Peptides Controlling Stiffness of Connective Tissue in Sea Cucumbers

Birenheide, R.; Tamori, Masaki; Motokawa, Tatsuo; Ohtani, Masahiro; Iwakoshi, Eiko; Muneoka, Yojiro; Fujita, Tetsuro; Minakata, Hiroyuki; Nomoto, Kyosuke

doi:10.2307/1543095

Cited by 58 publications

(54 citation statements)

References 17 publications

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“…GABA inhibited the AChinduced contraction in Sclerodactyla briareus , whereas in Actinopyga it had excitatory effects (Devlin, 2001). Muneoka and coworkers (Iwakoshi et al ., 1995;Birenheide et al ., 1998;Ohtani et al ., 1999) isolated 25 peptides from the present sea cucumber. Some of them may well inhibit AChinduced contraction, because about half of the peptides isolated showed inhibitory effects on the twitch contraction of LMBW invoked by electrical stimulation, and because stichopin, one of the 25 peptides, inhibits action of ACh in the body-wall catch connective tissue of the present sea cucumber (Birenheide et al , 1998).…”

Section: Discussionmentioning

confidence: 99%

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Innervation of Holothurian Body Wall Muscle: Inhibitory Effects and Localization of 5-HT

Inoue¹,

Tamori²,

Motokawa³

2002

Zoological Science

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Section: Discussionmentioning

confidence: 99%

“…Recently, several types of neuropeptides have been found in the nervous system of echinoderms (Thorndyke and Candia Carnevali, 2001). In sea cucumbers, it is suggested that some peptides work as neurotransmitters controlling muscles and catch connective tissues (Díaz-Miranda et al ., 1995;Birenheide et al ., 1998;Inoue et al ., 1999).…”

Section: Introductionmentioning

confidence: 99%

Innervation of Holothurian Body Wall Muscle: Inhibitory Effects and Localization of 5-HT

Inoue¹,

Tamori²,

Motokawa³

2002

Zoological Science

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“…It should be noted, however, that Ca 2+ depletion was not the essential condition for producing the soft state. The isolated dermis in nASW softened in response to various stimuli such as acetylcholine, holokinin, an endogenous peptide of sea cucumbers, and very strong mechanical stimulation (Motokawa, 1987;Motokawa, 1988;Birenheide et al, 1998), and thus the dermis could take the soft state with the presence of normal Ca 2+ concentration in bathing media. The exceptional case in nASW of the present study did show that tensilin could exert effects, although not strong, under the normal ionic condition with Ca 2+ .…”

Section: H-tensilin Stiffened the Dermis In The Soft Statementioning

confidence: 99%

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

Tamori

Yamada

Nishida

et al. 2006

Journal of Experimental Biology

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SUMMARY The dermis of sea cucumbers is a catch connective tissue or mutable connective tissue that exhibits large changes in mechanical properties. A stiffening protein, tensilin, has been isolated from the sea cucumber Cucumaria frondosa. We purified a similar protein, H-tensilin, from Holothuria leucospilota, which belongs to a different family to C. frondosa. H-tensilin appeared as a single band with an apparent molecular mass of 34 kDa on SDS-PAGE. No sugar chain was detected. Tryptic fragments of the protein had homology to known tensilin. H-tensilin aggregated isolated collagen fibrils in vitro in a buffer containing 0.5 mol l–1 NaCl with or without 10 mmol l–1 Ca2+. The activity of H-tensilin was quantitatively studied by dynamic mechanical tests on the isolated dermis. H-tensilin increased stiffness of the dermis in the soft state, induced by Ca2+-free artificial seawater, to a level comparable to that of the standard state, which was the state found in the dermis rested in artificial seawater with normal ionic condition. H-tensilin decreased the energy dissipation ratio of the soft dermis to a level comparable to that of the standard state. When H-tensilin was applied on the dermis in the standard state, it did not alter stiffness nor dissipation ratio. The subsequent application of artificial seawater in which the potassium concentration was raised to 100 mmol l–1increased stiffness by one order of magnitude. These findings suggest that H-tensilin is involved in the changes from the soft state to the standard state and that some stiffening factors other than tensilin are necessary for the changes from the standard to the stiff state.

