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Research Article | Open Access

Insights into sensitizing and eliciting capacity of gastric and gastrointestinal digestion products of shrimp (Penaeus vannamei) proteins in BALB/c mice

Yao LiuaSongyi Lina,bKexin LiuaShan WangaWang LiaNa Suna,b( )
National Engineering Research Center of Seafood, School of Food Science and Technology, Dalian Polytechnic University, Dalian 116034, China
Collaborative Innovation Center of Seafood Deep Processing, Dalian Polytechnic University, Dalian 116034, China

Peer review under responsibility of Tsinghua University Press.

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Abstract

Shrimp (Penaeus vannamei) proteins have been shown an allergenic potential; however, little information is available on the sensitizing and eliciting capacity of shrimp protein digestion products. In this study, a BALB/c mice model was used to explore the allergenicity of shrimp protein sample (SPS) and their gastric and gastrointestinal digestion products (GDS/GIDS). As compared with the SPS groups, the GDS/GIDS groups caused lower specific immunoglobulins (IgE/IgG1) levels (P < 0.05), but higher than the control groups, indicating that the digestion products sensitized the mice. Meanwhile, spleen index, mouse mast cell protease-1(mMCP-1) concentration and proportion of degranulated mast cells were significantly reduced in the GDS/GIDS groups (P < 0.05); simultaneously, allergic symptoms, vascular permeability and histopathological changes of tissues were alleviated. Nevertheless, the allergenicity of digestion products cannot be eliminated and still cause systemic allergic reactions in mice. The study showed that the digestion products of shrimp still had high sensitizing and eliciting capacity.

References

[1]

K. Majumder, Y. Jin, H. Shibata, et al., Oral intervention of Lactobacillus pentosus S-PT84 attenuates the allergenic responses in a BALB/c mouse model of egg allergy, Mol. Immunol. 120 (2020) 43-51. https://doi.org/10.1016/j.molimm.2020.01.025.

[2]

X. Dong, J. Wang, V. Raghavan, Critical reviews and recent advances of novel non-thermal processing techniques on the modification of food allergens, Crit. Rev. Food Sci. Nutr. 61 (2021) 196-210. https://doi.org/10.1080/10408398.2020.1722942.

[3]

L. Connors, A. O’Keefe, L. Rosenfield, et al., Non-IgE-mediated food hypersensitivity, Allergy Asthma Cl. Im. 14 (2018) 56. https://doi.org/10.1186/s13223-018-0285-2.

[4]

D.I. Pritchard, F.H. Falcone, P.D. Mitchell, The evolution of IgE-mediated type Ⅰ hypersensitivity and its immunological value, Allergy 76 (2021) 1024-1040. https://doi.org/10.1111/all.14570.

[5]

Y.V. Virkud, Y.C. Chen, E.S. Stieb, et al., Analysis of oral food challenge outcomes in IgE-mediated food allergies to almond in a large cohort, J. Aller. Cl. Imm. -Pract. 7 (2019) 2359-2368. https://doi.org/10.1016/j.jaip.2019.03.049.

[6]

N. Shimojo, A. Yagami, F. Ohno, et al., Fish collagen as a potential indicator of severe allergic reactions among patients with fish allergies, Clin. Exp. Allergy 52 (2022) 183-187. https://doi.org/10.1111/cea.14028.

[7]

C.M. Davis, R.S. Gupta, O.N. Aktas, et al., Clinical management of seafood allergy, J. Aller. Cl. Imm. -Pract. 8 (2020) 37-44. https://doi.org/10.1016/j.jaip.2019.10.019.

[8]

C.H. Lee, C.C. Wu, Y.C. Tyan, et al., Identification of pyruvate kinase as a novel allergen in whiteleg shrimp (Litopenaeus vannamei) by specific-IgE present in patients with shrimp allergy, Food Chem. 258 (2018) 359-365. https://doi.org/10.1016/j.foodchem.2018.03.088.

[9]

M. Múnera, D. Martínez, J. Wortmann, et al., Structural and allergenic properties of the fatty acid binding protein from shrimp Litopenaeus vannamei, Allergy 77 (2022) 1534-1544. https://doi.org/10.1111/all.15154.

[10]

R.M. Boaventura, R.B. Mendonça, F.A. Fonseca, et al., Nutritional status and food intake of children with cow’s milk allergy, Allergologia et Immunopathol. 47 (2019) 544-550. https://doi.org/10.1016/j.aller.2019.03.003.

[11]

S. Seo, L. L’Hocine, S. Karboune, Allergenicity of potato proteins and of their conjugates with galactose, galactooligosaccharides, and galactan in native, heated, and digested forms, J. Agric. Food Chem. 62 (2014) 3591-3598.

[12]

H. Rao, Y. Tian, W. Fu, et al., In vitro digestibility and immunoreactivity of thermally processed peanut, Food Agr. Immunol. 29 (2018) 989-1001. https://doi.org/10.1080/09540105.2018.1499710.

[13]

Y.H. Shao, Y. Zhang, J. Liu, et al., Influence of ultrasonic pretreatment on the structure, antioxidant and IgG/IgE binding activity of β-lactoglobulin during digestion in vitro, Food Chem. 312 (2020) 126080. https://doi.org/10.1016/j.foodchem.2019.126080.

[14]

L. Martín-Pedraza, C. Mayorga, F. Gomez, et al., IgE-reactivity pattern of tomato seed and peel nonspecific lipid-transfer proteins after in vitro gastrointestinal digestion, J. Agric. Food Chem. 69 (2021) 3511-3518. https://doi.org/10.1021/acs.jafc.0c06949.

[15]

F. Zhou, S. He, H. Sun, et al., Advances in epitope mapping technologies for food protein allergens: a review, Trends Food Sci. Techno. 107 (2021) 226-239. https://doi.org/10.1016/j.tifs.2020.10.035.

[16]

W.M. Chen, Y.H. Shao, Z. Wang, et al., Simulated in vitro digestion of α-lactalbumin modified by phosphorylation: detection of digestive products and allergenicity, Food Chem. 372 (2022) 131308. https://doi.org/10.1016/j.foodchem.2021.131308.

[17]

Y.H. Shao, Y. Zhang, J. Liu, et al., Investigation into predominant peptide and potential allergenicity of ultrasonicated β-lactoglobulin digestion products, Food Chem. 361 (2021) 130099. https://doi.org/10.1016/j.foodchem.2021.130099.

[18]

O.T. Toomer, A.B. Do, T.J. Fu, et al., Digestibility and immunoreactivity of shrimp extracts using an in vitro digestibility model with pepsin and pancreatin, J. Food Sci. 80 (2015) T1633-T1639. https://doi.org/10.1111/1750-3841.12917.

[19]

Z. Zhang, X.M. Li, H. Xiao, et al., IgE-binding epitope mapping of tropomyosin allergen (Exo m 1) from Exopalaemon modestus, the freshwater Siberian prawn, Food Chem. 309 (2020) 125603. https://doi.org/10.1016/j.foodchem.2019.125603.

[20]

R. Korte, J. Bräcker, J. Brockmeyer, Gastrointestinal digestion of hazelnut allergens on molecular level: elucidation of degradation kinetics and resistant immunoactive peptides using mass spectrometry, Mol. Nutr. Food Res. 61(2017) 1700130. https://doi.org/10.1002/mnfr.201700130.

[21]

C. Gámez, M.P. Zafra, V. Sanz, et al., Simulated gastrointestinal digestion reduces the allergic reactivity of shrimp extract proteins and tropomyosin, Food Chem. 173 (2015) 475-481. https://doi.org/10.1016/j.foodchem.2014.10.063.

[22]

G.M. Liu, Y.Y. Huang, Q.F. Cai, et al., Comparative study of in vitro digestibility of major allergen, tropomyosin and other proteins between grass prawn (Penaeus monodon) and Pacific white shrimp (Litopenaeus vannamei), J. Sci. Food Agr. 91 (2011) 163-170. https://doi.org/10.1002/jsfa.4167.

[23]

Y.Y. Huang, G.M. Liu, Q.F. Cai, et al., Stability of major allergen tropomyosin and other food proteins of mud crab (Scylla serrata) by in vitro gastrointestinal digestion, Food Chem. Toxico. 48 (2010) 1196-1201. https://doi.org/10.1016/j.fct.2010.02.010.

[24]

H.L. Chen, M.J. Cao, Q.F. Cai, et al., Purification and characterisation of sarcoplasmic calcium-binding protein, a novel allergen of red swamp crayfish (Procambarus clarkii), Food Chem. 139 (2013) 213-223. https://doi.org/10.1016/j.foodchem.2013.01.119.

