Transcriptome analysis of microRNAs in developing cerebral cortex of rat

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Yao, Mao jin ^a,b   Chen, Gang ^a,b   Zhao, Ping ping ^a,b   Lu, Ming hua ^c,d   Jian, Jiang ^a,b   Liu, Mo fang ^c,d   Yuan, Xiao bing ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^d Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

Cerebral cortex; Development; MicroRNA; RNA editing

Indexed keywords

DICER; MICRORNA; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DNA FLANKING REGION; DNA MODIFICATION; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; RAT; RNA ANALYSIS; RNA SEQUENCE; RNA SYNTHESIS; SYNAPTOGENESIS;

ANIMALS; CEREBRAL CORTEX; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICRORNAS; RATS; RATS, SPRAGUE-DAWLEY; SEQUENCE ANALYSIS, RNA;

RATTUS;

EID: 84861994366     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-232     Document Type: Article

References (75)

1. Rakic P. A Century of Progress in Corticoneurogenesis: From Silver Impregnation to Genetic Engineering. Cerebral Cortex 2006, 16(1):i3-i17. 10.1093/cercor/bhk036, 16766705.
2. Bystron I, Blakemore C, Rakic P. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 2008, 9(2):110-122. 10.1038/nrn2252, 18209730.
3. Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 2008, 9(3):219-230. 10.1038/nrm2347, 18270516.
4. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116(2):281-297. 10.1016/S0092-8674(04)00045-5, 14744438.
5. Kawahara Y, Zinshteyn B, Sethupathy P, Iizasa H, Hatzigeorgiou AG, Nishikura K. Redirection of Silencing Targets by Adenosine-to-Inosine Editing of miRNAs. Science 2007, 315(5815):1137-1140. 10.1126/science.1138050, 2953418, 17322061.
6. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 2003, 9(10):1274-1281. 10.1261/rna.5980303, 1370491, 13130141.
7. Meza-Sosa KF, Valle-Garcia D, Pedraza-Alva G, Perez-Martinez L. Role of microRNAs in central nervous system development and pathology. J Neurosci Res 2012, 90(1):1-12. 10.1002/jnr.22701, 21922512.
8. Denli AM, Cao X, Gage FH. miR-9 and TLX: chasing tails in neural stem cells. Nat Struct Mol Biol 2009, 16(4):346-347. 10.1038/nsmb0409-346, 19343066.
9. 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(5):597-611. 10.1016/j.neuron.2010.01.027, 2843397, 20223197.
10. Zhao X, He X, Han X, Yu Y, Ye F, Chen Y, Hoang T, Xu X, Mi QS, Xin M, et al. MicroRNA-mediated control of oligodendrocyte differentiation. Neuron 2010, 65(5):612-626. 10.1016/j.neuron.2010.02.018, 2855245, 20223198.
11. Cheng LC, Pastrana E, Tavazoie M, Doetsch F. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat Neurosci 2009, 12(4):399-408. 10.1038/nn.2294, 2766245, 19287386.
12. 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 Dev 2007, 21(7):744-749. 10.1101/gad.1519107, 1838526, 17403776.
13. 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(7074):283-289. 10.1038/nature04367, 16421561.
14. Hughes AE, Bradley DT, Campbell M, Lechner J, Dash DP, Simpson DA, Willoughby CE. Mutation Altering the miR-184 Seed Region Causes Familial Keratoconus with Cataract. Am J Hum Genet 2011, 89(5):628-633. 10.1016/j.ajhg.2011.09.014, 3213395, 21996275.
15. Mencia A, Modamio-Hoybjor S, Redshaw N, Morin M, Mayo-Merino F, Olavarrieta L, Aguirre LA, del Castillo I, Steel KP, Dalmay T, et al. Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat Genet 2009, 41(5):609-613. 10.1038/ng.355, 19363479.
16. Wang G, van der Walt JM, Mayhew G, Li YJ, Zuchner S, Scott WK, Martin ER, Vance JM. Variation in the miRNA-433 binding site of FGF20 confers risk for Parkinson disease by overexpression of alpha-synuclein. Am J Hum Genet 2008, 82(2):283-289. 10.1016/j.ajhg.2007.09.021, 2427225, 18252210.
