Abstract
Bet v 1 is an important cause of hay fever in the northern hemisphere. Bet v 1 isoforms from the European white birch (Betula pendula) have been investigated extensively, but the allergenic potency of other birch species is unknown. PR-10 genes were cloned and sequenced from 8 different birch species, representing all major groups within the genus, to establish the presence of these genes. In total, 134 unique sequences were discovered. Sequences were attributed to different PR-10 genes or pseudogenes that were subdivided into 7 subfamilies. Five subfamilies were common to all birch species. Q-TOF LC-MSE was applied to identify which PR-10/Bet v 1 genes are expressed in pollen and to determine relative abundances of individual isoforms in the pollen proteome. This showed that genes of two subfamilies were expressed in pollen, while each species expressed a mixture of isoforms with at least 4–5 different isoforms. Q-TOF LC-MSE allowed fast screening of Bet v 1 isoforms in pollen by determining the presence and relative abundance of isoforms similar to those with a known high IgE-reactivity (Bet v 1a =PR-10.01A01) and to the hypoallergenic isoform Bet v 1d (=PR-10.01B01). Betula pendula contains a Bet v 1 mixture in which both isoforms with a high and low IgE-reactivity are abundant. The presence of isoforms with high IgE-reactivity is a condition for determining the influence for the allergenicity of this species. Birch species that express isoforms similar to Bet v 1a are predicted to be allergenic as well.
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References
Abe, Y., Kimura, S., Kokubo, T., et al. (1997). Epitope analysis of birch pollen allergen in Japanese subjects. J Allergy Clin Immunol, 17, 485–493.
Ahrazem, O., Jimeno, L., López-Torrejón, G., et al. (2007). Assessing allergen levels in peach and nectarine cultivars. Ann Allergy Asthma Immunol, 99, 42–47.
Atkinson, M.D. (1992). Biological flora of the British Isles: Betula penduala Roth (B. verrucosa Ehrh.) and B. pubescens Ehrh. J Ecol, 80, 837–870.
Bantignies, B., Séguin, J., Muzac, I., et al. (2000). Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots. Plant Mol Biol, 42, 871–881.
Bhalla, P.L., Singh, M.B. (2004). Knocking out expression of plant allergen genes. Methods, 32, 340–345.
Bohle, B., Vieths, S. (2004). Improving diagnostic tests for food allergy with recombinant allergens. Methods, 32, 292–299.
Bolhaar, S.T.H.P., van de Weg, W.E., van Ree, R., et al. (2005). In vivo assessment with prick-to-prick testing and double-blind, placebo-controlled food challenge of allergenicity of apple cultivars. J Allergy Clin Immunol, 116, 1080–1086.
Breiteneder, H., Ebner, C. (2000). Molecular and biochemical classification of plant-derived food allergens. J Allergy Clin Immunol, 106, 27–36.
Breiteneder, H., Pettenburger, K., Bito, A., et al. (1989). The gene coding for the major birch pollen allergen Bet v I, is highly homologous to a pea disease resistance response gene. EMBO Journal, 8, 1935–1938.
Burney, P., Malmberg, E., Chinn, S., et al. (1997). The distribution of total and specific serum IgE in the European Community Respiratory Health Survey. J Allergy Clin Immunol, 99, 314–322.
Carnés, J., Ferrer, A., Fernández-Caldas, E. (2006). Allergenicity of 10 different apple varieties. Ann Allergy Asthma Immunol, 96, 564–570.
Castro, A.J., Alche, J.D., Cuevas, J., et al. (2003). Pollen from different olive tree cultivars contains varying amounts of the major allergen Ole e 1. Int Arch Allergy Immunol, 131, 164–173.
Corsico, R., Falagiani, P., Ariano, R., et al. (2000). An epidemiological survey on the allergological importance of some emerging pollens in Italy. J Invest Allerg Clin, 10, 155–161.
Crimi, E., Voltolini, S., Gianiorio, P., et al. (1990). Effect of seasonal exposure to pollen on specific bronchial sensitivity in allergic patients. J Allergy Clin Immunol, 85, 1014–1019.
Ekramoddoullah, A.K.M., Yu, X.S., Sturrock, R., et al. (2000). Detection and seasonal expression pattern of a pathogenesis-related protein (PR-10) in Douglas-fir (Pseudotsuga menziesii) tissues. Physiol Plant, 110, 240–247.
Eriksson, N.E., Holmén, A., Möller, C., et al. (1998). Sensitization according to skin prick testings in atopic patients with asthma or rhinitis at 24 allergy clinica in Northern Europe and Asia. Allergol Int, 47, 187–196.
Ferreira, F., Hawranek, T., Gruber, P., et al. (2004). Allergic cross-reactivity: From gene to the clinic. Allergy, 59, 243–267.
