Transcriptome Analysis of Zebrafish Embryogenesis Using Microarrays

Zebrafish (Danio rerio) is a well-recognized model for the study of vertebrate developmental genetics, yet at the same time little is known about the transcriptional events that underlie zebrafish embryogenesis. Here we have employed microarray analysis to study the temporal activity of developmentally regulated genes during zebrafish embryogenesis. Transcriptome analysis at 12 different embryonic time points covering five different developmental stages (maternal, blastula, gastrula, segmentation, and pharyngula) revealed a highly dynamic transcriptional profile. Hierarchical clustering, stage-specific clustering, and algorithms to detect onset and peak of gene expression revealed clearly demarcated transcript clusters with maximum gene activity at distinct developmental stages as well as co-regulated expression of gene groups involved in dedicated functions such as organogenesis. Our study also revealed a previously unidentified cohort of genes that are transcribed prior to the mid-blastula transition, a time point earlier than when the zygotic genome was traditionally thought to become active. Here we provide, for the first time to our knowledge, a comprehensive list of developmentally regulated zebrafish genes and their expression profiles during embryogenesis, including novel information on the temporal expression of several thousand previously uncharacterized genes. The expression data generated from this study are accessible to all interested scientists from our institute resource database (http://giscompute.gis.a-star.edu.sg/~govind/zebrafish/data_download.html).

[1]  E. Linney,et al.  Microarray gene expression profiling during the segmentation phase of zebrafish development. , 2004, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[2]  D. Wagner,et al.  Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. , 2004, Developmental cell.

[3]  D. Wagner,et al.  Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. , 2004, Developmental cell.

[4]  A. Sharov,et al.  Dynamics of global gene expression changes during mouse preimplantation development. , 2004, Developmental cell.

[5]  Ronald W Davis,et al.  A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. , 2004, Developmental cell.

[6]  Lester F. Lau,et al.  Silencing of RNA Helicase II/Guα Inhibits Mammalian Ribosomal RNA Production* , 2003, Journal of Biological Chemistry.

[7]  M. Yamashita Apoptosis in zebrafish development. , 2003, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[8]  B. Valdez,et al.  Down-regulation of RNA Helicase II/Gu Results in the Depletion of 18 and 28 S rRNAs in Xenopus Oocyte* , 2003, Journal of Biological Chemistry.

[9]  Kevin P White,et al.  Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. , 2003, Developmental cell.

[10]  Wael Tadros,et al.  Regulation of maternal transcript destabilization during egg activation in Drosophila. , 2003, Genetics.

[11]  N. Sato,et al.  Survivin acts as an antiapoptotic factor during the development of mouse preimplantation embryos. , 2003, Developmental biology.

[12]  Weiping Ma,et al.  Embryogenesis Microarray for Profiling Gene Expression Patterns during 15,000 Unique Zebrafish Est Clusters and Their Future Use in Material Supplemental , 2022 .

[13]  E Terry Papoutsakis,et al.  A segmental nearest neighbor normalization and gene identification method gives superior results for DNA-array analysis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  L. Lau,et al.  Silencing of RNA helicase II/Gualpha inhibits mammalian ribosomal RNA production. , 2003, The Journal of biological chemistry.

[15]  Cheol‐Hee Kim,et al.  Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. , 2003, Developmental cell.

[16]  M. Ashburner,et al.  Systematic determination of patterns of gene expression during Drosophila embryogenesis , 2002, Genome Biology.

[17]  P. S. Klein,et al.  β-Catenin/Tcf-regulated transcription prior to the midblastula transition , 2002, Development.

[18]  A. Sandler,et al.  Survivin mRNA is down‐regulated during early Xenopus laevis embryogenesis , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[19]  B. Fritz,et al.  Zygotic control of maternal cyclin A1 translation and mRNA stability , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[20]  L. Ramakrishnan,et al.  Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. , 2002, Immunity.

[21]  Philip M. Long,et al.  Optimal gene expression analysis by microarrays. , 2002, Cancer cell.

