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MicroRNA Expression in Zebrafish Embryonic Development
Erno Wienholds,1Wigard P. Kloosterman,1Eric Miska,2,3Ezequiel Alvarez-Saavedra,2Eugene Berezikov,1Ewart de Bruijn,1H. Robert Horvitz,2Sakari Kauppinen,4Ronald H. A. Plasterk1*
MicroRNAs (miRNAs) are small noncoding RNAs, about 21 nucleotidesin length, that can regulate gene expression by base-pairingto partially complementary mRNAs. Regulation by miRNAs can playessential roles in embryonic development. We determined thetemporal and spatial expression patterns of 115 conserved vertebratemiRNAs in zebrafish embryos by microarrays and by in situ hybridizations,using locked-nucleic acidmodified oligonucleotide probes.Most miRNAs were expressed in a highly tissue-specific mannerduring segmentation and later stages, but not early in development,which suggests that their role is not in tissue fate establishmentbut in differentiation or maintenance of tissue identity.
1 Hubrecht Laboratory, Centre for Biomedical Genetics, 3584 CT Utrecht, the Netherlands. 2 Howard Hughes Medical Institute, Department of Biology and McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USA. 3 Wellcome Trust, Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK. 4 Wilhelm Johannsen Centre for Functional Genome Research, Institute of Medical Biochemistry and Genetics, University of Copenhagen, DK-2200 Copenhagen N, Denmark.
* To whom correspondence should be addressed. E-mail: plasterk{at}niob.knaw.nl
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L. M. Friedman, A. A. Dror, E. Mor, T. Tenne, G. Toren, T. Satoh, D. J. Biesemeier, N. Shomron, D. M. Fekete, E. Hornstein, et al. (2009)
PNAS
106, 7915-7920
|Abstract »|Full Text »|PDF »
Evolutionary Origin and Genomic Organization of Micro-RNA Genes in Immunoglobulin Lambda Variable Region Gene Family.
MicroRNA expression profiling during neural differentiation of mouse embryonic carcinoma P19 cells.
B. Huang, W. Li, B. Zhao, C. Xia, R. Liang, K. Ruan, N. Jing, and Y. Jin (2009)
Acta Biochim Biophys Sin
41, 231-236
|Abstract »|Full Text »|PDF »
Pattern formation via small RNA mobility.
D. H. Chitwood, F. T.S. Nogueira, M. D. Howell, T. A. Montgomery, J. C. Carrington, and M. C.P. Timmermans (2009)
Genes & Dev.
23, 549-554
|Abstract »|Full Text »|PDF »
Zebrafish miR-1 and miR-133 shape muscle gene expression and regulate sarcomeric actin organization.
Y. Mishima, C. Abreu-Goodger, A. A. Staton, C. Stahlhut, C. Shou, C. Cheng, M. Gerstein, A. J. Enright, and A. J. Giraldez (2009)
Genes & Dev.
23, 619-632
|Abstract »|Full Text »|PDF »
miR-451 regulates zebrafish erythroid maturation in vivo via its target gata2.
L. Pase, J. E. Layton, W. P. Kloosterman, D. Carradice, P. M. Waterhouse, and G. J. Lieschke (2009)
Blood
113, 1794-1804
|Abstract »|Full Text »|PDF »
Coherent but overlapping expression of microRNAs and their targets during vertebrate development.
A. Shkumatava, A. Stark, H. Sive, and D. P. Bartel (2009)
Genes & Dev.
23, 466-481
|Abstract »|Full Text »|PDF »
Uncovering Growth-Suppressive MicroRNAs in Lung Cancer.
X. Liu, L. F. Sempere, F. Galimberti, S. J. Freemantle, C. Black, K. H. Dragnev, Y. Ma, S. Fiering, V. Memoli, H. Li, et al. (2009)
Clin. Cancer Res.
