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Abstract:

Endogenous lectins can control critical biological responses, including cell communication, signaling, angiogenesis and immunity by decoding glycan-containing information on a variety of cellular receptors and the extracellular matrix. Galectin-1 (Gal-1), a prototype member of the galectin family, displays only one carbohydrate recognition domain and occurs in a subtle homodimerization equilibrium at physiologic concentrations. Such equilibrium critically governs the function of this lectin signaling by allowing tunable interactions with a preferential set of glycosylated receptors. Here, we used a combination of experimental and computational approaches to analyze the kinetics and mechanisms connecting Gal-1 ligand unbinding and dimer dissociation processes. Kinetic constants of both processes were found to differ by an order of magnitude. By means of steered molecular dynamics simulations, the ligand unbinding process was followed monitoring water occupancy changes. By determining the water sites in a carbohydrate binding place during the unbinding process, we found that rupture of ligand-protein interactions induces an increase in energy barrier while ligand unbinding process takes place, whereas the entry of water molecules to the binding groove and further occupation of their corresponding water sites contributes to lowering of the energy barrier. Moreover, our findings suggested local asymmetries between the two subunits in the dimer structure detected at a nanosecond timescale. Thus, integration of experimental and computational data allowed a more complete understanding of lectin ligand binding and dimerization processes, suggesting new insights into the relationship between Gal-1 structure and function and renewing the discussion on the biophysics and biochemistry of lectin-ligand lattices. © The Author 2016.

Registro:

Documento: Artículo
Título:Impact of human galectin-1 binding to saccharide ligands on dimer dissociation kinetics and structure
Autor:Romero, J.M.; Trujillo, M.; Estrin, D.A.; Rabinovich, G.A.; Di Lella, S.
Filiación:Departamento de Química Biológica, IQUIBICEN, CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad de Buenos Aires, C1428EHA, Argentina
Departamento de Química Inorgánica, Analítica y Química Física, INQUIMAE, CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad de Buenos Aires, C1428EHA, Argentina
Departamento de Bioquímica, Center for Free Radical and Biomedical Research, Facultad de Medicina, Universidad de la República, Montevideo, 11800, Uruguay
Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental, CONICET, Ciudad de Buenos Aires, C1428ADN, Argentina
Institute of Biology, Humboldt-Universität zu Berlin, Invalidenstraße 43, Berlin, 10115, Germany
Palabras clave:Carbohydrate-binding protein; Dimer dissociation kinetics; Galectin-1; Lattices; Ligand-binding kinetics; carbohydrate; dimer; galectin 1; lactose; lectin; ligand; monomer; water; galectin 1; LGALS1 protein, human; polysaccharide; Article; beta sheet; dilution; dimerization; dissociation; dissociation constant; energy; enthalpy; entropy; equilibrium constant; fluorescence spectroscopy; human; hydrogen bond; kinetics; ligand binding; ligand protein interaction; molecular dynamics; molecular mechanics; nonhuman; priority journal; protein interaction; proton transport; quantum mechanics; static electricity; surface area; binding site; chemistry; kinetics; metabolism; protein conformation; thermodynamics; Binding Sites; Dimerization; Galectin 1; Humans; Kinetics; Ligands; Molecular Dynamics Simulation; Polysaccharides; Protein Conformation; Thermodynamics
Año:2016
Volumen:26
Número:12
Página de inicio:1317
Página de fin:1327
DOI: http://dx.doi.org/10.1093/glycob/cww052
Título revista:Glycobiology
Título revista abreviado:Glycobiology
ISSN:09596658
CODEN:GLYCE
CAS:galectin 1, 258495-34-0; lactose, 10039-26-6, 16984-38-6, 63-42-3, 64044-51-5; water, 7732-18-5; Galectin 1; LGALS1 protein, human; Ligands; Polysaccharides
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_09596658_v26_n12_p1317_Romero

Referencias:

  • Barondes, S.H., Castronovo, V., Cooper, D.N.W., Cummings, R.D., Drickamer, K., Felzi, T., Gitt, M.A., Kasal, K., Galectins: A family of animal beta-galactoside-binding lectins (1994) Cell, 76, pp. 597-598
  • Barondes, S.H., Cooper, D.N., Gitt, M.A., Leffler, H., Galectins. Structure and function of a large family of animal lectins (1994) J Biol Chem., 269, pp. 20807-20810
  • Bashford, D., Case, D.A., Generalized born models of macromolecular solvation effects (2000) Annu Rev Phys Chem., 51, pp. 129-152
  • Berendsen, H.J., Postma, J.P.M., Van Gunsteren, W.F., DiNola, A., Haak, J.R., Molecular dynamics with coupling to an external bath (1984) J Chem Phys., 81 (8), p. 3684
  • Brewer, C.F., Carrie Miceli, M., Baum, L.G., Clusters, bundles, arrays and lattices: Novel mechanisms for lectin-saccharide-mediated cellular interactions (2002) Curr Opin Struct Biol., 12, pp. 616-623
  • Case, D.A., Babin, V., Berryman, J.T., Betz, R.M., Cai, Q., Cerutti, D.S., Cheatham, T.E., Gohlke, H., (2014) AMBER 14, , University of California, San Francisco
  • Cho, M., Cummings, R.D., Galectin-1, a β-galactoside-binding lectin in Chinese hamster ovary cells (1995) J Biol Chem., 270 (10), p. 5198
  • Cho, M., Cummings, R.D., Characterization of monomeric forms of galectin-1 generated by site-directed mutagenesis (1996) Biochemistry, 35 (40), pp. 13081-13088
  • Croci, D.O., Cerliani, J.P., Dalotto-Moreno, T., Méndez-Huergo, S.P., Mascanfroni, I.D., Dergan-Dylon, S., Toscano, M.A., Ouyang, J., Glycosylation-dependent lectin-receptor interactions preserve angiogenesis in anti-VEGF refractory tumors (2014) Cell, 156 (4), pp. 744-758
  • Dalotto-Moreno, T., Croci, D.O., Cerliani, J.P., Martinez-Allo, V.C., Dergan-Dylon, S., Méndez-Huergo, S.P., Stupirski, J.C., Toscano, M.A., Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease (2013) Cancer Res., 73 (3), pp. 1107-1117
  • Dam, T.K., Gabius, H.J., André, S., Kaitner, H., Lensch, M., Brewer, C.F., Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants (2005) Biochemistry, 44, pp. 12564-12571
  • Di Lella, S., Martí, M.A., Álvarez, R.M.S., Estrin, D.A., Ricci, J.C.D., Characterization of the galectin-1 carbohydrate recognition domain in terms of solvent occupancy (2007) J Phys Chem B, 111 (25), pp. 7360-7366
  • Di Lella, S., Martí, M.A., Croci, D.O., Guardia, C.M., Diáz-Ricci, J.C., Rabinovich, G.A., Caramelo, J., Estrin, D.A., Linking the structure and thermal stability of beta-galactoside-binding protein galectin-1 to ligand binding and dimerization equilibria (2010) Biochemistry, 49 (35), pp. 7652-7658
  • Di Lella, S., Sundblad, V., Cerliani, J.P., Guardia, C.M., Estrin, D.A., Vasta, G.R., Rabinovich, G.A., When galectins recognize glycans: From biochemistry to physiology and back again (2011) Biochemistry, 50 (37), pp. 7842-7857
  • Earl, L.A., Bi, S., Baum, L.G., Galectin multimerization and lattice formation are regulated by linker region structure (2011) Glycobiology, 21 (1), pp. 6-12
  • Echeverria, I., Amzel, M.L., Disaccharide binding to galectin-1: Free energy calculations and molecular recognition mechanism (2011) Biophys J., 100 (9), pp. 2283-2292
  • Elola, M.T., Blidner, A.G., Ferragut, F., Bracalente, C., Rabinovich, G.A., Assembly, organization and regulation of cell-surface receptors by lectin-glycan complexes (2015) Biochemical Journal, 469 (1), pp. 1-16
  • Garner, O.B., Baum, L.G., Galectin-glycan lattices regulate cell-surface glycoprotein organization and signalling (2008) Biochem Soc Trans., 36, pp. 1472-1477
  • Gauto, D.F., Petruk, A.A., Modenutti, C.P., Blanco, J.I., Di Lella, S., Martí, M.A., Solvent structure improves docking prediction in lectin-carbohydrate complexes (2013) Glycobiology, 23 (2), pp. 241-258
  • Göhler, A., Büchner, C., André, S., Doose, S., Kaltner, H., Gabius, H.J., Analysis of homodimeric avian and human galectins by two methods based on fluorescence spectroscopy: Different structural alterations upon oxidation and ligand binding (2012) Biochimie., 94 (12), pp. 2649-2655
  • Hiramatsu, H., Takeuchi, K., Takeuchi, H., Involvement of histidine residues in the pH-dependent β-galactoside binding activity of human galectin-1 (2013) Biochemistry, 52, pp. 2371-2380
  • Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., Simmerling, C., Comparison of multiple amber force fields and development of improved protein backbone parameters (2006) Proteins, 65 (3), pp. 712-725
  • Ilarregui, J.M., Croci, D., Bianco, G.A., Toscano, M.A., Salatino, M., Vermeulen, M.E., Geffner, J.R., Rabinovich, G.A., Tolerogenic signals delivered by dendritic cells to t cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10 (2009) Nat Immunol., 10 (9), pp. 981-991
  • Jarzynski, C., Equilibrium free-energy differences from nonequilibrium measurements: A master-equation approach (1997) Phys Rev E, 56, pp. 5018-5035
  • Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., Klein, M., Comparison of simple potential functions for simulating liquid water (1983) J Chem Phys., 79 (2), p. 926
