The developmental miRNA profiles of zebrafish as determined by small RNA cloning.

MicroRNAs (miRNAs) represent a family of small, regulatory, noncoding RNAs that are found in plants and animals. Here, we describe the miRNA profile of the zebrafish Danio rerio resolved in a developmental and cell-type-specific manner. The profiles were obtained from larger-scale sequencing of small RNA libraries prepared from developmentally staged zebrafish, and two adult fibroblast cell lines derived from the caudal fin (ZFL) and the liver epithelium (SJD). We identified a total of 154 distinct miRNAs expressed from 343 miRNA genes. Other experimental/computational sources support an additional 10 miRNAs encoded by 19 genes. The miRNAs can be classified into 87 distinct families. Cross-species comparison indicates that 81 families are conserved in mammals, 17 of which also have at least one member conserved in an invertebrate. Our analysis reveals that the zygotes are essentially devoid of miRNAs and that their expression begins during the blastula period with a zebrafish-specific family of miRNAs encoded by closely spaced multicopy genes. Computational predictions of zebrafish miRNA targets are provided that take into account the depth of evolutionary conservation. Besides miRNAs, we identified a prominent class of repeat-associated small interfering RNAs (rasiRNAs).

[1]  G. Rubin,et al.  Computational identification of Drosophila microRNA genes , 2003, Genome Biology.

[2]  E. Birney,et al.  EnsMart: a generic system for fast and flexible access to biological data. , 2003, Genome research.

[3]  A. Bradley,et al.  Identification of mammalian microRNA host genes and transcription units. , 2004, Genome research.

[4]  D. Marks,et al.  The small RNA profile during Drosophila melanogaster development. , 2003, Developmental cell.

[5]  Anton J. Enright,et al.  Human MicroRNA Targets , 2004, PLoS biology.

[6]  V. Ambros,et al.  An Extensive Class of Small RNAs in Caenorhabditis elegans , 2001, Science.

[7]  S. Moon,et al.  Human embryonic stem cells express a unique set of microRNAs. , 2004, Developmental biology.

[8]  T. Tuschl,et al.  Cloning of Small RNA Molecules , 2003, Current protocols in molecular biology.

[9]  C. Burge,et al.  Prediction of Mammalian MicroRNA Targets , 2003, Cell.

[10]  T. Tuschl,et al.  Identification of Novel Genes Coding for Small Expressed RNAs , 2001, Science.

[11]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[12]  O. Hobert Common logic of transcription factor and microRNA action. , 2004, Trends in biochemical sciences.

[13]  P. Sharp,et al.  Embryonic stem cell-specific MicroRNAs. , 2003, Developmental cell.

[14]  T. Tuschl,et al.  Identification of Tissue-Specific MicroRNAs from Mouse , 2002, Current Biology.

[15]  Konstantin Khrapko,et al.  A microRNA array reveals extensive regulation of microRNAs during brain development. , 2003, RNA.

[16]  C. Burge,et al.  Conserved Seed Pairing, Often Flanked by Adenosines, Indicates that Thousands of Human Genes are MicroRNA Targets , 2005, Cell.

[17]  C. Lima,et al.  Structure and mechanism of RNA ligase. , 2004, Structure.

[18]  S. Elledge,et al.  Dicer is essential for mouse development , 2003, Nature Genetics.

[19]  T. Tuschl,et al.  Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. , 2004, Molecular cell.

[20]  Daniel Gautheret,et al.  Profile-based detection of microRNA precursors in animal genomes , 2005, Bioinform..

[21]  C. Burge,et al.  The microRNAs of Caenorhabditis elegans. , 2003, Genes & development.

[22]  A. Schier Nodal signaling in vertebrate development. , 2003, Annual review of cell and developmental biology.

[23]  T. Oda,et al.  Inhibition of Jagged-mediated Notch signaling disrupts zebrafish biliary development and generates multi-organ defects compatible with an Alagille syndrome phenocopy , 2004, Development.

[24]  D. Bartel,et al.  Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs , 2004, Nature Reviews Genetics.

[25]  Toru Suzuki,et al.  Stage‐specific expression of microRNAs during Xenopus development , 2005, FEBS letters.

[26]  Michael Zuker,et al.  MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression , 2004, Nature Genetics.

[27]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[28]  V. Ambros The functions of animal microRNAs , 2004, Nature.

[29]  V. Ambros,et al.  Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-Complex gene activity. , 2003, Developmental biology.

[30]  V. Ambros,et al.  MicroRNAs and Other Tiny Endogenous RNAs in C. elegans , 2003, Current Biology.

[31]  Anton J. Enright,et al.  Identification of Virus-Encoded MicroRNAs , 2004, Science.

[32]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[33]  Anton J. Enright,et al.  Materials and Methods Figs. S1 to S4 Tables S1 to S5 References and Notes Micrornas Regulate Brain Morphogenesis in Zebrafish , 2022 .

[34]  Edwin Cuppen,et al.  The microRNA-producing enzyme Dicer1 is essential for zebrafish development , 2003, Nature Genetics.

[35]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[36]  C. Burge,et al.  Vertebrate MicroRNA Genes , 2003, Science.

[37]  R. Martienssen,et al.  The role of RNA interference in heterochromatic silencing , 2004, Nature.

[38]  K. Gunsalus,et al.  Combinatorial microRNA target predictions , 2005, Nature Genetics.

[39]  Damian Smedley,et al.  Ensembl 2004 , 2004, Nucleic Acids Res..

[40]  Nikolaus Rajewsky,et al.  Computational identification of microRNA targets , 2004, Genome Biology.

[41]  L. Lim,et al.  An Abundant Class of Tiny RNAs with Probable Regulatory Roles in Caenorhabditis elegans , 2001, Science.

[42]  Lin He,et al.  MicroRNAs: small RNAs with a big role in gene regulation , 2004, Nature reviews genetics.

[43]  J. Eisen,et al.  Headwaters of the zebrafish — emergence of a new model vertebrate , 2002, Nature Reviews Genetics.