Is muscle involved in the mechanical adaptability of echinoderm mutable collagenous tissue?
School of Biological and Biomedical Sciences, Glasgow Caledonian University, Glasgow G4 0BA, Scotland
*e-mail: i.wilkie{at}gcal.ac.uk
Accepted 6 November 2001
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: Echinodermata, mutable collagenous tissue, connective tissue, extracellular matrix, muscle, juxtaligamental cell, mechanical properties, variable tensility.
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
What is the current concept of mutable connective tissue? |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
It is clear from transmission electron microscope observations that changes in the mechanical properties of MCT result from alterations in interfibrillar cohesion rather than in the collagen fibrils themselves. Other molecules that have been isolated from MCT can influence its interfibrillar cohesion. These include a stiparin inhibitor, which binds to stiparin and prevents its interaction with collagen, a stiffener and a plasticiser. There is evidence that the stiffener and plasticiser are stored in the juxtaligamental cells and that the mechanical properties of MCT are modulated by the release of these factors from the juxtaligamental cells by Ca2+-dependent cellular mechanisms (see Szulgit and Shadwick, 1994, 2000
; Trotter and Koob, 1995
; Trotter et al., 1996
, 1999
; Thurmond and Trotter, 1996
; Koob et al., 1999
; Wilkie et al., 1999
; Trotter, 2000
). The current concept of MCT thus attributes its mechanical adaptability entirely to the modulation of interactions between components of the extracellular matrix. Elphick and Melarange (2001
), in contrast, believe that enough evidence is available to justify the suggestion that this is not the whole story and that the mechanical adaptability of at least some mutable collagenous structures is due partly or, in one case, wholly to contractile cells.
![]() |
Mutable collagenous structures are functionally diverse |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The word friable is used here in an attempt to depict the complete loss of tensile strength and tendency to disintegrate of MCT in this physiological state. It should also be noted that there may not be a clear distinction between types A and B, since some type A structures may be able, in unusual circumstances, to destiffen enough to bring about detachment of body parts (Wilkie, 2001) and since experimental (but physiologically relevant) treatments can elicit extreme weakening of some type A structures in vitro. The order is also chosen deliberately to suggest an evolutionary sequence, with type A the most primitive and type C the most advanced, although the justification for this will be argued elsewhere.
In addition to changes in passive mechanical properties, some crinoid ligaments can generate an active contractile force (Birenheide and Motokawa, 1996b, 1998
; Birenheide et al., 2000
). As no myocytes or other possible cellular source of tension development have been detected in these ligaments (Birenheide and Motokawa, 1996b
, 1998
; Birenheide et al., 2000
; Holland and Grimmer, 1981a
), it appears that force production must be added to the functional repertoire of the MCT extracellular matrix.
Table 1 shows the pattern of passive tensile changes exhibited by all confirmed mutable collagenous structures and also indicates the occurrence of muscle cells in these structures. The following discussion assesses the possible role of muscle first in irreversible and then in reversible changes in mechanical properties.
|
![]() |
Irreversible destabilisation |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Reversible stiffening and destiffening |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
(i) Table 1 shows that muscle cells have been found in only four (21 %) of the 19 separate structures in which the capacity to stiffen and destiffen reversibly has been demonstrated. It thus seems reasonable to conclude that muscle plays no role in the mechanical adaptability of most mutable collagenous structures since it is highly unlikely that, over a period of 25 years, a succession of electron microscopists has overlooked myocytes, or other cells containing a contractile apparatus, that are numerous enough, or can generate sufficiently powerful contractions, to be responsible for the wide variation in stiffness shown by the structures containing them.
