Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development

Yusuke Nagao, Takao Suzuki, Atsushi Shimizu, Tetsuaki Kimura, Ryoko Seki, Tomoko Adachi, Chikako Inoue, Yoshihiro Omae, Yasuhiro Kamei, Ikuyo Hara, Yoshihito Taniguchi, Kiyoshi Naruse, Yuko Wakamatsu, Robert N. Kelsh, Masahiko Hibi, Hisashi Hashimoto

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Mechanisms generating diverse cell types from multipotent progenitors are crucial for normal development. Neural crest cells (NCCs) are multipotent stem cells that give rise to numerous cell-types, including pigment cells. Medaka has four types of NCC-derived pigment cells (xanthophores, leucophores, melanophores and iridophores), making medaka pigment cell development an excellent model for studying the mechanisms controlling specification of distinct cell types from a multipotent progenitor. Medaka many leucophores-3 (ml-3) mutant embryos exhibit a unique phenotype characterized by excessive formation of leucophores and absence of xanthophores. We show that ml-3 encodes sox5, which is expressed in premigratory NCCs and differentiating xanthophores. Cell transplantation studies reveal a cell-autonomous role of sox5 in the xanthophore lineage. pax7a is expressed in NCCs and required for both xanthophore and leucophore lineages; we demonstrate that Sox5 functions downstream of Pax7a. We propose a model in which multipotent NCCs first give rise to pax7a-positive partially fate-restricted intermediate progenitors for xanthophores and leucophores; some of these progenitors then express sox5, and as a result of Sox5 action develop into xanthophores. Our results provide the first demonstration that Sox5 can function as a molecular switch driving specification of a specific cell-fate (xanthophore) from a partially-restricted, but still multipotent, progenitor (the shared xanthophore-leucophore progenitor).
LanguageEnglish
Article numbere1004246
Pages1-14
Number of pages14
JournalPlos Genetics
Volume10
Issue number4
DOIs
StatusPublished - 3 Apr 2014

Cite this

Nagao, Y., Suzuki, T., Shimizu, A., Kimura, T., Seki, R., Adachi, T., ... Hashimoto, H. (2014). Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development. Plos Genetics, 10(4), 1-14. [e1004246]. https://doi.org/10.1371/journal.pgen.1004246

Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development. / Nagao, Yusuke; Suzuki, Takao; Shimizu, Atsushi; Kimura, Tetsuaki; Seki, Ryoko; Adachi, Tomoko; Inoue, Chikako; Omae, Yoshihiro; Kamei, Yasuhiro; Hara, Ikuyo; Taniguchi, Yoshihito; Naruse, Kiyoshi; Wakamatsu, Yuko; Kelsh, Robert N.; Hibi, Masahiko; Hashimoto, Hisashi.

In: Plos Genetics, Vol. 10, No. 4, e1004246, 03.04.2014, p. 1-14.

Research output: Contribution to journalArticle

Nagao, Y, Suzuki, T, Shimizu, A, Kimura, T, Seki, R, Adachi, T, Inoue, C, Omae, Y, Kamei, Y, Hara, I, Taniguchi, Y, Naruse, K, Wakamatsu, Y, Kelsh, RN, Hibi, M & Hashimoto, H 2014, 'Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development', Plos Genetics, vol. 10, no. 4, e1004246, pp. 1-14. https://doi.org/10.1371/journal.pgen.1004246
Nagao Y, Suzuki T, Shimizu A, Kimura T, Seki R, Adachi T et al. Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development. Plos Genetics. 2014 Apr 3;10(4):1-14. e1004246. https://doi.org/10.1371/journal.pgen.1004246
Nagao, Yusuke ; Suzuki, Takao ; Shimizu, Atsushi ; Kimura, Tetsuaki ; Seki, Ryoko ; Adachi, Tomoko ; Inoue, Chikako ; Omae, Yoshihiro ; Kamei, Yasuhiro ; Hara, Ikuyo ; Taniguchi, Yoshihito ; Naruse, Kiyoshi ; Wakamatsu, Yuko ; Kelsh, Robert N. ; Hibi, Masahiko ; Hashimoto, Hisashi. / Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development. In: Plos Genetics. 2014 ; Vol. 10, No. 4. pp. 1-14.
@article{4616cfc6dc604cf9b1aa94887d451d62,
title = "Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development",
abstract = "Mechanisms generating diverse cell types from multipotent progenitors are crucial for normal development. Neural crest cells (NCCs) are multipotent stem cells that give rise to numerous cell-types, including pigment cells. Medaka has four types of NCC-derived pigment cells (xanthophores, leucophores, melanophores and iridophores), making medaka pigment cell development an excellent model for studying the mechanisms controlling specification of distinct cell types from a multipotent progenitor. Medaka many leucophores-3 (ml-3) mutant embryos exhibit a unique phenotype characterized by excessive formation of leucophores and absence of xanthophores. We show that ml-3 encodes sox5, which is expressed in premigratory NCCs and differentiating xanthophores. Cell transplantation studies reveal a cell-autonomous role of sox5 in the xanthophore lineage. pax7a is expressed in NCCs and required for both xanthophore and leucophore lineages; we demonstrate that Sox5 functions downstream of Pax7a. We propose a model in which multipotent NCCs first give rise to pax7a-positive partially fate-restricted intermediate progenitors for xanthophores and leucophores; some of these progenitors then express sox5, and as a result of Sox5 action develop into xanthophores. Our results provide the first demonstration that Sox5 can function as a molecular switch driving specification of a specific cell-fate (xanthophore) from a partially-restricted, but still multipotent, progenitor (the shared xanthophore-leucophore progenitor).",
author = "Yusuke Nagao and Takao Suzuki and Atsushi Shimizu and Tetsuaki Kimura and Ryoko Seki and Tomoko Adachi and Chikako Inoue and Yoshihiro Omae and Yasuhiro Kamei and Ikuyo Hara and Yoshihito Taniguchi and Kiyoshi Naruse and Yuko Wakamatsu and Kelsh, {Robert N.} and Masahiko Hibi and Hisashi Hashimoto",
year = "2014",
month = "4",
day = "3",
doi = "10.1371/journal.pgen.1004246",
language = "English",
volume = "10",
pages = "1--14",
journal = "Plos Genetics",
issn = "1553-7390",
publisher = "Public Library of Science (PLOS)",
number = "4",

