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FGF signaling regulates Wnt ligand expression to control vulval cell lineage polarity in C. elegans

Minor, Paul J. and He, Ting-Fang and Sohn, Chang Ho and Asthagiri, Anand R. and Sternberg, Paul W. (2013) FGF signaling regulates Wnt ligand expression to control vulval cell lineage polarity in C. elegans. Development, 140 (18). pp. 3882-3891. ISSN 0950-1991. PMCID PMC3754481. doi:10.1242/dev.095687.

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The interpretation of extracellular cues leading to the polarization of intracellular components and asymmetric cell divisions is a fundamental part of metazoan organogenesis. The Caenorhabditis elegans vulva, with its invariant cell lineage and interaction of multiple cell signaling pathways, provides an excellent model for the study of cell polarity within an organized epithelial tissue. Here, we show that the fibroblast growth factor (FGF) pathway acts in concert with the Frizzled homolog LIN-17 to influence the localization of SYS-1, a component of the Wnt/β-catenin asymmetry pathway, indirectly through the regulation of cwn-1. The source of the FGF ligand is the primary vulval precursor cell (VPC) P6.p, which controls the orientation of the neighboring secondary VPC P7.p by signaling through the sex myoblasts (SMs), activating the FGF pathway. The Wnt CWN-1 is expressed in the posterior body wall muscle of the worm as well as in the SMs, making it the only Wnt expressed on the posterior and anterior sides of P7.p at the time of the polarity decision. Both sources of cwn-1 act instructively to influence P7.p polarity in the direction of the highest Wnt signal. Using single molecule fluorescence in situ hybridization, we show that the FGF pathway regulates the expression of cwn-1 in the SMs. These results demonstrate an interaction between FGF and Wnt in C. elegans development and vulval cell lineage polarity, and highlight the promiscuous nature of Wnts and the importance of Wnt gradient directionality within C. elegans.

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Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2013. Published by The Company of Biologists Ltd. Accepted 3 July 2013. Posted online before print August 14, 2013. We thank Takao Inoue, Jennifer Green, Wendy Katz, Adeline Seah and Michael Stern for insightful comments and laying the groundwork for this project; Long Cai for use of his microscope for FISH; Gladys Medina and Barbara Perry for technical assistance; and members of the Sternberg laboratory, especially Mihoko Kato, Amir Sapir, James Lee and Hillel Schwartz, for helpful discussions and critically reading the manuscript. We thank WormBase and the Caenorhabditis Genetics Center. Funding: P.J.M. was supported by a National Institutes of Health (NIH) United States Public Health Service Training Grant [T32GM07616]; and the Howard Hughes Medical Institute (HHMI). P.W.S. is an HHMI investigator. T.-F.H. and C.H.S. were supported by the NIH [R01 HD075605 to Long Cai]. Deposited in PMC for release after 6 months. Author contributions: P.J.M., A.A. and P.W.S. conceived the experiments. P.J.M. carried out all the experiments with help from T.-F.H. and C.H.S. for the FISH experiments. P.J.M. and P.W.S. wrote the manuscript.
Funding AgencyGrant Number
NIH Predoctoral FellowshipT32GM07616
NIHR01 HD075605
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:FGF, Wnt, C. elegans, Vulval development, Cell polarity
Issue or Number:18
PubMed Central ID:PMC3754481
Record Number:CaltechAUTHORS:20130920-074404035
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:41431
Deposited By: Tony Diaz
Deposited On:20 Sep 2013 19:27
Last Modified:10 Nov 2021 04:30

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