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Open Access

Laccase/caffeic acid-catalyzed crosslinking coupled with galactomannan alters the conformational structure of ovalbumin and alleviates Th2-mediated allergic asthma

Ishfaq Ahmeda,bSuidong OuyangaShengquan Wua,cHaochang Songa,cMiaoyuan Zhanga,cRenxing Luoa,cPeishan Lua,cJiaqi Denga,cTingting ZhengaYanyan WangaXinguang LiuaGonghua Huanga( )
Guangdong Provincial Key Laboratory of Medical Molecular Diagnostics, The First Dongguan Affiliated Hospital, Guangdong Medical University, Dongguan 523808, China
Haide College, Ocean University of China, Laoshan Campus, Qingdao 266100, China
School of Medical Technology, Guangdong Medical University, Dongguan 523808, China

Peer review under responsibility of Tsinghua University Press.

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Highlights

• Lac/CA crosslinking plus Man conjugation altered the structure of OVA.

• Lac-Man/OVA revealed enhanced the gastrointestinal digestibility.

• Lac-Man/OVA modulated BMDCs maturation and suppressed proinflammatory cytokines.

• Lac/CA crosslinking plus Man conjugation effectively ameliorated allergic asthma.

Graphical Abstract

Abstract

Ovalbumin (OVA) is the major allergenic protein that can induce T helper 2 (Th2)-allergic reactions, for which current treatment options are inadequate. In this study, we developed a polymerized hypoallergenic OVA product via laccase/caffeic acid (Lac/CA)-catalyzed crosslinking in conjunction with galactomannan (Man). The formation of high molecular weight crosslinked polymers and the IgG-binding were analyzed by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) and Western blotting. The study indicated that Lac/CA-catalyzed crosslinking plus Man conjugation substantially altered secondary and tertiary structures of OVA along with the variation in surface hydrophobicity. Gastrointestinal digestion stability assay indicated that crosslinked OVA exhibited less resistance in simulated gastric fl uid (SGF) and simulated intestinal fluid (SIF). Mouse model study indicated that Lac-Man/OVA ameliorated eosinophilic airway inflammatory response and efficiently downregulated the expression of Th2-related cytokines (interleukin (IL)-4, IL-5, and IL-13), and upregulated IFN-γ and IL-10 expression. Stimulation of bone marrow-derived dendritic cells with Lac-Man/OVA suppressed the expression of phenotypic maturation markers (CD80 and CD86) and MHC class Ⅱ molecules, and suppressed the expression levels of proinfl ammatory cytokines. The knowledge obtained in the present study offers an effective way to acquire a hypoallergenic OVA product that can have a therapeutic effect in alleviating OVA-induced allergic asthma.

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References

[1]

H. Renz, K.J. Allen, S.H. Sicherer, et al., Food allergy, Nat. Rev. Dis. Primers 4(1) (2018) 1-20. https://doi.org/10.1038/nrdp.2017.98.

[2]

H.A. Sampson, L. O’Mahony, A.W. Burks, et al., Mechanisms of food allergy. J. Allergy Clin. Immunol. 141(1) (2018) 11-19. https://doi.org/10.1016/j.jaci.2017.11.005.

[3]

S.M. Jones, A.W. Burks, Food allergy, New Eng. J. Med. 377(12) (2017) 1168-1176. https://doi.org/10.1056/nejmcp1611971.

[4]

S.S. Athari, Targeting cell signaling in allergic asthma, Signal Transduct. Target Ther. 4(1) (2019) 1-19. https://doi.org/10.1038/s41392-019-0079-0.

[5]

P.S. Foster, S. Maltby, H.F. Rosenberg, et al., Modeling TH2 responses and airway inflammation to understand fundamental mechanisms regulating the pathogenesis of asthma, Immunol. Rev. 278(1) (2017) 20-40. https://doi.org/10.1111/imr.12549.

[6]

M. Kubo, Innate and adaptive type 2 immunity in lung allergic inflammation, Immunol. Rev. 278(1) (2017) 162-172. https://doi.org/10.1111/imr.12557.

[7]

M. Botha, W. Basera, H.E. Facey-Thomas, et al., Rural and urban food allergy prevalence from the South African Food Allergy (SAFFA) study, J. Allergy Clin. Immunol. 143(2) (2018) 662-668. https://doi.org/10.1016/j.jaci.2018.07.023.

[8]

R.L. Peters, J.J. Koplin, L.C. Gurrin, et al., The prevalence of food allergy and other allergic diseases in early childhood in a population-based study: HealthNuts age 4-year follow-up, J. Allergy Clin. Immunol. 140(1) (2017) 145-153. https://doi.org/10.1016/j.jaci.2017.02.019.