Ferreira, F., Hirtenlehner, K., Jilek, A., et al. (1996). 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, 599–609.
Feugey, L., Strullu, D. G., Poupard, P., et al. (1999). Induced defense responses limit Hartig net formation in ectomycorrhizal birch roots. New Phytol, 144, 541–547.
Flores, T., Alape-Girón, A., Flores-Díaz, M., et al. (2002). A novel tuber storage protein from the Andean tuber crop oca with antibacterial and antifungal activities. Plant Physiol, 128, 1291–1302.
Frewer, L., Lassen, J., Kettlitz, B., et al. (2004). Societal aspects of genetically modified foods. Food Chem Toxicol, 42, 1181–1193.
Friedl-Hajek, R., Radauer, C., O’Riordain, G., et al. (1999). New Bet v 1 isoforms including a naturally occurring truncated form of the protein derived from Austrian birch pollen. Mol Immunol, 36, 639–645.
Fujimoto, Y., Nagata, R., Fukasawa, H., et al. (1998). Purification and cDNA cloning of cytokinin-specific binding protein from mung bean (Vigna radiata). Eur J Biochem, 258, 794–802.
Gao, Z.S., van de Weg, W.E., Schaart, J.G., et al. (2005). Genomic cloning and linkage mapping of the Mal d 1 (PR-10) gene family in apple (Malus domestica). Theor Appl Genet, 111, 171–183.
Gioulekas, D., Papakosta, D., Damialis, A., et al. (2004). Allergenic pollen records (15 years) and sensitization in patients with respiratory allergy in Thessaloniki, Greece. Allergy, 59, 174–184.
Gislason, D., Björnsson, E., Gislason, T., et al. (1999). Sensitization to airborne and food allergens in Reykjavík (Iceland) and Uppsala (Sweden) — a comparative study.Allergy, 54, 1160–1167.
Hoffmann-Sommergruber, K., Vanek-Krebitz, M., Radauer, C., et al. (1997). Genomic characterization of members of the Bet v 1 family: Genes coding for allergens and pathogenesis-related proteins share intron positions. Gene, 197, 91–100.
Horak, F., Studnicka, M., Gartner, C., et al. (2002). Parental farming protects childen aganist atopy: Longituinal evidence involving skin prick test. Clin Exp Allergy, 32, 1155–1159.
Huang, J.C., Chang,, F.C., Wang, C.S. (1997). Characterization of a lily tapetal transcript that shares sequence similarity with a class of intracellular pathogenesis-related (IPR) proteins. Plant Mol Biol, 34, 681–686.
Jarolim, E., Rumpold, H., Endler, A.T., et al. (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.
Jãgi, R., Janson, C., Björnsson, E., et al. (1998). Atopy and allergic disorders among adults in Tartu, Estonia compared with Uppsala, Sweden. Clin Exp Allergy, 28, 1072–1080.
Koistinen, K.M., Hassinen, V.H., Gynther, P.A.M., et al. (2002). Birch PR-10c is induced by factors causing oxidative stress but appears not to confer tolerance to these agents. New Phytol, 155, 381–391.
Kootstra, H.S., Vlieg-Boerstra, B.J., Dubois, A.E.J. (2007). Assessment of the reduced allergenic properties of the Santana apple. Ann Allergy Asthma, Immunol, 99, 522–525.
Koppelman, S.J., Vlooswijk, R.A.A., Knippels, L.M.J., et al. (2001). Quantification of major peanut allergens Ara h 1 and Ara h 2 in the peanut varieties Runner, Spanish, Virginia, and Valencia, bred in different parts of the world. Allergy, 56, 132–137.
Larsen, J.N. (1995). Isoallergens — significance in allergen exposure and response. ACI News, 7, 141–160.
Latalowa, M., Mietus, M., Uruska, A. (2002). Seasonal variations in the atmospheric Betula pollen count in Gdańsk (southern Baltic coast) in relation to meteorological parameters. Aerobiologia, 18, 33–43.
Le, L.Q., Mahler, V., Lorenz, Y., et al. (2006). Reduced allergenicity of tomato fruits harvested from Lyc e 1-silenced transgenic tomato plants. J Allergy Clin Immunol, 118, 1176–1183.
Liu, J.J., Ekramoddoullah, A.K.M. (2004). Characterization, expression and evolution of two novel subfamilies of Pinus monticola cDNAs encoding pathogenesis-related (PR)-10 proteins. Tree Physiol, 24, 1377–1385.
Liu, J.J., Ekramoddoullah, A.K.M., Yu, X.S. (2003). Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant, 119, 544–553.
Markovic-Housley, Z., Degano, M., Lamba, D., et al. (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.
Marzban, G., Puehringer, H., Dey, R., et al. (2005). Localisation and distribution of the major allergens in apple fruits. Plant Sci, 169, 387–394.
