Microarray analysis of microRNA expression in the developing mammalian brain
Abstract
Background: MicroRNAs are a large new class of tiny regulatory RNAs found in nematodes, plants, insects and mammals. MicroRNAs are thought to act as post-transcriptional modulators of gene expression. In invertebrates microRNAs have been implicated as regulators of developmental timing, neuronal differentiation, cell proliferation, programmed cell death and fat metabolism. Little is known about the roles of microRNAs in mammals. Results: We isolated 18-26 nucleotide RNAs from developing rat and monkey brains. From the sequences of these RNAs and the sequences of the rat and human genomes we determined which of these small RNAs are likely to have derived from stem-loop precursors typical of microRNAs. Next, we developed a microarray technology suitable for detecting microRNAs and printed a microRNA microarray representing 138 mammalian microRNAs corresponding to the sequences of the microRNAs we cloned as well as to other known microRNAs. We used this microarray to determine the profile of microRNAs expressed in the developing mouse brain. We observed a temporal wave of expression of microRNAs, suggesting that microRNAs play important roles in the development of the mammalian brain. Conclusion: We describe a microarray technology that can be used to analyze the expression of microRNAs and of other small RNAs. MicroRNA microarrays offer a new tool that should facilitate studies of the biological roles of microRNAs. We used this method to determine the microRNA expression profile during mouse brain development and observed a temporal wave of gene expression of sequential classes of microRNAs.
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During development, many miRNAs are expressed in neurons or show distinct expression patterns within the developing CNS, implying their importance in brain development and function.
“During development, many miRNAs are expressed in neurons or show distinct expression patterns within the developing central nervous system (CNS), implying their importance in brain development and function (Krichevsky et al. 2003;Miska et al. 2004;Sempere et al. 2004;Smirnova et al. 2005;Wienholds et al. 2005).”
From MicroRNA expression in the adult mouse central nervous system (2008) · cites this paper as Miska et al. 2004
miR-124a expression can be detected in E11.5 mouse embryos and continues to be expressed in neurons of adult mice.
“While miR-124a expression can be detected in E11.5 mouse embryos and it continues to be expressed in neurons of adult mice (Miska et al. 2004;Visvanathan et al. 2007)”
From MicroRNA expression in the adult mouse central nervous system (2008) · cites this paper as Miska et al. 2004
Other miRNAs are temporally expressed during development of the CNS and are repressed in the mature CNS.
“other miRNAs are temporally expressed during development of the CNS being repressed in the mature CNS (Miska et al. 2004).”
From MicroRNA expression in the adult mouse central nervous system (2008) · cites this paper as Miska et al. 2004
Several miRNAs, including miR-9, miR-124a, miR-125b, miR-127, miR-128, and members of the let-7 family, were highly enriched in the mouse brain, giving strong hybridization signals on miRNA arrays.
“In agreement with previous reports, several miRNAs, including miR-9, miR-124a, miR-125b, miR-127, miR-128, and members of the let-7 family, were highly enriched in the mouse brain, giving strong hybridization signals on the miRNA arrays (Fig. 1A; Babak et al. 2004;Barad et al. 2004;Miska et al. 2004;Sempere et al. 2004;Shingara et al. 2005;Thomson et al. 2004).”
From MicroRNA expression in the adult mouse central nervous system (2008) · cites this paper as Miska et al. 2004
Expression profiling in adult tissues has identified miRNAs enriched in the CNS, suggesting that these miRNAs could play important regulatory roles in mature neurons.
“On the other hand, expression profiling in adult tissues has identified miRNAs enriched in the CNS, suggesting that these miRNAs could play important regulatory roles in mature neurons (Babak et al. 2004;Barad et al. 2004;Miska et al. 2004;Sempere et al. 2004;Thomson et al. 2004).”
