Abstract
In the past three decades a lot of research has been done on the extended family of carbohydrate-binding proteins from Sambucus nigra, including several so-called type 2 RIPs as well as hololectins. Although all these proteins have been studied for their carbohydrate-binding properties using hapten inhibition assays, detailed carbohydrate specificity studies have only been performed for a few Sambucus proteins. In particular SNA-I, has been studied extensively. Because of its unique binding characteristics this lectin was developed as an important tool in glycoconjugate research to detect sialic acid containing glycoconjugates. At present much less information is available with respect to the detailed carbohydrate binding specificity of other S. nigra lectins and RIPs, and as a consequence their applications remain limited. In this paper we report a comparative analysis of several lectins from S. nigra using the glycan microarray technology. Ultimately a better understanding of the ligands for each lectin can contribute to new/more applications for these lectins in glycoconjugate research. Furthermore, the data from glycan microarray analyses combined with the previously obtained sequence information can help to explain how evolution within a single lectin family eventually yielded a set of carbohydrate-binding proteins with a very broad specificity range.
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References
Broekaert, W.F., Nsimba-Lubaki, M., Peeters, B., Peumans, W.J.: A lectin from elder (Sambucus nigra L.) bark. Biochem. J. 221, 163–169 (1984)
Shibuya, N., Goldstein, I.J., Broekaert, W.F., Nsimba-Lubaki, M., Peeters, B., Peumans, W.J.: The elderberry (Sambucus nigra L.) bark lectin recognizes the NeuAc(α2,6)-Gal/GalNAc sequence. J. Biol. Chem. 262, 1596–1601 (1987)
Van Damme, E.J.M., Barre, A., Rougé, P., Van Leuven, F., Peumans, W.J.: The NeuAc(a-2,6) Gal/Gal-NAc-binding lectin from elderberry (Sambucus nigra) bark, a type-2 ribosome-inactivating protein with an unusual specificity and structure. Eur. J. Biochem. 235, 128–137 (1996)
Girbés, T., Ferreras, J.M., Arias, F.J., Muñoz, R., Iglesias, R., Jimenez, P., Rojo, M.A., Arias, Y., Perez, Y., Benitez, J., Sanchez, D., Gayoso, M.J.: Non-toxic type 2 ribosome-inactivating proteins (RIPs) from Sambucus: occurrence, cellular and molecular activities and potential uses. Cell. Mol. Biol. 49, 537–545 (2003)
Peumans, W.J., Kellens, J.T.C., Allen, A.K., Van Damme, E.J.M.: Isolation and characterization of a seed lectin from elderberry (Sambucus nigra) and its relationship to the bark lectins. Carbohydr. Res. 213, 7–17 (1991)
Kaku, H., Peumans, W.J., Goldstein, I.J.: Isolation and characterization of a second lectin (SNA-II) present in elderberry (Sambucus nigra L.) bark. Arch. Biochem. Biophys. 277, 255–262 (1990)
Mach, L., Waltraud, S., Ammann, M., Poetsch, J., Bertsch, W., Marz, L., Glossl, J.: Purification and partial characterization of a novel lectin from elder (Sambucus nigra L.) fruit. Biochem. J. 278, 667–671 (1991)
Van Damme, E.J.M., Barre, A., Rougé, P., Leuven, F.V., Peumans, W.J.: Characterization and molecular cloning of Sambucus nigra agglutinin V (nigrin b), a GalNAc-specific type-2 ribosome-inactivating protein from the bark of elderberry (Sambucus nigra). Eur. J. Biochem. 237, 505–513 (1996)
Van Damme, E.J.M., Roy, S., Rarre, A., Rougé, P., Van Leuven, F., Peumans, W.J.: The major elderberry fruit protein is a lectin derived from a truncated type 2 ribosome-inactivating protein. Plant J. 12, 1251–1260 (1997)
Peumans, W.J., Roy, S., Barre, A., Rougé, P., Van Leuven, F., Van Damme, E.J.: Elderberry (Sambucus nigra) contains truncated Neu5Ac(α-2,6)Gal/GalNAc-binding type 2 ribosome-inactivating proteins. FEBS Lett. 425, 35–39 (1998)
Van Damme, E.J.M., Barre, A., Rougé, P., Van Leuven, F., Peumans, W.J.: Isolation and molecular cloning of a novel type 2 ribosome-inactivating protein with an inactive B-chain from elderberry (Sambucus nigra) bark. J. Biol. Chem. 272, 8353–8360 (1997)
Mach, L., Kerschbaumer, R., Schwihla, H., Glossl, J.: Elder (Sambucus nigra L.) fruit lectin (SNA-IV) occurs in monomeric, dimeric and oligomeric isoforms. Biochem. J. 315, 1061 (1996)
