A gradient of maternal Bicaudal-C controls vertebrate embryogenesis via translational repression of mRNAs encoding cell fate regulators

Sookhee Park; Susanne Blaser; Melissa A Marchal; Douglas W Houston; Michael D Sheets

doi:10.1242/dev.131359

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A gradient of maternal Bicaudal-C controls vertebrate embryogenesis via translational repression of mRNAs encoding cell fate regulators

Journal article

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Peer reviewed

A gradient of maternal Bicaudal-C controls vertebrate embryogenesis via translational repression of mRNAs encoding cell fate regulators

Sookhee Park, Susanne Blaser, Melissa A Marchal, Douglas W Houston and Michael D Sheets

Development (Cambridge), Vol.143(5), pp.864-871

03/01/2016

DOI: 10.1242/dev.131359

PMCID: PMC4813341

PMID: 26811381

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Abstract

Vertebrate Bicaudal-C (Bicc1) has important biological roles in the formation and homeostasis of multiple organs, but direct experiments to address the role of maternal Bicc1 in early vertebrate embryogenesis have not been reported. Here, we use antisense phosphorothioate-modified oligonucleotides and the host-transfer technique to eliminate specifically maternal stores of both bicc1 mRNA and Bicc1 protein from Xenopus laevis eggs. Fertilization of these Bicc1-depleted eggs produced embryos with an excess of dorsal-anterior structures and overexpressed organizer-specific genes, indicating that maternal Bicc1 is crucial for normal embryonic patterning of the vertebrate embryo. Bicc1 is an RNA-binding protein with robust translational repression function. Here, we show that the maternal mRNA encoding the cell-fate regulatory protein Wnt11b is a direct target of Bicc1-mediated repression. It is well established that the Wnt signaling pathway is crucial to vertebrate embryogenesis. Thus, the work presented here links the molecular function of Bicc1 in mRNA target-specific translation repression to its biological role in the maternally controlled stages of vertebrate embryogenesis.

Xenopus laevis - embryology

Signal Transduction

Oocytes - metabolism

MicroRNAs - metabolism

Embryonic Development

RNA, Messenger - metabolism

Wnt Proteins - metabolism

Cell Lineage

Phenotype

Animals

Oligonucleotides, Antisense - genetics

Gene Expression Regulation, Developmental

RNA, Messenger, Stored - genetics

Female

Transcription, Genetic

Xenopus Proteins - metabolism

Mutation

RNA-Binding Proteins - metabolism

Details

Title: Subtitle: A gradient of maternal Bicaudal-C controls vertebrate embryogenesis via translational repression of mRNAs encoding cell fate regulators
Creators: Sookhee Park - Department of Biomolecular Chemistry, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53706, USA
Susanne Blaser - Department of Biomolecular Chemistry, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53706, USA
Melissa A Marchal - Department of Biology, University of Iowa, Iowa City, IA 52242, USA
Douglas W Houston - Department of Biology, University of Iowa, Iowa City, IA 52242, USA
Michael D Sheets - Department of Biomolecular Chemistry, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI 53706, USA mdsheets@wisc.edu
Resource Type: Journal article
Publication Details: Development (Cambridge), Vol.143(5), pp.864-871
DOI: 10.1242/dev.131359
PMID: 26811381
PMCID: PMC4813341
NLM abbreviation: Development
ISSN: 1477-9129
eISSN: 1477-9129
Publisher: England
Grant note: R01 GM083999 / NIGMS NIH HHS R01GM083999 / NIGMS NIH HHS
Language: English
Date published: 03/01/2016
Academic Unit: Pathology; Biology
Record Identifier: 9983991964002771

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