Structural aspects of binding of-linked digalactosides to human galectin-1

Glycobiology

Volumn 21, Issue 12, 2011, Pages 1627-1641

  Miller, Michelle C ^a   Ribeiro, João P ^b   Roldós, Virginia ^b   Martín Santamaría, Sonsoles ^c   Cañada, F Javier ^b   Nesmelova, Irina A ^a   André, Sabine ^d   Pang, Mabel ^e   Klyosov, Anatole A ^f   Baum, Linda G ^e   Jiménez Barbero, Jesús ^b   Gabius, Hans Joachim ^d   Mayo, Kevin H ^a  

^a University of Minnesota   (United States)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c UNIVERSIDAD SAN PABLO CEU   (Spain)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Galectin Therapeutics   (United States)

Author keywords

agglutinin; glycolipid; glycoprotein; lectin; sugar code

Indexed keywords

ALPHA(1-3)LINKED DIGALACTOSIDE; ALPHA(1-4)LINKED DIGALACTOSIDE; GALACTOSIDE; GALECTIN 1; LACTOSE; MELIBIOSE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROGEN BOND; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; SATURATION TRANSFER DIFFERE NUCLEAR MAGNETIC RESONANCE;

BINDING SITES; GALACTOSIDES; GALECTIN 1; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION;

EID: 81855194817     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwr083     Document Type: Article

References (68)

