Dose-dependent nuclear β-catenin response segregates endomesoderm along the sea star primary axis

Development. 2015 Jan 1;142(1):207-17. doi: 10.1242/dev.113043.

Abstract

In many invertebrates, the nuclearization of β-catenin at one pole of the embryo initiates endomesoderm specification. An intriguing possibility is that a gradient of nuclear β-catenin (nβ-catenin), similar to that operating in vertebrate neural tube patterning, functions to distinguish cell fates in invertebrates. To test this hypothesis, we determined the function of nβ-catenin during the early development of the sea star, which undergoes a basal deuterostomal mode of embryogenesis. We show that low levels of nβ-catenin activity initiate bra, which is expressed in the future posterior endoderm-fated territory; intermediate levels are required for expression of foxa and gata4/5/6, which are later restricted to the endoderm; and activation of ets1 and erg in the mesoderm-fated territory requires the highest nβ-catenin activity. Transcription factors acting downstream of high nβ-catenin segregate the endoderm/mesoderm boundary, which is further reinforced by Delta/Notch signaling. Significantly, therefore, in sea stars, endomesoderm segregation arises through transcriptional responses to levels of nβ-catenin activity. Here, we describe the first empirical evidence of a dose-dependent response to a dynamic spatiotemporal nβ-catenin activity that patterns cell fates along the primary axis in an invertebrate.

Keywords: Echinoderm; Endomesoderm; Gene regulatory network; Nuclear β-catenin; Patiria.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Blastula / drug effects
  • Blastula / metabolism
  • Body Patterning* / drug effects
  • Body Patterning* / genetics
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism*
  • Embryo, Nonmammalian / drug effects
  • Embryo, Nonmammalian / metabolism
  • Endoderm / drug effects
  • Endoderm / embryology*
  • Endoderm / metabolism
  • Gene Expression Regulation, Developmental
  • Gene Regulatory Networks
  • Hepatocyte Nuclear Factor 3-gamma / metabolism
  • Lithium Chloride / pharmacology
  • Mesoderm / drug effects
  • Mesoderm / embryology*
  • Mesoderm / metabolism
  • Models, Biological
  • Receptors, Notch / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Starfish / embryology
  • Starfish / genetics
  • Time Factors
  • Transcription, Genetic / drug effects
  • beta Catenin / metabolism*

Substances

  • Receptors, Notch
  • beta Catenin
  • Hepatocyte Nuclear Factor 3-gamma
  • Lithium Chloride