Biomechanics of Adhesion in Sea Cucumber Cuvierian Tubules (Echinodermata, Holothuroidea) (original) (raw)
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Instantaneous adhesion of Cuvierian tubules in the sea cucumber Holothuria forskali
Biointerphases, 2014
The peculiar Cuvierian tubules of sea cucumbers function as a defense mechanism. They thwart attacks by creating a sticky network composed of elongated tubules within which the potential predator is entangled in a matter of seconds and thus immobilized. Cuvierian tubules are typical instantaneous adhesive organs in which tissue integrity is destroyed during the release of the adhesive secretion. However, very little information is available about this adhesion process. The adhesive epithelium-the mesothelium-and the sticky material it produces were studied in the species Holothuria forskali using different microscopy techniques (light microscopy, transmission electron microscopy, scanning electron microscopy, and atomic force microscopy). The mesothelium consists of two cell types-peritoneocytes and granular cells-organized in superimposed layers. In tubules before expulsion, peritoneocytes form an outer protective cell layer preventing adhesion when not needed. After expulsion, the elongation process removes this protective layer and allows granular cells to unfold and to become exposed at the tubule surface. At this stage, Cuvierian tubules are still not sticky. Upon contact with a surface, however, granular cells release their granule contents. Once released, this material changes in aspect, swells, and spreads readily on any type of substrate where it forms a thin homogeneous layer. After tubule peeling, this layer remains on the surface but is often contaminated with collagen fibers. Atomic force microscopy demonstrated the adhesive layer to be made up of globular nanostructures measuring about 70 nm in diameter and to be more adhesive than the collagen fibers left on it. The morphological organization of Cuvierian tubules therefore allows contact-dependent deposition of an adhesive material presenting a high affinity for various surfaces. It is certainly an adaptive advantage for a defense organ to be able to entangle different types of predators. V
Marine Biotechnology, 2003
Sea cucumbers possess a peculiar specialized defense system: the so-called Cuvierian tubules. The system is mobilized when the animal is mechanically stimulated, resulting in the discharge of a few white filaments, the tubules. Their great adhesivity, combined with their high tensile strength, allows Cuvierian tubules to entangle and immobilize potential predators. The cellular origin and composition of the Cuvierian tubule adhesive were investigated in the species Holothuria forskali by studying prints left on the substratum after mechanical detachment of the tubule. Polyclonal antibodies raised against tubule print material were used to locate the origin of tubule print constituents in the tubules. Extensive immunoreactivity was detected in the secretory granules of mesothelial granular cells, suggesting that their secretions make up the bulk of the adhesive material. Tubule print material consists of 60% proteins and 40% carbohydrates, a composition that is unique among the adhesive secretions of marine invertebrates. Although it is highly insoluble, a small fraction of this material can be extracted using denaturing buffers. Electrophoretic analysis of the extracts revealed that it contains about 10 proteins with apparent molecular masses ranging from 17 to 220 kDa and with closely related amino acid compositions, rich in acidic and in small side-chain amino acids. The adhesive from the Cuvierian tubules of H. forskali shares these characteristics with many marine bioadhesives and structural biomaterials.
Mechanical adaptability of sea cucumber Cuvierian tubules involves a mutable collagenous tissue
The Journal of experimental biology, 2017
Despite their soft body and slow motion, sea cucumbers present a low predation rate, reflecting the presence of efficient defence systems. For instance, members of the family Holothuriidae rely on Cuvierian tubules for their defence. These tubules are normally stored in the posterior coelomic cavity of the animal, but when the sea cucumber is threatened by a potential predator, they are expelled through the cloacal aperture, elongate, become sticky and entangle and immobilise the predator in a matter of seconds. The mechanical properties (extensibility, tensile strength, stiffness and toughness) of quiescent (i.e. in the body cavity) and elongated (i.e. after expulsion) Cuvierian tubules were investigated in the species Holothuria forskali using traction tests. Important mechanical differences were measured between the two types of tubules, reflecting adaptability to their operating mode: to ease elongation, quiescent tubules present a low resistance to extension, while elongated tu...
Evidence-Based Complementary and Alternative Medicine, 2011
The sea cucumberHolothuria forskålipossesses a specialized system called Cuvierian tubules. During mechanical stimulation white filaments (tubules) are expelled and become sticky upon contact with any object. We isolated a protein with adhesive properties from protein extracts of Cuvierian tubules fromH. forskåli. This protein was identified by antibodies against recombinant precollagen D which is located in the byssal threads of the musselMytilus galloprovincialis. To find out the optimal procedure for extraction and purification, the identified protein was isolated by several methods, including electroelution, binding to glass beads, immunoprecipitation, and gel filtration. Antibodies raised against the isolated protein were used for localization of the adhesive protein in Cuvierian tubules. Immunostaining and immunogold electron microscopical studies revealed the strongest immunoreactivity in the mesothelium; this tissue layer is involved in adhesion. Adhesion of Cuvierian tubule...
InTech eBooks, 2011
Biomaterials-Physics and Chemistry 246 immobilise most organisms with which they come into contact (VandenSpiegel & Jangoux, 1987). The tubules, once expelled, are immediately adhesive on contact with a solid surface (VandenSpiegel & Jangoux, 1987), such as the exoskeleton or skin of a predator. Crabs, molluscs and sea stars can stimulate tubule expulsion, and the tubules stick to these species. This adhesion happens entirely under water, and does not need the mixed environment of the intertidal zone where many of the other potential adhesives are sourced. Sticky tubules are found only within the family Holothuridae within the order Aspidochirotida, and mostly in the genus Bohadschia and the genus Holothuria. Various authors have described the ultrastructure of the tubules, especially for H.