1. Ahmed H, Allen HJ, Sharma A, Matta KL. 1990. Human splenic galaptin: Carbohydrate-binding specificity and characterization of the combining site. Biochemistry. 29:5315-5319. (Pubitemid 20193937)
2. Alonso-Plaza JM, Canales MA, Jiménez M, Roldán JL, García-Herrero A, Iturrino L, Asensio JL, Cañada FJ, Romero A, Siebert H-C, et al. 2001. NMR investigations of protein-carbohydrate interactions: Insights into the topology of the bound conformation of a lactose isomer and β-galactosyl xyloses to mistletoe lectin and galectin-1. Biochim Biophys Acta. 1568:225-236. (Pubitemid 34107297)
3. André S, Giguère D, Dam TK, Brewer CF, Gabius H-J, Roy R. 2010. Synthesis and screening of a small glycomimetic library for inhibitory activity on medically relevant galactoside-specific lectins in assays of increasing biorelevance. New J Chem. 34:2229-2240.
4. André S, Pei Z, Siebert H-C, Ramström O, Gabius H-J. 2006. Glycosyldisulfides from dynamic combinatorial libraries as O-glycoside mimetics for plant and endogenous lectins: Their reactivities in solid-phase and cell assays and conformational analysis by molecular dynamics simulations. Bioorg Med Chem. 14:6314-6326. (Pubitemid 44224074)
5. André S, Sanchez-Ruderisch H, Nakagawa H, Buchholz M, Kopitz J, Forberich P, Kemmner W, Böck C, Deguchi K, Detjen KM, et al. 2007. Tumor suppressor p16INK4a: Modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J. 274:3233-3256. (Pubitemid 47028461)
6. Appukuttan PS. 2002. Terminal α-linked galactose rather than N-acetyllactosamine is ligand for bovine heart galectin-1 in N-linked oligosaccharides of glycoproteins. J Mol Recogn. 15:180-187. (Pubitemid 35249839)
7. Appukuttan PS, Geetha M, Annamma KI. 1995. Anomer specificity of the 14 kDa galactose-binding lectin, a reappraisal. J Biosci. 20:377-384.
8. Asensio JL, Espinosa JF, Dietrich H, Cañada FJ, Schmidt RR, Martín-Lomas M, André S, Gabius H-J, Jiménez-Barbero J. 1999. Bovine heart galectin-1 selects a unique (syn) conformation of C-lactose, a flexible lactose analogue. J Am Chem Soc. 121:8995-9000.
9. Barondes SH, Cooper DNW, Gitt MA, Leffler H. 1994. Galectins. Structure and function of a large family of animal lectins. J Biol Chem. 269:20807-20810.
10. Batchelor RJ, Green DF, Johnston BD, Patrick BO, Pinto BM. 2001. Conformational preferences in glycosylamines. Implications for the exo-anomeric effect. Carbohydr Res. 330:421-426. (Pubitemid 32206412)
11. Bharadwaj S, Kaltner H, Korchagina EY, Bovin NV, Gabius H-J, Surolia A. 1999. Microcalorimetric indications for ligand binding as a function of the protein for galactoside-specific plant and avian lectins. Biochim Biophys Acta. 1472:191-196. (Pubitemid 29486529)
12. Bourne Y, Bolgiano B, Liao DI, Strecker G, Cantau P, Herzberg O, Feizi T, Cambillau C. 1994. Crosslinking of mammalian lectin (galectin-1) by complex biantennary saccharides. Nat Struct Biol. 1:863-870. (Pubitemid 24974809)
13. Case DA, Darden TA, Cheatham TE, III, Simmerling CL, Wang J, Duke RE, Luo R, Crowley M, Walker RC, Zhang W, et al. 2008. AMBER 10. San Francisco: University of California.
14. Cooper DNW. 2002. Galectinomics: finding themes in complexity. Biochim Biophys Acta. 1572:209-231.
15. Dam TK, Gabius H-J, André S, Kaltner H, Lensch M, Brewer CF. 2005. Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants. Biochemistry. 44:12564-12571. (Pubitemid 41324347)
16. Darden T, York D, Pedersen L. 1993. Particle mesh Ewald: An N log(N) method for Ewald sums in large systems. J Chem Phys. 98:10089-10092.
17. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. 1995. NMRpipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR. 6:277-293.
18. Dhirapong A, Lleo A, Leung P, Gershwin ME, Liu F-T. 2009. The immunological potential of galectins-1 and-3. Autoimmun Rev. 8:360-363.
19. Fischer C, Sanchez-Ruderisch H, Welzel M, Wiedenmann B, Sakai T, André S, Gabius H-J, Khachigian L, Detjen KM, Rosewicz S. 2005. Galectin-1 interacts with the α5β1 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J Biol Chem. 280:37266-37277. (Pubitemid 41587811)
20. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA, Jr., Vreven T, Kudin KN, Burant JC, et al. 2004. Gaussian 03, Revision C.02 ed. Wallingford (CT): Gaussian, Inc.
21. Gabius H-J. 2006. Cell surface glycans: The why and how of their functionality as biochemical signals in lectin-mediated information transfer. Crit Rev Immunol. 26:43-79.
22. Gabius H-J, editors. (2009) The Sugar Code. Fundamentals of Glycosciences. Weinheim: Wiley-VCH.
23. Gabius H-J, André S, Jiménez-Barbero J, Romero A, Solís D. 2011. From lectin structure to functional glycomics: Principles of the sugar code. Trends Biochem Sci. 36:298-313.
24. Gabius H-J, Darro F, Remmelink M, André S, Kopitz J, Danguy A, Gabius S, Salmon I, Kiss R. 2001. Evidence for stimulation of tumor proliferation in cell lines and histotypic cultures by clinically relevant low doses of the galactoside-binding mistletoe lectin, a component of proprietary extracts. Cancer Invest. 19:114-126. (Pubitemid 32236689)