17. Schaefer A, O'Carroll D, Tan CL, Hillman D, Sugimori M, Llinas R, Greengard P. Cerebellar neurodegeneration in the absence of microRNAs. Journal of Experimental Medicine 2007, 204(7):1553-1558. 10.1084/jem.20070823, 2118654, 17606634.
18. Bremer J, O'Connor T, Tiberi C, Rehrauer H, Weis J, Aguzzi A. Ablation of Dicer from murine Schwann cells increases their proliferation while blocking myelination. PLoS One 2010, 5(8):e12450. 10.1371/journal.pone.0012450, 2929198, 20805985.
19. Cuellar TL, Davis TH, Nelson PT, Loeb GB, Harfe BD, Ullian E, McManus MT. Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc Natl Acad Sci U S A 2008, 105(14):5614-5619. 10.1073/pnas.0801689105, 2291142, 18385371.
20. Davis TH, Cuellar TL, Koch SM, Barker AJ, Harfe BD, McManus MT, Ullian EM. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J Neurosci 2008, 28(17):4322-4330. 10.1523/JNEUROSCI.4815-07.2008, 18434510.
21. Han X, Wu X, Chung WY, Li T, Nekrutenko A, Altman NS, Chen G, Ma H. Transcriptome of embryonic and neonatal mouse cortex by high-throughput RNA sequencing. Proc Natl Acad Sci U S A 2009, 106(31):12741-12746. 10.1073/pnas.0902417106, 2722358, 19617558.
22. 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. 10.1186/1471-2199-7-3, 1413964, 16448564.
23. Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, Zhao Y, McDonald H, Zeng T, Hirst M, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 2008, 18(4):610-621. 10.1101/gr.7179508, 2279248, 18285502.
24. Kato M, de Lencastre A, Pincus Z, Slack FJ. Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 2009, 10(5):R54. 10.1186/gb-2009-10-5-r54, 2718520, 19460142.
25. Raedler E, Raedler A. Autoradiographic study of early neurogenesis in rat neocortex. Anat Embryol (Berl) 1978, 154(3):267-284.
26. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39:D152-157. 10.1093/nar/gkq1027, 3013655, 21037258.
27. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, et al. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 2005, 33(20):e179. 10.1093/nar/gni178, 1292995, 16314309.
28. Tay YM, Tam WL, Ang YS, Gaughwin PM, Yang H, Wang W, Liu R, George J, Ng HH, Perera RJ, et al. MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1. Stem Cells 2008, 26(1):17-29. 10.1634/stemcells.2007-0295, 17916804.
29. Gao J, Wang WY, Mao YW, Graff J, Guan JS, Pan L, Mak G, Kim D, Su SC, Tsai LH. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 2010, 466(7310):1105-1109. 10.1038/nature09271, 2928875, 20622856.
30. Christensen M, Larsen LA, Kauppinen S, Schratt G. Recombinant Adeno-Associated Virus-Mediated microRNA Delivery into the Postnatal Mouse Brain Reveals a Role for miR-134 in Dendritogenesis in Vivo. Front Neural Circuits 2010, 3(16):1-10.
31. Yuan X. Axon guidance and neuronal migration research in China. Sci China Life Sci 2010, 53(3):304-314. 10.1007/s11427-010-0068-6, 20596924.
32. Smrt RD, Szulwach KE, Pfeiffer RL, Li X, Guo W, Pathania M, Teng ZQ, Luo Y, Peng J, Bordey A, et al. MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 2010, 28(6):1060-1070. 10.1002/stem.431, 3140955, 20506192.
33. Linsen SE, de Wit E, de Bruijn E, Cuppen E. Small RNA expression and strain specificity in the rat. BMC Genomics 2010, 11:249. 10.1186/1471-2164-11-249, 2864251, 20403161.
34. Colon-Ramos DA. Synapse formation in developing neural circuits. Curr Top Dev Biol 2009, 87:53-79.
35. Chen X, Li Q, Wang J, Guo X, Jiang X, Ren Z, Weng C, Sun G, Wang X, Liu Y, et al. Identification and characterization of novel amphioxus microRNAs by Solexa sequencing. Genome Biol 2009, 10(7):R78. 10.1186/gb-2009-10-7-r78, 2728532, 19615057.
36. Sauvageot CM, Stiles CD. Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol 2002, 12(3):244-249. 10.1016/S0959-4388(02)00322-7, 12049929.
37. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009, 19(1):92-105. 2612969, 18955434.
38. Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 2007, 4(9):721-726. 10.1038/nmeth1079, 17694064.
39. Liu N, Abe M, Sabin LR, Hendriks GJ, Naqvi AS, Yu Z, Cherry S, Bonini NM. The exoribonuclease Nibbler controls 3' end processing of microRNAs in Drosophila. Curr Biol 2011, 21(22):1888-1893. 10.1016/j.cub.2011.10.006, 3255556, 22055292.
40. Han BW, Hung JH, Weng Z, Zamore PD, Ameres SL. The 3'-to-5' exoribonuclease Nibbler shapes the 3' ends of microRNAs bound to Drosophila Argonaute1. Curr Biol 2011, 21(22):1878-1887. 10.1016/j.cub.2011.09.034, 3236499, 22055293.
41. Marti E, Pantano L, Banez-Coronel M, Llorens F, Minones-Moyano E, Porta S, Sumoy L, Ferrer I, Estivill X. A myriad of miRNA variants in control and Huntington's disease brain regions detected by massively parallel sequencing. Nucleic Acids Res 2010, 38(20):7219-7235. 10.1093/nar/gkq575, 2978354, 20591823.
42. Nishikura K. Functions and Regulation of RNA Editing by ADAR Deaminases. Annual Review of Biochemistry 2010, 79(1):321-349. 10.1146/annurev-biochem-060208-105251, 2953425, 20192758.
43. Mehler MF, Mattick JS. Noncoding RNAs and RNA editing in brain development, functional diversification, and neurological disease. Physiol Rev 2007, 87(3):799-823. 10.1152/physrev.00036.2006, 17615389.
44. Kawahara Y, Megraw M, Kreider E, Iizasa H, Valente L, Hatzigeorgiou AG, Nishikura K. Frequency and fate of microRNA editing in human brain. Nucleic Acids Research 2008, 36(16):5270-5280. 10.1093/nar/gkn479, 2532740, 18684997.
45. Caiment F, Charlier C, Hadfield T, Cockett N, Georges M, Baurain D. Assessing the effect of the CLPG mutation on the microRNA catalog of skeletal muscle using high-throughput sequencing. Genome Res 2010, 20(12):1651-1662. 10.1101/gr.108787.110, 2989991, 20944086.
46. Reid JG, Nagaraja AK, Lynn FC, Drabek RB, Muzny DM, Shaw CA, Weiss MK, Naghavi AO, Khan M, Zhu H, et al. Mouse let-7 miRNA populations exhibit RNA editing that is constrained in the 5'-seed/cleavage/anchor regions and stabilize predicted mmu-let-7a:mRNA duplexes. Genome Res 2008, 18(10):1571-1581. 10.1101/gr.078246.108, 2556275, 18614752.
47. Athanasiadis A, Rich A, Maas S. Widespread A-to-I RNA Editing of Alu-Containing mRNAs in the Human Transcriptome. PLoS Biology 2004, 2(12):e391. 10.1371/journal.pbio.0020391, 526178, 15534692.
48. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M. A Mammalian microRNA Expression Atlas Based on Small RNA Library Sequencing. Cell 2007, 129(7):1401-1414. 10.1016/j.cell.2007.04.040, 2681231, 17604727.
49. Li JB, Levanon EY, Yoon JK, Aach J, Xie B, LeProust E, Zhang K, Gao Y, Church GM. Genome-Wide Identification of Human RNA Editing Sites by Parallel DNA Capturing and Sequencing. Science 2009, 324(5931):1210-1213. 10.1126/science.1170995, 19478186.
50. Junker A, Hohlfeld R, Meinl E. The emerging role of microRNAs in multiple sclerosis. Nat Rev Neurol 2011, 7(1):56-59. 10.1038/nrneurol.2010.179, 21151203.
51. Ambasudhan R, Talantova M, Coleman R, Yuan X, Zhu S, Lipton SA, Ding S. Direct Reprogramming of Adult Human Fibroblasts to Functional Neurons under Defined Conditions. Cell Stem Cell 2011, 9(2):113-118. 10.1016/j.stem.2011.07.002, 21802386.
52. Yoo AS, Sun AX, Li L, Shcheglovitov A, Portmann T, Li Y, Lee-Messer C, Dolmetsch RE, Tsien RW, Crabtree GR. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 2011, 476(7359):228-231. 10.1038/nature10323, 3348862, 21753754.
53. 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(9):R68. 10.1186/gb-2004-5-9-r68, 522875, 15345052.
54. Reenan RA. The RNA world meets behavior: A- I pre-mRNA editing in animals. Trends Genet 2001, 17(2):53-56. 10.1016/S0168-9525(00)02169-7, 11173098.
