In silico analysis of antibody-carbohydrate interactions and its application to xenoreactive antibodies

Molecular Immunology

Volumn 47, Issue 2-3, 2009, Pages 233-246

  Agostino, Mark ^a   Sandrin, Mauro S ^b   Thompson, Philip E ^a   Yuriev, Elizabeth ^a   Ramsland, Paul A ^b,c,d  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c BURNET INSTITUTE   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

Gal epitope; Carbohydrate antibody interactions; Molecular modelling; Organ rejection; Xenotransplantation

Indexed keywords

ALPHA GALACTOSIDASE; ANTIBODY; CARBOHYDRATE; CARBOHYDRATE ANTIGEN; HYDROGEN; MONOCLONAL ANTIBODY;

ANTIGEN ANTIBODY REACTION; ANTIGEN RECOGNITION; ARTICLE; BLOOD GROUP ABO INCOMPATIBILITY; COMPUTER MODEL; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOLYSIS; ERYTHROCYTE MEMBRANE; GRAFT REJECTION; HYDROGEN BOND; IMMUNE RESPONSE; MOLECULAR DOCKING; MOLECULAR RECOGNITION; PRIORITY JOURNAL; REPRODUCIBILITY; SPECIES DIFFERENCE; SWINE; XENOTRANSPLANTATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, HETEROPHILE; ANTIBODIES, MONOCLONAL; BINDING SITES, ANTIBODY; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CARBOHYDRATES; COMPLEMENTARITY DETERMINING REGIONS; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; GALACTOSE; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; REPRODUCIBILITY OF RESULTS; SEQUENCE ALIGNMENT; SUS SCROFA;

SUIDAE;

EID: 70450242830     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.09.031     Document Type: Article

References (80)

