Multiomic atlas with functional stratification and developmental dynamics of zebrafish cis-regulatory elements

被引:54
作者
Baranasic, Damir [1 ,2 ]
Hortenhuber, Matthias [3 ]
Balwierz, Piotr J. [1 ,2 ,4 ]
Zehnder, Tobias [1 ,2 ,5 ]
Mukarram, Abdul Kadir [3 ]
Nepal, Chirag [6 ]
Varnai, Csilla [4 ,7 ]
Hadzhiev, Yavor [4 ]
Jimenez-Gonzalez, Ada [4 ]
Li, Nan [4 ]
Wragg, Joseph [4 ]
D'Orazio, Fabio M. [4 ]
Relic, Dorde [8 ,9 ]
Pachkov, Mikhail [8 ,9 ]
Diaz, Noelia [10 ,35 ]
Hernandez-Rodriguez, Benjamin [10 ]
Chen, Zelin [11 ,12 ,13 ]
Stoiber, Marcus [14 ]
Dong, Michael [3 ]
Stevens, Irene [3 ]
Ross, Samuel E. [15 ]
Eagle, Anne [16 ]
Martin, Ryan [16 ]
Obasaju, Oluwapelumi [4 ]
Rastegar, Sepand [17 ]
McGarvey, Alison C. [18 ]
Kopp, Wolfgang [18 ]
Chambers, Emily [19 ]
Wang, Dennis [19 ,20 ]
Kim, Hyejeong R. [21 ]
Acemel, Rafael D. [22 ,23 ]
Naranjo, Silvia [22 ]
Lapinski, Maciej [24 ]
Chong, Vanessa [25 ]
Mathavan, Sinnakaruppan [26 ]
Peers, Bernard [27 ]
Sauka-Spengler, Tatjana [25 ]
Vingron, Martin [5 ]
Carninci, Piero [28 ,36 ]
Ohler, Uwe [18 ,29 ]
Lacadie, Scott Allen
Burgess, Shawn M. [12 ]
Winata, Cecilia [24 ]
van Eeden, Freek [21 ]
Vaquerizas, Juan M. [1 ,2 ,10 ]
Luis Gomez-Skarmeta, Jose [22 ]
Onichtchouk, Daria [30 ,31 ]
Brown, Ben James [14 ]
Bogdanovic, Ozren [15 ,32 ]
van Nimwegen, Erik [8 ,9 ]
机构
[1] MRC London Inst Med Sci, London, England
[2] Imperial Coll London, Fac Med, Inst Clin Sci, Hammersmith Hosp Campus, London, England
[3] NEO, Dept Biosci & Nutr, Karolinska Inst, Huddinge, Sweden
[4] Univ Birmingham, Coll Med & Dent Sci, Birmingham Ctr Genome Biol, Inst Canc & Genom Sci, Birmingham, W Midlands, England
[5] Max Planck Inst Mol Genet, Dept Computat Mol Biol, Berlin, Germany
[6] Univ Copenhagen, Biotech Res & Innovat Ctr BRIC, Dept Hlth & Med Sci, Copenhagen, Denmark
[7] Univ Birmingham, Ctr Computat Biol, Birmingham, W Midlands, England
[8] Univ Basel, Biozentrum, Basel, Switzerland
[9] Swiss Inst Bioinformat, Basel, Switzerland
[10] Max Planck Inst Mol Biomed, Munster, Germany
[11] NHGRI, Translat & Funct Genom Branch, Bethesda, MD 20892 USA
[12] Southern Marine Sci & Engn Guangdong Lab, Guangzhou, Peoples R China
[13] Chinese Acad Sci, South China Sea Inst Oceanol, CAS Key Lab Trop Marine Bioresources & Ecol, Guangzhou, Peoples R China
[14] Lawrence Berkeley Natl Lab, Environm Genom & Syst Biol, Berkeley, CA USA
[15] Garvan Inst Med Res, Genom & Epigenet Div, Sydney, NSW, Australia
[16] Univ Oregon, Inst Neurosci, Eugene, OR 97403 USA
[17] Karlsruhe Inst Technol, Inst Biol & Chem Syst Biol Informat Proc IBCS BIP, Karlsruhe, Germany
[18] Helmholtz Assoc, Berlin Inst Med Syst Biol BIMSB, Max Delbruck Ctr Mol Med, Berlin, Germany
[19] Univ Sheffield, Sheffield Inst Translat Neurosci, Sheffield Bioinformat Core, Sheffield, S Yorkshire, England
[20] Singapore Inst Clin Sci, Singapore, Singapore
[21] Univ Sheffield, Bateson Ctr Biomed Sci, Sheffield, S Yorkshire, England
[22] Univ Pablo de Olavide Junta Andalucia, Ctr Andaluz Biol Desarrollo CABD, CSIC, Seville, Spain
[23] Max Delbruck Ctr Mol Med, Berlin Inst Med Syst Biol, Epigenet & Sex Dev Grp, Berlin, Germany
[24] Int Inst Mol & Cell Biol Warsaw, Warsaw, Poland
[25] Univ Oxford, MRC Weatherall Inst Mol Med, Radcliffe Dept Med, Oxford, England
