Pea (Pisum sativum) allergy in children: Pis s 1 is an immunodominant major pea allergen and presents IgE binding sites with potential diagnostic value.


Journal

Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology
ISSN: 1365-2222
Titre abrégé: Clin Exp Allergy
Pays: England
ID NLM: 8906443

Informations de publication

Date de publication:
05 2020
Historique:
received: 02 09 2019
revised: 07 02 2020
accepted: 15 02 2020
pubmed: 23 2 2020
medline: 13 8 2021
entrez: 21 2 2020
Statut: ppublish

Résumé

Food allergy to pea (Pisum sativum) has been rarely studied in children at the clinical and molecular levels. To elucidate the allergenic relevance and diagnostic value of pea 7S globulin Pis s 1, nsLTP, and 2S albumins PA1 and PA2 in children. Children with pea-specific IgE ≥ 0.35 kU 19 pea-sensitized children were included, 14 with doctors' diagnosed allergy and 5 with tolerance to pea (median age 3.5 and 4.5 years, respectively). 11/14 (78%) pea-allergic and 1/5 (20%) tolerant children were sensitized to Pis s 1. Under the reducing conditions of immunoblot analysis, IgE binding to rPA1 was negligible, sensitization to rPA2 and nsLTP undetectable. Compared to pea total protein extract, rPis s 1 displayed on average 58% IgE binding capacity and a 20-fold higher mediator release potency. Selected Pis s 1-related peptides displayed IgE binding in pea-allergic but not in pea-tolerant children. In this study group, Pis s 1 is a major immunodominant allergen in pea-allergic children. Evidence for sensitization to nsLTP and 2S albumins was low but requires further verification with regard to conformational epitopes. Recombinant Pis s 1 and related peptides which were exclusively recognized by pea-allergic children may improve in vitro diagnosis of pea allergy once verified in prospective studies with larger study groups.

Sections du résumé

BACKGROUND
Food allergy to pea (Pisum sativum) has been rarely studied in children at the clinical and molecular levels.
OBJECTIVE
To elucidate the allergenic relevance and diagnostic value of pea 7S globulin Pis s 1, nsLTP, and 2S albumins PA1 and PA2 in children.
METHODS
Children with pea-specific IgE ≥ 0.35 kU
RESULTS
19 pea-sensitized children were included, 14 with doctors' diagnosed allergy and 5 with tolerance to pea (median age 3.5 and 4.5 years, respectively). 11/14 (78%) pea-allergic and 1/5 (20%) tolerant children were sensitized to Pis s 1. Under the reducing conditions of immunoblot analysis, IgE binding to rPA1 was negligible, sensitization to rPA2 and nsLTP undetectable. Compared to pea total protein extract, rPis s 1 displayed on average 58% IgE binding capacity and a 20-fold higher mediator release potency. Selected Pis s 1-related peptides displayed IgE binding in pea-allergic but not in pea-tolerant children.
CONCLUSIONS AND CLINICAL RELEVANCE
In this study group, Pis s 1 is a major immunodominant allergen in pea-allergic children. Evidence for sensitization to nsLTP and 2S albumins was low but requires further verification with regard to conformational epitopes. Recombinant Pis s 1 and related peptides which were exclusively recognized by pea-allergic children may improve in vitro diagnosis of pea allergy once verified in prospective studies with larger study groups.

Identifiants

pubmed: 32078204
doi: 10.1111/cea.13590
doi:

Substances chimiques

Allergens 0
Plant Proteins 0
Immunoglobulin E 37341-29-0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

625-635

Informations de copyright

© 2020 The Authors. Clinical & Experimental Allergy published by John Wiley & Sons Ltd.

