Secret of the major birch pollen allergen Bet v 1: Identification of the physiological ligand

Biochemical Journal

Volumn 457, Issue 3, 2014, Pages 379-390

  Von Loetzen, Christian Seutter ^a   Hoffmann, Thomas ^b   Hartl, Maximilian J ^a   Schweimer, Kristian ^a   Schwab, Wilfried ^b   Rösch, Paul ^a   Hartl Spiegelhauer, Olivia ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Allergen; Bet v 1; NMR; Quercetin 3 O sophoroside(Q3OS)

Indexed keywords

GLYCOSIDE; IMMUNOGLOBULIN E; LIGAND; POLLEN ALLERGEN BET V 1; POLLEN ANTIGEN; QUERCETIN; QUERCETIN 3 O SOPHOROSIDE; QUERCETIN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; BIRCH; FLUORESCENCE SPECTROSCOPY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; INFLAMMATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FUNCTION; ULTRAVIOLET SPECTROSCOPY;

ANTIGENS, PLANT; BETULA; BINDING SITES; GERMINATION; GLYCOSIDES; LIGANDS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR DOCKING SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PLANT PROTEINS; POLLEN; POLLINATION; QUERCETIN; RECOMBINANT PROTEINS; SELF-FERTILIZATION; SPECTROPHOTOMETRY; TITRIMETRY; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84892188196     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130413     Document Type: Article

References (70)

1. Ipsen, H. and Lowenstein, H. (1983) Isolation and immunochemical characterization of the major allergen of birch pollen (betula verrucosa ). J. Allergy Clin. Immunol. 72, 150-159
2. Schenk, M. F., Cordewener, J. H., America, A. H., Van't Westende, W. P., Smulders, M. J. and Gilissen, L. J. (2009) Characterization of PR-10 genes from eight betula species and detection of Bet v 1 isoforms in birch pollen. BMC Plant. Biol. 9, 24
3. D'Amato, G., Spieksma, F. T., Liccardi, G., Jager, S., Russo, M., Kontou-Fili, K., Nikkels, H., Wuthrich, B. and Bonini, S. (1998) Pollen-related allergy in europe. Allergy 53, 567-578
4. Wuthrich, B., Schindler, C., Leuenberger, P. and Ackermann-Liebrich, U. (1995) Prevalence of atopy and pollinosis in the adult population of switzerland (SAPALDIA study). Swiss study on air pollution and lung diseases in adults. Int. Arch. Allergy Immunol. 106, 149-156
5. Vieths, S., Scheurer, S. and Ballmer-Weber, B. (2002) Current understanding of cross-reactivity of food allergens and pollen. Ann. N.Y. Acad. Sci. 964, 47-68
6. Jarolim, E., Rumpold, H., Endler, A. T., Ebner, H., Breitenbach, M., Scheiner, O. and Kraft, D. (1989) IgE and IgG antibodies of patients with allergy to birch pollen as tools to define the allergen profile of Betula verrucosa . Allergy 44, 385-395
7. Moverare, R., Westritschnig, K., Svensson, M., Hayek, B., Bende, M., Pauli, G., Sorva, R., Haahtela, T., Valenta, R. and Elfman, L. (2002) Different IgE reactivity profiles in birch pollen-sensitive patients from six european populations revealed by recombinant allergens: an imprint of local sensitization. Int. Arch. Allergy Immunol. 128, 325-335
8. Dreborg, S. (1988) Food allergy in pollen-sensitive patients. Ann. Allergy. 61, 41-46
9. Geroldinger-Simic, M., Zelniker, T., Aberer, W., Ebner, C., Egger, C., Greiderer, A., Prem, N., Lidholm, J., Ballmer-Weber, B., Vieths, S. and Bohle, B. (2011) Birch pollen-related food allergy: clinical aspects and the role of allergen-specific IgE and IgG4 antibodies. J. Allergy Clin. Immunol. 127, 616-622
10. Liu, J. and Ekramoddoullah, A. K. M. (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol. Mol. Plant Pathol. 68, 3-13
11. Breda, C., Sallaud, C., el-Turk, J., Buffard, D., de Kozak, I., Esnault, R. and Kondorosi, A. (1996) Defense reaction in medicago sativa: a gene encoding a class 10 PR protein is expressed in vascular bundles. Mol. Plant Microbe Interact. 9, 713-719
12. Robert, N., Ferran, J., Breda, C., Coutos-Thévenot, P., Boulay, M., Buffard, D. and Esnault, R. (2001) Molecular characterization of the incompatible interaction of Vitis vinifera leaves with Pseudomonas syringae pv. pisi: expression of genes coding for stilbene synthase and class 10 PR protein. Eur. J. Plant Pathol. 107, 249-261
13. Somssich, I. E., Schmelzer, E., Bollmann, J. and Hahlbrock, K. (1986) Rapid activation by fungal elicitor of genes encoding "pathogenesis- related" proteins in cultured parsley cells. Proc. Natl. Acad. Sci. U.S.A. 83, 2427-2430
14. Walter, M. H., Liu, J. W., Grand, C., Lamb, C. J. and Hess, D. (1990) Bean pathogenesis-related (PR) proteins deduced from elicitor-induced transcripts are members of a ubiquitous new class of conserved PR proteins including pollen allergens. Mol. Gen. Genet. 222, 353-360
15. Warner, S. A. J., Scott, R. and Draper, J. (1992) Characterisation of a wound-induced transcript from the monocot asparagus that shares similarity with a class of intracellular pathogenesis-related (PR) proteins. Plant Mol. Biol. 19, 555-561
16. Walter, M. H., Liu, J. W., Wunn, J. and Hess, D. (1996) Bean ribonuclease-like pathogenesis-related protein genes (Ypr10) display complex patterns of developmental, dark-induced and exogenous-stimulus-dependent expression. Eur. J. Biochem. 239, 281-293
17. Hoffmann-Sommergruber, K. (2000) Plant allergens and pathogenesis-related proteins. what do they have in common? Int. Arch. Allergy Immunol. 122, 155-166
18. Ferreira, F. D., Hoffmann-Sommergruber, K., Breiteneder, H., Pettenburger, K., Ebner, C., Sommergruber, W., Steiner, R., Bohle, B., Sperr, W. R. and Valent, P. (1993) Purification and characterization of recombinant Bet v I, the major birch pollen allergen. immunological equivalence to natural Bet v I. J. Biol. Chem. 268, 19574-19580
19. Swoboda, I., Jilek, A., Ferreira, F., Engel, E., Hoffmann-Sommergruber, K., Scheiner, O., Kraft, D., Breiteneder, H., Pittenauer, E. and Schmid, E. (1995) Isoforms of Bet v 1, the major birch pollen allergen, analyzed by liquid chromatography, mass spectrometry, and cDNA cloning. J. Biol. Chem. 270, 2607-2613
20. Faber, C., Lindemann, A., Sticht, H., Ejchart, A., Kungl, A., Susani, M., Frank, R. W., Kraft, D., Breitenbach, M. and Rösch, P. (1996) Secondary structure and tertiary fold of the birch pollen allergen Bet v 1 in solution. J. Biol. Chem. 271, 19243-19250
21. Gajhede, M., Osmark, P., Poulsen, F. M., Ipsen, H., Larsen, J. N., Joost van Neerven, R. J., Schou, C., Lowenstein, H. and Spangfort, M. D. (1996) X-ray and NMR structure of Bet v1, the origin of birch pollen allergy. Nat. Struct. Biol. 3, 1040-1045
22. Schweimer, K., Sticht, H., Nerkamp, J., Boehm, M., Breitenbach, M., Vieths, S. and Rösch, P. (1999) NMR spectroscopy reveals common structural features of the birch pollen allergen Bet v 1 and the cherry allergen Pru a 1. Appl. Magn. Reson. 17, 449-456
23. Ferreira, F., Ebner, C., Kramer, B., Casari, G., Briza, P., Kungl, A. J., Grimm, R., Jahn-Schmid, B., Breiteneder, H., Kraft, D. et al. (1998) Modulation of IgE reactivity of allergens by site-directed mutagenesis: potential use of hypoallergenic variants for immunotherapy. FASEB J. 12, 231-242
24. Krebitz, M., Wiedermann, U., Essl, D., Steinkellner, H., Wagner, B., Turpen, T. H., Ebner, C., Scheiner, O. and Breiteneder, H. (2000) Rapid production of the major birch pollen allergen Bet v 1 in Nicotiana benthamiana plants and its immunological in vitro and in vivo characterization. FASEB J. 14, 1279-1288
25. Mirza, O., Henriksen, A., Ipsen, H., Larsen, J. N., Wissenbach, M., Spangfort, M. D. and Gajhede, M. (2000) 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, 331-338
26. Spangfort, M. D., Mirza, O., Ipsen, H., Joost van Neerven, R. J., Gajhede, M. and Larsen, J. N. (2003) 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, 3084-3090
27. Mittag, D., Batori, V., Neudecker, P., Wiche, R., Friis, E. P., Ballmer-Weber, B. K., Vieths, S. and Roggen, E. L. (2006) A novel approach for investigation of specific and cross-reactive IgE epitopes on Bet v 1 and homologous food allergens in individual patients. Mol. Immunol. 43, 268-278
28. Mogensen, J. E., Wimmer, R., Larsen, J. N., Spangfort, M. D. and Otzen, D. E. (2002) The major birch allergen, Bet v 1, shows affinity for a broad spectrum of physiological ligands. J. Biol. Chem. 277, 23684-23692
29. Markovic-Housley, Z., Degano, M., Lamba, D., von Roepenack-Lahaye, E., Clemens, S., Susani, M., Ferreira, F., Scheiner, O. and Breiteneder, H. (2003) 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, 123-133
30. Mogensen, J. E., Ferreras, M., Wimmer, R., Petersen, S. V., Enghild, J. J. and Otzen, D. E. (2007) The major allergen from birch tree pollen, Bet v 1, binds and permeabilizes membranes. Biochemistry 46, 3356-3365
31. Koistinen, K. M., Kokko, H. I., Hassinen, V. H., Tervahauta, A. I., Auriola, S. and Kärenlampi, S. O. (2002) Stress-related RNase PR-10c is post-translationally modified by glutathione in birch. Plant Cell Environ. 25, 707-715
32. Koistinen, K. M., Soininen, P., Venalainen, T. A., Hayrinen, J., Laatikainen, R., Perakyla, M., Tervahauta, A. I. and Karenlampi, S. O. (2005) Birch PR-10c interacts with several biologically important ligands. Phytochemistry 66, 2524-2533
33. Kofler, S., Asam, C., Eckhard, U., Wallner, M., Ferreira, F. and Brandstetter, H. (2012) Crystallographically mapped ligand binding differs in high and low IgE binding isoforms of birch pollen allergen Bet v 1. J. Mol. Biol. 422, 109-123
34. Grote, M., Vrtala, S. and Valenta, R. (1993) Monitoring of two allergens, Bet v I and profilin, in dry and rehydrated birch pollen by immunogold electron microscopy and immunoblotting. J. Histochem. Cytochem. 41, 745-750
35. Bollen, M. A., Garcia, A., Cordewener, J. H., Wichers, H. J., Helsper, J. P., Savelkoul, H. F. and van Boekel, M. A. (2007) Purification and characterization of natural bet v 1 from birch pollen and related allergens from carrot and celery. Mol. Nutr. Food Res. 51, 1527-1536
36. Johnson, B. A. and Blevins, R. A. (1994) NMRview: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614
37. Trott, O. and Olson, A. J. (2010) AutoDock vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461
38. Schüttelkopf, A. W. and van Aalten, D. M. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 1355-1363
39. Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S. and Olson, A. J. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791
40. Bufe, A. (1998) The biological function of allergens: relevant for the induction of allergic diseases? Int. Arch. Allergy Immunol. 117, 215-219
41. Harborne, J. B., Baxter, H. and Moss, G. P. (1999) Phytochemical Dictionary: a Handbook of Bioactive Compounds From Plants, CRC Press, London
42. Ross, S. A., ElSohly, M. A., Sultana, G. N., Mehmedic, Z., Hossain, C. F. and Chandra, S. (2005) Flavonoid glycosides and cannabinoids from the pollen of cannabis sativa L. Phytochem. Anal. 16, 45-48
43. Arraez-Roman, D., Zurek, G., Bässmann, C., Almaraz-Abarca, N., Quirantes, R., Segura-Carretero, A. and Fernandez-Gutierrez, A. (2007) Identification of phenolic compounds from pollen extracts using capillary electrophoresis-electrospray time-of-flight mass spectrometry. Anal. Bioanal. Chem. 389, 1909-1917
