Abstract
The evolution of cell-adhesion mechanisms in animals facilitated the assembly of organized multicellular tissues. Studies in traditional animal models have revealed two predominant adhesion structures, the adherens junction (AJ) and focal adhesions (FAs), which are involved in the attachment of neighboring cells to each other and to the secreted extracellular matrix (ECM), respectively. The AJ (containing cadherins and catenins) and FAs (comprising integrins, talin, and paxillin) differ in protein composition, but both junctions contain the actin-binding protein vinculin. The near ubiquity of these structures in animals suggests that AJ and FAs evolved early, possibly coincident with multicellularity. However, a challenge to this perspective is that previous studies of sponges-a divergent animal lineage-indicate that their tissues are organized primarily by an alternative, sponge-specific cell-adhesion mechanism called "aggregation factor." In this study, we examined the structure, biochemical properties, and tissue localization of a vinculin ortholog in the sponge Oscarella pearsei (Op). Our results indicate that Op vinculin localizes to both cell-cell and cell-ECM contacts and has biochemical and structural properties similar to those of vertebrate vinculin. We propose that Op vinculin played a role in cell adhesion and tissue organization in the last common ancestor of sponges and other animals. These findings provide compelling evidence that sponge tissues are indeed organized like epithelia in other animals and support the notion that AJ- and FA-like structures extend to the earliest periods of animal evolution.
Highlights
The evolution of cell-adhesion mechanisms in animals facilitated the assembly of organized multicellular tissues
These findings provide compelling evidence that sponge tissues are organized like epithelia in other animals and support the notion that adherens junction (AJ)- and focal adhesions (FAs)-like structures extend to the earliest periods of animal evolution
Our results indicate that Oscarella pearsei (Op) vinculin is an ortholog of vertebrate vinculin and that its protein-binding partners and subcellular distribution are consistent with potential roles in both AJ- and FA-mediated cell adhesions
Summary
The O. pearsei genome [47] and transcriptome [48] was found to encode three predicted sequences with homology to the protein superfamily of ␣E-catenin, vinculin, and ␣-catulin (VIN-family proteins; Fig. 1). In O. pearsei, this sequence has a vinculin-like D2 domain (Fig. 1C), and the clade to which it clustered lacks close affinity with vinculin, ␣-catenin, and ␣-catulin, so we refer to this protein as “Op uncharacterized.”. Op vinculin lacks domain 2, which typically distinguishes vinculin from ␣-catenin in other animals and may contribute to the autoinhibition of F-actin binding (Fig. 1C). The domain organizations of Op talin and -catenin are more highly conserved than in VIN proteins or cadherins As in their mammalian counterparts, Op talin has an N-terminal FERM domain followed by a talin middle domain, vinculin-binding sites, and an I/WLEQ domain. The localization of Op vinculin to cell– cell contacts in the pinacoderm and choanoderm is consistent with a possible AJ in these tissues, despite the lack of ultrastructural evidence [35]
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