Tensilin-like stiffening protein from<i>Holothuria leucospilota</i>does not induce the stiffest state of catch connective tissue

Tamori, Masaki; Yamada, Akira; Nishida, Norimasa; Motobayashi, Y.; Oiwa, Kazuhiro; Motokawa, Tatsuo

doi:10.1242/jeb.02178

Cited by 32 publications

(78 citation statements)

References 28 publications

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“…Specimens of the sea cucumbers (Holothuria leucospilota) were obtained from a commercial wholesaler (Marine Life) and delivered to the synchrotron SAXD beamline (in tanks of artificial sea water) a few hours before use. To prepare sea cucumber samples for the mechanical testing in different ionic solutions, we followed a protocol similar that used in previous studies of the mechanics of sea cucumber dermis (19,62). Specifically, after letting the sea cucumbers rest for 1 h in sea water, samples from the white central part of the body wall dermis (Fig.…”

Section: Methodsmentioning

confidence: 99%

Interfibrillar stiffening of echinoderm mutable collagenous tissue demonstrated at the nanoscale

Prévost

Blowes

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The mutable collagenous tissue (MCT) of echinoderms (e.g., sea cucumbers and starfish) is a remarkable example of a biological material that has the unique attribute, among collagenous tissues, of being able to rapidly change its stiffness and extensibility under neural control. However, the mechanisms of MCT have not been characterized at the nanoscale. Using synchrotron small-angle X-ray diffraction to probe time-dependent changes in fibrillar structure during in situ tensile testing of sea cucumber dermis, we investigate the ultrastructural mechanics of MCT by measuring fibril strain at different chemically induced mechanical states. By measuring a variable interfibrillar stiffness (E IF ), the mechanism of mutability at the nanoscale can be demonstrated directly. A model of stiffness modulation via enhanced fibrillar recruitment is developed to explain the biophysical mechanisms of MCT. Understanding the mechanisms of MCT quantitatively may have applications in development of new types of mechanically tunable biomaterials. mutable collagenous tissue | synchrotron small-angle X-ray diffraction | nanoscale mechanics | fibrillar deformation | sea cucumbers

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Section: Methodsmentioning

confidence: 99%

Interfibrillar stiffening of echinoderm mutable collagenous tissue demonstrated at the nanoscale

Prévost

Blowes

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Specimens of the sea cucumber Holothuria leucospilota Brandt were collected and kept in an aquarium, as described previously (Tamori et al, 2006). The body wall dermis was dissected and used for isolation of a stiffening factor and collagen fibrils, purification of H-tensilin and dynamic mechanical tests.…”

Section: Materials and Methods Animals Tissues And Dynamic Mechanicamentioning

confidence: 99%

“…Dynamic mechanical tests of the dermal pieces in nASW and CFASW were performed as described previously (Tamori et al, 2006). In brief, sinusoidal perturbation at the frequency of 0.3Hz was imposed on the isolated dermal pieces, and the tensile force was monitored.…”

Section: Materials and Methods Animals Tissues And Dynamic Mechanicamentioning

confidence: 99%

“…However, we revealed that the mechanism suggested above is at best only part of the whole story (Tamori et al, 2006). We isolated a protein that is similar to tensilin of Cucumaria frondosa from the dermis of the aspidochirotid sea cucumber Holothuria leucospilota.…”

Section: +mentioning

confidence: 96%

“…The tissues contain a large amount of the extracellular matrix, mainly consisting of collagen fibrils, proteoglycans and microfibrils (Trotter and Koob, 1989;Trotter et al, 1994;Thurmond and Trotter, 1996;Thurmond et al, 1997;Szulgit, 2007). The unique properties of these collagenous tissues might be due to lack of permanent associations between the collagen fibrils and the surrounding extracellular matrix because it is easy to isolate collagen fibrils from catch connective tissues -unlike collagenous tissues of adult vertebrates (Matsumura, 1974;Trotter and Koob, 1989;Trotter et al, 1994;Tamori et al, 2006;Szulgit, 2007). It seems that crosslinking of the collagen fibrils with adjacent ones and other components of the extracellular matrix is formed or broken during changes in the mechanical properties of catch connective tissues.…”

