Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
European Journal of Nutrition
Published in: European Journal of Nutrition 1/2021

01-02-2021 | Respiratory Microbiota | Original Contribution

Alleviation effects of Bifidobacterium breve on DSS-induced colitis depends on intestinal tract barrier maintenance and gut microbiota modulation

Authors: Yang Chen, Yan Jin, Catherine Stanton, R. Paul Ross, Jianxin Zhao, Hao Zhang, Bo Yang, Wei Chen

Published in: European Journal of Nutrition | Issue 1/2021

Login to get access

Abstract

Purpose

The study aimed to investigate the discrepancy and potential mechanisms of different CLA-producing B. breve on dextran sulphate sodium (DSS)-induced colitis.

Methods

Colitis was induced in C57BL/6 J mice using DSS. Disease activity index (DAI), histopathological changes, epithelial barrier integrity and epithelial apoptosis were determined. Gut microbiota were gauged to evaluate the systemic effects of CLA-producing B. breve.

Results

Oral administration of different B. breve showed different effects, in which B. breve M1 and B. breve M2 alleviated the inflammation induced by DSS as well as significantly increased the concentration of mucin2 (MUC2) and goblet cells, but neither B. breve M3 nor B. breve M4 had those protective effects. Meanwhile, B. breve M1 and B. breve M2 treatments significantly up-regulated the tight junction (TJ) proteins and ameliorated the epithelial apoptosis lead by DSS challenge. Moreover, inflammatory cytokines (TNF-α, IL-6) were modulated by B. breve M1 and B. breve M2, neither B. breve M3 nor B. breve M4. Furthermore, B. breve M1 and B. breve M2 reduced the abundance of Bacteroides and increased the abundance of Odoribacter, then rebalanced the damaged gut microbiota. Colonic CLA concentrations in mice fed with B. breve M1, B. breve M2, B. breve M3 and B. breve M4 decreased successively, which showed significant positive correlation with the effectiveness of relieving colitis.