(ii) Elphick and Melarange (2001) refer explicitly to two of the four structures recorded as containing myocytes in Table 1. They consider that the contractile state of the small muscles connecting ossicles in the aboral dermis of asteroids probably influences the stiffness of the body wall. However, this supposition is not supported by the available evidence. In its stiffened state, the whole body wall of the spinulosid starfish Echinaster spinulosus has a breaking strength of approximately 40 MPa (ONeill, 1989
). The strongest known muscle is the anterior byssus retractor muscle (ABRM) of Mytilus edulis. Its breaking strength while generating a maximal isometric force of 1.4 MPa is approximately 10 MPa (Sugi et al., 1999
). Thus, the breaking strength of whole starfish body wall, less than 1 % of the volume of which is occupied by interossicular muscles (ONeill, 1989
), is four times that of the ABRM. The interossicular muscles cannot be responsible for the stiffened state of E. spinulosus body wall. Even in starfish that never become as rigid as spinulosids, such as forcipulatids, the variable tensility of the body wall cannot be attributed to these muscles: the breaking strength of Coscinasterias calamaria body wall, which probably contains approximately the same amount of muscle as that of E. spinulosus, is 3.3 MPa (ONeill and Withers, 1995
), and Wilkie et al. (1990
) estimated that, were they to be responsible for the acetylcholine-induced stiffening of the body wall of Asterias rubens, the muscular components would have to generate an active stress of 4.4 MPa, i.e. three times the maximal tension produced by the bivalve ABRM (Sugi et al., 1999
).
The second muscle-containing collagenous structure discussed by Elphick and Melarange (2001) is the capsular ligament, or catch apparatus, of the echinoid spine joint. They observe correctly that studies of this ligament led to the initial concept of neurally controlled connective tissue catch, but then state that "... the problem with this model is that there is no plausible molecular mechanism by which release of neurotransmitters by nerves could influence the mechanical state of collagen fibrils". This comment contains two inaccuracies. First, it has long been accepted that the variable tensility of MCT depends on changes in interfibrillar cohesion, not in the collagen fibrils themselves. Second, no-one, as far as I am aware, has ever suggested that neurotransmitters affect directly the mechanical properties of the extracellular matrix of this or any other mutable collagenous structure. The tensility of many isolated MCT preparations is affected by exogenous neurotransmitters that have always been assumed to be acting on cellular targets either juxtaligamental cells or neural elements that modulate the activity of these cells that remain in a functioning state in the excised tissue (Motokawa, 1987
; Wilkie et al., 1990
, 1995a
; Birenheide et al., 1996
, 2000
). For example, since there are juxtaligamental perikarya intermingling with conventional axons both within the capsular ligament and on its outer surface, isolated preparations of this ligament are bound to include intact juxtaligamental cells and perhaps also neurons (Takahashi, 1967a
; Smith et al., 1981
; Hidaka and Takahashi, 1983
; Peters, 1985
).
In support of their case, Elphick and Melarange (2001) cite the hypothesis of del Castillo and co-workers (del Castillo et al., 1995
; del Castillo and Smith, 1996
; Pérez-Acevedo et al., 1998
) according to which the destiffened state of the capsular ligament results from the sliding of ligament loops round calcite bars in the ossicle insertion regions, and the stiffened or catch condition is achieved by contraction of the intraligamental myocytes, which pulls the ligament loops against the calcite bars and prevents their slippage, a model that dispenses with the concept of mutable collagenous tissue altogether. This hypothesis is untenable for a number of reasons (detailed by Wilkie, 1996b
), the main one being that it depends on the myocytes being in series with the collagen fibres and being the only mechanically important linkage between them, even in the maximally stiffened state. This would mean that when the ligament supports a tensile load all of this load would be sustained by the myocytes. Hidaka and Takahashi (1983
) found that the acetylcholine-stiffened capsular ligament of Anthocidaris crassispina had a tensile strength of 1838 MPa. The myocytes occupy approximately 3 % of the cross-sectional area of this ligament. Were they in series with the collagen fibres, their tensile strength would need to be at least 600 MPa, 60 times that of the mollusc ABRM, which is highly improbable. Furthermore, this hypothesis ignores other evidence that the capsular ligament consists of MCT. It is, for example, stiffened dramatically by agents that cause cell disruption, such as distilled water or the non-ionic detergent Triton X-100 (Shadwick and Pollock, 1988
; Szulgit and Shadwick, 1994
), effects that could not be mediated by myocytes and that occur in other mutable collagenous structures that lack myocytes (Trotter and Koob, 1995
; Wilkie et al., 1995b
; Trotter and Chino, 1997
).