15, 1177-1183
|Abstract »|Full Text »|PDF »
Mir-144 selectively regulates embryonic {alpha}-hemoglobin synthesis during primitive erythropoiesis.
Y.-F. Fu, T.-T. Du, M. Dong, K.-Y. Zhu, C.-B. Jing, Y. Zhang, L. Wang, H.-B. Fan, Y. Chen, Y. Jin, et al. (2009)
Blood
113, 1340-1349
|Abstract »|Full Text »|PDF »
Evolution of microRNA expression during human bronchial squamous carcinogenesis.
C. Mascaux, J. F. Laes, G. Anthoine, A. Haller, V. Ninane, A. Burny, and J. P. Sculier (2009)
Eur. Respir. J.
33, 352-359
|Abstract »|Full Text »|PDF »
miR2Disease: a manually curated database for microRNA deregulation in human disease.
Q. Jiang, Y. Wang, Y. Hao, L. Juan, M. Teng, X. Zhang, M. Li, G. Wang, and Y. Liu (2009)
Nucleic Acids Res.
37, D98-D104
|Abstract »|Full Text »|PDF »
Experimental identification of microRNA-140 targets by silencing and overexpressing miR-140.
F. E. Nicolas, H. Pais, F. Schwach, M. Lindow, S. Kauppinen, V. Moulton, and T. Dalmay (2008)
RNA
14, 2513-2520
|Abstract »|Full Text »|PDF »
Genome-scale spatiotemporal analysis of Caenorhabditis elegans microRNA promoter activity.
N. J. Martinez, M. C. Ow, J. S. Reece-Hoyes, M. I. Barrasa, V. R. Ambros, and A. J.M. Walhout (2008)
Genome Res.
18, 2005-2015
|Abstract »|Full Text »|PDF »
Human multipotent stromal cells from bone marrow and microRNA: Regulation of differentiation and leukemia inhibitory factor expression.
A. Z. Oskowitz, J. Lu, P. Penfornis, J. Ylostalo, J. McBride, E. K. Flemington, D. J. Prockop, and R. Pochampally (2008)
PNAS
105, 18372-18377
|Abstract »|Full Text »|PDF »
MicroRNA-338 Regulates Local Cytochrome c Oxidase IV mRNA Levels and Oxidative Phosphorylation in the Axons of Sympathetic Neurons.
A. Aschrafi, A. D. Schwechter, M. G. Mameza, O. Natera-Naranjo, A. E. Gioio, and B. B. Kaplan (2008)
J. Neurosci.
28, 12581-12590
|Abstract »|Full Text »|PDF »
microRNA-138 modulates cardiac patterning during embryonic development.
S. U. Morton, P. J. Scherz, K. R. Cordes, K. N. Ivey, D. Y. R. Stainier, and D. Srivastava (2008)
PNAS
105, 17830-17835
|Abstract »|Full Text »|PDF »
The Steady-State Level of the Nervous-System-Specific MicroRNA-124a Is Regulated by dFMR1 in Drosophila.
X.-L. Xu, Y. Li, F. Wang, and F.-B. Gao (2008)
J. Neurosci.
28, 11883-11889
|Abstract »|Full Text »|PDF »
Analysis of regulatory network topology reveals functionally distinct classes of microRNAs.
X. Yu, J. Lin, D. J. Zack, J. T. Mendell, and J. Qian (2008)
Nucleic Acids Res.
36, 6494-6503
|Abstract »|Full Text »|PDF »
Podocyte-Specific Deletion of Dicer Alters Cytoskeletal Dynamics and Causes Glomerular Disease.
S. J. Harvey, G. Jarad, J. Cunningham, S. Goldberg, B. Schermer, B. D. Harfe, M. T. McManus, T. Benzing, and J. H. Miner (2008)
J. Am. Soc. Nephrol.
19, 2150-2158
|Abstract »|Full Text »|PDF »
Podocyte-Specific Loss of Functional MicroRNAs Leads to Rapid Glomerular and Tubular Injury.
