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Articles, Development/Plasticity/Repair

Wnt Signaling Specifies Anteroposterior Progenitor Zone Identity in the Drosophila Visual Center

Takumi Suzuki, Olena Trush, Tetsuo Yasugi, Rie Takayama and Makoto Sato
Journal of Neuroscience 15 June 2016, 36 (24) 6503-6513; https://doi.org/10.1523/JNEUROSCI.0864-16.2016
Takumi Suzuki
1Laboratory of Developmental Neurobiology, Brain/Liver Interface Medicine Research Center,
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Olena Trush
2Graduate School of Medical Sciences, and
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Tetsuo Yasugi
3Mathematical Neuroscience Unit, Institute for Frontier Science Initiative, Kanazawa University, Ishikawa 920-8640, Japan, and
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Rie Takayama
3Mathematical Neuroscience Unit, Institute for Frontier Science Initiative, Kanazawa University, Ishikawa 920-8640, Japan, and
4Core Research for Evolutional Science and Technology, JST, Saitama 332-0012, Japan
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Makoto Sato
1Laboratory of Developmental Neurobiology, Brain/Liver Interface Medicine Research Center,
2Graduate School of Medical Sciences, and
3Mathematical Neuroscience Unit, Institute for Frontier Science Initiative, Kanazawa University, Ishikawa 920-8640, Japan, and
4Core Research for Evolutional Science and Technology, JST, Saitama 332-0012, Japan
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Abstract

During brain development, various types of neuronal populations are produced from different progenitor pools to produce neuronal diversity that is sufficient to establish functional neuronal circuits. However, the molecular mechanisms that specify the identity of each progenitor pool remain obscure. Here, we show that Wnt signaling is essential for the specification of the identity of posterior progenitor pools in the Drosophila visual center. In the medulla, the largest component of the visual center, different types of neurons are produced from two progenitor pools: the outer proliferation center (OPC) and glial precursor cells (GPCs; also known as tips of the OPC). We found that OPC-type neurons are produced from the GPCs at the expense of GPC-type neurons when Wnt signaling is suppressed in the GPCs. In contrast, GPC-type neurons are ectopically induced when Wnt signaling is ectopically activated in the OPC. These results suggest that Wnt signaling is necessary and sufficient for the specification of the progenitor pool identity. We also found that Homothorax (Hth), which is temporally expressed in the OPC, is ectopically induced in the GPCs by suppression of Wnt signaling and that ectopic induction of Hth phenocopies the suppression of Wnt signaling in the GPCs. Thus, Wnt signaling is involved in regionalization of the fly visual center through the specification of the progenitor pool located posterior to the medulla by suppressing Hth expression.

SIGNIFICANCE STATEMENT Brain consists of considerably diverse neurons of different origins. In mammalian brain, excitatory and inhibitory neurons derive from the dorsal and ventral telencephalon, respectively. Multiple progenitor pools also contribute to the neuronal diversity in fly brain. However, it has been unclear how differences between these progenitor pools are established. Here, we show that Wnt signaling, an evolutionarily conserved signaling, is involved in the process that establishes the differences between these progenitor pools. Because β-catenin signaling, which is under the control of Wnt ligands, specifies progenitor pool identity in the developing mammalian thalamus, Wnt signaling-mediated specification of progenitor pool identity may be conserved in insect and mammalian brains.

  • Drosophila
  • GPC
  • OPC
  • optic lobe
  • wingless
  • Wnt
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The Journal of Neuroscience: 36 (24)
Journal of Neuroscience
Vol. 36, Issue 24
15 Jun 2016
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Wnt Signaling Specifies Anteroposterior Progenitor Zone Identity in the Drosophila Visual Center
Takumi Suzuki, Olena Trush, Tetsuo Yasugi, Rie Takayama, Makoto Sato
Journal of Neuroscience 15 June 2016, 36 (24) 6503-6513; DOI: 10.1523/JNEUROSCI.0864-16.2016

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Wnt Signaling Specifies Anteroposterior Progenitor Zone Identity in the Drosophila Visual Center
Takumi Suzuki, Olena Trush, Tetsuo Yasugi, Rie Takayama, Makoto Sato
Journal of Neuroscience 15 June 2016, 36 (24) 6503-6513; DOI: 10.1523/JNEUROSCI.0864-16.2016
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Keywords

  • Drosophila
  • GPC
  • OPC
  • optic lobe
  • wingless
  • WNT

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