1. Almond A., Petersen B.O., and Duus J.Ø. Oligosaccharides implicated in recognition are predicted to have relatively ordered structures. Biochemistry 43 (2004) 5853-5863
2. Ban N., Escobar C., Hasel K.W., Day J., Greenwood A., and McPherson A. Structure of an anti-idiotypic Fab against feline peritonitis virus-neutralizing antibody and a comparison with the complexed Fab. FASEB J. 9 (1995) 107-114
3. Blanchard B., Nurisso A., Hollville E., Tétaud C., Wiels J., Pokorná M., Wimmerova M., Varrot A., and Imberty A. Structural basis of the preferential binding for globo-series glycosphingolipids displayed by Pseudomonas aeruginosa lectin I. J. Mol. Biol. 383 (2008) 837-853
4. Brandl U., Michel S., Erhardt M., Brenner P., Burdorf L., Jöckle H., Bittman I., Rössle M., Mordstein V., Baschnegger H., Bauer A., Hammer C., Reichart B., and Schmoeckel M. Transgenic animals in experimental xenotransplantation models: orthotopic heart transplantation in the pig-to-baboon model. Transplant. Proc. 39 (2007) 577-578
5. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., Read R.J., Rice L.M., Simonson T., and Warren G.L. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54 (1998) 905-921
6. Bundle D.R., Baumann H., Brisson J.-R., Gagne S.M., Zdanov A., and Cygler M. The solution structure of a trisaccharide-antibody complex: comparison of NMR measurements with a crystal structure. Biochemistry 33 (1994) 5183-5192
7. Calarese D.A., Scanlan C.N., Zwick M.B., Deechongkit S., Mimura Y., Kunert R., Zhu P., Wormald M.R., Stanfield R.L., Roux K.H., Kelly J.W., Rudd P.M., Dwek R.A., Katinger H., Burton D.R., and Wilson I.A. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300 (2003) 2065-2071
8. Calarese D.A., Lee H.-K., Huang C.-Y., Best M.D., Astronomo R.D., Stanfield R.L., Katinger H., Burton D.R., Wong C.-H., and Wilson I.A. Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 13372-13377
9. Cho K.-I., Kim D., and Lee D. A feature-based approach to modeling protein-protein interaction hot spots. Nucleic Acids Res. 37 (2009) 2672-2687
10. Christiansen D., Milland J., Mouhtouris E., Vaughan H., Pellicci D.G., McConville M.J., Godfrey D.I., and Sandrin M.S. Humans lack iGb3 due to the absence of functional iGb3-synthase: implications for NKT cell development and transplantation. PLoS Biol. 6 (2008) 1527-1538
11. Chuang S., Velkov T., Horne J., Porter C.J.H., and Scanlon M.J. Characterization of the drug binding specificity of rat liver fatty acid binding protein. J. Med. Chem. 51 (2008) 3755-3764
12. Cooper D.K.C., Good A.H., Koren E., Oriol R., Malcolm A.J., Ippolito R.M., Neethling F.A., Ye Y., Romano E., and Zuhdi N. Identification of α-galactosyl and other carbohydrate epitopes that are bound by human anti-pig antibodies: relevance to discordant xenografting in man. Transpl. Immunol. 1 (1993) 198-205
13. Corzana F., Bettler E., Hervé du Penhoat C., Tyrtysh T.V., Bovin N.V., and Imberty A. Solution structure of two xenoantigens: αGal-LacNAc and αGal-Lewis X. Glycobiology 12 (2002) 241-250
14. Cygler M., Rose D.R., and Bundle D.R. Recognition of a cell-surface oligosaccharide of pathogenic Salmonella by an antibody Fab fragment. Science 253 (1991) 442-445
15. Cygler M., Wu S., Zdanov A., Bundle D.R., and Rose D.R. Recognition of a carbohydrate antigenic determinant of Salmonella by an antibody. Biochem. Soc. Trans. 21 (1993) 437-441
16. Cygler M. Recognition of carbohydrates by antibodies. Res. Immunol. 145 (1994) 36-40
17. Davis A.M., St-Gallay S.A., and Kleywegt G.J. Limitations and lessons in the use of X-ray structural information in drug design. Drug Discov. Today 13 (2008) 831-841
18. DeMarco M.L., and Woods R.J. Structural glycobiology: a game of snakes and ladders. Glycobiology 18 (2008) 426-440
19. Friesner R.A., Banks J.L., Murphy R.B., Halgren T.A., Klicic J.J., Mainz D.T., Repasky M.P., Knoll E.H., Shelley M., Perry J.K., Shaw D.E., Francis P., and Shenkin P.S. Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem. 47 (2004) 1739-1749
20. Galili U. Interaction of the natural anti-Gal antibody with alpha-galactosyl epitopes: a major obstacle for xenotransplantation in humans. Immunol. Today 14 (1994) 480-482