J. Ho, K. H. Ng, S. Rosen, A. Dostal, R. I. Gregory, and J. A. Kreidberg (2008)
J. Am. Soc. Nephrol.
19, 2069-2075
|Abstract »|Full Text »|PDF »
Maternal Argonaute 2 Is Essential for Early Mouse Development at the Maternal-Zygotic Transition.
K. Lykke-Andersen, M. J. Gilchrist, J. B. Grabarek, P. Das, E. Miska, and M. Zernicka-Goetz (2008)
Mol. Biol. Cell
19, 4383-4392
|Abstract »|Full Text »|PDF »
Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation.
M. E. Dinger, P. P. Amaral, T. R. Mercer, K. C. Pang, S. J. Bruce, B. B. Gardiner, M. E. Askarian-Amiri, K. Ru, G. Solda, C. Simons, et al. (2008)
Genome Res.
18, 1433-1445
|Abstract »|Full Text »|PDF »
Dispatched Homolog 2 is targeted by miR-214 through a combination of three weak microRNA recognition sites.
N. Li, A. S. Flynt, H. R. Kim, L. Solnica-Krezel, and J. G. Patton (2008)
Nucleic Acids Res.
36, 4277-4285
|Abstract »|Full Text »|PDF »
Circulating microRNAs as stable blood-based markers for cancer detection.
P. S. Mitchell, R. K. Parkin, E. M. Kroh, B. R. Fritz, S. K. Wyman, E. L. Pogosova-Agadjanyan, A. Peterson, J. Noteboom, K. C. O'Briant, A. Allen, et al. (2008)
PNAS
105, 10513-10518
|Abstract »|Full Text »|PDF »
Inducible expression of microRNA-194 is regulated by HNF-1{alpha} during intestinal epithelial cell differentiation.
K. Hino, K. Tsuchiya, T. Fukao, K. Kiga, R. Okamoto, T. Kanai, and M. Watanabe (2008)
RNA
14, 1433-1442
|Abstract »|Full Text »|PDF »
Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis.
N. S. Sokol, P. Xu, Y.-N. Jan, and V. Ambros (2008)
Genes & Dev.
22, 1591-1596
|Abstract »|Full Text »|PDF »
Conservation of small RNA pathways in platypus.
E. P. Murchison, P. Kheradpour, R. Sachidanandam, C. Smith, E. Hodges, Z. Xuan, M. Kellis, F. Grutzner, A. Stark, and G. J. Hannon (2008)
Genome Res.
18, 995-1004
|Abstract »|Full Text »|PDF »
A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach.
E. A. Glazov, P. A. Cottee, W. C. Barris, R. J. Moore, B. P. Dalrymple, and M. L. Tizard (2008)
Genome Res.
18, 957-964
|Abstract »|Full Text »|PDF »
The miR-200 Family Inhibits Epithelial-Mesenchymal Transition and Cancer Cell Migration by Direct Targeting of E-cadherin Transcriptional Repressors ZEB1 and ZEB2.
M. Korpal, E. S. Lee, G. Hu, and Y. Kang (2008)
J. Biol. Chem.
283, 14910-14914
|Abstract »|Full Text »|PDF »
RNAs as extracellular signaling molecules.
M. E Dinger, T. R Mercer, and J. S Mattick (2008)
J. Mol. Endocrinol.
40, 151-159
|Abstract »|Full Text »|PDF »
Alterations in Micro-Ribonucleic Acid Expression Profiles Reveal a Novel Pathway for Estrogen Regulation.
A. Cohen, M. Shmoish, L. Levi, U. Cheruti, B. Levavi-Sivan, and E. Lubzens (2008)
Endocrinology
149, 1687-1696
|Abstract »|Full Text »|PDF »
Gene Regulation by Transcription Factors and MicroRNAs.
Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver.
