The carbohydrate-binding site in galectin-3 is preorganized to recognize a sugarlike framework of oxygens: Ultra-high-resolution structures and water dynamics

Biochemistry

Volumn 51, Issue 1, 2012, Pages 296-306

  Saraboji, Kadhirvel ^a   Hakansson, Maria ^b   Genheden, Samuel ^c   Diehl, Carl ^a   Qvist, Johan ^a   Weininger, Ulrich ^a   Nilsson, Ulf J ^c   Leffler, Hakon ^c   Ryde, Ulf ^c   Akke, Mikael ^a   Logan, Derek T ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b SARomics Biostructures AB   (Sweden)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BULK WATER; CARBOHYDRATE-RECOGNITION DOMAINS; CRYO-CRYSTALLOGRAPHY; DEUTERIUM NUCLEAR MAGNETIC RESONANCE; DRUG DISCOVERY; ENERGY LANDSCAPE; HEAVY ATOMS; INHIBITOR DESIGN; ISOTHERMAL TITRATION CALORIMETRY; LIGAND-FREE; LIVING CELL; MOLECULAR BASIS; MOLECULAR DYNAMICS SIMULATIONS; OXYGEN ATOM; PROTEIN INTERACTION; RATIONAL DESIGN; RELAXATION DISPERSION; ROOM TEMPERATURE; SCREENING METHODS; SITE EXCHANGE; SYNTHETIC LIGANDS; TIME-SCALES; WATER BINDING; WATER DYNAMICS; WATER MOLECULE;

ATOMS; BINDING ENERGY; BINDING SITES; CRYSTALLOGRAPHY; GLYCEROL; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXYGEN; SUGARS;

ORGANIC COMPOUNDS;

GALECTIN 3; GLYCEROL; LACTOSE; WATER;

ARTICLE; CRYSTAL STRUCTURE; DEUTERON NUCLEAR MAGNETIC RESONANCE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN STRUCTURE; SIMULATION;

APOPROTEINS; CARBOHYDRATE CONFORMATION; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ENERGY METABOLISM; GALECTIN 3; GLYCEROL; HUMANS; LACTOSE; LIGANDS; MOLECULAR DYNAMICS SIMULATION; OXYGEN; PROTEIN BINDING; SURFACE PROPERTIES; WATER;

EID: 84856906856     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201459p     Document Type: Article

References (79)

