Journal Home > Volume 13 , Issue 1
Food Science and Human Wellness 2024, 13(1): 124-136 https://doi.org/10.26599/FSHW.2022.9250010
Research Article | Open Access | Issue | Published: 01 June 2023

Milk fat globule membrane supplementation protects against β-lactoglobulininduced food allergy in mice via upregulation of regulatory T cells and enhancement of intestinal barrier in a microbiota-derived short-chain fatty acids manner

Show Author's Information Han Gonga,,  Tiange Lib,  Dong Liangc,  Jingxin Gaoa,  Xiaohan Liua,  Xueying Maoa( )
Key Laboratory of Functional Dairy, Ministry of Education, College of Food Science and Nutritional Engineering;China Agricultural University, Beijing 100083, China
Henan Engineering Technology Research Center of Food Processing and Circulation Safety Control, College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China
Applied Nutrition I, China National Center for Food Safety Risk Assessment, Beijing 100022, China

Peer review under responsibility of Tsinghua University Press.

Keywords:
Gut microbiota, Short-chain fatty acid, Cow’s milk allergy, Milk fat globule membrane, G protein-coupled receptor, Regulatory T cell
Cite this article:
Gong H, Li T, Liang D, et al. Milk fat globule membrane supplementation protects against β-lactoglobulininduced food allergy in mice via upregulation of regulatory T cells and enhancement of intestinal barrier in a microbiota-derived short-chain fatty acids manner. Food Science and Human Wellness, 2024, 13(1): 124-136. https://doi.org/10.26599/FSHW.2022.9250010
Download citation
EndNote(RIS)
BibTeX

2049

Views

325

Downloads

Citations

0

Crossref

0

WoS

0

Scopus

0

CSCD

Abstract Full text Electronic supplementary material About this article

Milk fat globule membrane (MFGM), which contains abundant glycoproteins and phospholipids, exerts beneficial effects on intestinal health and immunomodulation. The aim of this study was to evaluate the protective effects and possible underlying mechanisms of MFGM on cow’s milk allergy (CMA) in a β-lactoglobulin (BLG)-induced allergic mice model. MFGM was supplemented to allergic mice induced by BLG at a dose of 400 mg/kg body weight. Results demonstrated that MFGM alleviated food allergy symptoms, decreased serum levels of lipopolysaccharide, pro-inflammatory cytokines, immunoglobulin (Ig) E, IgG1, and Th2 cytokines including interleukin (IL)-4, while increased serum levels of Th1 cytokines including interferon-γ and regulatory T cells (Tregs) cytokines including IL-10 and transforming growth factor-β. MFGM modulated gut microbiota and enhanced intestinal barrier of BLG-allergic mice, as evidenced by decreased relative abundance of Desulfobacterota, Rikenellaceae, Lachnospiraceae, and Desulfovibrionaceae, while increased relative abundance of Bacteroidetes, Lactobacillaceae and Muribaculaceae, and enhanced expressions of tight junction proteins including Occludin, Claudin-1 and zonula occludens-1. Furthermore, MFGM increased fecal short-chain fatty acids (SCFAs) levels, which elevated G protein-coupled receptor(GPR) 43 and GPR109A expressions. The increased expressions of GPR43 and GPR109A induced CD103+ dendritic cells accumulation and promoted Tregs differentiation in mesenteric lymph node to a certain extent. In summary, MFGM alleviated CMA in a BLG-induced allergic mice model through enhancing intestinal barrier and promoting Tregs differentiation, which may be correlated with SCFAs-mediated activation of GPRs. These findings suggest that MFGM may be useful as a promising functional ingredient against CMA.


menu
Abstract
Full text
Outline
Electronic supplementary material
About this article

Milk fat globule membrane supplementation protects against β-lactoglobulininduced food allergy in mice via upregulation of regulatory T cells and enhancement of intestinal barrier in a microbiota-derived short-chain fatty acids manner

