1. Developmental Biology
  2. Neuroscience

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
https://doi.org/10.7554/eLife.03596
Share this article
Cite this article
  1. Yonggang Xie
  2. Xiaosu Li
  3. Xian Zhang
  4. Shaolin Mei
  5. Hongyu Li
  6. Andreacarola Urso
  7. Sijun Zhu
(2014)
The Drosophila Sp8 transcription factor buttonhead prevents premature differentiation of intermediate neural progenitors
eLife 3:e03596.
https://doi.org/10.7554/eLife.03596
  2. Download BibTeX
  3. Download .RIS

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.

Metrics

  • 1,827
    Page views
  • 208
    Downloads
  • 19
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Yonggang Xie
  2. Xiaosu Li
  3. Xian Zhang
  4. Shaolin Mei
  5. Hongyu Li
  6. Andreacarola Urso
  7. Sijun Zhu
(2014)
The Drosophila Sp8 transcription factor buttonhead prevents premature differentiation of intermediate neural progenitors
eLife 3:e03596.
https://doi.org/10.7554/eLife.03596

Categories and tags

Research organism

Further reading

    1. Stem Cells and Regenerative Medicine

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

    Hideyuki Komori et al.
    Research Article Updated

    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.

    1. Stem Cells and Regenerative Medicine
    2. Developmental Biology

    Neuroblasts: Maintaining neural stem cell identity in the brain

    Yanrui Jiang, Heinrich Reichert
    Insight

    In the developing fruit fly brain, a protein called Trithorax increases the number of neural cells produced from a single stem cell, in part by regulating the transcription of the target genes buttonhead and pointed.

    1. Cell Biology
    2. Developmental Biology

    Zebrafish fin regeneration involves generic and regeneration-specific osteoblast injury responses

    Ivonne Sehring et al.
    Research Article Updated

    Successful regeneration requires the coordinated execution of multiple cellular responses to injury. In amputated zebrafish fins, mature osteoblasts dedifferentiate, migrate towards the injury, and form proliferative osteogenic blastema cells. We show that osteoblast migration is preceded by cell elongation and alignment along the proximodistal axis, which require actomyosin, but not microtubule (MT) turnover. Surprisingly, osteoblast dedifferentiation and migration can be uncoupled. Using pharmacological and genetic interventions, we found that NF-ĸB and retinoic acid signalling regulate dedifferentiation without affecting migration, while the complement system and actomyosin dynamics affect migration but not dedifferentiation. Furthermore, by removing bone at two locations within a fin ray, we established an injury model containing two injury sites. We found that osteoblasts dedifferentiate at and migrate towards both sites, while accumulation of osteogenic progenitor cells and regenerative bone formation only occur at the distal-facing injury. Together, these data indicate that osteoblast dedifferentiation and migration represent generic injury responses that are differentially regulated and can occur independently of each other and of regenerative growth. We conclude that successful fin bone regeneration appears to involve the coordinated execution of generic and regeneration-specific responses of osteoblasts to injury.