Linear triazole-linked pseudo oligogalactosides as scaffolds for galectin inhibitor development.
1,2,3-triazole
X-ray crystallography
carbohydrate mimetics
galectin
galectin-3 inhibitor
oligogalactosides
Journal
Chemical biology & drug design
ISSN: 1747-0285
Titre abrégé: Chem Biol Drug Des
Pays: England
ID NLM: 101262549
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
20
08
2019
revised:
10
01
2020
accepted:
14
03
2020
pubmed:
29
3
2020
medline:
8
7
2021
entrez:
29
3
2020
Statut:
ppublish
Résumé
Galectins play key roles in numerous biological processes. Their mode of action depends on their localization which can be extracellular, cytoplasmic, or nuclear and is partly mediated through interactions with β-galactose containing glycans. Galectins have emerged as novel therapeutic targets notably for the treatment of inflammatory disorders and cancers. This has stimulated the design of carbohydrate-based inhibitors targeting the carbohydrate recognition domains (CRDs) of the galectins. Pursuing this approach, we reasoned that linear oligogalactosides obtained by straightforward iterative click chemistry could mimic poly-lactosamine motifs expressed at eukaryote cell surfaces which the extracellular form of galectin-3, a prominent member of the galectin family, specifically recognizes. Affinities toward galectin-3 consistently increased with the length of the representative oligogalactosides but without reaching that of oligo-lactosamines. Elucidation of the X-ray crystal structures of the galectin-3 CRD in complex with a synthesized di- and tri-galactoside confirmed that the compounds bind within the carbohydrate-binding site. The atomic structures revealed that binding interactions mainly occur with the galactose moiety at the non-reducing end, primarily with subsites C and D of the CRD, differing from oligo-lactosamine which bind more consistently across the whole groove formed by the five subsites (A-E) of the galectin-3 CRD.
Substances chimiques
Biopolymers
0
Galactosides
0
Galectins
0
Triazoles
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1123-1133Informations de copyright
© 2020 John Wiley & Sons A/S.
Références
André, S., Frisch, B., Kaltner, H., Desouza, D. L., Schuber, F., & Gabius, H. J. (2000). Lectin-mediated drug targeting : Selection of valency, sugar type (Gal/Lac), and spacer length for cluster glycosides as parameters to distinguish ligand binding to C-type asialoglycoprotein receptors and galectins. Pharmaceutical Research, 17(8), 985-990.
André, S., Renaudet, O., Bossu, I., Dumy, P., & Gabius, H.-J. (2011). Cyclic neoglycodecapeptides: How to increase their inhibitory activity and selectivity on lectin/toxin binding to a glycoprotein and cells. Journal of Peptide Science, 17(6), 427-437. https://doi.org/10.1002/psc.1338
André, S., Wang, G.-N., Gabius, H.-J., & Murphy, P. V. (2014). Combining glycocluster synthesis with protein engineering: An approach to probe into the significance of linker length in a tandem-repeat-type lectin (galectin-4). Carbohydrate Research, 389, 25-38. https://doi.org/10.1016/j.carres.2013.12.024
Atmanene, C., Ronin, C., Téletchéa, S., Gautier, F.-M., Djedaïni-Pilard, F., Ciesielski, F., … Grandjean, C. (2017). Biophysical and structural characterization of mono/di-arylated lactosamine derivatives interaction with human galectin-3. Biochemical and Biophysical Research Communications, 489(3), 281-286. https://doi.org/10.1016/j.bbrc.2017.05.150
Baron, A., Blériot, Y., Sollogoub, M., & Vauzeilles, B. (2008). Phenylenediamine catalysis of « click glycosylations » in water : Practical and direct access to unprotected neoglycoconjugates. Organic & Biomolecular Chemistry, 6(11), 1898-1901. https://doi.org/10.1039/b805528a
Barondes, S. H., Castronovo, V., Cooper, D. N., Cummings, R. D., Drickamer, K., Feizi, T., … Kasai, K. (1994). Galectins: A family of animal beta-galactoside-binding lectins. Cell, 76(4), 597-598.