Show Author's information Han Gonga,, Tiange Lib, Dong Liangc, Jingxin Gaoa, Xiaohan Liua, Xueying Maoa( )
Key Laboratory of Functional Dairy, Ministry of Education, College of Food Science and Nutritional Engineering;China Agricultural University, Beijing 100083, China
Henan Engineering Technology Research Center of Food Processing and Circulation Safety Control, College of Food Science and Technology, Henan Agricultural University, Zhengzhou 450002, China
Applied Nutrition I, China National Center for Food Safety Risk Assessment, Beijing 100022, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Milk fat globule membrane (MFGM), which contains abundant glycoproteins and phospholipids, exerts beneficial effects on intestinal health and immunomodulation. The aim of this study was to evaluate the protective effects and possible underlying mechanisms of MFGM on cow’s milk allergy (CMA) in a β-lactoglobulin (BLG)-induced allergic mice model. MFGM was supplemented to allergic mice induced by BLG at a dose of 400 mg/kg body weight. Results demonstrated that MFGM alleviated food allergy symptoms, decreased serum levels of lipopolysaccharide, pro-inflammatory cytokines, immunoglobulin (Ig) E, IgG1, and Th2 cytokines including interleukin (IL)-4, while increased serum levels of Th1 cytokines including interferon-γ and regulatory T cells (Tregs) cytokines including IL-10 and transforming growth factor-β. MFGM modulated gut microbiota and enhanced intestinal barrier of BLG-allergic mice, as evidenced by decreased relative abundance of Desulfobacterota, Rikenellaceae, Lachnospiraceae, and Desulfovibrionaceae, while increased relative abundance of Bacteroidetes, Lactobacillaceae and Muribaculaceae, and enhanced expressions of tight junction proteins including Occludin, Claudin-1 and zonula occludens-1. Furthermore, MFGM increased fecal short-chain fatty acids (SCFAs) levels, which elevated G protein-coupled receptor(GPR) 43 and GPR109A expressions. The increased expressions of GPR43 and GPR109A induced CD103+ dendritic cells accumulation and promoted Tregs differentiation in mesenteric lymph node to a certain extent. In summary, MFGM alleviated CMA in a BLG-induced allergic mice model through enhancing intestinal barrier and promoting Tregs differentiation, which may be correlated with SCFAs-mediated activation of GPRs. These findings suggest that MFGM may be useful as a promising functional ingredient against CMA.

Keywords: Gut microbiota, Short-chain fatty acid, Cow’s milk allergy, Milk fat globule membrane, G protein-coupled receptor, Regulatory T cell

References(68)

[1]

A. Golkar, J.M. Milani, T. Vasiljevic, Altering allergenicity of cow’s milk by food processing for applications in infant formula, Crit. Rev. Food Sci. Nutr. 59 (2019) 159-172. https://doi.org/10.1080/10408398.2017.1363156.
DOI Google Scholar
[2]

S. Kaminogawa, S. Hachimura, H. Nakajima-adachi, Food allergens and mucosal immune systems with special reference to recognition of food allergens by gut-associated lymphoid tissue, Allergol. Int. 48 (1999) 15-23. https://doi.org/10.1046/j.1440-1592.1999.00112.x.
DOI Google Scholar
[3]

L. Fu, J. Song, C. Wang, et al., Bifidobacterium infantis potentially alleviates shrimp tropomyosin-induced allergy by tolerogenic dendritic cell-dependent induction of regulatory T cells and alterations in gut microbiota, Front. Immunol. 8 (2017) 1-14. https://doi.org/10.3389/fimmu.2017.01536.
DOI Google Scholar
[4]

R.M. Steinman, Decisions about dendritic cells: past, present, and future, Annu. Rev. Immunol. 30 (2012) 1-22. https://doi.org/10.1146/annurev-immunol-100311-102839.
DOI Google Scholar
[5]

J. Tan, C. McKenzie, P.J. Vuillermin, G. Goverse, et al., Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways, Cell Rep. 15 (2016) 2809-2824. https://doi.org/10.1016/j.celrep.2016.05.047.
DOI Google Scholar
[6]

G. Matteoli, E. Mazzini, I.D. Iliev, et al., Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction, Gut. 59 (2010) 595-604. https://doi.org/10.1136/gut.2009.185108.
DOI Google Scholar
[7]

C. Perrier, B. Corthésy, Gut permeability and food allergies, Clin. Exp. Allergy. 41 (2011) 20-28. https://doi.org/10.1111/j.1365-2222.2010.03639.x.
DOI Google Scholar
[8]

A. Koh, F. De Vadder, P. Kovatcheva-Datchary, et al., From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites, Cell 165 (2016) 1332-1345. https://doi.org/10.1016/j.cell.2016.05.041.
DOI Google Scholar
[9]

F. De Filippis, L. Paparo, R. Nocerino, et al., Specific gut microbiome signatures and the associated pro-inflamatory functions are linked to pediatric allergy and acquisition of immune tolerance, Nat. Commun. 12 (2021). https://doi.org/10.1038/s41467-021-26266-z.
DOI Google Scholar
[10]

