Ci-Rga, a gene encoding an MtN3/saliva family transmembrane protein, is essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis

Mayuko Hamada, Shuichi Wada, Kenji Kobayashi, Nori Satoh

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

A novel gene (Ci-Rga) essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis is reported here. This gene was identified through functional screening of Ciona genes required for development by translational inhibition experiments with morpholino antisense oligonucleotides. The deduced protein of Ci-Rga contains two copies of a domain with unknown function called the MtN3/saliva domain. Phylogenetic analysis showed that Ci-Rga belongs to the MtN3/saliva family of genes conserved among metazoans and plants, and is an ortholog of mouse Rga (Recombination-activating gene 1 gene activation). During Ciona embryogenesis, both maternal and zygotic transcripts of Ci-Rga were expressed. Translational inhibition of Ci-Rga with specific morpholino resulted in abnormal embryos in which the cleavage pattern became atypical and expression of marker genes for each of the six major tissues, namely the endoderm, muscle, mesenchyme, notochord, neural tissue, and epidermis, was lost or suppressed at the tailbud stage. Although differentiation of all the six major tissues was affected by Ci-Rga knock-down, the degree of abnormalities and the timing of appearance of abnormalities were different among tissues. Expression analysis of developmentally important genes involved in the fate specification, such as Ci-Bra, Ci-Twist-like1a, Ci-Otx, Ci-Fgf9/16/20, Ci-Lhx3, Ci-FoxD, and Ci-Tbx6b, showed that an initial step of the fate specification of notochord, mesenchyme, and neural tissue, but not of endoderm or muscle, is impaired in the knock-down embryo. These results showed that Ci-Rga is a multifunctional gene essential for tissue differentiation during embryogenesis, and is primarily required for the fate specification of notochord, mesenchyme, and neural tissue, and provide some insights into the function of this little-known group of genes.

Original languageEnglish
Pages (from-to)364-376
Number of pages13
JournalDifferentiation
Volume73
Issue number7
DOIs
Publication statusPublished - Sep 2005
Externally publishedYes

Fingerprint

RAG-1 Genes
Ciona intestinalis
Urochordata
Saliva
Transcriptional Activation
Embryonic Development
Notochord
Genes
Proteins
Mesoderm
Morpholinos
Endoderm
Embryonic Structures
Gene Knockdown Techniques
Muscles
Antisense Oligonucleotides
Essential Genes
Epidermis
Mothers
Gene Expression

Keywords

  • Ciona intestinalis
  • Differentiation
  • Embryogenesis
  • Gene function
  • Morpholino
  • MtN3/saliva
  • Novel gene
  • Transmembrane protein

ASJC Scopus subject areas

  • Pathology and Forensic Medicine
  • Developmental Biology
  • Cell Biology

Cite this

Ci-Rga, a gene encoding an MtN3/saliva family transmembrane protein, is essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis. / Hamada, Mayuko; Wada, Shuichi; Kobayashi, Kenji; Satoh, Nori.

In: Differentiation, Vol. 73, No. 7, 09.2005, p. 364-376.

Research output: Contribution to journalArticle

@article{6006bc6cd3904cc6acedf0c65b5fa9d8,
title = "Ci-Rga, a gene encoding an MtN3/saliva family transmembrane protein, is essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis",
abstract = "A novel gene (Ci-Rga) essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis is reported here. This gene was identified through functional screening of Ciona genes required for development by translational inhibition experiments with morpholino antisense oligonucleotides. The deduced protein of Ci-Rga contains two copies of a domain with unknown function called the MtN3/saliva domain. Phylogenetic analysis showed that Ci-Rga belongs to the MtN3/saliva family of genes conserved among metazoans and plants, and is an ortholog of mouse Rga (Recombination-activating gene 1 gene activation). During Ciona embryogenesis, both maternal and zygotic transcripts of Ci-Rga were expressed. Translational inhibition of Ci-Rga with specific morpholino resulted in abnormal embryos in which the cleavage pattern became atypical and expression of marker genes for each of the six major tissues, namely the endoderm, muscle, mesenchyme, notochord, neural tissue, and epidermis, was lost or suppressed at the tailbud stage. Although differentiation of all the six major tissues was affected by Ci-Rga knock-down, the degree of abnormalities and the timing of appearance of abnormalities were different among tissues. Expression analysis of developmentally important genes involved in the fate specification, such as Ci-Bra, Ci-Twist-like1a, Ci-Otx, Ci-Fgf9/16/20, Ci-Lhx3, Ci-FoxD, and Ci-Tbx6b, showed that an initial step of the fate specification of notochord, mesenchyme, and neural tissue, but not of endoderm or muscle, is impaired in the knock-down embryo. These results showed that Ci-Rga is a multifunctional gene essential for tissue differentiation during embryogenesis, and is primarily required for the fate specification of notochord, mesenchyme, and neural tissue, and provide some insights into the function of this little-known group of genes.",
keywords = "Ciona intestinalis, Differentiation, Embryogenesis, Gene function, Morpholino, MtN3/saliva, Novel gene, Transmembrane protein",
author = "Mayuko Hamada and Shuichi Wada and Kenji Kobayashi and Nori Satoh",
year = "2005",
month = "9",
doi = "10.1111/j.1432-0436.2005.00037.x",
language = "English",
volume = "73",
pages = "364--376",
journal = "Differentiation",
issn = "0301-4681",
publisher = "Elsevier BV",
number = "7",