[9]

X. Ma, R. Liang, Q. Xing, et al., Can food processing produce hypoallergenic egg?, J. Food Sci. 85(9) (2020) 2635-2644. https://doi.org/10.1111/1750-3841.15360.

[10]

D.K. Ingawale, S.K. Mandlik, S.S. Patel, Combination of sarsasapogenin and fluticasone attenuates ovalbumin-induced airway inflammation in a mouse asthma model, Immunopharmacol. Immunotoxicol. 42(2) (2020) 128-137. https://doi.org/10.1080/08923973.2020.1728541.

[11]

P. Rupa, Y. Mine, Comparison of glycated ovalbumin-monosaccharides in the attenuation of ovalbumin-induced allergic response in a BALB/c mouse model, J. Agric. Food Chem. 67(29) (2019) 8138-8148. https://doi.org/10.1021/acs.jafc.9b02132.

[12]

T.T. Zhang, Z.Y. Hu, Y.W. Cheng, et al., Changes in allergenicity of ovalbumin in vitro and in vivo on conjugation with quercetin, J. Agric. Food Chem. 68(13) (2020) 4027-4035. https://doi.org/10.1021/acs.jafc.0c00461.

[13]

T.B. Casale, J.R. Stokes, Immunotherapy: what lies beyond, J. Allergy Clin. Immunol. 133(3) (2014) 612-619. https://doi.org/10.1016/j.jaci.2014.01.007.

[14]

O. Pfaar, I. Agache, F. de Blay, et al., Perspectives in allergen immunotherapy: 2019 and beyond, Allergy 74(S108) (2019) 3-25. https://doi.org/10.1111/all.14077.

[15]

S. Sirvent, I. Soria, C. Cirauqui, et al., Novel vaccines targeting dendritic cells by coupling allergoids to nonoxidized mannan enhance allergen uptake and induce functional regulatory T cells through programmed death ligand 1, J. Allergy Clin. Immunol. 138(2) (2016) 558-567. https://doi.org/10.1016/j.jaci.2016.02.029.

[16]

I. Ahmed, H. Chen, J. Li, et al., Enzymatic crosslinking and food allergenicity: a comprehensive review, Compr. Rev. Food Sci. Food Saf. 20(6) (2021) 5856-5879. https://doi.org/10.1111/1541-4337.12855.

[17]

S. Isaschar-Ovdat, A. Fishman, Crosslinking of food proteins mediated by oxidative enzymes: a review, Trends Food Sci. Technol. 72 (2018) 134-143. https://doi.org/10.1016/J.TIFS.2017.12.011.

[18]

L. Lv, S. Tian, I. Ahmed, et al., Effect of laccase-catalyzed cross-linking on the structure and allergenicity of Paralichthys olivaceus parvalbumin mediated by propyl gallate, Food Chem. 297 (2019) 124972. https://doi.org/10.1016/j.foodchem.2019.124972.

[19]

I. Ahmed, H. Lin, L.L. Xu, et al., Immunomodulatory effect of laccase/ caffeic acid and transglutaminase in alleviating shrimp tropomyosin (Met e 1) allergenicity, J. Agric. Food Chem. 68(29) (2020) 7765-7778. https://doi.org/10.1021/acs.jafc.0c02366.

[20]

P. Rupa, S. Nakamura, S. Katayama, et al., Attenuation of allergic immune response phenotype by mannosylated egg white in orally induced allergy in BALB/c mice, J. Agric. Food Chem. 62(39) (2014) 9479-9487. https://doi.org/10.1021/jf503109r.

[21]

P. Rupa, S. Nakamura, S. Katayama, et al., Effects of ovalbumin glycoconjugates on alleviation of orally induced egg allergy in mice via dendritic-cell maturation and T-cell activation, Mol. Nutr. Food Res. 58(2) (2014) 405-417. https://doi.org/10.1002/mnfr.201300067.

[22]

E.E. Weinberger, M. Himly, J. Myschik, et al., Generation of hypoallergenic neoglycoconjugates for dendritic cell targeted vaccination: a novel tool for specific immunotherapy, J. Contr. Release 165(2) (2013) 101-109. https://doi.org/10.1016/j.jconrel.2012.11.002.

[23]

I. Ahmed, L.T. Lv, H. Lin, et al., Effect of tyrosinase-aided crosslinking on the IgE binding potential and conformational structure of shrimp (Metapenaeus ensis) tropomyosin, Food Chem. 248 (2018) 287-295. https://doi.org/10.1016/j.foodchem.2017.12.071.

