Top

Published in:

Open Access 01-12-2017 | Research

Sensitization to PR-10 proteins is indicative of distinctive sensitization patterns in adults with a suspected food allergy

Authors: Mark A. Blankestijn, André C. Knulst, Edward F. Knol, Thuy-My Le, Heike Rockmann, Henny G. Otten, Rob J. B. Klemans

Published in: Clinical and Translational Allergy | Issue 1/2017

Abstract

Background

The extent of co-sensitization within and between food protein families in an adult population is largely unknown. This study aimed to identify the most frequently recognized components in the PR-10 and storage protein family, as well as patterns in (co-)sensitization, in a birch-endemic area.

Methods

Results of ImmunoCAP ISAC, performed during routine care in Dutch adult outpatients suspected of food allergy, were collected.

Results

A total of 305 patients were selected, aged 16–79 years (median 32 years). Sensitization to one or more PR-10 proteins was most frequent (74% of all subjects), followed by 35% to storage protein and 15% to nsLTPs. Within the PR-10 family, subjects were most often sensitized to Bet v 1 (73% of 305), Cor a 1.04 (72%) and Mal d 1 (68%). Sensitization to PR-10s from soy, celery and kiwi occurred distinctively less often (< 55% of Bet v 1 sensitized subjects) compared to other food PR-10s (all > 70%). Subjects sensitized to these ‘less common PR-10 proteins’ were sensitized to more food and inhalant components on the ISAC, compared to subjects sensitized to ‘common PR-10 proteins’ (median 22 vs 13 out of 112, p < 0.0001). Seven subjects demonstrated sensitization to food PR-10 proteins, without concomitant sensitization to pollen PR-10s. Within the storage proteins, sensitization to multiple peanut allergens was most common (on average 3 out of 4).

Conclusions

Sensitization to PR-10 food proteins could occur without concomitant sensitization to common PR-10 from pollen in a subset of subjects. Less commonly recognized PR-10 proteins appear to be an indication of polysensitization.

Available only for authorised users

Canonica GW, Ansotegui IJ, Pawankar R, Schmid-Grendelmeier P, van Hage M, Baena-Cagnani CE, et al. A WAO–ARIA–GA2LEN consensus document on molecular-based allergy diagnostics. World Allergy Organ J. 2013;6:17. https://doi.org/10.1186/1939-4551-6-17.CrossRefPubMedPubMedCentral

van Hage M, Hamsten C, Valenta R. ImmunoCAP Assays: pros and cons in allergology. J Allergy Clin Immunol. 2017. https://doi.org/10.1016/j.jaci.2017.05.008.

Williams P, Önell A, Baldracchini F, Hui V, Jolles S, El-Shanawany T. Evaluation of a novel automated allergy microarray platform compared with three other allergy test methods. Clin Exp Immunol. 2016;184:1–10. https://doi.org/10.1111/cei.12721.CrossRefPubMedPubMedCentral

Ahlgrim C, Gutermuth J, Onell A, Borres MP, Schäffner I, Darsow U, et al. Comparison of molecular multiplex and singleplex analysis of IgE to grass pollen allergens in untreated German grass pollen-allergic patients. J Investig Allergol Clin Immunol. 2015;25:190–5.PubMed

Breiteneder H, Radauer C. A classification of plant food allergens. J Allergy Clin Immunol. 2004;113:821–30. https://doi.org/10.1016/j.jaci.2004.01.779 (quiz 831).CrossRefPubMed

Breiteneder H, Mills ENC. Molecular properties of food allergens. J Allergy Clin Immunol. 2005;115:14–23. https://doi.org/10.1016/j.jaci.2004.10.022 (quiz 24).CrossRefPubMed

Hoffmann-Sommergruber K, Mills ENC. Food allergen protein families and their structural characteristics and application in component-resolved diagnosis: new data from the EuroPrevall project. Anal Bioanal Chem. 2009;395:25–35. https://doi.org/10.1007/s00216-009-2953-z.CrossRefPubMed

Geroldinger-Simic M, Zelniker T, Aberer W, Ebner C, Egger C, Greiderer A, et al. Birch pollen-related food allergy: clinical aspects and the role of allergen-specific IgE and IgG4 antibodies. J Allergy Clin Immunol. 2011;127(616–622):e1. https://doi.org/10.1016/j.jaci.2010.10.027.

Masthoff LJ, Hoff R, Verhoeckx KCM, van Os-Medendorp H, Michelsen-Huisman A, Baumert JL, et al. A systematic review of the effect of thermal processing on the allergenicity of tree nuts. Allergy. 2013;14:983–93. https://doi.org/10.1111/all.12185.CrossRef

10.

