AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (1.5 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Whey protein hydrolysates alleviated food allergy in mice by balancing the Th1/Th2 pathway and increasing IgA antibody production

Xinkun Yin1Xiaohong Guo2Hui Hong1Yongkang Luo1Yuqing Tan1( )
Key Laboratory of Functional Dairy, China Agricultural University, College of Food Science and Nutritional Engineering, Beijing 100083, China
Xindongkang Nutrition Technology Co., Ltd., Shijiazhuang 052160, China
Show Author Information

Abstract

Whey protein, a by-product of cheese processing, is ubiquitously applied in infant formula. Nevertheless, it contains β-lactoglobulin, an allergenic component that can be enzymatically hydrolyzed to destroy its allergenic epitopes and antigenicity. The whey protein hydrolysate (WPH) obtained through enzymatic hydrolysis exhibits a wide range of biological activities. However, its utilization in preventing whey protein food allergies has received limited research attention. This study aimed to examine the preventive effect of WPH intervention on whey protein-induced food allergy in BALB/c mice. The results showed that WPH intervention notably mitigated the development of allergic reactions in mice with whey protein-induced food allergies. The intervention with WPH significantly reduced the symptom score of allergic reactions in mice with whey protein-induced food allergies (39.38%, P < 0.01). Early intervention with WPH also led to a significant reduction in the serum levels of antibodies and related cytokines, including IgE, histamine, IgG, and monocyte chemotactic protein-1 (MCP-1) in mice (P < 0.05). A potential mechanism for alleviating allergic reactions was identified from the proteomic findings. WPH was found to upregulate the Th1 differentiation pathway and IgA secretion pathway by increasing MHC II protein expression, thereby alleviating allergic reactions to whey protein in food. Regarding the gut microbiome, WPH intervention led to a decrease in the relative abundance of harmful bacteria, including Prevotellaceae_UCG-001, and Alloprevotella (5.4% and 2.3%, respectively; P< 0.05). It increased the relative abundance of beneficial bacteria such as Turicibacter, Roseburia, and Alistips (3.8%, 0.6%, and 1.4%, respectively; P < 0.05). The present study suggests early WPH intervention may attenuate whey protein-induced food allergic reactions.

References

[1]

Á. M. Candreva, P. L. Smaldini, A. Cauerhff, et al., A novel approach to ameliorate experimental milk allergy based on the oral administration of a short soy cross-reactive peptide, Food Chem. 346 (2021) 128926. https://doi.org/10.1016/j.foodchem.2020.128926.

[2]

M. D. Martinis, M. M. Sirufo, M. Suppa, L. Ginaldi, New perspectives in food allergy, Int. J. Mol. Sci. 21 (2020) 1474. https://doi.org/10.3390/ijms21041474.

[3]
H, Yang, Y. Z. Qu, Y. R. Gao, S. Y. Sun, et al., Role of the dietary components in food allergy: a comprehensive review, Food Chem. (2022) 386. https://doi.org/10.1016/j.foodchem.2022.132762.
[4]

T. G. Liu, S. Navarro, A. L. Lopata, Current advances of murine models for food allergy, Mol. Immunol. 70 (2016) 104–117. https://doi.org/10.1016/j.molimm.2015.11.011.

[5]

P. Çetinkaya, M. Ocak, U. Sahiner, et al., Food protein-induced allergic proctocolitis may have distinct phenotypes, Ann. Allergy Asthma Immunol. 126 (2022) 75–82.

[6]

G. W. Smithers, Whey-ing up the options: yesterday, today and tomorrow, Int. Dairy J. 48 (2015) 2–14. https://doi.org/10.1016/j.idairyj.2015.01.011.

[7]

H. Hochwallner, U. Schulmeister, I. Swoboda, et al., Cow’s milk allergy: From allergens to new forms of diagnosis, therapy and prevention, Methods 66 (2014) 22–33. https://doi.org/10.1016/j.ymeth.2013.08.005.

[8]

K. Mao, D. Li, J. Liu, et al., Investigation of serum IL-12, IL-16, and IL-17A as diagnostic biomarkers in children with cow’s milk protein allergy, Allergol. Immunopathol. 50 (2022) 162–168. https://doi.org/10.15586/aei.v50i5.592.

[9]

C. Sebastiani, C. Arcangeli, M. Torricelli, et al., Marker-assisted selection of dairy cows for β-casein gene A2 variant, Ital. J. Food Sci. 34 (2022) 21–27. https://doi.org/10.15586/ijfs.v34i2.2178.

[10]

A. C. Gomes-Santos, R. C. Fonseca, L. Lemos, et al., Hydrolyzed whey protein prevents the development of food allergy to β-lactoglobulin in sensitized mice, Cell Immunol. 298 (2015) 47–53. https://doi.org/10.1016/j.cellimm.2015.09.001.

