Abstract
Extracellular matrix (ECM) is considered central to the evolution of metazoan
multicellularity, however the repertoire of ECM proteins in non-bilaterians remains
unclear. Thrombospondins (TSPs) are known to be well-conserved from cnidarians
to vertebrates, yet to date have been considered a unique family, principally studied
for matricellular functions in vertebrates. Through searches utilizing the highlyconserved
C-terminal region of TSPs we identify undisclosed new families of
thrombospondin-related proteins in metazoans, designated mega-thrombospondin,
sushi-thrombospondin and poriferan-thrombospondin, each with a distinctive
phylogenetic distribution. These proteins share the TSP C-terminal region domain
architecture, as determined by domain composition and analysis of molecular
models against known structures. Mega-thrombospondins, the only form identified in ctenophores, are typically >2700aa and are also characterized by N-terminal
leucine-rich repeats and central cadherin/immunoglobulin domains. In cnidarians, which have a well-defined ECM, Mega-TSP was expressed throughout
embryogenesis in Nematostella vectensis, with dynamic endodermal expression in larvae and primary polyps and widespread ectodermal expression in adult N.
vectensis and Hydra magnipapillata polyps. Hydra Mega-TSP was also expressed
during regeneration and siRNA-silencing of Mega-TSP in Hydra caused specific
blockade of head regeneration. Molecular phylogenetic analyses based on the
conserved TSP C-terminal region identified each of the TSP-related groups to form clades distinct from the canonical TSPs. We discuss models for the evolution of the newly-defined TSP superfamily by gene duplications, radiation and gene losses from a debut in the last metazoan common ancestor. Together, the data provide new insight into the evolution of ECM and tissue organization in metazoans.
Original language | English |
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Article number | msz060 |
Pages (from-to) | 1220-1238 |
Number of pages | 19 |
Journal | Molecular Biology and Evolution |
Volume | 36 |
Issue number | 6 |
Early online date | 13 Mar 2019 |
DOIs | |
Publication status | Published - 1 Jun 2019 |
Bibliographical note
© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.Research Groups and Themes
- BrisSynBio
- Bristol BioDesign Institute
Keywords
- synthetic biology
- extracellular matrix
- multicellularity
- regeneration
- protein domains
- metazoa
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Emeritus Professor Jo Adams
- School of Biochemistry - Emeritus Professor of Cell Biology
- Cancer
- Dynamic Cell Biology
Person: Member, Honorary and Visiting Academic