The Structural Characterization of a C1q/TNF-α Domain Containing Lectin OXYL in the Feather Star Anneissia Japonica
DOI:
https://doi.org/10.64296/vijir.v1i1.03Keywords:
Lectin, C1q/TNF-α, β-Sandwich, Immunoglobulin G, Feather star, Anneissia japonicaAbstract
The structure of a lectin, OXYL, derived from the feather star, Anneissia japonica (phylum Echinodermata), was analyzed from biochemistry, informatics, and 3D structural prediction. OXYL’s primary structure resembled the globular domain of complement C1q in vertebrates. Structural simulations identified OXYL as part of the C1q/TNF superfamily, characterized by a jellyroll β-sandwich fold. The subunits can form monomer to nonamer (9-mer), with trimers being the most stable. However, gel permeation chromatography indicated tetramers as the significant form. In hemagglutination inhibition tests, OXYL bound type-2 N-acetyllactosamine (LacNAc: Galβ1-4GlcNAc) and inhibited agglutination but did not bind lactose (Lac: Galβ1-4Glc). Glycan microarray analysis with 20 immobilized glycans confirmed OXYL’s specificity for type-2 LacNAc and its sialic acid α2-3 linkage. The structural simulation showed a suitable molecular docking between type-2 LacNAc and the lectin rather than lactose. OXYL bound to the LacNAc glycan on the microarray was also elucidated to capture human IgG. This finding suggests that the invertebrate C1q/TNF family lectin will mimic vertebrate C1qs, despite lacking evolutionally antibody systems, possess the potential to interact with antibodies.
References
[1] Abramson J. et al. Accurate structure prediction of biomolecular interactions with AlphaFold 3, Nature, 2024: 630, 493-500, https://www.nature.com/articles/s41586-024-07487-w
[2] Almeida, P. et al. Glycans in trained immunity: Educators of innate immune memory in homeostasis and disease, Carbohydr Res, 2024: 544, 109245.
https://doi.org/10.1016/j.carres.2024.109245
[3] Altschul, S. F. et al. Basic local alignment search tool, J. Mol. Biol, 1990: 215, 403-410, https://www.sciencedirect.com/science/article/abs/pii/S0022283605803602?via%3Dihub
[4] Combs, S.A. et al. Small-molecule ligand docking into comparative models with Rosetta. Nat. Protoc, 2013: 8, 1277–1298.
[5] Deluca, S. et al. Fully flexible docking of medium sized ligand libraries with RosettaLigand. PLOS One, 2015: 19, e0132508
[6] Duarte, P.L. et al. A fibrinogen-related lectin from Echinometra lucunter represents a new FReP family in Echinodermata phylum, Fish Shellfish Immunol, 2022: 131, 150-159. https://linkinghub.elsevier.com/retrieve/pii/S1050464822006507
[7] Giga, Y. Ikai, A., & Takahashi, K. The complete amino acid sequence of echinoidin, a lectin from the coelomic fluid of the sea urchin Anthocidaris crassispina, Homologies with mammalian and insect lectins, J Biol Chem, 1987: 262, 6197-6203, https://www.jbc.org/article/S0021-9258(18)45556-1/pdf
[8] Hasan, I. et al. Functional characterization of OXYL, a SghC1qDC LacNAc-specific lectin from the crinoid feather star Anneissia japonica, Mar Drugs, 2019: 17, 136. https://www.mdpi.com/1660-3397/17/2/136
[9] Hashimoto, M. et al. Region-specific upregulation of HNK-1 glycan in the PRMT1-deficient brain, Biochim Biophys Acta, 2020: 1864, 129509.
https://doi.org/10.1016/j.bbagen.2019.129509
[10] Hatakeyama, T. et al. C-type lectin-like carbohydrate recognition of the hemolytic lectin CEL-III containing ricin-type β-trefoil folds, J Biol Chem, 2007: 282, 37826-37835, https://doi.org/10.1074/jbc.M705604200
[11] Hayashi, R. et al. Novel galectins purified from the sponge Chondrilla australiensis: Unique structural features and cytotoxic effects on colorectal cancer cells mediated by TF-antigen binding, Mar Drugs, 2024: 22, 400, https://doi.org/10.3390/md22090400
[12] Hirabayashi, J. et al. Lectin microarrays: Concept, principle and applications, Chem Soc Rev, 2013: 42, 443–458, https://doi.org/10.1039/C3CS35419A
[13] Holm, L., & Rosenström, P. Dali server: Conservation mapping in 3D. Nucleic Acids Res, 2010: 38, W545-549
https://academic.oup.com/nar/article/38/suppl_2/W545/1103717?login=true
[14] Imamichi, Y. et al. Purification, characterization and cDNA cloning of a lectin from the brittle star Ophioplocus japonicus, Comp Biochem Physiol B Biochem Mol Biol, 2022: 262, 110757, https://doi.org/10.1016/j.cbpb.2022.110757
[15] Kuno, A. et al. Evanescent-field fluorescence assisted lectin microarray: A new strategy for glycan profiling, Nat Methods, 2005: 2, 851–856.
https://doi.org/10.1038/nmeth803
[16] Li, Y. et al. Genomic insights of body plan transitions from bilateral to pentameral symmetry in Echinoderms, Commun Biol, 2020: 3, 371.
https://www.nature.com/articles/s42003-020-1091-1.
[17] Liu, F. T., & Stowell, S. R. The role of galectins in immunity and infection, Nat Rev Immunol, 2023: 23, 479-494, https://doi.org/10.1038/s41577-022-00829-7
[18] Lyskov, S. et al. Serverification of molecular modeling applications: The Rosetta Online Server that Includes Everyone (ROSIE), PLOS One, 2013, 8, e63906
[19] Matsumoto, R. et al. Glycomics of a novel type-2 N-acetyllactosamine-specific lectin purified from the feather star, Oxycomanthus japonicus (Pelmatozoa: Crinoidea), Comp Biochem Physiol B Biochem Mol Biol, 2011: 158, 266-273, https://doi.org/10.1016/j.cbpb.2010.12.004
[20] Mirdita, M. et al. ColabFold: Making protein folding accessible to all, Nat. Methods, 2022: 19, 679–682, https://www.nature.com/articles/s41592-022-01488-1
[21] Ozeki, Y. et al. Amino acid sequence and molecular characterization of a D-galactoside-specific lectin purified from sea urchin (Anthocidaris crassispina) eggs, Biochemistry, 1991: 30, 2391-2394.
https://pubs.acs.org/doi/abs/10.1021/bi00223a014
[22] Shao, Y. et al. Divergent immune roles of two fucolectin isoforms in Apostichopus japonicus, Dev Comp Immunol, 2018: 89, 1-6.
https://doi.org/10.1016/j.dci.2018.07.028
[23] Sugawara, H. et al. Characteristic recognition of N-acetylgalactosamine by an invertebrate C-type lectin, CEL-I, revealed by X-ray crystallographyic analysis, J Biol Chem, 2004: 279, 45219-45225. https://doi.org/10.1074/jbc.m408840200
[24] Yue, Z. et al. Advances in protein glycosylation and its role in tissue repair and regeneration, Glycoconj J, 2023: 40, 355-373. https://doi.org/10.1007/s10719-023-10117-8
[25] Zhang, C. et al. A tandem-repeat galectin-1 from Apostichopus japonicus with broad PAMP recognition pattern and antibacterial activity, Fish Shellfish Immunol, 2020: 99, 167-175. https://doi.org/10.1016/j.fsi.2020.02.011