1. Geijtenbeek, T. B., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Adema, G. J., van Kooyk, Y., and Figdor, C. G. (2000) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100, 575-585.
2. Sacchettini, J. C., Baum, L. G., and Brewer, C. F. (2001) Multivalent protein-carbohydrate interactions. A new paradigm for supermolecular assembly and signal transduction. Biochemistry 40, 3009-3015. (Pubitemid 32205344)
3. Karlsson A., Feuk-Lagerstedt, E., Almkvist, J., Leffler, H., and Dahlgren, C. (1999) Priming is required for galectin-3-induced neutrophil NADPH-oxidase activity. J. Leukocyte Biol.,, 25.
4. Henderson, N. C., and Sethi, T. (2009) The regulation of inflammation by galectin-3. Immunol. Rev. 230, 160-171.
5. von Itzstein, M. (2007) The war against influenza: Discovery and development of sialidase inhibitors. Nat. Rev. Drug Discovery 6, 967-974.
6. Bernardi, A., and Cheshev, P. (2008) Interfering with the Sugar Code: Design and Synthesis of Oligosaccharide Mimics. Chem.?Eur. J. 14, 7434-7441.
7. Ernst, B., and Magnani, J. L. (2009) From carbohydrate leads to glycomimetic drugs. Nat. Rev. Drug Discovery 8, 661-677.
8. Lepenies B., Yin, J., and Seeberger, P. H. (2010) Applications of synthetic carbohydrates to chemical biology. Curr. Opin. Chem. Biol.,, 1-8.
9. Dam, T. K., and Brewer, C. F. (2002) Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry. Chem. Rev. 102, 387-429. (Pubitemid 35381635)
10. Toone, E. J. (1994) Structure and Energetics of Protein Carbohydrate Complexes. Curr. Opin. Struct. Biol. 4, 719-728. (Pubitemid 24325291)
11. Garcia Hernandez, E., Zubillaga, R. A., Rojo Dominguez, A., Rodriguez Romero, A., and Hernandez Arana, A. (1997) New insights into the molecular basis of lectin-carbohydrate interactions: A calorimetric and structural study of the association of hevein to oligomers of N-acetylglucosamine. Proteins: Struct., Funct., Genet. 29, 467-477. (Pubitemid 27520200)
12. Garcia-Hernandez, E., and Hernandez-Arana, A. (1999) Structural bases of lectin-carbohydrate affinities: Comparison with protein-folding energetics. Protein Sci. 8, 1075-1086. (Pubitemid 29211745)
13. Lemieux, R. U. (1999) How water provides the impetus for molecular recognition in aqueous solution (vol 29, pg 373, 1996). Acc. Chem. Res. 32, 631.
14. Lis, H., and Sharon, N. (1998) Lectins: Carbohydrate-specific proteins that mediate cellular recognition. Chem. Rev. 98, 637-674. (Pubitemid 128631438)
15. Davis, A. P., and Wareham, R. S. (1999) Carbohydrate recognition through noncovalent interactions: A challenge for biomimetic and supramolecular chemistry. Angew. Chem., Int. Ed. 38, 2978-2996. (Pubitemid 29513669)
16. Sörme, P., Arnoux, P., Kahl-Knutsson, B., Leffler, H., Rini, J. M., and Nilsson, U. J. (2005) Structural and thermodynamic studies on cation-p interactions in lectin-ligand complexes: High-affinity galectin-3 inhibitors through fine-tuning of an arginine-arene interaction. J. Am. Chem. Soc. 127, 1737-1743. (Pubitemid 40233025)
17. del Carmen Fernandez-Alonso, M., Canada, F. J., Jimenez-Barbero, J., and Cuevas, G. (2005) Molecular recognition of saccharides by proteins. Insights on the origin of the carbohydratearomatic interactions. J. Am. Chem. Soc. 127, 7379-7386. (Pubitemid 40746022)
18. Laughrey, Z. R., Kiehna, S. E., Riemen, A. J., and Waters, M. L. (2008) Carbohydrate-p interactions: What are they worth? J. Am. Chem. Soc. 130, 14625-14633.
19. Ladbury, J. E. (1996) Just add water! The effect of water on the specificity of protein-ligand binding sites and its potential application to drug design. Chem. Biol. 3, 973-980. (Pubitemid 27058821)
20. Clarke, C., Woods, R. J., Gluska, J., Cooper, A., Nutley, M. A., and Boons, G. J. (2001) Involvement of water in carbohydrate-protein binding. J. Am. Chem. Soc. 123, 12238-12247. (Pubitemid 33136060)
21. Chervenak, M. C., and Toone, E. J. (1995) Calorimetric analysis of the binding of lectins with overlapping carbohydrate-binding ligand specificities. Biochemistry 34, 5685-5695.
