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Research Article | Open Access

Donkey whey proteins ameliorate dextran sulfate sodium-induced ulcerative colitis in mice by downregulating the S100A8-TRAF6-NF-κB axis-mediated inflammatory response

Mohan Lia,1, Qilong Lib,1, Rayhnigul Abdllaa, Jiali Chena, Xiqing Yuea( ), Siew Young Quekc,d( )
College of Food Science, Shenyang Agricultural University, Shenyang 110866, China
College of Animal Science and Veterinary Medicine, Shenyang Agricultural University, Shenyang 110866, China
Food Science, School of Chemical Sciences, The University of Auckland, Auckland 1010, New Zealand
Riddet Institute, Centre for Research Excellence in Food Research, Palmerston North 4474, New Zealand

1 These authors contributed equally to this work.

Peer review under responsibility of KeAi Communications Co., Ltd.

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Abstract

Donkey milk has a variety of physiological functions, including antibacterial and anti-inflammatory. Donkey whey proteins (DWPs), as the main functional component in donkey milk, its inhibitory effect on colitis is still unclear. In this study, the inhibitory effect and potential mechanism of DWPs on dextran sulfate sodium (DSS)-induced colitis were investigated. Firstly, the DWPs and bovine milk whey proteins (BWPs) were characterized using proteomics. Then, we administered DWPs and BWPs to mice with colitis via oral gavage. The results of immunohistochemistry and flow cytometry indicated that DWPs increased T regulatory cell accumulation and increased the abundance of the cluster of differentiation 205+ (CD205+) macrophages compared to those with BWPs and in model groups. In addition, DWPs exhibited a more remarkable ability to inhibit pro-inflammatory proteins (S100A8, TRAF6, and NF-κB) expression and inflammatory secretion than BWPs. In addition, DWPs significantly decreased NF-κB and CD86 levels more than BWPs or the negative control in both LPS-stimulated human peripheral blood mononuclear cells or cell lines. These findings indicate that DWPs comprise a promising anti-colitis functional food, and this work has established a foundation for future research on these compounds.

Keywords

ProteomicsNF-κBDonkey milkWhey proteins

References

[1]

A.C. Ford, P. Moayyedi, S.B. Hanauer, Ulcerative colitis, BMJ 346 (2013) f432. https://doi.org/10.1136/bmj.f432.
Crossref Google Scholar
[2]

M.H. Wanderås, B.A. Moum, M.L. Høivik, et al., Predictive factors for a severe clinical course in ulcerative colitis: results from population-based studies, World J. Gastrointest. Pharmacol. Ther. 7 (2016) 235-241. https://doi.org/10.4292/wjgpt.v7.i2.235.
Crossref Google Scholar
[3]

A. Lavelle, H. Sokol, Gut microbiota-derived metabolites as key actors in inflammatory bowel disease, Nat. Rev. Gastroenterol. Hepatol. 17 (2020) 223–237.
Crossref Google Scholar
[4]

X. Chang, S.L. Wang, S.B. Zhao, et al., Extracellular vesicles with possible roles in gut intestinal tract homeostasis and IBD, Mediators Inflamm. 2020 (2020).
Crossref Google Scholar
[5]

J. Meier, A. Sturm, Current treatment of ulcerative colitis, World J. Gastroenterol. 17 (2011) 3204.
Google Scholar
[6]

S. Singh, M. Fumery, W. Sandborn, et al., Systematic review with network meta-analysis: first-and second-line pharmacotherapy for moderate-severe ulcerative colitis, Aliment. Pharmacol. Ther. 47 (2018) 162-175.
Crossref Google Scholar
[7]

Q. Chen, H. Wang, C. Zhu, et al., Anti-apoptotic effects of milk-derived casein glycomacropeptide on mice with ulcerative colitis, Food Agric. Immunol. 25 (2014) 453-466.
Crossref Google Scholar
[8]

K. Matsuoka, Y. Uemura, T. Kanai, et al., Efficacy of Bifidobacterium breve fermented milk in maintaining remission of ulcerative colitis, Dig. Dis. Sci. 63 (2018) 1910-1919.
Crossref Google Scholar
[9]