21. Goodford P.J. A computational procedure for determining energetically favourable binding sites on biologically important macromolecules. J. Med. Chem. 28 (1985) 849-857
22. Goodford P. The basic principles of GRID. In: Cruciani G. (Ed). Molecular Interaction Fields (2006), Wiley-VCH, Weinheim
23. Grahn E., Askarieh G., Holmner A., Tateno H., Winter H.C., Goldstein I.J., and Krengel U. Crystal structure of the Marasmius oreades mushroom lectin in complex with a xenotransplantation epitope. J. Mol. Biol. 369 (2007) 710-721
24. Greco A., Ho J.G.S., Lin S.-J., Palcic M.M., Rupnik M., and Ng K.K.-S. Carbohydrate recognition by Clostridium difficile toxin A. Nat. Struct. Mol. Biol. 13 (2006) 460-461
25. Halgren T. New method for fast and accurate binding-site identification and analysis. Chem. Biol. Drug Des. 69 (2007) 146-148
26. Hubbard S.J., and Thornton J.M. NACCESS (1993), Department of Biochemistry and Molecular Biology, University College, London
27. Imberty A., Mikros E., Koca J., Mollicone R., Oriol R., and Pérez S. Computer simulation of histo-blood group oligosaccharides: energy maps of all constituting disaccharides and potential energy surfaces of 14 ABH and Lewis carbohydrate antigens. Glycoconj. J. 12 (1995) 331-349
28. Jeffrey P.D., Bajorath J., Chang C.Y., Yelton D., Hellström I., Hellström K.E., and Sheriff S. The X-ray structure of an anti-tumor antibody in complex with antigen. Nat. Struct. Biol. 2 (1995) 466-471
29. Jiménez-Barbero J., Díaz M.D., and Nieto P.M. NMR structural studies of oligosaccharides related to cancer processes. Anti-Cancer Agent. Med. Chem. 8 (2008) 52-63
30. Kabat E.A., Wu T.T., Perry H.M., Gottesman K.S., and Foeller C. Sequences of Proteins of Immunological Interest (1991), National Institute of Health, Washington, DC
31. Kearns-Jonker M., Barteneva N., Mencel R., Hussain N., Shulkin I., Xu A., Yew M., and Cramer D.V. Use of molecular modelling and site-directed mutagenesis to define the structural basis for the immune response to carbohydrate xenoantigens. BMC Immunol. 8 (2007) 3
32. Kelly M.D., and Mancera R.L. Expanded interaction fingerprint method for analyzing ligand binding modes in docking and structure-based drug design. J. Chem. Inf. Comput. Sci. 44 (2004) 1942-1951
33. Kiernan K., Harnden I., Gunthart M., Gregory C., Meisner J., and Kearns-Jonker M. The anti-non-Gal xenoantibody response to xenoantigens on Gal knockout pig cells is encoded by a restricted number of germline progenitors. Am. J. Transplant. 8 (2008) 1829-1839
34. Kjer-Nielsen L., Dunstone M.A., Kostenko L., Ely L.K., Beddoe T., Mifsud N.A., Purcell A.W., Brooks A.G., McCluskey J., and Rossjohn J. Crystal structure of the human T cell receptor CD3εγ heterodimer complexed to the therapeutic mAb OKT3. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 7675-7680
35. Kortemme T., and Baker D. A simple physical model for binding energy hot spots in protein-protein complexes. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 14116-14121
36. Kortemme T., Kim D.E., and Baker D. Computational alanine scanning of protein-protein interfaces. Sci. STKE (2004) l2
37. Kroemer R.T., Vulpetti A., McDonald J.J., Rohrer D.C., Trosset J.-Y., Giordanetto F., Cotesta S., McMartin C., Kihlén M., and Stouten P.F.W. Assessment of docking poses: interaction-based accuracy classification (IBAC) versus crystal structure deviations. J. Chem. Inf. Comput. Sci. 44 (2004) 871-881
38. Lafont V., Schaefer M., Stote R.H., Altschuh D., and Dejaegere A. Protein-protein recognition and interaction hot spots in an antigen-antibody complex: free energy decomposition identifies "efficient amino acids". Proteins 67 (2007) 418-434
39. Lee M., Lloyd P., Zhang X., Schallhorn J.M., Sugimoto K., Leach A.G., Sapiro G., and Houk K.N. Shapes of antibody binding sites: qualitative and quantitative analyses based on a geomorphic classification scheme. J. Org. Chem. 71 (2006) 5082-5092
40. Lefranc M.-P., Pommié C., Manuel R., Giudicelli V., Foulquier E., Truong L., Thouvenin-Contet V., and Lefranc G. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev. Comp. Immunol. 27 (2003) 55-77