Shibuya, N., Tazaki, K., Song, Z.W., Tarr, G.E., Goldstein, I.J., Peumans, W.J.: A comparative study of bark lectins from three elderberry (Sambucus) species. J. Biochem. 106, 1098–1103 (1989)
Maveyraud, L., Niwa, H., Guillet, V., Svergun, D.I., Konarev, P.V., Palmer, R.A., Peumans, W.J., Rouge, P., Van Damme, E.J.M., Reynolds, C.D., Mourey, L.: Structural basis for sugar recognition, including the Tn carcinoma antigen, by the lectin SNA-II from Sambucus nigra. Proteins 75, 89–103 (2009)
Rhodes, J.M., Campbell, B.J., Yu, L.G.: Lectin-epithelial interactions in the human colon. Biochem. Soc. Trans. 36, 1482–1486 (2008)
Boscher, C., Dennis, J.W., Nabi, I.R.: Glycosylation, galectins and cellular signaling. Curr. Opin. Cell Biol. 23, 383–392 (2011)
Van Damme, E.J.M., Smith, D.F., Cummings, R., Peumans, W.J.: Glycan arrays to decipher the specificity of plant lectins. Adv. Exp. Med. Biol. 705, 757–768 (2011)
Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M.E., Alvarez, R., Bryan, M.C., Fazio, F., Calarese, D., Stevens, J., Razi, N., Stevens, D.J., Skehel, J.J., Van Die, I., Burton, D.R., Wilson, I.A., Cummings, R., Bovin, N., Wong, C.H., Paulson, J.C.: Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. U. S. A. 101, 17033–17038 (2004)
Thompson, J.D., Higgins, D.G., Gilson, T.J.: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994)
Papadopoulos, J.S., Agarwala, R.: COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 23, 1073–1079 (2007)
Smith, D.F., Song, X., Cummings, R.D.: Use of glycan microarrays to explore specificity of glycan-binding proteins. Methods Enzymol. 480, 417–444 (2010)
Song, X., Yu, H., Chen, X., Lasanajak, Y., Tappert, M.M., Air, G.M., Tiwari, V.K., Cao, H., Chokhawala, H.A., Zheng, H., Cummings, R.D., Smith, D.F.: A sialylated glycan microarray reveals novel interactions of modified sialic acids with proteins and viruses. J. Biol. Chem. 286, 31610–31622 (2011)
Padler-Karavani, V., Song, X., Yu, H., Hurtado-Ziola, H., Huang, S., Muthana, S., Chokhawala, H.A., Cheng, J., Verhagen, A., Langereis, M.A., Kleene, R., Schachner, M., De Groot, R.J., Lasanajak, Y., Matsuda, H., Schwab, R., Chen, X., Smith, D.F., Cummings, R.D., Varki, A.: Cross-comparison of protein recognition of sialic acid diversity on two novel sialoglycan microarrays. J. Biol. Chem. 287, 22593–22608 (2012)
Stanley, P., Cummings, R.D.: Structures common to different glycans. In: Varki, A., Cummings, R.D., Esko, J.D., Freeze, P., Stanley, P., Bertozzi, C.R., Hart, G.W., Etzler, M.E. (eds.) Essentials of Glycobiology, 2nd edn, pp. 175–198. Cold Spring Harbor Laboratory Press, NY (2009)
Hazes, B.: The (QxW)3 domain: A flexible lectin scaffold. Protein Sci. 5, 1490–1501 (1996)
Robertus, J.D., Ready, M.P.: Ricin B-chain and discoidin I share a common primitive protein fold. J. Biol. Chem. 259, 13953–13956 (1984)
Rutenber, E., Ready, M., Robertus, J.: Structure and evolution of ricin B-chain. Nature 326, 624–626 (1987)
Montfort, W., Villafranca, J.E., Monzingo, A.F., Ernst, S.R., Katzin, B., Rutenber, E., Xuong, N.H., Hamlin, R., Robertus, J.D.: The three-dimensional structure of ricin at 2.8 Å. J. Biol. Chem. 262, 5398–5403 (1987)
Rutenber, E., Roberus, J.D.: Structure of ricin B-chain at 2.5 Å resolution. Proteins 10, 240–250 (1991)
Pascal, J.M., Day, P.J., Monzingo, A.F., Ernst, S.R., Robertus, J.D., Iglesias, R., Pérez, Y., Férreras, J.M., Citores, L., Girbés, T.: 2.8-Å Crystal structure of a nontoxic type-II ribosome-inactivating protein, ebulin l. proteins: structure, function. Genetics 43, 319–326 (2001)
Kaku, H., Kaneko, H., Minamihara, N., Iwata, K., Jordan, E.T., Rojo, M.A., Minami-Ishii, N., Minami, E., Hisajima, S., Shibuya, N.: Elderberry bark lectins evolved to recognize Neu5Acα2,6Gal/GalNAc sequence from a Gal/GalNAc binding lectin through the substitution of amino-acid residues critical for the binding to sialic acid. Biochem. J. 142, 393–401 (2007)
Van Damme, E.J.M., Roy, S., Barre, A., Citores, L., Mostafapous, K., Rougé, P., Van Leuven, F., Girbés, T., Goldstein, I.J., Peumans, W.J.: Elderberry (Sambucus nigra) bark contains two structurally different Neu5Ac(α-2,6)Gal/GalNAc-binding type 2 ribosome-inactivating proteins. Eur. J. Biochem. 245, 648–655 (1997)
