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

doi:10.1016/j.mod.2003.08.009

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^*

^*Corresponding author for this work

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

34 Scopus citations

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 language	English (US)
Pages (from-to)	1489-1504
Number of pages	16
Journal	Mechanisms of Development
Volume	120
Issue number	12
DOIs	https://doi.org/10.1016/j.mod.2003.08.009
State	Published - Dec 2003
Externally published	Yes

Bibliographical note

Funding Information:
We are grateful to Drs N. Satoh and H. Nishida for helpful discussions, K. Ishida for technical advice on in situ hybridization. We wish to thank Drs Lamaire and Gurdon for allowing us to use the pBluescript RN3 and all members of the Marine Biological Station of Asamushi for supplying the living materials. This work was supported by a Grant-in-Aid from the Ministry of Education, Science and Culture, Japan and NIG Cooperative Research Programs (72-'96, 56-'97, 63-'98, 46-'99) to H.Y.

Keywords

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

ASJC Scopus subject areas

Embryology
Developmental Biology

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10.1016/j.mod.2003.08.009

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@article{0c66bbeb291c494eb28402f4ed77f086,

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",

note = "Funding Information: We are grateful to Drs N. Satoh and H. Nishida for helpful discussions, K. Ishida for technical advice on in situ hybridization. We wish to thank Drs Lamaire and Gurdon for allowing us to use the pBluescript RN3 and all members of the Marine Biological Station of Asamushi for supplying the living materials. This work was supported by a Grant-in-Aid from the Ministry of Education, Science and Culture, Japan and NIG Cooperative Research Programs (72-'96, 56-'97, 63-'98, 46-'99) to H.Y.",

year = "2003",

month = dec,

doi = "10.1016/j.mod.2003.08.009",

language = "English (US)",

volume = "120",

pages = "1489--1504",

journal = "Mechanisms of Development",

issn = "0925-4773",

publisher = "Elsevier BV",

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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

N1 - Funding Information: We are grateful to Drs N. Satoh and H. Nishida for helpful discussions, K. Ishida for technical advice on in situ hybridization. We wish to thank Drs Lamaire and Gurdon for allowing us to use the pBluescript RN3 and all members of the Marine Biological Station of Asamushi for supplying the living materials. This work was supported by a Grant-in-Aid from the Ministry of Education, Science and Culture, Japan and NIG Cooperative Research Programs (72-'96, 56-'97, 63-'98, 46-'99) to H.Y.

PY - 2003/12

Y1 - 2003/12

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.

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KW - Ascidian

KW - Eye

KW - Microphthalmia

KW - Mitf

KW - Neural crest

KW - Pax37

KW - Pigment cells

KW - Transcription factor

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SP - 1489

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JO - Mechanisms of Development

JF - Mechanisms of Development

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ER -

Cloning and functional analysis of ascidian Mitf in vivo: Insights into the origin of vertebrate pigment cells

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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