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A Regulatory Gene Network That Directs Micromere Specification in the Sea Urchin Embryo

Oliveri, Paola and Carrick, Deanna M. and Davidson, Eric H. (2002) A Regulatory Gene Network That Directs Micromere Specification in the Sea Urchin Embryo. Developmental Biology, 246 (1). pp. 209-228. ISSN 0012-1606. https://resolver.caltech.edu/CaltechAUTHORS:20160121-071018052

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Abstract

Micromeres and their immediate descendants have three known developmental functions in regularly developing sea urchins: immediately after their initial segregation, they are the source of an unidentified signal to the adjacent veg2 cells that is required for normal endomesodermal specification; a few cleavages later, they express Delta, a Notch ligand which triggers the conditional specification of the central mesodermal domain of the vegetal plate; and they exclusively give rise to the skeletogenic mesenchyme of the postgastrular embryo. We demonstrate the key components of the zygotic regulatory gene network that accounts for micromere specificity. This network is a subelement of the overall endomesoderm specification network of the Strongylocentrotus purpuratus embryo. A central role is played by a newly discovered gene encoding a paired class homeodomain transcription factor which in micromeres acts as a repressor of a repressor: the gene is named pmar1 (paired-class micromere anti-repressor). pmar1 is expressed only during cleavage and early blastula stages, and exclusively in micromeres. It is initially activated as soon as the micromeres are formed, in response to Otx and β-Catenin/Tcf inputs. The repressive nature of the interactions mediated by the pmar1 gene product was shown by the identical effect of introducing mRNA encoding the Pmar1 factor, and mRNA encoding an Engrailed-Pmar1 (En-Pmar1) repressor domain fusion. In both cases, the effects are derepression: of the delta gene; and of skeletogenic genes, including several transcription factors normally expressed only in micromere descendants, and also a set of downstream skeletogenic differentiation genes. The spatial phenotype of embryos bearing exogenous mRNA encoding Pmar1 factor or En-Pmar1 is expansion of the domains of expression of the downstream genes over most or all of the embryo. This results in transformation of much of the embryo into skeletogenic mesenchyme cells that express skeletogenic markers. The normal role of pmarl is to prevent, exclusively in the micromeres, the expression of a repressor that is otherwise operative throughout the embryo. This function accounts for the localization of delta transcription in micromeres, and thereby for the conditional specification of the vegetal plate mesoderm. It also explains why skeletogenic differentiation gene batteries normally function only in micromere descendants. More generally, the regulatory network subelement emerging from this work shows how the specificity of micromere function depends on continuing global regulatory interactions, as well as on early localized inputs.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1006/dbio.2002.0627DOIArticle
http://www.sciencedirect.com/science/article/pii/S0012160602906275PublisherArticle
Additional Information:© 2002 Elsevier Science. Received for publication January 3, 2002. Revised February 13, 2002. Accepted February 13, 2002. Available online 23 May 2002. We thank Dr. David R. McClay of Duke University and Dr. Ellen Rothenberg of Caltech for critical reviews of the manuscript. We are pleased to acknowledge the extremely useful technical assistance of Özlem Yüce in the summer of 2001, and the generosity of Hyla Sweet in providing us with a cDNA probe for Spdelta. This research was supported by NIH HD-37105, and by the Stowers Institute for Medical Research.
Funders:
Funding AgencyGrant Number
NIHHD-37105
Stowers Institute for Medical ResearchUNSPECIFIED
Subject Keywords:sea urchin embryo; homeodomain; pmar1; tbrain; delta; gene regulatory network
Issue or Number:1
Record Number:CaltechAUTHORS:20160121-071018052
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160121-071018052
Official Citation:Paola Oliveri, Deanna M. Carrick, Eric H. Davidson, A Regulatory Gene Network That Directs Micromere Specification in the Sea Urchin Embryo, Developmental Biology, Volume 246, Issue 1, 1 June 2002, Pages 209-228, ISSN 0012-1606, http://dx.doi.org/10.1006/dbio.2002.0627. (http://www.sciencedirect.com/science/article/pii/S0012160602906275)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:63819
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:21 Jan 2016 19:15
Last Modified:03 Oct 2019 09:31

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