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Research Article | Open Access

Site-specific N-glycosylation characterization and allergenicity analysis of globulin-1 S allele from wheat

Linglin Fua, Rongrong Wanga, Jinru Zhoua,b, Chong Wanga, Yanbo Wanga()
Food Safety Key Laboratory of Zhejiang Province, School of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou 310018, China
Zhejiang Engineering Research Institute of Food & Drug Quality and Safety, School of Management and E-Business, Zhejiang Gongshang University, Hangzhou 310018, China

Peer review under responsibility of KeAi Communications Co., Ltd.

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Abstract

N-glycans in many proteins are of great concern because of their strong association with food allergies. Triticum aestivum (bread wheat), a major food crop, is known as one of the "Big Eight" allergenic groups. However, little research has been done about N-glycans in wheat glycoproteins. In this study, a soluble wheat glycoprotein was purified from wheat and further identified as globulin-1 S allele (GSA). The wheat GSA displayed significant IgE-binding activity. Moreover, one N-glycosylation site and 6 kinds of N-glycans were identified by mass spectrometry, including 3 high mannose types and 3 complex types. Furthermore, the IgE-binding activity of wheat GSA is proved to be reduced by the removal of N-glycan, thermal treatment (temperatures > 80 ℃), and strong acidic treatment (pH 3.0). These findings would provide a better understanding of the effects of N-glycosylation, thermal treatment, and acidic treatment on the molecular characteristics of GSA, and further provide new insights into the development of hypoallergenic wheat products.

Keywords

Triticum aestivumAllergenGlycoproteinN-glycansN-glycosylationC18-RPLC-MS/MS

References

[1]

T.W. Song, J.Y. Hong, K.E. Lee, et al., IgE reactivity to carbohydrate moieties of glycoproteins in wheat allergy, Allergy Asthma Proc. 36(3) (2015) 192-199. https://doi.org/10.2500/aap.2015.36.3815.

Crossref Google Scholar
[2]

M.E. Levin, C.L. Gray, J. Marrugo, Food allergy: international and developing world perspectives, Curr. Pediatr. Rep. 4(3) (2016) 129-137. https://doi.org/10.1007/s40124-016-0104-5.

Crossref Google Scholar
[3]

M. Calvani, I. Berti, A. Fiocchi, et al., Oral food challenge: safety, adherence to guidelines and predictive value of skin prick testing, Pediatr. Allergy Immunol. 23(8) (2012) 755-761. https://doi.org/10.1111/pai.12016.

Crossref Google Scholar
[4]

X.Y. Wang, Y. Zhuang, T.T. Ma, et al., Prevalence of self-reported food allergy in six regions of inner Mongolia, northern China: a population-based survey, Med. Sci. Monit. 24 (2018) 1902-1911. https://doi.org/10.12659/msm.908365.

Crossref Google Scholar
[5]

L. Li, C. Wang, S. Qiang, et al., Mass spectrometric analysis of n-glycoforms of soybean allergenic glycoproteins separated by SDS-PAGE, J. Agric. Food Chem. 64(39) (2016) 7367-7376. https://doi.org/10.1021/acs.jafc.6b02773.

Crossref Google Scholar
[6]

M. Kamalakannan, L.M. Chang, G. Grishina, et al., Identification and characterization of DC-SIGN-binding glycoproteins in allergenic foods, Allergy 71(8) (2016) 1145-1155. https://doi.org/10.1111/all.12873.

Crossref Google Scholar
[7]

G.A. Rabinovich, M.A. Toscano, Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation, Nat. Rev. Immunol. 9(5) (2009) 338-352. https://doi.org/10.1038/nri2536.

Crossref Google Scholar
[8]

A. Homann, G. Schramm, U. Jappe, Glycans and glycan-specific IgE in clinical and molecular allergology: sensitization, diagnostics, and clinical symptoms, J. Allergy Clin. Immunol. 140(2) (2017) 356-368. https://doi.org/10.1016/j.jaci.2017.04.019.

Crossref Google Scholar
[9]

A. Yang, H. Deng, Q. Zu, et al., Structure characterization and IgE-binding of soybean 7S globulin after enzymatic deglycosylation, Int. J. Food Prop. 21(1) (2018) 186-197. https://doi.org/10.1080/10942912.2018.1437628.

Crossref Google Scholar
[10]

Z. Zhang, H. Xiao, X. Zhang, et al., Insight into the effects of deglycosylation and glycation of shrimp tropomyosin on in vivo allergenicity and mast cell function, Food Funct. 10(7) (2019) 3934-3941. https://doi.org/10.1039/c9fo00699k.

