Terminal sialic acids on CD44 N-glycans can block hyaluronan binding by forming competing intramolecular contacts with arginine sidechains

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 11, 2014, Pages 3079-3089

  Faller, Christina E ^a   Guvench, Olgun ^a  

^a UNIVERSITY OF NEW ENGLAND   (United States)

Author keywords

Carbohydrate; Charge pairing; Extracellular matrix; Glycosylation; Hydrogen bond; Molecular dynamics

Indexed keywords

ARGININE; GLYCAN DERIVATIVE; GLYCOPROTEIN; HERMES ANTIGEN; HYALURONIC ACID; SIALIC ACID DERIVATIVE; ASPARAGINE; CD44 PROTEIN, HUMAN; POLYSACCHARIDE;

ARTICLE; HYDROGEN BOND; MOLECULAR DYNAMICS; PRIORITY JOURNAL; SIALYLATION; BINDING SITE; CARBOHYDRATE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; GLYCOSYLATION; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION;

ANTIGENS, CD44; ARGININE; ASPARAGINE; BINDING SITES; CARBOHYDRATE SEQUENCE; GLYCOSYLATION; HUMANS; HYALURONIC ACID; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN CONFORMATION; SIALIC ACIDS;

EID: 84929196554     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24668     Document Type: Article

References (80)