22. Dunitz, J. D. (1994) The entropic cost of bound water in crystals and biomolecules. Science 264, 670. (Pubitemid 24186849)
23. Kadirvelraj, R., Foley, B. L., Dyekjaer, J. D., and Woods, R. J. (2008) Involvement of Water in Carbohydrate-Protein Binding: Concanavalin A Revisited. J. Am. Chem. Soc. 130, 16933-16942.
24. Lemieux, R. U. (1996) How water provides the impetus for molecular recognition in aqueous solution. Acc. Chem. Res. 29, 373-380. (Pubitemid 126453219)
25. Di Lella, S., Ma, L., Ricci, J. C., Rabinovich, G. A., Asher, S. A., and Alvarez, R. M. (2009) Critical role of the solvent environment in galectin-1 binding to the disaccharide lactose. Biochemistry 48, 786-791.
26. Li, Z., and Lazaridis, T. (2005) The effect of water displacement on binding thermodynamics: concanavalin A. J. Phys. Chem. B 109, 662-670. (Pubitemid 40121013)
27. Asensio, J. L., Siebert, H. C., von der Lieth, C. W., Laynez, J., Bruix, M., Soedjanaamadja, U. M., Beintema, J. J., Canada, F. J., Gabius, H. J., and Jimenez-Barbero, J. (2000) NMR investigations of protein-carbohydrate interactions: Studies on the relevance of Trp/ Tyr variations in lectin binding sites as deduced from titration microcalorimetry and NMR studies on hevein domains. Determination of the NMR structure of the complex between pseudohevein and N,N',N?-triacetylchitotriose. Proteins: Struct., Funct., Genet. 40, 218-236. (Pubitemid 30413626)
28. Leffler, H., Carlsson, S., Hedlund, M., Qian, Y., and Poirier, F. (2004) Introduction to galectins. Glycoconjugate J. 19, 433-440. (Pubitemid 38316516)
29. Rabinovich, G. A., Liu, F. T., Hirashima, M., and Anderson, A. (2007) An emerging role for galectins in tuning the immune response: Lessons from experimental models of inflammatory disease, autoimmunity and cancer. Scand. J. Immunol. 66, 143-158. (Pubitemid 47063211)
30. MacKinnon, A. C., Farnworth, S. L., Hodkinson, P. S., Henderson, N. C., Atkinson, K. M., Leffler, H., Nilsson, U. J., Haslett, C., Forbes, S. J., and Sethi, T. (2008) Regulation of alternative macrophage activation by galectin-3. J. Immunol. 180, 2650-2658.
31. Delacour, D., Koch, A., and Jacob, R. (2009) The role of galectins in protein trafficking. Traffic 10, 1405-1413.
32. Liu, F. T., and Rabinovich, G. A. (2010) Galectins: Regulators of acute and chronic inflammation. Ann. N.Y. Acad. Sci. 1183, 158-182.
33. Grigorian, A., and Demetriou, M. (2010) Manipulating cell surface glycoproteins by targeting N-glycan-galectin interactions. Methods Enzymol. 480, 245-266.
34. Nieminen, J., Kuno, A., Hirabayashi, J., and Sato, S. (2007) Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer. J. Biol. Chem. 282, 1374-1383. (Pubitemid 47076550)
35. Seelenmeyer, C., Wegehingel, S., Tews, I., Kunzler, M., Aebi, M., and Nickel, W. (2005) Cell surface counter receptors are essential components of the unconventional export machinery of galectin-1. J. Cell Biol. 171, 373-381. (Pubitemid 41540028)
36. Baptiste, T. A., James, A., Saria, M., and Ochieng, J. (2007) Mechano-transduction mediated secretion and uptake of galectin-3 in breast carcinoma cells: Implications in the extracellular functions of the lectin. Exp. Cell Res. 313, 652-664. (Pubitemid 46198812)
37. Dennis, J. W., Lau, K. S., Demetriou, M., and Nabi, I. R. (2009) Adaptive regulation at the cell surface by N-glycosylation. Traffic 10, 1569-1578.
38. Almkvist, J., and Karlsson, A. (2004) Galectins as inflammatory mediators. Glycoconjugate J. 19, 575-581. (Pubitemid 38316532)
39. Dumic, J., Dabelic, S., and Flogel, M. (2006) Galectin-3: An open-ended story. Biochim. Biophys. Acta 1760, 616-635. (Pubitemid 44382499)
40. Liu, F. T. (2005) Regulatory roles of galectins in the immune response. Int. Arch. Allergy Immunol. 136, 385-400.
41. Liu, F. T., and Rabinovich, G. A. (2005) Galectins as modulators of tumour progression. Nat. Rev. Cancer 5, 29-41. (Pubitemid 40052323)
