Reciprocal regulation of microRNA and mRNA profiles in neuronal development and synapse formation

BMC Genomics

Volumn 10, Issue , 2009, Pages 419-

  Manakov, Sergei A ^a,b   Grant, Seth G N ^a   Enright, Anton J ^b  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; MICRORNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCATION; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NONHUMAN; RNA STABILITY; RNA SYNTHESIS; RNA TRANSLATION; STEADY STATE; SYNAPSE; SYNAPTOGENESIS; UPREGULATION; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; GENOME; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PRENATAL DEVELOPMENT; SEQUENCE ANALYSIS;

ANIMALS; CLUSTER ANALYSIS; EMBRYO, MAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; MICE; MICE, INBRED C57BL; MICRORNAS; NEUROGENESIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA;

EID: 70350445696     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-419     Document Type: Article

References (70)

1. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, John-son JM. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773. 10.1038/nature03315, 15685193.
2. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008, 455:64-71. 2745094, 18668037, 10.1038/nature07242.
3. Giraldez AJ. MicroRNAs Regulate Brain Morphogenesis in Zebrafish. Science 2005, 308:833-838. 10.1126/science.1109020, 15774722.
4. Valor LM, Charlesworth P, Humphreys L, An-derson CNG, Grant SGN. Network activity-independent coordinated gene expression program for synapse assembly. Proceedings of the National Academy of Sciences 2007, 104:4658-4663.
5. Mody M, Cao Y, Cui Z, Tay KY, Shyong A, Shimizu E, Pham K, Schultz P, Welsh D, Tsien JZ. Genome-wide gene expression profiles of the developing mouse hippocampus. Proc Natl Acad Sci USA 2001, 98:8862-8867. 37526, 11438693, 10.1073/pnas.141244998.
6. 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. 395763, 15003116, 10.1186/gb-2004-5-3-r13.
7. 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. 522875, 15345052, 10.1186/gb-2004-5-9-r68.
8. Krichevsky AM, 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. 1370491, 13130141, 10.1261/rna.5980303.
9. Dogini DB, Ribeiro PAO, Rocha C, Pereira TC, Lopes-Cendes I. MicroRNA expression profile in murine central nervous system development. J Mol Neurosci 2008, 35:331-337. 10.1007/s12031-008-9068-4, 18452032.
10. Bayer SA, Altman J. Neocortical development 1991, New York: Raven Press.
11. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63. 10.1038/nature07228, 18668040.
12. Huang J, Babak T, Corson T, Chua G, Khan S. Using expression profiling data to identify human microRNA targets. Nat Meth 2007, 4:1045-1050.
13. Parkinson H, Kapushesky M, Kolesnikov N, Rustici G, Shojatalab M, Abeygunawardena N, Berube H, Dylag M, Emam I, Farne A, Holloway E, Lukk M, Malone J, Mani R, Pilicheva E, Rayner TF, Rezwan F, Sharma A, Williams E, Bradley XZ, Adamusiak T, Brandizi M, Burdett T, Coulson R, Krestyani-nova M, Kurnosov P, Maguire E, Neogi SG, Rocca-Serra P, Sansone SA, Sklyar N, Zhao M, Sarkans U, Brazma A. ArrayExpress update-from an archive of functional genomics experiments to the atlas of gene expression. Nucleic Acids Res 2009, 37:D868-872. 2686529, 19015125, 10.1093/nar/gkn889.
14. van Dongen S. Graph Clustering by Flow Simulation. PhD thesis 2000, University of Utrecht.
15. Freeman TC, Goldovsky L, Brosch M, van Don-gen S, Mazière P, Grocock RJ, Freilich S, Thorn-ton J, Enright AJ. Construction, visualisation, and clustering of transcription networks from microarray expression data. PLoS Comput Biol 2007, 3:2032-2042. 2041979, 17967053, 10.1371/journal.pcbi.0030206.
16. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Ep-pig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29. 10.1038/75556, 10802651.
17. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG. Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 2000, 3:661-669. 10.1038/76615, 10862698.
18. Collins MO, Husi H, Yu L, Brandon JM, Anderson CNG, Blackstock WP, Choudhary JS, Grant SGN. Molecular characterization and comparison of the components and multiprotein complexes in the postsynaptic proteome. Journal of Neurochemistry 2006, 97(Suppl 1):16-23. 10.1111/j.1471-4159.2005.03507.x, 16635246.
19. Genes to Cognition (G2C). , http://www.genes2cognition.org/
20. Siebler M, Koller H, Stichel C, Moller H. Spontaneous Activity and Recurrent Inhibition in Cultured Hippocampal Networks. Synapse 1993, 14:206-213. 10.1002/syn.890140304, 8211707.
21. Lewis B, Burge C, Bartel D. Conserved Seed Pairing, Often Flanked by Adenosines, Indicates that Thousands of Human Genes are MicroRNA Targets. Cell 2005, 120:15-20. 10.1016/j.cell.2004.12.035, 15652477.
22. van Dongen S, Abreu-Goodger C, Enright A. Detecting microRNA binding and siRNA off-target effects from expression data. Nat Meth 2008, 5:1023-1025.
23. Arora A, Simpson DA. Individual mRNA expression profiles reveal the effects of specific microRNAs. Genome Biol 2008, 9:R82. 2441468, 18485210, 10.1186/gb-2008-9-5-r82.
24. Gennarino V, Sardiello M, Avellino R, Meola N, Maselli V, Anand S, Cutillo L, Ballabio A, Banfi S. MicroRNA target prediction by expression analysis of host genes. Genome Res 2009, 19:481-490. 2661810, 19088304, 10.1101/gr.084129.108.
25. Cao X, Pfaff SL, Gage FH. A functional study of miR-124 in the developing neural tube. Genes & Development 2007, 21:531-536. 1820895, 17344415, 10.1101/gad.1519207.
26. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes & Development 2007, 21:744-749. 1838526, 17403776, 10.1101/gad.1519107.
27. Makeyev EV, Zhang J, Carrasco MA, Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell 2007, 27:435-448. 10.1016/j.molcel.2007.07.015, 17679093.
28. Yu JY, Chung KH, Deo M, Thompson RC, Turner DL. MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp Cell Res 2008, 314:2618-2633. 2702206, 18619591, 10.1016/j.yexcr.2008.06.002.
29. Silber J, Lim DA, Petritsch C, Persson AI, Mau-nakea AK, Yu M, Vandenberg SR, Ginzinger DG, James CD, Costello JF, Bergers G, Weiss WA, Alvarez-Buylla A, Hodgson JG. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC medicine 2008, 6:14. 2443372, 18577219, 10.1186/1741-7015-6-14.
30. Zhang Y, Chao T, Li R, Liu W, Chen Y, Yan X, Gong Y, Yin B, Qiang B, Zhao J, Yuan J, Peng X. MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J Mol Med 2008, 87:43-51. 10.1007/s00109-008-0403-6, 18810376.
31. Ferretti E, Smaele ED, Miele E, Laneve P, Po A, Pelloni M, Paganelli A, Marcotullio LD, Caffarelli E, Screpanti I, Bozzoni I, Gulino A. Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J 2008, 27:2616-2627. 10.1038/emboj.2008.172, 18756266.
32. Laneve P, Marcotullio LD, Gioia U, Fiori ME, Fer-retti E, Gulino A, Bozzoni I, Caffarelli E. The interplay between microRNAs and the neu-rotrophin receptor tropomyosin-related kinase C controls proliferation of human neu-roblastoma cells. Proc Natl Acad Sci USA 2007, 104:7957-7962. 1876554, 17483472, 10.1073/pnas.0700071104.
33. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG. Regulation of miRNA expression during neural cell specification. Eur J Neurosci 2005, 21:1469-1477. 10.1111/j.1460-9568.2005.03978.x, 15845075.
34. Mizutani K, Saito T. Progenitors resume generating neurons after temporary inhibition of neurogenesis by Notch activation in the mammalian cerebral cortex. Development 2005, 132:1295-1304. 10.1242/dev.01693, 15750183.
35. Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM. Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci 2000, 20:5012-5023.
36. Qiu R, Wang X, Davy A, Wu C, Murai K, Zhang H, Flanagan JG, Soriano P, Lu Q. Regulation of neural progenitor cell state by ephrin-B. J Cell Biol 2008, 181:973-983. 2426945, 18541704, 10.1083/jcb.200708091.
37. Guillemot F. Cell fate specification in the mammalian telencephalon. Prog Neurobiol 2007, 83:37-52. 10.1016/j.pneurobio.2007.02.009, 17517461.
38. Stuckmann I, Weigmann A, Shevchenko A, Mann M, Huttner WB. Ephrin B1 is expressed on neu-roepithelial cells in correlation with neocorti-cal neurogenesis. J Neurosci 2001, 21:2726-2737.
39. Baskerville S, Bartel DP. Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 2005, 11:241-247. 1370713, 15701730, 10.1261/rna.7240905.
40. Xu J, Wong C. A computational screen for mouse signaling pathways targeted by mi-croRNA clusters. RNA 2008, 14:1276-1283. 2441985, 18511500, 10.1261/rna.997708.
41. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 2008, 36:D154-D158. 2238936, 17991681, 10.1093/nar/gkm952.
42. Shalgi R, Lieber D, Oren M, Pilpel Y. Global and local architecture of the mammalian microRNA-transcription factor regulatory network. PLoS Comput Biol 2007, 3:e131. 1914371, 17630826, 10.1371/journal.pcbi.0030131.
43. Martinez NJ, Ow MC, Barrasa MI, Hammell M, Sequerra R, Doucette-Stamm L, Roth FP, Ambros VR, Walhout AJM. A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes & Development 2008, 22:2535-2549. 2546694, 18794350, 10.1101/gad.1678608.
44. Tsang J, Zhu J, van Oudenaarden A. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Molecular Cell 2007, 26:753-767. 2072999, 17560377, 10.1016/j.molcel.2007.05.018.
45. Liu H, Kohane IS. Tissue and process specific microRNA-mRNA co-expression in mammalian development and malignancy. PLoS ONE 2009, 4:e5436. 2673043, 19415117, 10.1371/journal.pone.0005436.
46. Lagace DC, Benavides DR, Kansy JW, Mapelli M, Greengard P, Bibb JA, Eisch AJ. Cdk5 is essential for adult hippocampal neurogenesis. Proc Natl Acad Sci USA 2008, 105:18567-18571. 2587597, 19017796, 10.1073/pnas.0810137105.
47. Nakata H, Kozasa T. Functional characterization of Galphao signaling through G protein-regulated inducer of neurite outgrowth 1. Mol Pharmacol 2005, 67:695-702. 10.1124/mol.104.003913, 15585744.
48. Moseley AE, Lieske SP, Wetzel RK, James PF, He S, Shelly DA, Paul RJ, Boivin GP, Witte DP, Ramirez JM, Sweadner KJ, Lingrel JB. The Na,K-ATPase alpha 2 isoform is expressed in neurons, and its absence disrupts neuronal activity in newborn mice. J Biol Chem 2003, 278:5317-5324. 10.1074/jbc.M211315200, 12458206.
49. Katsimpardi L, Gaitanou M, Malnou CE, Lledo PM, Charneau P, Matsas R, Thomaidou D. BM88/Cend1 expression levels are critical for proliferation and differentiation of subven-tricular zone-derived neural precursor cells. Stem Cells 2008, 26:1796-1807. 10.1634/stemcells.2007-0921, 18499894.
50. Meng H, Walker N, Su Y, Qiao X. Stargazin mutation impairs cerebellar synaptogenesis, synaptic maturation and synaptic protein distribution. Brain Res 2006, 1124:197-207. 10.1016/j.brainres.2006.09.086, 17070505.
51. Osterweil E, Wells D, Mooseker M. A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis. J Cell Biol 2005, 168:329-338. 2171578, 15657400, 10.1083/jcb.200410091.
52. Matthews L, Gopinath G, Gillespie M, Caudy M, Croft D, de Bono B, Garapati P, Hemish J, Herm-jakob H, Jassal B, Kanapin A, Lewis S, Mahajan S, May B, Schmidt E, Vastrik I, Wu G, Birney E, Stein L, D'Eustachio P. Reactome knowledgebase of human biological pathways and processes. Nucleic Acids Res 2009, 37:D619-622. 2686536, 18981052, 10.1093/nar/gkn863.
