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Research Article | Open Access

Impact of Bifidobacterium longum NSP001 on DSS-induced colitis in conventional and humanised mice

Menglin Chen, Hong Yao, Huizi Tan, Wenqi Huang, Quanyong Wu, Shaoping Nie( )
State Key Laboratory of Food Science and Technology, China-Canada Joint Laboratory of Food Science and Technology (Nanchang), Nanchang University, Nanchang 330047, China
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Abstract

Most scientific investigations regarding inflammatory bowel disease (IBD) pathogenesis or therapeutic strategies use dextran sulfate sodium (DSS)-induced models performed on mice. However, differences between human and animal microbiota may confound the data reproducibility from rodent experiments to clinical trials. In this study, the intervention effects of Bifidobacterium longum NSP001 on DSS-induced colitis were investigated using mice colonized with either native or humanised microbiota. Disorders in disease activity index (DAI), morphology and histology of colon tissue, intestinal permeability, and secretion of MPO, TNF-α and IL-6 were ameliorated by daily intake of live B. longum NSP001 cells in both conventional and humanised colitis mice. But the abnormal thymus index, and colonic production of ZO-1 and iNOS were improved only in colitis mice treated with B. longum NSP001 and humanised microbiome. The accumulation of acetic acid and propionic acid in colon microbiome, and the optimization of primary bile acid biosynthesis and glycerophospholipid metabolism pathways in cecum commensals were likely to explain the beneficial effects of B. longum NSP001. These data revealed that intestinal microbiome baseline would possibly affect the manifestation features of interventions by probiotics or dietary components and highlighted the necessity to include humanised microbiome while investigating potential therapeutic strategies based on rodent models.

Keywords

InflammationUlcerative colitisBifidobacterium longumHumanised miceMetabolism pathways

References

[1]

B. Siegmund, M. Zeitz, Innate and adaptive immunity in inflammatory bowel disease, World J. Gastroenterol. 17(27) (2011) 3178-3183. https://doi.org/10.3748/wjg.v17.i27.3178.
Crossref Google Scholar
[2]

T.A. Malik, Inflammatory bowel disease: historical perspective, epidemiology, and risk factors, Surg. Clin. North Am. 95(6) (2015) 1105-1122. https://doi.org/10.1016/j.suc.2015.07.006.
Crossref Google Scholar
[3]

P.K. Randhawa, K. Singh, N. Singh, et al., A review on chemical-induced inflammatory bowel disease models in rodents, Korean J. Physiol. Pharmacol. 18(4) (2014) 279-288. https://doi.org/10.4196/kjpp.2014.18.4.279.
Crossref Google Scholar
[4]

A.W. Walker, J.D. Sanderson, C. Churcher, et al., High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease, BMC Microbiol. 11(1) (2011) 7. https://doi.org/10.1186/1471-2180-11-7.
Crossref Google Scholar
[5]

A.I. Sanchez-Garrido, V. Prieto-Vicente, V. Blanco-Gozalo, et al., Preventive effect of cardiotrophin-1 administration before DSS-Induced ulcerative colitis in mice, J. Clin. Med. 8(12) (2019) 2086. https://doi.org/10.3390/jcm8122086.
Crossref Google Scholar
[6]

P. Tian, R. Zou, L. Song, et al., Ingestion of Bifidobacterium longum subspecies infantis strain CCFM687 regulated emotional behavior and the central BDNF pathway in chronic stress-induced depressive mice through reshaping the gut microbiota, Food Funct. 10(11) (2019) 7588-7598. https://doi.org/10.1039/c9fo01630a.
Crossref Google Scholar
[7]

J. Liang, S.M. Sha, K.C. Wu, Role of the intestinal microbiota and fecal transplantation in inflammatory bowel diseases, J. Dig. Dis. 15(12) (2014) 641-646. https://doi.org/10.1111/1751-2980.12211.
Crossref Google Scholar
[8]

A.D. Kostic, R.J. Xavier, G. Dirk, The microbiome in inflammatory bowel disease: current status and the future ahead, Gastroenterology 146(6) (2014) 1489-1499. https://doi.org/10.1053/j.gastro.2014.02.009.
Crossref Google Scholar
[9]

P.R. Marteau, M. de Vrese, C.J. Cellier, et al., Protection from gastrointestinal diseases with the use of probiotics, Am. J. Clin. Nutr. 73(2 Suppl) (2001) 430S-436S. https://doi.org/10.1093/ajcn/73.2.430s.
Crossref Google Scholar
[10]

