Structure, Immunogenicity, and IgE Cross-Reactivity Among Walnut and Peanut Vicilin-Buried Peptides

Overview

Journal J Agric Food Chem

Specialties Chemistry
Nutritional Sciences

Date 2022 Feb 9

PMID 35139305

Authors

Alexander C Y Foo

Jacqueline B Nesbit

Stephen A Y Gipson

Hsiaopo Cheng

Pierre Bushel

Eugene F DeRose

Catherine H Schein

Suzanne S Teuber

Barry K Hurlburt

Soheila J Maleki

Geoffrey A Mueller

Affiliations

Soon will be listed here.

Abstract

Vicilin-buried peptides (VBPs) from edible plants are derived from the N-terminal leader sequences (LSs) of seed storage proteins. VBPs are defined by a common α-hairpin fold mediated by conserved CxxxCxCxxxC motifs. Here, peanut and walnut VBPs were characterized as potential mediators of both peanut/walnut allergenicity and cross-reactivity despite their low (∼17%) sequence identity. The structures of one peanut (AH1.1) and 3 walnut (JR2.1, JR2.2, JR2.3) VBPs were solved using solution NMR, revealing similar α-hairpin structures stabilized by disulfide bonds with high levels of surface similarity. Peptide microarrays identified several peptide sequences primarily on AH1.1 and JR2.1, which were recognized by peanut-, walnut-, and dual-allergic patient IgE, establishing these peanut and walnut VBPs as potential mediators of allergenicity and cross-reactivity. JR2.2 and JR2.3 displayed extreme resilience against endosomal digestion, potentially hindering epitope generation and likely contributing to their reduced allergic potential.

Citing Articles

Structural and Stability Analysis of GRP Family Allergens Pru p 7 and Cry j 7, Which Cause Pollen and Food Allergy Syndrome.

Zheng J, Kumeta H, Kumaki Y, Iizuka T, Yoshikawa I, Hanaoka A Biomolecules. 2025; 15(2).

PMID: 40001535 PMC: 11852976. DOI: 10.3390/biom15020232.

Precision engineering for localization, validation, and modification of allergenic epitopes.

Pomes A, Smith S, Chruszcz M, Mueller G, Brackett N, Chapman M J Allergy Clin Immunol. 2024; 153(3):560-571.

PMID: 38181840 PMC: 10939758. DOI: 10.1016/j.jaci.2023.12.017.

Food Allergens of Plant Origin.

Zhang Y, Che H, Li C, Jin T Foods. 2023; 12(11).

PMID: 37297475 PMC: 10252803. DOI: 10.3390/foods12112232.

Structure and IgE Cross-Reactivity among Cashew, Pistachio, Walnut, and Peanut Vicilin-Buried Peptides.

Foo A, Nesbit J, Gipson S, DeRose E, Cheng H, Hurlburt B J Agric Food Chem. 2023; 71(6):2990-2998.

PMID: 36728846 PMC: 10402694. DOI: 10.1021/acs.jafc.2c07061.

Still SDAPing Along: 20 Years of the Structural Database of Allergenic Proteins.

Schein C, Negi S, Braun W Front Allergy. 2022; 3:863172.

PMID: 35386653 PMC: 8974667. DOI: 10.3389/falgy.2022.863172.

References

Foo A, Mueller G . Abundance and Stability as Common Properties of Allergens. Front Allergy. 2022; 2:769728. PMC: 8974735. DOI: 10.3389/falgy.2021.769728. View

Weinberger T, Sicherer S . Current perspectives on tree nut allergy: a review. J Asthma Allergy. 2018; 11:41-51. PMC: 5875412. DOI: 10.2147/JAA.S141636. View

Kabasser S, Pratap K, Kamath S, Taki A, Dang T, Koplin J . Identification of vicilin, legumin and antimicrobial peptide 2a as macadamia nut allergens. Food Chem. 2021; 370:131028. PMC: 7614219. DOI: 10.1016/j.foodchem.2021.131028. View

Downs M, Semic-Jusufagic A, Simpson A, Bartra J, Fernandez-Rivas M, Rigby N . Characterization of low molecular weight allergens from English walnut (Juglans regia). J Agric Food Chem. 2014; 62(48):11767-75. DOI: 10.1021/jf504672m. View

Wang F, Robotham J, Teuber S, Tawde P, Sathe S, Roux K . Ana o 1, a cashew (Anacardium occidental) allergen of the vicilin seed storage protein family. J Allergy Clin Immunol. 2002; 110(1):160-6. DOI: 10.1067/mai.2002.125208. View