(iii) Elphick and Melarange (2001) believe that pharmacological data from two separate collagenous structures provide a further indication of the involvement of muscle in the variable tensility of MCT. Takahashi (1967b
) first reported that, when the echinoid capsular ligament is stretching under a constant load, acetylcholine arrests and adrenaline accelerates its extension. Because acetylcholine is the major excitatory neuromuscular transmitter in echinoderms, Elphick and Melarange (2001
) suggest that this, in itself, implies the involvement of muscle. It is also relevant to mention here that, by recording separately active force development and passive stiffness, del Castillo and co-workers discovered that there are similarities in the pharmacological characteristics of the contractile response of the capsular ligament, which is undoubtedly due to the myocytes, and its stiffening response (Morales et al., 1989
, 1993
; Vidal et al., 1993
). This was taken to indicate that contraction and catch are different aspects of one phenomenon shortening of the myocytes and led to the hypothesis discussed above. However, it has already been argued that the myocytes cannot be responsible for the changes in the passive mechanical properties of the capsular ligament that are induced by acetylcholine. Moreover, exogenous acetylcholine affects the mechanical properties of echinoderm collagenous structures that lack myocytes: it increases the stiffness of the central spine ligament of an echinoid (Motokawa, 1983
), destiffens the cirral ligament of a crinoid (Birenheide et al., 2000
) and has a biphasic stiffening/destiffening effect on the dermis of a holothurian (Motokawa, 1987
).
Clearly, then, there is no correlation between acetylcholine-induced changes in passive mechanical properties and the presence of muscle cells. The effects of acetylcholine on the stiffness of all these structures, capsular ligament included, can be explained only in terms of changes in the tensility of the extracellular matrix, and the only possible cellular effectors bringing about these changes are the juxtaligamental cells. That the activities of these cells are controlled at least partly by cholinergic pathways is indicated by both pharmacological data (cited above) and ultrastructural evidence for functional contacts between cholinergic nerve fibres and juxtaligamental perikarya (Cobb, 1985; Welsch et al., 1995
).
Elphick and Melarange (2001) also refer to two neuropeptides that have been isolated from the body wall of the aspidochirote holothurian Stichopus japonicus: NGIWYamide causes contraction of the longitudinal body wall muscle of this animal and increases the stiffness of isolated preparations of its dermis, whereas holokinin 1 inhibits electrically invoked contractions of the muscle and destiffens the dermis (Iwakoshi et al., 1995
; Birenheide et al., 1998
; Inoue et al., 1999
). Elphick and Melarange suggest that the responses of the dermis are due to muscle cells. Indeed, they assert that "It seems most likely that this effect of [holokinin 1] on body wall dermis is mediated by constituent muscle cells..." [my emphases]. This ignores the fact that ultrastructural investigations have failed to locate muscle cells in the dermis of S. japonicus (Motokawa, 1982b
) or other aspidochirotes (Junqueira et al., 1980
; Trotter and Chino, 1997
), and Stott et al. (1974
) found that a high-ionic-strength extract of the dermis of yet another aspidochirote showed no ATP-sensitivity, indicating that there is no contractile mechanism based on an actin/myosin interaction.
It needs to be reiterated that echinoderms possess two major mechano-effector systems consisting of muscles, which actively contract and relax, and extracellular matrix/juxtaligamental cell complexes, which undergo changes in passive stiffness (and sometimes develop force). These systems can form composites, as in the echinoid capsular ligament, or separate organs, such as aspidochirote body wall muscles and dermis. Whatever their mutual relationship, the two systems receive independent innervation, as has been demonstrated indisputably in crinoids (Birenheide et al., 2000), ophiuroids (Wilkie, 1979
) and holothurians (Inoue et al., 1999
) and for which there is evidence in the echinoid capsular ligament (Peters, 1985
). The pharmacological results cited above inform us only that there are features common to the control pathways regulating the two mechano-effector systems in echinoids and holothurians, i.e. they employ the same neurotransmitters or neuromodulators, and/or they include, at unknown locations, cellular receptors with similar properties.
![]() |
What is the role of muscle in the mutable collagenous structures that contain it? |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Intraligamental myocytes may, in particular circumstances, work synergistically with adjacent conventional muscles. For example, one function of the myocytes in the echinoid capsular ligament may be to assist the spine muscle in re-erecting the spine.
