Guardia, C.M.A.; Gauto, D.F.; Di Lella, S.; Rabinovich, G.A.; Martí, M.A.; Estrin, D.A. "An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network" (2011) Journal of Chemical Information and Modeling. 51(8):1918-1930
La versión final de este artículo es de uso interno de la institución.
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


Galectins, a family of evolutionarily conserved animal lectins, have been shown to modulate signaling processes leading to inflammation, apoptosis, immunoregulation, and angiogenesis through their ability to interact with poly-N-acetyllactosamine-enriched glycoconjugates. To date 16 human galectin carbohydrate recognition domains have been established by sequence analysis and found to be expressed in several tissues. Given the divergent functions of these lectins, it is of vital importance to understand common and differential features in order to search for specific inhibitors of individual members of the human galectin family. In this work we performed an integrated computational analysis of all individual members of the human galectin family. In the first place, we have built homology-based models for galectin-4 and -12 N-terminus, placental protein 13 (PP13) and PP13-like protein for which no experimental structural information is available. We have then performed classical molecular dynamics simulations of the whole 15 members family in free and ligand-bound states to analyze protein and protein-ligand interaction dynamics. Our results show that all galectins adopt the same fold, and the carbohydrate recognition domains are very similar with structural differences located in specific loops. These differences are reflected in the dynamics characteristics, where mobility differences translate into entropy values which significantly influence their ligand affinity. Thus, ligand selectivity appears to be modulated by subtle differences in the monosaccharide binding sites. Taken together, our results may contribute to the understanding, at a molecular level, of the structural and dynamical determinants that distinguish individual human galectins. © 2011 American Chemical Society.


Documento: Artículo
Título:An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network
Autor:Guardia, C.M.A.; Gauto, D.F.; Di Lella, S.; Rabinovich, G.A.; Martí, M.A.; Estrin, D.A.
Filiación:Departamento de Química Inorgánica, Analítica y Química Física, INQUIMAE-CONICET, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EHA Ciudad de Buenos Aires, Argentina
Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental (IBYME), CONICET, C1428ADN Ciudad de Buenos Aires, Argentina
Palabras clave:Angiogenesis; Carbohydrate-recognition domains; Classical molecular dynamics; Computational analysis; Dynamics characteristic; Entropy value; Galectins; Glycoconjugates; Immunoregulation; Ligand affinity; Ligand binding; Molecular levels; Protein-ligand interactions; Sequence analysis; Signaling process; Specific inhibitors; Structural differences; Structural information; Binding energy; Binding sites; Carbohydrates; Cell death; Computational methods; Dynamics; Glucose; Molecular dynamics; Proteins; Structural analysis; Tissue; Ligands; epitope; galectin; galectin 12, human; galectin 4; LGALS13 protein, human; ligand; placenta protein; poly N acetyllactosamine; poly-N-acetyllactosamine; polysaccharide; amino acid sequence; article; binding site; chemical structure; chemistry; entropy; human; immunology; metabolism; methodology; molecular dynamics; molecular genetics; nuclear magnetic resonance spectroscopy; phylogeny; physiology; protein binding; protein database; protein tertiary structure; sequence homology; signal transduction; systems biology; X ray crystallography; Amino Acid Sequence; Binding Sites; Crystallography, X-Ray; Databases, Protein; Entropy; Epitopes; Galectin 4; Galectins; Humans; Ligands; Magnetic Resonance Spectroscopy; Models, Molecular; Molecular Dynamics Simulation; Molecular Sequence Data; Phylogeny; Polysaccharides; Pregnancy Proteins; Protein Binding; Protein Structure, Tertiary; Sequence Homology, Amino Acid; Signal Transduction; Systems Biology
Página de inicio:1918
Página de fin:1930
Título revista:Journal of Chemical Information and Modeling
Título revista abreviado:J. Chem. Inf. Model.