J. Singh, A. Rivenson, M. Tomita, et al., Bifidobacterium longum, a lactic acid-producing intestinal bacterium inhibits colon cancer and modulates the intermediate biomarkers of colon carcinogenesis, Carcinogenesis 18(4) (1997) 833-841. https://doi.org/10.1093/carcin/18.4.833.
Crossref Google Scholar
[11]

F. Turroni, V. Taverniti, P. Ruas-Madiedo, et al., Bifidobacterium bifidum PRL2010 modulates the host innate immune response, Appl. Environ. Microb. 80(2) (2014) 730-740. https://doi.org/10.1128/AEM.03313-13.
Crossref Google Scholar
[12]

S. Yamazaki, T. Kaneko, N. Taketomo, et al., 2-Amino-3-carboxy-1,4-naphthoquinone affects the end-product profile of bifidobacteria through the mediated oxidation of NAD(P)H, Appl. Microbiol. Biot. 59(1) (2002) 72-78. https://doi.org/10.1007/s00253-002-0982-z.
Crossref Google Scholar
[13]

J. Stephani, K. Radulovic, J.H. Niess, Gut microbiota, probiotics and inflammatory bowel disease, Arch. Immunol. Ther. Exp. (Warsz). 59(3) (2011) 161-177. https://doi.org/10.1007/s00005-011-0122-5.
Crossref Google Scholar
[14]

D. Meng, W.S. Zhu, K. Ganguli, et al., Anti-inflammatory effects of Bifidobacterium longum subspinfantis secretions on fetal human enterocytes are mediated by TLR-4 receptors, Am. J. Physiol. Gastrointest. Liver Physiol. 311(4) (2016) G744-G753. https://doi.org/10.1152/ajpgi.00090.2016.
Crossref Google Scholar
[15]

K.R. Bergmann, R. Tian, A. Kushnir, et al., Bifidobacteria stabilize claudins at tight junctions and prevent intestinal barrier dysfunction in mouse necrotizing enterocolitis, Am. J. Pathol. 182(5) (2013) 1595-1606. https://doi.org/10.1016/j.ajpath.2013.01.013.
Crossref Google Scholar
[16]

X.Y. Gao, Q.H. Xie, L. Liu, et al., Metabolic adaptation to the aqueous leaf extract of Moringa oleifera Lam. supplemented diet is related to the modulation of gut microbiota in mice, Appl. Microbiol. Biot. 101(12) (2017) 5115-5130. https://doi.org/10.1007/s00253-017-8233-5.
Crossref Google Scholar
[17]

F. Bäckhed, H. Ding, T. Wang, et al., The gut microbiota as an environmental factor that regulates fat storage, Proc. Natl. Acad. Sci. USA. 101(44) (2004) 15718-15723. https://doi.org/10.1073/pnas.0407076101.
Crossref Google Scholar
[18]

P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, et al., An obesity-associated gut microbiome with increased capacity for energy harvest, Nature 444(7122) (2006) 1027-1031. https://doi.org/10.1038/nature05414.
Crossref Google Scholar
[19]

L.L. Fan, S. Zuo, H.Z. Tan, et al., Preventive effects of pectin with various degrees of esterification on ulcerative colitis in mice, Food Funct. 11(4) (2020) 2886-2897. https://doi.org/10.1039/c9fo03068a.
Crossref Google Scholar
[20]

A. Zarrinpar, A. Chaix, Z.Z. Xu, et al., Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signaling and colonic metabolism, Nat. Commun. 9(1) (2018) 2872. https://doi.org/10.1038/s41467-018-05336-9.
Crossref Google Scholar
[21]

D.H. Reikvam, A. Erofeev, A. Sandvik, et al., Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression, PLoS One 6(3) (2011) e17996. https://doi.org/10.1371/journal.pone.0017996.
Crossref Google Scholar
[22]

H.S. Cooper, S.N. Murthy, R.S. Shah, et al., Clinicopathologic study of dextran sulfate sodium experimental murine colitis, Lab. Invest. 69(2) (1993) 238-249.
Google Scholar
[23]

X.T. Zhou, W.C. Qi, T. Hong, et al., Exopolysaccharides from Lactobacillus plantarum NCU116 regulate intestinal epithelial barrier function via STAT3 signaling pathway, J. Agric. Food Chem. 66(37) (2018) 9719-9727. https://doi.org/10.1021/acs.jafc.8b03340.
Crossref Google Scholar
[24]

