AI Chat Paper
Discover the SciOpen Platform and Achieve Your Research Goals with Ease.
• Epicutaneously sensitized mouse model of food allergy was compared in two strains.
• Both BALB/c and C57BL/6 mice showed food-allergic symptoms after cutaneous exposure.
• C57BL/6 mice showed a stronger Th2 response and more severely disrupted gut homeostasis.
• C57BL/6 mouse was fitter for establishing cutaneously sensitized models of food allergy.
Cutaneous exposure to food allergens through a disrupted skin barrier is recognized as an important cause of food allergy, and the cutaneous sensitized mouse model has been established to investigate relevant allergic disorders. However, the role of different genetic backgrounds of mice on immune responses to food allergens upon epicutaneous sensitization is largely unknown. In this study, two strains of mice, i.e., the BALB/c and C57BL/6 mice, were epicutaneously sensitized with ovalbumin on atopic dermatitis (AD)-like skin lesions, followed by intragastric challenge to induce IgE-mediated food allergy. Allergic outcomes were measured as clinical signs, specific antibodies and cytokines, and immune cell subpopulations, as well as changes in intestinal barrier function and gut microbiota. Results showed that both strains of mice exhibited typical food-allergic symptoms with a Th2-skewed response. The C57BL/6 mice, rather than the BALB/c mice, were fitter for establishing an epicutaneously sensitized model of food allergy since a stronger Th2-biased response and severer disruptions in the intestinal barrier and gut homeostasis were observed. This study provides knowledge for selecting an appropriate mouse model to study food-allergic responses associated with AD-like skin lesions and highlights the role of genetic variations in the immune mechanism underlying pathogenesis of food allergy.
Q. Zhang, Y. Wang, L. Fu, Dietary advanced glycation end-products: perspectives linking food processing with health implications, Compr. Rev. Food Sci. Food Saf. 19 (2020) 2559-2587. https://doi.org/10.1111/1541-4337.12593.
S.H. Sicherer, H.A. Sampson, Food allergy: epidemiology, pathogenesis, diagnosis, and treatment, J. Allergy Clin. Immunol. 133 (2014) 291-307. https://doi.org/10.1016/j.jaci.2013.11.020.
T. 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.
Q. Zhang, Y. Wang, L. Fu, Application of (multi-) omics approaches for advancing food allergy: an updated review, Curr. Opin. Food Sci. (2022) 100854. https://doi.org/10.1016/j.cofs.2022.100854.
S.A. Shu, A.W.T. Yuen, E. Woo, et al., Microbiota and Food Allergy, Clin. Rev. Allerg. Immu. 57 (2018) 83-97. https://doi.org/10.1007/s12016-018-8723-y.
F. Rancé, Food allergy in children suffering from atopic eczema, Pediatr. Allergy Immunol. 19 (2008) 279-284. https://doi.org/10.1111/j.1399-3038.2008.00719.x.
J.A. Boyce, A. Assa’ad, A.W. Burks, et al., Guidelines for the diagnosis and management of food allergy in the United States: summary of the NIAIDSponsored Expert Panel Report, J. Am. Acad. Dermatol. 64 (2011) 175-192. https://doi.org/10.1016/j.jaad.2010.11.020.
T. Tsakok, T. Marrs, M. Mohsin, et al., Does atopic dermatitis cause food allergy? A systematic review, Lancet 389 (2017) S95. https://doi.org/10.1016/s0140-6736(17)30491-9.
M. Noti, B.S. Kim, M.C. Siracusa, et al., Exposure to food allergens through inflamed skin promotes intestinal food allergy through the thymic stromal lymphopoietin-basophil axis, J. Allergy Clin. Immunol. 133 (2014) 1390-1399. https://doi.org/10.1016/j.jaci.2014.01.021.