J. Elmen, M. Lindow, A. Silahtaroglu, M. Bak, M. Christensen, A. Lind-Thomsen, M. Hedtjarn, J. B. Hansen, H. F. Hansen, E. M. Straarup, et al. (2008)
Nucleic Acids Res.
36, 1153-1162
|Abstract »|Full Text »|PDF »
Micromanaging regeneration.
E. M. Tanaka and G. Weidinger (2008)
Genes & Dev.
22, 700-705
|Full Text »|PDF »
MicroRNA expression in the adult mouse central nervous system.
M. Bak, A. Silahtaroglu, M. Moller, M. Christensen, M. F. Rath, B. Skryabin, N. Tommerup, and S. Kauppinen (2008)
RNA
14, 432-444
|Abstract »|Full Text »|PDF »
MicroRNAs and the advent of vertebrate morphological complexity.
A. M. Heimberg, L. F. Sempere, V. N. Moy, P. C. J. Donoghue, and K. J. Peterson (2008)
PNAS
105, 2946-2950
|Abstract »|Full Text »|PDF »
Dicer-dependent pathways regulate chondrocyte proliferation and differentiation.
T. Kobayashi, J. Lu, B. S. Cobb, S. J. Rodda, A. P. McMahon, E. Schipani, M. Merkenschlager, and H. M. Kronenberg (2008)
PNAS
105, 1949-1954
|Abstract »|Full Text »|PDF »
Development of a Dual-Luciferase Reporter System for In Vivo Visualization of MicroRNA Biogenesis and Posttranscriptional Regulation.
J. Y. Lee, S. Kim, D. W. Hwang, J. M. Jeong, J.-K. Chung, M. C. Lee, and D. S. Lee (2008)
J. Nucl. Med.
49, 285-294
|Abstract »|Full Text »|PDF »
Asymmetric Involution of the Myocardial Field Drives Heart Tube Formation in Zebrafish.
S. Rohr, C. Otten, and S. Abdelilah-Seyfried (2008)
Circ. Res.
102, e12-e19
|Abstract »|Full Text »|PDF »
Altered MicroRNA Expression Confined to Specific Epithelial Cell Subpopulations in Breast Cancer.
L. F. Sempere, M. Christensen, A. Silahtaroglu, M. Bak, C. V. Heath, G. Schwartz, W. Wells, S. Kauppinen, and C. N. Cole (2007)
Cancer Res.
67, 11612-11620
|Abstract »|Full Text »|PDF »
Emerging Role of MicroRNAs in Cardiovascular Biology.
M. V.G. Latronico, D. Catalucci, and G. Condorelli (2007)
Circ. Res.
101, 1225-1236
|Abstract »|Full Text »|PDF »
MicroRNA-21 Knockdown Disrupts Glioma Growth In vivo and Displays Synergistic Cytotoxicity with Neural Precursor Cell Delivered S-TRAIL in Human Gliomas.
M. F. Corsten, R. Miranda, R. Kasmieh, A. M. Krichevsky, R. Weissleder, and K. Shah (2007)
Cancer Res.
67, 8994-9000
|Abstract »|Full Text »|PDF »
A simple array platform for microRNA analysis and its application in mouse tissues.
X. Tang, J. Gal, X. Zhuang, W. Wang, H. Zhu, and G. Tang (2007)
RNA
13, 1803-1822
|Abstract »|Full Text »|PDF »
MicroRNA (miRNA) Transcriptome of Mouse Retina and Identification of a Sensory Organ-specific miRNA Cluster.
S. Xu, P. D. Witmer, S. Lumayag, B. Kovacs, and D. Valle (2007)
J. Biol. Chem.
282, 25053-25066
|Abstract »|Full Text »|PDF »
MicroRNAs in the Human Heart: A Clue to Fetal Gene Reprogramming in Heart Failure.