A. Sulaiman, H. Zuzana, S. Behnam, et al., Dynamics of early histopathological changes in GVHD after busulphan/cyclophosphamide conditioning regimen, Int. J. Clin. Exp. Patho. 4(6) (2011) 596-605.
Google Scholar
[25]

B. Chassaing, J.D. Aitken, M. Malleshappa, et al., Dextran sulfate sodium (DSS)-induced colitis in mice, Curr. Protoc. Immunol. 104(1) (2014) 1-14. https://doi.org/10.1002/0471142735.im1525s104.
Crossref Google Scholar
[26]

P.D. Cani, S. Possemiers, Y. Guiot, et al., Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability, Gut 58(8) (2009) 1091-1103. https://doi.org/10.1136/gut.2008.165886.
Crossref Google Scholar
[27]

H. Tan, J. Zhao, H. Zhang, et al., Novel strains of Bacteroides fragilis and Bacteroides ovatus alleviate the LPS-induced inflammation in mice, Appl. Microbiol. Biotechnol. 103(5) (2019) 2353-2365. https://doi.org/10.1007/s00253-019-09617-1.
Crossref Google Scholar
[28]

L. Zhao, F. Zhang, X. Ding, et al., Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes, Science 359(6380) (2018) 1151-1156. https://doi.org/10.1126/science.aao5774.
Crossref Google Scholar
[29]

J. Zhou, Z. Zhou, P. Ji, et al., Effect of fecal microbiota transplantation on experimental colitis in mice, Exp. Ther. Med. 17(4) (2019) 2581-2586. https://doi.org/10.3892/etm.2019.7263.
Crossref Google Scholar
[30]

M. Lleal, G. Sarrabayrouse, J. Willamil, et al., A single faecal microbiota transplantation modulates the microbiome and improves clinical manifestations in a rat model of colitis, Ebio. Medicine 48 (2019) 630-641. https://doi.org/10.1016/j.ebiom.2019.10.002.
Crossref Google Scholar
[31]

M. Harbord, R. Eliakim, D. Bettenworth, et al., Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo-anal pouch disorders, J. Crohns. Colitis 11(6) (2017) 649-670. https://doi.org/10.1093/ecco-jcc/jjx008.
Crossref Google Scholar
[32]

D. Pizzuti, M. Bortolami, E. Mazzon, et al., Transcriptional downregulation of tight junction protein ZO-1 in active coeliac disease is reversed after a gluten-free diet, Dig. Liver Dis. 36(5) (2004) 337-341. https://doi.org/10.1016/j.dld.2004.01.013.
Crossref Google Scholar
[33]

B. Xu, Y. Li, M. Xu, et al., Geniposide ameliorates TNBS-induced experimental colitis in rats via reducing inflammatory cytokine release and restoring impaired intestinal barrier function, Acta. Pharmacol. Sin. 38(5) (2017) 688-698. https://doi.org/10.1038/aps.2016.168.
Crossref Google Scholar
[34]

S. Stefan, R. Andreas, P. Ralf, et al., Increased activation of isolated intestinal lamina propria mononuclear cells in inflammatory bowel disease, Gastroenterology 101(4) (1991) 1020-1030. https://doi.org/10.1016/0016-5085(91)90729-5.
Crossref Google Scholar
[35]

G.D. Buffinton, W.F. Doe, Depleted mucosal antioxidant defences in inflammatory bowel disease, Free Radic Biol. Med. 19(6) (1995) 911-918. https://doi.org/10.1016/0891-5849(95)94362-h.
Crossref Google Scholar
[36]

A.E.V. Quaglio, A.C.S. Castilho, L.C.D. Stasi, Experimental evidence of heparanase, Hsp70 and NF-κB gene expression on the response of anti-inflammatory drugs in TNBS-induced colonic inflammation, Life Sci. 141 (2015) 179-187. https://doi.org/10.1016/j.lfs.2015.09.023.
Crossref Google Scholar
[37]

R. Toumi, I. Soufli, H. Rafa, et al., Probiotic bacteria lactobacillus and bifidobacterium attenuate inflammation in dextran sulfate Sodium-Induced experimental colitis in mice, Int. J. Immunopathol. Ph. 27(4) (2014) 615-627. https://doi.org/10.1177/039463201402700418.
Crossref Google Scholar
[38]

L. Zuo, K.T. Yuan, L. Yu, et al., Bifidobacterium infantis attenuates colitis by regulating T cell subset responses, World J. Gastroenterol. 20(48) (2014) 18316-18329. https://doi.org/10.3748/wjg.v20.i48.18316.
Crossref Google Scholar
[39]

