[en] More than 100 triterpene glycosides (saponins) have been characterized in holothuroids in the past several decades. In particular, Holothuria forskali contains 26 saponins in its Cuvierian tubules and 12 in its body wall. This high diversity could be linked to a chemical defense mechanism, the most commonly accepted biological role for these secondary metabolites. We performed an integrated study of the body-wall saponins of H. forskali. The saponins are mainly localized in the epidermis and in the mesothelium of the body wall and appear to be released when the holothuroid is stressed. Among the saponins present in the epidermis, one (holothurinoside G) was detected in the seawater surrounding non-stressed holothuroids and three others (holohurinosides C and F, and desholothurin A) were secreted when the animals were stressed. In addition, two new congeners (detected at m/z 1301 and 1317) were also present in the immediate surroundings of stressed holothuroids. These new saponins do not originate from the epidermis and could come from an internal organ. Quantities of secreted saponins were very low compared with the body wall and Cuvierian tubules concentrations. At natural concentrations, saponins do not represent a threat to the health of predatory fish. The deterrent effect of saponins seems therefore to act as an aposematic signal, warning potential predators of the unpalatability of the holothuroid tissues.
Bakus, G. J. (1968). Defensive mechanisms and ecology of some tropical holothurians. Mar. Biol. 2, 23-32.
Becker, P. T. and Flammang, P. (2010). Unravelling the sticky threads of sea cucumbers - a comparative study on Cuvierian tubule morphology and histochemistry. In Biological Adhesive Systems - From Nature to Technical and Medical Application (ed. J. von Byern and I. Grunwald), pp. 87-98. Wien: Springer.
Bingham, B. L. and Braithwaite, L. F. (1986). Defense adaptations of the dendrochirote holothurian Psolus chitonoides Clark. J. Exp. Mar. Biol. Ecol. 98, 311-322.
Camazine, S. (1985). Olfactory aposematism. J. Chem. Ecol. 11, 1289-1295.
Caprioli, R. M., Farmer, T. B., and Gile, J. (1997). Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS. Anal Chem. 69, 4751-4760.
Da Silva, J., Cameron, J. L. and Frankboner, P. V. (1986). Movement and orientation patterns in the commercial sea cucumber Parastichopus californicus (Stimpson) (Holothuroidea: Aspidochirotida). Mar. Behav. Physiol. 12, 133-147.
Eisner, T. and Grant, R. P. (1980). Toxicity, odor aversion, and "olfactory aposematism". Science 213, 476.
Elyakov, G. B., Stonik, V. A., Levina, E. V., Slanke, V. P., Kuznetsova, T. A. and Levin, V. S. (1973). Glycosides of marine invertebrates - I. A comparative study of the glycosides fraction of Pacific sea cucumbers. Comp. Biochem. Physiol. 44, 325-336.
Flammang, P. and Jangoux, M. (1992). Functional morphology of the locomotory podia of Holothuria forskali (Echinodermata, Holothuroida). Zoomorphology 111, 167-178.
Francour, P. (1997). Predation on holothurians: a literature review. Invert. Biol. 116, 52-60.
Froese, R. and Pauly, D. (2010). FishBase, version 09/2010. World Wide Web electronic publication (www.fishbase.org
Hamel, J. F. and Mercier, A. (2000). Cuvierian tubules in tropical holothurian: usefulness and efficiency as a defence mechanism. Mar. Freshw. Behav. Physiol. 33, 115-139.
Kabat, E. A. and Mayer, M. M. (1967). Experimental Immunochemistry, 2nd edn, pp. 527. Springfield, IL: Thomas, C. C. Publisher.
Kalinin, V. I. (2000). System-theoretical (holistic) approach to the modeling of structural-functional relationships of biomolecules and their evolution: an example of triterpene glycosides from sea cucumbers (Echinodermata, Holothuroidea). J. Theor. Biol. 206, 151-168.
Kalinin, V. I., Prokofieva, N. G., Likhatskaya, G. N., Schentsova, E. B., Agafonova, I. G., Avilov, S. A. and Drozdova, O. A. (1996). Hemolytic activities of triterpene glycosides from the holothurian order Dendrochirotida: some trends in the evolution of this group of toxins. Toxicon 34, 475-483. (Pubitemid 26130126)
Kalinin, V. I., Aminin, D. L., Avilov, S. A., Silchenko, A. S. and Stonik, V. A. (2008). Triterpene glycosides from sea cucumbers (Holothurioidea, Echinodermata). Biological activities and function. Stud. Nat. Prod. Chem. 35, 135-196.
Kalyani, G. A., Kakrani, H. K. and Hukeri, V. I. (1988). Holothurin - a review. Indian J. Nat. Prod. 4, 3-8.
Kobayashi, M., Hori, M., Kan, K., Yasuzawa, T., Matsui, M., Suzuki, S. and Kitagawa, I. (1991). Marine natural product. XXVII. Distribution of lanostane-type triterpene oligoglycosides in ten kinds of Okinawan sea cucumbers. Chem. Pharm. Bull. 39, 2282-2287.
Kroop, R. K. (1982). Responses of five holothurian species to attacks by a predatory gastropod, Tonnax perdix. Pacific Sci. 36, 445-452.