CAS:Epitopes; Galectin 4; Galectins; LGALS13 protein, human; Ligands; Polysaccharides; Pregnancy Proteins; galectin 12, human; poly-N-acetyllactosamine, 82441-98-3


  • Cooper, D.N.W., Galectinomics: Finding themes in complexity (2002) Biochimica et Biophysica Acta - General Subjects, 1572 (2-3), pp. 209-231. , DOI 10.1016/S0304-4165(02)00310-0, PII S0304416502003100
  • Yang, R.Y., Rabinovich, G.A., Liu, F.T., Galectins: Structure, function and therapeutic potential (2008) Expert Rev. Mol. Med., 10, p. 17
  • Rabinovich, G.A., Toscano, M.A., Turning 'sweet' on immunity: Galectin-glycan interactions in immune tolerance and inflammation (2009) Nat. Rev. Immunol., 9, pp. 338-352
  • Toscano, M.A., Bianco, G.A., Ilarregui, J.M., Croci, D.O., Correale, J., Hernandez, J.D., Zwirner, N.W., Rabinovich, G.A., Differential glycosylation of TH1, TH2 and T H-17 effector cells selectively regulates susceptibility to cell death (2007) Nature Immunology, 8 (8), pp. 825-834. , DOI 10.1038/ni1482, PII NI1482
  • Rabinovich, G.A., Ilarregui, J.M., Conveying glycan information into T-cell homeostatic programs: A challenging role for galectin-1 in inflammatory and tumor microenvironments (2009) Immunol. Rev., 230, pp. 144-159
  • Laderach, D.J., Compagno, D., Toscano, M.A., Croci, D.O., Dergan-Dylon, S., Salatino, M., Rabinovich, G.A., Dissecting the signal transduction pathways triggered by galectin-glycan interactions in physiological and pathological settings (2010) IUBMB Life, 62, pp. 1-13
  • Cooper, D., Ilarregui, J.M., Pesoa, S.A., Croci, D.O., Perretti, M., Rabinovich, G.A., Multiple Functional Targets of the Immunoregulatory Activity of Galectin-1: Control of Immune Cell Trafficking, Dendritic Cell Physiology, and T-Cell Fate (2010) Methods Enzymol., 480, pp. 199-244
  • Ilarregui, J.M., Croci, D.O., Bianco, G.A., Toscano, M., Salatino, M., Vermeuen, 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, pp. 981-991
  • Dam, T.K., Brewer, C.F., Lectins as pattern recognition molecules: The effects of epitope density in innate immunity (2010) Glycobiology, 20, pp. 270-279
  • Lopez-Lucendo, M.F., Solis, D., Andre, 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) Journal of Molecular Biology, 343 (4), pp. 957-970. , DOI 10.1016/j.jmb.2004.08.078, PII S0022283604010782
  • Cho, M., Cummings, R.D., Galectin-1, a beta-galactoside-binding lectin in Chinese hamster ovary cells. I. Physical and chemical characterization (1995) J. Biol. Chem., 270, pp. 5198-5206
  • Liao, D.I., Kapadia, G., Ahmed, H., Vasta, G.R., Herzberg, O., Structure of S-lectin, a developmentally regulated vertebrate beta-galactoside-binding protein (1994) Proc. Natl. Acad. Sci. U.S.A., 91, pp. 1428-1432
  • Seetharaman, J., Kfanigsberg, A., Slaaby, R., Leffler, H., Barondes, S.H., Rini, J.M., X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-A resolution (1998) Journal of Biological Chemistry, 273 (21), pp. 13047-13052. , DOI 10.1074/jbc.273.21.13047
  • Nagae, M., Nishi, N., Nakamura-Tsuruta, S., Hirabayashi, J., Wakatsuki, S., Kato, R., Structural Analysis of the Human Galectin-9 N-terminal Carbohydrate Recognition Domain Reveals Unexpected Properties that Differ from the Mouse Orthologue (2008) Journal of Molecular Biology, 375 (1), pp. 119-135. , DOI 10.1016/j.jmb.2007.09.060, PII S0022283607012089
