Intra- and intermolecular interactions of human galectin-3: Assessment by full-assignment-based NMR

Glycobiology

Volumn 26, Issue 8, 2016, Pages 888-903

  Ippel, Hans ^a,b   Miller, Michelle C ^a   Vértesy, Sabine ^c   Zheng, Yi ^d   Cañada, F Javier ^e   Suylen, Dennis ^b   Umemoto, Kimiko ^f   Romanò, Cecilia ^g   Hackeng, Tilman ^b   Tai, Guihua ^d   Leffler, Hakon ^h   Kopitz, Jürgen ⁱ   André, Sabine ^c   Kübler, Dieter ^j   Jiménez Barbero, Jesús ^k,l   Oscarson, Stefan ^g   Gabius, Hans Joachim ^c   Mayo, Kevin H ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF MUNICH   (Germany)

^d NORTHEAST NORMAL UNIVERSITY   (China)

^e CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^f INTERNATIONAL CHRISTIAN UNIVERSITY   (Japan)

^g UNIVERSITY COLLEGE DUBLIN   (Ireland)

^h Glycobiology Section ^*  (Sweden)

ⁱ UNIVERSITY OF HEIDELBERG   (Germany)

^j GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^k CIC BIOGUNE   (Spain)

^l BASQUE FOUNDATION FOR SCIENCE   (Spain)

more..

Author keywords

adhesion; apoptosis; lectin; phosphorylation; self association

Indexed keywords

BETA GALACTOSIDASE; GALECTIN 3; CARBON; GALECTIN-3, HUMAN; NITROGEN; PEPTIDE; PROTEIN BINDING; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; ALPHA HELIX; BETA SHEET; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENE VECTOR; GENETICS; HUMAN; METABOLISM; MOLECULAR CLONING; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN DOMAIN; SEQUENCE ALIGNMENT; SYNTHESIS;

AMINO ACID SEQUENCE; BINDING SITES; CARBON ISOTOPES; CLONING, MOLECULAR; ESCHERICHIA COLI; GALECTIN 3; GENE EXPRESSION; GENETIC VECTORS; HUMANS; MODELS, MOLECULAR; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84988535559     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cww021     Document Type: Article

References (68)

