| Original Article |
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Protective effect and mechanism insight of purified Antarctic krill phospholipids against mice ulcerative colitis combined with bioinformatics |
| Rong Huang, Jiaxu Yao, Li Zhou, Xiang Li, Jinrui Zhu, Yueqi Hu, Jikai Liu |
| National Demonstration Center for Experimental Ethnopharmacology Education, School of Pharmaceutical Sciences, South-Central MinZu University, Wuhan, 430074, People's Republic of China |
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Abstract Antarctic krill oil is functional oil and has a complex phospholipids composition that poses difficulties in elucidating its effect mechanism on ulcerative colitis (UC). The mechanism of UC action was studied by bioinformatics, and the therapeutic effect of Antarctic krill phospholipids (APL) on dextran sulfate sodium (DSS)-induced colitis mice was verified. GO functional enrichment analysis uncovered an enrichment of these genes in the regulation of cell-cell adhesion, membrane region, signaling receptor activator activity, and cytokine activity. Meanwhile, the KEGG results revealed the genes were enriched in the TNF signaling pathway, pathogenic Escherichia coli infection, inflammatory bowel disease and tight junction. Animal experiments showed that APL treatment alleviated the UC symptoms and reduced inflammatory damage. Meanwhile, the expressions of the tight junction (TJ) proteins, ZO-1 and occludin, were restored, and the levels of IL-6 and TNF-α were reduced. Moreover, Firmicutes/Bacteroidetes ratio in the intestinal microbiota was regulated, and the contents of short-chain fatty acids metabolites were raised. These findings would provide an insight for the beneficial effects of APL and dietary therapy strategies for UC.
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| Keywords
Ulcerative colitis
Krill phospholipids
Bioinformatics analysis
Tight junction protein
Intestinal microbiota
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| Fund:This work received supports from the National Natural Science Foundation of China (3150152, 21502239) and the Fundamental Research Funds for the Central Universities, South-Central MinZu University (CZY19032, CZQ21017). |
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Corresponding Authors:
Li Zhou,E-mail:zhou2018@scuec.edu.cn;Jikai Liu,E-mail:liujikai@mail.scuec.edu.cn
E-mail: zhou2018@scuec.edu.cn;liujikai@mail.scuec.edu.cn
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Issue Date: 18 May 2023
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1 Pile JE, Navalta JW, Davis CD, Sharma NC. Interventional effects of plumbagin on experimental ulcerative colitis in mice. J Nat Prod. 2013;76:1001-6.
2 Yan Y, Ren F, Wang P, Sun Y, Xing J. Synthesis and evaluation of a prodrug of 5-aminosalicylic acid for the treatment of ulcerative colitis. Iran J Basic Med Sci. 2019;22:1452-61.
3 Steed H. Ulcerative colitis. Medicine. 2019;47:371-6.
4 Armuzzi A, Liguori G. Quality of life in patients with moderate to severe ulcerative colitis and the impact of treatment:a narrative review. Dig Liver Dis. 2021;53:803-8.
5 Bhattacharya S, Cross RK. Medical treatment of ulcerative colitis. Semin Colon Rectal Surg. 2022;33:1-5.
6 Liu Y, Li BG, Su YH, Zhao RX, Song P, Li H, Ren X. Potential activity of traditional Chinese medicine against ulcerative colitis:a review. J Ethnopharmacol. 2022;289:115084.
7 Lakatos PL, Lakatos L. Once daily 5-aminosalicylic acid for the treatment of ulcerative colitis; are we there yet? Pharmacol Res. 2008;58:190-5.
8 Ocon B, Aranda CJ, Gamez-Belmonte R, Suarez MD, Zarzuelo A, Martinez-Augustin O, Sanchez de Medina F. The glucocorticoid budesonide has protective and deleterious effects in experimental colitis in mice. Biochem Pharmacol. 2016;116:73-88.
9 Lamers CR, de Roos NM, Witteman BJM. The association between inflammatory potential of diet and disease activity:results from a cross-sectional study in patients with inflammatory bowel disease. BMC Gastroenterol. 2020;20:316.
