Wbp2nl has a developmental role in establishing neural and non-neural ectodermal fates

Dev Biol. 2017 Sep 1;429(1):213-224. doi: 10.1016/j.ydbio.2017.06.025. Epub 2017 Jun 27.

Abstract

In many animals, maternally synthesized mRNAs are critical for primary germ layer formation. In Xenopus, several maternal mRNAs are enriched in the animal blastomere progenitors of the embryonic ectoderm. We previously identified one of these, WW-domain binding protein 2 N-terminal like (wbp2nl), that others previously characterized as a sperm protein (PAWP) that promotes meiotic resumption. Herein we demonstrate that it has an additional developmental role in regionalizing the embryonic ectoderm. Knock-down of Wbp2nl in the dorsal ectoderm reduced cranial placode and neural crest gene expression domains and expanded neural plate domains; knock-down in ventral ectoderm reduced epidermal gene expression. Conversely, increasing levels of Wbp2nl in the neural plate induced ectopic epidermal and neural crest gene expression and repressed many neural plate and cranial placode genes. The effects in the neural plate appear to be mediated, at least in part, by down-regulating chd, a BMP antagonist. Because the cellular function of Wbp2nl is not known, we mutated several predicted motifs. Expressing mutated proteins in embryos showed that a putative phosphorylation site at Thr45 and an α-helix in the PH-G domain are required to ectopically induce epidermal and neural crest genes in the neural plate. An intact YAP-binding motif also is required for ectopic epidermal gene expression as well as for down-regulating chd. This work reveals novel developmental roles for a cytoplasmic protein that promotes epidermal and neural crest formation at the expense of neural ectoderm.

Keywords: Neural crest; Neural plate; PAWP; Placodes; foxd3; zic2.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Bone Morphogenetic Proteins / metabolism
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • DNA-Binding Proteins
  • Ectoderm / embryology*
  • Ectoderm / metabolism*
  • Epidermis / embryology
  • Epidermis / metabolism
  • Gene Expression Regulation, Developmental
  • Mesoderm / embryology
  • Mesoderm / metabolism
  • Mutation / genetics
  • Nervous System / embryology*
  • Nervous System / metabolism*
  • Neural Crest / embryology
  • Neural Crest / metabolism
  • Neural Plate / embryology
  • Neural Plate / metabolism
  • Phenotype
  • Protein Domains
  • Protein Transport
  • Seminal Plasma Proteins / chemistry
  • Seminal Plasma Proteins / genetics
  • Seminal Plasma Proteins / metabolism*
  • Sequence Alignment
  • Xenopus Proteins / chemistry
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism*
  • Xenopus laevis / embryology*
  • Xenopus laevis / genetics
  • Xenopus laevis / metabolism*

Substances

  • Bone Morphogenetic Proteins
  • Carrier Proteins
  • DNA-Binding Proteins
  • Seminal Plasma Proteins
  • Wbp2nl protein, Xenopus
  • Xenopus Proteins