[11]

A. R. Ballegaard, K. L. Bøgh, Intestinal protein uptake and IgE-mediated food allergy, Food Res. Int. 163 (2023) 112150. https://doi.org/10.1016/j.foodres.2022.112150.

[12]

A. Brandelli, D. Daroit, A. Corrêa, Whey as a source of peptides with remarkable biological activities, Food Res. Int. 73 (2015) 149–161. https://doi.org/10.1016/j.foodres.2015.01.016.

[13]

D. Lozano-Ojalvo, L. Pérez-Rodríguez, A. Pablos-Tanarro, et al., Pepsin treatment of whey proteins under high pressure produces hypoallergenic hydrolysates, Innov. Food Sci. Emerg. Technol. 43 (2017) 154–162. https://doi.org/10.1016/j.ifset.2017.07.032.

[14]

Á. M. Candreva, P. L. Smaldini, R. Curciarello, et al., The major soybean allergen Gly m Bd 28K induces hypersensitivity reactions in mice sensitized to cow’s milk proteins, J. Agric. Food Chem. 64 (2016) 1590–1599. https://doi.org/10.1021/acs.jafc.5b05623.

[15]

I. Ahmed, H. Lin, Z. 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.

[16]

J. C. Saldanha, D. L. Gargiulo, S. S. Silva, et al., A model of chronic IgE-mediated food allergy in ovalbumin-sensitized mice, Braz. J. Med. Biol. Res. 37 (2004) 809–816. https://doi.org/10.1590/s0100-879x2004000600005.

[17]

Y. Liang, H. Zhang, L. Tian, et al., Gut microbiota and metabolic profile as affected by Maillard reaction products derived from bighead carp meat hydrolysates with galactose and galacto-oligosaccharides during in vitro pig fecal fermentation, Food Chem. 398 (2023) 133905. https://doi.org/10.1016/j.foodchem.2022.133905.

[18]

L. Christie, R. J. Hine, J. G. Parker, et al., Food allergies in children affect nutrient intake and growth, J. Am. Diet. Assoc. 102 (2002) 1648–1651. https://doi.org/10.1016/S0002-8223(02)90351-2.

[19]

N. C. Carvalho, T. B. Pessato, L. G. Fernandes, et al., Physicochemical characteristics and antigenicity of whey protein hydrolysates obtained with and without pH control, Int. Dairy J. 71 (2017) 24–34. https://doi.org/10.1016/j.idairyj.2017.02.007.

[20]

R. R. Bansode, P. D. Randolph, N. J. Plundrich, et al., Peanut protein-polyphenol aggregate complexation suppresses allergic sensitization to peanut by reducing peanut-specific IgE in C3H/HeJ mice, Food Chem. 299 (2019) 125025. https://doi.org/10.1016/j.foodchem.2019.125025.

[21]

K. B. Ahn, J. H. Jeon, S. S. Kang, et al., IgE in the absence of allergen induces the expression of monocyte chemoattractant protein-1 in the rat basophilic cell-line RBL-2H3, Mol. Immunol. 62 (2014) 114–121. https://doi.org/10.1016/j.molimm.2014.06.008.

[22]

P. Conti, X. Pang, W. Boucher, et al., Impact of Rantes and MCP-1 chemokines on in vivo basophilic cell recruitment in rat skin injection model and their role in modifying the protein and mRNA levels for histidine decarboxylase, Blood 89 (1997) 4120–4127. https://doi.org/10.1182/blood.V89.11.4120.

[23]

X. Liang, H. Yang, J. Sun, Effects of enzymatic treatments on the hydrolysis and antigenicity reduction of natural cow milk, Food Sci. Nutr. 9 (2021) 985–993. https://doi.org/10.1002/fsn3.2066.

[24]

K. Adel-Patient, S. Wavrin, H. Bernard, et al., Oral tolerance and Treg cells are induced in BALB/c mice after gavage with bovine β-lactoglobulin, Allergy 66 (2011) 1312–1321. https://doi.org/10.1111/j.1398-9995.2011.02653.x.

[25]

X. Liang, Z. Wang, H. Yang, et al., Evaluation of allergenicity of cow milk treated with enzymatic hydrolysis through a mouse model of allergy, J. Dairy Sci. 105 (2022) 1039–1050. https://doi.org/10.3168/jds.2021-20686.

[26]

T. Vo, B. Ryu, S. Kim, Purification of novel anti-inflammatory peptides from enzymatic hydrolysate of the edible microalgal Spirulina maxima, J. Funct. Foods. 5 (2013) 1336–1346. https://doi.org/10.1016/j.jff.2013.05.001.

[27]
L. Ramachandra, D. Simmons, C. V. Harding, MHC molecules and microbial antigen processing in phagosomes, Cur. Opin. Immunol. 21 (2009) 98–104. https://doi.org/10.1016/j.coi.2009.01.001.
[28]

D. von Bubnoff, E. Geiger, T. Bieber, Antigen-presenting cells in allergy, J. Allergy Clin. Immunol. 108 (2001) 329–339. https://doi.org/10.1067/mai.2001.117457.