From MicroRNA expression in the adult mouse central nervous system (2008) · cites this paper as Miska et al. 2004
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Cites
Mfold web server for nucleic acid folding and hybridization prediction
Zuker, M. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg595 · Cited by 13,404 · see citing works
The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14
Lee, R. C., Feinbaum, R. L., & Ambros, V. (1993) · Cell · doi:10.1016/0092-8674(93)90529-y · Cited by 12,948 · see citing works
Wightman, B., Ha, I., & Ruvkun, G. (1993) · Cell · doi:10.1016/0092-8674(93)90530-4 · Cited by 4,292 · see citing works
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · see citing works
Self-citationSempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., & Ambros, V. (2004) · Genome Biology · doi:10.1186/gb-2004-5-3-r13 · Cited by 1,578 · see citing works
A microRNA array reveals extensive regulation of microRNAs during brain development
KRICHEVSKY, A. M., KING, K. S., DONAHUE, C. P., KHRAPKO, K., & KOSIK, K. S. (2003) · RNA · doi:10.1261/rna.5980303 · Cited by 1,040 · see citing works
Flagged first, then by citations
Research works printed but not linked: 49
- Bartel DP MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004 116 281 297 14744438 10.1016/S0092-8674(04)00045-5 · DOI
- Ambros V Horvitz HR Heterochronic mutants of the nematode Caenorhabditis elegans Science 1984 226 409 416 6494891
- Reinhart BJ Slack FJ Basson M Pasquinelli AE Bettinger JC Rougvie AE Horvitz HR Ruvkun G The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans Nature 2000 403 901 906 10706289 10.1038/35002607 · DOI
- Reinhart BJ Weinstein EG Rhoades MW Bartel B Bartel DP MicroRNAs in plants. Genes Dev 2002 16 1616 1626 12101121 10.1101/gad.1004402 PMC186362 · DOI
- Lim LP Lau NC Weinstein EG Abdelhakim A Yekta S Rhoades MW Burge CB Bartel DP The microRNAs of Caenorhabditis elegans Genes Dev 2003 17 991 1008 12672692 10.1101/gad.1074403 PMC196042 · DOI · Paper page
- Lim LP Glasner ME Yekta S Burge CB Bartel DP Vertebrate microRNA genes. Science 2003 299 1540 12624257 10.1126/science.1080372 · DOI · Paper page
- Ambros V Lee RC Lavanway A Williams PT Jewell D MicroRNAs and other tiny endogenous RNAs in C. elegans Curr Biol 2003 13 807 818 12747828 10.1016/S0960-9822(03)00287-2 · DOI · Paper page
- Grad Y Aach J Hayes GD Reinhart BJ Church GM Ruvkun G Kim J Computational and experimental identification of C. elegans microRNAs. Mol Cell 2003 11 1253 1263 12769849 10.1016/S1097-2765(03)00153-9 · DOI
- Kim J Krichevsky A Grad Y Hayes GD Kosik KS Church GM Ruvkun G Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci USA 2004 101 360 365 14691248 10.1073/pnas.2333854100 PMC314190 · DOI
- Lee RC Ambros V An extensive class of small RNAs in Caenorhabditis elegans Science 2001 294 862 864 11679672 10.1126/science.1065329 · DOI · Paper page
- Lagos-Quintana M Rauhut R Lendeckel W Tuschl T Identification of novel genes coding for small expressed RNAs. Science 2001 294 853 858 11679670 10.1126/science.1064921 · DOI · Paper page
- Lau NC Lim LP Weinstein EG Bartel DP An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans Science 2001 294 858 862 11679671 10.1126/science.1065062 · DOI · Paper page
- Lagos-Quintana M Rauhut R Yalcin A Meyer J Lendeckel W Tuschl T Identification of tissue-specific microRNAs from mouse. Curr Biol 2002 12 735 739 12007417 10.1016/S0960-9822(02)00809-6 · DOI · Paper page
- Lagos-Quintana M Rauhut R Meyer J Borkhardt A Tuschl T New microRNAs from mouse and human. RNA 2003 9 175 179 12554859 10.1261/rna.2146903 PMC1370382 · DOI · Paper page
- Mourelatos Z Dostie J Paushkin S Sharma A Charroux B Abel L Rappsilber J Mann M Dreyfuss G miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev 2002 16 720 728 11914277 10.1101/gad.974702 PMC155365 · DOI · Paper page
- Dostie J Mourelatos Z Yang M Sharma A Dreyfuss G Numerous microRNPs in neuronal cells containing novel microRNAs. RNA 2003 9 180 186 12554860 10.1261/rna.2141503 PMC1370383 · DOI · Paper page
- Johnston RJ Hobert O A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans Nature 2003 426 845 849 14685240 10.1038/nature02255 · DOI
- Xu P Vernooy SY Guo M Hay BA The Drosophila microRNA mir-14 suppresses cell death and is required for normal fat metabolism. Curr Biol 2003 13 790 795 12725740 10.1016/S0960-9822(03)00250-1 · DOI
- Brennecke J Hipfner DR Stark A Russell RB Cohen SM bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila Cell 2003 113 25 36 12679032 10.1016/S0092-8674(03)00231-9 · DOI · Paper page
- Chen CZ Li L Lodish HF Bartel DP MicroRNAs modulate hematopoietic lineage differentiation. Science 2004 303 83 86 14657504 10.1126/science.1091903 · DOI · Paper page
- Calin GA Dumitru CD Shimizu M Bichi R Zupo S Noch E Aldler H Rattan S Keating M Rai K Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002 99 15524 15529 12434020 10.1073/pnas.242606799 PMC137750 · DOI · Paper page
