Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Beilstein J Nanotechnol
2018 Jan 01;9:2071-2086. doi: 10.3762/bjnano.9.196.
Show Gene links
Show Anatomy links
The structural and chemical basis of temporary adhesion in the sea star Asterina gibbosa.
Lengerer B
,
Bonneel M
,
Lefevre M
,
Hennebert E
,
Leclère P
,
Gosselin E
,
Ladurner P
,
Flammang P
.
???displayArticle.abstract???
Background: Marine biological adhesives are a promising source of inspiration for biomedical and industrial applications. Nevertheless, natural adhesives and especially temporary adhesion systems are mostly unexplored. Sea stars are able to repeatedly attach and detach their hydraulic tube feet. This ability is based on a duo-gland system and, upon detachment, the adhesive material stays behind on the substrate as a ''footprint''. In recent years, characterization of sea star temporary adhesion has been focussed on the forcipulatid species Asterias rubens. Results: We investigated the temporary adhesion system in the distantly related valvatid species Asterina gibbosa. The morphology of tube feet was described using histological sections, transmission-, and scanning electron microscopy. Ultrastructural investigations revealed two adhesive gland cell types that both form electron-dense secretory granules with a more lucid outer rim and one de-adhesive gland cell type with homogenous granules. The footprints comprised a meshwork on top of a thin layer. This topography was consistently observed using various methods like scanning electron microscopy, 3D confocal interference microscopy, atomic force microscopy, and light microscopy with crystal violet staining. Additionally, we tested 24 commercially available lectins and two antibodies for their ability to label the adhesive epidermis and footprints. Out of 15 lectins labelling structures in the area of the duo-gland adhesive system, only one also labelled footprints indicating the presence of glycoconjugates with α-linked mannose in the secreted material. Conclusion: Despite the distant relationship between the two sea star species, the morphology of tube feet and topography of footprints in A. gibbosa shared many features with the previously described findings in A. rubens. These similarities might be due to the adaptation to a benthic life on rocky intertidal areas. Lectin- and immuno-labelling indicated similarities but also some differences in adhesive composition between the two species. Further research on the temporary adhesive of A. gibbosa will allow the identification of conserved motifs in sea star adhesion and might facilitate the development of biomimetic, reversible glues.
Figure 1. External morphology of the sea star Asterina gibbosa and of its tube feet. (A) Image of a living adult, attached to a rock. (B) Oral side of an adult, showing the arrangement of the tube feet in the ambulacral grooves along the five arms. (C) Overview of an amputated tube foot with SEM. (D) SEM image of the disc distal surface with a layer of adhesive material. (E) Details of secretory pores and cilia (SEM). AM - adhesive material; CI - cilia; D - disc; G - granule; M - mouth; MI - microvilli; P - pores; S - stem; TF - tube feet. Scale bars: (A) 1 cm; (B) 0.2 cm; (C) 100 µm; (D) 10 µm; (E) 0.5 µm.
Figure 2. Fine structure of the tube feet of Asterina gibbosa observed in light microscopy (A,B) and TEM (C–H). (A,B) Longitudinal histological section through a tube foot stained with Heidenhain’s azan trichrome. Arrow highlights remains of adhesive material. (C–H) TEM images of longitudinal tube foot sections, arrowhead in (H) indicates inner core of secretory granule. See text for details. AC - adhesive gland cell; AE - adhesive epidermis; CL - cuticular layer; CT - connective tissue; DAC - de-adhesive gland cell; E - epidermis; M - myomesothelium; MV - microvilli; N - nerve strands; SC - supportive cell. Scale bars: (A) 100 µm; (B) 50 µm; (C) 5 µm; (D) 2 µm; (E) 1 µm; (F,G) 0.2 µm; (H) 0.5 µm.
Figure 3. Ultrastructure of the tube foot adhesive epidermis of Asterina gibbosa observed in light microscopy (A) and TEM (B–G). (A) Semi thin cross-section of a tube foot at the level of the disc, boxes indicate approximate area of TEM images. (B–G) Ultrastructure of cells in the adhesive epidermis: (B,C) in the basal part of the disc, at the level of the connective tissue, and (D–G) in the apical part of the disc. Arrow in (C) highlights the collagen fibres of the connective tissue. AC - adhesive gland cell; CI - cilia; CL - cuticular layer; CT - connective tissue; DAC - de-adhesive gland cell; IF - intermediate filaments; MV - microvilli; SC - supportive cell; SEC - sensory cell; SMV - specialized microvilli. Scale bars: (A) 50 µm; (B) 5 µm; (C,G) 1 µm; (D,E,F) 2 µm.
Figure 4. Scanning electron microscopy of footprints in Asterina gibbosa. (A) Overview of a complete footprint. (B) Characteristic area of a footprint with visible meshwork. Arrows indicate thicker parts, where the meshwork is not distinguishable. (C,D) Details of the meshwork at higher magnifications. MW - meshwork; TL - thin layer. Scale bars: (A) 100 µm; (B) 10 µm; (C) 2 µm; (D) 0.5 µm.
Figure 5. Topography of the footprints in A. gibbosa shown with 3D confocal interference microscopy (A) and AFM (B,C). (A) Overview of a footprint with 3D confocal interference microscopy in 3D and 2D. (B,C) AFM images of footprint meshwork in (B) 3D and at higher resolution in (C) 2D.
