1. Developmental Biology
  2. Neuroscience
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The Drosophila Sp8 transcription factor buttonhead prevents premature differentiation of intermediate neural progenitors

  1. Yonggang Xie
  2. Xiaosu Li
  3. Xian Zhang
  4. Shaolin Mei
  5. Hongyu Li
  6. Andreacarola Urso
  7. Sijun Zhu  Is a corresponding author
  1. State University of New York Upstate Medical University, United States
  2. Syracuse University, United States
Research Article
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Cite this article as: eLife 2014;3:e03596 doi: 10.7554/eLife.03596

Abstract

Intermediate neural progenitor cells (INPs) need to avoid differentiation and cell cycle exit while maintaining restricted developmental potential, but mechanisms preventing differentiation and cell cycle exit of INPs are not well understood. Here we report that the Drosophila homolog of mammalian Sp8 transcription factor Buttonhead (Btd) prevents premature differentiation and cell cycle exit of INPs in Drosophila larval type II neuroblast (NB) lineages. We show that loss of Btd leads to elimination of mature INPs due to premature differentiation of INPs into terminally dividing ganglion mother cells. We provide evidence to demonstrate that Btd prevents the premature differentiation by suppressing the expression of the homeodomain protein Prospero in immature INPs. We further show that Btd functions cooperatively with the Ets transcription factor Pointed P1 to promote the generation of INPs. Thus, our work reveals a critical mechanism that prevents premature differentiation and cell cycle exit ofDrosophila INPs.

Article and author information

Author details

  1. Yonggang Xie

    State University of New York Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Xiaosu Li

    State University of New York Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Xian Zhang

    State University of New York Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Shaolin Mei

    State University of New York Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Hongyu Li

    State University of New York Upstate Medical University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Andreacarola Urso

    Syracuse University, Syracuse, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Sijun Zhu

    State University of New York Upstate Medical University, Syracuse, United States
    For correspondence
    zhus@upstate.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

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

Publication history

  1. Received: June 7, 2014
  2. Accepted: September 28, 2014
  3. Accepted Manuscript published: October 6, 2014 (version 1)
  4. Version of Record published: November 6, 2014 (version 2)

Copyright

© 2014, Xie 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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Further reading

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    Trithorax maintains the functional heterogeneity of neural stem cells through the transcription factor Buttonhead

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    The mechanisms that maintain the functional heterogeneity of stem cells, which generates diverse differentiated cell types required for organogenesis, are not understood. In this study, we report that Trithorax (Trx) actively maintains the heterogeneity of neural stem cells (neuroblasts) in the developing Drosophila larval brain. trx mutant type II neuroblasts gradually adopt a type I neuroblast functional identity, losing the competence to generate intermediate neural progenitors (INPs) and directly generating differentiated cells. Trx regulates a type II neuroblast functional identity in part by maintaining chromatin in the buttonhead (btd) locus in an active state through the histone methyltransferase activity of the SET1/MLL complex. Consistently, btd is necessary and sufficient for eliciting a type II neuroblast functional identity. Furthermore, over-expression of btd restores the competence to generate INPs in trx mutant type II neuroblasts. Thus, Trx instructs a type II neuroblast functional identity by epigenetically promoting Btd expression, thereby maintaining neuroblast functional heterogeneity.

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