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Research Article | Open Access

Allergen degradation of bee pollen by lactic acid bacteria fermentation and its alleviatory effects on allergic reactions in BALB/c mice

Shuting Yina,1Qiangqiang Lia,1( )Yuxiao TaoaEnning ZhouaKun WangbWanwen ChencXiangxin LiaLiming Wua,( )
Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China
Department of Animal Science, McGill University, Quebec H9X 3V9, Canada
State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi 214122, China

1 These authors have contributed equally to this work.

Peer review under responsibility of Tsinghua University Press.

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Graphical Abstract

Abstract

Food allergy as a global health problem threatens food industry. Bee pollen (BP) is a typical food with allergenic potentials, although it performs various nutritional/pharmacological functions to humans. In this study, lactic acid bacteria (LAB) were used to ferment Brassica napus BP for alleviating its allergenicity. Four novel allergens (glutaredoxin, oleosin-B2, catalase and lipase) were identified with significant decreases in LAB-fermented BP (FBP) than natural BP by proteomics. Meanwhile, metabolomics analysis showed significant increases of 28 characteristic oligopeptides and amino acids in FBP versus BP, indicating the degradation of LAB on allergens. Moreover, FBP showed alleviatory effects in BALB/c mice, which relieved pathological symptoms and lowered production of allergic mediators. Microbial high-throughput sequencing analysis showed that FBP could regulate gut microbiota and metabolism to strengthen immunity, which were closely correlated with the alleviation of allergic reactivity. These findings could contribute to the development and utilization of hypoallergenic BP products.

References

[1]

F. Ekezie, J.H. Cheng, D.W. Sun, Effects of nonthermal food processing technologies on food allergens: a review of recent research advances, Trends Food Sci. Technol. 74 (2018) 12-25. https://doi.org/10.2174/2212798409666170328145150.

[2]

M. Thakur, V. Nanda, Composition and functionality of bee pollen: a review, Trends Food Sci. Technol. 98 (2020) 82-106. https://doi.org/10.1016/j.tifs.2020.02.001.

[3]

C. Nonotte-Varly, Allergenicity of Artemisia contained in bee pollen is proportional to its mass, Eur. Ann. Allergy Clin. Immunol. 47 (2015) 218-224. https://doi.org/10.1016/j.aller.2015.05.003.

[4]

A. Singh, S. Shahi, R.K. Katiyar, et al., Hypersensitivity to pollen of four different species of Brassica: a clinico-immunologic evaluation in patients of respiratory allergy in India, Asia Pac. Allergy. 4 (2014) 197-205. https://doi.org/10.5415/apallergy.2014.4.4.197.

[5]

S. Yin, Y. Tao, Y. Jiang, et al., A combined proteomic and metabolomic strategy for allergens characterization in natural and fermented Brassica napus bee pollen, Front. Nutr. 9 (2022) 822033. https://doi.org/10.3389/fnut.2022.822033.

[6]

X. Pi, Y. Yang, Y. Sun, et al., Recent advances in alleviating food allergenicity through fermentation, Crit. Rev. Food Sci. Nutr. 62 (2022) 7255-7268. https://doi.org/10.1080/10408398.2021.1913093.

[7]

S. Yan, Q. Li, X. Xue, et al., Analysis of improved nutritional composition of bee pollen (Brassica campestris L.) after different fermentation treatments, Int. J. Food Sci. Technol. 54 (2019) 2169-2181. https://doi.org/10.1111/ijfs.14124.

[8]

X. Rui, J. Huang, G.L. Xing, et al., Changes in soy protein immunoglobulin E reactivity, protein degradation, and conformation through fermentation with Lactobacillus plantarum strains, LWT-Food Sci. Technol. 99 (2019) 156-165. https://doi.org/10.1016/j.lwt.2018.09.034.

[9]

Q. Lu, L. Zuo, Z. Wu, et al., Characterization of the protein structure of soymilk fermented by Lactobacillus and evaluation of its potential allergenicity based on the sensitized-cell model, Food Chem. 366 (2022) 130569. https://doi.org/10.1016/j.foodchem.2021.130569.

[10]

W. Fu, W. Xue, C. Liu, et al., Screening of lactic acid bacteria and yeasts from sourdough as starter cultures for reduced allergenicity wheat products, Foods 9 (2020) 751. https://doi.org/10.3390/foods9060751.

[11]

P. Zimmermann, N. Messina, W.W. Mohn, et al., Association between the intestinal microbiota and allergic sensitization, eczema, and asthma: a systematic review, J. Allergy Clin. Immunol. 143 (2019) 467-485. https://doi.org/10.1016/j.jaci.2018.09.025.