Figure 6. Lectin labelling of tube foot sections in Asterina gibbosa with (A1,A2) Con A, (B1,B2) Jacalin, (C1,C2) WGA, (D1,D2) PNA, (E1,E2) SBA, and (F1,F2) LCA. (A1–F1) Overlay of corresponding fluorescence- and differential interference contrast images. (A2–F2) Confocal z-projections of lectin labelling. Scale bars: 10 µm; (inset) 2 µm.
Figure 7. Structure of the footprints of Asterina gibbosa (light microscopy). (A1,A2) Cristal violet staining of a fresh footprint. (B1,B2) ConA labelling of a PFA fixed footprint, confocal z-projections. (B2) Confocal z-projection exclusively at the level of the meshwork, above the thin layer. Scale bars: (A1,B1) 100 µm; (A2) 20 µm; (B2) 5 µm.
Byrne,
Life history diversity and evolution in the Asterinidae.
2006, Pubmed,
Echinobase
Byrne,
Life history diversity and evolution in the Asterinidae.
2006,
Pubmed
,
Echinobase
Cha,
Development of bioadhesives from marine mussels.
2008,
Pubmed
Engster,
Histology and ultrastructure of the tube foot epithelium in the phanerozonian starfish, Astropecten.
1972,
Pubmed
,
Echinobase
Flammang,
A study of the temporary adhesion of the podia in the sea star asterias rubens (Echinodermata, asteroidea) through their footprints.
1998,
Pubmed
,
Echinobase
Flammang,
The Role of Podial Secretions in Adhesion in Two Species of Sea Stars (Echinodermata).
1994,
Pubmed
,
Echinobase
Haesaerts,
Evaluation of the attachment strength of individuals of Asterina gibbosa (Asteroidea, Echinodermata) during the perimetamorphic period.
2005,
Pubmed
,
Echinobase
Haesaerts,
Adaptations to benthic development: functional morphology of the attachment complex of the brachiolaria larva in the sea star Asterina gibbosa.
2006,
Pubmed
,
Echinobase
Hamwood,
Preliminary characterisation and extraction of anterior adhesive secretion in monogenean (platyhelminth) parasites.
2002,
Pubmed
,
Echinobase
Harris,
Intermediate filaments, microtubules and microfilaments in epidermis of sea urchin tube foot.
1984,
Pubmed
,
Echinobase
Hennebert,
Evaluation of the different forces brought into play during tube foot activities in sea stars.
2010,
Pubmed
,
Echinobase
Hennebert,
An integrated transcriptomic and proteomic analysis of sea star epidermal secretions identifies proteins involved in defense and adhesion.
2015,
Pubmed
,
Echinobase
Hennebert,
Sea star tenacity mediated by a protein that fragments, then aggregates.
2014,
Pubmed
,
Echinobase
Hennebert,
Experimental strategies for the identification and characterization of adhesive proteins in animals: a review.
2015,
Pubmed
,
Echinobase
Hennebert,
Micro- and nanostructure of the adhesive material secreted by the tube feet of the sea star Asterias rubens.
2008,
Pubmed
,
Echinobase
Hennebert,
Characterisation of the carbohydrate fraction of the temporary adhesive secreted by the tube feet of the sea star Asterias rubens.
2011,
Pubmed
,
Echinobase
Kamino,
Underwater adhesive of marine organisms as the vital link between biological science and material science.
2008,
Pubmed
Lebesgue,
Deciphering the molecular mechanisms underlying sea urchin reversible adhesion: A quantitative proteomics approach.
2016,
Pubmed
,
Echinobase
Lengerer,
Adhesive organ regeneration in Macrostomum lignano.
2016,
Pubmed
Lengerer,
Biological adhesion of the flatworm Macrostomum lignano relies on a duo-gland system and is mediated by a cell type-specific intermediate filament protein.
2014,
Pubmed
Lengerer,
Organ specific gene expression in the regenerating tail of Macrostomum lignano.
2018,
Pubmed
Linchangco,
The phylogeny of extant starfish (Asteroidea: Echinodermata) including Xyloplax, based on comparative transcriptomics.
2017,
Pubmed
,
Echinobase
Maier,
Siderophores and mussel foot proteins: the role of catechol, cations, and metal coordination in surface adhesion.
2017,
Pubmed
Rodrigues,
Profiling of adhesive-related genes in the freshwater cnidarian Hydra magnipapillata by transcriptomics and proteomics.
2016,
Pubmed
Rodrigues,
Molecular biology approaches in bioadhesion research.
2014,
Pubmed
Santos,
First insights into the biochemistry of tube foot adhesive from the sea urchin Paracentrotus lividus (Echinoidea, Echinodermata).
2009,
Pubmed
,
Echinobase
Santos,
Adhesion of echinoderm tube feet to rough surfaces.
2005,
Pubmed
,
Echinobase
Santos,
Comparative histological and immunohistochemical study of sea star tube feet (Echinodermata, Asteroidea).
2005,
Pubmed
,
Echinobase
Santos,
Morphology and tenacity of the tube foot disc of three common European sea urchin species: a comparative study.
2006,
Pubmed
,
Echinobase
Toubarro,
Cloning, Characterization, and Expression Levels of the Nectin Gene from the Tube Feet of the Sea Urchin Paracentrotus Lividus.
2016,
Pubmed
,
Echinobase
Zayas,
The use of lectins as markers for differentiated secretory cells in planarians.
2010,
Pubmed
von Byern,
Histochemical characterization of the adhesive organ of three Idiosepius spp. species.
2008,
Pubmed
von Byern,
Characterization of the adhesive dermal secretion of Euprymna scolopes Berry, 1913 (Cephalopoda).
2017,
Pubmed
