Cloning and functional analysis of ascidian Mitf in vivo

Insights into the origin of vertebrate pigment cells

Ichiro Yajima, Kosuke Endo, Shigeru Sato, Reiko Toyoda, Hiroshi Wada, Shigeki Shibahara, Takaharu Numakunai, Kazuho Ikeo, Takashi Gojobori, Colin R. Goding, Hiroaki Yamamoto

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

The microphthalmia-associated transcription factor (Mitf) is a basic-helix-loop-helix-leucine zipper (bHLH-ZIP) transcription factor essential for the development and function of all melanin-producing pigment cells in vertebrates. To elucidate the evolutionary history of Mitf and the antiquity of its association with pigment cells, we have isolated and characterized HrMitf, a sole member of the Mitf-TFE bHLH-ZIP subfamily in the ascidian Halocynthia roretzi. Maternal HrMitf mRNA is detected in the fertilized egg and in the animal hemisphere from 4-cell stage through the gastrula stage. From the neurula through the early tailbud stage, HrMitf is preferentially expressed in the pigment-lineage cells that express the lineage-specific melanogenesis genes tyrosinase (HrTyr) and Tyrp. Overexpression of HrMitf induced ectopic expression of HrTyr enzyme activity in mesenchymal cells where the same enzyme activity was induced by overexpression of HrPax3/7, suggesting that a part(s) of the Pax3-Mitf-tyrosinase gene regulatory cascade seen in vertebrate melanocytes is operative during ascidian embryogenesis. We also show HrMitf and mouse Mitf-A, a Mitf isoform abundantly expressed in pigmented epithelial cells, share similar functional characteristics. These results suggest antiquity of the association of the Mitf-TFE subfamily with pigment cells and may support the idea that acquisition of multiple promoters (isoforms) by an ancestral Mitf gene has allowed the evolution of multiple pigment cell types.

Original languageEnglish
Pages (from-to)1489-1504
Number of pages16
JournalMechanisms of Development
Volume120
Issue number12
DOIs
Publication statusPublished - 2003 Jan 1
Externally publishedYes

Keywords

  • Ascidian
  • Eye
  • Microphthalmia
  • Mitf
  • Neural crest
  • Pax37
  • Pigment cells
  • Transcription factor
  • Tyrosinase
  • Tyrp

ASJC Scopus subject areas

  • Embryology
  • Developmental Biology

Cite this

Cloning and functional analysis of ascidian Mitf in vivo : Insights into the origin of vertebrate pigment cells. / Yajima, Ichiro; Endo, Kosuke; Sato, Shigeru; Toyoda, Reiko; Wada, Hiroshi; Shibahara, Shigeki; Numakunai, Takaharu; Ikeo, Kazuho; Gojobori, Takashi; Goding, Colin R.; Yamamoto, Hiroaki.

In: Mechanisms of Development, Vol. 120, No. 12, 01.01.2003, p. 1489-1504.

Research output: Contribution to journalArticle

Yajima, I, Endo, K, Sato, S, Toyoda, R, Wada, H, Shibahara, S, Numakunai, T, Ikeo, K, Gojobori, T, Goding, CR & Yamamoto, H 2003, 'Cloning and functional analysis of ascidian Mitf in vivo: Insights into the origin of vertebrate pigment cells', Mechanisms of Development, vol. 120, no. 12, pp. 1489-1504. https://doi.org/10.1016/j.mod.2003.08.009
Yajima, Ichiro ; Endo, Kosuke ; Sato, Shigeru ; Toyoda, Reiko ; Wada, Hiroshi ; Shibahara, Shigeki ; Numakunai, Takaharu ; Ikeo, Kazuho ; Gojobori, Takashi ; Goding, Colin R. ; Yamamoto, Hiroaki. / Cloning and functional analysis of ascidian Mitf in vivo : Insights into the origin of vertebrate pigment cells. In: Mechanisms of Development. 2003 ; Vol. 120, No. 12. pp. 1489-1504.
@article{84b5573657e14ffc9eeee44e38166daa,
title = "Cloning and functional analysis of ascidian Mitf in vivo: Insights into the origin of vertebrate pigment cells",
abstract = "The microphthalmia-associated transcription factor (Mitf) is a basic-helix-loop-helix-leucine zipper (bHLH-ZIP) transcription factor essential for the development and function of all melanin-producing pigment cells in vertebrates. To elucidate the evolutionary history of Mitf and the antiquity of its association with pigment cells, we have isolated and characterized HrMitf, a sole member of the Mitf-TFE bHLH-ZIP subfamily in the ascidian Halocynthia roretzi. Maternal HrMitf mRNA is detected in the fertilized egg and in the animal hemisphere from 4-cell stage through the gastrula stage. From the neurula through the early tailbud stage, HrMitf is preferentially expressed in the pigment-lineage cells that express the lineage-specific melanogenesis genes tyrosinase (HrTyr) and Tyrp. Overexpression of HrMitf induced ectopic expression of HrTyr enzyme activity in mesenchymal cells where the same enzyme activity was induced by overexpression of HrPax3/7, suggesting that a part(s) of the Pax3-Mitf-tyrosinase gene regulatory cascade seen in vertebrate melanocytes is operative during ascidian embryogenesis. We also show HrMitf and mouse Mitf-A, a Mitf isoform abundantly expressed in pigmented epithelial cells, share similar functional characteristics. These results suggest antiquity of the association of the Mitf-TFE subfamily with pigment cells and may support the idea that acquisition of multiple promoters (isoforms) by an ancestral Mitf gene has allowed the evolution of multiple pigment cell types.",
keywords = "Ascidian, Eye, Microphthalmia, Mitf, Neural crest, Pax37, Pigment cells, Transcription factor, Tyrosinase, Tyrp",
author = "Ichiro Yajima and Kosuke Endo and Shigeru Sato and Reiko Toyoda and Hiroshi Wada and Shigeki Shibahara and Takaharu Numakunai and Kazuho Ikeo and Takashi Gojobori and Goding, {Colin R.} and Hiroaki Yamamoto",
year = "2003",
month = "1",
day = "1",
doi = "10.1016/j.mod.2003.08.009",
language = "English",
volume = "120",
pages = "1489--1504",
journal = "Mechanisms of Development",
issn = "0925-4773",
publisher = "Elsevier Ireland Ltd",
number = "12",

}

TY - JOUR

T1 - Cloning and functional analysis of ascidian Mitf in vivo

T2 - Insights into the origin of vertebrate pigment cells

AU - Yajima, Ichiro

AU - Endo, Kosuke

AU - Sato, Shigeru

AU - Toyoda, Reiko

AU - Wada, Hiroshi

AU - Shibahara, Shigeki

AU - Numakunai, Takaharu

AU - Ikeo, Kazuho

AU - Gojobori, Takashi

AU - Goding, Colin R.

AU - Yamamoto, Hiroaki

PY - 2003/1/1

Y1 - 2003/1/1

N2 - The microphthalmia-associated transcription factor (Mitf) is a basic-helix-loop-helix-leucine zipper (bHLH-ZIP) transcription factor essential for the development and function of all melanin-producing pigment cells in vertebrates. To elucidate the evolutionary history of Mitf and the antiquity of its association with pigment cells, we have isolated and characterized HrMitf, a sole member of the Mitf-TFE bHLH-ZIP subfamily in the ascidian Halocynthia roretzi. Maternal HrMitf mRNA is detected in the fertilized egg and in the animal hemisphere from 4-cell stage through the gastrula stage. From the neurula through the early tailbud stage, HrMitf is preferentially expressed in the pigment-lineage cells that express the lineage-specific melanogenesis genes tyrosinase (HrTyr) and Tyrp. Overexpression of HrMitf induced ectopic expression of HrTyr enzyme activity in mesenchymal cells where the same enzyme activity was induced by overexpression of HrPax3/7, suggesting that a part(s) of the Pax3-Mitf-tyrosinase gene regulatory cascade seen in vertebrate melanocytes is operative during ascidian embryogenesis. We also show HrMitf and mouse Mitf-A, a Mitf isoform abundantly expressed in pigmented epithelial cells, share similar functional characteristics. These results suggest antiquity of the association of the Mitf-TFE subfamily with pigment cells and may support the idea that acquisition of multiple promoters (isoforms) by an ancestral Mitf gene has allowed the evolution of multiple pigment cell types.

AB - The microphthalmia-associated transcription factor (Mitf) is a basic-helix-loop-helix-leucine zipper (bHLH-ZIP) transcription factor essential for the development and function of all melanin-producing pigment cells in vertebrates. To elucidate the evolutionary history of Mitf and the antiquity of its association with pigment cells, we have isolated and characterized HrMitf, a sole member of the Mitf-TFE bHLH-ZIP subfamily in the ascidian Halocynthia roretzi. Maternal HrMitf mRNA is detected in the fertilized egg and in the animal hemisphere from 4-cell stage through the gastrula stage. From the neurula through the early tailbud stage, HrMitf is preferentially expressed in the pigment-lineage cells that express the lineage-specific melanogenesis genes tyrosinase (HrTyr) and Tyrp. Overexpression of HrMitf induced ectopic expression of HrTyr enzyme activity in mesenchymal cells where the same enzyme activity was induced by overexpression of HrPax3/7, suggesting that a part(s) of the Pax3-Mitf-tyrosinase gene regulatory cascade seen in vertebrate melanocytes is operative during ascidian embryogenesis. We also show HrMitf and mouse Mitf-A, a Mitf isoform abundantly expressed in pigmented epithelial cells, share similar functional characteristics. These results suggest antiquity of the association of the Mitf-TFE subfamily with pigment cells and may support the idea that acquisition of multiple promoters (isoforms) by an ancestral Mitf gene has allowed the evolution of multiple pigment cell types.

KW - Ascidian

KW - Eye

KW - Microphthalmia

KW - Mitf

KW - Neural crest

KW - Pax37

KW - Pigment cells

KW - Transcription factor

KW - Tyrosinase

KW - Tyrp

UR - http://www.scopus.com/inward/record.url?scp=0345707673&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0345707673&partnerID=8YFLogxK

U2 - 10.1016/j.mod.2003.08.009

DO - 10.1016/j.mod.2003.08.009

M3 - Article

VL - 120

SP - 1489

EP - 1504

JO - Mechanisms of Development

JF - Mechanisms of Development

SN - 0925-4773

IS - 12

ER -