Critical Role of the Solvent Environment in Galectin-1 Binding to the Disaccharide Lactose

Overview

Journal Biochemistry

Specialty Biochemistry

Date 2009 Jan 9

PMID 19128029

Citations 12

Authors

Santiago Di Lella

Lu Ma

Juan C Diaz Ricci

Gabriel A Rabinovich

Sanford A Asher

R Maria S Alvarez

Affiliations

Soon will be listed here.

Abstract

Galectin-1 (Gal-1), a member of a family of evolutionarily conserved glycan-binding proteins, binds specifically to poly-N-acetyllactosamine-enriched glycoconjugates. Through interactions with these glycoconjugates, this protein modulates inflammatory responses and contributes to tumor progression and immune cell homeostasis. The carbohydrate recognition domain includes the single protein tryptophan (Trp68). UV resonance Raman spectroscopy and molecular dynamic simulation were used to examine the change in the environment of the Trp on ligand binding. The UV Raman spectra and the calculated water radial distribution functions show that, while no large structural changes in the protein follow lactose binding, substantial solvent reorganization occurs. These new insights into the microscopic role of water molecules in Gal-1 binding to its specific carbohydrate ligands provides a better understanding of the physicochemical properties of Gal-1-saccharide interactions, which will be useful for the design of synthetic inhibitors for therapeutic purposes.

Citing Articles

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References

Miura T, Takeuchi H, Harada I . Characterization of individual tryptophan side chains in proteins using Raman spectroscopy and hydrogen-deuterium exchange kinetics. Biochemistry. 1988; 27(1):88-94. DOI: 10.1021/bi00401a015. View

Case D, Cheatham 3rd T, Darden T, Gohlke H, Luo R, Merz Jr K . The Amber biomolecular simulation programs. J Comput Chem. 2005; 26(16):1668-88. PMC: 1989667. DOI: 10.1002/jcc.20290. View

Toscano M, Ilarregui J, Bianco G, Campagna L, Croci D, Salatino M . Dissecting the pathophysiologic role of endogenous lectins: glycan-binding proteins with cytokine-like activity?. Cytokine Growth Factor Rev. 2007; 18(1-2):57-71. DOI: 10.1016/j.cytogfr.2007.01.006. View

Cho M, Cummings R . Galectin-1, a beta-galactoside-binding lectin in Chinese hamster ovary cells. I. Physical and chemical characterization. J Biol Chem. 1995; 270(10):5198-206. DOI: 10.1074/jbc.270.10.5198. View

Lopez-Lucendo M, Solis D, Andre S, Hirabayashi J, Kasai K, Kaltner H . 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. J Mol Biol. 2004; 343(4):957-70. DOI: 10.1016/j.jmb.2004.08.078. View

Elola M, Wolfenstein-Todel C, Troncoso M, Vasta G, Rabinovich G . Galectins: matricellular glycan-binding proteins linking cell adhesion, migration, and survival. Cell Mol Life Sci. 2007; 64(13):1679-700. PMC: 11136145. DOI: 10.1007/s00018-007-7044-8. View

Barrionuevo P, Beigier-Bompadre M, Ilarregui J, Toscano M, Bianco G, Isturiz M . A novel function for galectin-1 at the crossroad of innate and adaptive immunity: galectin-1 regulates monocyte/macrophage physiology through a nonapoptotic ERK-dependent pathway. J Immunol. 2006; 178(1):436-45. DOI: 10.4049/jimmunol.178.1.436. View

Rabinovich G, Liu F, Hirashima M, Anderson A . An emerging role for galectins in tuning the immune response: lessons from experimental models of inflammatory disease, autoimmunity and cancer. Scand J Immunol. 2007; 66(2-3):143-58. DOI: 10.1111/j.1365-3083.2007.01986.x. View

Chi Z, Asher S . UV resonance Raman determination of protein acid denaturation: selective unfolding of helical segments of horse myoglobin. Biochemistry. 1998; 37(9):2865-72. DOI: 10.1021/bi971161r. View

10.

Clarke C, Woods R, Gluska J, Cooper A, Nutley M, Boons G . Involvement of water in carbohydrate-protein binding. J Am Chem Soc. 2001; 123(49):12238-47. DOI: 10.1021/ja004315q. View

11.

Asensio J, Siebert H, Von der Lieth C, Laynez J, Bruix M, Soedjanaamadja U . 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.... Proteins. 2000; 40(2):218-36. View

12.

Ahmad N, Gabius H, Sabesan S, Oscarson S, Brewer C . Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin-3, and the carbohydrate recognition domain of galectin-3. Glycobiology. 2004; 14(9):817-25. DOI: 10.1093/glycob/cwh095. View

13.

Pace K, Hahn H, Baum L . Preparation of recombinant human galectin-1 and use in T-cell death assays. Methods Enzymol. 2003; 363:499-518. DOI: 10.1016/S0076-6879(03)01075-9. View

14.

Ahmed Z, Beta I, Mikhonin A, Asher S . UV-resonance raman thermal unfolding study of Trp-cage shows that it is not a simple two-state miniprotein. J Am Chem Soc. 2005; 127(31):10943-50. DOI: 10.1021/ja050664e. View

15.

Kopitz J, von Reitzenstein C, Burchert M, Cantz M, Gabius H . Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J Biol Chem. 1998; 273(18):11205-11. DOI: 10.1074/jbc.273.18.11205. View

16.

Takeuchi H . Raman structural markers of tryptophan and histidine side chains in proteins. Biopolymers. 2003; 72(5):305-17. DOI: 10.1002/bip.10440. View

17.

Walzel H, Schulz U, Neels P, Brock J . Galectin-1, a natural ligand for the receptor-type protein tyrosine phosphatase CD45. Immunol Lett. 1999; 67(3):193-202. DOI: 10.1016/s0165-2478(99)00012-7. View

18.

Andre S, Kojima S, Yamazaki N, Fink C, Kaltner H, Kayser K . Galectins-1 and -3 and their ligands in tumor biology. Non-uniform properties in cell-surface presentation and modulation of adhesion to matrix glycoproteins for various tumor cell lines, in biodistribution of free and liposome-bound galectins and.... J Cancer Res Clin Oncol. 1999; 125(8-9):461-74. DOI: 10.1007/s004320050303. View

19.

Di Lella S, Marti M, Alvarez R, Estrin D, Diaz Ricci J . Characterization of the galectin-1 carbohydrate recognition domain in terms of solvent occupancy. J Phys Chem B. 2007; 111(25):7360-6. DOI: 10.1021/jp068989k. View

20.

Cheatham 3rd T, Cieplak P, Kollman P . A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J Biomol Struct Dyn. 1999; 16(4):845-62. DOI: 10.1080/07391102.1999.10508297. View