[22]  B. S. Baker,et al.  Gene Expression During the Life Cycle of Drosophila melanogaster , 2002, Science.

[23]  V. Dzau,et al.  Construction of a zebrafish cDNA microarray: gene expression profiling of the zebrafish during development. , 2002, Biochemical and biophysical research communications.

[24]  C. Voolstra,et al.  Comparative analysis of somitogenesis related genes of the hairy/Enhancer of split class in Fugu and zebrafish , 2002, BMC Genomics.

[25]  T. Kornberg,et al.  Expression profiling of Drosophila imaginal discs , 2002, Genome biology.

[26]  Z. Gong,et al.  Expressed sequence tag analysis of expression profiles of zebrafish testis and ovary. , 2002, Gene.

[27]  Zhanjiang Liu,et al.  Translational machinery of channel catfish: I. A transcriptomic approach to the analysis of 32 40S ribosomal protein genes and their expression. , 2002, Gene.

[28]  Nancy Hopkins,et al.  Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development , 2002, Nature Genetics.

[29]  Hiroaki Tateno,et al.  Tissue-specific Expression of Rhamnose-binding Lectins in the Steelhead Trout (Oncorhynchus mykiss) , 2002, Bioscience, biotechnology, and biochemistry.

[30]  Mark C. Fishman,et al.  Zebrafish--the Canonical Vertebrate , 2001, Science.

[31]  D. Tautz,et al.  Homologues of c-hairy1 (her9) and lunatic fringe in zebrafish are expressed in the developing central nervous system, but not in the presomitic mesoderm , 2001, Development Genes and Evolution.

[32]  K. White,et al.  Patterns of Gene Expression During Drosophila Mesoderm Development , 2001, Science.

[33]  Jin Hyuk KIm,et al.  A novel method using edge detection for signal extraction from cDNA microarray image analysis , 2001, Experimental & Molecular Medicine.

[34]  V. Korzh,et al.  Developmental analysis of ceruloplasmin gene and liver formation in zebrafish , 2001, Mechanisms of Development.

[35]  R. Tibshirani,et al.  Significance analysis of microarrays applied to the ionizing radiation response , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Y. Audic,et al.  Zygotic Regulation of Maternal Cyclin A1 and B2 mRNAs , 2001, Molecular and Cellular Biology.

[37]  T. Kondo,et al.  Dispersion of cyclin B mRNA aggregation is coupled with translational activation of the mRNA during zebrafish oocyte maturation. , 2001, Developmental biology.

[38]  T. Ogawa,et al.  A Novel Rhamnose-binding Lectin Family from Eggs of Steelhead Trout (Oncorhynchus mykiss) with Different Structures and Tissue Distribution , 2001, Bioscience, biotechnology, and biochemistry.

[39]  M. Fishman Genomics. Zebrafish--the canonical vertebrate. , 2001, Science.

[40]  Jiann-Ruey Hong,et al.  Cloning and characterization of a novel nuclear Bcl-2 family protein, zfMcl-1a, in zebrafish embryo. , 2000, Biochemical and biophysical research communications.

[41]  M. Fishman,et al.  Identification, characterization, and mapping of expressed sequence tags from an embryonic zebrafish heart cDNA library. , 2000, Genome research.

[42]  Z. Gong,et al.  Asynchronous activation of 10 muscle‐specific protein (MSP) genes during zebrafish somitogenesis , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[43]  S. Ekker,et al.  Effective targeted gene ‘knockdown’ in zebrafish , 2000, Nature Genetics.

[44]  A. Haas,et al.  Ubiquitination and Degradation of the Zebrafish Paired‐Like Homeobox Protein Vsx‐1 , 2000, Journal of neurochemistry.

[45]  L. Zon,et al.  Zebrafish: a model system for the study of human disease. , 2000, Current opinion in genetics & development.