McFadden, H.G., Chapple, R., de Feyter, R., et al. (2001). Expression of pathogenesis-related genes in cotton stems in response to infection by Verticillium dahliae. Physiol Mol Plant Pathol, 58, 119–131.
Meltzer, E.O. (2001). Quality of life in adults and children with allergic rhinitis. J Allergy Clin Immunol, 108, S45–S53.
Moiseyev, G.P., Fedoreyeva, L.I., Zhuravlev, Y.N., et al. (1997). FEBS Letters, 407, 207–210.
Moons, A., Prinsen, E., Bauw, G., et al. (1997). Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell, 9, 2243–2259.
Nowak, D., Heinrich, J., Jörres, R., et al. (1996). Prevalence of respiratory symptoms, bronchial hyperresponsiveness and atopy among adults: West and East Germany. Eur Respir J, 9, 2541–2552.
Park, C.J., Kim, K.J., Shin, R., et al. (2004). Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J, 37, 186–198.
Pauli, G., Oster, J. P., Deviller, P., et al. (1996). Skin testing with recombinant allergens rBet v 1 and birch profilin, rBet v 2: Diagnostic value for birch pollen and associated allergies. J Allergy Clin I mmunol, 97, 1100–1109.
Pinto, M.P., Ribeiro, A., Regalado, A.P., et al. (2005). Expression of Lupinus albus PR-10 proteins during root and leaf development. Biol Plant, 49, 187–193.
Poupard, P., Brunel, N., Leduc, N., et al. (2001). Expression of a Bet v 1 homologue gene encoding a PR 10 protein in birch roots: induction by auxin and localization of the transcripts by in situ hybridization. Aust J Plant Physiol, 28, 57–63.
Poupard, P., Parisi, L., Campion, C., et al. (2003). A wound-and ethephon-inducible PR-10 gene subclass from apple is differentially expressed during infection with a compatible and an incompatible race of Venturia inaequalis. Physiol Mol Plant Pathol, 62, 3–12.
Poupard, P., Strullu, D.G., Simoneau, P. (1998). Two members of the Bet v 1 gene family encoding birch pathogenesis-related proteins display different patterns of root expression and wound-inducibility. Aust J Plant Physiol, 25, 459–464.
Pühringer, H., Moll, D., Hoffmann-Sommergruber, K., et al. (2000). The promoter of an apple Ypr10 gene, encoding the major allergen Mal d 1, is stress-and pathogen-inducible. Plant Sci, 152, 35–50.
Rasmussen, A. (2002). The effects of climate change on the birch pollen season in Denmark. Aerobiologia, 18, 253–265.
Raukas-Kivioja, A., Raukas, E., Loit, H.M., et al. (2003). Allergic sensitization among adults in Tallinn, Estonia. Clin Exp Allergy, 33, 1342–1348.
Richard-Molard, C., Brugière, N., Moille, M., et al. (2004). Molecular characterization of a gene encoding a vegetative storage protein (CiVSP) from Cichorium intybus and its expression in the root and shoot in relation to nitrogen status and pathogen resistance. Physiol Plant, 121, 568–577.
Riedler, J., Eder, W., Oberfeld, G., et al. (2000). Austrian children living on a farm have less hay fever, asthma and allergic sensitization. Clin Exp Allergy, 3, 194–200.
Robert, N., Ferran, J., Breda, C., et al. (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.
Schenk, M..F, Gilissen, L.J.W.J., Esselink, G.D., et al. (2006). Seven different genes encode a diverse mixture of isoforms of Bet v I, the major birch pollen allergen. BMC Genomics, 7, 168.
Schenk, M.F., Thienpont, C.N., Koopman, W.J.M., et al. (2008a). Phylogenetic relationships in Betula (Betulaceae) based on AFLP markers. Tree Genet Genom, 4, 911–924.
Schenk, M.F., Fischer, A.R.H., Frewer, L.J., et al. (2008b). The influence of perceived benefits on acceptance of GM applications for allergy prevention. Health, Risk Soc, 10, 263–282.
Schenk, M.F., Cordewener, J.H.G., America, A.H.P., et al. (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.
Schenk, M.F., Gilissen, L.J.W.J., et al. (2010). Editorial. Mass spectrometry and pollen allergies. Exp Rev Proteom, 7, 627–630.
Schenk, M.F., Cordewener, J.H.G., America, A.H.P., et al. (2011a). Proteomic analysis of the major birch allergen Bet v 1 predicts allergenicity for 15 birch species. J Proteom, 74, 1290–1300.
Schenk, M.F., van der Maas, M.P., Smulders, et al. (2011b). Consumer attitudes towards hypoallergenic apples that alleviate mild apple allergy. Food Qual Pref, 22, 83–91.