[12]

J.J. Wang, Q.M. Zhang, W.W. Ni, et al., Modulatory effect of Lactobacillus acidophilus KLDS 1.0738 on intestinal short-chain fatty acids metabolism and GPR41/43 expression in β-lactoglobulin-sensitized mice, Microbiol. Immunol. 63 (2019) 303-315. https://doi.org/10.1111/1348-0421.12723.

[13]

A. Nomura, A. Matsubara, S. Goto, et al., Relationship between gut microbiota composition and sensitization to inhaled allergens, Allergol. Int. 69 (2020) 437-442. https://doi.org/10.1016/j.alit.2019.12.010.

[14]

M.G. Boroujerdnia, M.E. Azemi, A.A. Hemmati, et al., Immunomodulatory effects of Astragalus gypsicolus hydroalcoholic extract in ovalbumininduced allergic mice model, Iran. J. Allergy Asthma Immunol. 10 (2011) 281-288. https://doi.org/010.04/ijaai.281288.

[15]

B. Kim, S. Lee, Sophoricoside from Styphnolobium japonicum improves experimental atopic dermatitis in mice, Phytomedicine 82 (2021) 153463. https://doi.org/10.1016/j.phymed.2021.15346.

[16]

B. Guy, T. Krell, V. Sanchez, et al., Do Th1 or Th2 sequence motifs exist in proteins? identification of amphipatic immunomodulatory domains in Helicobacter pylori catalase, Immunol. Lett. 96 (2005) 261-275. https://doi.org/10.1016/j.imlet.2004.09.011.

[17]

J. Nikoli, A. Neši, S. Kull, et al., Employment of proteomic and immunological based methods for the identification of catalase as novel allergen from banana, J. Proteomics. 175 (2018) 87-94. https://doi.org/10.1016/j.jprot.2018.01.007.

[18]

D. Benndorf, A. Müller, K. Bock, et al., Identification of spore allergens from the indoor mould Aspergillus versicolor, Allergy 63 (2008) 454-460. https://doi.org/10.1111/j.1398-9995.2007.01603.x.

[19]

C. Upton, J.T. Buckley, A new family of lipolytic enzymes?, Trends Biochem. Sci. 20 (1995) 178-179. https://doi.org/10.1016/s0968-0004(00)89002-7.

[20]

B.A. Jameson, H. Wolf, The antigenic index: a novel algorithm for predicting antigenic determinants, Comput. Appl. Biosci. 4 (1988) 181-186. https://doi.org/10.1093/bioinformatics/4.1.181.

[21]

J.B. Rothbard, W.R. Taylor, A sequence pattern common to T cell epitopes, EMBO J. 7 (1988) 93-100. https://doi.org/10.1002/j.1460-2075.1988.tb02787.x.

[22]

X.M. Gao, F.Y. Liew, J.P. Tite, Identification and characterization of T helper epitopes in the nucleoprotein of influenza A virus, J. Immunol. 143(1989) 3007-3014.

[23]

H. Miura, T. Tobe, Y. Nakano, Analysis of epitope regions for autoantibodies in catalase, Immunol. Invest. 39 (2010) 796-806. https://doi.org/10.3109/08820139.2010.497832.

[24]

W. Wu, J. Qiao, X. Xiao, et al., In vitro and in vivo digestion comparison of bee pollen with or without wall-disruption, J. Sci. Food Agric. 101 (2021) 2744-2755. https://doi.org/10.1002/jsfa.10902.

[25]

D. Lozano-Ojalvo, C. Berin, L. Tordesillas, Immune basis of allergic reactions to food, J. Investig. Allergol. Clin. Immunol. 29 (2019) 1-14. https://doi.org/10.18176/jiaci.0355.

[26]

W. Fu, C. Liu, X. Meng, et al., Co-culture fermentation of Pediococcus acidilactici XZ31 and yeast for enhanced degradation of wheat allergens, Int. J. Food Microbiol. 347 (2021) 109190. https://doi.org/10.1016/j.ijfoodmicro.2021.109190.

[27]

H. Zhang, Q. Lu, R. Liu, Widely targeted metabolomics analysis reveals the effect of fermentation on the chemical composition of bee pollen, Food Chem. 375 (2022) 131908. https://doi.org/10.1016/j.foodchem.2021.131908.

[28]

K. Mukai, M. Tsai, H. Saito, et al., Mast cells as sources of cytokines, chemokines, and growth factors, Immunol. Rev. 282 (2018) 121-150. https://doi.org/10.1111/imr.12634.

[29]

E.B. Thangam, E.A. Jemima, H. Singh, et al., The role of histamine and histamine receptors in mast cell-mediated allergy and inflammation: the hunt for new therapeutic targets, Front. Immunol. 9 (2018) 1873. https://doi.org/10.3389/fimmu.2018.01873.