44. Falkovskaia, E., Sengupta, P. K. and Kasha, M. (1998) Photophysical induction of dual fluorescence of quercetin and related hydroxyflavones upon intermolecular H-bonding to solvent matrix. Chem. Phys. Lett. 297, 109-114
45. Ghiasi, M., Taheri, S. and Tafazzoli, M. (2010) Dynamic stereochemistry of rutin (vitamin P) in solution: theoretical approaches and experimental validation. Carbohydr. Res. 345, 1760-1766
46. Bundle, D. R. and Young, N. M. (1992) Carbohydrate-protein interactions in antibodies and lectins. Curr. Opin. Struct. Biol. 2, 666-673
47. Toone, E. J. (1994) Structure and energetics of protein-carbohydrate complexes. Curr. Opin. Struct. Biol. 4, 719-728
48. García-Hernández, E., Zubillaga, R. A., Rojo-Domínguez, A., Rodríguez-Romero, A. and Herníndez- Arana, A. (1997) New insights into the molecular basis of lectin-carbohydrate interactions: a calorimetric and structural study of the association of hevein to oligomers of N-acetylglucosamine. Proteins: Struct., Funct., Bioinf. 29, 467-477
49. García-Hernández, E. and Hernández-Arana, A. (1999) Structural bases of lectin-carbohydrate affinities: comparison with protein-folding energetics. Protein Sci. 8, 1075-1086
50. Dam, T. K. and Brewer, C. F. (2002) Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry. Chem. Rev. 102, 387-430
51. Dunitz, J. D. (1995) Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions. Chem. Biol. 2, 709-712
52. Holgersson, J., Gustafsson, A. and Breimer, M. E. (2005) Characteristics of protein-carbohydrate interactions as a basis for developing novel carbohydrate-based antirejection therapies. Immunol. Cell Biol. 83, 694-708
53. Wilhelm, D., Behnken, H. N. and Meyer, B. (2012) Glycosylation assists binding of HIV protein gp120 to human CD4 receptor. ChemBioChem 13, 524-527
54. Robinson, B. W., Venaille, T. J., Mendis, A. H. and McAleer, R. (1990) Allergens as proteases: an Aspergillus fumigatus proteinase directly induces human epithelial cell detachment. J. Allergy Clin. Immunol. 86, 726-731
55. Herbert, C. A., King, C. M., Ring, P. C., Holgate, S. T., Stewart, G. A., Thompson, P. J. and Robinson, C. (1995) Augmentation of permeability in the bronchial epithelium by the house dust mite allergen der p1. Am. J. Respir. Cell Mol. Biol. 12, 369-378
56. Hassim, Z., Maronese, S. E. and Kumar, R. K. (1998) Injury to murine airway epithelial cells by pollen enzymes. Thorax 53, 368-371
57. Miller, K. D., Guyon, V., Evans, J. N., Shuttleworth, W. A. and Taylor, L. P. (1999) Purification, cloning, and heterologous expression of a catalytically efficient flavonol 3-O-galactosyltransferase expressed in the male gametophyte of petunia hybrida. J. Biol. Chem. 274, 34011-34019
58. Brunetti, C., Di Ferdinando, M., Fini, A., Pollastri, S. and Tattini, M. (2013) Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. Int. J. Mol. Sci. 14, 3540-3555
59. Karioti, A., Kitsaki, C. K., Zygouraki, S., Ziobora, M., Djeddi, S., Skaltsa, H. and Liakopoulos, G. (2008) Occurrence of flavonoids in ophrys (orchidaceae) flower parts. Flora 203, 602-609
60. Mo, Y., Nagel, C. and Taylor, L. P. (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc. Natl. Acad. Sci. U.S.A. 89, 7213-7217
61. Ceska, O. and Styles, E. D. (1984) Flavonoids from Zea mays pollen. Phytochemistry 23, 1822-1823
62. Taylor, L. P. and Miller, K. D. (2002) The use of a photoactivatable kaempferol analogue to probe the role of flavonol 3-O-galactosyltransferase in pollen germination. Adv. Exp. Med. Biol. 505, 41-50
63. Vogt, T. and Taylor, L. P. (1995) Flavonol 3-O-glycosyltransferases associated with petunia pollen produce gametophyte-specific flavonol diglycosides. Plant Physiol. 108, 903-911
64. Mattila, K. and Renkonen, R. (2009) Modelling of Bet v 1 binding to lipids. Scand. J. Immunol. 70, 116-124
65. Golebski, K., Röschmann, K. I., Toppila-Salmi, S., Hammad, H., Lambrecht, B. N., Renkonen, R., Fokkens, W. J. and van Drunen, C. M. (2013) The multi-faceted role of allergen exposure to the local airway mucosa. Allergy 68, 152-160
66. Strack, D., Meurer, B., Wray, V., Grotjahn, L., Austenfeld, F. A. and Wiermann, R. (1984) Quercetin 3-glucosylgalactoside from pollen of Corylus avellana . Phytochemistry 23, 2970-2971
67. Xu, P., Vogt, T. and Taylor, L. P. (1997) Uptake and metabolism of flavonols during in vitro germination of Petunia hybrida (L.) pollen. Planta 202, 257-265
68. Zerback, R., Bokel, M., Geiger, H. and Hess, D. (1989) A kaempferol 3-glucosylgalactoside and further flavonoids from pollen of petunia hybrida. Phytochemistry 28, 897-899
69. Taylor, L. P. and Hepler, P. K. (1997) Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 461-491
70. Ryan, K. G., Markham, K. R., Bloor, S. J., Bradley, J. M., Mitchell, K. A. and Jordan, B. R. (1998) UVB radiation induced increase in quercetin: kaempferol ratio in wild-type and transgenic lines of Petunia. Photochem. Photobiol. 68, 323-330