1. Marth JD, Grewal PK. Mammalian glycosylation in immunity. Nat Rev Immunol 2008;8(11):874-887.
2. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME. Essentials of glycobiology. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1999.
3. Schauer R. Sialic acids as regulators of molecular and cellular interactions. Curr Opin Struct Biol 2009;19(5):507-514.
4. Dennis JW, Lau KS, Demetriou M, Nabi IR. Adaptive regulation at the cell surface by N-glycosylation. Traffic 2009;10(11):1569-1578.
5. Miyagi T, Yamaguchi K. Sialic acids. In: Kamerling J, Boona G, Lee Y, Suzuki A, Taniguchi N, Voragen A, editors. Biochemistry of glycans: sialic acids in comprehensive glycoscience. Amsterdam: Elsevier BV; 2007. pp 297-322.
6. Monti E, Preti A, Venerando B, Borsani G. Recent development in mammalian sialidase molecular biology. Neurochem Res 2002;27(7-8):649-663.
7. Mozzi A, Mazzacuva P, Zampella G, Forcella ME, Fusi PA, Monti E. Molecular insight into substrate recognition by human cytosolic sialidase NEU2. Proteins 2012;80(4):1123-1132.
8. Monti E, Bonten E, D'Azzo A, Bresciani R, Venerando B, Borsani G, Schauer R, Tettamanti G. Sialidases in vertebrates: a family of enzymes tailored for several cell functions. Adv Carbohydr Chem Biochem 2010;64:403-479.
9. Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R. CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 2001;153(6):1277-1286.
10. Inforzato A, Reading PC, Barbati E, Bottazzi B, Garlanda C, Mantovani A. The "sweet" side of a long pentraxin: how glycosylation affects PTX3 functions in innate immunity and inflammation. Front Immunol 2012;3:407.
11. Nightingale TD, Frayne ME, Clasper S, Banerji S, Jackson DG. A mechanism of sialylation functionally silences the hyaluronan receptor LYVE-1 in lymphatic endothelium. J Biol Chem 2009;284(6):3935-3945.
12. Zhuo Y, Chammas R, Bellis SL. Sialylation of beta1 integrins blocks cell adhesion to galectin-3 and protects cells against galectin-3-induced apoptosis. J Biol Chem 2008;283(32):22177-22185.
13. Janik ME, Litynska A, Vereecken P. Cell migration-the role of integrin glycosylation. Biochim Biophys Acta 2010;1800(6):545-555.
14. Pochec E, Litynska A, Bubka M, Amoresano A, Casbarra A. Characterization of the oligosaccharide component of alpha3beta1 integrin from human bladder carcinoma cell line T24 and its role in adhesion and migration. Eur J Cell Biol 2006;85(1):47-57.
15. Nadanaka S, Sato C, Kitajima K, Katagiri K, Irie S, Yamagata T. Occurrence of oligosialic acids on integrin alpha 5 subunit and their involvement in cell adhesion to fibronectin. J Biol Chem 2001;276(36):33657-33664.
16. Margraf-Schonfeld S, Bohm C, Watzl C. Glycosylation affects ligand binding and function of the activating natural killer cell receptor 2B4 (CD244) protein. J Biol Chem 2011;286(27):24142-24149.
17. Woronowicz A, Amith SR, De Vusser K, Laroy W, Contreras R, Basta S, Szewczuk MR. Dependence of neurotrophic factor activation of Trk tyrosine kinase receptors on cellular sialidase. Glycobiology 2007;17(1):10-24.
18. Marhaba R, Zoller M. CD44 in cancer progression: adhesion, migration and growth regulation. J Mol Histol 2004;35(3):211-231.
19. Toole BP. Hyaluronan-CD44 Interactions in Cancer: paradoxes and Possibilities. Clin Cancer Res 2009;15(24):7462-7468.
20. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003;4(1):33.
21. English NM, Lesley, JF, Hyman, R. Site-specific De-N-glycosylation of CD44 Can Acitvate Hyaluronan Binding, and CD44 Activation State Shows Distinct Threshold Densities for Hyaluronan Binding. Cancer Res 1998;58(16):3736-3742.
22. Katoh S, Miyagi T, Taniguchi H, Matsubara Y, Kadota J, Tominaga A, Kincade PW, Matsukura S, Kohno S. Cutting edge: an inducible sialidase regulates the hyaluronic acid binding ability of CD44-bearing human monocytes. J Immunol 1999;162(9):5058-5061.
23. Katoh S, Zheng Z, Oritani K, Shimozato T, Kincade PW. Glycosylation of CD44 negatively regulates its recognition of hyaluronan. J Exp Med 1995;182(2):419-429.
24. Skelton TP, Zeng C, Nocks A, Stamenkovic I. Glycosylation provides both stimulatory and inhibitory effects on cell surface and soluble CD44 binding to hyaluronan. J Cell Biol 1998;140(2):431-446.
25. Screaton GR, Bell MV, Jackson DG, Cornelis FB, Gerth U, Bell JI. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc Natl Acad Sci USA 1992;89(24):12160-12164.
26. Thankamony SP, Knudson W. Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J Biol Chem 2006;281(45):34601-34609.
27. Lee JL, Wang MJ, Sudhir PR, Chen JY. CD44 engagement promotes matrix-derived survival through the CD44-SRC-integrin axis in lipid rafts. Mol Cell Biol 2008;28(18):5710-5723.
