The prickle-related gene in vertebrates is essential for gastrulation cell movements

Curr Biol. 2003 Apr 15;13(8):674-9. doi: 10.1016/s0960-9822(03)00245-8.

Abstract

Involving dynamic and coordinated cell movements that cause drastic changes in embryo shape, gastrulation is one of the most important processes of early development. Gastrulation proceeds by various types of cell movements, including convergence and extension, during which polarized axial mesodermal cells intercalate in radial and mediolateral directions and thus elongate the dorsal marginal zone along the anterior-posterior axis [1,2]. Recently, it was reported that a noncanonical Wnt signaling pathway, which is known to regulate planar cell polarity (PCP) in Drosophila [3,4], participates in the regulation of convergent extension movements in Xenopus as well as in the zebrafish embryo [5-8]. The Wnt5a/Wnt11 signal is mediated by members of the seven-pass transmembrane receptor Frizzled (Fz) and the signal transducer Dishevelled (Dsh) through the Dsh domains that are required for the PCP signal [6-8]. It has also been shown that the relocalization of Dsh to the cell membrane is required for convergent extension movements in Xenopus gastrulae. Although it appears that signaling via these components leads to the activation of JNK [9,10] and rearrangement of microtubules, the precise interplay among these intercellular components is largely unknown. In this study, we show that Xenopus prickle (Xpk), a Xenopus homolog of a Drosophila PCP gene [11-13], is an essential component for gastrulation cell movement. Both gain-of-function and loss-of-function of Xpk severely perturbed gastrulation and caused spina bifida embryos without affecting mesodermal differentiation. We also demonstrate that XPK binds to Xenopus Dsh as well as to JNK. This suggests that XPK plays a pivotal role in connecting Dsh function to JNK activation.

Publication types

  • Comparative Study

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Blotting, Northern
  • Cell Movement / genetics
  • Cell Movement / physiology*
  • DNA-Binding Proteins / genetics*
  • Dishevelled Proteins
  • Drosophila Proteins / genetics*
  • Frizzled Receptors
  • Gastrula / metabolism
  • Gastrula / physiology*
  • Glycoproteins / metabolism
  • Immunohistochemistry
  • In Situ Hybridization
  • JNK Mitogen-Activated Protein Kinases
  • LIM Domain Proteins
  • Mitogen-Activated Protein Kinases / metabolism
  • Phosphoproteins / metabolism
  • Precipitin Tests
  • Proteins / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology*
  • Wnt Proteins
  • Wnt-5a Protein
  • Xenopus Proteins
  • Xenopus laevis / embryology*

Substances

  • Adaptor Proteins, Signal Transducing
  • DNA-Binding Proteins
  • DVL1 protein, Xenopus
  • Dishevelled Proteins
  • Drosophila Proteins
  • Frizzled Receptors
  • Glycoproteins
  • LIM Domain Proteins
  • Phosphoproteins
  • Proteins
  • Proto-Oncogene Proteins
  • WNT5A protein, human
  • Wnt Proteins
  • Wnt-5a Protein
  • Xenopus Proteins
  • dsh protein, Drosophila
  • pk protein, Drosophila
  • wnt11b protein, Xenopus
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinases