Prediction of IgE-binding epitopes by means of allergen surface comparison and correlation to cross-reactivity

Journal of Allergy and Clinical Immunology

Volumn 128, Issue 4, 2011, Pages 872-879.e8

  Dall'Antonia, Fabio ^a,c   Gieras, Anna ^b   Devanaboyina, Siva Charan ^a,d   Valenta, Rudolf ^b   Keller, Walter ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

allergen surfaces; allergen specific immunotherapy; Allergy; cross reactivity; epitope prediction; hypoallergenic derivatives; IgE binding; x ray structures

Indexed keywords

ALLERGEN; BETA LACTOGLOBULIN; EPITOPE; IMMUNOGLOBULIN E; LIPOCALIN; POLLEN ANTIGEN; LACTOGLOBULIN; PLANT ANTIGEN;

ARTICLE; COMPUTER PROGRAM; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; GRASS POLLEN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; SURFACE COMPARISON BASED PREDICTION OF ALLERGENIC DISCONTINUOUS EPITOPE; ALGORITHM; ANIMAL; CATTLE; CHEMICAL STRUCTURE; COMPARATIVE STUDY; FEMALE; GENETICS; HAY FEVER; HUMAN; IMMUNOLOGY; MALE; METABOLISM;

ALGORITHMS; ALLERGENS; ANIMALS; ANTIGENS, PLANT; CATTLE; CROSS REACTIONS; EPITOPES; FEMALE; HUMANS; IMMUNOGLOBULIN E; LACTOGLOBULINS; MALE; MODELS, MOLECULAR; RHINITIS, ALLERGIC, SEASONAL; SOFTWARE;

EID: 80053568367     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2011.07.007     Document Type: Article

References (74)

1. R. Valenta, F. Ferreira, M. Focke-Tejkl, B. Linhart, V. Niederberger, and I. Swoboda From allergen genes to allergy vaccines Annu Rev Immunol 28 2010 211 241
2. R. Valenta The future of antigen-specific immunotherapy of allergy Nat Rev Immunol 2 2002 446 453 (Pubitemid 37328752)
3. K. Westritschnig, M. Focke, P. Verdino, W. Goessler, W. Keller, and A. Twardosz Generation of an allergy vaccine by disruption of the three-dimensional structure of the cross-reactive calcium-binding allergen, Phl p 7 J Immunol 172 2004 5684 5692 (Pubitemid 38542072)
4. I. Swoboda, A. Bugajska-Schretter, B. Linhart, P. Verdino, W. Keller, and U. Schulmeister A recombinant hypoallergenic parvalbumin mutant for immunotherapy of IgE-mediated fish allergy J Immunol 178 2007 6290 6296 (Pubitemid 46717412)
5. M. Niemi, S. Jylha, M.L. Laukkanen, H. Soderlund, S. Makinen-Kiljunen, and J.M. Kallio Molecular interactions between a recombinant IgE antibody and the beta-lactoglobulin allergen Structure 15 2007 1413 1421 (Pubitemid 350051924)
6. S. Padavattan, S. Flicker, T. Schirmer, C. Madritsch, S. Randow, and G. Reese High-affinity IgE recognition of a conformational epitope of the major respiratory allergen Phl p 2 as revealed by X-ray crystallography J Immunol 182 2009 2141 2151
7. R. Valenta, and D. Kraft Recombinant allergen molecules: tools to study effector cell activation Immunol Rev 179 2001 119 127 (Pubitemid 32171279)
8. J.M. Thornton, M.S. Edwards, W.R. Taylor, and D.J. Barlow Location of 'continuous' antigenic determinants in the protruding regions of proteins EMBO J 5 1986 409 413
9. E. Westhof, D. Altschuh, D. Moras, A.C. Bloomer, A. Mondragon, and A. Klug Correlation between segmental mobility and the location of antigenic determinants in proteins Nature 311 1984 123 126 (Pubitemid 14072200)
10. T.P. Hopp, and K.R. Woods Prediction of protein antigenic determinants from amino acid sequences Proc Natl Acad Sci U S A 78 1981 3824 3828 (Pubitemid 11060471)
11. U. Kulkarni-Kale, S. Bhosle, and A.S. Kolaskar CEP: a conformational epitope prediction server Nucleic Acids Res 33 2005 W168 W171
12. J. Ponomarenko, H.H. Bui, W. Li, N. Fusseder, P.E. Bourne, and A. Sette ElliPro: a new structure-based tool for the prediction of antibody epitopes BMC Bioinformatics 9 2008 514
13. P. Haste Andersen, M. Nielsen, and O. Lund Prediction of residues in discontinuous B-cell epitopes using protein 3D structures Protein Sci 15 2006 2558 2567 (Pubitemid 44771693)
14. N.D. Rubinstein, I. Mayrose, E. Martz, and T. Pupko Epitopia: a web-server for predicting B-cell epitopes BMC Bioinformatics 10 2009 287
15. J. Sun, D. Wu, T. Xu, X. Wang, X. Xu, and L. Tao SEPPA: a computational server for spatial epitope prediction of protein antigens Nucleic Acids Res 37 2009 W612 W616
16. R. Furmonaviciene, B.J. Sutton, F. Glaser, C.A. Laughton, N. Jones, and H.F. Sewell An attempt to define allergen-specific molecular surface features: a bioinformatic approach Bioinformatics 21 2005 4201 4204 (Pubitemid 41724297)
17. S. Saha, and G.P. Raghava Prediction of continuous B-cell epitopes in an antigen using recurrent neural network Proteins 65 2006 40 48 (Pubitemid 44320614)
18. S. Vieths, S. Scheurer, and B. Ballmer-Weber Current understanding of cross-reactivity of food allergens and pollen Ann N Y Acad Sci 964 2002 47 68 (Pubitemid 34596831)
19. R.C. Aalberse Assessment of allergen cross-reactivity Clin Mol Allergy 5 2007 2
20. R. Valenta, P. Steinberger, M. Duchene, and D. Kraft Immunological and structural similarities among allergens: prerequisite for a specific and component-based therapy of allergy Immunol Cell Biol 74 1996 187 194 (Pubitemid 26173825)
21. J.A. Jenkins, S. Griffiths-Jones, P.R. Shewry, H. Breiteneder, and E.N. Mills Structural relatedness of plant food allergens with specific reference to cross-reactive allergens: an in silico analysis J Allergy Clin Immunol 115 2005 163 170 (Pubitemid 40075438)
22. Y. Kaneta, N. Shoji, T. Ohkawa, and H. Nakamura A method of comparing protein molecular surface based on normal vectors with attributes and its application to function identification Inform Sci 146 2002 41 54 (Pubitemid 35214289)
23. T.A. Binkowski, P. Freeman, and J. Liang pvSOAR: detecting similar surface patterns of pocket and void surfaces of amino acid residues on proteins Nucleic Acids Res 32 2004 W555 W558
24. M.C. Lawrence, and P.M. Colman Shape complementarity at protein/protein interfaces J Mol Biol 234 1993 946 950 (Pubitemid 24027225)
25. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, and H. Weissig The Protein Data Bank Nucleic Acids Res 28 2000 235 242 (Pubitemid 30047768)
26. M. Shatsky, R. Nussinov, and H.J. Wolfson A method for simultaneous alignment of multiple protein structures Proteins 56 2004 143 156 (Pubitemid 38720846)
27. W. Kabsch Solution for best rotation to relate 2 sets of vectors Acta Crystallogr A 32 1976 922 923
28. S.C. Lovell, J.M. Word, J.S. Richardson, and D.C. Richardson The penultimate rotamer library Proteins 40 2000 389 408 (Pubitemid 30624447)
29. T.J. Dolinsky, P. Czodrowski, H. Li, J.E. Nielsen, J.H. Jensen, and G. Klebe PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res 35 2007 W522 W525
30. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc Natl Acad Sci U S A 98 2001 10037 10041 (Pubitemid 32802969)
31. M.F. Sanner, A.J. Olson, and J.C. Spehner Reduced surface: an efficient way to compute molecular surfaces Biopolymers 38 1996 305 320
32. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific Palo Alto (CA)
33. D.A. Stern, J. Riedler, D. Nowak, C. Braun-Fahrlander, I. Swoboda, and N. Balic Exposure to a farming environment has allergen-specific protective effects on TH2-dependent isotype switching in response to common inhalants J Allergy Clin Immunol 119 2007 351 358 (Pubitemid 46210077)
34. E. Oksanen, V.P. Jaakola, T. Tolonen, K. Valkonen, B. Akerstrom, and N. Kalkkinen Reindeer beta-lactoglobulin crystal structure with pseudo-body-centered noncrystallographic symmetry Acta Crystallogr D Biol Crystallogr 62 2006 1369 1374 (Pubitemid 44630215)
35. J. Rouvinen, J. Rautiainen, T. Virtanen, T. Zeiler, J. Kauppinen, and A. Taivainen Probing the molecular basis of allergy. Three-dimensional structure of the bovine lipocalin allergen Bos d 2 J Biol Chem 274 1999 2337 2343
36. B.N. Chaudhuri, G.J. Kleywegt, J. Bjorkman, L.D. Lehman-McKeeman, J.D. Oliver, and T.A. Jones The structures of alpha 2u-globulin and its complex with a hyaline droplet inducer Acta Crystallogr D Biol Crystallogr 55 1999 753 762 (Pubitemid 29194521)
37. M. Gajhede, P. Osmark, F.M. Poulsen, H. Ipsen, J.N. Larsen, and R.J. Joost van Neerven X-ray and NMR structure of Bet v 1, the origin of birch pollen allergy Nat Struct Biol 3 1996 1040 1045 (Pubitemid 27014633)
38. P. Neudecker, K. Schweimer, J. Nerkamp, S. Scheurer, S. Vieths, and H. Sticht Allergic cross-reactivity made visible: solution structure of the major cherry allergen Pru av 1 J Biol Chem 276 2001 22756 22763
39. T. Schirmer, K. Hoffimann-Sommergrube, M. Susani, H. Breiteneder, and Z. Markovic-Housley Crystal structure of the major celery allergen Api g 1: molecular analysis of cross-reactivity J Mol Biol 351 2005 1101 1109 (Pubitemid 41133455)
40. J. Biesiadka, G. Bujacz, M.M. Sikorski, and M. Jaskolski Crystal structures of two homologous pathogenesis-related proteins from yellow lupine J Mol Biol 319 2002 1223 1234 (Pubitemid 34729430)
41. O. Pasternak, G.D. Bujacz, Y. Fujimoto, Y. Hashimoto, F. Jelen, and J. Otlewski Crystal structure of Vigna radiata cytokinin-specific binding protein in complex with zeatin Plant Cell 18 2006 2622 2634 (Pubitemid 44749893)
42. N. Zaborsky, M. Brunner, M. Wallner, M. Himly, T. Karl, and R. Schwarzenbacher Antigen aggregation decides the fate of the allergic immune response J Immunol 184 2010 725 735
43. Z. Markovic-Housley, M. Degano, D. Lamba, E. von Roepenack-Lahaye, S. Clemens, and M. Susani Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier J Mol Biol 325 2003 123 133 (Pubitemid 36153002)
44. T.J. Suutari, K.H. Valkonen, T.J. Karttunen, B.M. Ehn, B. Ekstrand, and U. Bengtsson IgE cross reactivity between reindeer and bovine milk beta-lactoglobulins in cow's milk allergic patients J Investig Allergol Clin Immunol 16 2006 296 302 (Pubitemid 44580256)
45. F. Ferreira, K. Hirtenlehner, A. Jilek, J. Godnik-Cvar, H. Breiteneder, and R. Grimm Dissection of immunoglobulin E and T lymphocyte reactivity of isoforms of the major birch pollen allergen Bet v 1: potential use of hypoallergenic isoforms for immunotherapy J Exp Med 183 1996 599 609 (Pubitemid 26059521)
46. O. Mirza, A. Henriksen, H. Ipsen, J.N. Larsen, M. Wissenbach, and M.D. Spangfort Dominant epitopes and allergic cross-reactivity: complex formation between a Fab fragment of a monoclonal murine IgG antibody and the major allergen from birch pollen Bet v 1 J Immunol 165 2000 331 338 (Pubitemid 30429524)
47. M. Focke, B. Linhart, A. Hartl, U. Wiedermann, W.R. Sperr, and P. Valent Non-anaphylactic surface-exposed peptides of the major birch pollen allergen, Bet v 1, for preventive vaccination Clin Exp Allergy 34 2004 1525 1533 (Pubitemid 39389328)
48. A. Gieras, P. Cejka, K. Blatt, M. Focke-Tejkl, B. Linhart, and S. Flicker Mapping of conformational IgE epitopes with peptide-specific monoclonal antibodies reveals simultaneous binding of different IgE antibodies to a surface patch on the major birch pollen allergen, Bet v 1 J Immunol 186 2011 5333 5344
49. M.D. Spangfort, O. Mirza, H. Ipsen, R.J. Van Neerven, M. Gajhede, and J.N. Larsen Dominating IgE-binding epitope of Bet v 1, the major allergen of birch pollen, characterized by X-ray crystallography and site-directed mutagenesis J Immunol 171 2003 3084 3090 (Pubitemid 37098339)
50. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc Natl Acad Sci U S A 98 2001 10037 10041 (Pubitemid 32802969)
51. T.J. Dolinsky, P. Czodrowski, H. Li, J.E. Nielsen, J.H. Jensen, and G. Klebe PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res 35 2007 W522 W525
52. S.D. Black, and D.R. Mould Development of hydrophobicity parameters to analyze proteins which bear post- or cotranslational modifications Anal Biochem 193 1991 72 82
53. C. Radauer, M. Bublin, S. Wagner, A. Mari, and H. Breiteneder Allergens are distributed into few protein families and possess a restricted number of biochemical functions J Allergy Clin Immunol 121 2008 847 852 e7
54. A. Mari Importance of databases in experimental and clinical allergology Int Arch Allergy Immunol 138 2005 88 96 (Pubitemid 41291570)
55. T. Kawabata MATRAS: a program for protein 3D structure comparison Nucleic Acids Res 31 2003 3367 3369 (Pubitemid 37442161)
56. T.J. Suutari, K.H. Valkonen, T.J. Karttunen, B.M. Ehn, B. Ekstrand, and U. Bengtsson IgE cross reactivity between reindeer and bovine milk beta-lactoglobulins in cow's milk allergic patients J Investig Allergol Clin Immunol 16 2006 296 302 (Pubitemid 44580256)
57. U. Kulkarni-Kale, S. Bhosle, and A.S. Kolaskar CEP: a conformational epitope prediction server Nucleic Acids Res 33 2005 W168 W171
58. P. Haste Andersen, M. Nielsen, and O. Lund Prediction of residues in discontinuous B-cell epitopes using protein 3D structures Protein Sci 15 2006 2558 2567 (Pubitemid 44771693)
59. J. Ponomarenko, H.H. Bui, W. Li, N. Fusseder, P.E. Bourne, and A. Sette ElliPro: a new structure-based tool for the prediction of antibody epitopes BMC Bioinformatics 9 2008 514
60. N.D. Rubinstein, I. Mayrose, E. Martz, and T. Pupko Epitopia: a web-server for predicting B-cell epitopes BMC Bioinformatics 10 2009 287
61. J. Sun, D. Wu, T. Xu, X. Wang, X. Xu, and L. Tao SEPPA: a computational server for spatial epitope prediction of protein antigens Nucleic Acids Res 37 2009 W612 W616
62. H. Breiteneder, and C. Radauer A classification of plant food allergens J Allergy Clin Immunol 113 2004 821 831
63. A. Petersen, R. Suck, B. Lindner, D. Georgieva, M. Ernst, and H. Notbohm Phl p 3: structural and immunological characterization of a major allergen of timothy grass pollen Clin Exp Allergy 36 2006 840 849 (Pubitemid 43972980)
64. S. Padavattan, S. Flicker, T. Schirmer, C. Madritsch, S. Randow, and G. Reese High-affinity IgE recognition of a conformational epitope of the major respiratory allergen Phl p 2 as revealed by X-ray crystallography J Immunol 182 2009 2141 2151
65. W.R. Pearson Rapid and sensitive sequence comparison with FASTP and FASTA Methods Enzymol 183 1990 63 98 (Pubitemid 20148813)
66. E. Westhof, D. Altschuh, D. Moras, A.C. Bloomer, A. Mondragon, and A. Klug Correlation between segmental mobility and the location of antigenic determinants in proteins Nature 311 1984 123 126 (Pubitemid 14072200)
67. M. Gajhede, P. Osmark, F.M. Poulsen, H. Ipsen, J.N. Larsen, and R.J. Joost van Neerven X-ray and NMR structure of Bet v 1, the origin of birch pollen allergy Nat Struct Biol 3 1996 1040 1045 (Pubitemid 27014633)
68. O. Mirza, A. Henriksen, H. Ipsen, J.N. Larsen, M. Wissenbach, and M.D. Spangfort Dominant epitopes and allergic cross-reactivity: complex formation between a Fab fragment of a monoclonal murine IgG antibody and the major allergen from birch pollen Bet v 1 J Immunol 165 2000 331 338 (Pubitemid 30429524)
69. A. Gustchina, M. Li, S. Wunschmann, M.D. Chapman, A. Pomes, and A. Wlodawer Crystal structure of cockroach allergen Bla g 2, an unusual zinc binding aspartic protease with a novel mode of self-inhibition J Mol Biol 348 2005 433 444 (Pubitemid 40462107)
70. M. Li, A. Gustchina, J. Alexandratos, A. Wlodawer, S. Wunschmann, and C.L. Kepley Crystal structure of a dimerized cockroach allergen Bla g 2 complexed with a monoclonal antibody J Biol Chem 283 2008 22806 22814
71. Z. Markovic-Housley, G. Miglierini, L. Soldatova, P.J. Rizkallah, U. Muller, and T. Schirmer Crystal structure of hyaluronidase, a major allergen of bee venom Structure 8 2000 1025 1035 (Pubitemid 32667466)
72. S. Padavattan, T. Schirmer, M. Schmidt, C. Akdis, R. Valenta, and I. Mittermann Identification of a B-cell epitope of hyaluronidase, a major bee venom allergen, from its crystal structure in complex with a specific Fab J Mol Biol 368 2007 742 752 (Pubitemid 46527617)
73. K.M. Oliveira, V.L. Valente-Mesquita, M.M. Botelho, L. Sawyer, S.T. Ferreira, and I. Polikarpov Crystal structures of bovine beta-lactoglobulin in the orthorhombic space group C222(1). Structural differences between genetic variants A and B and features of the Tanford transition Eur J Biochem 268 2001 477 483 (Pubitemid 32862681)
74. M. Niemi, S. Jylha, M.L. Laukkanen, H. Soderlund, S. Makinen-Kiljunen, and J.M. Kallio Molecular interactions between a recombinant IgE antibody and the beta-lactoglobulin allergen Structure 15 2007 1413 1421 (Pubitemid 350051924)