L.M. Bartnikas, M.F. Gurish, O.T. Burton, et al., Epicutaneous sensitization results in IgE-dependent intestinal mast cell expansion and food-induced anaphylaxis, J. Allergy Clin. Immunol. 131 (2013). https://doi.org/10.1016/j.jaci.2012.11.032.
A. Kawasaki, N. Ito, H. Murai, et al., Skin inflammation exacerbates food allergy symptoms in epicutaneously sensitized mice, Allergy Eur. J. Allergy Clin. Immunol. 73 (2018) 1313-1321. https://doi.org/10.1111/all.13404.
A. Fukushima, T. Yamaguchi, W. Ishida, et al., Genetic background determines susceptibility to experimental immune-mediated blepharoconjunctivitis: comparison of BALB/C and C57BL/6 mice, Exp. Eye Res. 82 (2006) 210-218. https://doi.org/10.1016/j.exer.2005.06.010.
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. Wellness 7 (2018) 235-243. https://doi.org/10.1016/j.fshw.2018.10.002.
N. Tosa, K. Yoshimatsu, M. Takahashi, et al., Comparison of immune response in mice sensitized to an animal allergen, Can f 1, and to a food allergen, ovalbumin, Biomed. Res. 40 (2019) 9-15. https://doi.org/10.2220/biomedres.40.9.
Q. Liu, Y. Zhang, Z. Shu, et al., Sulfated oligosaccharide of Gracilaria lemaneiformis protect against food allergic response in mice by up-regulating immunosuppression, Carbohydr. Polym. 230 (2020) 115567. https://doi.org/10.1016/j.carbpol.2019.115567.
J. Kong, K. Chalcraft, T.S. Mandur, et al., Comprehensive metabolomics identifies the alarmin uric acid as a critical signal for the induction of peanut allergy, Allergy Eur. J. Allergy Clin. Immunol. 70 (2015) 495-505. https://doi.org/10.1111/all.12579.
M.M. Gueders, G. Paulissen, C. Crahay, et al., Mouse models of asthma: a comparison between C57BL/6 and BALB/c strains regarding bronchial responsiveness, inflammation, and cytokine production, Inflamm. Res. 58 (2009) 845–854. https://doi.org/10.1007/s00011-009-0054-2.
M. Kodama, K. Asano, T. Oguma, et al., Strain-specific phenotypes of airway inflammation and bronchial HYPERRESPONSIVENESS induced by epicutaneous allergen sensitization in BALB/c and C57BL/6 mice, Int. Arch. Allergy Immunol. 152 (2010) 67-74. https://doi.org/10.1159/000312128.
D.J. Klinke, K.M. Brundage, Scalable analysis of flow cytometry data using R/Bioconductor, Cytom. Part A. 75 (2009) 699-706. https://doi.org/10.1002/cyto.a.20746.
Michael W.Pfaffl, A new mathematical model for relative quantification in real-time RT–PCR ΔΔ method, Nucleic Acids Res. 425 (2001) 2069-2082. https://doi.org/10.1111/j.1365-2966.2012.21196.x.
C. Galand, J.M. Leyva-Castillo, J. Yoon, et al., IL-33 promotes food anaphylaxis in epicutaneously sensitized mice by targeting mast cells, J. Allergy Clin. Immunol. 138 (2016) 1356-1366. https://doi.org/10.1016/j.jaci.2016.03.056.
Q. Zhang, L. Cheng, J. Wang, et al., Antibiotic-induced gut microbiota dysbiosis damages the intestinal barrier, increasing food allergy in adult mice, Nutrients 13 (2021). https://doi.org/10.3390/nu13103315.
D. Lee, H.S. Kim, E. Shin, et al., Polysaccharide isolated from Aloe vera gel suppresses ovalbumin-induced food allergy through inhibition of Th2 immunity in mice, Biomed. Pharmacother. 101 (2018) 201-210. https://doi.org/10.1016/j.biopha.2018.02.061.