A. Cait, E. Cardenas, P.A. Dimitriu, et al., Reduced genetic potential for butyrate fermentation in the gut microbiome of infants who develop allergic sensitization, J. Allergy Clin. Immunol. 144 (2019) 1638-1647.e3. https://doi.org/10.1016/j.jaci.2019.06.029.
DOI Google Scholar
[11]

M.R. Goldberg, H. Mor, D. Magid Neriya, et al., Microbial signature in IgE-mediated food allergies, Genome Med. 12 (2020). https://doi.org/10.1186/s13073-020-00789-4.
DOI Google Scholar
[12]

X. Yan, J. Yan, Q. Xiang, et al., Fructooligosaccharides protect against OVA-induced food allergy in mice by regulating the Th17/Treg cell balance using tryptophan metabolites, Food Funct. 12 (2021) 3191-3205. https://doi.org/10.1039/D0FO03371E.
DOI Google Scholar
[13]

M.J. Bae, H.S. Shin, H.J. See, et al., Baicalein induces CD4+ Foxp3+ T cells and enhances intestinal barrier function in a mouse model of food allergy, Sci. Rep. 6 (2016) 1-11. https://doi.org/10.1038/srep32225.
DOI Google Scholar
[14]

D. Markovic, R.A.J. Challiss, Alternative splicing of G protein-coupled receptors: physiology and pathophysiology, Cell. Mol. Life Sci. 66 (2009) 3337-3352. https://doi.org/10.1007/s00018-009-0093-4.
DOI Google Scholar
[15]

L. Macia, J. Tan, A.T. Vieira, et al., Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome, Nat. Commun. 6 (2015) 6734. https://doi.org/10.1038/ncomms7734.
DOI Google Scholar
[16]

L. Pan, Z. Ren, X. Tu, et al., GPR109A deficiency promotes IL-33 overproduction and type 2 immune response in food allergy in mice, Allergy 76 (2021) 2613-2616. https://doi.org/10.1111/all.14849.
DOI Google Scholar
[17]

R.S. Chinthrajah, J.D. Hernandez, S.D. Boyd, et al., Molecular and cellular mechanisms of food allergy and food tolerance, J. Allergy Clin. Immunol. 137 (2016) 984-997. https://doi.org/10.1016/j.jaci.2016.02.004.
DOI Google Scholar
[18]

D. Cheng, J.H. Xu, J.Y. Li, et al., Butyrate ameliorated-NLRC3 protects the intestinal barrier in a GPR43-dependent manner, Exp. Cell Res. 368 (2018) 101-110. https://doi.org/10.1016/j.yexcr.2018.04.018.
DOI Google Scholar
[19]

L. Paparo, R. Nocerino, E. Ciaglia, et al., Butyrate as a bioactive human milk protective component against food allergy, Allergy 76 (2021) 1398-1415. https://doi.org/10.1111/all.14625.
DOI Google Scholar
[20]

K. Dewettinck, R. Rombaut, N. Thienpont, et al., Nutritional and technological aspects of milk fat globule membrane material, Int. Dairy J. 18 (2008) 436-457. https://doi.org/10.1016/j.idairyj.2007.10.014.
DOI Google Scholar
[21]

Å. Nilsson, Role of sphingolipids in infant gut health and immunity, J. Pediatr. 173 (2016) S53-S59. https://doi.org/10.1016/j.jpeds.2016.02.076.
DOI Google Scholar
[22]

R. Zanabria, A.M. Tellez, M. Griffiths, et al., Modulation of immune function by milk fat globule membrane isolates, J. Dairy Sci. 97 (2014) 2017-2026. https://doi.org/10.3168/jds.2013-7563.
DOI Google Scholar
[23]

X. Zhang, Y. Wu, H. Ye, et al., Dietary milk fat globule membrane supplementation during late gestation increased the growth of neonatal piglets by improving their plasma parameters, intestinal barriers, and fecal microbiota, RSC Adv. 10 (2020) 16987-16998. https://doi.org/10.1039/d0ra02618b.
DOI Google Scholar
[24]

T. Li, J. Gao, M. Du, et al., Milk fat globule membrane supplementation modulates the gut microbiota and attenuates metabolic endotoxemia in high-fat diet-fed mice, J. Funct. Foods 47 (2018) 56-65. https://doi.org/10.1016/j.jff.2018.05.038.
DOI Google Scholar
[25]