  • Nagae, M., Nishi, N., Murata, T., Usui, T., Nakamura, T., Wakatsuki, S., Kato, R., Structural analysis of the recognition mechanism of poly-N- acetyllactosamine by the human galectin-9 N-terminal carbohydrate recognition domain (2009) Glycobiology, 19, pp. 112-117
  • Yoshida, H., Teraoka, M., Nishi, N., Nakakita, S., Nakamura, T., Hirashima, M., Kamitori, S., X-ray structures of human galectin-9 C-terminal domain in complexes with a biantennary oligosaccharide and sialyllactose (2010) J. Biol. Chem., 285, pp. 36969-36976
  • Zhou, D., Ge, H., Sun, J., Gao, Y., Teng, M., Niu, L., Crystal structure of the C-terminal conserved domain of human GRP, a galectin-related protein, reveals a function mode different from those of galectins (2008) Proteins: Structure, Function and Genetics, 71 (3), pp. 1582-1588. , DOI 10.1002/prot.22003
  • Walti, M.A., Thore, S., Aebi, M., Kunzler, M., Crystal structure of the putative carbohydrate recognition domain of human galectin-related protein (2008) Proteins: Structure, Function and Genetics, 72 (2), pp. 804-808. , DOI 10.1002/prot.22078
  • Kato-Murayama, M., Murayama, K., Terada, T., Shirouzu, M., Yokoyama, S., Crystal structure of N-terminal domain of mouse galectin-4 Riken Structural Genomics/Proteomics Initiative (RSGI), ,, RIKEN, Japan, 2006
  • Tomizawa, T., Kigawa, T., Saito, K., Koshiba, S., Inoue, M., Yokoyama, S., Solution structure of the C-terminal Gal-bind lectin domain from human galectin-4 Riken Structural Genomics/Proteomics Initiative (RSGI), ,, RIKEN, Japan, 2005
  • Kishishita, S., Nishino, A., Murayama, K., Terada, T., Shirouzu, M., Yokoyama, S., Crystal structure of N-terminal domain of human galectin-8 Riken Structural Genomics/Proteomics Initiative (RSGI), ,, RIKEN, Japan, 2007
  • Kishishita, S., Nishino, A., Murayama, K., Terada, T., Shirouzu, M., Yokoyama, S., Crystal structure of N-terminal domain of human galectin-8 with D-lactose Riken Structural Genomics/Proteomics Initiative (RSGI), ,, RIKEN, Japan, 2007
  • Tomizawa, T., Koshiba, S., Inoue, M., Kigawa, T., Yokoyama, S., Solution structure of the C-terminal Gal-bind lectin protein from human galectin-8 Riken Structural Genomics/Proteomics Initiative (RSGI), ,, RIKEN, Japan, 2007
  • Lobsanov, Y.E.A., X-ray crystal structure of the human dimeric S-Lac lectin, L-14-II, in complex with lactose at 2.9 A resolution (1998) J. Biol. Chem., 268, pp. 27034-27038
  • Leonidas, D.D., Vatzaki, E.H., Vorum, H., Celis, J.E., Madsen, P., Acharya, K.R., Structural basis for the recognition of carbohydrates by human galectin- 7 (1998) Biochemistry, 37 (40), pp. 13930-13940. , DOI 10.1021/bi981056x
  • Leonidas, D.D., Elbert, B.L., Zhou Zeqi, Leffler, H., Ackerman, S.J., Acharya, K.R., Crystal structure of human Charcot-Leyden crystal protein, an eosinophil lysophospholipase, identifies it as a new member of the carbohydrate-binding family of galectins (1995) Structure, 3 (12), pp. 1379-1393. , DOI 10.1016/S0969-2126(01)00275-1
  • Visegrady, B., Than, N.G., Kilar, F., Sumegi, B., Than, G.N., Bohn, H., Homology modelling and molecular dynamics studies of human placental tissue protein 13 (galectin-13) (2001) Protein Engineering, 14 (11), pp. 875-880
