β-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo

Abstract

In sea urchin embryos, the animal-vegetal axis is specified during oogenesis. After fertilization, this axis is patterned to produce five distinct territories by the 60-cell stage. Territorial specification is thought to occur by a signal transduction cascade that is initiated by the large micromeres located at the vegetal pole. The molecular mechanisms that mediate the specification events along the animal-vegetal axis in sea urchin embryos are largely unknown. Nuclear ␤-catenin is seen in vegetal cells of the early embryo, suggesting that this protein plays a role in specifying vegetal cell fates. Here, we test this hypothesis and show that ␤-catenin is necessary for vegetal plate specification and is also sufficient for endoderm formation. In addition, we show that ␤-catenin has pronounced effects on animal blastomeres and is critical for specification of aboral ectoderm and for ectoderm patterning, presumably via a noncell-autonomous mechanism. These results support a model in which a Wnt-like signal released by vegetal cells patterns the early embryo along the animalvegetal axis. Our results also reveal similarities between the sea urchin animal-vegetal axis and the vertebrate dorsalventral axis, suggesting that these axes share a common evolutionary origin.

Global regulatory logic for specification of an embryonic cell lineage

“…This experiment, which has been repeated with molecular markers (14), means that micromeres execute signaling functions that have inductive effects on adjacent cells. We now know that between fourth and ninth cleavage (5-12 h after fertilization) the micromeres in fact express three different intercellular signaling ligands: (i) Wnt8, which enhances nuclearization of ␤-catenin in recipient cells, including themselves (15)(16)(17); (ii) a still undefined ''early signal (ES),'' which is received by adjacent cells in the fourth-to sixth-cleavage interval and is required by them for the normal process of endomesoderm specification (18); and (iii) from seventh cleavage, the Notch ligand Delta. Reception of this signal causes the ring of cells then immediately adjacent to the micromere lineage to assume mesodermal fate (19,20).…”

Divergence of ectodermal and mesodermal gene regulatory network linkages in early development of sea urchins

“…I next sought to experimentally perturb O-A specification in Et to determine the extent to which this developmental program is conserved in echinoids. In euechinoids, perturbation of animal-vegetal axis polarity by disruption of nuclearization of β-catenin indirectly disrupts O-A axis specification (31,33). One mechanism underlying the crosstalk of these two deuterostome specification events is the restriction of foxq2 to ANE, with its presence in OE blocking nodal transcription (23) Fig.…”

“…Abundant comparative evidence exists for other euechinoid taxa as well, including Lytechinus variegatus (Lv) (31)(32)(33)(34)(35)(36)(37) and Paracentrotus lividus (Pl) (38)(39)(40)(41)(42). Data from these indirectdeveloping euechinoids indicate that although these taxa diverged from one another ∼90 mya (9, 43), very little appreciable change to their developmental GRNs has accrued (44)(45)(46).…”

Nodal/activin signaling establishes oral–aboral polarity in the early sea urchin embryo

“…Recent experiments have shown that components of the Wnt (EmilyFenouil et al, 1998;Wikramanayake et al, 1998;Logan et al, 1999;Huang et al, 2000;Vonica et al, 2000) and the bone morphogenetic protein (BMP) 2/4 (Angerer et al, 2000) signaling pathway play important roles in patterning cell fates along the sea urchin primary or animal-vegetal (AV) axis. In contrast, the molecular mechanisms underlying patterning of the second embryonic axis, the aboral/oral (AO) axis, are poorly understood.…”