H. Gong, Q. Yuan, J. Pang, et al., Dietary milk fat globule membrane restores decreased intestinal mucosal barrier development and alterations of intestinal flora in infant-formula-fed rat pups, Mol. Nutr. Food Res. 64 (2020) 1-12. https://doi.org/10.1002/mnfr.202000232.
DOI Google Scholar
[26]

S. Lamothe, G. Robitaille, D. St-Gelais, et al., Butter making from caprine creams: effect of washing treatment on phospholipids and milk fat globule membrane proteins distribution, J. Dairy Res. 75 (2008) 439-443. https://doi.org/10.1017/S002202990800349X.
DOI Google Scholar
[27]

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.
DOI Google Scholar
[28]

Z. Shu, Q. Liu, C. Xing, et al., Viridicatol isolated from deep-sea Penicillium griseofulvum alleviates anaphylaxis and repairs the intestinal barrier in mice by suppressing mast cell activation, Mar. Drugs. 18 (2020) 517. https://doi.org/10.3390/md18100517.
DOI Google Scholar
[29]

T. Liu, P. Chen, M. Munir, et al., HMOs modulate immunoregulation and gut microbiota in a β-lactoglobulin-induced allergic mice model, J. Funct. Foods 70 (2020) 103993. https://doi.org/10.1016/j.jff.2020.103993.
DOI Google Scholar
[30]

C. Chen, L. Lianhua, S. Nana, et al., Development of a BALB/c mouse model for food allergy: comparison of allergy-related responses to peanut agglutinin, β-lactoglobulin and potato acid phosphatase, Toxicol. Res. (Camb). 6 (2017) 251-261. https://doi.org/10.1039/c6tx00371k.
DOI Google Scholar
[31]

K. Adel-Patient, C. Créminon, H. Bernard, et al., Evaluation of a high IgE-responder mouse model of allergy to bovine β-lactoglobulin (BLG): development of sandwich immunoassays for total and allergen-specific IgE, IgG1 and IgG2a in BLG-sensitized mice, J. Immunol. Methods. 235 (2000) 21-32. https://doi.org/10.1016/S0022-1759(99)00210-0.
DOI Google Scholar
[32]

P. Chen, S. Lei, M. Tong, et al., Effect of polysaccharide fractions from Fortunella margarita on the fecal microbiota of mice and SCFA production in vitro, Food Sci. Hum. Wellness 11 (2022) 97-108. https://doi.org/10.1016/j.fshw.2021.07.011.
DOI Google Scholar
[33]

J. Ma, J. Zhang, Q. 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.
DOI Google Scholar
[34]

J. Gao, J. Song, M. Du, et al., Bovine α-lactalbumin hydrolysates (α-LAH) attenuate high-fat diet induced nonalcoholic fatty liver disease by modulating hepatic lipid metabolism in C57BL/6J mice, J. Funct. Foods 54 (2019) 254-262. https://doi.org/10.1016/j.jff.2019.01.027.
DOI Google Scholar
[35]

Z. Cheng, J. Lin, N. Gao, et al., Blueberry malvidin-3-galactoside modulated gut microbial dysbiosis and microbial TCA cycle KEGG pathway disrupted in a liver cancer model induced by HepG2 cells, Food Sci. Hum. Wellness 9 (2020) 245-255. https://doi.org/10.1016/j.fshw.2020.04.006.
DOI Google Scholar
[36]

D. Mariat, O. Firmesse, F. Levenez, et al., The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age, BMC Microbiol. 9 (2009) 123. https://doi.org/10.1186/1471-2180-9-123.
DOI Google Scholar
[37]

Y. Shao, Y. Zhang, L. Zhang, et al., Mechanism of reduction in allergenicity and altered human intestinal microbiota of digested β-lactoglobulin modified by ultrasonic pretreatment combined with glycation, J. Agric. Food Chem. 69 (2021) 14004-14012. https://doi.org/10.1021/acs.jafc.1c03501.
DOI Google Scholar
[38]

T. Li, Q. Yuan, H. Gong, et al., Gut microbiota mediates the alleviative effect of polar lipids-enriched milk fat globule membrane on obesity-induced glucose metabolism disorders in peripheral tissues in rat dams, Int. J. Obes. (2022). https://doi.org/10.1038/s41366-021-01029-4.
DOI Google Scholar
[39]
Y. Yang, G. Chen, Q. Yang, et al., Gut microbiota drives the attenuation of dextran sulphate sodium-induced colitis by Huangqin decoction, 8 (2017) 48863-48874.
DOI
[40]

