A biphasic role of non-canonical Wnt16 signaling during early anterior-posterior patterning and morphogenesis of the sea urchin embryo

Development. 2019 Dec 16;146(24):dev168799. doi: 10.1242/dev.168799.

Abstract

A Wnt signaling network governs early anterior-posterior (AP) specification and patterning of the deuterostome sea urchin embryo. We have previously shown that non-canonical Fzl1/2/7 signaling antagonizes the progressive posterior-to-anterior downregulation of the anterior neuroectoderm (ANE) gene regulatory network (GRN) by canonical Wnt/β-catenin and non-canonical Wnt1/Wnt8-Fzl5/8-JNK signaling. This study focuses on the non-canonical function of the Wnt16 ligand during early AP specification and patterning. Maternally supplied wnt16 is expressed ubiquitously during cleavage and zygotic wnt16 expression is concentrated in the endoderm/mesoderm beginning at mid-blastula stage. Wnt16 antagonizes the ANE restriction mechanism and this activity depends on a functional Fzl1/2/7 receptor. Our results also show that zygotic wnt16 expression depends on both Fzl5/8 and Wnt/β-catenin signaling. Furthermore, Wnt16 is necessary for the activation and/or maintenance of key regulatory endoderm/mesoderm genes and is essential for gastrulation. Together, our data show that Wnt16 has two functions during early AP specification and patterning: (1) an initial role activating the Fzl1/2/7 pathway that antagonizes the ANE restriction mechanism; and (2) a subsequent function in activating key endoderm GRN factors and the morphogenetic movements of gastrulation.

Keywords: Anterior-posterior; Deuterostome evolution; Frizzled; Gene regulatory networks; Wnt signal transduction; Wnt16.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / genetics*
  • Embryo, Nonmammalian
  • Frizzled Receptors / genetics
  • Frizzled Receptors / physiology
  • Gastrulation / genetics
  • Gene Expression Regulation, Developmental
  • Mesoderm / embryology
  • Mesoderm / metabolism
  • Morphogenesis / genetics*
  • Neural Plate / embryology
  • Neural Plate / metabolism
  • Sea Urchins* / embryology
  • Sea Urchins* / genetics
  • Wnt Proteins / genetics
  • Wnt Proteins / physiology*
  • Wnt Signaling Pathway / physiology

Substances

  • Frizzled Receptors
  • Wnt Proteins