Conclusions

Bifidobacterium breve M1 and B. breve M2 alleviated DSS-induced colitis by producing CLA, inhibiting the inflammatory cytokines, maintaining of the intestinal epithelial barrier and regulating the gut microbiota.
Appendix
Available only for authorised users
Literature
1.
Molodecky NA, Soon S, Rabi DM, Ghali WA, Ferris M, Chernoff G et al (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142:46–54PubMed
2.
Sairenji T, Collins KL, Evans DV (2017) An update on inflammatory bowel disease. Prim Care 44:673–692PubMed
3.
Hanauer SB (2006) Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis 12:S3–S9PubMed
4.
Ungaro R, Mehandru S, Allen PB, Peyrin-Biroulet L, Colombel JF (2017) Ulcerative colitis. Lancet 389:1756–1770
5.
Green JR, Lobo AJ, Holdsworth CD, Leicester RJ, Gibson JA, Kerr GD et al (1998) Balsalazide is more effective and better tolerated than mesalamine in the treatment of acute ulcerative colitis. Gastroenterology 114:15–22PubMed
6.
Pearson C (2004) Inflammatory bowel disease. Clin Adv Nutr 100:86–90
7.
Osman N, Adawi D, Molin G, Ahrne S, Berggren A, Jeppsson B (2006) Bifidobacterium infantis strains with and without a combination of oligofructose and inulin (OFI) attenuate inflammation in DSS-induced colitis in rats. BMC Gastroenterol 6:6–31
8.
Bassaganya-Riera J, Hontecillas R (2006) CLA and n-3 PUFA differentially modulate clinical activity and colonic PPAR-responsive gene expression in a pig model of experimental IBD. Clin Nutr 25:454–465PubMed
9.
Bassaganya-Riera J, Reynolds K, Martino-Catt S, Cui Y, Hennighausen L, Gonzalez F (2004) Hontecillas, Activation of PPAR [gamma] and [delta] by conjugated linoleic acid mediates protection from experimental inflammatory bowel disease. Gastroenterology 127:777–791PubMed
10.
Clément L, Poirier H, Niot I, Bocher V, Guerre-Millo M, Krief S et al (2002) Dietary trans-10, cis-12 conjugated linoleic acid induces hyperinsulinemia and fatty liver in the mouse. J Lipid Res 43:1400–1409PubMed
11.
Kelley DS, Bartolini GL, Warren JM, Simon VA, Mackey BE, Erickson KL (2004) Contrasting effects of t10, c12- and c9, t11-conjugated linoleic acid isomers on the fatty acid profiles of mouse liver lipids. Lipids 39:135–141PubMed
12.
Jaudszus A, Moeckel P, Hamelmann E, Jahreis G (2010) Trans-10, cis-12-CLA-caused lipodystrophy is associated with profound changes of fatty acid profiles of liver, white adipose tissue and erythrocytes in mice: possible link to tissue-specific alterations of fatty acid desaturation. Ann Nutr Metab 57:103–111PubMed
13.
Takahashi Y, Kushiro M, Shinohara K, Ide T (2003) Activity and mRNA levels of enzymes involved in hepatic fatty acid synthesis and oxidation in mice fed conjugated linoleic acid. BBA-Mol Cell Biol L 1631:265–273
14.
Rasooly R, Kelley DS, Greg J, Mackey BE, Belury MA, Belury MA et al (2007) Dietary trans 10, cis 12-conjugated linoleic acid reduces the expression of fatty acid oxidation and drug detoxification enzymes in mouse liver. Brit J Nutr 97:58–66PubMed
15.
Coakley M, Ross RP, Nordgren M, Fitzgerald G, Devery R, Stanton C (2003) Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. J Appl Microbiol 94:138–145PubMed
16.
Chung SH, Kim IH, Park HG, Kang HS, Yoon CS, Jeong HY et al (2008) Synthesis of conjugated linoleic acid by human-derived Bifidobacterium breve LMC 017: utilization as a functional starter culture for milk fermentation. J Agric Food Chem 56:3311–3316PubMed
17.
Kepler CR, Tucker WP, Tove SB (1971) Biohydrogenation of unsaturated fatty acids. V. Stereospecificity of proton addition and mechanism of action of linoleic acid Δ12-cis, Δ11-trans-isomerase from Butyrivibrio fibrisolvens. J Biol Chem 246:2765–2771PubMed
18.
Raimondi S, Amaretti A, Leonardi A, Quartieri A, Gozzoli C, Rossi M (2016) Conjugated linoleic acid production by bifidobacteria: screening, kinetic, and composition. Biomed Res Int 2016:1–9
19.
Wang J, Chen H, Yang B, Gu Z, Zhang H, Chen W et al (2016) Lactobacillus plantarum ZS2058 produces CLA to ameliorate DSS-induced acute colitis in mice. RSC Adv 6:14457–14464
20.
Yang B, Chen H, Gao H, Wang J, Stanton C, Ross RP et al (2018) Bifidobacterium breve CCFM683 could ameliorate DSS-induced colitis in mice primarily via conjugated linoleic acid production and gut microbiota modulation. J Funct Foods 49:61–72
21.
Yang B, Chen H, Gu Z, Tian F, Ross RP, Stanton C et al (2014) Synthesis of conjugated linoleic acid by the linoleate isomerase complex in food-derived lactobacilli. J Appl Microbiol 117:430–439PubMedPubMedCentral
22.
Fang Z, Li L, Liu X, Lu W, Zhao J, Zhang H et al (2019) Strain-specific ameliorating effect of Bifidobacterium longum on atopic dermatitis in mice. J Funct Foods 60:103426
23.
Mennigen R, Nolte K, Rijcken E, Utech M, Loeffler B, Senninger N et al (2009) Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol-Gastr L 296:G1140–G1149
24.
