期刊论文详细信息
BMC Genomics
Ontogeny of small RNA in the regulation of mammalian brain development
Murray J Cairns1  Darryl W Eyles2  Frederick R Walker3  Elizabeth A Mason4  Adam P Carroll3  Belinda J Goldie1  Sharon L Hollins3 
[1] Schizophrenia Research Institute, Sydney, NSW, Australia;Queensland Centre for Mental Health Research, Wacol, Qld 4076, Australia;Centre for Translational Neuroscience and Mental Health, Hunter Medical Research Institute, Newcastle, NSW 2305, Australia;Queensland Brain Institute, University of Queensland, Brisbane, Qld 4072, Australia
关键词: Neurogenesis;    mRNA;    MicroRNA;    Interactions;    Cortex;   
Others  :  1140655
DOI  :  10.1186/1471-2164-15-777
 received in 2014-07-30, accepted in 2014-09-04,  发布年份 2014
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【 摘 要 】

Background

MicroRNAs (miRNAs) play a pivotal role in coordinating messenger RNA (mRNA) transcription and stability in almost all known biological processes, including the development of the central nervous system. Despite our broad understanding of their involvement, we still have a very sparse understanding of specifically how miRNA contribute to the strict regional and temporal regulation of brain development. Accordingly, in the current study we have examined the contribution of miRNA in the developing rat telencephalon and mesencephalon from just after neural tube closure till birth using a genome-wide microarray strategy.

Results

We identified temporally distinct expression patterns in both the telencephalon and mesencephalon for both miRNAs and their target genes. We demonstrate direct miRNA targeting of several genes involved with the migration, differentiation and maturation of neurons.

Conclusions

Our findings suggest that miRNA have significant implications for the development of neural structure and support important mechanisms that if disrupted, may contribute to or drive neurodevelopmental disorders.