R. Pastuszka, J. Barłowska, Z. Litwińczuk, Allergenicity of milk of different animal species in relation to human milk, Postepy. Hig. Med. Dosw. 70 (2016) 1451-1459. https://doi.org/10.5604/17322693.1227842.
Crossref Google Scholar
[10]

M. Li, W. Li, J. Wu, et al., Quantitative lipidomics reveals alterations in donkey milk lipids according to lactation, Food Chem. 310 (2020) 125866. https://doi.org/10.1016/j.foodchem.2019.125866.
Crossref Google Scholar
[11]

M. Li, Y. Liu, Q. Li, et al., Comparative exploration of free fatty acids in donkey colostrum and mature milk based on a metabolomics approach, J. Dairy Sci. 103 (2020) 6022-6031. https://doi.org/10.3168/jds.2019-17720.
Crossref Google Scholar
[12]

S. Vincenzetti, P. Polidori, P. Mariani, et al., Donkey's milk protein fractions characterization, Food Chem. 106 (2008) 640-649. https://doi.org/10.1016/j.foodchem.2007.06.026.
Crossref Google Scholar
[13]

F. Tidona, A. Criscione, T.G. Devold, et al., Protein composition and micelle size of donkey milk with different protein patterns: effects on digestibility, Int. Dairy J. 35 (2014) 57-62. https://doi.org/10.1016/j.idairyj.2013.10.018.
Crossref Google Scholar
[14]

R. Derdak, S. Sakoui, O.L. Pop, et al., Insights on health and food applications of Equus asinus (donkey) milk bioactive proteins and peptides— an overview, Foods 9 (2020) 1302. https://doi.org/10.3390/foods9091302.
Crossref Google Scholar
[15]

D. Brumini, A. Criscione, S. Bordonaro, et al., Whey proteins and their antimicrobial properties in donkey milk: a brief review, Dairy Sci. Technol. 96 (2016) 1-14. https://doi.org/10.1007/s13594-015-0246-1.
Crossref Google Scholar
[16]

D. Brumini, C.B. Furlund, I. Comi, et al., Antiviral activity of donkey milk protein fractions on echovirus type 5, Int. Dairy J. 28 (2013) 109-111. https://doi.org/10.1016/j.idairyj.2012.08.010.
Crossref Google Scholar
[17]

X. Mao, J. Gu, Y. Sun, et al., Anti-proliferative and anti-tumour effect of active components in donkey milk on A549 human lung cancer cells, Int. Dairy J. 19 (2009) 703-708. https://doi.org/10.1016/j.idairyj.2009.05.007.
Crossref Google Scholar
[18]

S. Yvon, M. Olier, M. Leveque, et al., Donkey milk consumption exerts antiinflammatory properties by normalizing antimicrobial peptides levels in Paneth's cells in a model of ileitis in mice, Eur. J. Nutr. 57 (2018) 155-166.
Crossref Google Scholar
[19]

A. Tafaro, T. Magrone, F. Jirillo, et al., Immunological properties of donkeys milk: its potential use in the prevention of atherosclerosis, Curr. Pharm. Design 13 (2007) 3711-3717. https://doi.org/10.2174/138161207783018590.
Crossref Google Scholar
[20]

F. Lamine, J. Fioramonti, L. Bueno, et al., Nitric oxide released by lactobacillus farciminis improves TNBS-induced colitis in rats, Scand. J. Gastroenterol. 39 (2004) 37-45.
Crossref Google Scholar
[21]

M. Li, H. Yu, J. Chen, et al., Novel insights into whey protein differences between donkey and bovine milk, Food Chem. 365 (2021) 130397. https://doi.org/10.1016/j.foodchem.2021.130397.
Crossref Google Scholar
[22]

M.L. Molina, J. Guerrero, J.A. Cidlowski, et al., LPS regulates the expression of glucocorticoid receptor α and β isoforms and induces a selective glucocorticoid resistance in vitro, J. Inflamm. Lond Engl. 14 (2017) 22. https://doi.org/10.1186/s12950-017-0169-0.
Crossref Google Scholar
[23]