T. Thum, P. Galuppo, C. Wolf, J. Fiedler, S. Kneitz, L. W. van Laake, P. A. Doevendans, C. L. Mummery, J. Borlak, A. Haverich, et al. (2007)
Circulation
116, 258-267
|Abstract »|Full Text »|PDF »
Role of Dicer and Drosha for Endothelial MicroRNA Expression and Angiogenesis.
A. Kuehbacher, C. Urbich, A. M. Zeiher, and S. Dimmeler (2007)
Circ. Res.
101, 59-68
|Abstract »|Full Text »|PDF »
Noncoding RNAs and RNA Editing in Brain Development, Functional Diversification, and Neurological Disease.
Gallus Expression In Situ Hybridization Analysis: A Chicken Embryo Gene Expression Database.
P. B. Antin, S. Kaur, S. Stanislaw, S. Davey, J. H. Konieczka, T. A. Yatskievych, and D. K. Darnell (2007)
Poult. Sci.
86, 1472-1477
|Abstract »|Full Text »|PDF »
Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates.
H. Kikuta, M. Laplante, P. Navratilova, A. Z. Komisarczuk, P. G. Engstrom, D. Fredman, A. Akalin, M. Caccamo, I. Sealy, K. Howe, et al. (2007)
Genome Res.
17, 545-555
|Abstract »|Full Text »|PDF »
Dicer Dependent MicroRNAs Regulate Gene Expression and Functions in Human Endothelial Cells.
Y. Suarez, C. Fernandez-Hernando, J. S. Pober, and W. C. Sessa (2007)
Circ. Res.
100, 1164-1173
|Abstract »|Full Text »|PDF »
miRNAs in cancer: approaches, aetiology, diagnostics and therapy.
Discovery and profiling of bovine microRNAs from immune-related and embryonic tissues.
L. L. Coutinho, L. K. Matukumalli, T. S. Sonstegard, C. P. Van Tassell, L. C. Gasbarre, A. V. Capuco, and T. P. L. Smith (2007)
Physiol Genomics
29, 35-43
|Abstract »|Full Text »|PDF »
Identification and Characterization of MicroRNAs Expressed in the Mouse Eye.
M. Karali, I. Peluso, V. Marigo, and S. Banfi (2007)
Invest. Ophthalmol. Vis. Sci.
48, 509-515
|Abstract »|Full Text »|PDF »
Post-transcriptional regulation of the let-7 microRNA during neural cell specification.
F. G. Wulczyn, L. Smirnova, A. Rybak, C. Brandt, E. Kwidzinski, O. Ninnemann, M. Strehle, A. Seiler, S. Schumacher, and R. Nitsch (2007)
FASEB J
21, 415-426
|Abstract »|Full Text »|PDF »
Global analysis of microRNA target gene expression reveals that miRNA targets are lower expressed in mature mouse and Drosophila tissues than in the embryos.
Z. Yu, Z. Jian, S.-H. Shen, E. Purisima, and E. Wang (2007)
Nucleic Acids Res.
35, 152-164
|Abstract »|Full Text »|PDF »
MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development.
P. L. Boutz, G. Chawla, P. Stoilov, and D. L. Black (2007)
Genes & Dev.
21, 71-84
|Abstract »|Full Text »|PDF »
MicroRNAs: regulators of gene expression and cell differentiation.
MIR-206 regulates connexin43 expression during skeletal muscle development.
C. Anderson, H. Catoe, and R. Werner (2006)
Nucleic Acids Res.
34, 5863-5871
|Abstract »|Full Text »|PDF »
Denoising feedback loops by thresholding--a new role for microRNAs..
S. M. Cohen, J. Brennecke, and A. Stark (2006)
Genes & Dev.
20, 2769-2772
|Full Text »|PDF »
Optimization of Feline Immunodeficiency Virus Vectors for RNA Interference.
S. Q. Harper, P. D. Staber, C. R. Beck, S. K. Fineberg, C. Stein, D. Ochoa, and B. L. Davidson (2006)
J. Virol.
80, 9371-9380
|Abstract »|Full Text »|PDF »
Many novel mammalian microRNA candidates identified by extensive cloning and RAKE analysis.