Finally, it is not impossible that intraligamental myocytes influence the passive mechanical properties of mutable collagenous structures when the extracellular matrix is itself in a compliant state, in the way that smooth muscle cells affect the wall stiffness of mammalian blood vessels, although this might be an incidental effect rather than a biological function of the myocytes in MCT. At present, however, there is no evidence for this, and none will be forthcoming until techniques are devised to incapacitate selectively either the intraligamental muscle or the molecular mechanisms responsible for the variable tensility of the extracellular matrix.
![]() |
Concluding remarks |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Birenheide, R. and Motokawa, T. (1994). Morphological basis and mechanics of arm movement in the stalked crinoid Metacrinus rotundus (Echinodermata, Crinoida). Mar. Biol. 121, 273283.
Birenheide, R. and Motokawa, T. (1996a). To be stiff or to be soft the dilemma of the echinoid tooth ligament. I. Morphology. Biol. Bull. 190, 218230.
Birenheide, R. and Motokawa, T. (1996b). Contractile connective tissue in crinoids. Biol. Bull. 191, 14.
Birenheide, R. and Motokawa, T. (1998). Crinoid ligaments: catch and contractility. In Echinoderms: San Francisco (ed. R. Mooi and M. Telford), pp. 139144. Rotterdam: Balkema.
Birenheide, R., Tamori, M., Motokawa, T., Ohtani, M., Iwakoshi, E., Muneoka, Y., Fujita, T., Minakata, H. and Nomoto, K. (1998). Peptides controlling stiffness of connective tissue in sea cucumbers. Biol. Bull. 194, 253259.
Birenheide, R., Tsuchi, A. and Motokawa, T. (1996). To be stiff or to be soft the dilemma of the echinoid tooth ligament. II. Mechanical properties. Biol. Bull. 190, 231236.
Birenheide, R., Yokoyama, K. and Motokawa, T. (2000). Cirri of the stalked crinoid Metacrinus rotundus: neural elements and the effect of cholinergic agonists on mechanical properties. Proc. R. Soc. Lond. B 267, 716.[Medline]
Byrne, M. (1985). The mechanical properties of the autotomy tissues of Eupentacta quinquesemita (Echinodermata: Holothuroidea) and the effects of certain physico-chemical agents. J. Exp. Biol. 117, 6986.
Byrne, M. (2001). The morphology of the autotomy structures in the sea cucumber Eupentacta quinquesemita before and during evisceration. J. Exp. Biol. 204, 849863.
Candia Carnevali, M. D., Bonasoro, F. and Wilkie, I. C. (1994). Structural and mechanical aspects of the mouth-frame of the brittlestar Ophioderma longicaudum (Retz.). In Echinoderms through Time (ed. B. David, A. Guille, J. P. Féral and M. Roux), pp. 387392. Rotterdam: Balkema.
Cobb, J. L. S. (1985). The motor innervation of the oral plate ligament in the brittlestar Ophiura ophiura (L.). Cell Tissue Res. 242, 685688.
del Castillo, J. and Smith, D. S. (1996). We still invoke friction and Occams razor to explain catch in the spines of Eucidaris tribuloides. Biol. Bull. 190, 243244.
del Castillo, J., Smith, D. S., Vidal, A. M. and Sierra, C. (1995). Catch in the primary spines of the sea urchin Eucidaris tribuloides: A brief review and a new interpretation. Biol. Bull. 188, 120127.
Elphick, M. R. and Melarange, R. (2001). Neural control of muscle relaxation in echinoderms. J. Exp. Biol. 204, 875885.
Grimmer, J. C., Holland, N. D. and Hayami, I. (1985). Fine structure of the stalk of an isocrinid sea lily (Metacrinus rotundus) (Echinodermata, Crinoidea). Zoomorphology 105, 3950.
Hidaka, M. and Takahashi, K. (1983). Fine structure and mechanical properties of the catch apparatus of the sea-urchin spine, a collagenous connective tissue with muscle-like holding capacity. J. Exp. Biol. 103, 114.
Hilgers, H. and Splechtna, H. (1982). Zur Steuerung der Ablösung von Giftpedizellarien bei Sphaerechinus granularis (Lam.) und Paracentrotus lividus (Lam.) (Echinodermata, Echinoidea). Zool. Jb. Anat. 107, 442457.
Hill, R. B. (2001). Role of Ca2+ in excitationcontraction coupling in echinoderm muscle: comparison with role in other tissues. J. Exp. Biol. 204, 897908.