[46]  R. Shemer,et al.  Isolation and characterization of medaka ribosomal protein S3a (fte-1) cDNA and gene. , 2000, Gene.

[47]  Scott A. Rifkin,et al.  Microarray analysis of Drosophila development during metamorphosis. , 1999, Science.

[48]  A. Amsterdam,et al.  A large-scale insertional mutagenesis screen in zebrafish. , 1999, Genes & development.

[49]  E. Davidson,et al.  A view from the genome: spatial control of transcription in sea urchin development. , 1999, Current opinion in genetics & development.

[50]  H. Wang,et al.  Characterization of two zebrafish cDNA clones encoding egg envelope proteins ZP2 and ZP3. , 1999, Biochimica et biophysica acta.

[51]  T. Yager,et al.  Developmental activation of the capability to undergo checkpoint-induced apoptosis in the early zebrafish embryo. , 1999, Developmental biology.

[52]  M. Kloc,et al.  Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster , 1999, The EMBO journal.

[53]  J. B. Rattner,et al.  Mapping and characterization of the functional domains of the nucleolar protein RNA helicase II/Gu. , 1999, Experimental cell research.

[54]  L. Zon,et al.  Zebrafish: a new model for human disease. , 1999, Genome research.

[55]  P. Brown,et al.  DNA arrays for analysis of gene expression. , 1999, Methods in enzymology.

[56]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Y L Wang,et al.  Zebrafish hox clusters and vertebrate genome evolution. , 1998, Science.

[58]  K. Manova,et al.  RNA helicase A is essential for normal gastrulation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Z. Gong,et al.  Rapid identification and isolation of zebrafish cDNA clones. , 1997, Gene.

[60]  P. Brown,et al.  Exploring the metabolic and genetic control of gene expression on a genomic scale. , 1997, Science.

[61]  M. Farrell,et al.  GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene. , 1997, Development.

[62]  C. Pickart,et al.  Structure and function of ubiquitin conjugating enzyme E2-25K: the tail is a core-dependent activity element. , 1997, Biochemistry.

[63]  P. Brown,et al.  Parallel human genome analysis: microarray-based expression monitoring of 1000 genes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[64]  B. Edgar,et al.  Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program. , 1996, Genes & development.

[65]  A. Amsterdam,et al.  Highly efficient germ-line transmission of proviral insertions in zebrafish. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[66]  J. Campos-Ortega,et al.  Expression domains of a zebrafish homologue of the Drosophila pair-rule gene hairy correspond to primordia of alternating somites. , 1996, Development.

[67]  B. Geiger,et al.  Zebrafish cyclin E regulation during early embryogenesis , 1996, Developmental dynamics : an official publication of the American Association of Anatomists.

[68]  M. Kirschner,et al.  Identification of a novel ubiquitin-conjugating enzyme involved in mitotic cyclin degradation , 1996, Current Biology.

[69]  B. Geiger,et al.  Zebrafish cyclin D1 is differentially expressed during early embryogenesis. , 1995, Biochimica et biophysica acta.

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

[71]  C. Kimmel,et al.  The zebrafish midblastula transition. , 1993, Development.

[72]  E. Oxtoby,et al.  Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. , 1993, Nucleic acids research.

[73]  P. Kingsley,et al.  Tissue-restricted accumulation of a ribosomal protein mRNA is not coordinated with rRNA transcription and precedes growth of the sea urchin pluteus larva. , 1992, Developmental biology.

[74]  P. O’Farrell,et al.  The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string , 1990, Cell.

[75]  I. Bozzoni,et al.  Expression of ribosomal protein genes and regulation of ribosome biosynthesis in Xenopus development. , 1989, Trends in biochemical sciences.

[76]  I. Bozzoni,et al.  Expression of ribosomal-protein genes in Xenopus laevis development , 1982, Cell.

[77]  N. Rott,et al.  Changes in the rate of cell divisions in the course of early development of diploid and haploid loach embryos. , 1968, Journal of embryology and experimental morphology.