Ivanciuc O, Midoro-Horiuti T, Schein C, Xie L, Hillman G, Goldblum R . The property distance index PD predicts peptides that cross-react with IgE antibodies. Mol Immunol. 2008; 46(5):873-83. PMC: 2651743. DOI: 10.1016/j.molimm.2008.09.004. View

Micsonai A, Wien F, Bulyaki E, Kun J, Moussong E, Lee Y . BeStSel: a web server for accurate protein secondary structure prediction and fold recognition from the circular dichroism spectra. Nucleic Acids Res. 2018; 46(W1):W315-W322. PMC: 6031044. DOI: 10.1093/nar/gky497. View

Cabrera A, Randall T, Ogburn R, Mebrahtu B, Johnson J, Foo A . Are allergens more abundant and/or more stable than other proteins in pollens and dust?. Allergy. 2019; 75(5):1267-1269. PMC: 7237293. DOI: 10.1111/all.14121. View

Nesbit J, Schein C, Braun B, Gipson S, Cheng H, Hurlburt B . Epitopes with similar physicochemical properties contribute to cross reactivity between peanut and tree nuts. Mol Immunol. 2020; 122:223-231. DOI: 10.1016/j.molimm.2020.03.017. View

10.

Guntert P, Buchner L . Combined automated NOE assignment and structure calculation with CYANA. J Biomol NMR. 2015; 62(4):453-71. DOI: 10.1007/s10858-015-9924-9. View

11.

Nolde S, Vassilevski A, Rogozhin E, Barinov N, Balashova T, Samsonova O . Disulfide-stabilized helical hairpin structure and activity of a novel antifungal peptide EcAMP1 from seeds of barnyard grass (Echinochloa crus-galli). J Biol Chem. 2011; 286(28):25145-53. PMC: 3137087. DOI: 10.1074/jbc.M110.200378. View

12.

Willison L, Tawde P, Robotham J, Penney 4th R, Teuber S, Sathe S . Pistachio vicilin, Pis v 3, is immunoglobulin E-reactive and cross-reacts with the homologous cashew allergen, Ana o 1. Clin Exp Allergy. 2008; 38(7):1229-38. DOI: 10.1111/j.1365-2222.2008.02998.x. View

13.

Burks A, Shin D, Cockrell G, Stanley J, Helm R, Bannon G . Mapping and mutational analysis of the IgE-binding epitopes on Ara h 1, a legume vicilin protein and a major allergen in peanut hypersensitivity. Eur J Biochem. 1997; 245(2):334-9. DOI: 10.1111/j.1432-1033.1997.t01-1-00334.x. View

14.

Tordesillas L, Goswami R, Benede S, Grishina G, Dunkin D, Jarvinen K . Skin exposure promotes a Th2-dependent sensitization to peanut allergens. J Clin Invest. 2014; 124(11):4965-75. PMC: 4347216. DOI: 10.1172/JCI75660. View

15.

Micsonai A, Wien F, Kernya L, Lee Y, Goto Y, Refregiers M . Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy. Proc Natl Acad Sci U S A. 2015; 112(24):E3095-103. PMC: 4475991. DOI: 10.1073/pnas.1500851112. View

16.

Wichers H, De Beijer T, Savelkoul H, van Amerongen A . The major peanut allergen Ara h 1 and its cleaved-off N-terminal peptide; possible implications for peanut allergen detection. J Agric Food Chem. 2004; 52(15):4903-7. DOI: 10.1021/jf049697o. View

17.

Ghosh D, Mueller G, Schramm G, Edwards L, Petersen A, London R . Primary identification, biochemical characterization, and immunologic properties of the allergenic pollen cyclophilin cat R 1. J Biol Chem. 2014; 289(31):21374-85. PMC: 4118102. DOI: 10.1074/jbc.M114.559971. View

18.

Ng Y, Yang Y, Sze K, Zhang X, Zheng Y, Shaw P . Structural characterization and anti-HIV-1 activities of arginine/glutamate-rich polypeptide Luffin P1 from the seeds of sponge gourd (Luffa cylindrica). J Struct Biol. 2011; 174(1):164-72. DOI: 10.1016/j.jsb.2010.12.007. View

19.

Garcia B, Lizaso M . Cross-reactivity syndromes in food allergy. J Investig Allergol Clin Immunol. 2011; 21(3):162-70. View

20.

Aalberse R, Mueller G, Derksen N, Aalberse J, Edwards L, Pomes A . Identification of the amino-terminal fragment of Ara h 1 as a major target of the IgE-binding activity in the basic peanut protein fraction. Clin Exp Allergy. 2019; 50(3):401-405. PMC: 7047623. DOI: 10.1111/cea.13554. View