<i>Blautia producta</i> displays potential probiotic properties against dextran sulfate sodium-induced colitis in mice

Bingyong Mao; Weiling Guo; Shumao Cui; Qiuxiang Zhang; Jianxin Zhao; Xin Tang; Hao Zhang

doi:10.26599/FSHW.2022.9250060

Food Science and Human Wellness 2024, 13(2): 709-720 https://doi.org/10.26599/FSHW.2022.9250060

Open Access | Issue | Published: 25 September 2023

Blautia producta displays potential probiotic properties against dextran sulfate sodium-induced colitis in mice

Show Author's Information Hide Author's Information Bingyong Mao^{^a^,^b^,}, Weiling Guo^{^a^,^b}, Shumao Cui^{^a^,^b}, Qiuxiang Zhang^{^a^,^b}, Jianxin Zhao^{^a^,^b}, Xin Tang^{^a^,^b}(

), Hao Zhang^{^a^,^b^,^c}

State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China

School of Food Science and Technology, Jiangnan University, Wuxi 214122, China

National Engineering Research Center for Functional Food, Jiangnan University, Wuxi 214122, China

Peer review under responsibility of Tsinghua University Press.

Keywords:

TLR4/NF-κB pathway, Colitis, Blautia producta D4, Intestinal mechanical barrier, Intestinal microbiot

Cite this article:

Mao B, Guo W, Cui S, et al. Blautia producta displays potential probiotic properties against dextran sulfate sodium-induced colitis in mice. Food Science and Human Wellness, 2024, 13(2): 709-720. https://doi.org/10.26599/FSHW.2022.9250060

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Abstract Full text Electronic supplementary material About this article

Abstract

Blautia has attracted attention because of its potential efficacy in ameliorating host energy metabolism and inflammation. This study aims to investigate the influences of Blautia producta D4 on colitis induced by dextran sulfate sodium (DSS) and to reveal the underlying mechanisms. Results showed that B. producta D4 intervention significantly relieved body weight loss, and suppressed the elevation of pro-inflammatory cytokines (including interleukin-6 (IL-6), tumor necrosis factor-α (TNF-α), and interleukin-1β (IL-1β)) and excessive oxidative stress (myeloperoxidease (MPO) activity, superoxide dismutase (SOD) activity, glutathione peroxidase (GSH-Px) activity, and malondialdehyde (MDA) level) in colitis mice. Moreover, the concentrations of tight junction proteins (occludin, claudin-1, and ZO-1) related to the intestinal barrier were obviously elevated, and colitis-related TLR4/NF-κB pathway activation was remarkably inhibited after B. producta D4 intervention. The intestinal microbial disorder was evidently ameliorated by increasing the relative abundance of Clostridium sensu stricto 1, Bifidobacterium, GCA-900066225, Enterorhabdus, and reducing the relative abundance of Lachnospiraceae NK4A136 group. In conclusion, oral administration of B. producta D4 could ameliorate DSS-induced colitis by suppressing inflammatory responses, maintaining the intestinal barrier, inhibiting TLR4/NF-κB pathway, and regulating intestinal microbiota balance. These results are conducive to accelerate the development of B. producta D4 as a functional probiotic for colitis.

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About this article

Blautia producta displays potential probiotic properties against dextran sulfate sodium-induced colitis in mice

Show Author's information Hide Author's Information Bingyong Mao^{^a^,^b^,}, Weiling Guo^{^a^,^b}, Shumao Cui^{^a^,^b}, Qiuxiang Zhang^{^a^,^b}, Jianxin Zhao^{^a^,^b}, Xin Tang^{^a^,^b}(

), Hao Zhang^{^a^,^b^,^c}

State Key Laboratory of Food Science and Resources, Jiangnan University, Wuxi 214122, China

School of Food Science and Technology, Jiangnan University, Wuxi 214122, China

National Engineering Research Center for Functional Food, Jiangnan University, Wuxi 214122, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Keywords: TLR4/NF-κB pathway, Colitis, Blautia producta D4, Intestinal mechanical barrier, Intestinal microbiot

References(51)

[1]

D. van der Lelie, A. Oka, S. Taghavi, et al., Rationally designed bacterial consortia to treat chronic immune-mediated colitis and restore intestinal homeostasis, Nat. Commun. 12 (2021) 3105. https://doi.org/10.1038/s41467-021-23460-x.

