Analysis of a vinculin homolog in a sponge (phylum Porifera) reveals that vertebrate-like cell adhesions emerged early in animal evolution

Miller, Phillip W.; Pokutta, Sabine; Mitchell, Jennyfer M.; Chodaparambil, Jayanth V.; Clarke, D. Nathaniel; Nelson, W. James; Weis, William I.; Nichols, Scott A.

doi:10.1074/jbc.ra117.001325

Title: Analysis of a vinculin homolog in a sponge (phylum Porifera) reveals that vertebrate-like cell adhesions emerged early in animal evolution

Journal Article · Thu Jun 07 00:00:00 EDT 2018 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.ra117.001325· OSTI ID:1469753

Miller, Phillip W. ^[1]; Pokutta, Sabine ^[1]; Mitchell, Jennyfer M. ^[2]; Chodaparambil, Jayanth V. ^[1];

^[1]; Nelson, W. James ^[1]; Weis, William I. ^[1];

^[2]

Stanford Univ., Stanford, CA (United States)
Univ. of Denver, Denver, CO (United States)

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. Furthermore, 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.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-76SF00515; R35GM118064; R01GM114462; 15-EXO15_2–0027

OSTI ID:: 1469753

Journal Information:: Journal of Biological Chemistry, Vol. 293, Issue 30; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 14 works

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The significance of sponges for comparative studies of developmental evolution Colgren, Jeffrey; Nichols, Scott A. WIREs Developmental Biology, Vol. 9, Issue 2 https://doi.org/10.1002/wdev.359	journal	July 2019
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Modelling the early evolution of extracellular matrix from modern Ctenophores and Sponges Draper, Graham W.; Shoemark, Deborah K.; Adams, Josephine C. Essays in Biochemistry, Vol. 63, Issue 3 https://doi.org/10.1042/ebc20180048	journal	August 2019
Diverse cell junctions with unique molecular composition in tissues of a sponge (Porifera) Mitchell, Jennyfer M.; Nichols, Scott A. EvoDevo, Vol. 10, Issue 1 https://doi.org/10.1186/s13227-019-0139-0	journal	October 2019

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