【 授权许可】

   
2014 Hollins et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Eagleson KL, Lillien L, Chan AV, Levitt P: Mechanisms specifying area fate in cortex include cell-cycle-dependent decisions and the capacity of progenitors to express phenotype memory. Development 1997, 124:1623-1630.
  • [2]Florio M, Leto K, Muzio L, Tinterri A, Badaloni A, Croci L, Zordan P, Barili V, Albieri I, Guillemot F, Rossi F, Consalez GG: Neurogenin 2 regulates progenitor cell-cycle progression and Purkinje cell dendritogenesis in cerebellar development. Development 2012, 139:2308-2320.
  • [3]Stead JDH, Neal C, Meng F, Wang Y, Evans S, Vazquez DM, Watson SJ, Akil H: Transcriptional profiling of the developing rat brain reveals that the most dramatic regional differentiation in gene expression occurs postpartum. J Neurosci 2006, 26:345-353.
  • [4]Cai Y, Yu X, Hu S, Yu J: A brief review on the mechanisms of miRNA regulation. Genomics Proteomics Bioinformatics 2009, 7:147-154.
  • [5]Fabian MR, Sonenberg N, Filipowicz W: Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010, 79:351-379.
  • [6]Goldie BJ, Cairns MJ: Post-transcriptional trafficking and regulation of neuronal gene expression. Mol Neurobiol 2012, 45:99-108.
  • [7]Carroll AP, Tooney PA, Cairns MJ: Context-specific microRNA function in developmental complexity. J Mol Cell Biol 2013, 5:73-84.
  • [8]Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, Rakic P, Constantine-Paton M, Horvitz HR: Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 2004, 5:R68. BioMed Central Full Text
  • [9]Smirnova L, Gräfe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG: Regulation of miRNA expression during neural cell specification. Eur J Neurosci 2005, 21:1469-1477.
  • [10]Smith B, Treadwell J, Zhang D, Ly D, McKinnell I, Walker PR, Sikorska M: Large-scale expression analysis reveals distinct microRNA profiles at different stages of human neurodevelopment. PLoS One 2010, 5:e11109.
  • [11]Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS: A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 2003, 9:1274-1281.
  • [12]Kapsimali M, Kloosterman WP, de Bruijn E, Rosa F, Plasterk RHA, Wilson SW: MicroRNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol 2007, 8:R173. BioMed Central Full Text
  • [13]Mukhopadhyay P, Brock G, Appana S, Webb C, Greene RM, Pisano MM: MicroRNA gene expression signatures in the developing neural tube. Birth Defects Res (Part A) Clin Mol Teratol 2011, 91:744-762.
  • [14]Coolen M, Thieffry D, Drivenes Ø, Becker TS, Bally-Cuif L: miR-9 controls the timing of neurogenesis through the direct inhibition of antagonistic factors. Dev Cell 2012, 22:1052-1064.
  • [15]Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V: Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 2004, 5:R13. BioMed Central Full Text
  • [16]Beveridge NJ, Tooney PA, Carroll AP, Tran N, Cairns MJ: Down-regulation of miR-17 family expression in response to retinoic acid induced neuronal differentiation. Cell Signal 2009, 21:1837-1845.
  • [17]Manakov SA, Grant SGN, Enright AJ: Reciprocal regulation of microRNA and mRNA profiles in neuronal development and synapse formation. BMC Genomics 2009, 10:419. BioMed Central Full Text
  • [18]Nielsen JA, Lau P, Maric D, Barker JL, Hudson LD: Integrating microRNA and mRNA expression profiles of neuronal progenitors to identify regulatory networks underlying the onset of cortical neurogenesis. BMC Neurosci 2009, 10:98. BioMed Central Full Text
  • [19]Hua Y-J, Tang Z-Y, Tu K, Zhu L, Li Y-X, Xie L, Xiao H-S: Identification and target prediction of miRNAs specifically expressed in rat neural tissue. BMC Genomics 2009, 10:214. BioMed Central Full Text
  • [20]Olde Loohuis NFM, Kos A, Martens GJM, Van Bokhoven H, Nadif Kasri N, Aschrafi A: MicroRNA networks direct neuronal development and plasticity. Cell Mol Life Sci 2011, 69:89-102.
  • [21]Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME: A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
  • [22]Smrt RD, Szulwach KE, Pfeiffer RL, Li X, Guo W, Pathania M, Teng Z-Q, Luo Y, Peng J, Bordey A, Jin P, Zhao X: MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 2010, 28:1060-1070.
  • [23]Maiorano NA, Mallamaci A: Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev 2009, 4:1-16. BioMed Central Full Text
  • [24]Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, Hammond SM, Bartel DP, Schier AF: MicroRNAs regulate brain morphogenesis in zebrafish. Science (80-) 2005, 308:833-838.
  • [25]Conaco C, Otto S, Han J-J, Mandel G: Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci U S A 2006, 103:2422-2427.