DOI Google Scholar

[2]

J.F. Colombel, U. Mahadevan, Inflammatory bowel disease 2017: innovations and changing paradigms, Gastroenterology 152 (2017) 309-912. https://doi.org/10.1053/j.gastro.2016.12.004.

DOI Google Scholar

[3]

S.M. Vindigni, T.L. Zisman, D.L. Suskind, et al., The intestinal microbiome, barrier function, and immune system in inflammatory bowel disease: a tripartite pathophysiological circuit with implications for new therapeutic directions, Therap. Adv. Gastroenterol. 9 (2016) 606-625. https://doi.org/10.1177/1756283x16644242.

DOI Google Scholar

[4]

E. Salvo Romero, C. Alonso Cotoner, C. Pardo Camacho, et al., The intestinal barrier function and its involvement in digestive disease, Rev. Esp. Enferm. Dig. 107 (2015) 686-696. https://doi.org/10.17235/reed.2015.3846/2015.

DOI Google Scholar

[5]

D. Bergemalm, E. Andersson, J. Hultdin, et al., Systemic inflammation in preclinical ulcerative colitis, Gastroenterology 161 (2021) 1526-1539. https://doi.org/10.1053/j.gastro.2021.07.026.

DOI Google Scholar

[6]

W. Liu, Y. Zhang, B. Qiu, et al., Quinoa whole grain diet compromises the changes of gut microbiota and colonic colitis induced by dextran Sulfate sodium in C57BL/6 mice, Sci. Rep. 8 (2018) 14916. https://doi.org/10.1038/s41598-018-33092-9.

DOI Google Scholar

[7]

J. Jin, S. Wu, Y. Xie, et al., Live and heat-killed cells of Lactobacillus plantarum Zhang-LL ease symptoms of chronic ulcerative colitis induced by dextran sulfate sodium in rats, J. Funct. Foods 71 (2020) 103994. https://doi.org/10.1016/j.jff.2020.103994.

DOI Google Scholar

[8]

S.M. Lim, J.J. Jeong, S.E. Jang, et al., A mixture of the probiotic strains Bifidobacterium longum CH57 and Lactobacillus brevis CH23 ameliorates colitis in mice by inhibiting macrophage activation and restoring the Th17/Treg balance, J. Funct. Foods 27 (2016) 295-309. https://doi.org/10.1016/j.jff.2016.09.011.

DOI Google Scholar

[9]

S.M. Cui, J.Y. Gu, X.M. Liu, et al., Lactulose significantly increased the relative abundance of Bifidobacterium and Blautia in mice feces as revealed by 16S rRNA amplicon sequencing, J. Sci. Food Agric. 101 (2021) 5721-5729. https://doi.org/10.1002/jsfa.11181.

DOI Google Scholar

[10]

S. Kalyana Chakravarthy, R. Jayasudha, G. Sai Prashanthi, et al., Dysbiosis in the gut bacterial microbiome of patients with uveitis, an inflammatory disease of the eye, Indian J. Microbiol. 58 (2018) 457-469. https://doi.org/10.1007/s12088-018-0746-9.

DOI Google Scholar

[11]

X.M. Liu, W.L. Guo, S.M. Cui, et al., A comprehensive assessment of the safety of Blautia producta DSM 2950, Microorganisms 9 (2021). https://doi.org/10.3390/microorganisms9050908.

DOI Google Scholar

[12]

N. Ozato, S. Saito, T. Yamaguchi, et al., Blautia genus associated with visceral fat accumulation in adults 20-76 years of age, NPJ Biofilms Microbi. 5 (2019) 28. https://doi.org/10.1038/s41522-019-0101-x.