Crossref Google Scholar
[11]

S.B. Lehrer, W.E. Horner, G. Reese, Why are some proteins allergenic? implications for biotechnology, Crit. Rev. Food Sci. Nutr. 36(6) (1996) 553-564. https://doi.org/10.1080/10408399609527739.

Crossref Google Scholar
[12]

R. van Ree, M. Cabanes-Macheteau, J. Akkerdaas, et al., Beta(1, 2)-xylose and alpha(1, 3)-fucose residues have a strong contribution in IgE binding to plant glycoallergens, J. Biol. Chem. 275(15) (2000) 11451-11458. https://doi.org/10.1074/jbc.275.15.11451.

Crossref Google Scholar
[13]

W. Hemmer, M. Focke, D. Kolarich, et al., Identification by immunoblot of venom glycoproteins displaying immunoglobulin E-binding N-glycans as cross-reactive allergens in honeybee and yellow jacket venom, Clin. Exp. Allergy 34(3) (2004) 460-469. https://doi.org/10.1111/j.1365-2222.2004.01897.x.

Crossref Google Scholar
[14]

W.S. Veraverbeke, J.A. Delcour, Wheat protein composition and properties of wheat glutenin in relation to breadmaking functionality, Crit. Rev. Food Sci. Nutr. 42(3) (2002) 179-208. https://doi.org/10.1080/10408690290825510.

Crossref Google Scholar
[15]

L. Gao, W. Ma, J. Chen, et al., Characterization and comparative analysis of wheat high molecular weight glutenin subunits by SDS-PAGE, RP-HPLC, HPCE, and MALDI-TOF-MS, J. Agric. Food Chem. 58(5) (2010) 2777-2786. https://doi.org/10.1021/jf903363z.

Crossref Google Scholar
[16]

M. Laurière, I. Bouchez, C. Doyen, et al., Identification of glycosylated forms of wheat storage proteins using two-dimensional electrophoresis and blotting, Electrophoresis 17(3) (1996) 497-501. https://doi.org/10.1002/elps.1150170312.

Crossref Google Scholar
[17]

S.J. Maleki, S.Y. Chung, E.T. Champagne, et al., The effects of roasting on the allergenic properties of peanut proteins, J. Allergy Clin. Immunol. 106(4) (2000) 763-768. https://doi.org/10.1067/mai.2000.109620.

Crossref Google Scholar
[18]

B.M. Ehn, B. Ekstrand, U. Bengtsson, et al., Modification of IgE binding during heat processing of the cow's milk allergen beta-lactoglobulin, J. Agric. Food Chem. 52(5) (2004) 1398-1403. https://doi.org/10.1021/jf0304371.

Crossref Google Scholar
[19]

R. Kasera, A.B. Singh, R. Kumar, et al., Effect of thermal processing and γ-irradiation on allergenicity of legume proteins, Food Chem. Toxicol. 50(10) (2012) 3456-3461. https://doi.org/10.1016/j.fct.2012.07.031.

Crossref Google Scholar
[20]

K.S. Hansen, B.K. Ballmer-Weber, D. Lüttkopf, et al., Roasted hazelnutsallergenic activity evaluated by double-blind, placebo-controlled food challenge, Allergy 58(2) (2003) 132-138. https://doi.org/10.1034/j.1398-9995.2003.23959.x.

Crossref Google Scholar
[21]

L.K. Kucek, L.D. Veenstra, P. Amnuaycheewa, et al., A grounded guide to gluten: how modern genotypes and processing impact wheat sensitivity, Compr. Rev. Food Sci. Food Saf. 14(3) (2015) 285-302. https://doi.org/10.1111/1541-4337.12129.

Crossref Google Scholar
[22]

R. Kazemi, A. Taheri-Kafrani, A. Motahari, et al., Allergenicity reduction of bovine milk β-lactoglobulin by proteolytic activity of lactococcus lactis BMC12C and BMC19H isolated from Iranian dairy products, Int. J. Biol. Macromol. 112 (2018) 876-881. https://doi.org/10.1016/j.ijbiomac.2018.02.044.

Crossref Google Scholar
[23]

X.H. Sun, K.X. Zhu, H.M. Zhou, Protein extraction from defatted wheat germ by reverse micelles: optimization of the forward extraction, J. Cereal Sci. 48(3) (2008) 829-835. https://doi.org/10.1016/j.jcs.2008.06.006.

Crossref Google Scholar
[24]

H.Y. Park, T.J. Yoon, H.H. Kim, et al., Changes in the antigenicity and allergenicity of ovalbumin in chicken egg white by N-acetylglucosaminidase, Food Chem. 217 (2017) 342-345. https://doi.org/10.1016/j.foodchem.2016.08.112.

