Sea Urchin Embryo: Specification of Cell Fates

Abstract

Specification of cell fate in sea urchin embryos involves initial asymmetric distribution of maternal molecules that establish posterior and anterior domains of transcription activity. Subsequently, fates of most blastomeres along the anterior–posterior and dorsal–ventral axes of the embryo are patterned by cell–cell interactions involving signalling ligands and cell surface receptors. These signalling pathways regulate the operation of networks of genes encoding transcription factors and additional signals, which guide the terminal differentiation of different cell types. Most of the signalling mechanisms that establish different embryonic territories and some of the transcription factors that specify cell types are highly conserved with those that pattern vertebrate embryos. The relative simplicity of the sea urchin embryo and the existence of tools for rapidly determining gene function provide clear advantages for understanding how early developmental processes work.

Key Concepts:

  • Sea urchin embryogenesis employs the two common mechanisms of early fate specification, inheritance of maternal molecules and signalling among cells.

  • The maternally derived initial state, in the absence of all known signals sent among the cells of the embryo, promotes development of anterior neuroectoderm, a region of ectoderm within which nerves develop.

  • Early posterior canonical Wnt signalling activates transcription factors followed by additional signals that convert posterior blastomeres to mesoderm and endoderm and restrict the anterior neuroectoderm fate to the anterior end of the embryo.

  • Patterning of anterior (neuroectoderm) and posterior (endomesoderm) fates requires mutual antagonism between the gene regulatory networks headed by Wnt and Six3, respectively.

  • Nodal signalling is necessary and sufficient for specification of fates along the dorsal–ventral axis, including oral and aboral ectoderm types.

  • Anterior–posterior (AP) and dorsal–ventral (DV) patterning are interconnected and temporally coordinated because early posterior canonical Wnt signalling is required to derepress nodal expression.

  • The components of the major tissue territory gene regulatory networks (GRNs) have been identified by studying embryos lacking signalling through canonical Wnt, Nodal or BMP, and their functional relationships determined by knocking down each of the corresponding proteins in vivo with morpholino oligonucleotides and monitoring effects on expression of other genes.

  • Individual cell types in sea urchin embryos are determined when their fates cannot be changed experimentally; this process requires stable activation of genes necessary for specification of a particular cell type and stable repression of those required for specification of other cell types.

  • The GRN devices that produce stable regulatory states are reinforcing cross‐regulatory and feedback loops among the component transcription factors, which render these states insensitive to signals.

  • The sea urchin embryo has enormous capacity before larval stages to change cell fates upon experimental challenge because the fates of many cells are only gradually specified and can be altered by signals sent from other cells.

Keywords: maternal determinants; cell–cell interactions; fate specification; transcription factors; signalling pathways

Figure 1.

Stages of sea urchin embryo development: (a) 16‐cell; (b) 60‐cell; (c) early mesenchyme blastula (24 h postfertilisation); (d) mid‐gastrula (36 h postfertilisation); (e, f) pluteus larva (72 h postfertilisation). Cell types and tissues are color‐coded. Embryo widths along dorsal–ventral axis are approximately 100 μm.

Figure 2.

(a–e) Formation of major regions of the embryo via signalling through canonical Wnt and the TGF‐β‐ligands, Nodal and BMP2/4. A wave of canonical Wnt signalling begins at fourth cleavage to specify mesoderm and endoderm and restrict the anterior neuroectoderm to the anterior end of the embryo. The remaining tissue becomes competent to form the epidermal tissues in the oral and aboral ectoderm as a result of Nodal and BMP2/4 signalling, respectively. Signalling through Nodal results in the production of Lefty, BMP2/4 and Chordin. Lefty, a Nodal antagonist, diffuses (diffusion is designated by dashed arrows) farther than Nodal and prevents its activity where the ciliary band forms. Chordin, a diffusible BMP2/4 antagonist, prevents BMP2/4 signalling in the oral ectoderm and ciliary band regions, but BMP2/4 can diffuse to the other side of the embryo where it supports aboral ectoderm differentiation. As a result of the combined activities of these TGF‐βs and their antagonists, a low level of TGF‐β signalling is created in a strip of cells between the oral and aboral ectoderm, which becomes the ciliary band, a second neuroectodermal territory. See text for details.

Figure 3.

A generic GRN in the sea urchin embryo. A gene encoding transcription factor 1 (TF1) is activated by a signal transduction pathway (Signal1) in cell type 1. It then activates expression of another gene encoding Signal2, which is secreted and binds to a receptor on another cell (Cell type 2), where it activates the GRN of that cell type. TF1 also activates genes encoding additional transcription factors (TFs 2–4) that either positively or negatively regulate each other's expression, creating a stable regulatory state that is independent of Signal1. TFs2–4 regulate the expression of additional genes that ether encode proteins required for the differentiated state (Diff1, Diff2) or additional transcription factors (e.g. TF5). A TF in the Cell Type1 GRN (shown here to be TF1) represses the operation of the Cell Type2 GRN. The structure of this network describes the basic scheme that leads from an initial inducing signal to the differentiation of one cell type and the exclusion of differentiation of another cell type.

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Peter IS and Davidson EH (2011) Evolution of gene regulatory networks controlling body plan development. Cell 144: 970–985.

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Angerer, Robert C, and Angerer, Lynne M(Jan 2012) Sea Urchin Embryo: Specification of Cell Fates. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001513.pub3]