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Inducible lectins with galectin properties and human IL1α epitopes opsonize yeast during the inflammatory response of the ascidian Ciona intestinalis

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Abstract

Studies on inducible ascidian lectins may shed light on the evolutionary emergence of cytokine functions. Here, we show that the levels of opsonins, with IL1α-epitopes, increase in Ciona intestinalis hemolymph as a response to an inflammatory stimulus and, in particular, to intratunic injection of lipopolysaccharide (LPS). The inflammatory agent promptly (within 4 h) enhances Ca2+-independent serum hemagglutinating and opsonizing activities, which are both inhibited by D-galactose and D-galactosides (α-lactose, N-acetyl-D-lactosamine, thio-digalactoside), suggesting that anti-rabbit erythrocyte lectins with galectin properties are involved as opsonins. Inducible galectin molecules contain interleukin-1α (IL1α) epitopes, and their activities are specifically inhibited by anti-human recombinant IL1α antibody. Analysis by SDS-polyacrylamide gel electrophoresis has revealed that the density of the bands of several serum proteins increases within 4 h after LPS injection, correlated with the enhanced serum activity. Moreover, Western blot patterns demonstrate that several serum proteins (59, 37, 30, 23, 15 kDa) cross-react with the antibody as early as 4 h post-injection. Although we have not been able to establish whether, in adition to galectins, various types of D-galactose-specific lectins are contained in the serum, we show, for the first time in invertebrates, that galectin molecules with opsonic properties can be enhanced in response to a non-specific inflammatory stimulus, and that their release can be further stimulated by LPS. Finally, we reveal that multiple galectins share human IL1α epitopes, probably because of steric configuration and the oligomerization process.

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Acknowledgements

We thank Prof. E.L. Cooper (David Geffen School of Medicine at UCLA) for helpful reading of the manuscript. Thanks are also due to Mr. G. Miceli for collecting the ascidians.

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Authors and Affiliations

  1. Dipartimento di Biologia Animale, Università di Palermo, Via Archirafi 18, 90123, Palermo, Italy

    Nicolò Parrinello, Vincenzo Arizza, Matteo Cammarata, Francesca Tiziana Giaramita, Margherita Pergolizzi, Mirella Vazzana, Aiti Vizzini & Daniela Parrinello

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  1. Nicolò Parrinello
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  2. Vincenzo Arizza
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  3. Matteo Cammarata
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Correspondence to Nicolò Parrinello.

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This work was supported by a research grant from the Italian Ministry of Education (PRIN 2004 4057000 to Nicolò Parrinello), co-funded by the University of Palermo.

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Parrinello, N., Arizza, V., Cammarata, M. et al. Inducible lectins with galectin properties and human IL1α epitopes opsonize yeast during the inflammatory response of the ascidian Ciona intestinalis . Cell Tissue Res 329, 379–390 (2007). https://doi.org/10.1007/s00441-007-0415-5

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