E. Berezikov, G. van Tetering, M. Verheul, J. van de Belt, L. van Laake, J. Vos, R. Verloop, M. van de Wetering, V. Guryev, S. Takada, et al. (2006)
Genome Res.
16, 1289-1298
|Abstract »|Full Text »|PDF »
From the Cover: Differences in vertebrate microRNA expression.
B. Ason, D. K. Darnell, B. Wittbrodt, E. Berezikov, W. P. Kloosterman, J. Wittbrodt, P. B. Antin, and R. H. A. Plasterk (2006)
PNAS
103, 14385-14389
|Abstract »|Full Text »|PDF »
A microRNA detection system based on padlock probes and rolling circle amplification.
H. K. Kim, Y. S. Lee, U. Sivaprasad, A. Malhotra, and A. Dutta (2006)
J. Cell Biol.
174, 677-687
|Abstract »|Full Text »|PDF »
Extensive post-transcriptional regulation of microRNAs and its implications for cancer.
J. M. Thomson, M. Newman, J. S. Parker, E. M. Morin-Kensicki, T. Wright, and S. M. Hammond (2006)
Genes & Dev.
20, 2202-2207
|Abstract »|Full Text »|PDF »
Improved In Situ Hybridization Efficiency with Locked-Nucleic-Acid-Incorporated DNA Probes.
K. Kubota, A. Ohashi, H. Imachi, and H. Harada (2006)
Appl. Envir. Microbiol.
72, 5311-5317
|Abstract »|Full Text »|PDF »
Myogenic factors that regulate expression of muscle-specific microRNAs.
P. K. Rao, R. M. Kumar, M. Farkhondeh, S. Baskerville, and H. F. Lodish (2006)
PNAS
103, 8721-8726
|Abstract »|Full Text »|PDF »
Post-transcriptional small RNA pathways in plants: mechanisms and regulations..
RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain.
P. T. NELSON, D. A. BALDWIN, W. P. KLOOSTERMAN, S. KAUPPINEN, R. H.A. PLASTERK, and Z. MOURELATOS (2006)
RNA
12, 187-191
|Abstract »|Full Text »|PDF »
Rapid Alteration of MicroRNA Levels by Histone Deacetylase Inhibition.
G. K. Scott, M. D. Mattie, C. E. Berger, S. C. Benz, and C. C. Benz (2006)
Cancer Res.
66, 1277-1281
|Abstract »|Full Text »|PDF »
MicroRNA Function and Mechanism: Insights from Zebra Fish.
A.F. SCHIER and A.J. GIRALDEZ (2006)
Cold Spring Harb Symp Quant Biol
71, 195-203
|Abstract »|PDF »
The expression profile of microRNAs in mouse embryos..
J. Mineno, S. Okamoto, T. Ando, M. Sato, H. Chono, H. Izu, M. Takayama, K. Asada, O. Mirochnitchenko, M. Inouye, et al. (2006)
Nucleic Acids Res.
34, 1765-1771
|Abstract »|Full Text »|PDF »
Cloning and expression of new microRNAs from zebrafish..
W. P. Kloosterman, F. A. Steiner, E. Berezikov, E. de Bruijn, J. van de Belt, M. Verheul, E. Cuppen, and R. H.A. Plasterk (2006)
Nucleic Acids Res.
34, 2558-2569
|Abstract »|Full Text »|PDF »
The Widespread Impact of Mammalian MicroRNAs on mRNA Repression and Evolution.
K. K.-H. Farh, A. Grimson, C. Jan, B. P. Lewis, W. K. Johnston, L. P. Lim, C. B. Burge, and D. P. Bartel (2005)
Science
310, 1817-1821
|Abstract »|Full Text »|PDF »
A novel C. elegans zinc finger transcription factor, lsy-2, required for the cell type-specific expression of the lsy-6 microRNA.