25. Gabius H-J, Walzel H, Joshi SS, Kruip J, Kojima S, Gerke V, Kratzin H, Gabius S. 1992. The immunomodulatory galactoside-specific lectin from mistletoe: Partial sequence analysis, cell and tissue binding, and impact on intracellular biosignalling of monocytic leukemia cells. Anticancer Res. 12:669-675.
26. Galanina OE, Kaltner H, Khraltsova LS, Bovin NV, Gabius H-J. 1997. Further refinement of the description of the ligand-binding characteristics for the galactoside-binding mistletoe lectin, a plant agglutinin with immunomodulatory potency. J Mol Recognit. 10:139-147. (Pubitemid 28012387)
27. Garner OB, Baum LG. 2008. Galectin-glycan lattices regulate cell-surface glycoprotein organization and signalling. Biochem Soc Trans. 36:1472-1477.
28. Garrett M, Morris RH, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. AutoDock4 and AutoDock Tools4: Automated Docking with selective receptor flexibility. J Comput Chem. 30:2785-2791.
29. Hirabayashi J, Hashidate T, Arata Y, Nishi N, Nakamura T, Hirashima M, Urashima T, Oka T, Futai M, Müller WEG, et al. 2002. Oligosaccharide specificity of galectins: A search by frontal affinity chromatography. Biochim Biophys Acta. 1572:232-254. (Pubitemid 35246347)
30. Jiménez M, André S, Barillari C, Romero A, Rognan D, Gabius H-J, Solís D. 2008. Domain versatility in plant AB-toxins: Evidence for a local, pH-dependent rearrangement in the 2γ lectin site of the mistletoe lectin by applying ligand derivatives and modelling. FEBS Lett. 582:2309-2312.
31. Jiménez M, André S, Siebert H-C, Gabius H-J, Solís D. 2006. AB-type lectin (toxin/agglutinin) from mistletoe: Differences in affinity of the two galactoside-binding Trp/Tyr-sites and regulation of their functionality by monomer/dimer equilibrium. Glycobiology. 16:926-937. (Pubitemid 44399122)
32. Jiménez-Barbero J, Dragoni E, Venturi C, Nannucci F, Ardá A, Fontanella M, André S, Cañada FJ, Gabius H-J, Nativi C. 2009. α-O-Linked glycopeptide mimetics: Synthesis, conformation analysis, and interactions with viscumin, a galactoside-binding model lectin. Chem Eur J. 15:10423-10431.
33. Jin R, Greenwald A, Peterson MD, Waddell TK. 2006. Human monocytes recognize porcine endothelium via the interaction of galectin-3 and α-GAL. J Immunol. 177:1289-1295. (Pubitemid 44036635)
34. Johnson BA, Blevins RA. 1994. NMR view: A computer program for the visualization and analysis of NMR data. J Biomol NMR. 4:603-614.
35. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. 1983. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 79:926-935.
36. Kasai K-I, Hirabayashi J. 1996. Galectins: A family of animal lectins that decipher glycocodes. J Biochem. 119:1-8. (Pubitemid 26048050)
37. Kirschner KN, Yongye AB, Tschampel SM, González-Outeiriño J, Daniels CR, Foley BL, Woods RJ. 2008. GLYCAM06: A generalizable biomolecular force field. Carbohydrates. J Comput Chem. 29:622-655. (Pubitemid 351238844)
38. Klyosov AA, Witczak ZJ, Platt D, editors. (2008) Galectins. Hoboken: J. Wiley & Sons.
39. Kopitz J, Bergmann M, Gabius H-J. 2010. How adhesion/growth-regulatory galectins-1 and-3 attain cell specificity: Case study defining their target on neuroblastoma cells (SK-N-MC) and marked affinity regulation by affecting microdomain organization of the membrane. IUBMB Life. 62:624-628.
40. Krzeminski M, Singh T, André S, Lensch M, Wu AM, Bonvin AMJJ, Gabius H-J. 2011. Human galectin-3 (Mac-2 antigen): Defining molecular switches of affinity to natural glycoproteins, structural and dynamic aspects of glycan binding by flexible ligand docking and putative regulatory sequences in the proximal promoter region. Biochim Biophys Acta. 1810:150-161.
41. Lacey ME, Subramanian R, Olson DL, Webb AG, Sweedler JV. 1999. High-resolution NMR spectroscopy of sample volumes from 1 nL to 10 μL. Chem Rev. 99:3133-3152. (Pubitemid 129582907)
42. Lee RT, Gabius H-J, Lee YC. 1992. Ligand binding characteristics of the major mistletoe lectin. J Biol Chem. 267:23722-23727. (Pubitemid 23088177)
43. Lee RT, Ichikawa Y, Allen HJ, Lee YC. 1990. Binding characteristics of galactoside-binding lectin (galaptin) from human spleen. J Biol Chem. 265:7864-7871.
44. López-Lucendo MF, Solís D, André S, Hirabayashi J, Kasai K-I, Kaltner H, Gabius H-J, Romero A. 2004. 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. 343:957-970. (Pubitemid 39345956)
45. Macher BA, Galili U. 2008. The Galα1,3Galβ1,4GlcNAc-R (α-Gal) epitope: A carbohydrate of unique evolution and clinical relevance. Biochim Biophys Acta. 1780:75-88.
46. Miller M, Klyosov A, Mayo KH. 2009. The α-galactomannan Davanat binds galectin-1 at a site different from the conventional galectin carbohydrate binding site. Glycobiology. 19:1034-1045.
47. Miller M, Nesmelova IV, Klyosov A, Platt D, Mayo KH. 2009. The carbohydrate binding domain on galectin-1 is more extensive for a complex glycan than for simple saccharides: Implications for galectin-glycan interactions at the cell surface. Biochem J. 421:211-221.