[26] Sankara Nethralayas, Vis Res Fdn, Chennai, Tamil Nadu, India
[27] Univ Liege, Lab Zebrafish Dev & Dis Models ZDDM, GIGA R, SART TILMAN, Liege, Belgium
[28] RIKEN Ctr Integrat Med Sci, Lab Transcriptome Technol, Yokohama, Kanagawa, Japan
[29] Humboldt Univ, Inst Biol, Berlin, Germany
[30] Univ Freiburg, Signalling Res Ctr BIOSS, Dept Dev Biol, Freiburg, Germany
[31] Univ Freiburg, CIBSS, Freiburg, Germany
[32] Univ New South Wales, Sch Biotechnol & Biomol Sci, Sydney, NSW, Australia
[33] Kings Coll London, Randall Ctr Cell & Mol Biophys, Guys Campus, London, England
[34] Sci Life Lab, Solna, Sweden
[35] Inst Marine Sci, Barcelona, Spain
[36] Fdn Human Technopole, Milan, Italy
基金
英国惠康基金; 英国生物技术与生命科学研究理事会; 欧盟地平线“2020”; 英国医学研究理事会;
关键词
CHROMATIN-STATE DISCOVERY; GENE-EXPRESSION; INTEGRATIVE ANALYSIS; SUPER-ENHANCERS; DNA METHYLATION; CELL IDENTITY; TRANSCRIPTION; GENOME; INITIATION; SEQUENCE;
D O I
10.1038/s41588-022-01089-w
中图分类号
Q3 [遗传学];
学科分类号
071007 [遗传学];
摘要
Zebrafish, a popular organism for studying embryonic development and for modeling human diseases, has so far lacked a systematic functional annotation program akin to those in other animal models. To address this, we formed the international DANIO-CODE consortium and created a central repository to store and process zebrafish developmental functional genomic data. Our data coordination center (https://danio-code.zfin.org) combines a total of 1,802 sets of unpublished and re-analyzed published genomic data, which we used to improve existing annotations and show its utility in experimental design. We identified over 140,000 cis-regulatory elements throughout development, including classes with distinct features dependent on their activity in time and space. We delineated the distinct distance topology and chromatin features between regulatory elements active during zygotic genome activation and those active during organogenesis. Finally, we matched regulatory elements and epigenomic landscapes between zebrafish and mouse and predicted functional relationships between them beyond sequence similarity, thus extending the utility of zebrafish developmental genomics to mammals.
引用
收藏
页码:1037 / +
页数:37
相关论文
共 101 条
[1]
Anderson EL, 2008, P NATL ACAD SCI USA, V105, P14976, DOI [10.1073/pnas.0807297105, 10.1038/s41598-019-45839-z]
[2]
An atlas of active enhancers across human cell types and tissues [J].
Andersson, Robin ;
Gebhard, Claudia ;
Miguel-Escalada, Irene ;
Hoof, Ilka ;
Bornholdt, Jette ;
Boyd, Mette ;
Chen, Yun ;
Zhao, Xiaobei ;
Schmidl, Christian ;
Suzuki, Takahiro ;
Ntini, Evgenia ;
Arner, Erik ;
Valen, Eivind ;
Li, Kang ;
Schwarzfischer, Lucia ;
Glatz, Dagmar ;
Raithel, Johanna ;
Lilje, Berit ;
Rapin, Nicolas ;
Bagger, Frederik Otzen ;
Jorgensen, Mette ;
Andersen, Peter Refsing ;
Bertin, Nicolas ;
Rackham, Owen ;
Burroughs, A. Maxwell ;
Baillie, J. Kenneth ;
Ishizu, Yuri ;
Shimizu, Yuri ;
Furuhata, Erina ;
Maeda, Shiori ;
Negishi, Yutaka ;
Mungall, Christopher J. ;
Meehan, Terrence F. ;
Lassmann, Timo ;
Itoh, Masayoshi ;
Kawaji, Hideya ;
Kondo, Naoto ;
Kawai, Jun ;
Lennartsson, Andreas ;
Daub, Carsten O. ;
Heutink, Peter ;
Hume, David A. ;
Jensen, Torben Heick ;
Suzuki, Harukazu ;
Hayashizaki, Yoshihide ;
Mueller, Ferenc ;
Forrest, Alistair R. R. ;
Carninci, Piero ;
Rehli, Michael ;
Sandelin, Albin .