J. Cox, M. Mann, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification, Nat. Biotechnol. 26 (2008) 1367-1372. https://doi.org/10.1038/nbt.1511.
Crossref Google Scholar
[24]

G.O. Consortium, The Gene Ontology (GO) database and informatics resource, Nucleic Acids Res. 32 (2004) D258-D261. https://doi.org/10.1093/nar/gkh036.
Crossref Google Scholar
[25]

M. Kanehisa, S. Goto, KEGG: Kyoto encyclopedia of genes and genomes, Nucleic Acids Res. 28 (2000) 27-30. https://doi.org/10.1093/nar/28.1.27.
Crossref Google Scholar
[26]

D.W. Huang, B.T. Sherman, R.A. Lempicki, Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists, Nucleic Acids Res. 37 (2009) 1-13. https://doi.org/10.1093/nar/gkn923.
Crossref Google Scholar
[27]

D.F.S. Araújo, G.C.B. Guerra, M.M.E. Pintado, et al., Intestinal antiinflammatory effects of goat whey on DNBS-induced colitis in mice, PLoS One 12 (2017) e0185382. https://doi.org/10.1371/journal.pone.0185382.
Crossref Google Scholar
[28]

M.K. Jeengar, D. Thummuri, M. Magnusson, et al., Uridine ameliorates dextran sulfate sodium (DSS)-induced colitis in mice, Sci Rep. Uk. 7 (2017) 3924. https://doi.org/10.1038/s41598-017-04041-9.
Crossref Google Scholar
[29]

B.T. Kurien, R.H. Scofield, Western blotting, Methods 38 (2006) 283-293. https://doi.org/10.1016/j.ymeth.2005.11.007.
Crossref Google Scholar
[30]

J. Wang, B. Lei, J. Yan, et al., Donkey milk oligosaccharides influence the growth-related characteristics of intestinal cells and induce G2/M growth arrest via the p38 pathway in HT-29 cells, Food Funct. 10 (2019) 4823-4833. https://doi.org/10.1039/c8fo02584c.
Crossref Google Scholar
[31]

S.H. Lee, J.E. Kwon, M.L. Cho, Immunological pathogenesis of inflammatory bowel disease, Intestinal. Res. 16 (2018) 26-42. https://doi.org/10.5217/ir.2018.16.1.26.
Crossref Google Scholar
[32]

H. Abo, K.L. Flannigan, D. Geem, et al., Combined IL-2 Immunocomplex and Anti-IL-5 mAb treatment expands Foxp3+ Treg cells in the absence of Eosinophilia and Ameliorates experimental colitis, Front. Immunol. 10 (2019) 459. https://doi.org/10.3389/fimmu.2019.00459.
Crossref Google Scholar
[33]

S. Wang, R. Song, Z. Wang, et al., S100A8/A9 in Inflammation, Front. Immunol. 9 (2018) 1298. https://doi.org/10.3389/fimmu.2018.01298.
Crossref Google Scholar
[34]

D.X. Hou, T. Yanagita, T. Uto, et al., Anthocyanidins inhibit cyclooxygenase-2 expression in LPS-evoked macrophages: structure–activity relationship and molecular mechanisms involved, Biochem. Pharmacol. 70 (2005) 417-425. https://doi.org/10.1016/j.bcp.2005.05.003.
Crossref Google Scholar
[35]

B. Chassaing, J.D. Aitken, M. Malleshappa, et al., Dextran sulfate sodium (DSS)-induced colitis in mice, Curr. Protoc. Immunol. 104 (2014) 15.25.1-15.25.14. https://doi.org/10.1002/0471142735.im1525s104.
Crossref Google Scholar
[36]

S. Wang, P. Xia, Y. Chen, et al., Regulatory innate lymphoid cells control innate intestinal inflammation, Cell 171 (2017) 201-216.e18. https://doi.org/10.1016/j.cell.2017.07.027.
Crossref Google Scholar
[37]