10 Lee D, Albenberg L, Compher C, Baldassano R, Piccoli D, Lewis JD, Wu GD. Diet in the pathogenesis and treatment of inflammatory bowel diseases. Gastroenterology. 2015;148:1087-106.
11 Sun J, Chen H, Kan J, Gou Y, Liu J, Zhang X, Jin C. Anti-inflammatory properties and gut microbiota modulation of an alkali-soluble polysaccharide from purple sweet potato in DSS-induced colitis mice. Int J Biol Macromol. 2020;153:708-22.
12 Xiao H, Li H, Wen Y, Jiang D, Zhu S, He X, Liang J. Tremella fuciformis polysaccharides ameliorated ulcerative colitis via inhibiting inflammation and enhancing intestinal epithelial barrier function. Int J Biol Macromol. 2021;180:633-42.
13 He J, Guo K, Chen Q, Wang Y, Jirimutu. Camel milk modulates the gut microbiota and has anti-inflammatory effects in a mouse model of colitis. J. Dairy Sci. 2022;105:3782-93.
14 Xie D, Gong M, Wei W, Jin J, Wang X, Wang X, Jin Q. Antarctic Krill (Euphausia superba) oil:a comprehensive review of chemical composition, extraction technologies, health benefits, and current applications. Compr Rev Food Sci Food Saf. 2019;18:514-34.
15 Grimstad T, Bjorndal B, Cacabelos D, Aasprong OG, Janssen EA, Omdal R, Berge RK. Dietary supplementation of krill oil attenuates inflammation and oxidative stress in experimental ulcerative colitis in rats. Scand J Gastroenterol. 2012;47:49-58.
16 Liu F, Smith AD, Solano-Aguilar G, Wang TTY, Pham Q, Beshah E, Li RW. 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. 2020;8:83.
17 Zhou X, Xiang X, Zhou Y, Zhou T, Deng S, Zheng B, Zheng P. Protective effects of Antarctic krill oil in dextran sulfate sodium-induced ulcerative colitis mice. J Funct Foods. 2021;79:1-13.
18 Xie D, Jin J, Sun J, Liang L, Wang X, Zhang W, Wang X, Jin Q. Comparison of solvents for extraction of krill oil from krill meal:lipid yield, phospholipids content, fatty acids composition and minor components. Food Chem. 2017;233:434-41.
19 Xie D, Mu H, Tang T, Wang X, Wei W, Jin J, Jin Q. Production of three types of krill oils from krill meal by a three-step solvent extraction procedure. Food Chem. 2018;248:279-86.
20 Zhou L, Wu X, Yang F, Zhang M, Huang R, Liu J. Characterization of molecular species and anti-inflammatory activity of purified phospholipids from Antarctic krill oil. Mar Drugs. 2021;19:1-15.
21 Chen ZA, Sun YF, Wang QX, Ma HH, Ma ZZ, Yang CJ. Integrated analysis of multiple microarray studies to identify novel gene signatures in ulcerative colitis. Front Genet. 2021;12:697514.
22 Qiu S, Munir A, Malik SI, Khan S, Hassan A. Identification of differentially expressed genes and pathways crosstalk analysis in rheumatoid and osteoarthritis using next-generation sequencing and protein-protein networks. Saudi J Biol Sci. 2021;28:4656-63.
23 Wang H, Wang C, Zhang L, Lu Y, Duan Q, Gong Z, Wang L. Analysis of the protein-protein interaction networks of differentially expressed genes in pulmonary embolism. Mol Med Rep. 2015;11:2527-33.
24 Lin LJ, Zhang Y, Lin Y, Jin Y, Zheng CQ. Identifying candidate genes for discrimination of ulcerative colitis and Crohn's disease. Mol Biol Rep. 2014;41:6349-55.
25 Xiu MX, Liu YM, Chen GY, Hu C, Kuang BH. identifying hub genes, key pathways and immune cell infiltration characteristics in pediatric and adult ulcerative colitis by integrated bioinformatic analysis. Dig Dis Sci. 2021;66:3002-14.
