Symmetry breakage in the frog Xenopus: role of Rab11 and the ventral-right blastomere

Genesis. 2014 Jun;52(6):588-99. doi: 10.1002/dvg.22766. Epub 2014 Mar 14.

Abstract

Vertebrates display asymmetric arrangements of inner organs such as heart and stomach. The Nodal signaling cascade in the left lateral plate mesoderm in all cases directs asymmetric morphogenesis and placement during organogenesis. Mechanisms that lead up to left-asymmetric Nodal induction seem to differ between the vertebrates. Cilia produce a leftward extracellular fluid flow in zebrafish, medaka, mouse, rabbit, and Xenopus embryos during neurulation. In Xenopus, earlier asymmetric cues were described. Some, such as Rab11, apparently act in the zygote. Others were efficiently manipulated in ventral-right cells at the four-cell stage, a lineage presumably independent of the ciliated gastrocoel roof plate (GRP) during neurulation. Here, we show that one- and four-cell manipulations of Rab11 showed equal low efficiencies of left-right disturbances. We also reevaluated the lineage of the GRP. By tracing back future ciliated cells from the gastrula to the four-cell stage, we show that ventral cells contribute to ciliated sensory cells at the border of the GRP. Knockdown of the Nodal inhibitor Coco in the ventral right lineage resulted in embryos with ectopic right-sided Nodal and Pitx2c expression. Together, these experiments support a cilia-based mechanism of symmetry breakage in the frog Xenopus.

Keywords: Coco; Nodal cascade; Rab11; Xenopus; cilia; leftward flow.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blastomeres / metabolism*
  • Body Patterning / physiology*
  • Gastrula / embryology
  • Gastrula / metabolism
  • Gene Expression Regulation, Developmental
  • Gene Knockdown Techniques
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Mesoderm / embryology
  • Mesoderm / metabolism
  • Xenopus / embryology*
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism
  • rab GTP-Binding Proteins / genetics*
  • rab GTP-Binding Proteins / metabolism

Substances

  • DAND5 protein, Xenopus
  • Homeodomain Proteins
  • Pitx2c protein, Xenopus
  • Xenopus Proteins
  • rab11 protein
  • rab GTP-Binding Proteins