Masthoff LJN, Mattsson L, Zuidmeer-Jongejan L, Lidholm J, Andersson K, Akkerdaas JH, et al. Sensitization to Cor a 9 and Cor a 14 is highly specific for a hazelnut allergy with objective symptoms in Dutch children and adults. J Allergy Clin Immunol. 2013;132:393–9. https://doi.org/10.1016/j.jaci.2013.02.024.CrossRefPubMed

11.

Pedrosa M, Boyano-Martínez T, García-Ara MC, Caballero T, Quirce S. Peanut seed storage proteins are responsible for clinical reactivity in Spanish peanut-allergic children. Pediatr Allergy Immunol. 2012;23:654–9. https://doi.org/10.1111/j.1399-3038.2012.01337.x.CrossRefPubMed

12.

Asero R, Mistrello G, Roncarolo D, Amato S, Falagiani P. Analysis of the heat stability of lipid transfer protein from apple. J Allergy Clin Immunol. 2003;112:1009–11. https://doi.org/10.1016/S0091-6749(03)02006-2.CrossRefPubMed

13.

van der Valk JPM, Gerth van Wijk R, Dubois AEJ, de Groot H, Reitsma M, Vlieg-Boerstra B, et al. Multicentre double-blind placebo-controlled food challenge study in children sensitised to cashew nut. PLoS ONE. 2016;11:e0151055. https://doi.org/10.1371/journal.pone.0151055.CrossRefPubMedPubMedCentral

14.

Santos A, Van Ree R. Profilins: mimickers of allergy or relevant allergens? Int Arch Allergy Immunol. 2011;155:191–204. https://doi.org/10.1159/000321178.CrossRefPubMed

15.

Bublin M, Breiteneder H. Cross-reactivity of peanut allergens. Curr Allergy Asthma Rep. 2014;14:426. https://doi.org/10.1007/s11882-014-0426-8.CrossRefPubMedPubMedCentral

16.

van der Valk JPM, J Dubois AE, Gerth van Wijk R, Wichers HJ, de Jong NW. Systematic review on cashew nut allergy. Allergy. 2014;69:692–8. https://doi.org/10.1111/all.12401.CrossRefPubMed

17.

Sirvent S, Cantó B, Gómez F, Blanca N, Cuesta-Herranz J, Canto G, et al. Detailed characterization of Act d 12 and Act d 13 from kiwi seeds: implication in IgE cross-reactivity with peanut and tree nuts. Allergy. 2014. https://doi.org/10.1111/all.12486.PubMed

18.

Masthoff LJ, van Hoffen E, Mattsson L, Lidholm J, Andersson K, Zuidmeer-Jongejan L, et al. Peanut allergy is common among hazelnut-sensitized subjects but is not primarily the result of IgE cross-reactivity. Allergy. 2015;70:265–74. https://doi.org/10.1111/all.12554.CrossRefPubMed

19.

van Hage M, Schmid-Grendelmeier P, Skevaki C, Plebani M, Canonica W, Kleine-Tebbe J, et al. Performance evaluation of ImmunoCAP^® ISAC 112: a multi-site study. Clin Chem Lab Med. 2017;55(4):571–7. https://doi.org/10.1515/cclm-2016-0586.PubMed

20.

Villalta D, Conte M, Asero R, Da Re M, Stella S, Martelli P. Isolated IgE reactivity to native walnut vicilin-like protein (nJug r 2) on ISAC™ microarray is due to cross-reactive carbohydrate epitopes. Clin Chem Lab Med. 2013;51:1991–5. https://doi.org/10.1515/cclm-2013-0027.CrossRefPubMed

21.

Villalta D, Asero R. Sensitization to the pollen pan-allergen profilin. Is the detection of immunoglobulin E to multiple homologous proteins from different sources clinically useful? J Investig Allergol Clin Immunol. 2010;20:591–5.PubMed

22.

Jahn-Schmid B, Radakovics A, Lüttkopf D, Scheurer S, Vieths S, Ebner C, et al. Bet v 1142-156 is the dominant T-cell epitope of the major birch pollen allergen and important for cross-reactivity with Bet v 1-related food allergens. J Allergy Clin Immunol. 2005;116:213–9. https://doi.org/10.1016/j.jaci.2005.04.019.CrossRefPubMed

23.

Roulias A, Pichler U, Hauser M, Himly M, Hofer H, Lackner P, et al. Differences in the intrinsic immunogenicity and allergenicity of Bet v 1 and related food allergens revealed by site-directed mutagenesis. Allergy Eur J Allergy Clin Immunol. 2014;69:208–15. https://doi.org/10.1111/all.12306.CrossRef

24.