}

TY - JOUR

T1 - Ci-Rga, a gene encoding an MtN3/saliva family transmembrane protein, is essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis

AU - Hamada, Mayuko

AU - Wada, Shuichi

AU - Kobayashi, Kenji

AU - Satoh, Nori

PY - 2005/9

Y1 - 2005/9

N2 - A novel gene (Ci-Rga) essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis is reported here. This gene was identified through functional screening of Ciona genes required for development by translational inhibition experiments with morpholino antisense oligonucleotides. The deduced protein of Ci-Rga contains two copies of a domain with unknown function called the MtN3/saliva domain. Phylogenetic analysis showed that Ci-Rga belongs to the MtN3/saliva family of genes conserved among metazoans and plants, and is an ortholog of mouse Rga (Recombination-activating gene 1 gene activation). During Ciona embryogenesis, both maternal and zygotic transcripts of Ci-Rga were expressed. Translational inhibition of Ci-Rga with specific morpholino resulted in abnormal embryos in which the cleavage pattern became atypical and expression of marker genes for each of the six major tissues, namely the endoderm, muscle, mesenchyme, notochord, neural tissue, and epidermis, was lost or suppressed at the tailbud stage. Although differentiation of all the six major tissues was affected by Ci-Rga knock-down, the degree of abnormalities and the timing of appearance of abnormalities were different among tissues. Expression analysis of developmentally important genes involved in the fate specification, such as Ci-Bra, Ci-Twist-like1a, Ci-Otx, Ci-Fgf9/16/20, Ci-Lhx3, Ci-FoxD, and Ci-Tbx6b, showed that an initial step of the fate specification of notochord, mesenchyme, and neural tissue, but not of endoderm or muscle, is impaired in the knock-down embryo. These results showed that Ci-Rga is a multifunctional gene essential for tissue differentiation during embryogenesis, and is primarily required for the fate specification of notochord, mesenchyme, and neural tissue, and provide some insights into the function of this little-known group of genes.

AB - A novel gene (Ci-Rga) essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis is reported here. This gene was identified through functional screening of Ciona genes required for development by translational inhibition experiments with morpholino antisense oligonucleotides. The deduced protein of Ci-Rga contains two copies of a domain with unknown function called the MtN3/saliva domain. Phylogenetic analysis showed that Ci-Rga belongs to the MtN3/saliva family of genes conserved among metazoans and plants, and is an ortholog of mouse Rga (Recombination-activating gene 1 gene activation). During Ciona embryogenesis, both maternal and zygotic transcripts of Ci-Rga were expressed. Translational inhibition of Ci-Rga with specific morpholino resulted in abnormal embryos in which the cleavage pattern became atypical and expression of marker genes for each of the six major tissues, namely the endoderm, muscle, mesenchyme, notochord, neural tissue, and epidermis, was lost or suppressed at the tailbud stage. Although differentiation of all the six major tissues was affected by Ci-Rga knock-down, the degree of abnormalities and the timing of appearance of abnormalities were different among tissues. Expression analysis of developmentally important genes involved in the fate specification, such as Ci-Bra, Ci-Twist-like1a, Ci-Otx, Ci-Fgf9/16/20, Ci-Lhx3, Ci-FoxD, and Ci-Tbx6b, showed that an initial step of the fate specification of notochord, mesenchyme, and neural tissue, but not of endoderm or muscle, is impaired in the knock-down embryo. These results showed that Ci-Rga is a multifunctional gene essential for tissue differentiation during embryogenesis, and is primarily required for the fate specification of notochord, mesenchyme, and neural tissue, and provide some insights into the function of this little-known group of genes.

KW - Ciona intestinalis

KW - Differentiation

KW - Embryogenesis

KW - Gene function

KW - Morpholino

KW - MtN3/saliva

KW - Novel gene

KW - Transmembrane protein

UR - http://www.scopus.com/inward/record.url?scp=33644829357&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33644829357&partnerID=8YFLogxK

U2 - 10.1111/j.1432-0436.2005.00037.x

DO - 10.1111/j.1432-0436.2005.00037.x

M3 - Article

C2 - 16219040

AN - SCOPUS:33644829357

VL - 73

SP - 364

EP - 376

JO - Differentiation

JF - Differentiation

SN - 0301-4681

IS - 7

ER -