55. Brusa R, Zimmermann F, Koh DS, Feldmeyer D, Gass P, Seeburg PH, Sprengel R. Early-onset epilepsy and postnatal lethality associated with an editing-deficient GluR-B allele in mice. Science 1995, 270(5242):1677-1680. 10.1126/science.270.5242.1677, 7502080.
56. Peng PL, Zhong X, Tu W, Soundarapandian MM, Molner P, Zhu D, Lau L, Liu S, Liu F, Lu Y. ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 2006, 49(5):719-733. 10.1016/j.neuron.2006.01.025, 16504947.
57. Bogerd HP, Wiegand HL, Doehle BP, Lueders KK, Cullen BR. APOBEC3A and APOBEC3B are potent inhibitors of LTR-retrotransposon function in human cells. Nucleic Acids Res 2006, 34(1):89-95. 10.1093/nar/gkj416, 1326241, 16407327.
58. Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 2009, 25:355-376. 10.1146/annurev.cellbio.24.110707.175327, 2780330, 19575643.
59. Reinhart BJ, Bartel DP. Small RNAs correspond to centromere heterochromatic repeats. Science 2002, 297(5588):1831. 10.1126/science.1077183, 12193644.
60. Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B, Gaasterland T, Meyer J, Tuschl T. The small RNA profile during Drosophila melanogaster development. Dev Cell 2003, 5(2):337-350. 10.1016/S1534-5807(03)00228-4, 12919683.
61. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007, 316(5825):744-747. 10.1126/science.1142612, 17446352.
62. Saito K, Nishida KM, Mori T, Kawamura Y, Miyoshi K, Nagami T, Siomi H, Siomi MC. Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 2006, 20(16):2214-2222. 10.1101/gad.1454806, 1553205, 16882972.
63. Aravin AA, Hannon GJ, Brennecke J. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 2007, 318(5851):761-764. 10.1126/science.1146484, 17975059.
64. Dharap A, Nakka VP, Vemuganti R. Altered Expression of PIWI RNA in the Rat Brain After Transient Focal Ischemia. Stroke 2011, 42(4):1105-1109. 10.1161/STROKEAHA.110.598391, 21311060.
65. Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T, Kandel ER. A Role for Neuronal piRNAs in the Epigenetic Control of Memory-Related Synaptic Plasticity. Cell 2012, 149(3):693-707. 10.1016/j.cell.2012.02.057, 22541438.
66. Sai Lakshmi S, Agrawal S. piRNABank: a web resource on classified and clustered Piwi-interacting RNAs. Nucleic Acids Res 2008, 36:D173-177. 2238943, 17881367.
67. Muotri AR, Chu VT, Marchetto MC, Deng W, Moran JV, Gage FH. Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition. Nature 2005, 435(7044):903-910. 10.1038/nature03663, 15959507.
68. Coufal NG, Garcia-Perez JL, Peng GE, Yeo GW, Mu Y, Lovci MT, Morell M, O'Shea KS, Moran JV, Gage FH. L1 retrotransposition in human neural progenitor cells. Nature 2009, 460(7259):1127-1131. 10.1038/nature08248, 2909034, 19657334.
69. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR. Rfam: updates to the RNA families database. Nucleic Acids Res 2009, 37:D136-140. 10.1093/nar/gkn766, 2686503, 18953034.
70. Griffiths-Jones S. Annotating non-coding RNAs with Rfam. Curr Protoc Bioinformatics 2005, 12:12-15.
71. Wu JQ, Habegger L, Noisa P, Szekely A, Qiu C, Hutchison S, Raha D, Egholm M, Lin H, Weissman S, et al. Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing. Proc Natl Acad Sci USA 2010, 107(11):5254-5259. 10.1073/pnas.0914114107, 2841935, 20194744.
72. Luo F, Khan L, Bastani F, Yen IL, Zhou J. A dynamically growing self-organizing tree (DGSOT) for hierarchical clustering gene expression profiles. Bioinformatics 2004, 20(16):2605-2617. 10.1093/bioinformatics/bth292, 15130935.
73. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009, 10:48. 10.1186/1471-2105-10-48, 2644678, 19192299.
74. Livak KJ, Schmittgen TD. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 - ΔΔCT Method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.
75. Wang Y, Bi Q, Dong L, Li X, Ge X, Zhang X, Fu J, Wu D, Li S. Quinacrine enhances cisplatin-induced cytotoxicity in four cancer cell lines. Chemotherapy 2010, 56(2):127-134. 10.1159/000313525, 20407239.