The reaction of the sponge Chondrosia reniformis to mechanical stimulation is mediated by the outer epithelium and the release of stiffening factor(s) (original) (raw)
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Journal of Experimental Biology, 2006
SUMMARY The marine sponge Chondrosia reniformis Nardo consists largely of a collagenous tissue, the mesohyl, which confers a cartilaginous consistency on the whole animal. This investigation was prompted by the incidental observation that, despite a paucity of potentially contractile elements in the mesohyl, intact C. reniformis stiffen noticeably when touched. By measuring the deflection under gravity of beam-shaped tissue samples, it was demonstrated that the flexural stiffness of the mesohyl is altered by treatments that influence cellular activities, including [Ca2+]manipulation, inorganic and organic calcium channel-blockers and cell membrane disrupters, and that it is also sensitive to extracts of C. reniformis tissue that have been repeatedly frozen then thawed. Since the membrane disrupters and tissue extracts cause marked stiffening of mesohyl samples, it is hypothesised that cells in the mesohyl store a stiffening factor and that the physiologically controlled release of t...
Marine Environmental Research, 2014
Echinoderms and sponges share a unique feature that helps them face predators and other environmental pressures. They both possess collagenous tissues with adaptable viscoelastic properties. In terms of morphology these structures are typical connective tissues containing collagen fibrils, fibroblastand fibroclast-like cells, as well as unusual components such as, in echinoderms, neurosecretory-like cells that receive motor innervation. The mechanisms underpinning the adaptability of these tissues are not completely understood. Biomechanical changes can lead to an abrupt increase in stiffness (increasing protection against predation) or to the detachment of body parts (in response to a predator or to adverse environmental conditions) that are regenerated. Apart from these advantages, the responsiveness of echinoderm and sponge collagenous tissues to ionic composition and temperature makes them potentially vulnerable to global environmental changes.
Dynamic structure of the mesohyl in the sponge Chondrosia reniformis (Porifera, Demospongiae)
Zoomorphology, 2001
The common demosponge Chondrosia reniformis possesses the capacity to undergo an unusual creep process which results in the formation of long outgrowths from the parent body. These shape changes, which have been interpreted as adaptive strategies related to environmental factors, asexual reproduction or localised locomotor phenomena, are due mainly to the structural and mechanical adaptability of the collagenous mesohyl. This contribution describes the morphological correlates of mesohyl plasticisation in C. reniformis. The microscopic anatomy of the mesohyl was examined when it was in different physiological conditions: (1) standard "resting" condition, (2) "stiffened" condition and (3) dynamic "creep" condition. In this last case four representative regions of the sponge body were analysed: the parent region, the elongation region, the transition region and the propagule region. The results show that the histological modification of the sponge mesohyl during plasticisation is limited and localised. The most significant structural changes involve mainly cytological features of specific cellular components characterised by granule inclusions (i.e. the spherulous cells) and the arrangement and density of the collagenous extracellular framework, though the integrity of the collagen fibrils themselves is not affected.
Ultrastructural Studies on the Collagen of the Marine Sponge Chondrosia reniformis Nardo
Biomacromolecules, 2007
The ultrastructure of isolated fibrils of Chondrosia reniformis sponge collagen was investigated by collecting characteristic data, such as fibril thickness, width, D-band periodicity, and height modulation, using atomic force microscopy (AFM) and transmission electron microscopy (TEM). Therefore an adapted pre-processing of the insoluble collagen into homogeneous suspensions using neutral buffer solutions was essential, and several purification steps have been developed. Fourier transform infrared reflection-absorption spectroscopy (FT-IRAS) of the purified sponge collagen showed remarkable analogy of peak positions and intensities with the spectra of fibrillar calf skin type I collagen, despite the diverse phylogenetic and evolutionary origin. The sponge collagen's morphology is compared with that of other fibrillar collagens, and the typical banding of the separated single fibrils is discussed by comparison of topographical data obtained using AFM and corresponding TEM investigations using common staining methods. As the TEM images of the negatively stained fibrils showed alternating dark and light bands, AFM revealed a characteristic periodicity of protrusions (overlap zones) followed by two equal interband regions (gap zones). AFM and TEM results were correlated and multiperiodicity in Chondrosia collagen's banding is demonstrated. The periodic dark bands observed in TEM images correspond directly to the periodic protrusions seen by AFM. As a result, we provide an improved, updated model of the collagen's structure and organization.
