Cohesin facilitates zygotic genome activation in zebrafish

At zygotic genome activation (ZGA), changes in chromatin structure are associated with new transcription immediately following the maternal-to-zygotic transition (MZT). The nuclear architectural proteins cohesin and CCCTC-binding factor (CTCF) contribute to chromatin structure and gene regulation. We show here that normal cohesin function is important for ZGA in zebrafish. Depletion of the cohesin subunit Rad21 delays ZGA without affecting cell cycle progression. In contrast, CTCF depletion has little effect on ZGA, whereas complete abrogation is lethal. Genome-wide analysis of Rad21 binding reveals a change in distribution from pericentromeric satellite DNA and other locations, including the miR-430 locus (the products of which are responsible for maternal transcript degradation), to genes, as embryos progress through the MZT. After MZT, a subset of Rad21 binding overlaps the pioneer factor Pou5f3, which activates early expressed genes. Rad21 depletion disrupts the formation of nucleoli and RNA polymerase II foci, suggestive of global defects in chromosome architecture. We propose that Rad21/cohesin redistribution to active areas of the genome is key to the establishment of chromosome organization and the embryonic developmental program. Summary: Cohesin contributes to dynamic changes in chromosome architecture that occur upon zygotic genome activation, raising the possibility that germline cohesinopathy mutations could lead to global alteration of the zygotic transcription program early in development.

[1]  Michael Rabiger,et al.  From Transcript to Assembly , 2020 .

[2]  J. Shepherd,et al.  Cycle. , 2020, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[3]  David A. Nix,et al.  Conserved roles of mouse DUX and human DUX4 in activating cleavage-stage genes and MERVL/HERVL retrotransposons , 2017 .

[4]  A. Koren,et al.  DNA replication timing during development anticipates transcriptional programs and parallels enhancer activation , 2017, Genome research.

[5]  L. Mirny,et al.  Targeted Degradation of CTCF Decouples Local Insulation of Chromosome Domains from Genomic Compartmentalization , 2017, Cell.

[6]  S. Tapscott,et al.  Conserved roles for murine DUX and human DUX4 in activating cleavage stage genes and MERVL/HERVL retrotransposons , 2017, Nature Genetics.

[7]  A. Shevchenko,et al.  Competition between histone and transcription factor binding regulates the onset of transcription in zebrafish embryos , 2017, bioRxiv.

[8]  D. Trono,et al.  A family of double-homeodomain transcription factors regulates zygotic genome activation in placental mammals , 2017, Nature Genetics.

[9]  Peter H. L. Krijger,et al.  Can We Just Say: Transcription Second? , 2017, Cell.

[10]  Juan M. Vaquerizas,et al.  Chromatin Architecture Emerges during Zygotic Genome Activation Independent of Transcription , 2017, Cell.

[11]  M. Gerstein,et al.  Dynamic RNA–protein interactions underlie the zebrafish maternal-to-zygotic transition , 2017, Genome research.

[12]  M. Pálfy,et al.  The timing of zygotic genome activation. , 2017, Current opinion in genetics & development.

[13]  Stephen J. Tapscott,et al.  Conservation and innovation in the DUX4-family gene network , 2017, Nature Genetics.

[14]  Ilya M. Flyamer,et al.  Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition , 2017, Nature.

[15]  Chuan He,et al.  m6A-dependent maternal mRNA clearance facilitates zebrafish maternal-to-zygotic transition , 2016, Nature.

[16]  Antonio Marco,et al.  Clearance of Maternal RNAs: Not a Mummy's Embryo Anymore. , 2017, Methods in molecular biology.

[17]  R. Ciosk,et al.  Cell Fate Maintenance and Reprogramming During the Oocyte-to-Embryo Transition. , 2017, Results and problems in cell differentiation.

[18]  M. Lampson,et al.  Cell Cycle Remodeling and Zygotic Gene Activation at the Midblastula Transition. , 2017, Advances in experimental medicine and biology.

[19]  E. Nora,et al.  CTCF and Cohesin in Genome Folding and Transcriptional Gene Regulation. , 2016, Annual review of genomics and human genetics.

[20]  Keji Zhao,et al.  Establishing Chromatin Regulatory Landscape during Mouse Preimplantation Development , 2016, Cell.

[21]  Fidel Ramírez,et al.  deepTools2: a next generation web server for deep-sequencing data analysis , 2016, Nucleic Acids Res..

[22]  M. Torres-Padilla,et al.  Building up the nucleus: nuclear organization in the establishment of totipotency and pluripotency during mammalian development , 2016, Genes & development.

[23]  W. Driever,et al.  Zygotic Genome Activators, Developmental Timing, and Pluripotency. , 2016, Current topics in developmental biology.

