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The evolution of galactose α2,3-sialyltransferase: Cionaintestinalis ST3GAL I/II and Takifugu rubripes ST3GAL II sialylate Galβ1,3GalNAc structures on glycoproteins but not glycolipids

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Abstract

Sialyltransferases are a family of enzymes catalyzing the transfer of sialic acid residues to terminal non-reducing positions of oligosaccharide chains of glycoproteins and glycolipids. Although expression of sialic acid is well documented in animals of the deuterostomian lineage, sialyltransferases have been predominantly described for relatively recent vertebrate lineages such as birds and mammals. This study outlines the characterization of the only sialyltransferase gene found in the tunicate Ciona intestinalis, the first such report of a non-vertebrate deuterostomian sialyltransferase, which has been discussed as a possible orthologue of the common ancestor of galactose α2,3-sialyltransferases. We also report for the first time the characterization of a ST3Gal II gene from the bony fish Takifugu rubripes. We demonstrate that both genes encode functional α2,3-sialyltransferases that are structurally and functionally related to the ST3Gal family of mammalian sialyltransferases. However, characterization of the recombinant, purified forms of both enzymes reveal novel acceptor substrate specificities, with sialylation of the disaccharide Galβ1-3GalNAc and asialofetuin, but not GM1 or GD1b observed. This is in contrast to the mammalian ST3Gal II that predominantly sialylates gangliosides. Taken together the ceramide binding/recognition site previously proposed for the mouse ST3Gal II might represent a unique feature of mammalian ST3Gal II that is missing in the evolutionary more distant fish and tunicate species reported here. This suggests that during the evolution of the ST3Gal II, probably following the separation of the teleosts, a significant shift in substrate specificity enabling the sialylation of gangliosides took place.

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Acknowledgements

FL gratefully acknowledges the Deutsche Forschungsgemeinschaft (DFG) for the awarding of a Research Fellowship. SK acknowledges the funding by a Sir Allan Sewell Fellowship. MvI thanks the Australian Research Council (ARC) for the award of a Federation Fellowship and the Alexander von Humboldt Stiftung for the award of a von Humboldt Forschungspreis. JT gratefully acknowledges the ARC for the awarding of an Australian Postdoctoral Fellowship. The authors also wish to thank Dr. Milton Kiefel for providing helpful advice. We also wish to acknowledge the Consortium for Functional Glycomics Grant number GM62116 for providing the oligosaccharides used in this study.

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Authors and Affiliations

  1. Institute for Glycomics, Gold Coast Campus, Griffith University, QLD, 4222, Australia

    Friederike Lehmann, Mark von Itzstein & Joe Tiralongo

  2. Centre for Biomolecular Interactions Bremen, Department of Biology and Chemistry, University Bremen, 28334, Bremen, Germany

    Sørge Kelm & Frank Dietz

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  1. Friederike Lehmann
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Correspondence to Joe Tiralongo.

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Lehmann, F., Kelm, S., Dietz, F. et al. The evolution of galactose α2,3-sialyltransferase: Cionaintestinalis ST3GAL I/II and Takifugu rubripes ST3GAL II sialylate Galβ1,3GalNAc structures on glycoproteins but not glycolipids. Glycoconj J 25, 323–334 (2008). https://doi.org/10.1007/s10719-007-9078-4

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