NATURE, 2014, 507 (7493) :455-+
[3]
MotEvo: integrated Bayesian probabilistic methods for inferring regulatory sites and motifs on multiple alignments of DNA sequences [J].
Arnold, Phil ;
Erb, Ionas ;
Pachkov, Mikhail ;
Molina, Nacho ;
van Nimwegen, Erik .
BIOINFORMATICS, 2012, 28 (04) :487-494
[4]
Zebrafish mutants and TEAD reporters reveal essential functions for Yap and Taz in posterior cardinal vein development [J].
Astone, Matteo ;
Lai, Jason Kuan Han ;
Dupont, Sirio ;
Stainier, Didier Y. R. ;
Argenton, Francesco ;
Vettori, Andrea .
SCIENTIFIC REPORTS, 2018, 8
[5]
ISMARA: automated modeling of genomic signals as a democracy of regulatory motifs [J].
Balwierz, Piotr J. ;
Pachkov, Mikhail ;
Arnold, Phil ;
Gruber, Andreas J. ;
Zavolan, Mihaela ;
van Nimwegen, Erik .
GENOME RESEARCH, 2014, 24 (05) :869-884
[6]
Methods for analyzing deep sequencing expression data: constructing the human and mouse promoterome with deepCAGE data [J].
Balwierz, Piotr J. ;
Carninci, Piero ;
Daub, Carsten O. ;
Kawai, Jun ;
Hayashizaki, Yoshihide ;
Van Belle, Werner ;
Beisel, Christian ;
van Nimwegen, Erik .
GENOME BIOLOGY, 2009, 10 (07)
[7]
Ribosome Profiling Shows That miR-430 Reduces Translation Before Causing mRNA Decay in Zebrafish [J].
Bazzini, Ariel A. ;
Lee, Miler T. ;
Giraldez, Antonio J. .
SCIENCE, 2012, 336 (6078) :233-237
[8]
Active DNA demethylation at enhancers during the vertebrate phylotypic period [J].
Bogdanovic, Ozren ;
Smits, Arne H. ;
de la Calle Mustienes, Elisa ;
Tena, Juan J. ;
Ford, Ethan ;
Williams, Ruth ;
Senanayake, Upeka ;
Schultz, Matthew D. ;
Hontelez, Saartje ;
van Kruijsbergen, Ila ;
Rayon, Teresa ;
Gnerlich, Felix ;
Carell, Thomas ;
Veenstra, Gert Jan C. ;
Manzanares, Miguel ;
Sauka-Spengler, Tatjana ;
Ecker, Joseph R. ;
Vermeulen, Michiel ;
Luis Gomez-Skarmeta, Jose ;
Lister, Ryan .
NATURE GENETICS, 2016, 48 (04) :417-+
[9]
Dynamics of enhancer chromatin signatures mark the transition from pluripotency to cell specification during embryogenesis [J].
Bogdanovic, Ozren ;
Fernandez-Minan, Ana ;
Tena, Juan J. ;
de la Calle-Mustienes, Elisa ;
Hidalgo, Carmen ;
van Kruysbergen, Ila ;
van Heeringen, Simon J. ;
Veenstra, Gert Jan C. ;
Luis Gomez-Skarmeta, Jose .
GENOME RESEARCH, 2012, 22 (10) :2043-2053
[10]
The dynamics of gene expression in vertebrate embryogenesis at single-cell resolution [J].
Briggs, James A. ;
Weinreb, Caleb ;
Wagner, Daniel E. ;
Megason, Sean ;
Peshkin, Leonid ;
Kirschner, Marc W. ;
Klein, Allon M. .
SCIENCE, 2018, 360 (6392) :980-+