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. (2020). https://doi.org/10.1016/j.ijbiomac.2020.10.254.
DOI Google Scholar
[41]

L. Fu, M. Xie, C. Wang, et al., Lactobacillus casei Zhang alleviates shrimp tropomyosin-induced food allergy by switching antibody isotypes through the NF-κB-dependent immune tolerance, Mol. Nutr. Food Res. 64 (2020). https://doi.org/10.1002/mnfr.201900496.
DOI Google Scholar
[42]

C. Huang, Y. Lin, T. Jan, Lactobacillus reuteri induces intestinal immune tolerance against food allergy in mice, J. Funct. Foods. 31 (2017) 44-51. https://doi.org/10.1016/j.jff.2017.01.034.
DOI Google Scholar
[43]

K.L. Ormerod, D.L.A. Wood, N. Lachner, et al., Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals, Microbiome 4 (2016) 36. https://doi.org/10.1186/s40168-016-0181-2.
DOI Google Scholar
[44]

H. Zeng, S.L. Ishaq, F.Q. Zhao, et al., Colonic inflammation accompanies an increase of β-catenin signaling and Lachnospiraceae/Streptococcaceae bacteria in the hind gut of high-fat diet-fed mice, J. Nutr. Biochem. 35 (2016) 30-36. https://doi.org/10.1016/j.jnutbio.2016.05.015.
DOI Google Scholar
[45]

R. Berni Canani, N. Sangwan, A.T. Stefka, et al., Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants, ISME J. 10 (2016) 742-750. https://doi.org/10.1038/ismej.2015.151.
DOI Google Scholar
[46]

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.
DOI Google Scholar
[47]

M. Milard, F. Laugerette, A. Durand, et al., Milk polar lipids in a high-fat diet can prevent body weight gain: modulated abundance of gut bacteria in relation with fecal loss of specific fatty acids, Mol. Nutr. Food Res. 63 (2019) 1801078. https://doi.org/10.1002/mnfr.201801078.
DOI Google Scholar
[48]

G.H. Norris, M. Milard, M.C. Michalski, et al., Protective properties of milk sphingomyelin against dysfunctional lipid metabolism, gut dysbiosis, and inflammation, J. Nutr. Biochem. 73 (2019) 108224. https://doi.org/10.1016/j.jnutbio.2019.108224.
DOI Google Scholar
[49]

C. Stevens, T. Millar, J. Clinch, et al., Antibacterial properties of xanthine oxidase in human milk, Lancet. 356 (2000) 829-830. https://doi.org/10.1016/S0140-6736(00)02660-X.
DOI Google Scholar
[50]

S.K. Lindén, Y.H. Sheng, A.L. Every, et al., MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy, PLoS Pathog. 5 (2009). https://doi.org/10.1371/journal.ppat.1000617.
DOI Google Scholar
[51]

M.F. Böttcher, E.K. Nordin, A. Sandin, et al., Microflora-associated characteristics in faeces from allergic and nonallergic infants, Clin. Exp. Allergy. 30 (2000) 1591-1596. https://doi.org/10.1046/j.1365-2222.2000.00982.x.
DOI Google Scholar
[52]

K. Struijs, T. Van De Wiele, T.T. Le, et al., Milk fat globule membrane glycoproteins prevent adhesion of the colonic microbiota and result in increased bacterial butyrate production, Int. Dairy J. 32 (2013) 99-109. https://doi.org/10.1016/j.idairyj.2013.05.001.
DOI Google Scholar
[53]

B. Tian, J. Zhao, M. Zhang, et al., Lycium ruthenicum anthocyanins attenuate high-fat diet-induced colonic barrier dysfunction and inflammation in mice by modulating the gut microbiota, Mol. Nutr. Food Res. 65 (2021) 1-16. https://doi.org/10.1002/mnfr.202000745.
DOI Google Scholar
[54]

P. Louis, H.J. Flint, Formation of propionate and butyrate by the human colonic microbiota, Environ. Microbiol. 19 (2017) 29-41. https://doi.org/10.1111/1462-2920.13589.
DOI Google Scholar
[55]