Références

Tulbek MC, Lam RSH, Wang Y, Asavajaru P, Lam A. Pea. In: SR Nadathur, JPD Wanasundara, L Scanlin, eds., Sustainable Protein Sources. Amsterdam: Elsevier; 2017:145-164.
Lavine E, Ben-Shoshan M. Anaphylaxis to hidden pea protein, A Canadian pediatric case series. J Allergy Clin Immunol Pract. 2019;7:2070-2071.
Richard C, Jacquenet S, Sergeant P, Moneret-Vautrin DA. Cross-reactivity of a new food ingredient, dun pea, with legumes, and risk of anaphylaxis in legume allergic children. Eur Ann Allergy Clin Immunol. 2015;47:118-125.
Smits M, Le T-M, Welsing P, Houben G, Knulst A, Verhoeckx K. Legume protein consumption and the prevalence of legume sensitization. Nutrients. 2018;10(1545):2-14.
Cabanillas B, Jappe U, Novak N. Allergy to peanut, soybean, and other legumes, recent advances in allergen characterization, stability to processing and IgE cross-reactivity. Mol Nutr Food Res. 2018;62(1):1-9.
Regulation (EU) No 1169/2011. Regulation (EU) No 1169/2011 of the European Parliament and of the Council of 25 October 2011 on the provision of food information to consumers, amending Regulations (EC) No 1924/2006 and (EC) No 1925/2006 of the European Parliament and of the Council, and repealing Commission Directive 87/250/EEC, Council Directive 90/496/EEC, Commission Directive 1999/10/EC, Directive 2000/13/EC of the European Parliament and of the Council, Commission Directives 2002/67/EC and 2008/5/EC and Commission Regulation (EC) No 608/2004 Text with EEA relevance OJ L 304, 22.11.2011; 18-63.
Klemans RJB, Liu X, Knulst AC, et al. IgE binding to peanut components by four different techniques, Ara h 2 is the most relevant in peanut allergic children and adults. Clin Exp Allergy. 2013;43:967-974.
Beyer K, Grabenhenrich L, Härtl M, et al. Predictive values of component-specific IgE for the outcome of peanut and hazelnut food challenges in children. Allergy. 2015;70:90-98.
Wensing M, Knulst AC, Piersma S, O’Kane F, Knol EF, Koppelman SJ. Patients with anaphylaxis to pea can have peanut allergy caused by cross-reactive IgE to vicilin (Ara h 1). J Allergy Clin Immunol. 2003;111:420-424.
Bähr M, Fechner A, Kaatz M, Jahreis G. Skin prick test reactivity to lupin in comparison to peanut, pea, and soybean in atopic and non-atopic German subjects, A preliminary cross-sectional study. Immun Inflamm Dis. 2014;2:114-120.
Tzitzikas EN, Vincken J-P, de Groot J, Gruppen H, Visser RGF. Genetic variation in pea seed globulin composition. J Agric Food Chem. 2006;54:425-433.
Sanchez-Monge R, Lopez-Torrejón G, Pascual CY, Varela J, Martin-Esteban M, Salcedo G. Vicilin and convicilin are potential major allergens from pea. Clin Exp Allergy. 2004;34:1747-1753.
Croy RR, Gatehouse JA, Tyler M, Boulter D. The purification and characterization of a third storage protein (convicilin) from the seeds of pea (Pisum sativum L.). Biochem J. 1980;191:509-516.
Bown D, Ellis TH, Gatehouse JA. The sequence of a gene encoding convicilin from pea (Pisum sativum L.) shows that convicilin differs from vicilin by an insertion near the N-terminus. Biochem J. 1988;251:717-726.
Bogdanov IV, Shenkarev ZO, Finkina EI, et al. A novel lipid transfer protein from the pea Pisum sativum, Isolation, recombinant expression, solution structure, antifungal activity, lipid binding, and allergenic properties. BMC Plant Biol. 2016;16(107):1-17.
Pastorello EA, Farioli L, Pravettoni V, et al. The major allergen of peach (Prunus persica) is a lipid transfer protein. J Allergy Clin Immunol. 1999;103:520-526.
Malley A, Baecher L, Mackler B, Perlman F. The isolation of allergens from the green pea. J Allergy Clin Immunol. 1975;56:282-290.
Sell M, Steinhart H, Paschke A. Influence of maturation on the alteration of allergenicity of green pea (Pisum sativum L.). J Agric Food Chem. 2005;53:1717-1722.
Higgins TJ, Beach LR, Spencer D, et al. cDNA and protein sequence of a major pea seed albumin (PA 2, Mr≈26 000). Plant Mol Biol. 1987;8:37-45.
Higgins TJ, Chandler PM, Randall PJ, et al. Gene structure, protein structure, and regulation of the synthesis of a sulfur-rich protein in pea seeds. J Biol Chem. 1986;261:11124-11130.
Croy RR, Hoque MS, Gatehouse JA, Boulter D. The major albumin proteins from pea (Pisum sativum L.). Purification and some properties. Biochem J. 1984;218:795-803.
Vioque J, Clemente A, Sánchez-Vioque R, Pedroche J, Bautista J, Millán F. Comparative study of Chickpea and Pea Pa2 Albumins. J Agric Food Chem. 1998;46:3609-3613.