[24]  J. Gerton,et al.  Improved transcription and translation with L-leucine stimulation of mTORC1 in Roberts syndrome , 2016, BMC Genomics.

[25]  S. V. van Heeringen,et al.  Embryonic transcription is controlled by maternally defined chromatin state , 2015, Nature Communications.

[26]  J. Horsfield,et al.  A neural crest origin for cohesinopathy heart defects. , 2015, Human molecular genetics.

[27]  S. Hadjur,et al.  Genetic Tailors: CTCF and Cohesin Shape the Genome During Evolution. , 2015, Trends in genetics : TIG.

[28]  Eric F. Wieschaus,et al.  Zygotic Genome Activation Triggers the DNA Replication Checkpoint at the Midblastula Transition , 2015, Cell.

[29]  Pedro P. Rocha,et al.  CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation , 2015, Science.

[30]  D. Odom,et al.  Comparative Hi-C Reveals that CTCF Underlies Evolution of Chromosomal Domain Architecture , 2015, Cell reports.

[31]  A. Straight,et al.  Histone titration against the genome sets the DNA-to-cytoplasm threshold for the Xenopus midblastula transition , 2015, Proceedings of the National Academy of Sciences.

[32]  D. Levy,et al.  Nuclear Size Scaling during Xenopus Early Development Contributes to Midblastula Transition Timing , 2015, Current Biology.

[33]  Howard Y. Chang,et al.  ATAC‐seq: A Method for Assaying Chromatin Accessibility Genome‐Wide , 2015, Current protocols in molecular biology.

[34]  M. Cárdenas,et al.  l-leucine partially rescues translational and developmental defects associated with zebrafish models of Cornelia de Lange syndrome , 2014, Human molecular genetics.

[35]  V. Franke,et al.  Sculpting the Transcriptome During the Oocyte-to-Embryo Transition in Mouse. , 2015, Current topics in developmental biology.

[36]  M. Lampson,et al.  Regulation of zygotic genome activation and DNA damage checkpoint acquisition at the mid-blastula transition , 2014, Cell cycle.

[37]  Zhaohui S. Qin,et al.  Insulator function and topological domain border strength scale with architectural protein occupancy , 2014, Genome Biology.

[38]  Melissa M. Harrison,et al.  Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition , 2014, bioRxiv.

[39]  Jennifer E. Phillips-Cremins.  Unraveling architecture of the pluripotent genome. , 2014, Current opinion in cell biology.

[40]  J. Dekker,et al.  Predictive Polymer Modeling Reveals Coupled Fluctuations in Chromosome Conformation and Transcription , 2014, Cell.

[41]  K. Yokomori,et al.  Mechanisms of cohesin-mediated gene regulation and lessons learned from cohesinopathies. , 2014, Biochimica et biophysica acta.

[42]  Yong Zhang,et al.  Canonical nucleosome organization at promoters forms during genome activation , 2014, Genome research.

[43]  Brian D. Slaughter,et al.  Cohesion promotes nucleolar structure and function , 2014, Molecular biology of the cell.

[44]  Alex T. Kalinka,et al.  The earliest transcribed zygotic genes are short, newly evolved, and different across species. , 2014, Cell reports.

[45]  M. Blanchette,et al.  Hox in motion: tracking HoxA cluster conformation during differentiation , 2013, Nucleic acids research.

[46]  Judith Marsman,et al.  Cohesin and CTCF differentially regulate spatiotemporal runx1 expression during zebrafish development. , 2014, Biochimica et biophysica acta.

[47]  R. Skibbens,et al.  Cohesinopathies of a Feather Flock Together , 2013, PLoS genetics.

[48]  E. Barta,et al.  A novel method to predict regulatory regions based on histone mark landscapes in macrophages. , 2013, Immunobiology.

[49]  Miler T. Lee,et al.  Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition , 2013, Nature.

[50]  Yun Zhu,et al.  The pluripotent genome in three dimensions is shaped around pluripotency factors , 2013, Nature.

[51]  W. Driever,et al.  Pou5f1 Transcription Factor Controls Zygotic Gene Activation In Vertebrates , 2013, Science.

[52]  Thomas Whitington,et al.  Transcription Factor Binding in Human Cells Occurs in Dense Clusters Formed around Cohesin Anchor Sites , 2013, Cell.

[53]  B. Cairns,et al.  Reprogramming the Maternal Zebrafish Genome after Fertilization to Match the Paternal Methylation Pattern , 2013, Cell.

[54]  Jing Zhang,et al.  Sperm, but Not Oocyte, DNA Methylome Is Inherited by Zebrafish Early Embryos , 2013, Cell.

[55]  Anton J. Enright,et al.  The zebrafish reference genome sequence and its relationship to the human genome , 2013, Nature.