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“…The three mechanical states differ not only in stiffness but also in various other mechanical parameters such as strain dependence and energy dissipation, and thus the standard state is not simply an intermediate state between the two extremes of soft and stiff states. These states could be produced in isolated dermis by various stimuli and peptides isolated from sea cucumbers (Birenheide et al, 1998). They are also produced by immersion of the isolated dermis in the following media: the standard state in natural seawater or artificial seawater with normal composition (nASW); the soft state in calcium-free artificial seawater (CaFASW); the stiff state in artificial seawater with elevated potassium concentration (KASW) (Motokawa and Tsuchi, 2003).…”

Section: Introductionmentioning

confidence: 99%

Evidence that water exudes when holothurian connective tissue stiffens

Tamori

Takemae

Motokawa

2010

Journal of Experimental Biology

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The only known molecule secreted from some cells that can change the stiffness is tensilin: a stiffening protein isolated from the body wall of sea cucumbers that causes aggregation of isolated collagen fibrils (Tipper et al., 2003). The amino acid sequence of tensilin is similar to that of the tissue inhibitor of metalloproteinase family proteins (Tipper et al., 2003). Based on these findings, Wilkie (Wilkie, 2005) presented a model of the molecular organization of catch connective tissues. He hypothesized that the tensilin and tensilin-specific protease system induces stiffening and destiffening. Our recent work, however, showed that his hypothesis can account for only half of the story at best: tensilin stiffens the soft dermis to form the standard state, but it does not cause further stiffening from the standard state to the stiff state (Tamori et al., 2006). So far, no protein has been isolated from the dermis that stiffens the dermis in the standard state to create the stiff state, and no model has been proposed for the molecular mechanism responsible for this transition. In the present study, we examined whether water movement is involved in this transition.The extracellular components of the holothurian dermis of the body wall include collagen fibers, microfibrils, proteoglycans, salts and water (Thurmond and Trotter, 1996). The microfibrils form a network (Thurmond and Trotter, 1996). Collagen fibers also seem Accepted 16 February 2010 SUMMARY The dermis of the body wall of sea cucumbers is composed mainly of extracellular materials such as collagens, proteoglycans and water; the water content is as high as 80%. Yet it shows rapid changes in stiffness under neural control. The dermis has been proposed to assume three mechanical states, soft, standard, and stiff. We investigated the relationship between the stiffness and the dermal mass and volume. Both the mass and volume decreased by 15% when the dermis stiffened from the standard state to the stiff state by mechanical stimulation and by chemical stimulation with potassium-rich seawater. The effect of the latter was abolished by anesthesia. The mass decrease was caused largely by water exudation. Tensilin, a holothurian protein that stiffens the soft dermis to form the standard state, did not cause any changes in mass. These results suggested that the stiffening mechanisms responsible for the transition from the soft state to the standard state, and that from the standard to the stiff state, are different. The removal of water from the dermis in the standard state, by soaking in hypertonic solution, caused only slight stiffening, which suggested that water exudation was not the direct cause of the stiffening. A change of pH of the surrounding medium, either more acidic or basic, was not associated with mass changes, although it caused a large increase in stiffness. The implications of the present results for the molecular mechanisms of the stiffness changes are discussed.

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Peptides Controlling Stiffness of Connective Tissue in Sea Cucumbers

Cited by 58 publications

References 17 publications

Innervation of Holothurian Body Wall Muscle: Inhibitory Effects and Localization of 5-HT

Innervation of Holothurian Body Wall Muscle: Inhibitory Effects and Localization of 5-HT

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

Evidence that water exudes when holothurian connective tissue stiffens

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