K.K. Sanchez, G.Y. Chen, A.M.P. Schieber, et al., Cooperative metabolic adaptations in the host can favor asymptomatic infection and select for attenuated virulence in an enteric pathogen, Cell 175 (2018) 146-158.e15. https://doi.org/10.1016/j.cell.2018.07.016.
Crossref Google Scholar
[38]

X. Song, X. Sun, S.F. Oh, et al., Microbial bile acid metabolites modulate gut RORγ+ regulatory T cell homeostasis, Nature 577 (2020) 410-415. https://doi.org/10.1038/s41586-019-1865-0.
Crossref Google Scholar
[39]

A. Bordoni, F. Danesi, D. Dardevet, et al, Dairy products and inflammation: a review of the clinical evidence, Crit. Rev. Food Sci. 57 (2015) 2497-2525. https://doi.org/10.1080/10408398.2014.967385.
Crossref Google Scholar
[40]

J.R. Kanwar, R.K. Kanwar, S. Stathopoulos, et al., Comparative activities of milk components in reversing chronic colitis, J. Dairy Sci. 99 (2016) 2488-2501. https://doi.org/10.3168/jds.2015-10122.
Crossref Google Scholar
[41]

E. Janssen, R.S. Geha, Primary immunodeficiencies caused by mutations in actin regulatory proteins, Immunol. Rev. 287 (2019) 121-134. https://doi.org/10.1111/imr.12716.
Crossref Google Scholar
[42]

F. Liu, A.D. Smith, G. Solano-Aguilar, et al., Mechanistic insights into the attenuation of intestinal inflammation and modulation of the gut microbiome by krill oil using in vitro and in vivo models, Microbiome 8 (2020) 83. https://doi.org/10.1186/s40168-020-00843-8.
Crossref Google Scholar
[43]

Y. Shimomura, E. Mizoguchi, K. Sugimoto, et al., Regulatory role of B-1 B cells in chronic colitis, Int. Immunol. 20 (2008) 729-737. https://doi.org/10.1093/intimm/dxn031.
Crossref Google Scholar
[44]

D. Bauché, B. Joyce-Shaikh, R. Jain, et al., LAG3+ regulatory T cells restrain interleukin-23-producing CX3CR1+ gut-resident macrophages during group 3 innate lymphoid cell-driven colitis, Immunity 49 (2018) 342-352.e5. https://doi.org/10.1016/j.immuni.2018.07.007.
Crossref Google Scholar
[45]

M.D. Giovangiulio, A. Rizzo, E. Franzè, et al., Tbet expression in regulatory T cells is required to initiate Th1-mediated colitis, Front. Immunol. 10 (2019) 2158. https://doi.org/10.3389/fimmu.2019.02158.
Crossref Google Scholar
[46]

Y.L. Chen, Y.L. Zhang, Y.C. Dai, et al., Systems pharmacology approach reveals the antiinflammatory effects of Ampelopsis grossedentata on dextran sodium sulfate-induced colitis, World J. Gastroentero. 24 (2018) 1398-1409. https://doi.org/10.3748/wjg.v24.i13.1398.
Crossref Google Scholar
[47]

S.L. Doyle, L.A.J. O'Neill, Toll-like rfeceptors: from the discovery of NFκB to new insights into transcriptional regulations in innate immunity, Biochem. Pharmacol. 72 (2006) 1102-1113. https://doi.org/10.1016/j.bcp.2006.07.010.
Crossref Google Scholar
Food Science and Human Wellness
Volume 12 Issue 5,
September 2023
Pages 1809-1819
DOI: 10.1016/j.fshw.2023.02.045
Cite this article:
Li M, Li Q, Abdlla R, et al. Donkey whey proteins ameliorate dextran sulfate sodium-induced ulcerative colitis in mice by downregulating the S100A8-TRAF6-NF-κB axis-mediated inflammatory response. Food Science and Human Wellness, 2023, 12(5): 1809-1819. https://doi.org/10.1016/j.fshw.2023.02.045

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Received: 21 December 2021
Revised: 03 February 2022
Accepted: 03 April 2021
Published: 21 March 2023
© 2023 Beijing Academy of Food Sciences.

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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