[24]

G.L. Xing, C.V.L. Giosafatto, X. Rui, et al., Microbial transglutaminase-mediated polymerization in the presence of lactic acid bacteria affects antigenicity of soy protein component present in bio-tofu, J. Funct. Food 53 (2019) 292-298. https://doi.org/10.1016/j.jff.2018.12.035.

[25]

I. Ahmed, H. Lin, Z.X. Li, et al., Tyrosinase/caffeic acid cross-linking alleviated shrimp (Metapenaeus ensis) tropomyosin-induced allergic responses by modulating the Th1/Th2 immunobalance, Food Chem. 340 (2021) 127948. https://doi.org/10.1016/j.foodchem.2020.127948.

[26]

M.M. Han, R. Hu, J.Y. Ma, et al., Fas signaling in dendritic cells mediates Th2 polarization in HDM-induced allergic pulmonary inflammation, Front. Immunol. 9 (2018) 3045. https://doi.org/10.3389/fimmu.2018.03045.

[27]

I. Ahmed, J.J. Ma, Z.X. Li, et al., Effect of tyrosinase and caffeic acid crosslinking of turbot parvalbumin on the digestibility, and release of mediators and cytokines from activated RBL-2H3 cells, Food Chem. 300 (2019) 125209. https://doi.org/10.1016/j.foodchem.2019.125209.

[28]

F.Z. Yuan, I. Ahmed, L.T. Lv, et al., Impacts of glycation and transglutaminase-catalyzed glycosylation with glucosamine on the conformational structure and allergenicity of bovine β-lactoglobulin, Food Funct. 9(7) (2018) 3944-3955. https://doi.org/10.1039/c8fo00909k.

[29]

L.N. Zheng, H. Lin, R. Pawar, et al., Mapping IgE binding epitopes of major shrimp (Penaeus monodon) allergen with immunoinformatics tools, Food Chem. Toxicol. 49(11) (2011) 2954-2960. https://doi.org/10.1016/j.fct.2011.07.043.

[30]
A.J. Barrett, J.F. Rawlings, Woessner, N.D., Handbook of Proteolytic Enzymes, (3rd Eds.), Academic Press, 2013. https://doi.org/10.1016/C2009-1-60990-4.
[31]

L. Böhm, J. Maxeiner, H. Meyer-Martin, et al., IL-10 and regulatory T cells cooperate in allergen-specific immunotherapy to ameliorate allergic asthma, J. Immunol. 194(3) (2015) 887-897. https://doi.org/10.4049/jimmunol.1401612.

[32]

C.Y. Chiang, C.C. Lee, C.K. Fan, et al., Osthole treatment ameliorates Th2-mediated allergic asthma and exerts immunomodulatory effects on dendritic cell maturation and function, Cell. Mol. Immunol. 14(11) (2017) 935-947. https://doi.org/10.1038/cmi.2017.71.

[33]

G. Pelaia, A. Vatrella, M.T. Busceti, et al., Cellular mechanisms underlying eosinophilic and neutrophilic airway inflammation in asthma, Mediat. Inflam. 2015 (2015) 879783. https://doi.org/10.1155/2015/879783.

[34]

S. Yoo, S.J. Ha, Generation of tolerogenic dendritic cells and their therapeutic applications, Immune Netw. 16(1) (2016) 52-60. https://doi.org/10.4110/in.2016.16.1.52.

[35]

X.J. Ma, W.J. Yan, H. Zheng, et al., Regulation of IL-10 and IL-12 production and function in macrophages and dendritic cells, F1000Research. 4 (2015). https://doi.org/10.12688/f1000research.7010.1.

[36]

M.B. Lutz, Therapeutic potential of semi-mature dendritic cells for tolerance induction, Front. Immunol. 3(123) (2012) 1-9. https://doi.org/10.3389/fimmu.2012.00123.

Food Science and Human Wellness
Pages 1962-1973
Cite this article:
Ahmed I, Ouyang S, Wu S, et al. Laccase/caffeic acid-catalyzed crosslinking coupled with galactomannan alters the conformational structure of ovalbumin and alleviates Th2-mediated allergic asthma. Food Science and Human Wellness, 2024, 13(4): 1962-1973. https://doi.org/10.26599/FSHW.2022.9250163

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Received: 09 September 2022
Revised: 21 November 2022
Accepted: 29 January 2023
Published: 20 May 2024
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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