  • Than, N.G., Pick, E., Bellyei, S., Szigeti, A., Burger, O., Berente, Z., Janaky, T., Sumegi, B., Functional analyses of placental protein 13/galectin-13 (2004) European Journal of Biochemistry, 271 (6), pp. 1065-1078. , DOI 10.1111/j.1432-1033.2004.04004.x
  • Hirabayashi, J., Kasai, K.-I., The family of metazoan metal-independent -galactoside-binding lectins: Structure, function and molecular evolution (1993) Glycobiology, 3 (4), pp. 297-304
  • Houzelstein, D., Goncalves, I.R., Fadden, A.J., Sidhu, S.S., Cooper, D.N.W., Drickamer, K., Leffler, H., Poirier, F., Phylogenetic analysis of the vertebrate galectin family (2004) Molecular Biology and Evolution, 21 (7), pp. 1177-1187. , DOI 10.1093/molbev/msh082
  • Lee, E.H., Hsin, J., Sotomayor, M., Comellas, G., Schulten, K., Discovery through the computational microscope (2009) Structure, 17, pp. 1295-1306
  • Leach, A.R., Molecular Modelling (2001) Principles and Applications, p. 744. , Pearson Education EMA: Harlow, England
  • Adcock, S.A., McCammon, J.A., Molecular dynamics: Survey of methods for simulating the activity of proteins (2006) Chemical Reviews, 106 (5), pp. 1589-1615. , DOI 10.1021/cr040426m
  • Eswar, N., Webb, B., Martí-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.Y., Pieper, U., Sali, A., Comparative protein structure modelling using MODELLER (2006) Current Protocols in Bioinformatics, pp. 561-5630. , In; John Wiley & Sons, Inc: New York, Chapter 5, Unit 5.6
  • Marti-Renom, M.A., Stuart, A.C., Fiser, A., Sanchez, R., Melo, F., Sali, A., Comparative protein structure modeling of genes and genomes (2000) Annual Review of Biophysics and Biomolecular Structure, 29, pp. 291-325. , DOI 10.1146/annurev.biophys.29.1.291
  • Thompson, J.D., Higgins, D.G., Gibson, T.J., CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice (1994) Nucleic Acids Research, 22 (22), pp. 4673-4680
  • Berendsen, H.J.C., 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, pp. 3684-3690
  • Van Gunsteren, W.F., Berendsen, H.J.C., Computer simulation of molecular dynamics: Methodology, applications, and perspectives in chemistry (1990) Angew. Chem., Int. Ed. Engl., 29, pp. 992-1023
  • Ryckaert, J.P., Ciccotti, G., Berendsen, H.J.C., Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes (1977) J. Comput. Phys., 23, pp. 327-341
  • 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: Structure, Function and Genetics, 65 (3), pp. 712-725. , DOI 10.1002/prot.21123
  • Woods, R.J., Dwek, R.A., Edge, C.J., Fraser-Reid, B., Molecular mechanical and molecular dynamic simulations of glycoproteins and oligosaccharides. 1. GLYCAM-93 parameter development (1995) J. Phys. Chem., 99, pp. 3832-3846
  • Kirschner, K.N., Yongye, A.B., Tschampel, S.M., Gonzalez-Outeirino, J., Daniels, C.R., Foley, B.L., Woods, R.J., GLYCAM06: A generalizable biomolecular force field. carbohydrates (2008) Journal of Computational Chemistry, 29 (4), pp. 622-655. , DOI 10.1002/jcc.20820
  • Amadei, A., Linssen, A.B.M., Berendsen, H.J.C., Essential dynamics of proteins (1993) Proteins: Structure, Function and Genetics, 17 (4), pp. 412-425. , DOI 10.1002/prot.340170408
  • Capece, L., Estrin, D.A., Marti, M.A., Dynamical characterization of the heme NO oxygen binding (HNOX) domain. Insight into soluble guanylate cyclase allosteric transition (2008) Biochemistry, 47, pp. 9416-9427
