, Cicchini J, Perroud E, Mehmeti S et al (2011) A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol 9: e1000582
24. Engelen E, Akinci U, Bryne JC, Hou J, Gontan C, Moen M, Szumska D, Kockx C, van Ijcken W, Dekkers DH, Demmers J, Rijkers EJ, Bhattacharya S, Philipsen S, Pevny LH, Grosveld FG, Rottier RJ, Lenhard B, Poot RA (2011) Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat Genet 43: 607-611
25. Faux C, Rakic S, Andrews W, Yanagawa Y, Obata K, Parnavelas JG (2010) Differential gene expression in migrating cortical interneurons during mouse forebrain development. J Comp Neurol 518: 1232-1248
26. Fietz SA, Lachmann R, Brandl H, Kircher M, Samusik N, Schroder R, Lakshmanaperumal N, Henry I, Vogt J, Riehn A, Distler W, Nitsch R, Enard W, Paabo S, Huttner WB (2012) Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor selfrenewal. Proc Natl Acad Sci USA 109: 11836-11841
27. Geschwind DH, Konopka G (2009) Neuroscience in the era of functional genomics and systems biology. Nature 461: 908-915
28. Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6: 777-788
29. Guillemot F (2007) Cell fate specification in the mammalian telencephalon. Prog Neurobiol 83: 37-52
30. 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
31. Hartl D, Irmler M, Romer I, Mader MT, Mao L, Zabel C, de Angelis MH, Beckers J, Klose J (2008) Transcriptome and proteome analysis of early embryonic mouse brain development. Proteomics 8: 1257-1265
32. Haubensak W, Attardo A, Denk W, Huttner WB (2004) Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101: 3196-3201
33. Hevner RF, Hodge RD, Daza RA, Englund C (2006) Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res 55: 223-233
34. Hirabayashi Y, Gotoh Y (2010) Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 11: 377-388
35. Hu XL, Wang Y, Shen Q (2012) Epigenetic control on cell fate choice in neural stem cells. Protein Cell 3: 278-290
36. Iacopetti P, Michelini M, Stuckmann I, Oback B, Aaku-Saraste E, Huttner WB (1999) Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc Natl Acad Sci USA 96: 4639-4644
37. Ip JY, Nakagawa S (2011) Long non-coding RNAs in nuclear bodies. Dev Growth Differ 54: 44-54
38. Ishikawa T, Gotoh N, Murayama C, Abe T, Iwashita M, Matsuzaki F, Suzuki T, Yamamoto T (2011) IgSF molecule MDGA1 is involved in radial migration and positioning of a subset of cortical upper-layer neurons. Dev Dyn 240: 96-107
39. Jabaudon D, Shnider SJ, Tischfield DJ, Galazo MJ, Macklis JD (2012) RORbeta induces barrel-like neuronal clusters in the developing neocortex. Cereb Cortex 22: 996-1006
40. Jepsen K, Solum D, Zhou T, McEvilly RJ, Kim HJ, Glass CK, Hermanson O, Rosenfeld MG (2007) SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron. Nature 450: 415-419
41. Kawaguchi A, Ikawa T, Kasukawa T, Ueda HR, Kurimoto K, Saitou M, Matsuzaki F (2008) Single-cell gene profiling defines differential progenitor subclasses in mammalian neurogenesis. Development 135: 3113-3124
42. Kwon GS, Hadjantonakis AK (2007) Eomes::GFP-a tool for live imaging cells of the trophoblast, primitive streak, and telencephalon in the mouse embryo. Genesis 45: 208-217
43. Lamprianou S, Chatzopoulou E, Thomas JL, Bouyain S, Harroch S (2011) A complex between contactin-1 and the protein tyrosine phosphatase PTPRZ controls the development of oligodendrocyte precursor cells. Proc Natl Acad Sci USA 108: 17498-17503
44. Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5: 320-331
45. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR et al (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176
46. Lim IK (2006) TIS21 (/BTG2/PC3) as a link between ageing and cancer: cell cycle regulator and endogenous cell death molecule. J Cancer Res Clin Oncol 132: 417-426
47. Ling KH, Hewitt CA, Beissbarth T, Hyde L, Banerjee K, Cheah PS, Cannon PZ, Hahn CN, Thomas PQ, Smyth GK, Tan SS, Thomas T, Scott HS (2009) Molecular networks involved in mouse cerebral corticogenesis and spatio-temporal regulation of Sox4 and Sox11 novel antisense transcripts revealed by transcriptome profiling. Genome Biol 10: R104
48. Lv J, Liu H, Huang Z, Su J, He H, Xiu Y, Zhang Y, Wu Q (2013) Long non-coding RNA identification over mouse brain development by integrative modeling of chromatin and genomic features. Nucleic Acids Res (advance online publication 13 September 2013; doi:10.1093/nar/gkt818)