Kubanek, J., Pawlik, J. R., Eve, T. M. and Fenical, W. (2000). Triterpene glycosides defend the Caribbean reef sponge Erylus formosus from predatory fishes. Mar. Ecol. Prog. Ser. 207, 69-77. (Pubitemid 32062390)
Kubanek, J., Whalen, K. E., Engel, S., Kelly, S. R., Henkel, T. P., Fenical, W. and Pawlik, J. R. (2002). Multiple defensive roles for triterpene glycosides from two Caribbean sponges. Oecologia 131, 125-136. (Pubitemid 36059204)
Lawrence, J. M. (1987). A Functional Biology of Echinoderms. London, Sydney: Croom Helm.
Lemaire, R., Tabet, J. C., Ducoroy, P., Hendra, J. B., Salzet, M. and Fournier, I. (2006). Solid ionic matrixes for direct tissue analysis and MALDI imaging. Anal. Chem. 78, 809-819. (Pubitemid 43230188)
Mackie, A. M., Lasker, R. and Grant, P. T. (1968). Avoidance reactions of a mollusc Buccinum undatum to saponin-like surface-active substances in extracts of the starfish Asterias rubens and Marthasterias glacialis. Comp. Biochem. Physiol. 26, 415-428.
Maier, S. M. (2008). Biological activities of sulphated glycosides from echinoderms. Nat. Prod. Chem. 35, 311-354.
Margolin, A. S. (1976). Swimming of the sea cucumber Parastichopus californicus (Stimpson) in response to sea stars. Ophelia 15, 105-114.
Massin, C. and Jangoux, M. (1976). Observations écologiques sur Holothuria tubulosa, H. polii et H. forskali et comportement alimentaire de H. tubulosa. Cah. Biol. Mar. 17, 45-59.
Motokawa, T. (1984). Connective tissue catch in echinoderms. Biol. Rev. 59, 255-270.
Nigrelli, R. F. (1952). The effect of holothurin on fish, and mice with sarcoma 180. Zoologica 37, 89-90.
Padove Cohen, S. A., Hatt, H., Kubanek, J. and McCarty, N. A. (2008). Reconstitution of a chemical defense signaling pathway in a heterologous system. J. Exp. Biol. 211, 599-605. (Pubitemid 351428887)
Plasman, V., Braekman, J. C., Daloze, D., Luhmer, M., Windsor, D. and Pasteels, J. M. (2000a). Triterpene saponins in the defensive secretion of a chrysomelid beetle, Platyphora ligata. J. Nat. Prod. 63, 646-649. (Pubitemid 30395521)
Plasman, V., Braekman, J. C., Daloze, D., Windsor, D. and Pasteels, J. M. (2000b). Triterpene saponins, quaternary ammonium compounds, phosphatidyl cholines, and amino acids in the pronotal and elytral secretions of Platyphora opima and Despogramma subtropica. J. Nat. Prod. 63, 1261-1264.
Plasman, V., Plehiers, M., Braekman, J. C., Daloze, D., de Biseau, J. C. and Pasteels, J. M. (2001). Chemical defense in Platyphora kollari Baly and Leptinostarsa behrensi Harold (Coleoptera: Chrysomelidae). Hypotheses on the origin and evolution of leaf beetles toxins. Chemoecology 11, 107-112. (Pubitemid 32882092)
Popov, A. M. (2002). A comparative study of the haemolytic and cytotoxic activities of triterpenoids isolated from ginseng and sea cucumbers. Biol. Bull. 29, 120-128. (Pubitemid 34281184)
Rodrigez, J., Castro, R. and Riguera, R. (1991). Holothurinosides: new antitumour non sulphated triterpenoid glycosides from the sea cucumber Holothuria forskali. Tetrahedron 47, 4753-4762.
Schulte, B. A. and Bakus, G. J. (1992). Predation deterrence in marine sponges: laboratory versus field studies. Bull. Mar. Sci. 50, 205-211. (Pubitemid 23399295)
Van Dyck, S., Gerbaux, P. and Flammang, P. (2009). Elucidation of molecular diversity and body distribution of saponins in the sea cucumber Holothuria forskali (Echinodermata) by mass spectrometry. Comp. Biochem. Physiol. 152B, 124-134.
Van Dyck, S., Gerbaux, P. and Flammang, P. (2010a). Qualitative and quantitative saponin contents in five sea cucumbers from the Indian Ocean. Mar. Drugs 8, 173-189.
Van Dyck, S., Flammang, P., Mériaux, C., Bonnel, D., Salzet, M., Fournier, I. and Wisztorski, M. (2010b). Localization of secondary metabolites in marine invertebrates: contribution of MALDI MSI for the study of saponins in Cuvierian tubules of H. forskali. PLoS One 5, e13923.
VandenSpiegel, D., Flammang, P., Fourmeau, D. and Jangoux, M. (1995). Fine structure of the dorsal papillae in the holothuroid Holothuria forskali (Echinodermata). Tissue Cell 27, 457-465.
Wilkie, I. C. (1996). Mutable collagenous tissues: extracellular matrix as mechanoeffector. In Echinoderm Studies, Vol. 5 (ed. M. Jangoux and J. M. Lawrence), pp. 61-102. Rotterdam: Balkema.
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. 219-248. Berlin: Springer-Verlag.
Yamanouchi, T. (1955). On the poisonous substance contained in holothurians. Publ. Seto Mar. Biol. Lab. 4, 183-203.