  • Martí, M.A., Estrin, D.A., Roitberg, A.E., Molecular basis for the pH dependent structural transition of nitrophorin 4 (2009) J. Phys. Chem. B, 113, pp. 2135-2142
  • Capece, L., Marti, M.A., Bidon-Chanal, A., Nadra, A., Luque, F.J., Estrin, D.A., High pressure reveals structural determinants for globin hexacoordination: Neuroglobin and myoglobin cases (2009) Proteins, 75, pp. 885-894
  • Schlitter, J., Estimation of absolute and relative entropies of macromolecules using the covariance matrix (1993) Chem. Phys. Lett., 215, pp. 617-621
  • Andricioaei, I., Karplus, M., On the calculation of entropy from covariance matrices of the atomic fluctuations (2001) Journal of Chemical Physics, 115 (14), pp. 6289-6292. , DOI 10.1063/1.1401821
  • Harris, S.A., Gavathiotis, E., Searle, M.S., Orozco, M., Laughton, C.A., Cooperativity in drug-DNA recognition: A molecular dynamics study (2001) Journal of the American Chemical Society, 123 (50), pp. 12658-12663. , DOI 10.1021/ja016233n
  • Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., Klein, M.L., Comparison of simple potential functions for simulating liquid water (1983) J. Chem. Phys., 79, pp. 926-935
  • Bashford, D., Case, D.A., Generalized Born models of macromolecular salvation effects (2003) Annu. Rev. Phys. Chem., 51, pp. 129-152
  • 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, pp. 8033-8043
  • Case, D.A., Darden, T.A., Simmerling, C.L., Wang, J., Duke, R.E., Luo, R., Merz, K.M., Kollman, P.A., (2006) AMBER 9, , University of California: San Francisco, CA
  • Case, D.A., Cheatham III, T.E., Darden, T., Gohlke, H., Luo, R., Merz Jr., K.M., Onufriev, A., Woods, R.J., The Amber biomolecular simulation programs (2005) Journal of Computational Chemistry, 26 (16), pp. 1668-1688. , DOI 10.1002/jcc.20290
  • Constanciel, R., Contreras, R., Self consistent field theory of solvent effects representation by continuum models: Introduction of desolvation contribution (1984) Theor. Chim. Acta, 65, pp. 1-11
  • Still, W.C., Tempczyrk, A., Hawley, R.C., Hendrickson, T., Semianalytical treatment of solvation for molecular mechanics and dynamics (1990) J. Am. Chem. Soc., 112, pp. 6127-6129
  • Scheeff, E.D., Bourne, P.E., Structural evolution of the protein kinase-like superfamily (2005) PLoS Comput. Biol., 1, p. 49
  • Moens, L., Vanfleteren, J., Van De Peer, Y., Peeters, K., Kapp, O., Czeluzniak, J., Goodman, M., Vinogradov, S., Globins in nonvertebrate species: Dispersal by horizontal gene transfer and evolution of the structure-function relationships (1996) Molecular Biology and Evolution, 13 (2), pp. 324-333
  • Hirabayashi, J., Kasai, K.-I., Effect of amino acid substitution by site-directed mutagenesis on the carbohydrate recognition and stability of human 14-kDa -galactoside-binding lectin (1991) Journal of Biological Chemistry, 266 (35), pp. 23648-23653
  • Leffler, H., Barondes, S.H., Specificity of binding of three soluble rat lung lectins to substituted and unsubstituted mammalian -galactosides (1986) Journal of Biological Chemistry, 261 (22), pp. 10119-10126
  • Martin-Galiano, A.J., Buey, R.M., Cabezas, M., Andreu, J.M., Mapping flexibility and the assembly switch of cell division protein FtsZ by computational and mutational approaches (2010) J. Biol. Chem., 285, pp. 22554-22565
