Mechanical adaptability of a sponge extracellular matrix: evidence for cellular control of mesohyl stiffness inChondrosia reniformisNardo

Abstract

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 this factor is responsible for the touch-induced stiffening of intact animals.

Molecular Characterization of a Nonfibrillar Collagen from the Marine Sponge Chondrosia reniformis Nardo 1847 and Positive Effects of Soluble Silicates on Its Expression

“…The first ultrastructural studies have in principle shown some fibrillar forms (Heinemann et al 2007;Garrone et al 1975), and some recent findings have demonstrated other peculiarities of C. reniformis collagens, including the ability of mesohyl cells to affect collagen density. This process modifies directly extracellular macromolecules or the interactions between them, comparable with the dynamics known for the mutable collagenous tissue of echinoderms (Wilkie et al 2006). These peculiarities allow a very dynamic behavior of this species that can move or drop from its substratum, showing disarranged and separated fiber bundles, and the interfibrillar filamentous material that becomes markedly disorganized and rarefied (Bonasoro et al 2001).…”

“…1b), which should provide this molecule with some more flexibility (Exposito et al 2002), and the presence of some putative glycosylation sites also in the linker peptides and in the noncollagenic regions. These sites are probably involved in the mechanisms of specific cell-matrix interactions (Schröder et al 2006) or in protein-protein noncovalent interactions occurring in the complex and so far unexplained process of stiffening of C. reniformis tissues after mechanical stimuli (Wilkie et al 2006). The marine sponge C. reniformis is in fact one of the best available models for the molecular study of Porifera collagen.…”

“…The collagen of this animal has extraordinary characteristics of plasticity (Wilkie et al 2006), and its ultrastructural features (Heinemann et al 2007), as well as some details of its biochemical composition, have been described (Garrone et al 1975).…”

Molecular Cloning, Characterization, and Expression Analysis of a Prolyl 4-Hydroxylase from the Marine Sponge Chondrosia reniformis

“…The marine sponge Chondrosia reniformis is a common Mediterranean demosponge, which body consists of a large proportion of collagen. Due to its peculiar physical-chemical characteristics (Wilkie et al 2006), collagen derived from this sponge has been the object of study for 40 years (Garrone et al 1975;Heinemann et al 2007), and many biotechnological applications of C. reniformis collagen extracts in drug preparations (Nicklas et al 2009a, b) as well as in cosmetics (Swatschek et al 2002) have been described lately. Recently, a nonfibrillar collagen type from this sponge was cloned, and some information on the regulation of its gene expression (i.e., upregulation by soluble silicates) was also unveiled (Pozzolini et al 2012).…”

Matrix Metalloproteinases in a Sea Urchin Ligament with Adaptable Mechanical Properties

“…Aspects of it are admittedly speculative, but these are testable by further experimentation. The uniqueness of echinoderm MCT cannot be exaggerated: collagenous connective tissue that is directly innervated by the motor nervous system, and that can alter drastically and reversibly its mechanical properties within short physiological timescales, appears to have evolved only in the phylum Echinodermata (though a “pre-neural” version of the phenomenon occurs in the Porifera [55]). Despite this restricted taxonomic distribution, the investigation of MCT has the potential to provide information of widespread biomedical applicability [2], [56].…”