[30]

N.M. Kushnir-Sukhov, J.M. Brown, Y. Wu, et al., Human mast cells are capable of serotonin synthesis and release, J. Allergy Clin. Immunol. 119(2007) 498-499. https://doi.org/10.1016/j.jaci.2006.09.003.

[31]

A. Zinkevičienė, D. Kainov, I. Girkontaitė, et al., Activation of tryptophan and phenylalanine catabolism in the remission phase of allergic contact dermatitis: a pilot study, Int. Arch. Allergy Immunol. 170 (2016) 262-268. https://doi.org/10.1159/000450789.

[32]

Z. Xia, Y. Zhang, C. Li, et al., Traditional Tibetan medicine Anzhijinhua San attenuates ovalbumin-induced diarrhea by regulating the serotonin signaling system in mice, J. Ethnopharmacol. 236 (2019) 484-494. https://doi.org/10.1016/j.jep.2019.01.020.

[33]

M. Wawrzyniak, D. Groeger, R. Frei, et al., Spermidine and spermine exert protective effects within the lung, Pharmacol. Res. Perspect. 9 (2021) e00837. https://doi.org/10.1002/prp2.837.

[34]

G. Li, H. Ding, X. Yu, et al., Spermidine suppresses inflammatory DC function by activating the FOXO3 pathway and counteracts autoimmunity, iScience 23 (2020) 100807. https://doi.org/10.1016/j.isci.2019.100807.

[35]

T. Feehley, C.H. Plunkett, R. Bao, et al., Healthy infants harbor intestinal bacteria that protect against food allergy, Nat. Med. 25 (2019) 448-453. https://doi.org/10.1038/s41591-018-0324-z.

[36]

M. Noval Rivas, O.T. Burton, P. Wise, et al., A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis, J. Allergy Clin. Immunol. 131 (2013) 201-212. https://doi.org/10.1016/j.jaci.2012.10.026.

[37]

R. Aitoro, R. Simeoli, A. Amoroso, et al., Extensively hydrolyzed casein formula alone or with L. rhamnosus GG reduces β-lactoglobulin sensitization in mice, Pediatr. Allergy Immunol. 28 (2017) 230-237. https://doi.org/10.1111/pai.12687.

[38]

K. Vogel, N. Blümer, M. Korthals, et al., Animal shed Bacillus licheniformis spores possess allergy-protective as well as inflammatory properties, J. Allergy Clin. Immunol. 122 (2008) 307-312. https://doi.org/10.1016/j.jaci.2008.05.016.

[39]

J. Mai, B. Liang, Z. Xiong, et al., Oral administration of recombinant Bacillus subtilis spores expressing Helicobacter pylori neutrophil-activating protein suppresses peanut allergy via up-regulation of Tregs, Clin. Exp. Allergy. 49 (2019) 1605-1614. https://doi.org/10.1111/cea.13489.

[40]

T. Hoppenbrouwers, J.H. Cvejić Hogervorst, J. Garssen, et al., Long chain polyunsaturated fatty acids (LCPUFAs) in the prevention of food allergy, Front. Immunol. 10 (2019) 1118. https://doi.org/10.3389/fimmu.2019.01118.

[41]

C. Strehl, L. Ehlers, T. Gaber, et al., Glucocorticoids-all-rounders tackling the versatile players of the immune system, Front. Immunol. 10 (2019) 1744. https://doi.org/10.3389/fimmu.2019.01744.

[42]

Y. Kinjo, D. Wu, G. Kim, et al., Recognition of bacterial glycosphingolipids by natural killer T cells, Nature 434 (2005) 520-525. https://doi.org/10.1038/nature03407.

[43]

K. Gebeyew, C. Yang, Z. He, et al., Low-protein diets supplemented with methionine and lysine alter the gut microbiota composition and improve the immune status of growing lambs, Appl. Microbiol. Biotechnol. 105 (2021) 8393-8410. https://doi.org/10.1007/s00253-021-11620-4.

[44]

J. Debarry, A. Hanuszkiewicz, K. Stein, et al., The allergyprotective properties of Acinetobacter lwoffii F78 are imparted by its lipopolysaccharide, Allergy. 65 (2010) 690-697. https://doi.org/10.1111/j.1398-9995.2009.02253.x.

Food Science and Human Wellness
Pages 349-359
Cite this article:
Yin S, Li Q, Tao Y, et al. Allergen degradation of bee pollen by lactic acid bacteria fermentation and its alleviatory effects on allergic reactions in BALB/c mice. Food Science and Human Wellness, 2024, 13(1): 349-359. https://doi.org/10.26599/FSHW.2022.9250029

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Received: 06 April 2022
Revised: 09 June 2022
Accepted: 28 June 2022
Published: 01 June 2023
© 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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