The cellular basis of bioadhesion of the freshwater polyp Hydra
BMC Zoology, 2016
Background: The freshwater cnidarian Hydra temporarily binds itself to numerous natural substrates encountered underwater, such as stones, leafs, etc. This adhesion is mediated by secreted material from specialized ectodermal modified cells at the aboral end of the animal. The means by which Hydra polyps attach to surface remain unresolved, despite the fact that Hydra is a classic model in developmental and stem cell biology. Results: Here, we present novel observations on the attachment mechanism of Hydra using high pressure transmission electron microscopy, scanning electron microscopy, atomic force microscopy, super-resolution microscopy, and enzyme histochemistry. We analyzed the morphology of ectodermal basal disc cells, studied the secreted material, and its adhesive nature. By electron microscopy we identified four morphologically distinct secretory granules occurring in a single cell type. All the secretory granules contained glycans with different distribution patterns among the granule types. Footprints of the polyps were visualized under dry conditions by atomic force microscopy and found to consist of a meshwork with nanopores occurring in the interstices. Two antibodies AE03 and 3G11, previously used in cell differentiation studies, labelled both, basal disc cells and footprints. Our data suggest that the adhesive components of Hydra are produced, stored and delivered by a single cell type. Video microscopy analysis corroborates a role of muscle contractions for the detachment process. Conclusion: We clearly demonstrated that bioadhesion of Hydra relies on the secreted material. Our data suggest that glycans and/or glycoproteins represent an important fraction of the secreted material. Detachment seems to be initiated by mechanical forces by muscular contractions. Taken together, our study represents the characterization of an unique temporary adhesive system not known in aquatic organisms from other metazoan phyla.
Mechanisms of temporary adhesion in benthic animals
Biological Reviews, 2011
Adhesive systems are ubiquitous in benthic animals and play a key role in diverse functions such as locomotion, food capture, mating, burrow building, and defence. For benthic animals that release adhesives, surface and material properties and external morphology have received little attention compared to the biochemical content of the adhesives. We address temporary adhesion of benthic animals from the following three structural levels: (a) the biochemical content of the adhesive secretions, (b) the micro-and mesoscopic surface geometry and material properties of the adhesive organs, and (c) the macroscopic external morphology of the adhesive organs. We show that temporary adhesion of benthic animals is affected by three structural levels: the adhesive secretions provide binding to the substratum at a molecular scale, whereas surface geometry and external morphology increase the contact area with the irregular and unpredictable profile of the substratum from micro-to macroscales. The biochemical content of the adhesive secretions differs between abiotic and biotic substrata. The biochemistry of the adhesives suitable for biotic substrata differentiates further according to whether adhesion must be activated quickly (e.g. as a defensive mechanism) or more slowly (e.g. during adhesion of parasites). De-adhesion is controlled by additional secretions, enzymes, or mechanically. Due to deformability, the adhesive organs achieve intimate contact by adapting their surface profile to the roughness of the substratum. Surface projections, namely cilia, cuticular villi, papillae, and papulae increase the contact area or penetrate through the secreted adhesive to provide direct contact with the substratum. We expect that the same three structural levels investigated here will also affect the performance of artificial adhesive systems.
Cell Motility and The Cytoskeleton, 2001
Little is known about the presence and distribution of tubulin isotypes in MDCK cells although essential epithelial functions in these monolayers are regulated by dynamic changes in the microtubule architecture. Using specific antibodies, we show here that the βI, βII, and βIV isotypes are differentially distributed in the microtubules of these cells. Microtubules in subconfluent cells radiating from the perinuclear region contain βI and βII tubulins, while those extending to the cell edges are enriched in βII. Confluent cells contain similar proportions of βI and βII along the entire microtubule length. βIV is the less abundant isotype and shows a similar distribution to βII. The effect of modifying tubulin isotype ratios in the microtubules that could affect their dynamics and function was analyzed by stably expressing in MDCK cells βI tubulin from CHO cells. Three recombinant clones expressing different levels of the exogenous βI tubulin were selected and subcloned. Clone 17-2 showed the highest expression of CHO β1 tubulin. Total βI tubulin levels (MDCK+CHO) in the clones were approximately 1.8 to 1.1-fold higher than in mock-transfected cells only expressing MDCK β1 tubulin. In all the cells, βII tubulin levels remained unchanged. The cells expressing CHO β1 tubulin showed defective attachment, spreading, and delayed formation of adhesion sites at short times after plating, whereas mock-transfected cells attached and spread normally. Analysis of cytoskeletal fractions from clone 17-2 showed a MDCK βI/CHO βI ratio of 1.89 at 2 h that gradually decreased to 1.0 by 24 h. The ratio of the two isotypes in the soluble fraction remained unchanged, although with higher values than those found for the polymerized βI tubulin. By 24 h, the transfected cells had regained normal spreading and formed a confluent monolayer. Our results show that excess levels of total βI tubulin, resulting from the expression of the exogenous β1 isotype, and incorporation of it into microtubules affect their stability and some cellular functions. As the levels return to normal, the cells recover their normal phenotype. Regulation of βI tubulin levels implies the release of the MDCK βI isotype from the microtubules into the soluble fraction where it would be degraded. Cell Motil. Cytoskeleton 50:147–160, 2001. © 2001 Wiley-Liss, Inc.