  • Kirschner, K.N., Yongye, A.B., Tschampel, S.M., González-Outeiriño, J., Daniels, C.R., Foley, B.L., Woods, R.J., GLYCAM06 : A generalizable biomolecular force field (2008) J Comput Chem., 29 (4), pp. 622-655
  • Lau, K.S., Partridge, E.A., Grigorian, A., Silvescu, C.I., Reinhold, V.N., Demetriou, M., Dennis, J.W., Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation (2007) Cell, 129, pp. 123-134
  • López-Lucendo, M.F., Solís, D., André, S., Hirabayashi, J., Kasai, K.I., Kaltner, H., Gabius, H.J., Romero, A., Growth-regulatory human galectin-1: Crystallographic characterisation of the structural changes induced by single-site mutations and their impact on the thermodynamics of ligand binding (2004) J Mol Biol., 343 (4), pp. 957-970
  • Marth, J.D., Grewal, P.K., Mammalian glycosylation in immunity (2008) Nat Rev Immunol., 8, pp. 874-887
  • Motran, C.C., Molinder, K.M., Liu, S.D., Poirier, F., Miceli, M.C., Galectin - 1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function (2008) Eur J Immunol., 38 (11), pp. 3015-3027
  • Nesmelova, I.V., Ermakova, E., Daragan, V.A., Pang, M., Menéndez, M., Lagartera, L., Solís, D., Mayo, K.H., Lactose binding to galectin-1 modulates structural dynamics, increases conformational entropy, and occurs with apparent negative cooperativity (2010) J Mol Biol., 397 (5), pp. 1209-1230
  • Pace, K.E., Hahn, H.P., Baum, L.G., Preparation of recombinant human galectin-1 and use in T-cell death assays (2003) Methods Enzymol., 363, pp. 499-518
  • Partridge, E.A., Le Roy, C., Di Guglielmo, G.M., Pawling, J., Cheung, P., Granovsky, M., Nabi, I.R., Dennis, J.W., Regulation of cytokine receptors by golgi n-glycan processing and endocytosis (2004) Science, 306, pp. 120-124
  • Poncini, C.V., Ilarregui, J.M., Batalla, E.I., Engels, S., Cerliani, J.P., Cucher, M.A., Van Kooyk, Y., Rabinovich, G.A., Trypanosoma cruzi infection imparts a regulatory program in dendritic cells and T cells via galectin-1-dependent mechanisms (2015) J Immunol., 195 (7), pp. 3311-3324
  • Rabinovich, G.A., Croci, D.O., Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer (2012) Immunity, 36 (3), pp. 322-335
  • Rabinovich, G.A., Toscano, M.A., Turning 'Sweet' on immunity: Galectinglycan interactions in immune tolerance and inflammation (2009) Nat Rev Immunol., 9, pp. 338-352
  • Rabinovich, G.A., Toscano, M.A., Jackson, S.S., Vasta, G.R., Functions of cell surface galectin-glycoprotein lattices (2007) Curr Opin Struct Biol., 17, pp. 513-520
  • Schlitter, J., Estimation of absolute and relative entropies of macromolecules using the covariance matrix (1993) Chem Phys Lett., 215 (6), pp. 617-621
  • Schäfer, H., Mark, A.E., Van Gunsteren, W.F., Absolute entropies from molecular dynamics simulation trajectories (2000) J Chem Phys., 113 (18), pp. 7809-7817
  • Siebert, H.C., André, S., Lu, S.Y., Frank, M., Kaltner, H., Van Kuik, J.A., Korchagina, E.Y., Kaptein, R., Unique conformer selection of human growth-regulatory lectin galectin-1 for ganglioside gm1 versus bacterial toxins (2003) Biochemistry, 42, pp. 14762-14773
  • Starossom, S.C., Mascanfroni, I.D., Imitola, J., Cao, L., Raddassi, K., Hernandez, S.F., Bassil, R., Delacour, D., Galectin-1 deactivates classically activated microglia and protects from inflammationinduced neurodegeneration (2012) Immunity, 37 (2), pp. 249-263
  • Stowell, S.R., Cho, M., Feasley, C.L., Arthur, C.M., Song, X., Colucci, J.K., Karmakar, S., McEver, R.P., Ligand reduces galectin-1 sensitivity to oxidative inactivation by enhancing dimer formation (2009) J Biol Chem., 284 (8), pp. 4989-4999
  • Thijssen, V.L., Barkan, B., Shoji, H., Aries, I.M., Mathieu, V., Deltour, L., Hackeng, T.M., Poirier, F., Tumor cells secrete galectin-1 to enhance endothelial cell activity (2010) Cancer Res., 70 (15), pp. 6216-6224
  • Toscano, M.A., Ilarregui, J., Bianco, G., Campagna, L., Croci, D.O., Salatino, M., Rabinovich, G.A., Dissecting the pathophysiologic role of endogenous lectins: Glycan-binding proteins with cytokine-like activity? (2007) Cytokine Growth Factor Rev., 18 (1-2), pp. 57-71
  • Van Gunsteren, W.F., Berendsen, H.J.C., Computer simulation of molecular dynamics: Methodology, applications, and perspectives in chemistry (1990) Ang Chem Int Ed Engl., 29 (9), pp. 992-1023
  • Van Kooyk, Y., Rabinovich, G.A., Protein-glycan interactions in the control of innate and adaptive immune responses (2008) Nat Immunol., 9, pp. 593-601
  • Williams, T., Kelley, C., (2010) Gnuplot 4.4: An Interactive Plotting Program, , Official gnuplot documentation
  • Yang, R.Y., Rabinovich, G.A., Liu, F.T., Galectins: Structure, function and therapeutic potential (2008) Expert Rev Mol Med., 10, p. e17
  • Zou, X., Sun, Y., Kuntz, I.D., Inclusion of solvation in ligand binding free energy calculations using the generalized-born model (1999) J Am Chem Soc., 121 (12), pp. 8033-8043