41. Li J., Ksebati M.B., Zhang W., Guo Z., Wang J., Yu L., Fang J., and Wang P.G. Conformational analysis of an α-galactosyl trisaccharide epitope involved in hyperacute rejection upon xenotransplantation. Carbohydr. Res. 315 (1999) 76-88
42. Macher B.A., and Galili U. The Galα1,3Galβ1,4GlcNAc-R (α-Gal) epitope: a carbohydrate of unique evolution and clinical relevance. Biochim. Biophys. Acta 1780 (2008) 75-88
43. Manyalich M., Costa A.N., and Paez G. 2008 international donation and transplantation activity. IRODaT preliminary data. Organs Tissues Cells 12 (2009) 5-8
44. Massova I., and Kollman P.A. Computational alanine scanning to probe protein-protein interactions: a novel approach to evaluate binding free energies. J. Am. Chem. Soc. 121 (1999) 8135-8143
45. Milland J., Yuriev E., Xing P.-X., McKenzie I.F.C., Ramsland P.A., and Sandrin M.S. Carbohydrate residues downstream of the terminal Galα(1,3)Gal epitope modulate the specificity of xenoreactive antibodies. Immunol. Cell Biol. 85 (2007) 623-632
46. Mobley D.L., and Dill K.A. Binding of small-molecule ligands to proteins: "what you see" is not always "what you get". Structure 17 (2009) 489-498
47. Morris G.M., Goodsell D.S., Halliday R.S., Huey R., Hart W.E., Belew R.K., and Olson A.J. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 14 (1998) 1639-1662
48. Nair D.T., Singh K., Siddiqui Z., Nayak B.P., Rao K.V.S., and Salunke D.M. Epitope recognition by diverse antibodies suggests conformational convergence in an antibody response. J. Immunol. 168 (2002) 2371-2382
49. Natchiar S.K., Srinivas O., Mitra N., Surolia A., Jayaraman N., and Vijayan M. Structural studies on peanut lectin complexed with disaccharides involving different linkages: further insights into the structure and interactions of the lectin. Acta Crystallogr. D 62 (2006) 1413-1421
50. Nguyen H.P., Seto N.O.L., MacKenzie C.R., Brade L., Kosma P., Brade H., and Evans S.V. Germline antibody recognition of distinct carbohydrate epitopes. Nat. Struct. Biol. 10 (2003) 1019-1025
51. Nissink J.W.M., and Taylor R. Combined use of physicochemical data and small-molecule crystallographic contact propensities to predict interactions in protein binding sites. Org. Biomol. Chem. 2 (2004) 3238-3249
52. Nottle M.B., Beebe L.F.S., Harrison S.J., McIlfatrick S.M., Ashman R.J., O'Connell P.J., Salvaris E.J., Fisicaro N., Pommey S., Cowan P.J., and d'Apice A.J.F. Production of homozygous α1,3 galactosyltransferase knockout pigs by breeding and somatic cell nuclear transfer. Xenotransplantation 14 (2007) 339-344
53. Nozawa S., Xing P.-X., Wu G.D., Gochi E., Kearns-Jonker M., Swensson J., Starnes V.A., Sandrin M.S., McKenzie I.F.C., and Cramer D.V. Characteristics of immunoglobulin gene usage of the xenoantibody binding to Gal-[alpha](1,3)Gal target antigens in the Gal knockout mouse. Transplantation 72 (2001) 147-155
54. Pérez-Neuno V.I., Rabal O., Borrell J.I., and Teixidó J. APIF: a new interaction fingerprint based on atom pairs and its application to virtual screening. J. Chem. Inf. Model. 49 (2009) 1245-1260
55. Ramsland P.A., Guddat L.W., Edmundson A.B., and Raison R.L. Diverse binding site structures revealed in homology models of polyreactive immunoglobulins. J. Comp. Aid. Mol. Des. 11 (1997) 453-461
56. Ramsland P.A., Kaushik A., Marchalonis J.J., and Edmundson A.B. Incorporation of long CDR3s into V domains: implications for the structural evolution of the antibody-combining site. Exp. Clin. Immunogenet. 18 (2001) 176-198
57. Ramsland P.A., Farrugia W., Yuriev E., Edmundson A.B., and Sandrin M.S. Evidence for structurally conserved recognition of the major carbohydrate xenoantigen by natural antibodies. Cell. Mol. Biol. 49 (2003) 307-317
58. Ramsland P.A., Farrugia W., Bradford T.M., Hogarth P.M., and Scott A.M. Structural convergence of antibody binding of carbohydrate determinants in Lewis Y tumor antigens. J. Mol. Biol. 340 (2004) 809-818
59. Rarey M., Kramer B., Lengauer T., and Klebe G. A fast flexible docking method using an incremental construction algorithm. J. Mol. Biol. 261 (1996) 470-489