28. Uff CR, Neame SJ, Isacke CM. Hyaluronan binding by CD44 is regulated by a phosphorylation-independent mechanism. Eur J Immunol 1995;25(7):1883-1887.
29. Neame SJ, Isacke CM. Phosphorylation of CD44 in vivo requires both Ser323 and Ser325, but does not regulate membrane localization or cytoskeletal interaction in epithelial cells. EMBO J 1992;11(13):4733-4738.
30. Peach RJ, Hollenbaugh D, Stamenkovic I, Aruffo A. Identification of hyaluronic acid binding sites in the extracellular domain of CD44. J Cell Biol 1993;122(1):257-264.
31. Banerji S, Wright AJ, Noble M, Mahoney DJ, Campbell ID, Day AJ, Jackson DG. Structures of the Cd44-hyaluronan complex provide insight into a fundamental carbohydrate-protein interaction. Nat Struct Mol Biol 2007;14(3):234-239.
32. Favreau A, J., Faller CE, Guvench O. CD44 receptor unfolding enhances binding by freeing basic amino acids to contact carbohydrate ligand. Biophys J 2013;105(5):1217-1226.
33. Lesley J, English N, Perschl A, Gregoroff J, Hyman R. Variant cell lines selected for alterations in the function of the hyaluronan receptor CD44 show differences in glycosylation. J Exp Med 1995;182(2):431-437.
34. Lesley J, He Q, Miyake K, Hamann A, Hyman R, Kincade PW. Requirements for hyaluronic acid binding by CD44: a role for the cytoplasmic domain and activation by antibody. J Exp Med 1992;175(1):257-266.
35. Lesley J, Hyman R. CD44 can be activated to function as an hyaluronic acid receptor in normal murine T cells. Eur J Immunol 1992;22(10):2719-2723.
36. Gee K, Kozlowski M, Kumar A. Tumor necrosis factor-alpha induces functionally active hyaluronan-adhesive CD44 by activating sialidase through p38 mitogen-activated protein kinase in lipopolysaccharide-stimulated human monocytic cells. J Biol Chem 2003;278(39):37275-37287.
37. Kincade PW, Zheng Z, Katoh S, Hanson L. The importance of cellular environment to function of the CD44 matrix receptor. Curr Opin Cell Biol 1997;9(5):635-642.
38. Katoh S, Maeda S, Fukuoka H, Wada T, Moriya S, Mori A, Yamaguchi K, Senda S, Miyagi T. A crucial role of sialidase Neu1 in hyaluronan receptor function of CD44 in T helper type 2-mediated airway inflammation of murine acute asthmatic model. Clin Exp Immunol 2010;161(2):233-241.
39. Woods R. Computational carbohydrate chemistry: what theoretical methods can tell us. Glycoconj J 1998;15(3):209-216.
40. Jo S, Lee HS, Skolnick J, Im W. Restricted N-glycan Conformational Space in the PDB and Its Implication in Glycan Structure Modeling. PLoS Comput Biol 2013;9(3):e1002946.
41. Takeda M, Ogino S, Umemoto R, Sakakura M, Kajiwara M, Sugahara KN, Hayasaka H, Miyasaka M, Terasawa H, Shimada I. Ligand-induced structural changes of the CD44 hyaluronan-binding domain revealed by NMR. J Biol Chem 2006;281(52):40089-40095.
42. Teriete P, Banerji S, Noble M, Blundell CD, Wright AJ, Pickford AR, Lowe E, Mahoney DJ, Tammi MI, Kahmann JD, Campbell ID, Day AJ, Jackson DG. Structure of the regulatory hyaluronan binding domain in the inflammatory leukocyte homing receptor CD44. Mol Cell 2004;13(4):483-496.
43. Bohne-Lang A, von der Lieth CW. GlyProt: in silico glycosylation of proteins. Nucleic Acids Res 2005;33(Web Server issue):W214-W219.
44. Jo S, Kim T, Iyer VG, Im W. CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem 2008;29(11):1859-1865.
45. Jo S, Song KC, Desaire H, MacKerell AD, Jr., Im W. Glycan reader: automated sugar identification and simulation preparation for carbohydrates and glycoproteins. J Comput Chem 2011;32(14):3135-3141.
46. Jo S, Im W. Glycan fragment database: a database of PDB-based glycan 3D structures. Nucleic Acids Res 2013;41(Database issue):D470-D474.
47. Group W. 2005-2014 GLYCAM Web. Complex Carbohydrate Research Center, University of Georgia, Athens, GA. http://www.glycam.org.
48. Bajorath J, Greenfield B, Munro SB, Day AJ, Aruffo A. Identification of CD44 residues important for hyaluronan binding and delineation of the binding site. J Biol Chem 1998;273(1):338-343.
49. Bartolazzi A, Nocks A, Aruffo A, Spring F, Stamenkovic I. Glycosylation of CD44 is implicated in CD44-mediated cell adhesion to hyaluronan. J Cell Biol 1996;132(6):1199-1208.
50. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983;79(2):926-935.
51. Durell SR, Brooks BR, Ben-Naim A. Solvent-induced forces between two hydrophilic groups. J Phys Chem 1994;98(8):2198-2202.
52. Brooks BR, Brooks CL, 3rd, Mackerell AD, Jr., Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S and others. CHARMM: the biomolecular simulation program. J Comput Chem 2009;30(10):1545-1614.
53. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 1983;4(2):187-217.