Hill, R. B. and Rahemtulla, F. (1998). Cellular mechanism of pressure-triggered local degeneration in the body wall of a sea cucumber. Exp. Biol. Online 3 (Suppl. A1), 18.
Holland, N. D. and Grimmer, J. C. (1981a). Fine structure of the cirri and a possible mechanism for their motility in stalkless crinoids (Echinodermata). Cell Tissue Res. 214, 207217.[Medline]
Holland, N. D. and Grimmer, J. C. (1981b). Fine structure of syzygial articulations before and after arm autotomy in Florometra serratissima (Echinodermata: Crinoidea). Zoomorphology 98, 169183.
Inoue, M., Birenheide, R., Koizumi, O., Kobayakawa, Y., Muneoka, Y. and Motokawa, T. (1999). Localization of the neuropeptide NGIWYamide in the holothurian nervous system and its effects on muscular contraction. Proc. R. Soc. Lond. B 266, 9931000.
Iwakoshi, E., Ohtani, M., Takahashi, T., Muneoka, Y., Ikeda, T., Fujita, T., Minakata, H. and Nomoto, K. (1995). Comparative aspects of structure and action of bioactive peptides isolated from the sea cucumber Stichopus japonicus. In Peptide Chemistry 1994 (ed. M. Ohno), pp. 261264. Osaka: Protein Research Foundation.
Junqueira, L. C. U., Montes, G. S., Mourão, P. A. S., Carneiro, J., Salles, L. M. M. and Bonetti, S. S. (1980). Collagen proteoglycans interaction during autotomy in the sea cucumber, Stichopus badionotus. Rev. Can. Biol. 39, 157164.
Koob, T. J., Koob-Emunds, M. M. and Trotter, J. A. (1999). Cell-derived stiffening and plasticizing factors in sea cucumber (Cucumaria frondosa) dermis. J. Exp. Biol. 202, 22912301.
Morales, M., del Castillo, J. and Smith, D. S. (1989). Acetylcholine sensitivity of the spine-test articular capsule of the sea urchin Eucidaris tribuloides. Comp. Biochem. Physiol. 94C, 547554.
Morales, M., Sierra, C., Vidal, A., del Castillo, J. and Smith, D. S. (1993). Pharmacological sensitivity of the articular capsule of the primary spines of Eucidaris tribuloides. Comp. Biochem. Physiol. 105C, 2530.
Motokawa, T. (1981). The stiffness change of the holothurian dermis caused by chemical and electrical stimulation. Comp. Biochem. Physiol. 70C, 4148.
Motokawa, T. (1982a). Rapid change in mechanical properties of echinoderm connective tissues caused by coelomic fluid. Comp. Biochem. Physiol. 73C, 223229.
Motokawa, T. (1982b). Fine structure of the dermis of the body wall of the sea cucumber, Stichopus chloronotus, a connective tissue which changes its mechanical properties. Galaxea 1, 5564.
Motokawa, T. (1983). Mechanical properties and structure of the spine-joint central ligament of the sea urchin, Diadema setosum (Echinodermata, Echinoidea). J. Zool., Lond. 201, 223235.
Motokawa, T. (1986). Morphology of spines and spine joint in the crown-of-thorns starfish Acanthaster planci (Echinodermata, Asteroida). Zoomorphology 106, 247253.
Motokawa, T. (1987). Cholinergic control of the mechanical properties of the catch connective tissue in the holothurian body wall. Comp. Biochem. Physiol. 86C, 333337.
ONeill, P. L. (1989). Structure and mechanics of starfish body wall. J. Exp. Biol. 147, 5389.[Abstract]
ONeill, P. L. and Withers, P. C. (1995). An analysis of the load curve of the body wall of Coscinasterias calamaria (Echinodermata: Asteroidea). Mar. Freshwater Behav. Physiol. 25, 245260.
Pérez-Acevedo, N. L., Marrero, H. and del Castillo, J. (1998). Transient wrinkles in a variable length echinoid tendon. In Echinoderms: San Francisco (ed. R. Mooi and M. Telford), pp. 783790. Rotterdam: Balkema.
Peters, B. H. (1985). The innervation of spines in the sea-urchin Echinus esculentus L. Cell Tissue Res. 239, 219228.
Reynolds, S. E. (1980). Cuticle plasticizing factors. In Neurohormonal Techniques in Insects (ed. T. A. Miller), pp. 179195. Berlin: Springer-Verlag.
Shadwick, R. E. and Pollock, C. (1988). Dynamic mechanical properties of sea urchin spine ligaments. In Echinoderm Biology (ed. R. D. Burke, P. V. Mladenov, P. Lambert and R. L. Parsley), pp. 635640. Rotterdam: Balkema.
Smith, D. S., Wainwright, S. A., Baker, J. and Cayer, M. L. (1981). Structural features associated with movement and catch of sea-urchin spines. Tissue Cell 13, 299320.[Medline]
Stott, R. S. H., Hepburn, H. R., Joffe, I. and Heffron, J. J. A. (1974). The mechanical defensive mechanism of a sea cucumber. S. Afr. J. Sci. 70, 4648.
Sugi, H., Iwamoto, H., Shimo, M. and Shirakawa, I. (1999). Evidence for load-bearing structures specialized for the catch state in Mytilus smooth muscle. Comp. Biochem. Physiol. 122A, 347353.
Szulgit, G. K. and Shadwick, R. E. (1994). The effects of calcium chelation and cell perforation on the mechanical properties of sea urchin ligaments. In Echinoderms through Time (ed. B. David, A. Guille, J. P. Féral and M. Roux), pp. 887892. Rotterdam: Balkema.
Szulgit, G. K. and Shadwick, R. E. (2000). Dynamic mechanical characterization of a mutable collagenous tissue: response of sea cucumber dermis to cell lysis and dermal extracts. J. Exp. Biol. 203, 15391550.
Takahashi, K. (1967a). The catch apparatus of the sea-urchin spine. I. Gross histology. J. Fac. Sci. Univ. Tokyo IV 11, 109120.
Takahashi, K. (1967b). The catch apparatus of the sea-urchin spine. II. Responses to stimuli. J. Fac. Sci. Univ. Tokyo IV 11, 121130.
Takahashi, K. (1967c). The ball-and-socket joint of the sea-urchin spine: Geometry and its functional implications. J. Fac. Sci. Univ. Tokyo IV 11, 131135.
Thurmond, F. A. and Trotter, J. A. (1996). Morphology and biomechanics of the microfibrillar network of sea cucumber dermis. J. Exp. Biol. 199, 18171828.
Trotter, J. A. (2000). Echinoderm collagenous tissues: smart biomaterials with dynamically controlled stiffness. Comp. Biochem. Physiol. 126B, S95.
Trotter, J. A. and Chino, K. (1997). Regulation of cell-dependent viscosity in the dermis of the sea cucumber Actinopyga agassizi. Comp. Biochem. Physiol. 118A, 805811.
Trotter, J. A. and Koob, T. J. (1995). Evidence that calcium-dependent cellular processes are involved in the stiffening response of holothurian dermis and that dermal cells contain an organic stiffening factor. J. Exp. Biol. 198, 19511961.
Trotter, J. A., Lyons-Levy, G., Chino, K., Koob, T. J., Keene, D. R. and Atkinson, M. A. L. (1999). Collagen fibril aggregation inhibitor from sea cucumber dermis. Matrix Biol. 18, 569578.[Medline]
Trotter, J. A., Lyons-Levy, G., Luna, D., Koob, T. J., Keene, D. R. and Atkinson, M. A. L. (1996). Stiparin: a glycoprotein from sea cucumber dermis that aggregates collagen fibrils. Matrix Biol. 15, 99110.[Medline]
Vidal, A. M., del Castillo, J. and Smith, D. S. (1993). Contractile properties of the articular capsule or ligament, in the primary spines of the sea urchin Eucidaris tribuloides. Comp. Biochem. Physiol. 106C, 643647.
Welsch, U., Lange, A., Bals, R. and Heinzeller, T. (1995). Juxtaligamental cells in feather stars and isocrinids. In Echinoderm Research 1995 (ed. R. H. Emson, A. B. Smith and A. C. Campbell), pp. 129135. Rotterdam: Balkema.