DOI Google Scholar

[13]

Q. Liu, H. Tian, Y. Kang, et al., Probiotics alleviate autoimmune hepatitis in mice through modulation of gut microbiota and intestinal permeability, J. Nutr. Biochem. 98 (2021) 108863. https://doi.org/10.1016/j.jnutbio.2021.108863.

DOI Google Scholar

[14]

S.G. Pathmanathan, B. Lawley, M. McConnell, et al., Gut bacteria characteristic of the infant microbiota down-regulate inflammatory transcriptional responses in HT-29 cells, Anaerobe 61 (2020) 102112. https://doi.org/10.1016/j.anaerobe.2019.102112.

DOI Google Scholar

[15]

R. Mennigen, M. Bruewer, Effect of probiotics on intestinal barrier function, Ann. N. Y. Acad. Sci. 1165 (2009) 183-189. https://doi.org/10.1111/j.1749-6632.2009.04059.x.

DOI Google Scholar

[16]

Y. Xia, Y. Chen, G. Wang, et al., Lactobacillus plantarum AR113 alleviates DSS-induced colitis by regulating the TLR4/MyD88/NF-κB pathway and gut microbiota composition, J. Funct. Foods 67 (2020) 103854. https://doi.org/10.1016/j.jff.2020.103854.

DOI Google Scholar

[17]

B. Yang, H. Chen, H. Gao, et al., Bifidobacterium breve CCFM683 could ameliorate DSS-induced colitis in mice primarily via conjugated linoleic acid production and gut microbiota modulation, J. Funct. Foods 49 (2018) 61-72. https://doi.org/10.1016/j.jff.2018.08.014.

DOI Google Scholar

[18]

J. Wang, C. Zhang, C. Guo, et al., Chitosan ameliorates DSS-induced ulcerative colitis mice by enhancing intestinal barrier function and improving microflora, Int. J. Mol. Sci. 20 (2019) 5751. https://doi.org/10.3390/ijms20225751.

DOI Google Scholar

[19]

M. Wlodarska, C.A. Thaiss, R. Nowarski, et al., NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion, Cell 156 (2014) 1045-1059. https://doi.org/10.1016/j.cell.2014.01.026.

DOI Google Scholar

[20]

W.L. Guo, J.B. Guo, B.Y. Liu, et al., Ganoderic acid A from Ganoderma lucidum ameliorates lipid metabolism and alters gut microbiota composition in hyperlipidemic mice fed a high-fat diet, Food Funct. 11 (2020) 6818-6833. https://doi.org/10.1039/d0fo00436g.

DOI Google Scholar

[21]

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. doi: 10.1021/acs.jafc.1c01781.

DOI Google Scholar

[22]

Y. Qi, L. Chen, K. Gao, et al., Effects of Schisandra chinensis polysaccharides on rats with antibiotic-associated diarrhea, Int. J. Biol. Macromol. 124 (2019) 627-634. https://doi.org/10.1016/j.ijbiomac.2018.11.250.

DOI Google Scholar

[23]

K. Secombe, J. Bowen, J. Coller, et al., Pre-treatment Blautia abundance regulates chemotherapy-induced gastrointestinal toxicity risk: a pilot study, Asia-Pac. J. Clin. Oncol. 14 (2018) 59-59.

Google Scholar

[24]

DOI Google Scholar

[25]

S.K. Oh, D. Kim, K. Kim, et al., RORα is crucial for attenuated inflammatory response to maintain intestinal homeostasis, PNAS 116 (2019) 21140. https://doi.org/10.1073/pnas.1907595116.

DOI Google Scholar

[26]

W.T. Kuo, L. Zuo, M.A. Odenwald, et al., The tight junction protein ZO-1 is dispensable for barrier function but critical for effective mucosal repair, Gastroenterology 161 (2021). https://doi.org/10.1053/j.gastro.2021.08.047.

DOI Google Scholar

[27]

X. Chen, J. Shen, J.M. Zhao, et al., Cedrol attenuates collagen-induced arthritis in mice and modulates the inflammatory response in LPS-mediated fibroblast-like synoviocytes, Food Funct. 11(2020) 4752-4764. https://doi.org/10.1039/d0fo00549e.