L. Fang, F. Zhou, F. Wu, et al., A mouse allergic asthma model induced by shrimp tropomyosin, Int. Immunopharmacol. 91 (2021) 107289. https://doi.org/10.1016/j.intimp.2020.107289.
Y. Luo, S. Wang, X. Liu, et al., Langerhans cells mediate the skin-induced tolerance to ovalbumin via Langerin in a murine model, Allergy Eur. J. Allergy Clin. Immunol. 74 (2019) 1738-1747. https://doi.org/10.1111/all.13813.
K. Masaki, Y. Suzuki, S. Kagawa, et al., Dual role of interleukin-23 in epicutaneously-sensitized asthma in mice, Allergol. Int. 63 (2014) 13-22. https://doi.org/10.2332/allergolint.13-OA-0632.
G. Fu, K. Zhao, H. Chen, et al., Effect of 3 Lactobacilli on immunoregulation and intestinal microbiota in a β -lactoglobulin–induced allergic mouse model, J. Dairy Sci. 102 (2019) 1943-1958. https://doi.org/10.3168/jds.2018-15683.
M. Luo, M. Gan, X.M. Yu, et al., Study on the regulatory effects and mechanisms of action of bifidobacterial exopolysaccharides on anaphylaxes in mice, Int. J. Biol. Macromol. 165 (2020) 1447-1454. https://doi.org/10.1016/j.ijbiomac.2020.09.224.
S.K. Panda, M. Colonna, Innate lymphoid cells in mucosal immunity, Front. Immunol. 10 (2019) 1-13. https://doi.org/10.3389/fimmu.2019.00861.
C.M. Lloyd, R.J. Snelgrove, Type 2 immunity: expanding our view, Sci. Immunol. 3 (2018) 1-12. https://doi.org/10.1126/sciimmunol.aat1604.
M. Hussain, L. Borcard, K.P. Walsh, et al., Basophil-derived IL-4 promotes epicutaneous antigen sensitization concomitant with the development of food allergy, J. Allergy Clin. Immunol. 141 (2018) 223-234. https://doi.org/10.1016/j.jaci.2017.02.035.
M. Hussain, G. Bonilla-Rosso, C.K.C. Kwong Chung, et al., High dietary fat intake induces a microbiota signature that promotes food allergy, J. Allergy Clin. Immunol. 144 (2019) 157-170. https://doi.org/10.1016/j.jaci.2019.01.043.
Y. Liu, Y. Ma, Z. Chen, et al., Depolymerized sulfated galactans from Eucheuma serra ameliorate allergic response and intestinal flora in food allergic mouse model, Int. J. Biol. Macromol. 166 (2021) 977-985. https://doi.org/10.1016/j.ijbiomac.2020.10.254.
D.K. Chu, Z. Mohammed-Ali, R. Jiménez-Saiz, et al., T helper cell IL-4 drives intestinal Th2 priming to oral peanut antigen, under the control of OX40L and independent of innate-like lymphocytes, Mucosal Immunol. 7 (2014) 1395-1404. https://doi.org/10.1038/mi.2014.29.
H.F. Rosenberg, S. Phipps, P.S. Foster, Eosinophil trafficking in allergy and asthma, J. Allergy Clin. Immunol. 119 (2007) 1303-1310. https://doi.org/10.1016/j.jaci.2007.03.048.
S.S. Deo, K.J. Mistry, A.M. Kakade, et al., Role played by Th2 type cytokines in IgE mediated allergy and asthma, Lung India 27 (2010) 66-71. https://doi.org/10.4103/0970-2113.63609.
D.R. Wesemann, C.R. Nagler, The Microbiome, timing, and barrier function in the context of allergic disease, Immunity 44 (2016) 728-738. https://doi.org/10.1016/j.immuni.2016.02.002.
A.B. Muir, A.J. Benitez, K. Dods, et al., Microbiome and its impact on gastrointestinal atopy, Allergy Eur. J. Allergy Clin. Immunol. 71 (2016) 1256-1263. https://doi.org/10.1111/all.12943.