53. Huang E, Reichardt L. NEUROTROPHINS: Roles in Neuronal Development and Function. Annu Rev Neurosci 2001, 24:677-736. 10.1146/annurev.neuro.24.1.677, 11520916, 2758233.
54. Lugli G, Torvik VI, Larson J, Smalheiser NR. Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain. Journal of Neurochemistry 2008, 106:650-661. 10.1111/j.1471-4159.2008.05413.x, 18410515.
55. Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A, Brownstein MJ, Tuschl T, Mar-galit H. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res 2005, 33:2697-2706. 1110742, 15891114, 10.1093/nar/gki567.
56. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, van Dongen S, Inoue K, Enright AJ, Schier AF. Ze-brafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312:75-79. 10.1126/science.1122689, 16484454.
57. Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L. MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci 2008, 11:641-648. 10.1038/nn.2115, 18454145.
58. Shibata M, Kurokawa D, Nakao H, Ohmura T, Aizawa S. MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium. J Neurosci 2008, 28:10415-10421. 10.1523/JNEUROSCI.3219-08.2008, 18842901.
59. Falcon S, Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 2007, 23:257-258. 10.1093/bioinformatics/btl567, 17098774.
60. Lin SM, Du P, Huber W, Kibbe WA. Model-based variance-stabilizing transformation for Illu-mina microarray data. Nucleic Acids Research 2007, 36:e11-e11.
61. Du P, Kibbe WA, Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008, 24:1547-1548. 10.1093/bioinformatics/btn224, 18467348.
62. Smyth G. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3. Article3.
63. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JYH, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 545600, 15461798, 10.1186/gb-2004-5-10-r80.
64. Durinck S, Moreau Y, Kasprzyk A, Davis S, De B, Brazma A, Huber W. BioMart and Biocon-ductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 2005, 12:3439-3440.
65. Flicek P, Aken BL, Beal K, Ballester B, Caccamo M, Chen Y, Clarke L, Coates G, Cunningham F, Cutts T, Down T, Dyer SC, Eyre T, Fitzgerald S, Fernandez-Banet J, Graf S, Haider S, Hammond M, Holland R, Howe KL, Howe K, Johnson N, Jenk-inson A, Kahari A, Keefe D, Kokocinski F, Kule-sha E, Lawson D, Longden I, Megy K, Meidl P, Overduin B, Parker A, Pritchard B, Prlic A, Rice S, Rios D, Schuster M, Sealy I, Slater G, Smedley D, Spudich G, Trevanion S, Vilella AJ, Vogel J, White S, Wood M, Birney E, Cox T, Curwen V, Durbin R, Fernandez-Suarez XM, Herrero J, Hubbard TJP, Kasprzyk A, Proctor G, Smith J, Ureta-Vidal A, Searle S. Ensembl 2008. Nucleic Acids Res 2008, 36:D707-D714. 2238821, 18000006, 10.1093/nar/gkm988.
66. Rao Y, Lee Y, Jarjoura D, Ruppert A, Liu C. A Comparison of Normalization Techniques for MicroRNA Microarray Data. Stat Appl Genet Mol Biol 2008, 7. Article22.
67. Ning Z, Cox AJ, Mullikin JC. SSAHA: a fast search method for large DNA databases. Genome Res 2001, 11:1725-1729. 311141, 11591649, 10.1101/gr.194201.
68. Bak M, Silahtaroglu A, Moller M, Christensen M, Rath MF, Skryabin B, Tommerup N, Kauppinen S. MicroRNA expression in the adult mouse central nervous system. RNA 2008, 14:432-444. 2248253, 18230762, 10.1261/rna.783108.
69. Reactome Skypainter website. , http://www.reactome.org/cgi-bin/skypainter2
70. Flavell SW, Cowan CW, Kim TK, Greer PL, Lin Y, Paradis S, Griffith EC, Hu LS, Chen C, Greenberg ME. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 2006, 311:1008-1012. 10.1126/science.1122511, 16484497.