Section: Introductionmentioning

confidence: 99%

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A novel stiffening factor inducing the stiffest state of holothurian catch connective tissue

Yamada

Tamori

Iketani

et al. 2010

Journal of Experimental Biology

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SUMMARYThe dermis of sea cucumbers is a catch connective tissue or mutable collagenous tissue that shows large changes in stiffness. Extensive studies on the dermis revealed that it can adopt three different states having different mechanical properties that can be reversibly converted. These are the stiff, standard and soft states. The standard state is readily produced when a dermal piece is immersed in the sea water containing Ca 2+, whereas the soft state can be produced by removal of Ca 2+. A stiffening protein, tensilin, has been isolated from some sea cucumbers (Cucumaria frondosa and Holothuria leucospilota). Although tensilin converts the state of the dermis from soft to standard, it cannot convert from standard to stiff. In this study, we isolated and partially purified a novel stiffening factor from the dermis of Holothuria leucospilota. The factor stiffened the dermis in normal artificial sea water (ASW) but did not stiffen the soft dermis in Ca 2+ -free ASW. It also stiffened the dermis that had been converted to the standard state in Ca 2+ -free ASW by the action of tensilin. These results suggest that the factor produces the stiff dermis from the standard state but cannot work as a stiffener on the soft dermis. Its addition to longitudinal muscles of the sea cucumber produced no effects, suggesting that its effect is specific to the catch connective tissue. Its stiffening activity was susceptible to trypsin, meaning that it is a polypeptide, and its molecular mass estimated from gel filtration chromatography was 2.4kDa.

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Development of the zebrafish myoseptum with emphasis on the myotendinous junction

et al. 2011

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Zebrafish myosepta connect two adjacent muscle cells and transmit muscular forces to axial structures during swimming via the myotendinous junction (MTJ). The MTJ establishes transmembrane linkages system consisting of extracellular matrix molecules (ECM) surrounding the basement membrane, cytoskeletal elements anchored to sarcolema, and all intermediate proteins that link ECM to actin filaments. Using a series of zebrafish specimens aged between 24 h post-fertilization and 2 years old, the present paper describes at the transmission electron microscope level the development of extracellular and intracellular elements of the MTJ. The transverse myoseptum development starts during the segmentation period by deposition of sparse and loosely organized collagen fibrils. During the hatching period, a link between actin filaments and sarcolemma is established. The basal lamina underlining sarcolemma is well differentiated. Later, collagen fibrils display an orthogonal orientation and fibroblast-like cells invade the myoseptal stroma. A dense network of collagen fibrils is progressively formed that both anchor myoseptal fibroblasts and sarcolemmal basement membrane. The differentiation of a functional MTJ is achieved when sarcolemma interacts with both cytoskeletal filaments and extracellular components. This solid structural link between contractile apparatus and ECM leads to sarcolemma deformations resulting in the formation of regular invaginations, and allows force transmission during muscle contraction. This paper presents the first ultrastructural atlas of the zebrafish MTJ development, which represents an useful tool to analyse the mechanisms of the myotendinous system formation and their disruption in muscle disorders.

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Tensilin-like stiffening protein fromHolothuria leucospilotadoes not induce the stiffest state of catch connective tissue

Cited by 32 publications

References 28 publications

Interfibrillar stiffening of echinoderm mutable collagenous tissue demonstrated at the nanoscale

Interfibrillar stiffening of echinoderm mutable collagenous tissue demonstrated at the nanoscale

A novel stiffening factor inducing the stiffest state of holothurian catch connective tissue

Development of the zebrafish myoseptum with emphasis on the myotendinous junction

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