Planar cell polarity proteins differentially regulate extracellular matrix organization and assembly during zebrafish gastrulation
- PMID: 24021482
- DOI: 10.1016/j.ydbio.2013.08.027
Planar cell polarity proteins differentially regulate extracellular matrix organization and assembly during zebrafish gastrulation
Abstract
Zebrafish gastrulation cell movements occur in the context of dynamic changes in extracellular matrix (ECM) organization and require the concerted action of planar cell polarity (PCP) proteins that regulate cell elongation and mediolateral alignment. Data obtained using Xenopus laevis gastrulae have shown that integrin-fibronectin interactions underlie the formation of polarized cell protrusions necessary for PCP and have implicated PCP proteins themselves as regulators of ECM. By contrast, the relationship between establishment of PCP and ECM assembly/remodeling during zebrafish gastrulation is unclear. We previously showed that zebrafish embryos carrying a null mutation in the four-pass transmembrane PCP protein vang-like 2 (vangl2) exhibit increased matrix metalloproteinase activity and decreased immunolabeling of fibronectin. These data implicated for the first time a core PCP protein in the regulation of pericellular proteolysis of ECM substrates and raised the question of whether other zebrafish PCP proteins also impact ECM organization. In Drosophila melanogaster, the cytoplasmic PCP protein Prickle binds Van Gogh and regulates its function. Here we report that similar to vangl2, loss of zebrafish prickle1a decreases fibronectin protein levels in gastrula embryos. We further show that Prickle1a physically binds Vangl2 and regulates both the subcellular distribution and total protein level of Vangl2. These data suggest that the ability of Prickle1a to impact fibronectin organization is at least partly due to effects on Vangl2. In contrast to loss of either Vangl2 or Prickle1a function, we find that glypican4 (a Wnt co-receptor) and frizzled7 mutant gastrula embryos with disrupted non-canonical Wnt signaling exhibit the opposite phenotype, namely increased fibronectin assembly. Our data show that glypican4 mutants do not have decreased proteolysis of ECM substrates, but instead have increased cell surface cadherin protein expression and increased intercellular adhesion. These data indicate that Wnt/Glypican4/Frizzled signaling regulates ECM assembly through effects on cadherin-mediated cell cohesion. Together, our results demonstrate that zebrafish Vangl2/Prickle1a and non-canonical Wnt/Frizzled signaling have opposing effects on ECM organization underlying PCP and gastrulation cell movements.
Keywords: Cadherins; Fibronectin; Gastrulation; Metalloproteinases; Polarity; Zebrafish.
© 2013 Elsevier Inc. All rights reserved.
Similar articles
-
VANGL2 regulates membrane trafficking of MMP14 to control cell polarity and migration.J Cell Sci. 2012 May 1;125(Pt 9):2141-7. doi: 10.1242/jcs.097964. Epub 2012 Feb 22. J Cell Sci. 2012. PMID: 22357946 Free PMC article.
-
A dynamic intracellular distribution of Vangl2 accompanies cell polarization during zebrafish gastrulation.Development. 2015 Jul 15;142(14):2508-20. doi: 10.1242/dev.119032. Epub 2015 Jun 10. Development. 2015. PMID: 26062934 Free PMC article.
-
The PDZ domain protein Mcc is a novel effector of non-canonical Wnt signaling during convergence and extension in zebrafish.Development. 2014 Sep;141(18):3505-16. doi: 10.1242/dev.114033. Development. 2014. PMID: 25183869
-
WNT/PCP signaling pathway and human cancer (review).Oncol Rep. 2005 Dec;14(6):1583-8. Oncol Rep. 2005. PMID: 16273260 Review.
-
Core pathway proteins and the molecular basis of planar polarity in the zebrafish gastrula.Semin Cell Dev Biol. 2022 May;125:17-25. doi: 10.1016/j.semcdb.2021.09.015. Epub 2021 Oct 8. Semin Cell Dev Biol. 2022. PMID: 34635444 Review.
Cited by
-
Cellular and molecular mechanisms of convergence and extension in zebrafish.Curr Top Dev Biol. 2020;136:377-407. doi: 10.1016/bs.ctdb.2019.08.001. Epub 2019 Sep 3. Curr Top Dev Biol. 2020. PMID: 31959296 Free PMC article. Review.
-
Noncanonical Wnt/Ror2 signaling regulates cell-matrix adhesion to prompt directional tumor cell invasion in breast cancer.Mol Biol Cell. 2022 Sep 15;33(11):ar103. doi: 10.1091/mbc.E22-02-0055. Epub 2022 Aug 24. Mol Biol Cell. 2022. PMID: 36001375 Free PMC article.
-
Tyrosine-Based Signals Regulate the Assembly of Daple⋅PARD3 Complex at Cell-Cell Junctions.iScience. 2020 Feb 21;23(2):100859. doi: 10.1016/j.isci.2020.100859. Epub 2020 Jan 22. iScience. 2020. PMID: 32058970 Free PMC article.
-
Planar cell polarity of the kidney.Exp Cell Res. 2016 May 1;343(2):258-266. doi: 10.1016/j.yexcr.2014.11.003. Epub 2014 Nov 13. Exp Cell Res. 2016. PMID: 25445789 Free PMC article. Review.
-
Wnt-frizzled planar cell polarity signaling in the regulation of cell motility.Curr Top Dev Biol. 2022;150:255-297. doi: 10.1016/bs.ctdb.2022.03.006. Epub 2022 May 25. Curr Top Dev Biol. 2022. PMID: 35817505 Free PMC article. Review.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases