Mechanical adaptability of a sponge extracellular matrix: Evidence for cellular control of mesohyl stiffness in Chondrosia reniformis Nardo

Journal of Experimental Biology

Volumn 209, Issue 22, 2006, Pages 4436-4443

  Wilkie, I C ^a   Parma, L ^b   Bonasoro, F ^b   Bavestrello, G ^c   Cerrano, C ^d   Candia Carnevali, M D ^b  

^a GLASGOW CALEDONIAN UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

Author keywords

Connective tissue; Extracellular matrix; Mechanical properties; Mutable collagenous tissue; Sponge

Indexed keywords

ANIMAL; ARTICLE; BIOMECHANICS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DRUG EFFECT; EVOLUTION; EXTRACELLULAR MATRIX; HISTOLOGY; PHYSIOLOGY; SPONGE (PORIFERA); TENSILE STRENGTH;

ANIMALS; BIOMECHANICS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; EVOLUTION; EXTRACELLULAR MATRIX; PORIFERA; TENSILE STRENGTH;

ANIMALIA; CHONDROSIA RENIFORMIS;

EID: 33845800279     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.02527     Document Type: Article

References (35)

1. Bank, A. J., Wang, H., Holte, J. E., Mullen, K., Shammas, R. and Kubo, S. H. (1996). Contribution of collagen, elastin, and smooth muscle to in vivo human brachial artery wall stress and elastic modulus. Circulation 94, 3263-3270.
2. Bavestrello, G., Burlando, B. and Sarà, M. (1988). The architecture of the canal systems of Petrosia ficiformis and Chondrosia reniformis studied by corrosion casts (Porifera, Demospongiae). Zoomorphology 108, 161-166.
3. Bonasoro, F., Wilkie, I. C., Bavestrello, G., Cerrano, C. and Candia Carnevali, M. D. (2001). Dynamic structure of the mesohyl in the sponge Chondrosia reniformis (Porifera, Demospongiae). Zoomorphology 121, 109-121.
4. Bretting, H. and Königsmann, K. (1979). Investigations on the lectin-producing cells in the sponge Axinella polypoides (Schmidt). Cell Tissue Res. 201, 487-497.
5. Bretting, H., Jacobs, G., Donadey, C. and Vacelet, J. (1983). Immunohistochemical studies on the distribution and the function of the D-galactose-specific lectins in the sponge Axinella polypoides (Schmidt). Cell Tissue Res. 229, 551-571.
6. Chanas, B. and Pawlik, J. R. (1995). Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar. Ecol. Prog. Ser. 127, 195-211.
7. deVente, J. E., Lester, G. E., Trotter, J. A. and Dahners, L. E. (1997). Isolation of intact collagen fibrils from healing ligament. J. Electron Microsc. 46, 353-356.
8. Deutzmann, R., Fowler, S., Zhang, X., Boone, K., Dexter, S., Boot-Handford, R. P., Rachel, R. and Sarras, M. P. (2000). Molecular, biochemical and functional analysis of a novel and developmentally important fibrillar collagen (Hcol-I) in hydra. Development 127, 4669-4680.
9. Dixon, J. S., Hunter, J. A. A. and Steven, F. S. (1972). An electron microscopic study of the effect of crude bacterial α-amylase and ethylenediaminetetraacetic acid on human tendon. J. Ultrastruct. Res. 38, 466-472.
10. Gale, E. F., Cundliffe, E., Reynolds, P. E., Richmond, M. H. and Waring, M. J. (1981). The Molecular Basis of Antibiotic Action. London: John Wiley and Sons.
11. Garrone, R. (1978). Phylogenesis of Connective Tissue: Morphological Aspects and Biosynthesis of Sponge Intercellular Matrix (Frontiers of Matrix Biology 5). Basel: Karger.
12. Garrone, R., Huc, A. and Junqua, S. (1975). Fine structure and physicochemical studies on the collagen of the marine sponge Chondrosia reniformis Nardo. J. Ultrastruct. Res. 52, 261-275.
13. Grassé, P. P. (1973). Traité de Zoologie, Tome III: Spongiaires. Paris: Masson et Cie.
14. Harrison, F. W. and De Vos, L. (1991). Porifera. In Microscopic Anatomy of Invertebrates. Vol. 2 (ed. F. W. Harrison and E. E. Ruppert), pp. 29-89. New York: Wiley Liss.
15. Lorenz, B., Bohnensack, R., Gamulin, V., Steffen, R. and Müller, W. E. G. (1996). Regulation of motility of cells from marine sponges by calcium ions. Cell. Signal. 8, 517-524.
16. Motokawa, T. and Tsuchi, A. (2003). Dynamic mechanical properties of body-wall dermis in various mechanical states and their implications for the behavior of sea cucumbers. Biol. Bull. 205, 261-275.
17. Nickel, M. (2004). Kinetics and rhythm of body contractions in the sponge Tethya wilhelma (Porifera: Demospongiae). J. Exp. Biol. 207, 4515-4524.
18. Nickel, M. and Brümmer, F. (2003). In vitro sponge fragment culture of Chondrosia reniformis (Nardo, 1847). J. Biotechnol. 100, 147-159.
19. Ozeki, Y., Matsui, T., Yamamoto, Y., Funahashi, M., Hamako, J. and Titani, K. (1995). Tissue fibronectin is an endogenous ligand for galectin-1. Glycobiology 5, 255-261.
20. Redaelli, A., Vesentini, S., Soncini, M., Vena, P., Mantero, S. and Montevecchi, F. M. (2003). Possible role of decorin glycosaminoglycans in fibril to fibril force transfer in relative mature tendons - a computational study from molecular to microstructural level. J. Biomech. 36, 1555-1569.
21. Sarà, M. and Vacelet, J. (1973). Écologie des démosponges. In Traité de Zoologie, Tome III: Spongiaires (ed. P. P. Grassé), pp. 462-576. Paris: Masson et Cie.
22. Sasaki, N. and Odajima, S. (1996). Elongation mechanism of collagen fibrils and force-strain relations of tendon at each level of structural hierarchy. J. Biomech. 29, 1131-1136.
23. Simpson, T. L. (1984). The Cell Biology of Sponges. Berlin: Springer-Verlag.
24. Steven, F. S. (1967). The effect of chelating agents on collagen interfibrillar matrix interactions in connective tissue. Biochim. Biophys. Acta 140, 522-528.
25. 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, 1539-1550.
26. Tamori, M., Yamada, A., Nishida, N., Motobayashi, Y., Oiwa, K. and Motokawa, T. (2006). Tensilin-like stiffening protein from Holothuria leucospilota does not induce the stiffest state of catch connective tissue. J. Exp. Biol. 209, 1594-1602.
27. Tidball, J. G. (1994). Assembly of myotendinous junctions in the chick embryo: deposition of P68 is an early event in myotendinous junction formation. Dev. Biol. 163, 447-456.
28. Tipper, J. P., Lyons-Levy, G., Atkinson, M. A. L. and Trotter, J. A. (2003). Purification, characterization and cloning of tensilin, the collagen-fibril binding and tissue stiffening factor from Cucumaria frondosa dermis. Matrix Biol. 21, 625-635.
29. 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, 1951-1961.
30. Trotter, J. A., Lyons-Levy, G., Luna, D., Koob, T. J., Keene, D. and Atkinson, M. A. L. (1996). Stiparin: a glycoprotein from sea cucumber dermis that aggregates collagen fibrils. Matrix Biol. 15, 99-110.
31. Trotter, J. A., Tipper, J., Lyons-Levy, G., Chino, K., Heuer, A. H., Liu, Z., Mrksich, M., Hodneland, C., Dillmore, W. S., Koob, T. J. et al. (2000). Towards a fibrous composite with dynamically controlled stiffness: lessons from echinoderms. Biochem. Soc. Trans. 28, 357-362.
32. Wilkie, I. C. (2001). Autotomy as a prelude to regeneration in echinoderms. Microsc. Res. Tech. 55, 369-396.
33. Wilkie, I. C. (2005). Mutable collagenous tissue: overview and biotechnological perspective. In Echinodermata: Progress in Molecular and Subcellular Biology (39 Subseries, Marine Molecular Biotechnology) (ed. V. Matranga), pp. 221-250. Berlin: Springer-Verlag.
34. Wilkie, I. C., Bonasoro, F., Bavestrello, G., Cerrano, C. and Candia Carnevali, M. D. (2004). Mechanical properties of the collagenous mesohyl of Chondrosia reniformis: evidence for physiological control. Boll. Mus. Ist. Biol. Univ. Geneva 68, 665-672.
35. Zanetti, G. (2002). Dinamismo strutturale nella spugna Chondrosia reniformis (Porifera, Demospongiae): osservazioni in habitat. Tesi di Laurea, University of Milan, Italy.