Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum

Yusuke Seto; Tomoya Nakatani; Norihisa Masuyama; Shinichiro Taya; Minoru Kumai; Yasuko Minaki; Akiko Hamaguchi; Yukiko U. Inoue; Takayoshi Inoue; Satoshi Miyashita; Tomoyuki Fujiyama; Mayumi Yamada; Heather Chapman; Kenneth Campbell; Mark A. Magnuson; Christopher V. Wright; Yoshiya Kawaguchi; Kazuhiro Ikenaka; Hirohide Takebayashi; Shin'Ichi Ishiwata; Yuichi Ono; Mikio Hoshino

doi:10.1038/ncomms4337

Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum

Yusuke Seto, Tomoya Nakatani, Norihisa Masuyama, Shinichiro Taya, Minoru Kumai, Yasuko Minaki, Akiko Hamaguchi, Yukiko U. Inoue, Takayoshi Inoue, Satoshi Miyashita, Tomoyuki Fujiyama, Mayumi Yamada, Heather Chapman, Kenneth Campbell, Mark A. Magnuson, Christopher V. Wright, Yoshiya Kawaguchi, Kazuhiro Ikenaka, Hirohide Takebayashi, Shin'Ichi IshiwataYuichi Ono, Mikio Hoshino

Research output: Contribution to journal › Article › peer-review

77 Citations (Scopus)

Abstract

In the cerebellum, all GABAergic neurons are generated from the Ptf1a-expressing ventricular zone (Ptf1a domain). However, the machinery to produce different types of GABAergic neurons remains elusive. Here we show temporal regulation of distinct GABAergic neuron progenitors in the cerebellum. Within the Ptf1a domain at early stages, we find two subpopulations; dorsally and ventrally located progenitors that express Olig2 and Gsx1, respectively. Lineage tracing reveals the former are exclusively Purkinje cell progenitors (PCPs) and the latter Pax2-positive interneuron progenitors (PIPs). As development proceeds, PCPs gradually become PIPs starting from ventral to dorsal. In gain- and loss-of-function mutants for Gsx1 and Olig1/2, we observe abnormal transitioning from PCPs to PIPs at inappropriate developmental stages. Our findings suggest that the temporal identity transition of cerebellar GABAergic neuron progenitors from PCPs to PIPs is negatively regulated by Olig2 and positively by Gsx1, and contributes to understanding temporal control of neuronal progenitor identities.

Original language	English
Article number	3337
Journal	Nature communications
Volume	5
DOIs	https://doi.org/10.1038/ncomms4337
Publication status	Published - 18-02-2014
Externally published	Yes

All Science Journal Classification (ASJC) codes

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/ncomms4337

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Seto, Y., Nakatani, T., Masuyama, N., Taya, S., Kumai, M., Minaki, Y., Hamaguchi, A., Inoue, Y. U., Inoue, T., Miyashita, S., Fujiyama, T., Yamada, M., Chapman, H., Campbell, K., Magnuson, M. A., Wright, C. V., Kawaguchi, Y., Ikenaka, K., Takebayashi, H., ... Hoshino, M. (2014). Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum. Nature communications, 5, Article 3337. https://doi.org/10.1038/ncomms4337

@article{be3e42d5076e4581a367e123d671e2d2,

title = "Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum",

abstract = "In the cerebellum, all GABAergic neurons are generated from the Ptf1a-expressing ventricular zone (Ptf1a domain). However, the machinery to produce different types of GABAergic neurons remains elusive. Here we show temporal regulation of distinct GABAergic neuron progenitors in the cerebellum. Within the Ptf1a domain at early stages, we find two subpopulations; dorsally and ventrally located progenitors that express Olig2 and Gsx1, respectively. Lineage tracing reveals the former are exclusively Purkinje cell progenitors (PCPs) and the latter Pax2-positive interneuron progenitors (PIPs). As development proceeds, PCPs gradually become PIPs starting from ventral to dorsal. In gain- and loss-of-function mutants for Gsx1 and Olig1/2, we observe abnormal transitioning from PCPs to PIPs at inappropriate developmental stages. Our findings suggest that the temporal identity transition of cerebellar GABAergic neuron progenitors from PCPs to PIPs is negatively regulated by Olig2 and positively by Gsx1, and contributes to understanding temporal control of neuronal progenitor identities.",