  • [26]Dugas JC, Cuellar TL, Scholze A, Ason B, Ibrahim A, Emery B, Zamanian JL, Foo LC, McManus MT, Barres BA: Dicer1 and miR-219 Are required for normal oligodendrocyte differentiation and myelination. Neuron 2010, 65:597-611.
  • [27]Rice D, Barone S Jr: Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 2000, 108(Suppl):511-533.
  • [28]Clancy B, Finlay BL, Darlington RB, Anand KJS: Extrapolating brain development from experimental species to humans. Neurotoxicology 2007, 28:931-937.
  • [29]Paul A, Cai Y, Atwal GS, Huang ZJ: Developmental coordination of gene expression between synaptic partners during GABAergic circuit assembly in cerebellar cortex. Front Neural Circuits 2012, 6(June):37.
  • [30]Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I, Yee BK, Feldon J: The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci 2006, 26:4752-4762.
  • [31]Eyles D, Feldon J, Meyer U: Schizophrenia: do all roads lead to dopamine or is this where they start? Evidence from two epidemiologically informed developmental rodent models. Transl Psychiatry 2012, 2:e81.
  • [32]Farh KK-H, Grimson A, Jan C, Lewis BP, Johnston WK, Lim LP, Burge CB, Bartel DP: The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science (80-) 2005, 310:1817-1821.
  • [33]Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM: Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3’UTR evolution. Cell 2005, 123:1133-1146.
  • [34]Guo H, Ingolia NT, Weissman JS, Bartel DP: Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
  • [35]Ciani L, Boyle KA, Dickins E, Sahores M, Anane D, Lopes DM: Wnt7a signaling promotes dendritic spine growth and synaptic strength through Ca2+/Calmodulin-dependent protein kinase II. Proc Natl Acad Sci U S A 2011, 108:10732-10737.
  • [36]Nishimura N, Van Huyen Pham T, Hartomo TB, Lee MJ, Hasegawa D, Takeda H, Kawasaki K, Kosaka Y, Yamamoto T, Morikawa S, Yamamoto N, Kubokawa I, Mori T, Yanai T, Hayakawa A, Takeshima Y, Nishio H, Matsuo M: Rab15 expression correlates with retinoic acid-induced differentiation of neuroblastoma cells. Oncol Rep 2011, 26:145-151.
  • [37]Beffert U, Dillon GM, Sullivan JM, Stuart CE, Gilbert JP, Kambouris JA, Ho A: Microtubule plus-end tracking protein CLASP2 regulates neuronal polarity and synaptic function. J Neurosci 2012, 32:13906-13916.
  • [38]Quintana A, Sanz E, Wang W, Storey GP, Güler AD, Wanat MJ, Roller BA, La Torre A, Amieux PS, McKnight GS, Bamford NS, Palmiter RD: Lack of GPR88 enhances medium spiny neuron activity and alters motor- and cue-dependent behaviors. Nat Neurosci 2012, 15:1547-1555.
  • [39]Thomson JM, Newman M, Parker JS, Morin-kensicki EM, Wright T, Hammond SM: Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev 2006, 20:2202-2207.
  • [40]Roush S, Slack FJ: The let-7 family of microRNAs. Trends Cell Biol 2008, 18:505-516.
  • [41]Logarinho E, Maffini S, Barisic M, Marques A, Toso A, Meraldi P, Maiato H: CLASPs prevent irreversible multipolarity by ensuring spindle-pole resistance to traction forces during chromosome alignment. Nat Cell Biol 2012, 14:295-303.
  • [42]Tognini P, Pizzorusso T: MicroRNA212/132 family: molecular transducer of neuronal function and plasticity. Int J Biochem Cell Biol 2012, 44:6-10.
  • [43]Wanet A, Tacheny A, Arnould T, Renard P: miR-212/132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Res 2012, 40:4742-4753.
  • [44]Hollander JA, Im H, Amelio AL, Kocerha J, Bali P, Lu Q, Willoughby D, Wahlestedt C, Conkright MD, Paul J: Striatal microRNA controls cocaine intake through CREB signaling. Nature 2010, 466:197-202.
  • [45]Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K, Newman MA, Parker JS, Jin J, Hammond SM: microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 2007, 8:R27. BioMed Central Full Text
  • [46]Takai Y, Sasaki T, Matozaki T: Small GTP-binding proteins. Physiol Rev 2001, 81:153-208.
  • [47]Elferink LA, Anzai K, Scheller RH: rab15, a novel low molecular weight GTP-binding protein specifically expressed in rat brain. J Biol Chem 1992, 267:22693.
  • [48]Figueroa A, Kotani H, Toda Y, Mazan-mamczarz K, Mueller E, Otto A, Disch L, Norman M, Ramdasi RM, Keshtgar M, Gorospe M, Fujita Y: Novel roles of hakai in cell proliferation and oncogenesis. Mol Biol Cell 2009, 20:3533-3542.
  • [49]Kaido M, Wada H, Shindo M, Hayashi S: Essential requirement for RING finger E3 ubiquitin ligase Hakai in early embryonic development of Drosophila. Genes Cells 2009, 14:1067-1077.
