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Resilin-like protein in the clamp sclerites of the gill monogenean Diplozoon paradoxum Nordmann, 1832

Published online by Cambridge University Press:  03 September 2012

WEY LIM WONG ,
JAN MICHELS  and
STANISLAV N. GORB
WEY LIM WONG*
Affiliation:
Department of Functional Morphology and Biomechanics, Zoological Institute, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany
JAN MICHELS
Affiliation:
Department of Functional Morphology and Biomechanics, Zoological Institute, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany
STANISLAV N. GORB
Affiliation:
Department of Functional Morphology and Biomechanics, Zoological Institute, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany
*
*Corresponding author: Tel: +49 431 880 4517. Fax: +49 431 880 1389. E-mail: [email protected]
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Summary

Resilin is a soft and elastic protein, which is found in many exoskeletal structures of arthropods. Proteins with similar chemical properties have been described for other invertebrates including monogenean fish parasites. However, for the latter taxon no clear microscopic evidence for a resilin-like protein has been shown so far. Here, we present the results of detailed microscopic analyses of the clamp sclerites (attachment devices) of the monogenean Diplozoon paradoxum. Toluidine blue, which is known to stain resilin, selectively stained the material in the clamp sclerites. In addition, when exposed to UV light, this material exhibited an intense blue autofluorescence. The emission spectrum of this autofluorescence has its maximum at 424 nm and is nearly identical to emission spectra of blue autofluorescences observed in 2 well-studied structures containing high proportions of resilin in the exoskeleton of the locust Schistocerca gregaria. The results strongly indicate that the sclerite material of D. paradoxum contains a resilin-like protein. The presence of such a protein likely enhances the attachment efficiency of the clamp sclerites and increases their lifetime.