Vanekkrebitz M, Hoffmannsommergruber K, Machado MLD, Susani M, Ebner C, Kraft D, et al. Cloning and sequencing of Mal d 1, the major allergen from apple (Malus domestica), and its immunological relationship to Bet v 1, the major birch pollen allergen. Biochem Biophys Res Commun. 1995;214:538–51. https://doi.org/10.1006/bbrc.1995.2320.CrossRef

25.

Lüttkopf D, Müller U, Skov PS, Ballmer-Weber BK, Wüthrich B, Skamstrup Hansen K, et al. Comparison of four variants of a major allergen in hazelnut (Corylus avellana) Cor a 1.04 with the major hazel pollen allergen Cor a 1.01. Mol Immunol. 2002;38:515–25. https://doi.org/10.1016/S0161-5890(01)00087-6.CrossRefPubMed

26.

Mittag D, Akkerdaas J, Ballmer-Weber BK, Vogel L, Wensing M, Becker W-M, et al. Ara h 8, a Bet v 1—homologous allergen from peanut, is a major allergen in patients with combined birch pollen and peanut allergy. J Allergy Clin Immunol. 2004;114:1410–7. https://doi.org/10.1016/j.jaci.2004.09.014.CrossRefPubMed

27.

Oberhuber C, Bulley SM, Ballmer-Weber BK, Bublin M, Gaier S, DeWitt ÅM, et al. Characterization of Bet v 1-related allergens from kiwifruit relevant for patients with combined kiwifruit and birch pollen allergy. Mol Nutr Food Res. 2008. https://doi.org/10.1002/mnfr.200800146.

28.

Westman M, Lupinek C, Bousquet J, Andersson N, Pahr S, Baar A, et al. Early childhood IgE reactivity to pathogenesis-related class 10 proteins predicts allergic rhinitis in adolescence. J Allergy Clin Immunol. 2015;135:1199–206. https://doi.org/10.1016/j.jaci.2014.10.042.CrossRefPubMed

29.

Stemeseder T, Klinglmayr E, Moser S, Lueftenegger L, Lang R, Himly M, et al. Cross-sectional study on allergic sensitization of Austrian adolescents using molecule-based IgE profiling. Allergy. 2017;72:754–63. https://doi.org/10.1111/all.13071.CrossRefPubMed

30.

Bohle B, Zwölfer B, Heratizadeh A, Jahn-Schmid B, Antonia YD, Alter M, et al. Cooking birch pollen-related food: divergent consequences for IgE- and T cell-mediated reactivity in vitro and in vivo. J Allergy Clin Immunol. 2006;118:242–9. https://doi.org/10.1016/j.jaci.2006.03.011.CrossRefPubMed

31.

Tordesillas L, Goswami R, Benedé S, Grishina G, Dunkin D, Järvinen KM, et al. Skin exposure promotes a Th2-dependent sensitization to peanut allergens. J Clin Invest. 2014;124:4965–75. https://doi.org/10.1172/JCI75660.CrossRefPubMedPubMedCentral

32.

Flinterman AE, Akkerdaas JH, den Hartog Jager CF, Rigby NM, Fernandez-Rivas M, Hoekstra MO, et al. Lipid transfer protein-linked hazelnut allergy in children from a non-Mediterranean birch-endemic area. J Allergy Clin Immunol. 2008;121(423–428):e2. https://doi.org/10.1016/j.jaci.2007.10.009.

33.

Datema MR, Zuidmeer-Jongejan L, Asero R, Barreales L, Belohlavkova S, de Blay F, et al. Hazelnut allergy across Europe dissected molecularly: a EuroPrevall outpatient clinic survey. J Allergy Clin Immunol. 2015. https://doi.org/10.1016/j.jaci.2014.12.1949.PubMed

34.

Search results for “Bet v 1-like.” Allergome.org 2017. http://allergome.org/. Accessed 16 May 2017.

35.

Moreno FJ, Clemente A. 2S albumin storage proteins: what makes them food allergens? Open Biochem J. 2008;2:16–28. https://doi.org/10.2174/1874091X00802010016.CrossRefPubMedPubMedCentral

36.

Bublin M, Kostadinova M, Radauer C, Hafner C, Szépfalusi Z, Varga E-M, et al. IgE cross-reactivity between the major peanut allergen Ara h 2 and the nonhomologous allergens Ara h 1 and Ara h 3. J Allergy Clin Immunol. 2013;132:118–24. https://doi.org/10.1016/j.jaci.2013.01.022.CrossRefPubMed

37.

Lehmann K, Schweimer K, Reese G, Randow S, Suhr M, Becker W-M, et al. Structure and stability of 2S albumin-type peanut allergens: implications for the severity of peanut allergic reactions. Biochem J. 2006;395:463–72. https://doi.org/10.1042/BJ20051728.CrossRefPubMedPubMedCentral

38.

