Cell adhesion factors in cnidarians

Knack, Brent Andrew (2011) Cell adhesion factors in cnidarians. PhD thesis, James Cook University.

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Abstract

Cell adhesion is central to metazoan evolution and development, facilitating multicellularity, intercellular communication and co-ordinated cell movements. Morphological studies indicate that cellular and developmental processes involving dynamic changes in adhesive state, such as cell migration and gastrulation, were established early in metazoan evolution. However, much of our current understanding surrounding the involvement of cell adhesion molecules in these processes has been obtained from comparative analyses of bilaterian development. Cnidarians present an exciting opportunity to investigate cell adhesion and developmental processes in the simplest extant animals to possess a tissue layer level of organisation. As the nearest out-group to the Bilateria, cnidarians are ideally positioned for comparative studies between diploblastic and triploblastic development whilst being highly informative regarding ancestral gene function and protein family evolution.

The diversity of adhesion proteins in cnidarians has remained largely unexplored, with no single analysis offering an overview of the cnidarian adhesion complement or "adhesome". To better understand the complexity of the cnidarian adhesome, sequence data from four model cnidarians (Acropora millepora – coral, Nematostella vectensis – Sea Anemone, Hyrda magnipapillata – Hydra, Clytia hemispherica – Hydrozoan Jelly – fish) was annotated and all potential adhesion proteins categorised according to similarity to described protein families. The cnidarian adhesome shows overall similarity with that of invertebrate bilaterians, containing a substantial array of recognisable cadherins, integrins, lectins and extracellular matrix proteins comparable to Drosophila and sea urchin. Such conservation suggests that most recognised adhesion proteins involved in bilaterian development and innate immunity were already established in the ureumetazoan ancestor. All four species also demonstrated an expanded set of lectin domain containing putative pattern recognition receptors which may act in opsonisation of microbial pathogens. In contrast to this, each species lacked the large immunoglobulin complement observed in deuterostomes suggesting the predominate mechanism of microbial recognition may be facilitated by lectins rather than immunoglobulins.

Catenin binding cadherins and components of the planar cell polarity (PCP) pathway were among the developmentally significant proteins conserved between cnidarians and bilaterians. Expression of cadherins, such as E-Cadherin and N-Cadherin, which bind cytoplasmic β-catenin, strongly influence the ability of cells to undergo epithelial to mesenchymal transtion, a central event in developmental processes such as gastrulation. The assymetrical distribution of planar cell polarity cadherins and other PCP proteins at both the cell and tissue levels, also affects tissue morphology by co-ordinating cellular structures and providing positional cues during morphogenesis. To identify the potential for conserved catenin binding cadherins and PCP proteins to participate in cnidarian development, patterns of mRNA expression were assessed in embryos and larvae of the coral Acropora millepora. Surprisingly, the only known catenin binding Cadherin from coral and the first identified outside the Bilateria, Am_ACadherin, does not appear to participate in gastrulation, which is inconsistent with bilaterian modes of gastrulation. Planar cell polarity, however may be active during Acropora gastrulation, with AmVan Gogh (AmVangl) and AmDachsous (AmDs) expressed assymetrically during gastrulation. Am_ACadherin was instead implicated in oral pore development following gastrulation as indicated by a highly restricted pattern of expression in the oral ectoderm. In situ mRNA hybridisation also strongly suggests the involvement of non-canonical Wnt/PCP in oral pore development, however none of the PCP adhesion proteins exhibited oral pore restricted patterns of expression during larval stages. These results suggest both Cadherin-catenin signalling and PCP are signficant during cnidarian development and may facilitate co-ordinated tissue mobility such as involution of the oral ectoderm.

Survey of the cnidarian adhesome also identified α and β integrins, which, like cadherins, play signifcant roles in the early development of bilaterians. The expression patterns for 3 (1 α-Integrin & 2 β-Integrins) of the 5 (3 α-Integrins & 2 β-Integrins) integrins identified in Acropora have previously been reported, showing restiction to the presumptive endoderm throughout gastrulation. The ligand binding properties of basal integrins have not been reported, obscuring their developmental function. To identify the ligand binding properties of AmItgα1-ItgβCN1 and AmItgα1-AmItgβ2 integrin heterodimers, transgenic cell spreading assays were performed on a number of Drosophila ligands. These experiments suggested coral AmItgα1 containing integrins may bind to arginine-glycine-aspartate (RGD) sequence containing proteins. RGD specific integrins are abundant throughout the Bilateria, and along with Laminin binding integrins, have been suggested to be present in the Urbilaterian ancestor (the last common ancestor of the Bilateria). Phylogenetic analysis of α-Integrins including the more recently identified AmItgα3 (Acropora) and NvItgα2 (Nematostella) suggest that these proteins may bind to a second distinct ligand type. The ligand diversity of cnidarian integrins may therefore be comparable with basal bilaterians.

Item ID: 36991
Item Type: Thesis (PhD)
Keywords: Acropora millepora; adhesion proteins; adhesome; bilaterins; cadherins; catenins; cell adhesion; Clytia hemispherica; cnidaria; cnidarians; corals; Hydra magnipapillata; hydra; hydrozoan jellyfish; integrins; jelly fish; Nematostella vectensis; sea anemone; sea anemones
Date Deposited: 23 Dec 2014 23:10
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060409 Molecular Evolution @ 50%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060305 Evolution of Developmental Systems @ 50%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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