Wilkie, I. C. (1979). The juxtaligamental cells of Ophiocomina nigra (Abildgaard) (Echinodermata: Ophiuroidea) and their possible role in mechano-effector function of collagenous tissue. Cell Tissue Res. 197, 515530.[Medline]
Wilkie, I. C. (1988). Design for disaster: The ophiuroid intervertebral ligament as a typical mutable collagenous structure. In Echinoderm Biology (ed. R. D. Burke, P. V. Mladenov, P. Lambert and R. L. Parsley), pp. 2538. Rotterdam: Balkema.
Wilkie, I. C. (1992). Variable tensility of the oral arm plate ligaments of the brittlestar Ophiura ophiura (Echinodermata: Ophiuroidea). J. Zool., Lond. 228, 526.
Wilkie, I. C. (1996a). Mutable collagenous tissues: extracellular matrix as mechano-effector. In Echinoderm Studies, vol. 5 (ed. M. Jangoux and J. M. Lawrence), pp. 61102. Rotterdam: Balkema.
Wilkie, I. C. (1996b). Mutable collagenous structure or not? A comment on the reinterpretation by del Castillo et al., of the catch mechanism in the sea-urchin spine ligament. Biol. Bull. 190, 237242.
Wilkie, I. C. (2001). Autotomy as a prelude to regeneration in echinoderms. Microsc. Res. Tech. (in press).
Wilkie, I. C., Candia Carnevali, M. D. and Andrietti, F. (1993). Variable tensility of the peristomial membrane of the sea-urchin Paracentrotus lividus (Lamarck). Comp. Biochem. Physiol. 105A, 493501.
Wilkie, I. C., Candia Carnevali, M. D. and Andrietti, F. (1994a). Microarchitecture and mechanics of the sea-urchin peristomial membrane. Boll. Zool. 61, 3951.
Wilkie, I. C., Candia Carnevali, M. D. and Bonasoro, F. (1992). The compass depressors of Paracentrotus lividus (Echinodermata, Echinoida): Ultrastructural and mechanical aspects of their variable tensility and contractility. Zoomorphology 112, 143153.
Wilkie, I. C., Candia Carnevali, M. D. and Bonasoro, F. (1998). Organization and mechanical behaviour of myocyte-ligament composites in a sea-urchin lantern: the compass depressors of Stylocidaris affinis (Echinodermata, Echinoida). Zoomorphology 118, 87101.
Wilkie, I. C., Candia Carnevali, M. D. and Bonasoro, F. (1999). Evidence for the cellular calcium regulation hypothesis from simple mutable collagenous structures: the brachial and cirral syzygial ligaments of Antedon mediterranea (Lam). In Echinoderm Research 1998 (ed. M. D. Candia Carnevali and F. Bonasoro), pp. 119125. Rotterdam: Balkema.
Wilkie, I. C. and Emson, R. H. (1987). The tendons of Ophiocomina nigra and their role in autotomy (Echinodermata, Ophiuroida). Zoomorphology 107, 3344.
Wilkie, I. C., Emson, R. H. and Mladenov, P. V. (1984). Morphological and mechanical aspects of fission in Ophiocomella ophiactoides (H. L. Clark) (Echinodermata: Ophiuroida). Zoomorphology 104, 310322.
Wilkie, I. C., Emson, R. H. and Mladenov, P. V. (1995a). Autotomy mechanism and its control in the starfish Pycnopodia helianthoides. In Echinoderm Research 1995 (ed. R. H. Emson, A. B. Smith and A. C. Campbell), pp. 137146. Rotterdam: Balkema.
Wilkie, I. C., Emson, R. H. and Young, C. M. (1994b). Variable tensility of the ligaments in the stalk of a sea-lily. Comp. Biochem. Physiol. 109A, 633641.
Wilkie, I. C., Griffiths, G. V. R. and Glennie, S. F. (1990). Morphological and physiological aspects of the autotomy plane in the aboral integument of Asterias rubens L. (Echinodermata). In Echinoderm Research (ed. C. De Ridder, P. Dubois, M. C. LaHaye and M. Jangoux), pp. 301313. Rotterdam: Balkema.
Wilkie, I. C., McKew, M. and Candia Carnevali, M. D. (1995b). Anomalous physico-chemical properties of the compass rotular ligaments in two species of sea-urchins: preliminary observations. In Echinoderm Research 1995 (ed. R. H. Emson, A. B. Smith and A. C. Campbell), pp. 147152. Rotterdam: Balkema.