Citas:

---------- APA ----------
Romero, J.M., Trujillo, M., Estrin, D.A., Rabinovich, G.A. & Di Lella, S. (2016) . Impact of human galectin-1 binding to saccharide ligands on dimer dissociation kinetics and structure. Glycobiology, 26(12), 1317-1327.
http://dx.doi.org/10.1093/glycob/cww052
---------- CHICAGO ----------
Romero, J.M., Trujillo, M., Estrin, D.A., Rabinovich, G.A., Di Lella, S. "Impact of human galectin-1 binding to saccharide ligands on dimer dissociation kinetics and structure" . Glycobiology 26, no. 12 (2016) : 1317-1327.
http://dx.doi.org/10.1093/glycob/cww052
---------- MLA ----------
Romero, J.M., Trujillo, M., Estrin, D.A., Rabinovich, G.A., Di Lella, S. "Impact of human galectin-1 binding to saccharide ligands on dimer dissociation kinetics and structure" . Glycobiology, vol. 26, no. 12, 2016, pp. 1317-1327.
http://dx.doi.org/10.1093/glycob/cww052
---------- VANCOUVER ----------
Romero, J.M., Trujillo, M., Estrin, D.A., Rabinovich, G.A., Di Lella, S. Impact of human galectin-1 binding to saccharide ligands on dimer dissociation kinetics and structure. Glycobiology. 2016;26(12):1317-1327.
http://dx.doi.org/10.1093/glycob/cww052