Attachment of sponge cells to collagen substrata: Effect of a collagen assembly factor
Journal of Cell Science, 1985
Collagen, isolated from the sponge Geodia cydonium in the absence of denaturing agents, had the typical amino acid composition and was associated with the carbohydrates galactose and glucose. The resulting individual fibrils with a diameter of 23 nm, displayed a 19-5 nm periodicity with one intraperiod band. A collagen assembly factor (CAF) was identified in and partially purified from the extracellular space. The CAF reacted with antibodies against intact Geodia cells but not with antibodies against Geodia lectin and Geodia aggregation factor. In the presence of the CAF, the collagen fibrils reconstituted collagen bundles in an ordered sequence of events, which were followed by electron-microscopical and biochemical methods. Bundle formation was not dependent on the presence of the homologous lectin, glycoconjugates or aggregation factor. Homologous cells [Geodia archaeocytes) were determined to attach only to those Geodia collagen substrates that contained CAF. The attachment of these cells did not require fibronectin or Geodia lectin. Homologous glycoconjugates or NaOH-treated collagen inhibited cell attachment. Collagen from the sponge Chondrosia reniformis, even in the presence of Geodia CAF, was no appropriate substrate for Geodia cell attachment. Whether collagen is a component of cell-matrix interactions in sponge systems also in vivo is discussed.
Micro- and Macrorheology of Jellyfish Extracellular Matrix
Biophysical Journal, 2012
Mechanical properties of the extracellular matrix (ECM) play a key role in tissue organization and morphogenesis. Rheological properties of jellyfish ECM (mesoglea) were measured in vivo at the cellular scale by passive microrheology techniques: microbeads were injected in jellyfish ECM and their Brownian motion was recorded to determine the mechanical properties of the surrounding medium. Microrheology results were compared with macrorheological measurements performed with a shear rheometer on slices of jellyfish mesoglea. We found that the ECM behaved as a viscoelastic gel at the macroscopic scale and as a much softer and heterogeneous viscoelastic structure at the microscopic scale. The fibrous architecture of the mesoglea, as observed by differential interference contrast and scanning electron microscopy, was in accord with these scaledependent mechanical properties. Furthermore, the evolution of the mechanical properties of the ECM during aging was investigated by measuring microrheological properties at different jellyfish sizes. We measured that the ECM in adult jellyfish was locally stiffer than in juvenile ones. We argue that this stiffening is a consequence of local aggregations of fibers occurring gradually during aging of the jellyfish mesoglea and is enhanced by repetitive muscular contractions of the jellyfish.
Journal of Experimental Biology, 2005
Echinoderms possess mutable collagenous tissues (MCTs), which are capable of undergoing rapid changes in their passive mechanical properties mediated by secretions from a specific cell type, the juxtaligamental cell. In this study, the possible presence of MCTs in the tube feet of the echinoid Paracentrotus lividus and the asteroid Marthasterias glacialis was investigated by measuring their extensibility, tensile strength, stiffness and toughness after different treatments known to influence the physiological state of MCTs. Calcium removal reversibly induced a significant plasticization of the tube feet of both species. When exposed to celldisrupting solutions, the tube foot stem of sea urchins and sea stars showed a significant increase in strength, stiffness and toughness in the absence of calcium. This response, combined with the ultrastructural observation of juxtaligamental-like cells in the connective tissue, confirms that an MCT is present in both echinoid and asteroid tube feet. It was observed, however, that the tube foot stems of P. lividus and M. glacialis are affected differently by exposure to cell-disrupting solutions in the presence of calcium, indicating that their MCTs could be functionally different. In their soft state, MCTs could assist the muscles in tube foot protraction, bending and retraction; in their stiff state, they could play a role in the energy-sparing maintenance of position; for example, during strong attachment to the substratum to resist hydrodynamically generated loads.
Research Square (Research Square), 2021
In most animals, connective tissues such as the dermis or tendons present invariant mechanical properties, fine-tuned for their structural function. However, echinoderms, a group of sea creatures including sea cucumbers, possess the ability to voluntarily modify the mechanical properties of their connective tissues, which are therefore called mutable collagenous tissues (MCT). Understanding the molecular mechanism underlying MCT mutability is a prerequisite for the development of biomimetic smart dynamic materials. The stiffening and softening cycles of MCTs are made possible by the release of specialized effector proteins. We identified a stiffening factor from the dermis of Holothuria forskali, Hf-(D)Tensilin, and showed that it is localized in the secretory granules of juxtaligamental-like cells, a MCT specific cell type. Using recombinant proteins, we confirmed its effect on the dermis and its aggregation effect on extracted collagen fibrils. A model is proposed for the molecular interactions which mediate collagen fibrils cross-linking by tensilin.