49. Martin PM, Carnaud M, Garcia del Cano G, Irondelle M, Irinopoulou T, Girault JA, Dargent B, Goutebroze L (2008) Schwannomin-interacting protein-1 isoform IQCJ-SCHIP-1 is a late component of nodes of Ranvier and axon initial segments. J Neurosci 28: 6111-6117
50. Matsuki T, Hori G, Furuichi T (2005) Gene expression profiling during the embryonic development of mouse brain using an oligonucleotide-based microarray system. Brain Res Mol Brain Res 136: 231-254
51. Meissner A (2010) Epigenetic modifications in pluripotent and differentiated cells. Nat Biotechnol 28: 1079-1088
52. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10: 155-159
53. Metzker ML (2010) Sequencing technologies - the next generation. Nat Rev Genet 11: 31-46
54. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, BrockmanW, Kim TK, Koche RP, LeeW, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C et al (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560
55. Nagano T, Fraser P (2011) No-nonsense functions for long noncoding RNAs. Cell 145: 178-181
56. Ng SY, Bogu GK, Soh BS, Stanton LW (2013) The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. Mol Cell 51: 349-359
57. Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, Yamanaka I, Kiyosawa H, Yagi K, Tomaru Y, Hasegawa Y, Nogami A, Schonbach C, Gojobori T, Baldarelli R, Hill DP et al (2002) Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420: 563-573
58. Onoguchi M, Hirabayashi Y, Koseki H, Gotoh Y (2012) A noncoding RNA regulates the neurogenin1 gene locus during mouse neocortical development. Proc Natl Acad Sci USA 109: 16939-16944
59. Pauli A, Rinn JL, Schier AF (2011) Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12: 136-149
60. 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
61. Pinto L, Mader MT, Irmler M, Gentilini M, Santoni F, Drechsel D, Blum R, Stahl R, Bulfone A, Malatesta P, Beckers J, Götz M (2008) Prospective isolation of functionally distinct radial glial subtypes-lineage and transcriptome analysis. Mol Cell Neurosci 38: 15-42
62. Ramos AD, Diaz A, Nellore A, Delgado RN, Park KY, Gonzales- Roybal G, Oldham MC, Song JS, Lim DA (2013) Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 12: 616-628
63. Rapicavoli NA, Poth EM, Blackshaw S (2010) The long noncoding RNA RNCR2 directs mouse retinal cell specification. BMC Dev Biol 10: 49
64. Saburi S, Hester I, Goodrich L, McNeill H (2012) Functional interactions between Fat family cadherins in tissue morphogenesis and planar polarity. Development 139: 1806-1820
65. Sakurai T (2012) The role of NrCAM in neural development and disorders-beyond a simple glue in the brain. Mol Cell Neurosci 49: 351-363
66. Salomoni P, Calegari F (2010) Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 5: 332-342
67. Sheik Mohamed J, Gaughwin PM, Lim B, Robson P, Lipovich L (2010) Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 16: 324-337
68. Sone M, Hayashi T, Tarui H, Agata K, Takeichi M, Nakagawa S (2007) The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J Cell Sci 120: 2498-2506
69. Tarazona S, Garcia-Alcalde F, Dopazo J, Ferrer A, Conesa A (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21: 2213-2223
70. Terra R, Luo H, Qiao X, Wu J (2008) Tissue-specific expression of B-cell translocation gene 2 (BTG2) and its function in T-cell immune responses in a transgenic mouse model. Int Immunol 20: 317-326
71. Tirone F (2001) The gene PC3(TIS21/BTG2), prototype member of the PC3/BTG/TOB family: regulator in control of cell growth, differentiation, and DNA repair? J Cell Physiol 187: 155-165
72. Uhde CW, Vives J, Jaeger I, Li M (2010) Rmst is a novel marker for the mouse ventral mesencephalic floor plate and the anterior dorsal midline cells. PLoS One 5: e8641
73. Yao MJ, Chen G, Zhao PP, Lu MH, Jian J, Liu MF, Yuan XB (2012) Transcriptome analysis of microRNAs in developing cerebral cortex of rat. BMC Genomics 13: 232
74. Yu J, Carroll TJ, Rajagopal J, Kobayashi A, Ren Q, McMahon AP (2009) A Wnt7b-dependent pathway regulates the orientation of epithelial cell division and establishes the cortico-medullary axis of the mammalian kidney. Development 136: 161-171