Origin and evolution of the sponge aggregation factor gene family

Grice, Laura F.; Gauthier, Marie; Roper, Kathrein E.; Fernàndez‐Busquets, Xavier; Degnan, Sandie M.; Degnan, Bernard M.

doi:10.1093/molbev/msx058

Cited by 28 publications

(48 citation statements)

References 95 publications

(131 reference statements)

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“…One caveat to this interpretation is that O. pearsei belongs to the clade homoscleromorpha, which lacks clear orthologs of the core AF protein family characterized from demosponges (Ref. 19); but see Ref. 105); adhesion mechanisms may differ between modern sponge lineages, which underwent very ancient divergences (106).…”

Section: Vinculin Involved In Early Multicellular Evolutionmentioning

confidence: 99%

“…This process relies on a secreted proteoglycan complex termed the aggregation factor (AF) that functions both in cell adhesion and self/nonself recognition (14 -18). Core proteins of the AF have been identified and are structurally composed of calx-␤ domains and a sponge-specific "wreath" domain (19). Sulfated polysaccharide components of the AF undergo calcium-dependent, homophilic interactions that are considered to be the predominant adhesion mechanism in sponges (20).…”

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confidence: 99%

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

Miller

Pokutta

Mitchell

et al. 2018

Journal of Biological Chemistry

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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 (). Our results indicate that 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 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.

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Section: Vinculin Involved In Early Multicellular Evolutionmentioning

confidence: 99%

mentioning

confidence: 99%

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

Miller

Pokutta

Mitchell

et al. 2018

Journal of Biological Chemistry

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“…There are four extant classes of sponges ( [66][67][68][69][70][71]. These proteins can adopt unusual, ring-like conformations and appear to be specific to the demosponge lineage [72,73].…”

Section: Known Components Of Ecm In Ctenophores and Poriferansmentioning

confidence: 99%

Modelling the early evolution of extracellular matrix from modern Ctenophores and Sponges

Draper

Shoemark

Adams

2019

Essays in Biochemistry

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Animals (metazoans) include some of the most complex living organisms on Earth, with regard to their multicellularity, numbers of differentiated cell types, and lifecycles. The metazoan extracellular matrix (ECM) is well-known to have major roles in the development of tissues during embryogenesis and in maintaining homoeostasis throughout life, yet insight into the ECM proteins which may have contributed to the transition from unicellular eukaryotes to multicellular animals remains sparse. Recent phylogenetic studies place either ctenophores or poriferans as the closest modern relatives of the earliest emerging metazoans. Here, we review the literature and representative genomic and transcriptomic databases for evidence of ECM and ECM-affiliated components known to be conserved in bilaterians, that are also present in ctenophores and/or poriferans. Whereas an extensive set of related proteins are identifiable in poriferans, there is a strikingly lack of conservation in ctenophores. From this perspective, much remains to be learnt about the composition of ctenophore mesoglea. The principal ECM-related proteins conserved between ctenophores, poriferans, and bilaterians include collagen IV, laminin-like proteins, thrombospondin superfamily members, integrins, membrane-associated proteoglycans, and tissue transglutaminase. These are candidates for a putative ancestral ECM that may have contributed to the emergence of the metazoans.

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“…They are one of the most phylogenetically divergent groups of animals (King and Rokas, 2017;Simion et al, 2017), their anatomy is fundamentally different from other animals (Leys and Hill, 2012), and there are long-standing questions about the structure and homology of their tissues compared to epithelia in other animals (Leys et al, 2009;Tyler, 2003). It has been argued that sponge cell adhesion relies primarily upon an extracellular proteoglycan complex termed the Aggregation Factor (Bucior and Burger, 2004;Cauldwell et al, 1973;Grice et al, 2017;Haseley et al, 2001;Henkart et al, 1973;Humphreys, 1963;Vilanova et al, 2016). Antibodies raised against the Aggregation Factor have been reported to block reaggregation of dissociated cells (Schütze et al, 2001), and purified Aggregation Factor can mediate adhesion between beads in cell-free assays (Jarchow and Burger, 1998).…”

Section: Introductionmentioning

confidence: 99%

Diverse cell junctions with unique molecular composition in tissues of a sponge (Porifera)

Mitchell

Nichols

2019

Preprint

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The integrity and organization of animal tissues depends upon specialized protein complexes that mediate adhesion between cells with each other (cadherin-based adherens junctions), and with the extracellular matrix (integrin-based focal adhesions). Reconstructing how and when these cell junctions evolved is central to understanding early tissue evolution in animals. We examined focal adhesion protein homologs in tissues of the freshwater sponge, Ephydatia muelleri (phylum Porifera). We found that sponge homologs of focal adhesion proteins coprecipitate as a complex and localize to cell junctions in sponge tissues. These data support that the adhesion roles of these proteins evolved early, prior to the divergence of sponges and other animals. However, in contrast to the spatially partitioned distribution of cell junctions in epithelia of other animals, focal adhesion proteins were found to be co-distributed with the adherens junction protein Emβ-catenin in sponge tissues; both at certain cell-cell and cellextracellular matrix (ECM) adhesions. Sponge adhesion structures were found to be unique in other ways, too. The basopinacoderm (substrate-attachment epithelium) lacks typical polarity in that cell-ECM adhesions form on both basal and apical surfaces, and compositionally unique cell junctions form at the interface between cells with spicules (siliceous skeletal elements) and between cells and environmental bacteria. These results clarify the diversity, distribution and molecular composition of cell junctions in tissues of E. muelleri, but raise new questions about their function and homology with cell junctions in other animals." 1 " 8

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Origin and evolution of the sponge aggregation factor gene family

Cited by 28 publications

References 95 publications

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

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

Modelling the early evolution of extracellular matrix from modern Ctenophores and Sponges

Diverse cell junctions with unique molecular composition in tissues of a sponge (Porifera)

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