N. Samadi, M. Klems, E. Untersmayr, The role of gastrointestinal permeability in food allergy, Ann. Allergy, Asthma Immunol. 121 (2018) 168-173. https://doi.org/10.1016/j.anai.2018.05.010.
K. Huang, W. Dong, W. Liu, et al., 2-O-β-D-glucopyranosyl-L-ascorbic acid, an ascorbic acid derivative isolated from the fruits of Lycium Barbarum L., modulates gut microbiota and palliates colitis in dextran sodium sulfateinduced colitis in mice, J. Agric. Food Chem. 67 (2019) 11408-11419. https://doi.org/10.1021/acs.jafc.9b04411.
L. Su, L. Shen, D.R. Clayburgh, et al., Targeted epithelial tight junction dysfunction causes immune activation and contributes to development of experimental colitis, Gastroenterology 136 (2009) 551-563. https://doi.org/10.1053/j.gastro.2008.10.081.
C. Nunes, V. Freitas, L. Almeida, et al., Red wine extract preserves tight junctions in intestinal epithelial cells under inflammatory conditions: Implications for intestinal inflammation, Food Funct. 10 (2019) 1364-1374. https://doi.org/10.1039/c8fo02469c.
L. Yao, P. Yang, Y. Lin, et al., The regulatory effect of alginate on ovalbumin-induced gut microbiota disorders, J. Funct. Foods 86 (2021). https://doi.org/10.1016/j.jff.2021.104727.
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.
S. Bunyavanich, N. Shen, A. Grishin, et al., Early-life gut microbiome composition and milk allergy resolution, J. Allergy Clin. Immunol. 138 (2016) 1122-1130.
G. Lack, Epidemiologic risks for food allergy, J. Allergy Clin. Immunol. 121 (2008) 1331-1336. https://doi.org/10.1016/j.jaci.2008.04.032.
O.I. Iweala, C.R. Nagler, The microbiome and food allergy, Annu. Rev. Immunol. 37 (2019) 377-403. https://doi.org/10.1146/annurevimmunol-042718-041621.
W. Guo, Q. Xiang, B. Mao, et al., Protective effects of microbiome-derived inosine on lipopolysaccharide-induced acute liver damage and inflammation in mice via mediating the TLR4/NF-κB pathway, J. Agric. Food Chem. 69 (2021) 7619-7628. https://doi.org/10.1021/acs.jafc.1c01781.
C. Zhou, L.L. Chen, R.Q. Lu, et al., Alteration of intestinal microbiota composition in oral sensitized C3H/HeJ mice is associated with changes in dendritic cells and T cells in mesenteric lymph nodes, Front. Immunol. 12 (2021) 1-15. https://doi.org/10.3389/fimmu.2021.631494.
X. Shao, C. Sun, X. Tang, et al., Anti-inflammatory and intestinal microbiota modulation properties of Jinxiang Garlic (Allium sativum L.) polysaccharides toward dextran sodium sulfate-induced colitis, J. Agric. Food Chem. 68 (2020) 12295-12309. https://doi.org/10.1021/acs.jafc.0c04773.
J. Xu, Y. Ye, J. Ji, et al., Untargeted metabolomic profiling reveals changes in gut microbiota and mechanisms of its regulation of allergy in ovasensitive BALB/c mice, J. Agric. Food Chem. 70 (2022) 3344-3356. https://doi.org/10.1021/acs.jafc.1c07482.
Z. Ling, Z. Li, X. Liu, et al., Altered fecal microbiota composition associated with food allergy in infants, Appl. Environ. Microbiol. 80 (2014) 2546-2554. https://doi.org/10.1128/AEM.00003-14.
1540
Views
267
Downloads
0
Crossref
0
Web of Science
0
Scopus
0
CSCD
Altmetrics
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
