1. Developmental Biology
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TALE factors use two distinct functional modes to control an essential zebrafish gene expression program

  1. Franck Ladam
  2. William Stanney
  3. Ian J Donaldson
  4. Ozge Yildiz
  5. Nicoletta Bobola
  6. Charles G Sagerström  Is a corresponding author
  1. University of Massachusetts Medical School, United States
  2. University of Manchester, United Kingdom
Research Article
  • Cited 16
  • Views 1,249
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Cite this article as: eLife 2018;7:e36144 doi: 10.7554/eLife.36144

Abstract

TALE factors are broadly expressed embryonically and known to function in complexes with transcription factors (TFs) like Hox proteins at gastrula/segmentation stages, but it is unclear if such generally expressed factors act by the same mechanism throughout embryogenesis. We identify a TALE-dependent gene regulatory network (GRN) required for anterior development and detect TALE occupancy associated with this GRN throughout embryogenesis. At blastula stages, we uncover a novel functional mode for TALE factors, where they occupy genomic DECA motifs with nearby NF-Y sites. We demonstrate that TALE and NF-Y form complexes and regulate chromatin state at genes of this GRN. At segmentation stages, GRN-associated TALE occupancy expands to include HEXA motifs near PBX:HOX sites. Hence, TALE factors control a key GRN, but utilize distinct DNA motifs and protein partners at different stages - a strategy that may also explain their oncogenic potential and may be employed by other broadly expressed TFs.

Data availability

RNA-seq data has been deposited in GEO under accession code GSE102662ChIP-seq data has been deposited in ArrayExpress under accession code E-MTAB-5967

The following data sets were generated
    1. Ladam F
    2. Sagerstrom CG
    (2018) Zebrafish TALE KD RNA-seq
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE102662).
The following previously published data sets were used
    1. Hans-Jörg Warnatz
    (2015) Prep1 (ChIP-Seq)
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1545025).
    1. Ozren Bogdanovic
    (2012) H3K4me1_dome, danRer7
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM915193).
    1. Ozren Bogdanovic
    (2012) H3K4me3_dome, danRer7
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM915189).
    1. Ozren Bogdanovic
    (2012) H3K27ac_dome, danRer7
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM915197.
    1. Ozren Bogdanovic
    (2012) H3K27ac_80%epi, danRer7
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM915198).
    1. Ozren Bogdanovic
    (2012) H3K27ac_24hpf, danRer7
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM915199).
    1. Yong Zhang
    (2013) H3K27me3 ChIP-seq dome
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1081557).
    1. Yong Zhang
    (2013) nucleosome dome rep 1
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1081554).
    1. Yong Zhang
    (2013) Pol II ChIP-seq dome 8WG16
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1081560).
    1. Hyung Joo Lee
    (2015) MeDIP_4.5hpf
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1274386).
    1. Raja Jothi
    (2014) ChIP-Seq NF-YA
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1370111).
    1. ENCODE DCC
    (2012) LICR_ChipSeq_ES-E14_H3K4me1_E0
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1000121).
    1. ENCODE DCC
    (2012) LICR_ChipSeq_ES-E14_H3K4me3_E0
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1000124).
    1. ENCODE DCC
    (2012) LICR_ChipSeq_ES-E14_H3K27ac_E0
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1000126).
    1. ENCODE DCC
    (2012) LICR_ChipSeq_ES-Bruce4_H3K27me3_E
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1000089).
    1. ENCODE DCC
    (2012) UW_DnaseSeq_ES-E14_E0_129/Ola
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1014154).
    1. Chieh-Chun Chen
    (2014) E14 MeDIP-seq
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM859494).
    1. Hans-Jörg Warnatz
    (2015) Input_DNA (ChIP-Seq control)
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSM1545026).

Article and author information

Author details

  1. Franck Ladam

    Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. William Stanney

    Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Ian J Donaldson

    Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Ozge Yildiz

    Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Nicoletta Bobola

    Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7103-4932
  6. Charles G Sagerström

    Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, United States
    For correspondence
    Charles.Sagerstrom@umassmed.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1509-5810

Funding

National Institute of Neurological Disorders and Stroke (NS38183)

  • Charles G Sagerström

Biotechnology and Biological Sciences Research Council (BB/N00907X/1)

  • Nicoletta Bobola

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was submitted to and approved by the University of Massachusetts Medical School Institutional Animal Care and Use Committee (protocol A-1565) and the University of Massachusetts Medical School Institutional Review Board (protocol I-149).

Reviewing Editor

  1. Marianne Bronner, California Institute of Technology, United States

Publication history

  1. Received: February 22, 2018
  2. Accepted: June 8, 2018
  3. Accepted Manuscript published: June 18, 2018 (version 1)
  4. Version of Record published: June 28, 2018 (version 2)

Copyright

© 2018, Ladam et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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