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E proteins sharpen neurogenesis by modulating proneural bHLH transcription factors activity in an E-box-dependent manner

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Cite as: eLife 2018;7:e37267 doi: 10.7554/eLife.37267

Abstract

Class II HLH proteins heterodimerize with class I HLH/E proteins to regulate transcription. Here we show that E proteins sharpen neurogenesis by adjusting the neurogenic strength of the distinct proneural proteins. We find that inhibiting BMP signaling or its target ID2 in the chick embryo spinal cord, impairs the neuronal production from progenitors expressing ATOH1/ASCL1, but less severely that from progenitors expressing NEUROG1/2/PTF1a. We show this context-dependent response to result from the differential modulation of proneural proteins' activity by E proteins. E proteins synergize with proneural proteins when acting on CAGSTG motifs, thereby facilitating the activity of ASCL1/ATOH1 which preferentially bind to such motifs. Conversely, E proteins restrict the neurogenic strength of NEUROG1/2 by directly inhibiting their preferential binding to CADATG motifs. Since we find this mechanism to be conserved in corticogenesis, we propose this differential co-operation of E proteins with proneural proteins as a novel though general feature of their mechanism of action.

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Author details

  1. Gwenvael Le Dréau

    Department of Developmental Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    For correspondence
    gldbmc@ibmb.csic.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-6877-3670
  2. René Escalona

    Department of Developmental Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Raquel Fueyo

    Department of Molecular Genomics, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0001-7106-7163
  4. Antonio Herrera

    Department of Cell Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Juan D Martínez

    Department of Developmental Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Susana Usieto

    Department of Developmental Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Anghara Menendez

    Department of Cell Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Sebastian Pons

    Department of Cell Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Marian A Martinez-Balbas

    Department of Molecular Genomics, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  10. Elisa Marti

    Department of Developmental Biology, Instituto de Biología Molecular de Barcelona, CSIC, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0001-5839-7133

Funding

MINECO (BFU2016-81887-REDT)

  • Elisa Marti

MINECO (BFU2016-77498-P)

  • Elisa Marti

AECC (AIO2014)

  • Gwenvael Le Dréau

CONACYT

  • René Escalona

MECD (#FPU13/01384)

  • Raquel Fueyo

MINECO (#FJCI-2015-26175)

  • Antonio Herrera

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

Reviewing Editor

  1. Jeremy Nathans, Reviewing Editor, Johns Hopkins University School of Medicine, United States

Publication history

  1. Received: April 5, 2018
  2. Accepted: August 9, 2018
  3. Accepted Manuscript published: August 10, 2018 (version 1)

Copyright

© 2018, Le Dréau 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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