Bian, C.-F., Zhang, Y., Sun, H., Li, D.-F., & Wang, D.-C. (2011). Structural basis for distinct binding properties of the human galectins to Thomsen-Friedenreich antigen. PLoS ONE, 6(9), e25007. https://doi.org/10.1371/journal.pone.0025007
Bonandi, E., Christodoulou, M. S., Fumagalli, G., Perdicchia, D., Rastelli, G., & Passarella, D. (2017). The 1,2,3-triazole ring as a bioisostere in medicinal chemistry. Drug Discovery Today, 22(10), 1572-1581. https://doi.org/10.1016/j.drudis.2017.05.014
Bresalier, R. S., Byrd, J. C., Wang, L., & Raz, A. (1996). Colon cancer mucin: A new ligand for the beta-galactoside-binding protein galectin-3. Cancer Research, 56(19), 4354-4357.
Campo, V. L., Ivanova, I. M., Carvalho, I., Lopes, C. D., Carneiro, Z. A., Saalbach, G., … Field, R. A. (2015). Click chemistry oligomerisation of azido-alkyne-functionalised galactose accesses triazole-linked linear oligomers and macrocycles that inhibit Trypanosoma cruzi macrophage invasion. Tetrahedron, 71(39), 7344-7353. https://doi.org/10.1016/j.tet.2015.04.085
Collins, P. M., Bum-Erdene, K., Yu, X., & Blanchard, H. (2014). Galectin-3 interactions with glycosphingolipids. Journal of Molecular Biology, 426(7), 1439-1451. https://doi.org/10.1016/j.jmb.2013.12.004
Collins, P. M., Hidari, K. I. P. J., & Blanchard, H. (2007). Slow diffusion of lactose out of galectin-3 crystals monitored by X-ray crystallography: Possible implications for ligand-exchange protocols. Acta Crystallographica, Section D: Biological Crystallography, 63(Pt 3), 415-419. https://doi.org/10.1107/S090744490605270X
Dam, T. K., & Brewer, C. F. (2008). Effects of clustered epitopes in multivalent ligand-receptor interactions. Biochemistry, 47(33), 8470-8476. https://doi.org/10.1021/bi801208b
Dange, M. C., Srinivasan, N., More, S. K., Bane, S. M., Upadhya, A., Ingle, A. D., … Kalraiya, R. D. (2014). Galectin-3 expressed on different lung compartments promotes organ specific metastasis by facilitating arrest, extravasation and organ colonization via high affinity ligands on melanoma cells. Clinical & Experimental Metastasis, 31(6), 661-673. https://doi.org/10.1007/s10585-014-9657-2
Delaine, T., Collins, P., MacKinnon, A., Sharma, G., Stegmayr, J., Rajput, V. K., … Nilsson, U. J. (2016). Galectin-3-binding glycomimetics that strongly reduce bleomycin-induced lung fibrosis and modulate intracellular glycan recognition. ChemBioChem, 17(18), 1759-1770. https://doi.org/10.1002/cbic.201600285
Dion, J., Advedissian, T., Storozhylova, N., Dahbi, S., Lambert, A., Deshayes, F., … Grandjean, C. (2017). Development of a sensitive microarray platform for the ranking of galectin inhibitors: Identification of a selective galectin-3 inhibitor. ChemBioChem, 18(24), 2428-2440. https://doi.org/10.1002/cbic.201700544
Dubé-Delarosbil, C., & St-Pierre, Y. (2018). The emerging role of galectins in high-fatality cancers. Cellular and Molecular Life Sciences, 75(7), 1215-1226. https://doi.org/10.1007/s00018-017-2708-5
Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. (2010). Features and development of coot. Acta Crystallographica, Section D: Biological Crystallography, 66(Pt 4), 486-501. https://doi.org/10.1107/S0907444910007493
Fischöder, T., Laaf, D., Dey, C., & Elling, L. (2017). Enzymatic synthesis of N-acetyllactosamine (LacNAc) type 1 oligomers and characterization as multivalent galectin ligands. Molecules, 22(8), 1320. https://doi.org/10.3390/molecules22081320
Fort, S., Kim, H.-S., & Hindsgaul, O. (2006). Screening for galectin-3 inhibitors from synthetic lacto-N-biose libraries using microscale affinity chromatography coupled to mass spectrometry. Journal of Organic Chemistry, 71(19), 7146-7154. https://doi.org/10.1021/jo060485v
François-Heude, M., Méndez-Ardoy, A., Cendret, V., Lafite, P., Daniellou, R., Ortiz Mellet, C., … Djedaïni-Pilard, F. (2015). Synthesis of high-mannose oligosaccharide analogues through click chemistry: True functional mimics of their natural counterparts against lectins? Chemistry, 21(5), 1978-1991. https://doi.org/10.1002/chem.201405481
Giguère, D., Bonin, M.-A., Cloutier, P., Patnam, R., St-Pierre, C., Sato, S., & Roy, R. (2008). Synthesis of stable and selective inhibitors of human galectins-1 and -3. Bioorganic & Medicinal Chemistry, 16(16), 7811-7823. https://doi.org/10.1016/j.bmc.2008.06.044
Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hirashima, M., … Kasai, K. (2002). Oligosaccharide specificity of galectins: A search by frontal affinity chromatography. Biochimica Et Biophysica Acta, 1572(2-3), 232-254.