  • [50]Sun G, Ye P, Murai K, Lang M-F, Li S, Zhang H, Li W, Fu C, Yin J, Wang A, Ma X, Shi Y: miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat Commun 2011, 2:529.
  • [51]Geekiyanage H, Chan C: MicroRNA-137/181c regulates serine palmitoyltransferase and in turn amyloid β, novel targets in sporadic alzheimer’s disease. J Neurosci 2011, 31:14820-14830.
  • [52]Willemsen MH, Vallès A, Kirkels LAMH, Mastebroek M, Olde Loohuis N, Kos A, Wissink-Lindhout WM, de Brouwer APM, Nillesen WM, Pfundt R, Holder-Espinasse M, Vallée L, Andrieux J, Coppens-Hofman MC, Rensen H, Hamel BCJ, van Bokhoven H, Aschrafi A, Kleefstra T: Chromosome 1p21.3 microdeletions comprising DPYD and MIR137 are associated with intellectual disability. J Med Genet 2011, 48:810-819.
  • [53]Ripke S, Sanders AR, Kendler KS, Levinson DF, Sklar P, Holmans PA, Lin D-Y, Duan J, Ophoff RA, Andreassen OA, Scolnick E, Cichon S, St Clair D, Corvin A, Gurling H, Werge T, Rujescu D, Blackwood DHR, Pato CN, Malhotra AK, Purcell S, Dudbridge F, Neale BM, Rossin L, Visscher PM, Posthuma D, Ruderfer DM, Fanous A, Stefansson H, Steinberg S, et al.: Genome-wide association study identifies five new schizophrenia loci. Nat Genet 2011, 43:969-976.
  • [54]Green MJ, Cairns MJ, Wu J, Dragovic M, Jablensky A, Tooney PA, Scott RJ, Carr VJ: Genome-wide supported variant MIR137 and severe negative symptoms predict membership of an impaired cognitive subtype of schizophrenia. Mol Psychiatry 2012, 2013:774-780.
  • [55]Logue SF, Grauer SM, Paulsen J, Graf R, Taylor N, Sung MA, Zhang L, Hughes Z, Pulito VL, Liu F, Rosenzweig-Lipson S, Brandon NJ, Marquis KL, Bates B, Pausch M: The orphan GPCR, GPR88, modulates function of the striatal dopamine system: a possible therapeutic target for psychiatric disorders? Mol Cell Neurosci 2009, 42:438-447.
  • [56]Gogolla N, Galimberti I, Deguchi Y, Caroni P: Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 2009, 62:510-525.
  • [57]Gaughwin PM, Ciesla M, Lahiri N, Tabrizi SJ, Brundin P, Björkqvist M: Hsa-miR-34b is a plasma-stable microRNA that is elevated in pre-manifest Huntington’s disease. Hum Mol Genet 2011, 20:2225-2237.
  • [58]Lee S-T, Chu K, Im W-S, Yoon H-J, Im J-Y, Park J-E, Park K-H, Jung K-H, Lee SK, Kim M, Roh J-K: Altered microRNA regulation in Huntington’s disease models. Exp Neurol 2011, 227:172-179.
  • [59]Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, Hannon G, Abeliovich A: A microRNA feedback circuit in midbrain dopamine neurons. Science (80-) 2007, 317:1220-1224.
  • [60]Margis R, Margis R, Rieder CRM: Identification of blood microRNAs associated to Parkinsonĭs disease. J Biotechnol 2011, 152:96-101.
  • [61]Miñones-Moyano E, Porta S, Escaramís G, Rabionet R, Iraola S, Kagerbauer B, Espinosa-Parrilla Y, Ferrer I, Estivill X, Martí E: MicroRNA profiling of Parkinson’s disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum Mol Genet 2011, 20:3067-3078.
  • [62]Beveridge NJ, Gardiner E, Carroll AP, Tooney PA, Cairns MJ: Schizophrenia is associated with an increase in cortical microRNA biogenesis. Mol Psychiatry 2010, 15:1176-1189.
  • [63]Santarelli DM, Beveridge NJ, Tooney PA, Cairns MJ: Upregulation of dicer and microRNA expression in the dorsolateral prefrontal cortex Brodmann area 46 in schizophrenia. Biol Psychiatry 2011, 69:180-187.
  • [64]Wu JQ, Wang X, Beveridge NJ, Tooney PA, Scott RJ, Carr VJ, Cairns MJ: Transcriptome sequencing revealed significant alteration of cortical promoter usage and splicing in schizophrenia. PLoS One 2012, 7:e36351.
  • [65]Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T: The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 2006, 7:3. BioMed Central Full Text
  • [66]Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
  • [67]Huang DW, Sherman BT, Lempicki RA: Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13.
  • [68]Chang JT, Nevins JR: GATHER: a systems approach to interpreting genomic signatures. Bioinformatics 2006, 22:2926-2933.
  • [69]Carroll AP, Tooney PA, Cairns MJ: Design and interpretation of microRNA-reporter gene activity. Anal Biochem 2013, 437:164-171.
  • [70]Carroll AP, Tran N, Tooney PA, Cairns MJ: Alternative mRNA fates identified in microRNA-associated transcriptome analysis. BMC Genomics 2012, 13:561. BioMed Central Full Text
  • [71]John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS: Human MicroRNA targets. PLoS Biol 2004, 2:e363.
  • [72]Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998, 95:14863-14868.
  • [73]Saldanha AJ: Java Treeview-extensible visualization of microarray data. Bioinformatics 2004, 20:3246-3248.
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