[25]

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 (2015) 6271-6282. https://doi.org/10.1021/acs.jafc.5b01318.

[26]

J. Huang, C. Liu, Y. Wang, et al., Application of in vitro and in vivo models in the study of food allergy, Food Sci. Hum. Well. 7 (2018) 235-243. https://doi.org/10.1016/j.fshw.2018.10.002.

[27]

C. Gao, F. Wang, L. Yuan, et al., Physicochemical property, antioxidant activity, and cytoprotective effect of the germinated soybean proteins, Food Sci. Nutr. 7 (2019) 120-131. https://doi.org/10.1002/fsn3.822.

[28]

L. Yi, M.A.J.S. van Boekel, C.M.M. Lakemond, Extracting tenebrio molitor protein while preventing browning: effect of pH and NaCl on protein yield, J. Insects Food Feed 3 (2017) 21-31. https://doi.org/10.3920/JIFF2016.0015.

[29]

M. Minekus, M. Alminger, P. Alvito, et al., A standardised static in vitro digestion method suitable for food-an international consensus, Food Funct. 5(2014) 1113-1124. https://doi.org/10.1039/C3FO60702J.

[30]

N. Sun, T. Wang, D. Wang, et al., Antarctic krill derived nonapeptide as an effective iron-binding ligand for facilitating iron absorption via the small intestine, J. Agric. Food Chem. 68 (2020) 11290-11300. https://doi.org/10.1021/acs.jafc.0c03223.

[31]

R. Bastola, G. Noh, T. Keum, et al., Vaccine adjuvants: smart components to boost the immune system, Arch. Pharm. Res. 40 (2017) 1238-1248. https://doi.org/10.1007/s12272-017-0969-z.

[32]

A. Misra, R. Kumar, V. Mishra, et al., Potential allergens of green gram (Vigna radiata L. Millsp) identified as members of cupin superfamily and seed albumin, Clin. Exp. Allergy 41 (2011) 1157-1168. https://doi.org/10.1111/j.1365-2222.2011.03780.x.

[33]

B.V. Mohan Kumar, M. Vijaykrishnaraj, N.K. Kurrey, et al., Prolyl endopeptidase-degraded low immunoreactive wheat flour attenuates immune responses in Caco-2 intestinal cells and gluten-sensitized BALB/c mice, Food Chem. Toxicol. 129 (2019) 466-475. https://doi.org/10.1016/j.fct.2019.05.011.

[34]

V. Morafo, K. Srivastava, C.K. Huang, et al., Genetic susceptibility to food allergy is linked to differential TH2-TH1 responses in C3H/HeJ and BALB/c mice, J. Allergy Clin. Immunol. 111 (2003) 1122-1128. https://doi.org/10.1067/mai.2003.1463.

[35]

X.M. Li, D. Serebrisky, S.Y. Lee, et al., A murine model of peanut anaphylaxis: T-and B-cell responses to a major peanut allergen mimic human responses, J. Allergy Clin. Immunol. 106 (2000) 150-158. https://doi.org/10.1067/mai.2000.107395.

[36]

A. Kawasaki, N. Ito, H. Murai, et al., Skin inflammation exacerbates food allergy symptoms in epicutaneously sensitized mice, Allergy 73 (2018) 1313-1321. https://doi.org/10.1111/all.13404.

[37]

L. Xue, Y. Li, T. Li, et al., Phosphorylation and enzymatic hydrolysis with alcalase and papain effectively reduce allergic reactions to gliadins in normal mice, J. Agric. Food Chem. 67 (2019) 6313-6323. https://doi.org/10.1021/acs.jafc.9b00569.

[38]

I.T. Ansari, T. Mu, A murine model of wheat versus potato allergy: patatin and 53 kDa protein are the potential allergen from potato, Mol. Immunol. 101 (2018) 284-293. https://doi.org/10.1016/j.molimm.2018.07.012.

[39]

T. Jiang, F. He, S. Han, et al., Characterization of cAMP as an anti-allergic functional factor in Chinese jujube (Ziziphus jujuba Mill. ), J. Funct. Foods 60 (2019) 103414. https://doi.org/10.1016/j.jff.2019.06.016.

[40]

B. Yu, D. Bi, L. Yao, et al., The inhibitory activity of alginate against allergic reactions in an ovalbumin-induced mouse model, Food Funct. 11(2020) 2704-2713. https://doi.org/10.1039/D0FO00170H.