Hsieh, T.-J., Lin, H.-Y., Tu, Z., Huang, B.-S., Wu, S.-C., & Lin, C.-H. (2015). Structural basis underlying the binding preference of human galectins-1, -3 and -7 for Galβ1-3/4GlcNAc. PLoS ONE, 10(5), e0125946. https://doi.org/10.1371/journal.pone.0125946
Johannes, L., Jacob, R., & Leffler, H. (2018). Galectins at a glance. Journal of Cell Science, 131(9), https://doi.org/10.1242/jcs.208884
Kishor, C., Ross, R. L., & Blanchard, H. (2018). Lactulose as a novel template for anticancer drug development targeting galectins. Chemical Biology & Drug Design, 92(4), 1801-1808. https://doi.org/10.1111/cbdd.13348
Knibbs, R. N., Agrwal, N., Wang, J. L., & Goldstein, I. J. (1993). Carbohydrate-binding protein 35. II. Analysis of the interaction of the recombinant polypeptide with saccharides. Journal of Biological Chemistry, 268(20), 14940-14947.
Leffler, H., & Barondes, S. H. (1986). Specificity of binding of three soluble rat lung lectins to substituted and unsubstituted mammalian beta-galactosides. Journal of Biological Chemistry, 261(22), 10119-10126.
Marchiori, M. F., Souto, D. E. P., Bortot, L. O., Pereira, J. F., Kubota, L. T., Cummings, R. D., … Campo, V. L. (2015). Synthetic 1,2,3-triazole-linked glycoconjugates bind with high affinity to human galectin-3. Bioorganic & Medicinal Chemistry, 23(13), 3414-3425. https://doi.org/10.1016/j.bmc.2015.04.044
Murshudov, G. N., Vagin, A. A., & Dodson, E. J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallographica, Section D: Biological Crystallography, 53(Pt 3), 240-255. https://doi.org/10.1107/S0907444996012255
Nagae, M., Nishi, N., Murata, T., Usui, T., Nakamura, T., Wakatsuki, S., & Kato, R. (2009). Structural analysis of the recognition mechanism of poly-N-acetyllactosamine by the human galectin-9 N-terminal carbohydrate recognition domain. Glycobiology, 19(2), 112-117. https://doi.org/10.1093/glycob/cwn121
Oberg, C. T., Leffler, H., & Nilsson, U. J. (2011). Inhibition of galectins with small molecules. Chimia, 65(1-2), 18-23.