Crossref Google Scholar
[25]

N.K. Singh, K.W. Shepherd, G.B. Cornish, A simplified SDS-PAGE procedure for separating LMW subunits of glutenin, Journal of Cereal Science 14(3) 1991 203-208. https://doi.org/10.1016/S0733-5210(09)80039-8.

Crossref Google Scholar
[26]

Y.X. Zhang, H.L. Chen, S.J. Maleki, et al., Purification, characterization, and analysis of the allergenic properties of myosin light chain in Procambarus clarkii, J. Agric. Food Chem. 63(27) (2015) 6271-6282. https://doi.org/10.1021/acs.jafc.5b01318.

Crossref Google Scholar
[27]

H.W. Shen, M.J. Cao, Q.F. Cai, et al., Purification, cloning, and immunological characterization of arginine kinase, a novel allergen of Octopus fangsiao, J. Agric. Food Chem. 60(9) (2012) 2190-2199. https://doi.org/10.1021/jf203779w.

Crossref Google Scholar
[28]

S. Pahr, C. Constantin, N.G. Papadopoulos, et al., α-Purothionin, a new wheat allergen associated with severe allergy, J. Allergy Clin. Immunol. 132(4) (2013) 1000-3.e1-4. https://doi.org/10.1016/j.jaci.2013.05.016.

Crossref Google Scholar
[29]

Z. Zhang, H. Xiao, X. Zhang, et al., Conformation, allergenicity and human cell allergy sensitization of tropomyosin from Exopalaemon modestus: effects of deglycosylation and Maillard reaction, Food Chem. 276 (2019) 520-527. https://doi.org/10.1016/j.foodchem.2018.10.032.

Crossref Google Scholar
[30]

W. Song, M.G. Henquet, R.A. Mentink, et al., N-glycoproteomics in plants: perspectives and challenges, J. Proteomics 74(8) (2011) 1463-1474. https://doi.org/10.1016/j.jprot.2011.05.007.

Crossref Google Scholar
[31]

S. Mercx, N. Smargiasso, F. Chaumont, et al., Inactivation of the β(1, 2)-xylosyltransferase and the α(1, 3)-fucosyltransferase genes in Nicotiana tabacum BY-2 cells by a Multiplex CRISPR/Cas9 strategy results in glycoproteins without plant-specific glycans, Front. Plant Sci. 8 (2017) 403. https://doi.org/10.3389/fpls.2017.00403.

Crossref Google Scholar
[32]

T. Liu, Y. Li, J. Xu, et al., N-glycosylation and enzymatic activity of the rHuPH20 expressed in Chinese hamster ovary cells, Anal. Biochem. 632 (2021) 114380. https://doi.org/10.1016/j.ab.2021.114380.

Crossref Google Scholar
[33]

A. Rump, R. Risti, M.L. Kristal, et al., Dual ELISA using SARS-CoV-2 nucleocapsid protein produced in E. coli and CHO cells reveals epitope masking by N-glycosylation, Biochem. Biophys. Res. Commun. 534 (2021) 457-460. https://doi.org/10.1016/j.bbrc.2020.11.060.

Crossref Google Scholar
[34]

A.L. Lopata, R.E. O'Hehir, S.B. Lehrer, Shellfish allergy, Clin. Exp. Allergy 40(6) (2010) 850-858. https://doi.org/10.1111/j.1365-2222.2010.03513.x.

Crossref Google Scholar
[35]

R. Ayuso, G. Grishina, L. Bardina, et al., Myosin light chain is a novel shrimp allergen, Lit v 3, J. Allergy Clin. Immunol. 122(4) (2008) 795-802. https://doi.org/10.1016/j.jaci.2008.07.023.

Crossref Google Scholar
[36]

M.L. Bernardi, D. Picone, L. Tuppo, et al., Physico-chemical features of the environment affect the protein conformation and the immunoglobulin E reactivity of kiwellin (Act d 5), Clin. Exp. Allergy 40(12) (2010) 1819-1826. https://doi.org/10.1111/j.1365-2222.2010.03603.x.

Crossref Google Scholar
[37]

A. Taheri-Kafrani, J.C. Gaudin, H. Rabesona, et al., Effects of heating and glycation of beta-lactoglobulin on its recognition by IgE of sera from cow milk allergy patients, J. Agric. Food Chem. 57(11) (2009) 4974-4982. https://doi.org/10.1021/jf804038t.

Crossref Google Scholar
Food Science and Human Wellness
Volume 12 Issue 5,
September 2023
Pages 1601-1608
DOI: 10.1016/j.fshw.2023.02.020
Cite this article:
Fu L, Wang R, Zhou J, et al. Site-specific N-glycosylation characterization and allergenicity analysis of globulin-1 S allele from wheat. Food Science and Human Wellness, 2023, 12(5): 1601-1608. https://doi.org/10.1016/j.fshw.2023.02.020
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