48. Mocak J, Bond AM, Mitchell S, Scollary G. 1997. A statistical overview of standard (IUPAC and ACS) and new procedures for determining the limits of detection and quantification: Application to voltammetric and stripping techniques. Pure Appl Chem. 69:297-328.
49. Nesmelova IV, Ermakova E, Daragan VA, Pang M, Menéndez M, Lagartera L, Solís D, Baum LG, Mayo KH. 2010. Lactose binding to galectin-1 modulates structural dynamics, increases conformational entropy, and occurs with apparent negative cooperativity. J Mol Biol. 397:1209-1230.
50. Nesmelova IV, Pang M, Baum LG, Mayo KH. 2008. 1H, 13C, and 15N backbone and side-chain chemical shift assignments for the 29 kDa human galectin-1 protein dimer. J NMR Assign. 2:203-205.
51. Pace KE, Baum LG. 1997. Induction of T lymphocyte apoptosis: A novel function for galectin-1. Trends Glycosci Glycotechnol. 9:21-29. (Pubitemid 127621042)
52. Pace KE, Hahn HP, Pang M, Nguyen JT, Baum LG. 2000. CD7 delivers a pro-apoptotic signal during galectin-1-induced T cell death. J Immunol. 165:2332-2334.
53. Platt D, Klyosov AA, Zomer E. 2006. Carbohydrate drug design. In: Klyosov AA, Witczak ZJ, Platt D, editors. ACS Symposium Series 932. Washington (DC): American Chemical Society. p. 49-66.
54. Rajagopal P, Waygood EB, Reizer J, Saier MH, Klevit RE. 1997. Demonstration of protein-protein interaction specificity by NMR chemical shift mapping. Protein Sci. 6:2624-2627. (Pubitemid 28006699)
55. Rapoport EM, André S, Kurmyshkina OV, Pochechueva TV, Severov VV, Pazynina GV, Gabius H-J, Bovin NV. 2008. Galectin-loaded cells as a platform for the profiling of lectin specificity by fluorescent neoglycoconjugates: A case study on galectins-1 and-3 and the impact of assay setting. Glycobiology. 18:315-324. (Pubitemid 351461064)
56. Ribeiro JP, André S, Cañada FJ, Gabius H-J, Butera AP, Alves RJ, Jiménez-Barbero J. 2010. Lectin-based drug design: Combined strategy to identify lead compounds using STD NMR spectroscopy, solid-phase assays and cell binding for a plant toxin model. ChemMedChem. 5:415-419.
57. Ryckaert J-P, Ciccotti G, Berendsen HJC. 1977. Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J Comput Physics. 23:327-341.
58. Sanchez-Ruderisch H, Detjen KM, Welzel M, André S, Fischer C, Gabius H-J, Rosewicz S. 2011. Galectin-1 sensitizes carcinoma cells to anoikis via the fibronectin receptor α5β1-integrin. Cell Death Differ. 18:806-816.
59. Schrödinger LLC. 2005. The Maestro suite of programs: A powerful, allpurpose molecular modeling environment. New York: Schroedinger LLC.
60. Siebert H-C, Adar R, Arango R, Burchert M, Kaltner H, Kayser G, Tajkhorshid E, von der Lieth C-W, Kaptein R, Sharon N, et al. 1997. Involvement of laser photo-CIDNP (chemically induced dynamic nuclear polarization)-reactive amino acid side chains in ligand binding by galactoside-specific lectins in solution. Eur J Biochem. 249:27-38. (Pubitemid 27432592)
61. Siebert H-C, André S, Lu SY, Frank M, Kaltner H, van Kuik JA, Korchagina EY, Bovin NV, Tajkhorshid E, Kaptein R, et al. 2003. Unique conformer selection of human growth-regulatory lectin galectin-1 for ganglioside GM1 versus bacterial toxins. Biochemistry. 42:14762-14773. (Pubitemid 37553504)
62. Sparrow CP, Leffler H, Barondes SH. 1987. Multiple soluble β-galactosidebinding lectins from human lung. J Biol Chem. 262:7383-7390.
63. Stowell SR, Dias-Baruffi M, Penttilä L, Renkonen O, Nyame AK, Cummings RD. 2004. Human galectin-1 recognition of poly-N-acetyllactosamine and chimeric polysaccharides. Glycobiology. 14:157-167. (Pubitemid 38263100)
64. Villalobo A, Nogales-González A, Gabius H-J. 2006. A guide to signaling pathways connecting protein-glycan interaction with the emerging versatile effector functionality of mammalian lectins. Trends Glycosci Glycotechnol. 18:1-37. (Pubitemid 43723385)
65. Wang J, Lu ZH, Gabius H-J, Rohowsky-Kochan C, Ledeen RW, Wu G. 2009. Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T cell activity involving TRPC5 channel activation: Possible role in suppressing experimental autoimmune encephalomyelitis. J Immunol. 182:4036-4045.
66. Weiner SJ, Kollman PA, Case DA, Singh UC, Ghio C, Alagona G, Profeta S, Weiner P. 1984. A new force field for molecular mechanical simulation of nucleic acids and proteins. J Am Chem Soc. 106:765-784. (Pubitemid 14548426)
67. Wu AM, Singh T, Wu JH, Lensch M, André S, Gabius H-J. 2006. Interaction profile of galectin-5 with free saccharides and mammalian glycoproteins: Probing its fine specificity and the effect of naturally clustered ligand presentation. Glycobiology. 16:524-537. (Pubitemid 43779048)
68. Wu AM, Wu JH, Liu J-H, Singh T, André S, Kaltner H, Gabius H-J. 2004. Effects of polyvalency of glycotopes and natural modifications of human blood group ABH/Lewis sugars at the Galβ1-terminated core saccharides on the binding of domain-I of recombinant tandem-repeat-type galectin-4 from rat gastrointestinal tract (G4-N). Biochimie. 86:317-326. (Pubitemid 38780838)