Murthy SNS, Cooper HS, Shim H, Shah RS, Ibrahim SA, Sedergran DJ (1993) Treatment of dextran sulfate sodium-induced murine colitis by intra colonic cyclosporine. Digest Dis Sci 38:1722–1734PubMed
25.
Rees V (1998) Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol 114:385–391PubMed
26.
Steedman HF (1950) Alcian blue 8GS: a new stain for mucin. J Cell Sci 91:477–479
27.
Wu H, Ye L, Lu X, Xie S, Yang Q, Yu Q (2018) Lactobacillus acidophilus alleviated Salmonella-induced goblet cells loss and colitis by Notch pathway. Mol Nutr Food Res 62:1800552
28.
Tan GX, Wang XN, Tang YY, Cen WJ, Li ZH, Wang GC et al (2019) PP22 promotes autophagy and apoptosis in the nasopharyngeal carcinoma cell line CNE-2 by inducing endoplasmic reticulum stress, down regulating STAT3 signaling, and modulating the MAPK pathway. J Cell Physiol 234:2618–2630PubMed
29.
Classics Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
30.
Schwenke DC (2002) Alpha-tocopherol protects against diet induced atherosclerosis in New Zealand white rabbits. J Lipid Res 43:1927–1938PubMed
31.
Yang Q, Wang S, Ji Y, Chen H, Zhang H, Chen W et al (2017) Dietary intake of n-3 PUFAs modifies the absorption, distribution and bioavailability of fatty acids in the mouse gastrointestinal tract. Lipids Health Dis 16:10PubMedPubMedCentral
32.
Yan S, Yang B, Zhao J, Zhao J, Stanton C, Ross RP et al (2019) A ropy exopolysaccharide producing strain Bifidobacterium longum subsp. longum YS108R alleviates DSS-induced colitis by maintenance of the mucosal barrier and gut microbiota modulation. Food Funct 10:1595–1608PubMed
33.
Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M (2014) Dextran sulfate sodium (DSS)-induced colitis in mice. Curr Protoc Immunol 104:15–25PubMed
34.
Zwolinska-Wcislo M, Brzozowski T, Ptak-Belowska A, Targosz A, Urbanczyk K, Kwiecien S et al (2011) Nitric oxide-releasing aspirin but not conventional aspirin improves healing of experimental colitis. World J Gastroenterol 17:4076–4089PubMedPubMedCentral
35.
Xing J, You C, Dong K, Sun J, You H, Dong Y et al (2013) Ameliorative effects of 3,4-oxo-isopropylidene-shikimic acid on experimental colitis and their mechanisms in rats. Int Immunopharmacol 15:524–531PubMed
36.
Peterson LW, Artis D (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14:141–153PubMed
37.
Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12:319–330PubMedPubMedCentral
38.
Hansson GC (2012) Role of mucus layers in gut infection and inflammation. Curr Opin Microbio 15:57–62
39.
Van Klinken BJ, Van der Wal JW, Einerhand AW, Buller HA, Dekker J (1999) Sulphation and secretion of the predominant secretory human colonic mucin MUC2 in ulcerative colitis. Gut 44:387–393PubMedPubMedCentral
40.
Theodoratou E, Campbell H, Ventham NT, Kolarich D, Pucic-Bakovic M, Zoldos V et al (2014) The role of glycosylation in IBD. Nat Rev Gastroenterol Hepatol 11:588–600PubMed
41.
Schmitz H, Barmeyer C, Fromm M, Runkel N, Foss HD, Bentzel CJ et al (1999) Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis. Gastroenterology 116:301–309PubMed
42.
Shen L, Weber CR, Raleigh DR, Yu D, Turner JR (2011) Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73:283–309PubMedPubMedCentral
43.
Ivanov AI, Naydenov NG (2013) Dynamics and regulation of epithelial adherens junctions: recent discoveries and controversies. Int Rev Cell Mol Biol 303:27–99PubMed
44.
Ivanov AI, Parkos CA, Nusrat A (2010) Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol 177:512–524PubMedPubMedCentral
45.
Zakostelska Z, Kverka M, Klimesova K, Rossmann P, Mrazek J, Kopecny J et al (2011) Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS ONE 6:e27961PubMedPubMedCentral
46.
Srutkova D, Schwarzer M, Hudcovic T, Zakostelska Z, Drab V, Spanova A et al (2015) Bifidobacterium longum CCM 7952 promotes epithelial barrier function and prevents acute DSS-induced colitis in strictly strain-specific manner. PLoS ONE 10:e0134050PubMedPubMedCentral
47.
Wang G, Xu Q, Jin X, Hang F, Liu Z, Zhao J et al (2018) Effects of lactobacilli with different regulatory behaviours on tight junctions in mice with dextran sodium sulphate-induced colitis. J Funct Foods 47:107–115
48.
Liu HY, Roos S, Jonsson H, Ahl D, Dicksved J, Lindberg JE et al (2015) Effects of lactobacillus johnsonii and lactobacillus reuteri on gut barrier function and heat shock proteins in intestinal porcine epithelial cells. Physiol Rep 3:e12355PubMedPubMedCentral
49.
Fei L, Xu K (2016) Zhikang Capsule ameliorates dextran sodium sulfate-induced colitis by inhibition of inflammation, apoptosis, oxidative stress and MyD88-dependent TLR4 signaling pathway. J Ethnopharmacol 192:236–247PubMed
50.
Hegazy SK (2010) Effect of probiotics on pro-inflammatory cytokines and NF-κB activation in ulcerative colitis. World J Gastroenterol 16:4145–4151PubMedPubMedCentral
51.