26 Lei Y, Chen Y, Lin Z, Tian D, Han P. Comprehensive analysis of key biomarkers, immune infiltration and potential therapeutic agents for ulcerative colitis. Life Sci. 2020;260:118437.
27 Zhang D, Yan P, Han T, Cheng X, Li J. Identification of key genes and biological processes contributing to colitis associated dysplasia in ulcerative colitis. PeerJ. 2021;9:e11321.
28 Giner E, Recio MC, Rios JL, Giner RM. Oleuropein protects against dextran sodium sulfate-induced chronic colitis in mice. J Nat Prod. 2013;76:1113-20.
29 Lu J, Dong B, Chen A, He F, Peng B, Wu Z, Li W. Escherichia coli promotes DSSinduced murine colitis recovery through activation of the TLR4/NFkappaB signaling pathway. Mol Med Rep. 2019;19:2021-8.
30 Guo T, Lin Q, Li X, Nie Y, Wang L, Shi L, Luo F. Octacosanol attenuates inflammation in both RAW264.7 macrophages and a mouse model of colitis. J Agric Food Chem. 2017;65:3647-58.
31 Qiu Y, Jiang Z, Hu S, Wang L, Ma X, Yang X. Lactobacillus plantarum enhanced IL-22 production in natural killer (NK) cells that protect the integrity of intestinal epithelial cell barrier damaged by enterotoxigenic Escherichia coli. Int J Mol Sci. 2017;18:1-15.
32 Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology:short-chain fatty acids as key bacterial metabolites. Cell. 2016;165:1332-45.
33 Kim CH, Park J, Kim M. Gut microbiota-derived short-chain Fatty acids, T cells, and inflammation. Immune Netw. 2014;14:277-88.
34 Murch SH, Braegger CP, Sessa WC, MacDonald TT. High endothelin-1 immunoreactivity in Crohn's disease and ulcerative colitis. Lancet. 1992;339:381-5.
35 Nighot P, Al-Sadi R, Rawat M, Guo S, Watterson DM, Ma T. Matrix metalloproteinase 9-induced increase in intestinal epithelial tight junction permeability contributes to the severity of experimental DSS colitis. Am J Physiol Gastrointest Liver Physiol. 2015;309:G988-97.
36 Stallmach A, Chan CC, Ecker KW, Feifel G, Herbst H, Schuppan D, Zeitz M. Comparable expression of matrix metalloproteinases 1 and 2 in pouchitis and ulcerative colitis. Gut. 2000;47:415-22.
37 Damsky W, Peterson D, Ramseier J, Al-Bawardy B, Chun H, Proctor D, King B. The emerging role of Janus kinase inhibitors in the treatment of autoimmune and inflammatory diseases. J Allergy Clin Immunol. 2021;147:814-26.
38 Wang B, Lim JH, Kajikawa T, Li X, Vallance BA, Moutsopoulos NM, Hajishengallis G. Macrophage beta2-integrins regulate IL-22 by ILC3s and protect from lethal citrobacter rodentium-induced colitis. Cell Rep. 2019;26:1614-26.
39 Min X, Zhou Y, Xiang S, Sun R, Wu Q, Shi J, Chen X. Neferine, a natural alkaloid from Nelumbo nucifera, ameliorates experimental chronic ulcerative colitis in mice. Pharmacol Res Mod Chinese Med. 2021;1:100022.
40 Zhang W, Zhong W, Wang B, Yang J, Yang J, Yu Z, Guo W. ICAM-1-mediated adhesion is a prerequisite for exosome-induced T cell suppression. Dev Cell. 2022;57:329-43.
41 Kiener TK, Sleptsova-Friedrich I, Hunziker W. Identification, tissue distribution and developmental expression of tjp1/zo-1, tjp2/zo-2 and tjp3/zo-3 in the zebrafish, Danio rerio. Gene Expr Patterns. 2007;7:767-76.
42 Zhou N, Shen Y, Fan L, Sun Q, Huang C, Hao J, Yan H. The characteristics of intestinal-barrier damage in rats with IgA nephropathy. Am J Med Sci. 2020;359:168-76.