S. Wessler, S. Backert, Molecular mechanisms of epithelial-barrier disruption by Helicobacter pylori, Trends Microbiol. 16 (2008) 397-405. https://doi.org/10.1016/j.tim.2008.05.005.
DOI Google Scholar
[56]

X. Wang, S. Hirmo, R. Willen, et al., Inhibition of Helicobacter pylori infection by bovine milk glycoconjugates in a BALB/cA mouse model, J. Med. Microbiol. 50 (2001) 430-435. https://doi.org/10.1099/0022-1317-50-5-430.
DOI Google Scholar
[57]

T. Imaizumi, T. Aizawa-Yashiro, S. Watanabe, et al., TLR4 signaling induces retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5 in mesangial cells, J. Nephrol. 26 (2013) 886-893. https://doi.org/10.5301/jn.5000254.
DOI Google Scholar
[58]

B. Funke, F. Lasitschka, W. Roth, et al., Selective downregulation of retinoic acid-inducible gene i within the intestinal epithelial compartment in Crohn’s disease, Inflamm. Bowel Dis. 17 (2011) 1943-1954. https://doi.org/10.1002/ibd.21572.
DOI Google Scholar
[59]

Y. Wang, H.X. Zhang, Y.P. Sun, et al., Rig-I-/- mice develop colitis associated with downregulation of Gαi2, Cell Res. 17 (2007) 858-868. https://doi.org/10.1038/cr.2007.81.
DOI Google Scholar
[60]

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.
DOI Google Scholar
[61]

Y.J. Zhou, J. Gao, H.M. Yang, et al., The role of the lactadherin in promoting intestinal DCs development in vivo and vitro, Clin. Dev. Immunol. 2010 (2010) 1-9. https://doi.org/10.1155/2010/357541.
DOI Google Scholar
[62]

R. Sibilano, B. Frossi, C.E. Pucillo, Mast cell activation: a complex interplay of positive and negative signaling pathways, Eur. J. Immunol. 44 (2014) 2558-2566. https://doi.org/10.1002/eji.201444546.
DOI Google Scholar
[63]

N.Y. Lee, K.S. Chung, J.S. Jin, et al., The inhibitory effect of nodakenin on mast-cell-mediated allergic inflammation via downregulation of NF-κB and caspase-1 activation, J. Cell. Biochem. 118 (2017) 3993-4001. https://doi.org/10.1002/jcb.26055.
DOI Google Scholar
[64]

B.J. Wang, H.W. Chiu, Y.L. Lee, et al., Pterostilbene attenuates hexavalent chromium-induced allergic contact dermatitis by preventing cell apoptosis and inhibiting IL-1β-related NLRP3 inflammasome activation, J. Clin. Med. 7 (2018) 489. https://doi.org/10.3390/jcm7120489.
DOI Google Scholar
[65]

J. Tulyeu, H. Kumagai, E. Jimbo, et al., Probiotics prevents sensitization to oral antigen and subsequent increases in intestinal tight junction permeability in juvenile–young adult rats, Microorganisms 7 (2019) 1-19. https://doi.org/10.3390/microorganisms7100463.
DOI Google Scholar
[66]

N. Singh, A. Gurav, S. Sivaprakasam, et al., Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis, Immunity 40 (2014) 128-139. https://doi.org/10.1016/j.immuni.2013.12.007.
DOI Google Scholar
[67]

W. Feng, Y. Wu, G. Chen, et al., Sodium butyrate attenuates diarrhea in weaned piglets and promotes tight junction protein expression in colon in a GPR109A-dependent manner, Cell. Physiol. Biochem. 47 (2018) 1617-1629. https://doi.org/10.1159/000490981.
DOI Google Scholar
[68]

S. Huang, S. Hu, S. Liu, et al., Lithium carbonate alleviates colon inflammation through modulating gut microbiota and Treg cells in a GPR43-dependent manner, Pharmacol. Res. 175 (2022) 105992. https://doi.org/10.1016/j.phrs.2021.105992.
DOI Google Scholar
File
fshw-2024-9250010_ESM.pdf (119.2 KB)
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 12 April 2022
Revised: 20 May 2022
Accepted: 22 July 2022
Published: 01 June 2023
Issue date: January 2024

Copyright

© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

Acknowledgements

Acknowledgements

This work was supported by the National Key Research and Development Program of China (Grant No. 2019YFC1605000), National Natural Science Foundation of China (Grant No. 31871806), and the Beijing Livestock Industry Innovation Team (BAIC05-2023).

Rights and permissions

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

Return