Vioque J, Sánchez-Vioque R, Clemente A, Pedroche J, Bautista J, Millán F. Purification and partial characterization of chickpea 2S albumin. J Agric Food Chem. 1999;47:1405-1409.
Sampson HA, Gerth van Wijk R, Bindslev-Jensen C, et al. Standardizing double-blind, placebo-controlled oral food challenges: American Academy of Allergy, Asthma & Immunology-European Academy of Allergy and Clinical Immunology PRACTALL consensus report. J Allergy Clin Immunol. 2012;130:1260-1274.
Sampson HA. Anaphylaxis and emergency treatment. Pediatrics. 2003;111:1601-1608.
Gubesch M, Theler B, Dutta M, et al. Strategy for allergenicity assessment of ‘natural novel foods’, Clinical and molecular investigation of exotic vegetables (water spinach, hyacinth bean and Ethiopian eggplant). Allergy. 2007;62:1243-1250.
Albrecht M, Alessandri S, Conti A, et al. High level expression, purification and physico- and immunochemical characterisation of recombinant Pen a 1, A major allergen of shrimp. Mol Nutr Food Res. 2008;52(Suppl 2):S186-195.
Vogel L, Lüttkopf D, Hatahet L, Haustein D, Vieths S. Development of a functional in vitro assay as a novel tool for the standardization of allergen extracts in the human system. Allergy. 2005;60:1021-1028.
Kühne Y, Reese G, Ballmer-Weber BK, et al. A novel multipeptide microarray for the specific and sensitive mapping of linear IgE-binding epitopes of food allergens. Int Arch Allergy Immunol. 2015;166:213-224.
Saeed AI, Sharov V, White J, et al. TM4, A free, open-source system for microarray data management and analysis. BioTechniques. 2003;34:374-378.
Hansen CS, Dufva M, Bøgh KL, et al. Linear epitope mapping of peanut allergens demonstrates individualized and persistent antibody-binding patterns. J Allergy Clin Immunol. 2016;138:1728-1730.
Maruyama N, Katsube T, Wada Y, et al. The roles of the N-linked glycans and extension regions of soybean beta-conglycinin in folding, assembly and structural features. Eur J Biochem. 1998;258:854-862.
Lehmann K, Hoffmann S, Neudecker P, Suhr M, Becker W-M, Rösch P. High-yield expression in Escherichia coli, purification, and characterization of properly folded major peanut allergen Ara h 2. Protein Expr Purif. 2003;31:250-259.
Gatehouse JA, Lycett GW, Croy RR, Boulter D. The post-translational proteolysis of the subunits of vicilin from pea (Pisum sativum L.). Biochem J. 1982;207:629-632.
Klemans RJB, Knol EF, Michelsen-Huisman A, et al. Components in soy allergy diagnostics, Gly m 2S albumin has the best diagnostic value in adults. Allergy. 2013;68:1396-1402.
Ebisawa M, Brostedt P, Sjölander S, Sato S, Borres MP, Ito K. Gly m 2S albumin is a major allergen with a high diagnostic value in soybean-allergic children. J Allergy Clin Immunol. 2013;132:976-978.e1-5.
Peeters KABM, Koppelman SJ, van Hoffen E, et al. Does skin prick test reactivity to purified allergens correlate with clinical severity of peanut allergy? Clin Exp Allergy. 2007;37:108-115.
Blanc F, Adel-Patient K, Drumare M-F, Paty E, Wal J-M, Bernard H. Capacity of purified peanut allergens to induce degranulation in a functional in vitro assay, Ara h 2 and Ara h 6 are the most efficient elicitors. Clin Exp Allergy. 2009;39:1277-1285.

Auteurs

Jasmin Popp (J)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

Valérie Trendelenburg (V)

Department of Pediatric Pulmonology, Immunology and Intensive Care Medicine, Charité Universitätsmedizin Berlin, Berlin, Germany.

Bodo Niggemann (B)

Department of Pediatric Pulmonology, Immunology and Intensive Care Medicine, Charité Universitätsmedizin Berlin, Berlin, Germany.

Stefanie Randow (S)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

Elke Völker (E)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

Lothar Vogel (L)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

Andreas Reuter (A)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

Jelena Spiric (J)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

Dirk Schiller (D)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

Kirsten Beyer (K)

Department of Pediatric Pulmonology, Immunology and Intensive Care Medicine, Charité Universitätsmedizin Berlin, Berlin, Germany.

Thomas Holzhauser (T)

Division of Allergology, Paul-Ehrlich-Institut, Langen, Germany.

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