42. Walti, M. A., Walser, P. J., Thore, S., Grunler, A., Bednar, M., Kunzler, M., and Aebi, M. (2008) Structural basis for chitotetraose coordination by CGL3, a novel galectin-related protein from Coprinopsis cinerea. J. Mol. Biol. 379, 146-159.
43. Seetharaman, J., Kanigsberg, A., Slaaby, R., Leffler, H., Barondes, S. H., and Rini, J. M. (1998) X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-Å resolution. J. Biol. Chem. 273, 13047-13052. (Pubitemid 28246869)
44. Carlsson, S., Öberg, C. T., Carlsson, M. C., Sundin, A., Niisson, U. J., Smith, D., Cummings, R. D., Almkvist, J., Karlsson, A., and Leffler, H. (2007) Affinity of galectin-8 and its carbohydrate recognition domains for ligands in solution and at the cell surface. Glycobiology 17, 663-676. (Pubitemid 47062709)
45. Diehl, C., Genheden, S., Engström, O., Delaine, T., Ha°kansson, M., Leffler, H., Nilsson, U. J., Ryde, U., and Akke, M. (2010) Protein flexibility and conformational entropy in ligand design targeting the carbohydrate recognition domain of galectin-3. J. Am. Chem. Soc. 132, 14577-14589.
46. Salameh, B. A., Leffler, H., and Nilsson, U. J. (2005) 3-(1,2,3-Triazol-1-yl)-1-thio-galactosides as small, efficient, and hydrolytically stable inhibitors of galectin-3. Bioorg. Med. Chem. Lett. 15, 3344-3346. (Pubitemid 40835732)
47. Salameh, B. A., Cumpstey, I., Sundin, A., Leffler, H., and Nilsson, U. J. (2010) 1H-1,2,3-Triazol-1-yl thiodigalactoside derivatives as high affinity galectin-3 inhibitors. Bioorg. Med. Chem. 18, 5367-5378.
48. Yang, R. Y., Rabinovich, G. A., and Liu, F. T. (2008) Galectins: Structure, function and therapeutic potential. Expert Rev. Mol. Med. 10, e17.
49. Wu, M. H., Hong, T. M., Cheng, H. W., Pan, S. H., Liang, Y. R., Hong, H. C., Chiang, W. F., Wong, T. Y., Shieh, D. B., Shiau, A. L., Jin, Y. T., and Chen, Y. L. (2009) Galectin-1-mediated tumor invasion and metastasis, up-regulated matrix metalloproteinase expression, and reorganized actin cytoskeletons. Mol. Cancer Res. 7, 311-318.
50. Delaine, T., Cumpstey, I., Ingrassia, L., Le Mercier, M., Okechukwu, P., Leffler, H., Kiss, R., and Nilsson, U. J. (2008) Galectin-inhibitory thiodigalactoside ester derivatives have antimigratory effects in cultured lung and prostate cancer cells. J. Med. Chem. 51, 8109-8114.
51. Lin, C. I., Whang, E. E., Donner, D. B., Jiang, X., Price, B. D., Carothers, A. M., Delaine, T., Leffler, H., Nilsson, U. J., Nose, V., Moore, F. D., and Ruan, D. T. (2009) Galectin-3 targeted therapy with a small molecule inhibitor activates apoptosis and enhances both chemosensitivity and radiosensitivity in papillary thyroid cancer. Mol. Cancer Res. 7, 1655-1662.
52. Diehl, C., Genheden, S., Modig, K., Ryde, U., and Akke, M. (2009) Conformational entropy changes upon lactose binding to the carbohydrate recognition domain of galectin-3. J. Biomol. NMR 45, 157-169.
53. Massa, S. M., Cooper, D. N., Leffler, H., and Barondes, S. H. (1993) L-29, an endogenous lectin, binds to glycoconjugate ligands with positive cooperativity. Biochemistry 32, 260-267. (Pubitemid 23033344)
54. Kabsch, W. (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D66, 133-144.
55. Murshudov, G. N. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255. (Pubitemid 27235885)
56. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr. D59, 1131-1137. (Pubitemid 36872348)
57. Sheldrick, G. M. (2008) A short history of SHELX. Acta Crystallogr. A64, 112-122.
58. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D66, 486-501.
59. DeLano, W. L. (2002) The PyMOL Molecular Graphics System DeLano Scientific, Palo Alto, CA.
60. Teilum, K., Brath, U., Lundström, P., and Akke, M. (2006) Biosynthetic 13C labeling of aromatic side chains in proteins for NMR relaxation measurements. J. Am. Chem. Soc. 128, 2506-2507. (Pubitemid 43327906)