[41]

C. Luo, G. Chen, I. Ahmed, et al., Immunostimulatory and allergenic properties of emulsified and non-emulsified digestion products of parvalbumin (Scophthalmus maximus) in RBL-2H3 cells and BALB/c mouse models, Food Funct. 12 (2021) 5351-5360. https://doi.org/10.1039/D1FO00575H.

[42]

J. Bai, J. Hui, Q. Lu, et al., Effect of transglutaminase cross-linking on the allergenicity of tofu based on a BALB/c mouse model, Food Funct. 11 (2020) 404-413. https://doi.org/10.1039/C9FO02376C.

[43]

N. Mendez-Barbero, A. Yuste-Montalvo, E. Nuñez-Borque, et al., The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock, J. Allergy Clin. Immunol. 145 (2020) 583-596. https://doi.org/10.1016/j.jaci.2019.09.019.

[44]

H. Xie, S.H. He, Roles of histamine and its receptors in allergic and inflammatory bowel diseases, World J. Gastroenterol. 11 (2005) 2851-2857. https://doi.org/10.3748/wjg.v11.i19.2851.

[45]

S. Benedé, M. Cecilia Berin, Mast cell heterogeneity underlies different manifestations of food allergy in mice, PLoS One 13 (2018) e0190453. https://doi.org/10.1371/journal.pone.0190453

[46]

R.K. Gupta, A. Raghav, A. Sharma, et al., Glycation of clinically relevant chickpea allergen attenuates its allergic immune response in BALB/c mice, Food Chem. 235 (2017) 244-256. https://doi.org/10.1016/j.foodchem.2017.05.056.

[47]

F.G.C. Ekezie, D.W. Sun, J.H. Cheng, Altering the IgE binding capacity of king prawn (Litopenaeus vannamei) tropomyosin through conformational changes induced by cold argon-plasma jet, Food Chem. 300 (2019) 125143. https://doi.org/10.1016/j.foodchem.2019.125143.

[48]

M. Yang, C. Yang, F. Nau, et al., Immunomodulatory effects of egg white enzymatic hydrolysates containing immunodominant epitopes in a BALB/c mouse model of egg allergy, J. Agric. Food Chem. 57 (2009) 2241-2248. https://doi.org/10.1021/jf803372b.

[49]

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

[50]

L. Kropp, B. Jackson-Thompson, L.M. Thomas, et al., Chronic infection with a tissue-invasive helminth attenuates sublethal anaphylaxis and reduces granularity and number of mast cells, Clin. Exp. Allergy 50 (2020) 213-221. https://doi.org/10.1111/cea.13549.

[51]

A. Cianferoni, A. Muraro, Food-induced anaphylaxis, Immunol. Allergy Clin. 32 (2012) 165-195. https://doi.org/10.1016/j.iac.2011.10.002.

[52]

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 (2019) 8138-8148. https://doi.org/10.1021/acs.jafc.9b02132.

[53]

P. Tong, S. Chen, J. Gao, et al., Caffeic acid-assisted cross-linking catalyzed by polyphenol oxidase decreases the allergenicity of ovalbumin in a BALB/c mouse model, Food Chem. Toxicol. 111 (2018) 275-283. https://doi.org/10.1016/j.fct.2017.11.026.

[54]

R.A. Hatz, K.J. Bloch, P.R. Harmatz, et al., Divalent hapten-induced intestinal anaphylaxis in the mouse enhances macromolecular uptake from the stomach, Gastroenterology 98 (1990) 894-900. https://doi.org/10.1016/0016-5085(90)90013-Q.

[55]

S. Kumar, A. Sharma, R.K. Gupta, et al., Allergenicity assessment of Buchanania lanzan protein extract in BALB/c mice, Int. Immunopharmacol. 63 (2018) 170-182. https://doi.org/10.1016/j.intimp.2018.07.039.

Food Science and Human Wellness
Pages 339-348
Cite this article:
Liu Y, Lin S, Liu K, et al. Insights into sensitizing and eliciting capacity of gastric and gastrointestinal digestion products of shrimp (Penaeus vannamei) proteins in BALB/c mice. Food Science and Human Wellness, 2024, 13(1): 339-348. https://doi.org/10.26599/FSHW.2022.9250028

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Received: 14 April 2022
Revised: 26 May 2022
Accepted: 22 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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