[56]  P. Collas,et al.  Epigenetic marking of the zebrafish developmental program. , 2013, Current topics in developmental biology.

[57]  Cole Trapnell,et al.  TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions , 2013, Genome Biology.

[58]  S. V. van Heeringen,et al.  Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis , 2012, Genome research.

[59]  J. Wong,et al.  Interaction of nucleolin with ribosomal RNA genes and its role in RNA polymerase I transcription , 2012, Nucleic acids research.

[60]  C. Print,et al.  Diverse Developmental Disorders from The One Ring: Distinct Molecular Pathways Underlie the Cohesinopathies , 2012, Front. Gene..

[61]  A. Schier,et al.  Bivalent histone modifications in early embryogenesis. , 2012, Current opinion in cell biology.

[62]  Brian D. Slaughter,et al.  Cohesin Proteins Promote Ribosomal RNA Production and Protein Translation in Yeast and Human Cells , 2012, PLoS genetics.

[63]  Guangchuang Yu,et al.  clusterProfiler: an R package for comparing biological themes among gene clusters. , 2012, Omics : a journal of integrative biology.

[64]  C. Disteche,et al.  Loss of Maternal CTCF Is Associated with Peri-Implantation Lethality of Ctcf Null Embryos , 2012, PloS one.

[65]  A. Giraldez,et al.  Ribosome Profiling Shows That miR-430 Reduces Translation Before Causing mRNA Decay in Zebrafish , 2012, Science.

[66]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[67]  R. Young,et al.  Nanog-like regulates endoderm formation through the Mxtx2-Nodal pathway. , 2012, Developmental cell.

[68]  Sinnakaruppan Mathavan,et al.  Prepatterning of developmental gene expression by modified histones before zygotic genome activation. , 2011, Developmental cell.

[69]  Michael B. Eisen,et al.  Zelda Binding in the Early Drosophila melanogaster Embryo Marks Regions Subsequently Activated at the Maternal-to-Zygotic Transition , 2011, PLoS genetics.

[70]  Joachim Wittbrodt,et al.  One for All—A Highly Efficient and Versatile Method for Fluorescent Immunostaining in Fish Embryos , 2011, PloS one.

[71]  Marcel Martin.  Cutadapt removes adapter sequences from high-throughput sequencing reads , 2011 .

[72]  Lucian Ilie,et al.  SHRiMP2: Sensitive yet Practical Short Read Mapping , 2011, Bioinform..

[73]  Patrick J. Biggs,et al.  SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data , 2010, BMC Bioinformatics.

[74]  Kathryn E. Crosier,et al.  Positive regulation of c-Myc by cohesin is direct, and evolutionarily conserved. , 2010, Developmental biology.

[75]  Mathieu Blanchette,et al.  The three-dimensional architecture of Hox cluster silencing , 2010, Nucleic acids research.

[76]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[77]  Cohesinopathies, gene expression, and chromatin organization , 2010, The Journal of cell biology.

[78]  Aviv Regev,et al.  Chromatin signature of embryonic pluripotency is established during genome activation , 2010, Nature.

[79]  Aaron R. Quinlan,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2022 .

[80]  R. Young,et al.  Connecting transcriptional control to chromosome structure and human disease. , 2010, Cold Spring Harbor symposia on quantitative biology.

[81]  P. Collas,et al.  Fish'n ChIPs: chromatin immunoprecipitation in the zebrafish embryo. , 2009, Methods in molecular biology.

[82]  Clifford A. Meyer,et al.  Model-based Analysis of ChIP-Seq (MACS) , 2008, Genome Biology.

[83]  S. Hannenhalli,et al.  Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development , 2008, Development.

[84]  Kathryn E. Crosier,et al.  Cohesin-dependent regulation of Runx genes , 2007, Development.

[85]  Anton J. Enright,et al.  Zebrafish MiR-430 Promotes Deadenylation and Clearance of Maternal mRNAs , 2006, Science.

[86]  Andrej Shevchenko,et al.  Proteomics of early zebrafish embryos , 2006, BMC Developmental Biology.

[87]  K. Nasmyth,et al.  The structure and function of SMC and kleisin complexes. , 2005, Annual review of biochemistry.

[88]  Nansheng Chen,et al.  Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences , 2009, Current protocols in bioinformatics.

[89]  M. DePamphilis,et al.  Regulation of Gene Expression at the Beginning of Mammalian Development (*) , 1995, The Journal of Biological Chemistry.

[90]  M. Westerfield.  The zebrafish book : a guide for the laboratory use of zebrafish (Danio rerio) , 1995 .

[91]  M. Kirschner,et al.  The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle , 1987, Cell.

[92]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage , 1982, Cell.

[93]  M. Kirschner,et al.  A major developmental transition in early xenopus embryos: II. control of the onset of transcription , 1982, Cell.