  • Van Aalten, D.M.F., De Groot, B.L., Findlay, J.B.C., Berendsen, H.J.C., Amadei, A., A comparison of techniques for calculating protein essential dynamics (1997) Journal of Computational Chemistry, 18 (2), pp. 169-181
  • Swaminathan, G.J., Leonidas, D.D., Savage, M.P., Ackerman, S.J., Acharya, K.R., Selective recognition of mannose by the human eosinophil Charcot-Leyden crystal protein (galectin-10): A crystallographic study at 1.8 A resolution (1999) Biochemistry, 38 (42), pp. 13837-13843. , DOI 10.1021/bi990756e
  • Ford, M.G., Weimar, T., Kohli, T., Woods, R.J., Molecular dynamics simulations of galectin-1-oligosaccharide complexes reveal the molecular basis for ligand diversity (2003) Proteins: Structure, Function and Genetics, 53 (2), pp. 229-240. , DOI 10.1002/prot.10428
  • 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, pp. 1209-1230
  • Schwarz, F.P., Ahmed, H., Bianchet, M.A., Amzel, L.M., Vasta, G.R., Thermodynamics of bovine spleen galectin-1 binding to disaccharides: Correlation with structure and its effect on oligomerization at the denaturation temperature (1998) Biochemistry, 37 (17), pp. 5867-5877. , DOI 10.1021/bi9716478
  • Brewer, C.F., Thermodynamic binding studies of galectin-1, -3 and -7 (2002) Glycoconjugate Journal, 19 (7-9), pp. 459-465. , DOI 10.1023/B:GLYC.0000014075.62724.d0
  • Ideo, H., Seko, A., Ishizuka, I., Yamashita, K., The N-terminal carbohydrate recognition domain of galectin-8 recognizes specific glycosphingolipids with high affinity (2003) Glycobiology, 13 (10), pp. 713-723. , DOI 10.1093/glycob/cwg094
  • Anisimov, V.M., Cavasotto, C.N., Quantum mechanical binding free energy calculation for phosphopeptide inhibitors of the Lck SH2 domain (2011) J. Comput. Chem., 32, pp. 2254-2263
  • Stowell, S.R., Cho, M., Feasley, C.L., Arthur, C.M., Song, X., Colucci, J.K., Karmakar, S., Cummings, R.D., Ligand reduces galectin-1 sensitivity to oxidative inactivation by enhancing dimer formation (2009) J. Biol. Chem., 284, pp. 4989-4999
  • Di Lella, S., Martí, M.A., Croci, D.O., Guardia, C.M.A., Díaz-Ricci, J.C., Rabinovich, G.A., Caramelo, J.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, pp. 7652-7658


---------- APA ----------
Guardia, C.M.A., Gauto, D.F., Di Lella, S., Rabinovich, G.A., Martí, M.A. & Estrin, D.A. (2011) . An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network. Journal of Chemical Information and Modeling, 51(8), 1918-1930.
---------- CHICAGO ----------
Guardia, C.M.A., Gauto, D.F., Di Lella, S., Rabinovich, G.A., Martí, M.A., Estrin, D.A. "An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network" . Journal of Chemical Information and Modeling 51, no. 8 (2011) : 1918-1930.
---------- MLA ----------
Guardia, C.M.A., Gauto, D.F., Di Lella, S., Rabinovich, G.A., Martí, M.A., Estrin, D.A. "An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network" . Journal of Chemical Information and Modeling, vol. 51, no. 8, 2011, pp. 1918-1930.
---------- VANCOUVER ----------
Guardia, C.M.A., Gauto, D.F., Di Lella, S., Rabinovich, G.A., Martí, M.A., Estrin, D.A. An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network. J. Chem. Inf. Model. 2011;51(8):1918-1930.