DOI Google Scholar

[28]

J. Mauer, J.L. Denson, J.C. Brüning, Versatile functions for IL-6 in metabolism and cancer, Trends Immunol. 36 (2015) 92-101. https://doi.org/10.1016/j.it.2014.12.008.

DOI Google Scholar

[29]

S.D. Blackburn, E.J. Wherry, IL-10, T cell exhaustion and viral persistence, Trends Microbiol. 15 (2017) 143-146. https://doi.org/10.1016/j.tim.2007.02.006.

DOI Google Scholar

[30]

H. Li, Y. Wei, X. Li, et al., Diosmetin has therapeutic efficacy in colitis regulating gut microbiota, inflammation, and oxidative stress via the circ-Sirt1/Sirt1 axis, Acta Pharmacol. Sin. 43 (2021) 919-932. https://doi.org/10.1038/s41401-021-00726-0.

DOI Google Scholar

[31]

H.A.A. Elmaksoud, M.H. Motawea, A.A. Desoky, et al., Hydroxytyrosol alleviate intestinal inflammation, oxidative stress and apoptosis resulted in ulcerative colitis, Biomed. Pharmacother. 142 (2021) 112073. https://doi.org/10.1016/j.biopha.2021.112073.

DOI Google Scholar

[32]

B.C. Cruz, L.L. Conceição, T.A.O. Mendes, et al., Use of the synbiotic VSL#3 and yacon-based concentrate attenuates intestinal damage and reduces the abundance of Candidatus Saccharimonas in a colitis-associated carcinogenesis model, Food Res. Int. 137 (2020) 109721. https://doi.org/10.1016/j.foodres.2020.109721.

DOI Google Scholar

[33]

Y. Yang, H. Yan, M. Jing, et al., Andrographolide derivative AL-1 ameliorates TNBS-induced colitis in mice: involvement of NF-кB and PPAR-γ signaling pathways, Sci. Rep. 6 (2016) 29716. https://doi.org/10.1038/srep29716.

DOI Google Scholar

[34]

E.Y. Lin, H.J. Lai, Y.K. Cheng, et al., Neutrophil extracellular traps impair intestinal barrier function during experimental colitis, Biomedicines 8 (2020) 275. https://doi.org/10.3390/biomedicines8080275.

DOI Google Scholar

[35]

D. Yao, W. Shi, Y. Gou, et al., Fatty acid-mediated intracellular iron translocation: a synergistic mechanism of oxidative injury, Free Radic. Biol. Med. 39 (2005) 1385-1398. https://doi.org/10.1016/j.freeradbiomed.2005.07.015.

DOI Google Scholar

[36]

L. Fan, Y. Qi, S. Qu, et al., B. adolescentis ameliorates chronic colitis by regulating Treg/Th2 response and gut microbiota remodeling, Gut Microbes. 13 (2021) 1-17. https://doi.org/10.1080/19490976.2020.1826746.

DOI Google Scholar

[37]

B. Rupani, F.J. Caputo, A.C. Watkins, et al., Relationship between disruption of the unstirred mucus layer and intestinal restitution in loss of gut barrier function after trauma hemorrhagic shock, Surgery 141 (2007) 481-489. https://doi.org/10.1016/j.surg.2006.10.008.

DOI Google Scholar

[38]

C. Carrasco-Pozo, P.Morales, M. Gotteland, Polyphenols protect the epithelial barrier function of caco-2 cells exposed to indomethacin through the modulation of occludin and zonula occludens-1 expression, J. Agric. Food Chem. 61 (2013) 5291-5297. https://doi.org/10.1021/jf400150p.

DOI Google Scholar

[39]

M. Sun, W. Wu, L.Chen, et al., Microbiota-derived short-chain fatty acids promote Th1 cell IL-10 production to maintain intestinal homeostasis, Nat. Commun. 9 (2018) 3555. https://doi.org/10.1038/s41467-018-05901-2.

DOI Google Scholar

[40]

X.M. Liu, B.Y. Mao, J.Y. Gu, et al., Blautia-a new functional genus with potential probiotic properties? Gut Microbes. 13 (2021) 1-21. https://doi.org/10.1080/19490976.2021.1875796.