author = "Yusuke Seto and Tomoya Nakatani and Norihisa Masuyama and Shinichiro Taya and Minoru Kumai and Yasuko Minaki and Akiko Hamaguchi and Inoue, {Yukiko U.} and Takayoshi Inoue and Satoshi Miyashita and Tomoyuki Fujiyama and Mayumi Yamada and Heather Chapman and Kenneth Campbell and Magnuson, {Mark A.} and Wright, {Christopher V.} and Yoshiya Kawaguchi and Kazuhiro Ikenaka and Hirohide Takebayashi and Shin'Ichi Ishiwata and Yuichi Ono and Mikio Hoshino",

year = "2014",

month = feb,

day = "18",

doi = "10.1038/ncomms4337",

language = "English",

volume = "5",

journal = "Nature communications",

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Seto, Y, Nakatani, T, Masuyama, N, Taya, S, Kumai, M, Minaki, Y, Hamaguchi, A, Inoue, YU, Inoue, T, Miyashita, S, Fujiyama, T, Yamada, M, Chapman, H, Campbell, K, Magnuson, MA, Wright, CV, Kawaguchi, Y, Ikenaka, K, Takebayashi, H, Ishiwata, SI, Ono, Y & Hoshino, M 2014, 'Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum', Nature communications, vol. 5, 3337. https://doi.org/10.1038/ncomms4337

TY - JOUR

T1 - Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum

AU - Seto, Yusuke

AU - Nakatani, Tomoya

AU - Masuyama, Norihisa

AU - Taya, Shinichiro

AU - Kumai, Minoru

AU - Minaki, Yasuko

AU - Hamaguchi, Akiko

AU - Inoue, Yukiko U.

AU - Inoue, Takayoshi

AU - Miyashita, Satoshi

AU - Fujiyama, Tomoyuki

AU - Yamada, Mayumi

AU - Chapman, Heather

AU - Campbell, Kenneth

AU - Magnuson, Mark A.

AU - Wright, Christopher V.

AU - Kawaguchi, Yoshiya

AU - Ikenaka, Kazuhiro

AU - Takebayashi, Hirohide

AU - Ishiwata, Shin'Ichi

AU - Ono, Yuichi

AU - Hoshino, Mikio

PY - 2014/2/18

Y1 - 2014/2/18

N2 - In the cerebellum, all GABAergic neurons are generated from the Ptf1a-expressing ventricular zone (Ptf1a domain). However, the machinery to produce different types of GABAergic neurons remains elusive. Here we show temporal regulation of distinct GABAergic neuron progenitors in the cerebellum. Within the Ptf1a domain at early stages, we find two subpopulations; dorsally and ventrally located progenitors that express Olig2 and Gsx1, respectively. Lineage tracing reveals the former are exclusively Purkinje cell progenitors (PCPs) and the latter Pax2-positive interneuron progenitors (PIPs). As development proceeds, PCPs gradually become PIPs starting from ventral to dorsal. In gain- and loss-of-function mutants for Gsx1 and Olig1/2, we observe abnormal transitioning from PCPs to PIPs at inappropriate developmental stages. Our findings suggest that the temporal identity transition of cerebellar GABAergic neuron progenitors from PCPs to PIPs is negatively regulated by Olig2 and positively by Gsx1, and contributes to understanding temporal control of neuronal progenitor identities.

AB - In the cerebellum, all GABAergic neurons are generated from the Ptf1a-expressing ventricular zone (Ptf1a domain). However, the machinery to produce different types of GABAergic neurons remains elusive. Here we show temporal regulation of distinct GABAergic neuron progenitors in the cerebellum. Within the Ptf1a domain at early stages, we find two subpopulations; dorsally and ventrally located progenitors that express Olig2 and Gsx1, respectively. Lineage tracing reveals the former are exclusively Purkinje cell progenitors (PCPs) and the latter Pax2-positive interneuron progenitors (PIPs). As development proceeds, PCPs gradually become PIPs starting from ventral to dorsal. In gain- and loss-of-function mutants for Gsx1 and Olig1/2, we observe abnormal transitioning from PCPs to PIPs at inappropriate developmental stages. Our findings suggest that the temporal identity transition of cerebellar GABAergic neuron progenitors from PCPs to PIPs is negatively regulated by Olig2 and positively by Gsx1, and contributes to understanding temporal control of neuronal progenitor identities.

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DO - 10.1038/ncomms4337

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SN - 2041-1723

VL - 5

JO - Nature communications

JF - Nature communications

M1 - 3337

ER -

Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum

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