C.Z. Lin, X.L. Cai, J. Zhang, et al., Role of gut microbiota in the development and treatment of colorectal cancer, Digestion 100(1) (2019) 72-78. https://doi.org/10.1159/000494052.
Crossref Google Scholar
[40]

S. Fukuda, H. Toh, K. Hase, et al., Bifidobacteria can protect from enteropathogenic infection through production of acetate, Nature 469(7331) (2011) 543-547. https://doi.org/10.1038/nature09646.
Crossref Google Scholar
[41]

E. Hosseini, C. Grootaert, W. Verstraete, et al., Propionate as a health-promoting microbial metabolite in the human gut, Nutr Rev. 69(5) (2011) 245-258. https://doi.org/10.1111/j.1753-4887.2011.00388.x.
Crossref Google Scholar
[42]

R.K. Cruz-Bravo, R.G. Guevara-González, M. Ramos-Gómez M, et al., The fermented non-digestible fraction of common bean (Phaseolus vulgaris L.) triggers cell cycle arrest and apoptosis in human colon adenocarcinoma cells, Genes Nutr. 9(1) (2014) 359. https://doi.org/10.1007/s12263-013-0359-1.
Crossref Google Scholar
[43]

W.J. Yang, T.M. Yu, X.S. Huang, et al., Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity, Nat. Commun. 11(1) (2020) 4457. https://doi.org/10.1038/s41467-020-18262-6.
Crossref Google Scholar
[44]

P. Gonçalves, I. Gregório, T.A. Catarino, et al., The effect of oxidative stress upon the intestinal epithelial uptake of butyrate, Eur. J. Pharmacol. 699(1-3) (2013) 88-100. https://doi.org/10.1016/j.ejphar.2012.11.029.
Crossref Google Scholar
[45]

K.Y. Fung, L. Cosgrove, T. Lockett, et al., A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate, Br. J. Nutr. 108(5) (2012) 820-831. https://doi.org/10.1017/S0007114512001948.
Crossref Google Scholar
[46]

M. Joossens, G. Huys, M. Cnockaert, et al., Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives, Gut 60(5) (2011) 631-637. https://doi.org/10.1136/gut.2010.223263.
Crossref Google Scholar
[47]

S.H. Shan, C.H. Wu, J.Y. Shi, et al., Inhibitory effects of peroxidase from Foxtail Millet Bran on colitis-associated colorectal carcinogenesis by the blockade of glycerophospholipid metabolism, J. Agric. Food Chem. 68(31) (2020) 8295-8307. https://doi.org/10.1021/acs.jafc.0c03257.
Crossref Google Scholar
[48]

N. Jiao, S.S. Baker, A. Chapa-Rodriguez, et al., Suppressed hepatic bile acid signalling despite elevated production of primary and secondary bile acids in NAFLD, Gut 67(10) (2018) 1881-1891. https://doi.org/10.1136/gutjnl-2017-314307.
Crossref Google Scholar
[49]

J. Zou, Y. Shen, M. Chen, et al., Lizhong decoction ameliorates ulcerative colitis in mice via modulating gut microbiota and its metabolites, Appl. Microbiol. Biotechnol. 104(13) (2020) 5999-6012. https://doi.org/10.1007/s00253-020-10665-1.
Crossref Google Scholar
[50]

J.A. Winston, C.M. Theriot, Diversification of host bile acids by members of the gut microbiota, Gut Microbes. 11(2) (2020) 158-171. https://doi.org/10.1080/19490976.2019.1674124.
Crossref Google Scholar
[51]

D. Chiara, R. Stefania, B. Fabiola, et al., Microbiota modification with probiotics induces hepatic bile acid synthesis via downregulation of the Fxr-Fgf15 axis in mice, Cell Rep. 7(1) (2014) 12-18. https://doi.org/10.1016/j.celrep.2014.02.032.
Crossref Google Scholar
Food Science and Human Wellness
Volume 12 Issue 4,
July 2023
Pages 1109-1118
DOI: 10.1016/j.fshw.2022.10.028
Cite this article:
Chen M, Yao H, Tan H, et al. Impact of Bifidobacterium longum NSP001 on DSS-induced colitis in conventional and humanised mice. Food Science and Human Wellness, 2023, 12(4): 1109-1118. https://doi.org/10.1016/j.fshw.2022.10.028

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Received: 17 January 2021
Revised: 28 February 2021
Accepted: 24 March 2021
Published: 18 November 2022
© 2023 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

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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