Keywords

attachmentautofluorescenceclamp scleriteDiplozoon paradoxumresilinSchistocerca gregaria
Type
Research Article
Information
Parasitology , Volume 140 , Issue 1 , January 2013 , pp. 95 - 98
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Andersen, S. O. (1964). The cross-links in resilin identified as dityrosine and trityrosine. Biochimica et Biophysica Acta 93, 213–215.CrossRefGoogle ScholarPubMed
Andersen, S. O. and Weis-Fogh, T. (1964). Resilin. A rubberlike protein in arthropod cuticle. Advances in Insect Physiology 2, 1–65. doi: 10.1016/S0065-2806(08)60071-5.CrossRefGoogle Scholar
Appel, E. and Gorb, S. N. (2011). Resilin-bearing wing vein joints in the dragonfly Epiophlebia superstes. Bioinspiration & Biomimetics 6, 1–11. doi: 10.1088/1748-3182/6/4/046006.CrossRefGoogle ScholarPubMed
Bennet-Clark, H. C. and Lucey, E. C. A. (1967). The jump of the flea: A study of the energetics and a model of the mechanism. Journal of Experimental Biology 47, 59–76.CrossRefGoogle Scholar
Bovet, J. (1967). Contribution à la morphologie et à la biologie de Diplozoon paradoxum von Nordmann 1832. Bulletin de la Société Neuchâteloise de Sciences Naturelles 90, 63–159.Google Scholar
Burrows, M. (2009). A single muscle moves a crustacean limb joint rhythmically by acting against a spring containing resilin. BMC Biology 7, 27. doi: 10.1186/1741-7007-7-27.CrossRefGoogle ScholarPubMed
Burrows, M. (2010). Energy storage and synchronisation of hind leg movements during jumping in planthopper insects (Hemiptera, Issidae). Journal of Experimental Biology 213, 469–478. doi: 10.1242/jeb.037861.CrossRefGoogle ScholarPubMed
Bychowsky, B. E. and Nagibina, L. F. (1959). Systematics of the genus Diplozoon Nordmann (Monogenoidea). Zoologicheskii Zhurnal 38, 362–377.Google Scholar
DeVore, D. P. and Gruebel, R. J. (1978). Dityrosine in adhesive formed by the sea mussel, Mytilus edulis. Biochemical and Biophysical Research Communications 80, 993–999. doi: 10.1016/0006-291X(78)91343-8.CrossRefGoogle ScholarPubMed
Foerder, C. A. and Shapiro, B. M. (1977). Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. Proceedings of the National Academy of Sciences, USA 74, 4214–4218.CrossRefGoogle ScholarPubMed
Gorb, S. N. (1999). Serial elastic elements in the damselfly wing: Mobile vein joints contain resilin. Naturwissenschaften 86, 552–555. doi: 10.1007/s001140050674.CrossRefGoogle ScholarPubMed
Gosline, J., Lillie, M., Carrington, E., Guerette, P., Ortlepp, C. and Savage, K. (2002). Elastic proteins: biological roles and mechanical properties. Philosophical Transactions of the Royal Society, B 357, 121–132. doi: 10.1098/rstb.2001.1022.CrossRefGoogle ScholarPubMed
Haas, F., Gorb, S. and Blickhan, R. (2000). The function of resilin in beetle wings. Proceedings of the Royal Society of London, B 267, 1375–1381. doi: 10.1098/rspb.2000.1153.CrossRefGoogle ScholarPubMed
Lopez-Llorca, L. V. and Fry, S. C. (1989). Dityrosine, trityrosine and tetratyrosine, potential cross-links in structural proteins of plant-parasitic nematodes. Nematologica 35, 165–179. doi: 10.1163/002825989X00304.CrossRefGoogle Scholar
Lyons, K. M. (1966). The chemical nature and evolutionary significance of monogenean attachment sclerites. Parasitology 56, 63–101. doi: 10.1017/S0031182000071109.CrossRefGoogle ScholarPubMed
Michels, J. and Büntzow, M. (2010). Assessment of Congo red as a fluorescence marker for the exoskeleton of small crustaceans and the cuticle of polychaetes. Journal of Microscopy 238, 95–101. doi: 10.1111/j.1365-2818.2009.03360.x.CrossRefGoogle ScholarPubMed
Michels, J. and Gorb, S. N. (2012). Detailed three-dimensional visualization of resilin in the exoskeleton of arthropods using confocal laser scanning microscopy. Journal of Microscopy 245, 1–16. doi: 10.1111/j.1365-2818.2011.03523.x.CrossRefGoogle ScholarPubMed
Michels, J., Vogt, J. and Gorb, S. N. (2012). Tools for crushing diatoms – opal teeth in copepods feature a rubber-like bearing composed of resilin. Scientific Reports 2, 465. doi: 10.1038/srep00465.CrossRefGoogle ScholarPubMed
Milne, S. J. and Avenant-Oldewage, A. (2006). The fluorescent detection of Paradiplozoon sp. (Monogenea: Diplozoidae) attachment clamps’ sclerites and integumental proteins. Onderstepoort Journal of Veterinary Research 73, 149–152.CrossRefGoogle ScholarPubMed
Owen, I. L. (1963). The attachment of the monogenean Diplozoon paradoxum to the gills of Rutilus rutilus L. II. Structure and mechanism of the adhesive apparatus. Parasitology 53, 463–468. doi: 10.1017/S003118200007390X.CrossRefGoogle Scholar
Perez Goodwyn, P., Peressadko, A., Schwarz, H., Kastner, V. and Gorb, S. N. (2006). Material structure, stiffness, and adhesion: why attachment pads of the grasshopper (Tettigonia viridissima) adhere more strongly than those of the locust (Locusta migratoria) (Insecta: Orthoptera). Journal of Comparative Physiology A 192, 1233–1243. doi: 10.1007/s00359-006-0156-z.CrossRefGoogle ScholarPubMed
Ramalingam, K. (1973). Chemical nature of monogenean sclerites. I. Stabilization of clamp-protein by formation of dityrosine. Parasitology 66, 1–7. doi: 10.1017/S0031182000044383.CrossRefGoogle ScholarPubMed
Weis-Fogh, T. (1961). Molecular interpretation of the elasticity of resilin, a rubber-like protein. Journal of Molecular Biology 3, 648–667. doi: 10.1016/S0022-2836(61)80028-4.CrossRefGoogle Scholar