Pathigoolla, A., & Sureshan, K. M. (2013). A crystal-to-crystal synthesis of triazolyl-linked polysaccharide. Angewandte Chemie International Edition, 52(33), 8671-8675. https://doi.org/10.1002/anie.201303372
Rajput, V. K., Leffler, H., Nilsson, U. J., & Mukhopadhyay, B. (2014). Synthesis and evaluation of iminocoumaryl and coumaryl derivatized glycosides as galectin antagonists. Bioorganic & Medicinal Chemistry Letters, 24(15), 3516-3520. https://doi.org/10.1016/j.bmcl.2014.05.063
Rowan, A. S., Nicely, N. I., Cochrane, N., Wlassoff, W. A., Claiborne, A., & Hamilton, C. J. (2009). Nucleoside triphosphate mimicry: A sugar triazolyl nucleoside as an ATP-competitive inhibitor of B. anthracis pantothenate kinase. Organic & Biomolecular Chemistry, 7(19), 4029-4036. https://doi.org/10.1039/b909729e
Salameh, B. A., Cumpstey, I., Sundin, A., Leffler, H., & Nilsson, U. J. (2010). 1H-1,2,3-triazol-1-yl thiodigalactoside derivatives as high affinity galectin-3 inhibitors. Bioorganic & Medicinal Chemistry, 18(14), 5367-5378. https://doi.org/10.1016/j.bmc.2010.05.040
Sauerzapfe, B., Krenek, K., Schmiedel, J., Wakarchuk, W. W., Pelantová, H., Kren, V., & Elling, L. (2009). Chemo-enzymatic synthesis of poly-N-acetyllactosamine (poly-LacNAc) structures and their characterization for CGL2-galectin-mediated binding of ECM glycoproteins to biomaterial surfaces. Glycoconjugate Journal, 26(2), 141-159. https://doi.org/10.1007/s10719-008-9172-2
Schmidt, M. S., Götz, K. H., Koch, W., Grimm, T., & Ringwald, M. (2016). Studies toward the synthesis of linear triazole linked pseudo oligosaccharides and the use of ferrocene as analytical probe. Carbohydrate Research, 425, 28-34. https://doi.org/10.1016/j.carres.2016.03.005
Schüttelkopf, A. W., & van Aalten, D. M. F. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica, Section D: Biological Crystallography, 60(Pt 8), 1355-1363. https://doi.org/10.1107/S0907444904011679
Sciacchitano, S., Lavra, L., Morgante, A., Ulivieri, A., Magi, F., De Francesco, G. P., … Ricci, A. (2018). Galectin- 3: One molecule for an alphabet of diseases, from A to Z. International Journal of Molecular Sciences, 19(2), E379. https://doi.org/10.3390/ijms19020379
Srinivasan, N., Bane, S. M., Ahire, S. D., Ingle, A. D., & Kalraiya, R. D. (2009). Poly N-acetyllactosamine substitutions on N- and not O-oligosaccharides or Thomsen-Friedenreich antigen facilitate lung specific metastasis of melanoma cells via galectin-3. Glycoconjugate Journal, 26(4), 445-456. https://doi.org/10.1007/s10719-008-9194-9
Temelkoff, D. P., Zeller, M., & Norris, P. (2006). N-glycoside neoglycotrimers from 2,3,4,6-tetra-O-acetyl-beta-D-glucopyranosyl azide. Carbohydrate Research, 341(9), 1081-1090. https://doi.org/10.1016/j.carres.2006.04.011
Toscano, M. A., Martínez Allo, V. C., Cutine, A. M., Rabinovich, G. A., & Mariño, K. V. (2018). Untangling galectin-driven regulatory circuits in autoimmune inflammation. Trends in Molecular Medicine, 24(4), 348-363. https://doi.org/10.1016/j.molmed.2018.02.008
Tsuboi, S., Sutoh, M., Hatakeyama, S., Hiraoka, N., Habuchi, T., Horikawa, Y., … Ohyama, C. (2011). A novel strategy for evasion of NK cell immunity by tumours expressing core2 O-glycans. EMBO Journal, 30(15), 3173-3185. https://doi.org/10.1038/emboj.2011.215
van Hattum, H., Branderhorst, H. M., Moret, E. E., Nilsson, U. J., Leffler, H., & Pieters, R. J. (2013). Tuning the preference of thiodigalactoside- and lactosamine-based ligands to galectin-3 over galectin-1. Journal of Medicinal Chemistry, 56(3), 1350-1354. https://doi.org/10.1021/jm301677r
Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., … Wilson, K. S. (2011). Overview of the CCP4 suite and current developments. Acta Crystallographica, Section D: Biological Crystallography, 67(Pt 4), 235-242. https://doi.org/10.1107/S0907444910045749
Xu, H., Ren, B., Zhao, W., Xin, X., Lu, Y., Pei, Y., … Pei, Z. (2016). Regioselective mono and multiple alkylation of diols and polyols catalyzed by organotin and its applications on the synthesis of value-added carbohydrate intermediates. Tetrahedron, 72(24), 3490-3499. https://doi.org/10.1016/j.tet.2016.04.076
Zetterberg, F. R., Peterson, K., Johnsson, R. E., Brimert, T., Håkansson, M., Logan, D. T., … Nilsson, U. J. (2018). Monosaccharide derivatives with low-nanomolar lectin affinity and high selectivity based on combined fluorine-amide, phenyl-arginine, sulfur-π, and halogen bond interactions. ChemMedChem, 13(2), 133-137. https://doi.org/10.1002/cmdc.201700744