1. Agrwal N, Sun Q, Wang SY, Wang JL. 1993. Carbohydrate-binding protein 35. I. Properties of the recombinant polypeptide and the individuality of the domains. J Biol Chem. 268:14932-14939.
2. Ahmad N, Gabius H-J, André S, Kaltner H, Sabesan S, Roy R, Liu B, Macaluso F, Brewer CF. 2004. Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J Biol Chem. 279:10841-10847.
3. Ahmad N, Gabius H-J, Kaltner H, André S, Kuwabara I, Liu F-T, Oscarson S, Norberg T, Brewer CF. 2002. Thermodynamic binding studies of cell surface carbohyrate epitopes to galectins-1, -3, and -7: Evidence for differential binding specificities. Can J Chem. 80:1096-1104.
4. Barboni EA, Bawumia S, Henrick K, Hughes RC. 2000. Molecular modeling and mutagenesis studies of the N-terminal domains of galectin-3: Evidence for participation with the C-terminal carbohydrate recognition domain in oligosaccharide binding. Glycobiology. 10:1201-1208.
5. Berbís MA, André S, Cañada FJ, Pipkorn R, Ippel H, Mayo KH, Kübler D, Gabius H-J, Jiménez-Barbero J. 2014. Peptides derived from human galectin-3 N-terminal tail interact with its carbohydrate recognition domain in a phosphorylation-dependent manner. Biochem Biophys Res Commun. 443:126-131.
6. Birdsall B, Feeney J, Burdett ID, Bawumia S, Barboni EA, Hughes RC. 2001. NMR solution studies of hamster galectin-3 and electron microscopic visualization of surface-adsorbed complexes: Evidence for interactions between the N-and C-terminal domains. Biochemistry. 40:4859-4866.
7. Cooper DNW. 2002. Galectinomics: Finding themes in complexity. Biochim Biophys Acta. 1572:209-231.
8. Corfield AP, Berry M. 2015. Glycan variation and evolution in the eukaryotes. Trends Biochem Sci. 40:351-359.
9. Dawson H, André S, Karamitopoulou E, Zlobec I, Gabius H-J. 2013. The growing galectin network in colon cancer and clinical relevance of cytoplasmic galectin-3 reactivity. Anticancer Res. 33:3053-3059.
10. Diehl C, Engstrom O, Delaine T, Hakansson M, Genheden S, Modig K, Leffler H, Ryde U, Nilsson UJ, 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.
11. Diercks T, Ribeiro JP, Canada FJ, André S, Jiménez-Barbero J, Gabius H-J. 2009. Fluorinated carbohydrates as lectin ligands: Versatile sensors in 19F-detected saturation transfer difference NMR spectroscopy. Chem Eur J. 15:5666-5668.
12. Flores-Ibarra A, Ruiz FM, Vértesy S, André S, Gabius H-J, Romero A. 2015. Preliminary X-ray crystallographic analysis of an engineered variant of human chimera-type galectin-3 with a shortened N-terminal domain. Acta Crystallogr F. 71:184-188.
13. Funasaka T, Raz A, Nangia-Makker P. 2014. Nuclear transport of galectin-3 and its therapeutic implications. Semin Cancer Biol. 27:30-38.
14. Gabius H-J. 2015. The magic of the sugar code. Trends Biochem Sci. 40:341.
15. 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.
16. Gabius H-J, Kaltner H, Kopitz J, André S. 2015. The glycobiology of the CD system: A dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem Sci. 40:360-376.
17. Goddard TD, Kneller DG. 1995. Sparky 3. San Francisco: University of California.
18. Gohler A, André S, Kaltner H, Sauer M, Gabius H-J, Doose S. 2010. Hydrodynamic properties of human adhesion/growth-regulatory galectins studied by fluorescence correlation spectroscopy. Biophys J. 98:3044-3053.
19. Halimi H, Rigato A, Byrne D, Ferracci G, Sebban-Kreuzer C, ElAntak L, Guerlesquin F. 2014. Glycan dependence of galectin-3 self-association properties. PLoS ONE. 9:e111836.
20. Haudek KC, Spronk KJ, Voss PG, Patterson RJ,Wang JL, Arnoys EJ. 2010. Dynamics of galectin-3 in the nucleus and cytoplasm. Biochim Biophys Acta. 1800:181-189.
21. Hennet T, Cabalzar J. 2015. Congenital disorders of glycosylation: A concise chart of glycocalyx dysfunction. Trends Biochem Sci. 40: 377-384.
22. 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.
23. Houzelstein D, Gonalves IR, Fadden AJ, Sidhu SS, Cooper DNW, Drickamer K, Leffler H, Poirier F. 2004. Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol. 21:1177-1187.
24. Hrynchyshyn N, Jourdain P, Desnos M, Diebold B, Funck F. 2013. Galectin-3: A new biomarker for the diagnosis, analysis and prognosis of acute and chronic heart failure. Arch Cardiovasc Dis. 106:541-546.
