Spatially restricted translation of the xCR1 mRNA in Xenopus embryos

Mol Cell Biol. 2009 Jul;29(13):3791-802. doi: 10.1128/MCB.01865-08. Epub 2009 Apr 13.

Abstract

The xCR1 protein is a maternal determinant and cofactor for nodal signaling in vertebrate embryos. The xCR1 protein accumulates specifically in the animal cells of Xenopus embryos, but maternal xCR1 mRNA is distributed equally throughout all embryonic cells. Here, we show that vegetal cell-specific translational repression of xCR1 mRNA contributes to this spatially restricted accumulation of the xCR1 protein in Xenopus embryos. xCR1 mRNA was associated with polyribosomes in animal cells but not vegetal cells. A 351-nucleotide region of xCR1 mRNA's 3' untranslated region was sufficient to confer a spatially restricted pattern of translation to a luciferase reporter mRNA by repressing translation in vegetal cells. Repression depended upon the mRNA's 5' cap but not its 3' poly(A) tail. Furthermore, the region of xCR1 mRNA sufficient to confer vegetal cell-specific repression contained both Pumilio binding elements (PBEs) and binding sites for the CUG-BP1 protein. The PBEs and the CUG-BP1 sites were necessary but not sufficient for translation repression. Our studies of xCR1 mRNA document the first example of spatially regulated translation in controlling the asymmetric distribution of a maternal determinant in vertebrates.

Publication types

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

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Base Sequence
  • Cell Polarity
  • Gene Expression Regulation, Developmental*
  • Genes, Reporter
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Molecular Sequence Data
  • Oocytes / cytology
  • Oocytes / physiology
  • Poly A / genetics
  • Poly A / metabolism
  • Polyribosomes / genetics
  • Polyribosomes / metabolism
  • Protein Biosynthesis*
  • RNA Caps / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism*
  • Xenopus laevis / anatomy & histology*
  • Xenopus laevis / embryology*
  • Xenopus laevis / physiology

Substances

  • 3' Untranslated Regions
  • Membrane Proteins
  • PUM1 protein, Xenopus
  • RNA Caps
  • RNA, Messenger
  • RNA-Binding Proteins
  • Xenopus Proteins
  • tdgf1.3 protein, Xenopus
  • Poly A