DOI Google Scholar

[41]

W. Yin, Y. Li, Y. Song, et al., CCRL2 promotes antitumor T-cell immunity via amplifying TLR4-mediated immunostimulatory macrophage activation, PNAS 118 (2021) e2024171118. https://doi.org/10.1073/pnas.2024171118.

DOI Google Scholar

[42]

Z. Bian, Y. Qin, L. Li, et al., Schisandra chinensis (Turcz.) Baill. protects against DSS-induced colitis in mice: Involvement of TLR4/NF-κB/NLRP3 inflammasome pathway and gut microbiota, J. Ethnopharmacol. (2022) 115570. https://doi.org/10.1016/j.jep.2022.115570.

DOI Google Scholar

[43]

J.B. Jeong, H.J. Jeong, Rheosmin, a naturally occurring phenolic compound inhibits LPS-induced iNOS and COX-2 expression in RAW264.7 cells by blocking NF-kappaB activation pathway, Food Chem. Toxicol. 48 (2010) 2148-53. https://doi.org/10.1016/j.fct.2010.05.020.

DOI Google Scholar

[44]

Y. Xing, R. Wang, D. Chen, et al., COX2 is involved in hypoxia-induced TNF-α expression in osteoblast, Sci. Rep. 5 (2015) 10020. https://doi.org/10.1038/srep10020.

DOI Google Scholar

[45]

A.R. Vanani, H. Kalantari, M. Mahdavinia, et al., Dimethyl fumarate reduces oxidative stress, inflammation and fat deposition by modulation of Nrf2, SREBP-1c and NF-κB signaling in HFD fed mice, Life Sci. 283 (2021) 119852. https://doi.org/10.1016/j.lfs.2021.119852.

DOI Google Scholar

[46]

S. Singh, S. Vrishni, B.K. Singh, et al., Nrf2-ARE stress response mechanism: a control point in oxidative stress-mediated dysfunctions and chronic inflammatory diseases, Free Radic. Res. 44 (2010) 1267-1288. https://doi.org/10.3109/10715762.2010.507670.

DOI Google Scholar

[47]

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.

DOI Google Scholar

[48]

S. Galie, J. Garcia-Gavilan, L. Camacho-Barcia, et al., Effects of the mediterranean diet or nut consumption on gut microbiota composition and fecal metabolites and their relationship with cardiometabolic risk factors, Mol. Nutr. Food Res. 65 (2021) e2000982. https://doi.org/10.1002/mnfr.202000982.

DOI Google Scholar

[49]

P. Konturek, Y. Zopf, W. Dieterich, et al., Rifaximin and Saccharomyces boulardii increase stress resilience in TNBS-induced colitis, J. Crohns Colitis. 12 (2018) S148-S148. https://doi.org/10.1093/ecco-jcc/jjx180.236.

DOI Google Scholar

[50]

W. Li, H. Yang, Q. Zhao, et al., Polyphenol-rich Loquat fruit extract prevents fructose-induced nonalcoholic fatty liver disease by modulating glycometabolism, lipometabolism, oxidative stress, inflammation, intestinal barrier, and gut microbiota in mice, J. Agric. Food Chem. 67 (2019) 7726-7737. https://doi.org/10.1021/acs.jafc.9b02523.

DOI Google Scholar

[51]

K. Huang, Y. Yan, D. Chen, et al., Ascorbic acid derivative 2-O-β-D-glucopyranosyl-L-ascorbic acid from the fruit of lycium barbarum modulates microbiota in the small intestine and colon and exerts an immunomodulatory effect on cyclophosphamide-treated BALB/c mice, J. Agric. Food Chem. 68 (2020) 11128-11143. https://doi.org/10.1021/acs.jafc.0c04253.

DOI Google Scholar

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Received: 23 March 2022

Revised: 11 July 2022

Accepted: 10 October 2022

Published: 25 September 2023

Issue date: March 2024

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This work was supported by National Natural Science Foundation of China (31972086, 32172173, 32072197) and Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province.

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