Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis

Development. 2003 Oct;130(20):4847-58. doi: 10.1242/dev.00698. Epub 2003 Aug 20.

Abstract

To gain insight into the molecular mechanisms underlying the control of morphogenetic signals by H+ flux during embryogenesis, we tested Fusicoccin-A (FC), a compound produced by the fungus Fusicoccum amygdali Del. In plant cells, FC complexes with 14-3-3 proteins to activate H+ pumping across the plasma membrane. It has long been thought that FC acts on higher plants only; here, we show that exposing frog embryos to FC during early development specifically results in randomization of the asymmetry of the left-right (LR) axis (heterotaxia). Biochemical and molecular-genetic evidence is presented that 14-3-3-family proteins are an obligate component of Xenopus FC receptors and that perturbation of 14-3-3 protein function results in heterotaxia. The subcellular localization of 14-3-3 mRNAs and proteins reveals novel cytoplasmic destinations, and a left-right asymmetry at the first cell division. Using gain-of-function and loss-of-function experiments, we show that 14-3-3E protein is likely to be an endogenous and extremely early aspect of LR patterning. These data highlight a striking conservation of signaling pathways across kingdoms, suggest common mechanisms of polarity establishment between C. elegans and vertebrate embryos, and uncover a novel entry point into the pathway of left-right asymmetry determination.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • 14-3-3 Proteins
  • Animals
  • Body Patterning / physiology*
  • Embryo, Nonmammalian / physiology*
  • Glycosides / metabolism*
  • Signal Transduction / physiology*
  • Transforming Growth Factor beta / metabolism
  • Tyrosine 3-Monooxygenase / metabolism*
  • Xenopus
  • Xenopus Proteins

Substances

  • 14-3-3 Proteins
  • Glycosides
  • Transforming Growth Factor beta
  • Xenopus Proteins
  • nodal1 protein, Xenopus
  • fusicoccin
  • Tyrosine 3-Monooxygenase