}

TY - JOUR

T1 - Sox5 Functions as a Fate Switch in Medaka Pigment Cell Development

AU - Nagao, Yusuke

AU - Suzuki, Takao

AU - Shimizu, Atsushi

AU - Kimura, Tetsuaki

AU - Seki, Ryoko

AU - Adachi, Tomoko

AU - Inoue, Chikako

AU - Omae, Yoshihiro

AU - Kamei, Yasuhiro

AU - Hara, Ikuyo

AU - Taniguchi, Yoshihito

AU - Naruse, Kiyoshi

AU - Wakamatsu, Yuko

AU - Kelsh, Robert N.

AU - Hibi, Masahiko

AU - Hashimoto, Hisashi

PY - 2014/4/3

Y1 - 2014/4/3

N2 - Mechanisms generating diverse cell types from multipotent progenitors are crucial for normal development. Neural crest cells (NCCs) are multipotent stem cells that give rise to numerous cell-types, including pigment cells. Medaka has four types of NCC-derived pigment cells (xanthophores, leucophores, melanophores and iridophores), making medaka pigment cell development an excellent model for studying the mechanisms controlling specification of distinct cell types from a multipotent progenitor. Medaka many leucophores-3 (ml-3) mutant embryos exhibit a unique phenotype characterized by excessive formation of leucophores and absence of xanthophores. We show that ml-3 encodes sox5, which is expressed in premigratory NCCs and differentiating xanthophores. Cell transplantation studies reveal a cell-autonomous role of sox5 in the xanthophore lineage. pax7a is expressed in NCCs and required for both xanthophore and leucophore lineages; we demonstrate that Sox5 functions downstream of Pax7a. We propose a model in which multipotent NCCs first give rise to pax7a-positive partially fate-restricted intermediate progenitors for xanthophores and leucophores; some of these progenitors then express sox5, and as a result of Sox5 action develop into xanthophores. Our results provide the first demonstration that Sox5 can function as a molecular switch driving specification of a specific cell-fate (xanthophore) from a partially-restricted, but still multipotent, progenitor (the shared xanthophore-leucophore progenitor).

AB - Mechanisms generating diverse cell types from multipotent progenitors are crucial for normal development. Neural crest cells (NCCs) are multipotent stem cells that give rise to numerous cell-types, including pigment cells. Medaka has four types of NCC-derived pigment cells (xanthophores, leucophores, melanophores and iridophores), making medaka pigment cell development an excellent model for studying the mechanisms controlling specification of distinct cell types from a multipotent progenitor. Medaka many leucophores-3 (ml-3) mutant embryos exhibit a unique phenotype characterized by excessive formation of leucophores and absence of xanthophores. We show that ml-3 encodes sox5, which is expressed in premigratory NCCs and differentiating xanthophores. Cell transplantation studies reveal a cell-autonomous role of sox5 in the xanthophore lineage. pax7a is expressed in NCCs and required for both xanthophore and leucophore lineages; we demonstrate that Sox5 functions downstream of Pax7a. We propose a model in which multipotent NCCs first give rise to pax7a-positive partially fate-restricted intermediate progenitors for xanthophores and leucophores; some of these progenitors then express sox5, and as a result of Sox5 action develop into xanthophores. Our results provide the first demonstration that Sox5 can function as a molecular switch driving specification of a specific cell-fate (xanthophore) from a partially-restricted, but still multipotent, progenitor (the shared xanthophore-leucophore progenitor).

U2 - 10.1371/journal.pgen.1004246

DO - 10.1371/journal.pgen.1004246

M3 - Article

VL - 10

SP - 1

EP - 14

JO - Plos Genetics

T2 - Plos Genetics

JF - Plos Genetics

SN - 1553-7390

IS - 4

M1 - e1004246

ER -