Anchor cell signaling and vulval precursor cell positioning establish a reproducible spatial context during C. elegans vulval induction
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.
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.Attached Files
Supplemental Material - mmc1.pdf
Supplemental Material - mmc2.pdf
Supplemental Material - mmc3.xlsx
Supplemental Material - mmc4.xlsx
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Additional details
- Eprint ID
- 68535
- Resolver ID
- CaltechAUTHORS:20160620-132014255
- Centre National de la Recherche Scientifique (CNRS)
- Fondation ARC pour la Recherche sur le Cancer
- Fondation Schlumberger pour l'Education et la Recherche
- Ministère de l'Enseignement Supérieur et de la Recherche
- Agence Nationale de la Recherche (ANR)
- ANR12-BSV2-0004-01
- Agence Nationale de la Recherche (ANR)
- ANR10-LABX-54 MEMOLIFE
- Bettencourt Schueller Foundation
- Fondation pour la Recherche Médicale
- Created
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2016-06-21Created from EPrint's datestamp field
- Updated
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2021-11-11Created from EPrint's last_modified field