61. Lundström, P., Teilum, K., Carstensen, T., Bezsonova, I., Wiesner, S., Hansen, D. F., Religa, T. L., Akke, M., and Kay, L. E. (2007) Fractional 13C enrichment of isolated carbons using [1-13C]-or [2-13C]-glucose facilitates the accurate measurement of dynamics at backbone Ca and side-chain methyl positions in proteins. J. Biomol. NMR 38, 199-212. (Pubitemid 46979220)
62. Genheden, S., Luchko, T., Gusarov, S., Kovalenko, A., and Ryde, U. (2010) An MM/3D-RISM approach for ligand binding affinities. J. Phys. Chem. B 114, 8505-8516.
63. Young, T., Abel, R., Kim, B., Berne, B. J., and Friesner, R. A. (2007) Motifs for molecular recognition exploiting hydrophobic enclosure in protein-ligand binding. Proc. Natl. Acad. Sci. U.S.A. 104, 808-813. (Pubitemid 46154692)
64. Abel, R., Young, T., Farid, R., Berne, B. J., and Friesner, R. A. (2008) Role of the active-site solvent in the thermodynamics of factor Xa ligand binding. J. Am. Chem. Soc. 130, 2817-2831. (Pubitemid 351416242)
65. Shao, J. Y., Tanner, S. W., Thompson, N., and Cheatham, T. E. (2007) Clustering molecular dynamics trajectories: 1. Characterizing the performance of different clustering algorithms. J. Chem. Theory Comput. 3, 2312-2334.
66. Collins, P. M., Hidari, K. I., and Blanchard, H. (2007) Slow diffusion of lactose out of galectin-3 crystals monitored by X-ray crystallography: Possible implications for ligand-exchange protocols. Acta Crystallogr. D63, 415-419. (Pubitemid 46438535)
67. McDonald, I. K., and Thornton, J. M. (1994) Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793. (Pubitemid 24168633)
68. Pelton, J. G., Torchia, D. A., Meadow, N. D., and Roseman, S. (1993) Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated III(Glc), a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci. 2, 543-558. (Pubitemid 23119305)
69. Bachhawat, K., Thomas, C. J., Amutha, B., Krishnasastry, M. V., Khan, M. I., and Surolia, A. (2001) On the stringent requirement of mannosyl substitution in mannooligosaccharides for the recognition by garlic (Allium sativum) lectin. A surface plasmon resonance study. J. Biol. Chem. 276, 5541-5546.
70. Ahmad, N., Gabius, H. J., Sabesan, S., Oscarson, S., and Brewer, C. F. (2004) Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin-3, and the carbohydrate recognition domain of galectin-3. Glycobiology 14, 817-825. (Pubitemid 39206884)
71. Murray, C. W., and Blundell, T. L. (2010) Structural biology in fragment-based drug design. Curr. Opin. Struct. Biol. 20, 497-507.
72. Burley, S. K., Hirst, G., Sprengeler, P., and Reich, S. (2010) Fragment-based structure-guided drug discovery: Strategy, process, and lessons from human protein kinases. In Drug Design: Structure-and ligand-based approaches (Merz, K. M., Ringe, D., and Reynolds, C. H., Eds.) pp 30-40, Cambridge University Press, New York.
73. Umemoto, K., Leffler, H., Venot, A., Valafar, H., and Prestegard, J. H. (2003) Conformational differences in liganded and unliganded states of galectin-3. Biochemistry 42, 3688-3695. (Pubitemid 36402660)
74. Gauto, D. F., Di Lella, S., Guardia, C. M., Estrin, D. A., and Marti, M. A. (2009) Carbohydrate-binding proteins: Dissecting ligand structures through solvent environment occupancy. J. Phys. Chem. B 113, 8717-8724.
75. Halle, B., and Denisov, V. P. (2001) Magnetic relaxation dispersion studies of biomolecular solutions. Methods Enzymol. 338, 178-201. (Pubitemid 32666579)
76. Halle, B. (2004) Protein hydration dynamics in solution: A critical survey. Philos. Trans. R. Soc. London, Ser. B 359, 1207-1223.
77. Hills, B. P. (1991) Multinuclear NMR-studies of water in solutions of simple carbohydrates. 1. Proton and deuterium relaxation. Mol. Phys. 72, 1099-1121.
78. Di Lella, S., Marti, M. A., Alvarez, R. M. S., Estrin, D. A., and Ricci, J. C. D. (2007) Characterization of the galectin-1 carbohydrate recognition domain in terms of solvent occupancy. J. Phys. Chem. B 111, 7360-7366. (Pubitemid 47152524)
79. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B. III, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383.