Koppelman SJ, de Jong GAH, Laaper-Ertmann M, Peeters KABM, Knulst AC, Hefle SL, et al. Purification and immunoglobulin E-binding properties of peanut allergen Ara h 6: evidence for cross-reactivity with Ara h 2. Clin Exp Allergy. 2005;35:490–7. https://doi.org/10.1111/j.1365-2222.2005.02204.x.CrossRefPubMed

39.

Klemans RJB, Knol EF, Michelsen-Huisman A, Pasmans SGMA, de Kruijf-Broekman W, Bruijnzeel-Koomen CAFM, et al. Components in soy allergy diagnostics: Gly m 2S albumin has the best diagnostic value in adults. Allergy. 2013;68:1396–402. https://doi.org/10.1111/all.12259.CrossRefPubMed

40.

Blankestijn MA, Blom WM, Otten HG, Baumert JL, Taylor SL, Bruijnzeel-Koomen CAFM, et al. Specific IgE to Jug r 1 has no additional value compared with extract-based testing in diagnosing walnut allergy in adults. J Allergy Clin Immunol. 2017;139(688–690):e4. https://doi.org/10.1016/j.jaci.2016.07.026.

41.

Klemans RJB, Broekman HCHP, Knol EF, Bruijnzeel-Koomen CAFM, Otten HG, Pasmans SGMA, et al. Ara h 2 is the best predictor for peanut allergy in adults. J Allergy Clin Immunol Pract. 2013;1:632–8. https://doi.org/10.1016/j.jaip.2013.07.014.CrossRefPubMed

42.

Werfel T, Asero R, Ballmer-Weber BK, Beyer K, Enrique E, Knulst AC, et al. Position paper of the EAACI: food allergy due to immunological cross-reactions with common inhalant allergens. Allergy Eur J Allergy Clin Immunol. 2015;70:1079–90. https://doi.org/10.1111/all.12666.CrossRef

43.

Ebo DG, Bridts CH, Verweij MM, De Knop KJ, Hagendorens MM, De Clerck LS, et al. Sensitization profiles in birch pollen-allergic patients with and without oral allergy syndrome to apple: lessons from multiplexed component-resolved allergy diagnosis. Clin Exp Allergy. 2010;40:339–47. https://doi.org/10.1111/j.1365-2222.2009.03345.x.CrossRefPubMed

44.

Skamstrup Hansen K, Vieths S, Vestergaard H, Skov PS, Bindslev-Jensen C, Poulsen LK. Seasonal variation in food allergy to apple. J Chromatogr B Biomed Sci Appl. 2001;756:19–32. https://doi.org/10.1016/S0378-4347(01)00068-8.CrossRefPubMed

45.

Somville MA, Machiels J, Gilles JG, Saint-Remy JM. Seasonal variation in specific IgE antibodies of grass-pollen hypersensitive patients depends on the steady state IgE concentration and is not related to clinical symptoms. J Allergy Clin Immunol. 1989;83:486–94. https://doi.org/10.1016/0091-6749(89)90138-3.CrossRefPubMed

46.

Scala E, Alessandri C, Bernardi ML, Ferrara R, Palazzo P, Pomponi D, et al. Cross-sectional survey on immunoglobulin E reactivity in 23,077 subjects using an allergenic molecule-based microarray detection system. Clin Exp Allergy. 2010;40:911–21. https://doi.org/10.1111/j.1365-2222.2010.03470.x.CrossRefPubMed

Title: Sensitization to PR-10 proteins is indicative of distinctive sensitization patterns in adults with a suspected food allergy
Authors: Mark A. Blankestijn
André C. Knulst
Edward F. Knol
Thuy-My Le
Heike Rockmann
Henny G. Otten
Rob J. B. Klemans
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Clinical and Translational Allergy / Issue 1/2017
Electronic ISSN: 2045-7022
DOI: https://doi.org/10.1186/s13601-017-0177-4

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Sensitization to PR-10 proteins is indicative of distinctive sensitization patterns in adults with a suspected food allergy

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2017

Better recognition, diagnosis and management of non-IgE-mediated cow’s milk allergy in infancy: iMAP—an international interpretation of the MAP (Milk Allergy in Primary Care) guideline

Comparison of atopy patch testing to skin prick testing for diagnosing mite-induced atopic dermatitis: a systematic review and meta-analysis

Multi-morbidities of allergic rhinitis in adults: European Academy of Allergy and Clinical Immunology Task Force Report

Quality indicators for the acute and long-term management of anaphylaxis: a systematic review

Approach to the diagnosis of drug hypersensitivity reactions: similarities and differences between Europe and North America

CHRODIS criteria applied to the MASK (MACVIA-ARIA Sentinel NetworK) Good Practice in allergic rhinitis: a SUNFRAIL report