60. Sali A., and Blundell T. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993) 779-815
61. Salisburg A.M., Deline A.L., Lexa K.W., Shields G.C., and Kirschner K.N. Ramachandran-type plots for glycosidic linkages: examples from molecular dynamic simulations using the Glycam06 force field. J. Comput. Chem. 30 (2008) 910-921
62. Sandrin M.S., Vaughan H.A., Dabkowski P.L., and McKenzie I.F. Anti-pig IgM antibodies in serum respond predominantly with Gal(α1-3)Gal epitopes. Proc. Nat. Acad. Sci. U.S.A. 90 (1993) 11391-11395
63. Sandrin M.S., and McKenzie I.F. Galα(1,3)Gal, the major xenoantigen(s) recognised in pigs by human natural antibodies. Immunol. Rev. 141 (1994) 169-190
64. Staelens S., Hadders M.A., Vauterin S., Platteau C., De Maeyer M., Vanhoorelbeke K., Huizinga E.G., and Deckmyn H. Paratope determination of the antithrombotic antibody 82D6A3 based on the crystal structure of its complex with the von Willebrand factor A3-domain. J. Biol. Chem. 281 (2006) 2225-2231
65. Suh S.W., Bhat T.N., Navia M.A., Cohen G.H., Rao D.N., Rudikoff S., and Davies D.R. The galactan-binding immunoglobulin Fab J539. An X-ray diffraction study at 2.6-angstroms resolution. Proteins 1 (1986) 74-80
66. Tempel W., Tschampel S., and Woods R.J. The xenograft antigen bound to Griffonia simplicifolia lectin 1-B(4). X-ray crystal structure of the complex and molecular dynamics characterization of the binding site. J. Biol. Chem. 277 (2002) 6615-6621
67. Terzyan S., Ramsland P.A., Voss Jr. E.W., Herron J.N., and Edmundson A.B. Three-dimensional structures of idiotypically related Fabs with intermediate and high affinity for fluorescein. J. Mol. Biol. 339 (2004) 1141-1151
68. Thøgersen H., Lemieux R.U., Bock K., and Meyer B. Further justification for the exo-anomeric effect: conformational analysis based on nuclear magnetic-resonance spectroscopy of oligosaccharides. Can. J. Chem. 60 (1982) 44-57
69. van Gunsteren W.F., Dolenc J., and Mark A.E. Molecular simulation as an aid to experimentalists. Curr. Opin. Struct. Biol. 18 (2008) 149-153
70. van Roon A.M., Pannu N.S., de Vrind J.P.M., van der Marel G.A., van Boom J.H., Hokke C.H., Deelder A.M., and Abrahams J.P. Structure of an anti-Lewis X Fab fragment in complex with its Lewis X antigen. Structure 12 (2004) 1227-1236
71. Verdonk M.L., Cole J.C., Hartshorn M.J., Murray C.W., and Taylor R.D. Improved protein-ligand docking using GOLD. Proteins 52 (2003) 609-623
72. Vyas N.K., Vyas M.N., Chervenak M.C., Johnson M.A., Pinto B.M., Bundle D.R., and Quiocho F.A. Molecular recognition of oligosaccharide epitopes by a monoclonal Fab specific for Shigella flexneri Y lipopolysaccharide: X-ray structures and thermodynamics. Biochemistry 41 (2002) 13575-13586
73. Wallace A.C., Laskowski R.A., and Thornton J.M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8 (1995) 127-134
74. Walser P.J., Haebel P.W., Künzler M., Sargent D., Kües U., Aebi M., and Ban N. Structure and functional analysis of the fungal galectin CGL2. Structure 12 (2004) 689-702
75. Yuriev E., Ramsland P.A., and Edmundson A.B. Docking of combinatorial peptide libraries into a broadly cross-reactive human IgM. J. Mol. Recogn. 14 (2001) 172-184
76. Yuriev E., Farrugia W., Scott A.M., and Ramsland P.A. Three-dimensional structures of carbohydrate determinants of Lewis system antigens: implications for effective antibody targeting of cancer. Immunol. Cell Biol. 83 (2005) 709-717
77. Yuriev E., Sandrin M.S., and Ramsland P.A. Antibody-ligand docking: insights into peptide-carbohydrate mimicry. Mol. Simulat. 34 (2008) 461-469
78. Yuriev E., Agostino M., Farrugia W., Christiansen D., Sandrin M., and Ramsland P. Structural biology of carbohydrate xenoantigens. Expert Opin. Biol. Ther. 9 (2009) 1017-1029
79. Zdanov A., Li Y., Bundle D.R., Deng S.J., MacKenzie C.R., Narang S.A., Young N.M., and Cygler M. Structure of the single-chain antibody domain (Fv) fragment complexed with a carbohydrate antigen as 1.7 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 6423-6427
80. Zhong S.J., and MacKerell A.D.J. Binding response: a descriptor for selecting ligand binding site on protein surfaces. J. Chem. Inf. Model. 47 (2007) 2303-2315