Sea Urchin as a Universal Model for Studies of Gene Networks

Abstract

The purple sea urchin Strongylocentrotus purpuratus has been used for over 150 years as a model organism in developmental biology. Using this model species, scientists have been able to describe, in detail, the mechanisms of cell cycle control and cell adhesion, fertilization, calcium signaling, cell differentiation, and death. Massive parallel sequencing of the sea urchin genome enabled the deciphering of the main components of gene regulatory networks during the activation of embryonic signaling pathways. This knowledge helped to extrapolate aberrations in somatic cells that may lead to diseases, including cancer in humans. Furthermore, since many, if not all, developmental signaling pathways were shown to be controlled by non-coding RNAs (ncRNAs), the sea urchin organism represents an attractive experimental model. In this review, we discuss the main discoveries in the genetics, genomics, and transcriptomics of sea urchins during embryogenesis with the main focus on the role of ncRNAs. This information may be useful for comparative studies between different organisms, and may help identify new regulatory networks controlled by ncRNAs.

Keywords: cell signaling; gene expression; genomics; long non-coding RNA; sea urchin.

Figure 1

Truncated phylogenetic tree of popular model organisms based on combined analyses of morphology and molecular data (Laumer et al., 2015; Telford et al., 2015; Torruella et al., 2015; Cannon et al., 2016). The tree illustrates the evolutionary relationship between Homo sapiens and Strongylocentrotus purpuratus as members of the deuterostome branch of the animal kingdom. Caenorhabditis elegans and Drosophila melanogaster are members of the protostome branch. (Branch lengths are not proportional to time).

Figure 2

Simplified S. purpuratus life cycle, stages of which are connected by black arrows. The name of each stage is shown in the picture. The beginning of the life cycle is fertilization, which is marked by a black dotted line. In the center, the black and gray time scale represents hours and days after fertilization, correspondingly. The red circular gradient line represents the degradation of the general maternal transcripts. The circular blue gradient shows the beginning of zygotic genome activation and increases in transcribed gene numbers.

Figure 3

Simple outline of the current models of the canonical Notch, WNT, and Hh pathways. NOTCH: Delta, delta-like ligand, Notch, ADAM, ADAM-family metalloprotease; γ-sec, γ-secretase; NICD, notch intracellular domain; Co-A, transcription coactivator; MAM, conserved and essential nuclear factor mastermind; CSL, DNA-binding transcription factor. WNT: Frizzled; WNT, wingless-type MMTV integration site; LRP, low-density lipoprotein receptor-related protein; APC, adenomatous polyposis coli; Disheveled, cytoplasmic phosphoprotein; GSK3ß, glycogen synthase kinase-3; CK1α, casein kinase 1 alpha; TCF, T-cell-specific transcription factor; LEF, lymphoid enhancer-binding factor. Hedgehog: Hh, hedgehog; PTCH, patched; SMO, smoothened; SUFU, suppressor of fused; GLI, GLI-family zinc finger.

Figure 4

The percent content of transposable elements (TE) in genomes of the sea urchin S. purpuratus and other invertebrates. TE classes are marked with a color: nonLTR SINE – blue; LINE – red; LTR TE – yellow; DNA transposons – green; non-annotated repeats – lilac (from Lebedev et al., 2019).