Silva, J.C., Denny, R., Dorschel, C.A., et al. (2005). Quantitative proteomic analysis by accurate mass retention time pairs. Anal Chem, 77, 2187–2200.
Silvestri, M., Oddera, S., Rossi, G.A., et al. (1996). Sensitization to airborne allergens in children with respiratory symptoms. Ann Allergy Asthma Immunol, 76, 239–244.
Son, D.Y., Scheurer, S., Hoffmann, A., et al. (1999). Pollen-related food allergy: cloning and immunological analysis of isoforms and mutants of Mal d 1, the major apple allergen, and Bet v 1, the major birch pollen allergen. Eur J Nutrition, 38, 201–215.
Spieksma, F.T.M., Corden, J.M., Detandt, M., et al. (2003). Quantitative trends in annual totals of five common airborne pollen types (Betula, Quercus, Poaceae, Urtica, and Artemisia), at five pollen-monitoring stations in western Europe. Aerobiologia, 19, 171–184.
Srivastava, S., Fristensky, B., Kav, N.N.V. (2004). Constitutive expression of a PR10 protein enhances the germination of Brassica napus under saline conditions. Plant Cell Physiol, 45, 1320–1324.
Sunyer, J., Soriano, J., Antó, J.M., et al. (2000). Sensitization to individual allergens as risk factors for lower FEV1 in young adults. Int J Epidemiol, 29, 125–130.
Swoboda, I., Jilek, A., Ferreira, F., et al. (1995b). Isoforms of Bet v 1, the major birch pollen allergen, analyzed by liquid-chromatography, mass-spectrometry, and cDNA cloning. J Biol Chem, 27, 2607–2613.
Swoboda, I., Scheiner, O., Heberle-Bors, E., et al. (1995c). cDNA cloning and characterization of three genes in the Bet v 1 gene family that encode pathogenesis-related proteins. Plant Cell Environ, 18, 865–874.
Ukaji, N., Kuwabara, C., Takezawa, D., et al. (2004). Accumulation of pathogenesis-related (PR) 10/Bet v 1 protein homologues in mulberry (Morus bombycis Koidz.) tree during winter. Plant Cell Environ, 27, 1112–1121.
Utriainen, M., Kokko, H., Auriola, S., et al. (1998). PR-10 protein is induced by copper stress in roots and leaves of a Cu/Zn tolerant clone of birch, Betula pendula. Plant Cell Environ, 21, 821–828.
Valenta, R., Vrtala, S., Laffer, S., et al. (1998). Allergy reviews series II: Recombinant allergens. J Allergy Clin Immunol, 53, 552–561.
Valjakka, M., Luomala, E.M., Kangasjärvi, J., Vapaavuori, E. (1999). Expression of photosynthesis-and senescence-related genes during leaf development and senescence in silver birch (Betula pendula) seedlings. Physiol Plant, 106, 302–310.
van Ree, R., van Leeuwen, W.A., Akkerdaas, J.H., et al. (1999). How far can we simplify in vitro diagnostics for Fagales tree pollen allergy? A study with three whole pollen extracts and purified natural and recombinant allergens. Clin Exp Allergy, 29, 848–855.
Vartiainen, E., Petäys, T., Haahtela, T., et al. (2002). Allergic diseases, skin prick test responses, and IgE levels in North Karelia, Finland, and the Republic of Karelia, Russia. J Allergy Clin Immunol, 109, 643–648.
von Mutius, E., Weiland, S.K., Fritzsch, C., et al. (1998). Increasing prevalence of hay fever and atopy among children in Leipzig, East Germany. Lancet, 351, 862–866.
Walter, M.H., Liu, J.W., Wünn, J., et al. (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.
Wen, J., Vanek-Krebitz, M., Hoffmann-Sommergruber, K., et al. (1997). The potential of Betv1 homologues, a nuclear multigene family, as phylogenetic markers in flowering plants. Mol Phylogenet Evol, 8, 317–333.
Wensing, M., Akkerdaas, J.H., van Leeuwen, A., et al. (2002). IgE to Bet v 1 and profilin: Cross-reactivity patterns and clinical relevance. J Allergy Clin Immunol, 110, 435–442.
Zechendorf, B. (1994). What the public thinks about biotechnology-Better than synthetic food but worse than organ-transplantation-a survey of opinion polls. Biotechnology, 12, 870–875.
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Smulders, M.J.M., Schenk, M.F., Gilissen, L.J.W.J. (2012). In Search of Hypoallergenic Birch Trees: Characterization of PR-10 Genes from Eight Betula Species and Detection of Bet v 1 Isoforms in Birch Pollen Using a Combined Genomics- Proteomics Approach. In: Multidisciplinary Approaches to Allergies. Advanced Topics in Science and Technology in China. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-31609-8_20
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