Nuclear β-catenin-dependent Wnt8 signaling in vegetal cells of the early sea urchin embryo regulates gastrulation and differentiation of endoderm and mesodermal cell lineages

Athula Wikramanayake, Robert Peterson, Jing Chen, Ling Huang, Joanna M. Bince, David R. McClay, William H. Klein

Research output: Contribution to journalArticle

93 Citations (Scopus)

Abstract

The entry of β-catenin into vegetal cell nuclei beginning at the 16-cell stage is one of the earliest known molecular asymmetries seen along the animal-vegetal axis in the sea urchin embryo. Nuclear β-catenin activates a vegetal signaling cascade that mediates micromere specification and specification of the endomesoderm in the remaining cells of the vegetal half of the embryo. Only a few potential target genes of nuclear β-catenin have been functionally analyzed in the sea urchin embryo. Here, we show that SpWnt8, a Wnt8 homolog from Strongylocentrotus purpuratus, is zygotically activated specifically in 16-cell-stage micromeres in a nuclear β-catenin-dependent manner, and its expression remains restricted to the micromeres until the 60-cell stage. At the late 60-cell stage nuclear β-catenin-dependent SpWnt8 expression expands to the veg2 cell tier. SpWnt8 is the only signaling molecule thus far identified with expression localized to the 16-60-cell stage micromeres and the veg2 tier. Overexpression of SpWnt8 by mRNA microinjection produced embryos with multiple invagination sites and showed that, consistent with its localization, SpWnt8 is a strong inducer of endoderm. Blocking SpWnt8 function using SpWnt8 morpholino antisense oligonucleotides produced embryos that formed micromeres that could transmit the early endomesoderm-inducing signal, but these cells failed to differentiate as primary mesenchyme cells. SpWnt8-morpholino embryos also did not form endoderm, or secondary mesenchyme-derived pigment and muscle cells, indicating a role for SpWnt8 in gastrulation and in the differentiation of endomesodermal lineages. These establish SpWnt8 as a critical component of the endomesoderm regulatory network in the sea urchin embryo.

Original languageEnglish
Pages (from-to)194-205
Number of pages12
JournalGenesis
Volume39
Issue number3
DOIs
StatePublished - Jul 1 2004
Externally publishedYes

Fingerprint

Catenins
Gastrulation
Endoderm
Sea Urchins
Cell Lineage
Embryonic Structures
Morpholinos
Mesoderm
Strongylocentrotus purpuratus
Antisense Oligonucleotides
Microinjections
Cell Nucleus
Muscle Cells
Messenger RNA

Keywords

  • Differentiation
  • Embryo
  • Endomesoderm
  • Gastrulation
  • Primary mesenchyme cells
  • Sea urchin
  • Wnt8

ASJC Scopus subject areas

  • Genetics

Cite this

Nuclear β-catenin-dependent Wnt8 signaling in vegetal cells of the early sea urchin embryo regulates gastrulation and differentiation of endoderm and mesodermal cell lineages. / Wikramanayake, Athula; Peterson, Robert; Chen, Jing; Huang, Ling; Bince, Joanna M.; McClay, David R.; Klein, William H.

In: Genesis, Vol. 39, No. 3, 01.07.2004, p. 194-205.

Research output: Contribution to journalArticle

Wikramanayake, Athula ; Peterson, Robert ; Chen, Jing ; Huang, Ling ; Bince, Joanna M. ; McClay, David R. ; Klein, William H. / Nuclear β-catenin-dependent Wnt8 signaling in vegetal cells of the early sea urchin embryo regulates gastrulation and differentiation of endoderm and mesodermal cell lineages. In: Genesis. 2004 ; Vol. 39, No. 3. pp. 194-205.
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