25. Hsu DK, Zuberi RI, Liu F-T. 1992. Biochemical and biophysical characterization of human recombinant IgE-binding protein, an S-type animal lectin. J Biol Chem. 267:14167-14174.
26. Huflejt ME, Turck CW, Lindstedt R, Barondes SH, Leffler H. 1993. L-29, a soluble lactose-binding lectin, is phosphorylated on serine 6 and serine 12 in vivo and by casein kinase I. J Biol Chem. 268:26712-26718.
27. Hughes RC. 1994. Mac-2: A versatile galactose-binding protein of mammalian tissues. Glycobiology. 4:5-12.
28. Hughes RC. 1999. Secretion of the galectin family of mammalian carbohydratebinding proteins. Biochim Biophys Acta. 1473:172-185.
29. Ippel H, Miller MC, Berbís MA, Suylen D, André S, Hackeng TM, Canada FJ, Weber C, Gabius H-J, Jiménez-Barbero J, et al. 2015. 1H, 13C, and 15N backbone and side-chain chemical shift assignments for the 36 prolinecontaining, full length 29 kDa human chimera-type galectin-3. Biomol NMR Assign. 9:59-63.
30. Kaltner H, GabiusH-J. 2012. A toolbox of lectins for translating the sugar code: The galectin network in phylogenesis and tumors. Histol Histopathol. 27:397-416.
31. Kaltner H, Kübler D, Lopez-Merino L, Lohr M, Manning JC, Lensch M, Seidler J, Lehmann WD, André S, Solís D, et al. 2011. Toward comprehensive analysis of the galectin network in chicken: Unique diversity of galectin-3 and comparison of its localization profile in organs of adult animals to the other four members of this lectin family. Anat Rec. 294:427-444.
32. Knibbs RN, Agrwal N, Wang JL, Goldstein IJ. 1993. Carbohydrate-binding protein 35. II. Analysis of the interaction of the recombinant polypeptide with saccharides. J Biol Chem. 268:14940-14947.
33. Kopitz J, André S, von Reitzenstein C, Versluis K, Kaltner H, Pieters RJ, Wasano K, Kuwabara I, Liu F-T, Cantz M, et al. 2003. Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells. Oncogene. 22:6277-6288.
34. Kopitz J, Vértesy S, André S, Fiedler S, Schnolzer M, Gabius H-J. 2014. Human chimera-type galectin-3: Defining the critical tail length for high-affinity glycoprotein/cell surface binding and functional competition with galectin-1 in neuroblastoma cell growth regulation. Biochimie. 104:90-99.
35. Kübler D, Hung C-W, Dam TK. 2008. Phosphorylated human galectin-3: Facile large-scale preparation of active lectin and detection of structural changes by CD spectroscopy. Biochim Biophys Acta. 1780:716-722.
36. Laine RA. 1997. The information-storing potential of the sugar code. In: Gabius H-J, Gabius S, editors. Glycosciences: Status and Perspectives. London-Weinheim: Chapman & Hall. p. 1-14.
37. Ledeen RW, Wu G. 2015. The multi-tasked life of GM1 ganglioside, a true factotum of life. Trends Biochem Sci. 40:407-418.
38. Leffler H, Barondes SH. 1986. Specificity of binding of three soluble rat lung lectins to substituted and unsubstituted mammalian beta-galactosides. J Biol Chem. 261:10119-10126.
39. Leffler H, Carlsson S, Hedlund M, Qian Y, Poirier F. 2004. Introduction to galectins. Glycoconj J. 19:433-440.
40. Lepur A, Carlsson MC, Novak R, Dumic J, Nilsson UJ, Leffler H. 2012. Galectin-3 endocytosis by carbohydrate independent and dependent pathways in different macrophage like cell types. Biochim Biophys Acta. 1820:804-818.
41. Li S, Yu Y, Koehn CD, Zhang Z, Su K. 2013. Galectins in the pathogenesis of rheumatoid arthritis. J Clin Cell Immunol. 4:164.
42. Liu YH, DAmbrosio M, Liao Td, Peng H, Rhaleb NE, Sharma UC, André S, Gabius H-J, Carrataro OA. 2009. N-Acetyl-seryl-aspartyl-lysyl-proline prevents cardiac remodeling and dysfunction induced by galectin-3, a mammalian adhesion/growth-regulatory lectin. Am J Physiol Heart Circ Physiol. 296:H404-H412.
43. Lobsanov YD, Rini JM. 1997. Galectin structure. Trends Glycosci Glycotechnol. 9:145-154.
44. Matei E, André S, Glinschert A, Infantino AS, Oscarson S, Gabius H-J, Gronenborn AM. 2013. Fluorinated carbohydrates as lectin ligands: Dissecting glycan-cyanovirin interactions by using 19F-NMR spectroscopy. Chem Eur J. 19:5364-5374.
45. Mehul B, Bawumia S, Martin SR, Hughes RC. 1994. Structure of baby hamster kidney carbohydrate-binding protein CBP30, an S-type animal lectin. J Biol Chem. 269:18250-18258.
46. Mey A, Leffler H, Hmama Z, Normier G, Revillard JP. 1996. The animal lectin galectin-3 interacts with bacterial lipopolysaccharides via two independent sites. J Immunol. 156:1572-1577.