[29]

B. W. Ewanchuk, R. M. Yates, The phagosome and redox control of antigen processing, Free Radical Bio. Med. 125 (2018) 53–61. https://doi.org/10.1016/j.freeradbiomed.2018.03.040.

[30]

R. Czolk, J. Klueber, M. Sørensen, et al., IgE-mediated peanut allergy: current and novel predictive biomarkers for clinical phenotypes using multi-omics approaches, Front. Immunol. 11 (2021) 594350. https://doi.org/10.3389/fimmu.2020.594350.

[31]

A. N. Hegazy, M. Peine, C. Helmstetter, et al., Interferons direct Th2 cell reprogramming to generate a stable GATA-3+T-bet+ cell subset with combined Th2 and Th1 cell functions, Immunity 32 (2010) 116–128. https://doi.org/10.1016/j.immuni.2009.12.004.

[32]

S. H. Sicherer, H. A. Sampson, Food allergy: a review and update on epidemiology, pathogenesis, diagnosis, prevention, and management, J. Allergy Clin. Immunol. 141 (2018) 41–58. https://doi.org/10.1016/j.jaci.2017.11.003.

[33]

J. Y. Ma, J. Zhang, Q. H. Li, et al., Oral administration of a mixture of probiotics protects against food allergy via induction of CD103+ dendritic cells and modulates the intestinal microbiota, J. Funct. Foods 55 (2019) 65–75. https://doi.org/10.1016/j.jff.2019.02.010.

[34]

K. Atarashi, T. Tanoue, K. Oshima, Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota, Nature. 500 (2013) 232–236. https://doi.org/10.1038/nature12331.

[35]

D. J. Morrison, T. Preston, Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism, Gut Microbes. 7 (2016) 189–200. https://doi.org/10.1080/19490976.2015.1134082.

[36]
E. Stephen-Victor, T. A. Chatila, Regulation of oral immune tolerance by the microbiome in food allergy, Curr. Opin. Immunol, 60 (2019) 141–147. https://doi.org/10.1016/j.coi.2019.06.001.
[37]

S. Bunyavanich, N. Shen, A. Grishin, et al., Early-life gut microbiome composition and milk allergy resolution, J. Allergy Clin. Immun. 138 (2016) 1122–1130. https://doi.org/10.1016/j.jaci.2016.03.041.

[38]

M. Dzidic, T. R. Abrahamsson, A. Artacho, et al., Oral microbiota maturation during the first 7 years of life in relation to allergy development, Allergy 73 (2018) 2000–2011. https://doi.org/10.1111/all.13449.

[39]

J. Wang, H. Lu, L. Yu, et al., Aggravation of airway inflammation in RSV-infected asthmatic mice following infection-induced alteration of gut microbiota, Authorea 10 (2021) 5084–5097. https://doi.org/10.22541/au.160253797.76907107/v1.

[40]

Z. P. Kang, M. X. Wang, T. T. Wu, et al., Curcumin ameliorated dextran sulfate sodium-induced colitis via regulating the homeostasis of DCs and Treg and improving the composition of the gut microbiota, J. Funct. Foods 86 (2021) 104716. https://doi.org/10.1016/j.jff.2021.104716.

[41]

J. Li, C. Zou, Y. Liu, Amelioration of ovalbumin-induced food allergy in mice by targeted rectal and colonic delivery of cyanidin-3-O-glucoside, Foods 11 (2022) 1542. https://doi.org/10.3390/foods11111542.

[42]

Y. Furusawa, Y. Obata, S. Fukuda, Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells, Nature 504 (2013) 446–450. https://doi.org/10.1038/nature12721.

[43]

Z. L. Wang, J. H. Zhong, X. Y. Meng, et al., The gut microbiome-immune axis as a target for nutrition-mediated modulation of food allergy, Trends Food Sci. Technol. 114 (2021) 116–132. https://doi.org/10.1016/j.jpgs.2021.05.021.

[44]
B. C. Roberto, P. Lorella, N. Rita, et al., Gut microbiome as target for innovative strategies against food allergy, Front. Immunol. 10 (2019) 191. https://www.frontiersin.org/articles/10.3389/fimmu.2019.00191.
Food Science of Animal Products
Article number: 9240046
Cite this article:
Yin X, Guo X, Hong H, et al. Whey protein hydrolysates alleviated food allergy in mice by balancing the Th1/Th2 pathway and increasing IgA antibody production. Food Science of Animal Products, 2023, 1(4): 9240046. https://doi.org/10.26599/FSAP.2023.9240046

468

Views

70

Downloads

0

Crossref

Altmetrics

Received: 08 November 2023
Revised: 01 December 2023
Accepted: 10 January 2024
Published: 04 March 2024
© Beijing Academy of Food Sciences 2023.

Food Science of Animal Products published 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/).

Return