54. MacKerell AD, Jr, Bashford D, Bellorr M, Dunbrack RL, Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiórkiewicz-Kuczera J, Yin D, Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102(18):3586-3616.
55. Best RB, Zhu X, Shim J, Lopes PE, Mittal J, Feig M, Mackerell AD, Jr. Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone phi, psi and side-chain chi(1) and chi(2) dihedral angles. J Chem Theory Comput 2012;8(9):3257-3273.
56. MacKerell AD, Jr., Feig M, Brooks CL, 3rd. Improved treatment of the protein backbone in empirical force fields. J Am Chem Soc 2004;126(3):698-699.
57. Guvench O, Greene SN, Kamath G, Brady JW, Venable RM, Pastor RW, Mackerell AD, Jr. Additive empirical force field for hexopyranose monosaccharides. J Comput Chem 2008;29(15):2543-2564.
58. Guvench O, Hatcher ER, Venable RM, Pastor RW, Mackerell AD, Jr. CHARMM additive all-atom force field for glycosidic linkages between hexopyranoses. J Chem Theory Comput 2009;5(9):2353-2370.
59. Guvench O, Mallajosyula SS, Raman EP, Hatcher E, Vanommeslaeghe K, Foster TJ, Jamison FW, Jr., Mackerell AD, Jr. CHARMM additive all-atom force field for carbohydrate derivatives and its utility in polysaccharide and carbohydrate-protein modeling. J Chem Theory Comput 2011;7(10):3162-3180.
60. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kalé L, Schulten K. Scalable molecular dynamics with NAMD. J Comput Chem 2005;26(16):1781-1802.
61. Ryckaert JP, Ciccotti G, Brenderson HJC. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977;23(3):327-341.
62. Miyamoto S, Kollman PA. Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 1992;13(8):952-962.
63. Kubo R, Toda M, Hashitsume N. Statistical physics II: nonequilibrium statistical mechanics. New York: Springer; 1991.
64. Feller SE, Zhang Y, Pastor RW, Brooks BR. Constant pressure molecular dynamics simulation: the Langevin piston method. J Chem Phys 1995;103(11):4613-4621.
65. Brünger A, Brooks CL, 3rd, Karplus M. Stochastic boundary conditions for molecular dynamics simulations of ST2 water. Chem Phys Lett 1984;105(5):495-500.
66. Steinbach PJ, Brooks BR. New spherical-cutoff methods for long-range forces in macromolecular simulation. J Comput Chem 1994;15(7):667-683.
67. Darden T, York D, Pedersen L. Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J Chem Phys 1993;98:10089-10092.
68. Lee B, Richards FM. The interpretation of protein structures: estimation of static accessibility. J Mol Biol 1971;55(3):379-400.
69. Favreau AJ, Faller CE, Guvench O. CD44 receptor unfolding enhances binding by freeing basic amino acids to contact carbohydrate ligand. Biophys J 2013;105(5):1217-1226.
70. Hénin J, Fiorin G, Chipot C, Klein ML. Exploring multidimensional free energy landscapes using time-dependent biases on collective variables. J Chem Theory Comput 2010;6(1):35-47.
71. Darve E, Rodriguez-Gomez D, Pohorille A. Adaptive biasing force method for scalar and vector free energy calculations. J Chem Phys 2008;128(14):144120.
72. Ogino S, Nishida N, Umemoto R, Suzuki M, Takeda M, Terasawa H, Kitayama J, Matsumoto M, Hayasaka H, Miyasaka M and others. Two-state conformations in the hyaluronan-binding domain regulate CD44 adhesiveness under flow condition. Structure (Cambridge, MA, US) 2010;18(5):649-656.
73. Jamison FW, 2nd, Foster TJ, Barker JA, Hills RD, Jr., Guvench O. Mechanism of binding site conformational switching in the CD44-hyaluronan protein-carbohydrate binding interaction. J Mol Biol 2011;406(4):631-647.
74. Jackson DG, Bell JI, Dickinson R, Timans J, Shields J, Whittle N. Proteoglycan forms of the lymphocyte homing receptor CD44 are alternatively spliced variants containing the v3 exon. J Cell Biol 1995;128(4):673-685.
75. Mikami T, Kitagawa H. Biosynthesis and function of chondroitin sulfate. Biochim Biophys Acta 2013;1830(10):4719-4733.
76. Farber SJ, Schubert M, Schuster N. The binding of cations by chondroitin sulfate. J Clin Invest 1957;36(12):1715-1722.
77. Horkay F, Basser PJ, Hecht AM, Geissler E. Chondroitin sulfate in solution: effects of mono- and divalent salts. Macromolecules 2012;45(6):2882-2890.
78. Hunter GK. Chondroitin sulfate-derivatized agarose beads: a new system for studying cation binding to glycosaminoglycans. Anal Biochem 1987;165(2):435-441.
79. Hunter GK, Wong KS, Kim JJ. Binding of calcium to glycosaminoglycans: an equilibrium dialysis study. Arch Biochem Biophys 1988;260(1):161-167.
80. Uchisawa H, Okuzaki B-i, Ichita J, Matsue H. Binding between calcium ions and chondroitin sulfate chains of salmon nasal cartilage glycosaminoglycan. Int Cong Series 2001;1223(0):205-220.