Mo, H., Winter, H.C., Goldstein, I.J.: Purification and characterization of a Neu5Ac α2-6Galβ1-4Glc/GlcNAc-specific lectin from the fruiting body of the polypore mushroom Polyporus squamosus. J. Biol. Chem. 275, 10623–10629 (2000)
Kadirvelraj, R., Grant, O.C., Goldstein, I.J., Winter, H.C., Tateno, H., Fadda, E., Woods, R.J.: Structure and binding analysis of Polyporus squamosus lectin in complex with the Neu5Acα2-6 Galβ1-4GlcNAc human-type influenza receptor. Glycobiology 21, 973–984 (2011)
Yabe, R., Suzuki, R., Kuno, A., Fujimoto, Z., Jigami, Y., Hirabayashi, J.: Tailoring a novel sialic acid-binding lectin from a ricin-B chain-like galactose-binding protein by natural evolution-mimicry. J. Biochem. 141, 389–399 (2007)
Wang, Y., Yu, G., Han, Z., Yang, B., Hu, Y., Zhao, X., Wu, J., Lv, Y., Chai, W.: Specificities of Ricinus communis agglutinin 120 interaction with sulfated galactose. FEBS Lett. 585, 3927–3934 (2011)
Hu, D., Tateno, H., Kuno, A., Yabe, R., Hirabayashi, J.: Directed evolution of lectins with sugar-binding specificity for 6-sulfo-galactose. J. Biol. Chem. 287, 20313–20320 (2012)
Chen, Y., Rougé, P., Peumans, W.J., Van Damme, E.J.M.: Mutational analysis of carbohydrate-binding activity of the NeuAc(α-2,6)Gal/GalNAc-specific type 2 ribosome-inactivating protein from elderberry (Sambucus nigra) fruits. Biochem. J. 364, 587–592 (2002)
Van Damme, E.J.M., Peumans, W.J., Barre, A., Rougé, P.: Plant lectins: a composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles. Crit. Rev. Plt. Sci. 17, 575–692 (1998)
Ferreras, J.M., Citores, L., Iglesias, R., Jiménez, P., Girbés, T: Sambucus ribosome-inactivating proteins and lectins. (Lord, J.M., Hartley, M,R., Eds.), pp.122-123, Chapter 6. Toxic Plant Proteins, Plant Cell Monographs 18, Springer-Verlag Berlin Heidelberg (2010)
Chen, Y., Peumans, W.J., Van Damme, E.J.M.: The Sambucus nigra type-2 ribosome-inactivating protein SNA-I’ exhibits in planta antiviral activity in transgenic tobacco. FEBS J. 516, 27–30 (2002)
Shahidi Noghabi, S., Van Damme, E.J.M., Smagghe, S.: Carbohydrate-binding activity of the type-2 ribosome-inactivating protein SNA-I from elderberry (Sambucus nigra) is a determining factor for its insecticidal activity. Phytochemistry 69, 2972–2978 (2008)
Shahidi-Noghabi, S., Van Damme, E.J.M., Smagghe, G.: Expression of Sambucus nigra agglutinin (SNA-I’) from elderberry bark in transgenic tobacco plants results in enhanced resistance to different insect species. Transgenic Res. 18, 249–259 (2009)
Battelli, M., Citores, L., Buonamici, L., Ferreras, J.M., De Benito, F.M., Girbés, T., Stirpe, F.: Toxicity and cytotoxicity of nigrin b, a two-chain ribosome-inactivating protein from Sambucus nigra : comparison with ricin. Arch. Toxicol. 71, 360–364 (1997)
Shahidi-Noghabi, S., Van Damme, E.J.M., De Vos, W.H., Smagghe, G.: Internalization of Sambucus nigra agglutinins I and II in insect midgut cells. Arch. Insect Biochem. Physiol. 76, 211–222 (2011)
Shang, C., Madej, M., De Vos, W., Van Damme, E.J.M.: The ribosome-inactivating proteins (RIPs) from elderberry (Sambucus nigra) in the battle against cancer?? Glycoconj. J. 30, 355 (2013)
Acknowledgments
This work was funded primarily by the Fund for Scientific Research-Flanders (FWO grants G.0022.08) and the Research Council of Ghent University (project BOF10/GOA/003). Chenjing Shang is recipient of China Scholarship Council and receives doctoral co-funding from the Special Research Council of Ghent University. The authors want to thank the Consortium for Functional Glycomics funded by the NIGMS GM62116 for the glycan array analysis. Special thanks to Willy J. Peumans for purification of the proteins and critical reading of the manuscript.
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Shang, C., Van Damme, E.J.M. Comparative analysis of carbohydrate binding properties of Sambucus nigra lectins and ribosome-inactivating proteins. Glycoconj J 31, 345–354 (2014). https://doi.org/10.1007/s10719-014-9527-9
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DOI: https://doi.org/10.1007/s10719-014-9527-9