47. Miller MC, Ippel H, Suylen D, Klyosov AA, Traber PG, Hackeng T, Mayo KH. 2016. Binding of polysaccharides to human galectin-3 at a non-canonical site in its carbohydrate recognition domain. Glycobiology. 26:88-99.
48. Miller MC, Klyosov A, Mayo KH. 2009. The a-galactomannan Davanat binds galectin-1 at a site different from the conventional galectin carbohydrate binding site. Glycobiology. 19:1034-1045.
49. Miller MC, Klyosov A, Mayo KH. 2012. Structural features for a-galactomannan binding to galectin-1. Glycobiology. 22:543-551.
50. Morris S, Ahmad N, André S, Kaltner H, Gabius H-J, Brenowitz M, Brewer CF. 2004. Quaternary solution structures of galectins-1, -3 and -7. Glycobiology. 14:293-300.
51. Ochieng J, Platt D, Tait L, Hogan V, Raz T, Carmi P, Raz A. 1993. Structurefunction relationship of recombinant human galactoside-binding protein. Biochemistry. 32:4455-4460.
52. Sanchez-Ruderisch H, Fischer C, Detjen KM, Welzel M, Wimmel A, Manning JC, André S, Gabius H-J. 2010. Tumor suppressor p16INK4a: Downregulation of galectin-3, an endogenous competitor of the pro-anoikis effector galectin-1, in a pancreatic carcinoma model. FEBS J. 277:3552-3563.
53. Saraboji K, Hakansson M, Genheden S, Diehl C, Qvist J, Weininger U, Nilsson UJ, Leffler H, Ryde U, Akke M, et al. 2012. The carbohydratebinding site in galectin-3 is preorganized to recognize a sugar-like framework of oxygens: Ultra-high-resolution structures and water dynamics. Biochemistry. 51:296-306.
54. Sato S, Hughes RC. 1992. Binding specificity of a baby hamster kindey lectin for H type I and II chains, polylactosamine glycans, and appropriately glycosylated forms of laminin and fibronectin. J Biol Chem. 267:6983-6990.
55. Schengrund C-L. 2015. Gangliosides: Glycosphingolipids essential for normal neural development and function. Trends Biochem Sci. 40:397-406.
56. Schnolzer M, Alewood P, Jones A, Alewood D, Kent SBH. 1992. In situ neutralization in Boc-chemistry solid phase peptide synthesis. Rapid, highyield assembly of difficulty sequences. Int J Pept Protein Res. 40:180-193.
57. Seetharaman J, Kanigsberg A, Slaaby R, Leffler H, Barondes SH, Rini JM. 1998. X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1- resolution. J Biol Chem. 273:13047-13052.
58. Selenko P, Frueh DP, Elsaesser SJ, Haas W, Gygi SP, Wagner G. 2008. In situ observation of protein phosphorylation by high-resolution NMR spectroscopy. Nat Struct Mol Biol. 15:321-329.
59. Solís D, Bovin NV, Davis AP, Jiménez-Barbero J, Romero A, Roy R, Smetana Jr K, Gabius H-J. 2015. A guide into glycosciences: How chemistry, biochemistry and biology cooperate to crack the sugar code. Biochim Biophys Acta. 1850:186-235.
60. Spiro RG. 2002. Protein glycosylation: Nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology. 12:43R-56R.
61. Takenaka Y, Fukumori T, Yoshii T, Oka N, Inohara H, Kim H-RC, Bresalier RS, Raz A. 2004. Nuclear export of phosphorylated galectin-3 regulates its antiapoptotic activity in response to chemotherapeutic drugs. Mol Cell Biol. 24:4395-4406.
62. Toegel S, Bieder D, André S, Kayser K, Walzer SM, Hobusch G, Windhager R, Gabius H-J. 2014. Human osteoarthritic knee cartilage: Fingerprinting of adhesion/growth-regulatory galectins in vitro and in situ indicates differential upregulation in severe degeneration. Histochem Cell Biol. 142:373-388.
63. Tsay YG, Lin NY, Voss PG, Patterson RJ,Wang JL. 1999. Export of galectin-3 from nuclei of digitonin-permeabilized mouse 3T3 fibroblasts. Exp Cell Res. 252:250-261.
64. Umemoto K, Leffler H. 2001. Assignment of 1H, 15N and 13C resonances of the carbohydrate recognition domain of human galectin-3. J Biomol NMR. 20:91-92.
65. Umemoto K, Leffler H, Venot A, Valafar H, Prestegard JH. 2003. Conformational differences in liganded and unliganded states of galectin-3. Biochemistry. 42:3688-3695.
66. Woo H-J, Shaw LM, Messier JM, Mercurio AM. 1990. The major non-integrin laminin-binding protein of macrophages is identical to carbohydratebinding protein 35 (Mac-2). J Biol Chem. 265:7097-7099.
67. Yang R-Y, Hill PN, Hsu DK, Liu F-T. 1998. Role of the carboxyl-terminal lectin domain in self-association of galectin-3. Biochemistry. 37: 4086-4092.
68. Zuber C, Roth J. 2009. N-Glycosylation. In: Gabius H-J, editor. The Sugar Code. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH. p. 87-110.