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Anchor cell signaling and vulval precursor cell positioning establish a reproducible spatial context during C. elegans vulval induction

Grimbert, Stéphanie and Tietze, Kyria and Barkoulas, Michalis and Sternberg, Paul W. and Félix, Marie-Anne and Braendle, Christian (2016) Anchor cell signaling and vulval precursor cell positioning establish a reproducible spatial context during C. elegans vulval induction. Developmental Biology, 416 (1). pp. 123-135. ISSN 0012-1606. http://resolver.caltech.edu/CaltechAUTHORS:20160620-132014255

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Abstract

How cells coordinate their spatial positioning to successfully communicate is poorly understood. Here we address this topic using C. elegans vulval patterning during which hypodermal vulval precursor cells (VPCs) adopt distinct cell fates determined by their relative positions to the gonadal anchor cell (AC). LIN-3/EGF signaling by the AC induces the central VPC, P6.p, to adopt a 1° vulval fate. Exact alignment of AC and VPCs is thus critical for correct fate patterning, yet, as we show here, the initial AC-VPC positioning is both highly variable and asymmetric among individuals, with AC and P6.p only becoming aligned at the early L3 stage. Cell ablations and mutant analysis indicate that VPCs, most prominently 1° cells, move towards the AC. We identify AC-released LIN-3/EGF as a major attractive signal, which therefore plays a dual role in vulval patterning (cell alignment and fate induction). Additionally, compromising Wnt pathway components also induces AC-VPC alignment errors, with loss of posterior Wnt signaling increasing stochastic vulval centering on P5.p. Our results illustrate how intercellular signaling reduces initial spatial variability in cell positioning to generate reproducible interactions across tissues.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.ydbio.2016.05.036DOIArticle
http://www.sciencedirect.com/science/article/pii/S0012160616300963PublisherArticle
ORCID:
AuthorORCID
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2016 Elsevier Inc. Received date: 22 February 2016; Revised date: 5 April 2016; Accepted date: 31 May 2016. CB acknowledges financial support by the Centre National de la Recherche Scientifique (CNRS), the Agence Nationale de la Recherche, the Fondation ARC pour la Recherche sur le Cancer, and the Fondation Schlumberger pour l’Education et la Recherche. SG was supported by fellowships from the Ministère de l’Enseignement Supérieur et de la Recherche and the Fondation ARC pour la Recherche sur le Cancer. MAF acknowledges funding provided by the Agence Nationale de la Recherche (ANR12-BSV2-0004-01 and ANR10-LABX-54 MEMOLIFE) and the Bettencourt Schueller Foundation (Coup d’Elan 2011). MB was supported by a postdoctoral fellowship from the Fondation pour la Recherche Médicale. Author contributions: Conceived and designed the experiments: CB, MAF, PWS. Performed the experiments: SG, KT, MB. Analyzed the data: CB, SG. Wrote the paper: CB, MAF, SG. Competing Interests: None.
Funders:
Funding AgencyGrant Number
Centre National de la Recherche Scientifique (CNRS)UNSPECIFIED
Fondation ARC pour la Recherche sur le CancerUNSPECIFIED
Fondation Schlumberger pour l’Education et la RechercheUNSPECIFIED
Ministère de l’Enseignement Supérieur et de la RechercheUNSPECIFIED
Agence Nationale de la Recherche (ANR)ANR12-BSV2-0004-01
Agence Nationale de la Recherche (ANR)ANR10-LABX-54 MEMOLIFE
Bettencourt Schueller FoundationUNSPECIFIED
Fondation pour la Recherche MédicaleUNSPECIFIED
Record Number:CaltechAUTHORS:20160620-132014255
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160620-132014255
Official Citation:Stéphanie Grimbert, Kyria Tietze, Michalis Barkoulas, Paul W. Sternberg, Marie-Anne Félix, Christian Braendle, Anchor cell signaling and vulval precursor cell positioning establish a reproducible spatial context during C. elegans vulval induction, Developmental Biology, Volume 416, Issue 1, 1 August 2016, Pages 123-135, ISSN 0012-1606, http://dx.doi.org/10.1016/j.ydbio.2016.05.036. (http://www.sciencedirect.com/science/article/pii/S0012160616300963)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:68535
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:21 Jun 2016 23:54
Last Modified:09 Sep 2016 18:20

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