- Lee Y Jeon K Lee JT Kim S Kim VN MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 2002 21 4663 4670 12198168 10.1093/emboj/cdf476 PMC126204 · DOI
- Lee Y Ahn C Han J Choi H Kim J Yim J Lee J Provost P Radmark O Kim S Kim VN The nuclear RNase III Drosha initiates microRNA processing. Nature 2003 425 415 419 14508493 10.1038/nature01957 · DOI
- Yi R Qin Y Macara IG Cullen BR Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003 17 3011 3016 14681208 10.1101/gad.1158803 PMC305252 · DOI
- Lund E Guttinger S Calado A Dahlberg JE Kutay U Nuclear export of microRNA precursors. Science 2004 303 95 98 14631048 10.1126/science.1090599 · DOI
- Khvorova A Reynolds A Jayasena SD Functional siRNAs and miRNAs exhibit strand bias. Cell 2003 115 209 216 14567918 10.1016/S0092-8674(03)00801-8 · DOI · Paper page
- Schwarz DS Hutvagner G Du T Xu Z Aronin N Zamore PD Asymmetry in the assembly of the RNAi enzyme complex. Cell 2003 115 199 208 14567917 10.1016/S0092-8674(03)00759-1 · DOI · Paper page
- Hutvagner G Zamore PD A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002 297 2056 2060 12154197 10.1126/science.1073827 · DOI
- Seggerson K Tang L Moss EG Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev Biol 2002 243 215 225 11884032 10.1006/dbio.2001.0563 · DOI
- Olsen PH Ambros V The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 1999 216 671 680 10642801 10.1006/dbio.1999.9523 · DOI · Paper page
- Llave C Xie Z Kasschau KD Carrington JC Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 2002 297 2053 2056 12242443 10.1126/science.1076311 · DOI · Paper page
- Kasschau KD Xie Z Allen E Llave C Chapman EJ Krizan KA Carrington JC P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 2003 4 205 217 12586064 10.1016/S1534-5807(03)00025-X · DOI · Paper page
- Kidner CA Martienssen RA Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 2004 428 81 84 14999284 10.1038/nature02366 · DOI
- Juarez MT Kui JS Thomas J Heller BA Timmermans MC microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004 428 84 88 14999285 10.1038/nature02363 · DOI
- Aukerman MJ Sakai H Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 2003 15 2730 2741 14555699 10.1105/tpc.016238 PMC280575 · DOI
- Chen X A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 2004 303 2022 2025 12893888 10.1126/science.1088060 PMC5127708 · DOI
- Angevine JB Sidman RL Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 1961 192 766 17533671
- 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 5 337 350 12919683 10.1016/S1534-5807(03)00228-4 · DOI
- Duggan DJ Bittner M Chen Y Meltzer P Trent JM Expression profiling using cDNA microarrays. Nat Genet 1999 21 1 Suppl 10 14 9915494 10.1038/4434 · DOI
- Schena M Shalon D Davis RW Brown PO Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 1995 270 467 470 7569999
- Nimmakayalu M Henegariu O Ward DC Bray-Ward P Simple method for preparation of fluor/hapten-labeled dUTP. Biotechniques 2000 28 518 522 10723566
- Gupta V Cherkassky A Chatis P Joseph R Johnson AL Broadbent J Erickson T DiMeo J Directly labeled mRNA produces highly precise and unbiased differential gene expression data. Nucleic Acids Res 2003 31 e13 12582258 10.1093/nar/gng013 PMC150245 · DOI
- Chenn A Braisted JE McConnell SK O'Leary DDM Cowan WM, Jessell TM, Zipursky SL Development of the cerebral cortex: mechanisms controlling cell fate, laminar and areal patterning, and axonal connectivity. Molecular and Cellular Approaches to Neural Development 1997 New York: Oxford University Press 440 473
- Chen C Regehr WG Developmental remodeling of the retinogeniculate synapse. Neuron 2000 28 955 966 11163279 10.1016/S0896-6273(00)00166-5 · DOI · Paper page
- Eisen MB Spellman PT Brown PO Botstein D Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998 95 14863 14868 9843981 10.1073/pnas.95.25.14863 PMC24541 · DOI · Paper page
- Taniguchi M Miura K Iwao H Yamanaka S Quantitative assessment of DNA microarrays - comparison with Northern blot analyses. Genomics 2001 71 34 39 11161795 10.1006/geno.2000.6427 · DOI
- Griffiths-Jones S The miRNA Registry. Nucleic Acids Res 2004 32 Database issue D109 D111 14681370 10.1093/nar/gkh023 PMC308757 · DOI
- Breslauer KJ Frank R Blocker H Marky LA Predicting DNA duplex stability from the base sequence. Proc Natl Acad Sci USA 1986 83 3746 3750 3459152 PMC323600
- Gibbs RA Weinstock GM Metzker ML Muzny DM Sodergren EJ Scherer S Scott G Steffen D Worley KC Burch PE Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 2004 428 493 521 15057822 10.1038/nature02426 · DOI
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- Authors
- Miska, E. A., Alvarez-Saavedra, E., Townsend, M., Yoshii, A., Šestan, N., Rakic, P., Constantine-Paton, M., & Horvitz, H. R.
- Venue
- Genome Biology
- Published
- 2004-08-31
- Volume
- 5
- Issue
- 9
- ISSN
- 1474-760X
- PMC
- PMC522875
- Cited by
- 651
- References
- 6
- Language
- en
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