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

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. Furthermore, thesemore » 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.« less

Authors:
 [1];  [1];  [2];  [1]; ORCiD logo [1];  [1];  [1]; ORCiD logo [2]
  1. Stanford Univ., Stanford, CA (United States)
  2. Univ. of Denver, Denver, CO (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1469753
Grant/Contract Number:  
AC02-76SF00515; R35GM118064; R01GM114462; 15-EXO15_2–0027
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 293; Journal Issue: 30; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; adherens junction; focal adhesion; epithelium; protein evolution; evolution; Oscarella; Porifera; Sponge; Vinculin

Citation Formats

Miller, Phillip W., Pokutta, Sabine, Mitchell, Jennyfer M., Chodaparambil, Jayanth V., Clarke, D. Nathaniel, Nelson, W. James, Weis, William I., and Nichols, Scott A. Analysis of a vinculin homolog in a sponge (phylum Porifera) reveals that vertebrate-like cell adhesions emerged early in animal evolution. United States: N. p., 2018. Web. doi:10.1074/jbc.ra117.001325.
Miller, Phillip W., Pokutta, Sabine, Mitchell, Jennyfer M., Chodaparambil, Jayanth V., Clarke, D. Nathaniel, Nelson, W. James, Weis, William I., & Nichols, Scott A. Analysis of a vinculin homolog in a sponge (phylum Porifera) reveals that vertebrate-like cell adhesions emerged early in animal evolution. United States. https://doi.org/10.1074/jbc.ra117.001325
Miller, Phillip W., Pokutta, Sabine, Mitchell, Jennyfer M., Chodaparambil, Jayanth V., Clarke, D. Nathaniel, Nelson, W. James, Weis, William I., and Nichols, Scott A. Thu . "Analysis of a vinculin homolog in a sponge (phylum Porifera) reveals that vertebrate-like cell adhesions emerged early in animal evolution". United States. https://doi.org/10.1074/jbc.ra117.001325. https://www.osti.gov/servlets/purl/1469753.
@article{osti_1469753,
title = {Analysis of a vinculin homolog in a sponge (phylum Porifera) reveals that vertebrate-like cell adhesions emerged early in animal evolution},
author = {Miller, Phillip W. and Pokutta, Sabine and Mitchell, Jennyfer M. and Chodaparambil, Jayanth V. and Clarke, D. Nathaniel and Nelson, W. James and Weis, William I. and Nichols, Scott A.},
abstractNote = {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.},
doi = {10.1074/jbc.ra117.001325},
url = {https://www.osti.gov/biblio/1469753}, journal = {Journal of Biological Chemistry},
issn = {0021-9258},
number = 30,
volume = 293,
place = {United States},
year = {2018},
month = {6}
}

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    Works referencing / citing this record:

    The significance of sponges for comparative studies of developmental evolution
    journal, July 2019


    Modelling the early evolution of extracellular matrix from modern Ctenophores and Sponges
    journal, August 2019