43 Lee Y, Kamada N, Moon JJ. Oral nanomedicine for modulating immunity, intestinal barrier functions, and gut microbiome. Adv Drug Deliv Rev. 2021;179:114021.
44 Luo L, Liu Y, Cai X, Wang Y, Xue J, Zhang J, Yang F. Bletilla striata polysaccharides ameliorates lipopolysaccharide-induced injury in intestinal epithelial cells. Saudi J Gastroenterol. 2019;25:302-8.
45 Kobayashi T, Siegmund B, Le Berre C, Wei SC, Ferrante M, Shen B, Hibi T. Ulcerative colitis. Nat Rev Dis Primers. 2020;6:74.
46 Nakase H, Sato N, Mizuno N, Ikawa Y. The influence of cytokines on the complex pathology of ulcerative colitis. Autoimmun Rev. 2022;21:103017.
47 Kim JH, Hong SS, Lee M, Lee EH, Rhee I, Chang SY, Lim SJ. Krill oil-incorporated liposomes as an effective nanovehicle to ameliorate the inflammatory responses of DSS-induced colitis. Int J Nanomed. 2019;14:8305-20.
48 Hao W, Hao C, Wu C, Xu Y, Jin C. Aluminum induced intestinal dysfunction via mechanical, immune, chemical and biological barriers. Chemosphere. 2022;288:132556.
49 Zeng W, He D, Xing Y, Liu J, Su N, Zhang C, Xing X. Internal connections between dietary intake and gut microbiota homeostasis in disease progression of ulcerative colitis:a review. Food Sci Hum Wellness. 2021;10:119-30.
50 Franzosa EA, Sirota-Madi A, Avila-Pacheco J, Fornelos N, Haiser HJ, Reinker S, Vatanen T, Hall AB, Mallick H, McIver LJ, et al. Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nat Microbiol. 2019;4:293-305.
51 Mei Z, Huang X, Zhang H, Cheng D, Xu X, Fang M, Mei Y. Chitin derivatives ameliorate DSS-induced ulcerative colitis by changing gut microbiota and restoring intestinal barrier function. Int J Biol Macromol. 2022;202:375-87.
52 Tan M, Wang L, Guan K, Li C, Chen C. Spenceria ramalana Trimen total polyphenols modulate the inflammatory response and intestinal flora in DSS-induced ulcerative colitis in C57BL/6 mice. Pharmacol Res. 2022;2:100042.
53 Hofmanova J, Strakova N, Vaculova AH, Tylichova Z, Safarikova B, Skender B, Kozubik A. Interaction of dietary fatty acids with tumour necrosis factor family cytokines during colon inflammation and cancer. Mediators Inflamm. 2014;2014:848632.
54 Rios-Covian D, Ruas-Madiedo P, Margolles A, Gueimonde M, de Los R-G, Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front Microbiol. 2016;7:185.
55 Peng L, Li ZR, Green RS, Holzman IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr. 2009;139:1619-25.
56 Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47.
57 Langfelder P, Horvath S. WGCNA:an R package for weighted correlation network analysis. BMC Bioinform. 2008;9:559.
58 Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Mering CV. STRING v11:protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607-13.
59 Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. Cytoscape 2.8:new features for data integration and network visualization. Bioinformatics. 2011;27:431-2.
60 Yu G, Wang LG, Han Y, He QY. clusterProfiler:an R package for comparing biological themes among gene clusters. OMICS. 2012;16:284-7.
61 Ma J, Yin G, Lu Z, Xie P, Zhou H, Liu J, Yu L. Casticin prevents DSS induced ulcerative colitis in mice through inhibitions of NF-kappaB pathway and ROS signaling. Phytother Res. 2018;32:1770-83.
62 Zhou G, Chen L, Sun Q, Mo QG, Sun WC, Wang YW. Maqui berry exhibited therapeutic effects against DSS-induced ulcerative colitis in C57BL/6 mice. Food Funct. 2019;10:6655-65. |
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