title: A dynamic intracellular distribution of Vangl2 accompanies cell polarization during zebrafish gastrulation.
abstract: During vertebrate gastrulation, convergence and extension movements elongate embryonic tissues anteroposteriorly and narrow them mediolaterally. Planar cell polarity (PCP) signaling is essential for mediolateral cell elongation underlying these movements, but how this polarity arises is poorly understood. We analyzed the elongation, orientation and migration behaviors of lateral mesodermal cells undergoing convergence and extension movements in wild-type zebrafish embryos and mutants for the Wnt/PCP core component Vangl2 (Trilobite). We demonstrate that Vangl2 function is required at the time when cells transition to a highly elongated and mediolaterally aligned body. vangl2 mutant cells fail to undergo this transition and to migrate along a straight path with high net speed towards the dorsal midline. Instead, vangl2 mutant cells exhibit an anterior/animal pole bias in cell body alignment and movement direction, suggesting that PCP signaling promotes effective dorsal migration in part by suppressing anterior/animalward cell polarity and movement. Endogenous Vangl2 protein accumulates at the plasma membrane of mesenchymal converging cells at the time its function is required for mediolaterally polarized cell behavior. Heterochronic cell transplantations demonstrated that Vangl2 cell membrane accumulation is stage dependent and regulated by both intrinsic factors and an extracellular signal, which is distinct from PCP signaling or other gastrulation regulators, including BMP and Nodals. Moreover, mosaic expression of fusion proteins revealed enrichment of Vangl2 at the anterior cell edges of highly mediolaterally elongated cells. These results demonstrate that the dynamic Vangl2 intracellular distribution is coordinated with and necessary for the changes in convergence and extension cell behaviors during gastrulation.
authors.affiliation: Department of Developmental Biology, Washington University School of Medicine in St Louis, St Louis, MO 63110, USA.
authors.forename: Isabelle
authors.initials: I
authors.lastname: Roszko
authors.affiliation: Department of Developmental Biology, Washington University School of Medicine in St Louis, St Louis, MO 63110, USA.
authors.forename: Diane
authors.initials: D
authors.lastname: S Sepich
authors.affiliation: Department of Biology, Middle Tennessee State University, Murfreesboro, TN 37130, USA.
authors.forename: Jason R
authors.initials: JR
authors.lastname: Jessen
authors.affiliation: Division of Biological Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Anand
authors.initials: A
authors.lastname: Chandrasekhar
authors.affiliation: Department of Developmental Biology, Washington University School of Medicine in St Louis, St Louis, MO 63110, USA solnical@wustl.edu.
authors.forename: Lilianna
authors.initials: L
authors.lastname: Solnica-Krezel
mesh_terms: D000818:Animals; D019521:Body Patterning; D019070:Cell Lineage; D002462:Cell Membrane / Q000378:metabolism; D002465:Cell Movement; D016764:Cell Polarity / Q000502:physiology; D003593:Cytoplasm / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000378:metabolism; D005260:Female; D005775:Gastrula / Q000502:physiology*; D054262:Gastrulation; D018507:Gene Expression Regulation, Developmental; D008565:Membrane Proteins / Q000378:metabolism / Q000502:physiology*; D008648:Mesoderm / Q000378:metabolism; D009154:Mutation; D054258:Neural Plate / Q000378:metabolism; D015398:Signal Transduction; D051153:Wnt Proteins / Q000378:metabolism; D015027:Zebrafish; D029961:Zebrafish Proteins / Q000378:metabolism / Q000502:physiology*
chemical_list: D008565:Membrane Proteins; D051153:Wnt Proteins; D029961:Zebrafish Proteins; C491759:vangl2 protein, zebrafish
keywords: Cell movement; Cell polarity; Gastrulation; Vangl2; Wnt/PCP; Zebrafish