GSK3beta/shaggy mediates patterning along the animal-vegetal axis of the sea urchin embryo

Development. 1998 Jul;125(13):2489-98. doi: 10.1242/dev.125.13.2489.

Abstract

In the sea urchin embryo, the animal-vegetal axis is defined before fertilization and different embryonic territories are established along this axis by mechanisms which are largely unknown. Significantly, the boundaries of these territories can be shifted by treatment with various reagents including zinc and lithium. We have isolated and characterized a sea urchin homolog of GSK3beta/shaggy, a lithium-sensitive kinase which is a component of the Wnt pathway and known to be involved in axial patterning in other embryos including Xenopus. The effects of overexpressing the normal and mutant forms of GSK3beta derived either from sea urchin or Xenopus were analyzed by observation of the morphology of 48 hour embryos (pluteus stage) and by monitoring spatial expression of the hatching enzyme (HE) gene, a very early gene whose expression is restricted to an animal domain with a sharp border roughly coinciding with the future ectoderm / endoderm boundary. Inactive forms of GSK3beta predicted to have a dominant-negative activity, vegetalized the embryo and decreased the size of the HE expression domain, apparently by shifting the boundary towards the animal pole. These effects are similar to, but even stronger than, those of lithium. Conversely, overexpression of wild-type GSK3beta animalized the embryo and caused the HE domain to enlarge towards the vegetal pole. Unlike zinc treatment, GSK3beta overexpression thus appeared to provoke a true animalization, through extension of the presumptive ectoderm territory. These results indicate that in sea urchin embryos the level of GSKbeta activity controls the position of the boundary between the presumptive ectoderm and endoderm territories and thus, the relative extent of these tissue layers in late embryos. GSK3beta and probably other downstream components of the Wnt pathway thus mediate patterning both along the primary AV axis of the sea urchin embryo and along the dorsal-ventral axis in Xenopus, suggesting a conserved basis for axial patterning between invertebrate and vertebrate in deuterostomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Blastocyst / physiology
  • Body Patterning*
  • Calcium-Calmodulin-Dependent Protein Kinases / biosynthesis
  • Calcium-Calmodulin-Dependent Protein Kinases / chemistry
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism*
  • Cloning, Molecular
  • DNA Primers
  • Drosophila
  • Drosophila Proteins*
  • Embryo, Nonmammalian / physiology
  • Gene Expression Regulation, Developmental
  • Glycogen Synthase Kinase 3
  • Humans
  • Microtubule-Associated Proteins / metabolism
  • Molecular Sequence Data
  • Polymerase Chain Reaction
  • Protein Serine-Threonine Kinases / biosynthesis
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / metabolism*
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / metabolism
  • Sea Urchins / embryology*
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Xenopus

Substances

  • DNA Primers
  • Drosophila Proteins
  • Microtubule-Associated Proteins
  • Recombinant Proteins
  • Protein Serine-Threonine Kinases
  • Sgg protein, Drosophila
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Glycogen Synthase Kinase 3

Associated data

  • GENBANK/AJ222641