Horiuchi T, Mitoma H, Harashima S, Tsukamoto H, Shimoda T (2010) Transmembrane TNF-alpha: structure, function and interaction with anti-TNF agents. Rheumatology (Oxford) 49:1215–1228
52.
Lee IA, Bae EA, Lee JH, Lee H, Ahn YT, Huh CS et al (2010) Bifidobacterium longum HY8004 attenuates TNBS-induced colitis by inhibiting lipid peroxidation in mice. Inflamm Res 59:359–368PubMed
53.
Jin S, Zhao D, Cai C, Song D, Shen J, Xu A et al (2017) Low-dose penicillin exposure in early life decreases Th17 and the susceptibility to DSS colitis in mice through gut microbiota modification. Sci Rep 7:43662PubMedPubMedCentral
54.
Fujio-Vejar S, Vasquez Y, Morales P, Magne F, Vera-Wolf P, Ugalde JA et al (2017) The gut microbiota of healthy Chilean subjects reveals a high abundance of the phylum Verrucomicrobia. Front Microbiol 8:1–11
55.
Torres PJ, Siakowska M, Banaszewska B, Pawelczyk L, Duleba AJ, Kelley ST et al (2018) Gut microbial diversity in women with polycystic ovary syndrome correlates with hyperandrogenism. J Clin Endocr Metab 103:1502–1511PubMed
56.
Gomez-Arango LF, Barrett H, McIntyre D, Callaway LK, Morrison M, Nitert MD (2016) Increased systolic and diastolic blood pressure is associated with altered gut microbiota composition and butyrate production in early pregnancy. Hypertension 68:974–977PubMed
57.
Chen G, Ran X, Li B, Li Y, He D, Huang B et al (2018) Sodium butyrate inhibits inflammation and maintains epithelium barrier integrity in a TNBS-induced inflammatory bowel disease mice model. EBioMedicine 30:317–325PubMedPubMedCentral
58.
Chen L, Sun M, Wu W, Yang W, Huang X, Xiao Y (2019) Microbiota metabolite butyrate differentially regulates Th1 and Th17 cells’ differentiation and function in induction of colitis. Inflamm Bowel Dis 25:1450–1461PubMedPubMedCentral
59.
Kuwahara T, Yamashita A, Hirakawa H, Nakayama H, Toh H, Okada N et al (2004) Genomic analysis of Bacteroides fragilis reveals extensive DNA inversions regulating cell surface adaptation. Proc Natl Acad Sci 101:14919–14924PubMed
60.
Setoyama H, Imaoka A, Ishikawa H, Umesaki Y (2003) Prevention of gut inflammation by Bifidobacterium in dextran sulfate-treated gnotobiotic mice associated with Bacteroides strains isolated from ulcerative colitis patients. Microbes Infect 5:115–122PubMed
61.
Bamba T, Matsuda H, Endo M, Fujiyama Y (1995) The pathogenic role of Bacteroides vulgatus in patients with ulcerative colitis. J Gastroenterol 30:45–47PubMed
62.
Hudcovic T, Kozakova H, Kolinska J, Stepankova R, Hrncir T, Tlaskalova- Hogenova H (2009) Monocolonization with Bacteroides ovatus protects immu-nodeficient SCID mice from mortality in chronic intestinal inflammation caused by long-lasting dextran sodium sulfate treatment. Physiol Res 58:101–110PubMed
63.
Borniquel S, Jadert C, Lundberg JO (2012) Dietary conjugated linoleic acid activates PPARgamma and the intestinal trefoil factor in SW480 cells and mice with dextran sulfate sodium-induced colitis. J Nutr 142:2135–2140PubMed
64.
Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Carbo A, Shaykhutdinov R et al (2012) Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPAR gamma to suppress colitis. PLoS ONE 7:e31238PubMedPubMedCentral
65.
Chen Y, Yang B, Ross RP, Jin Y, Stanton C, Zhao J et al (2019) Orally administered CLA ameliorates DSS-induced colitis in mice via intestinal barrier improvement, oxidative stress reduction, and inflammatory cytokine and gut microbiota modulation. J Agric Food Chem 67:13282–13298
Metadata
Title
Alleviation effects of Bifidobacterium breve on DSS-induced colitis depends on intestinal tract barrier maintenance and gut microbiota modulation
Authors
Yang Chen
Yan Jin
Catherine Stanton
R. Paul Ross
Jianxin Zhao
Hao Zhang
Bo Yang
Wei Chen
Publication date
01-02-2021
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2021
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-020-02252-x

Other articles of this Issue 1/2021

European Journal of Nutrition 1/2021 Go to the issue

Original Contribution

The anserine to carnosine ratio: an excellent discriminator between white and red meats consumed by free-living overweight participants of the PREVIEW study

Original Contribution

Food matrix structure (from Biscuit to Custard) has an impact on folate bioavailability in healthy volunteers

Original Contribution

Enrichment of bread with beta-glucans or resistant starch induces similar glucose, insulin and appetite hormone responses in healthy adults

Original Contribution

Influence of total sugar intake on metabolic blood markers at 8 years of age in the Childhood Obesity Project

Original Contribution

Preconceptional diet quality is associated with birth outcomes among low socioeconomic status minority women in a high-income country

Original Contribution

Association of magnesium intake and vitamin D status with cognitive function in older adults: an analysis of US National Health and Nutrition Examination Survey (NHANES) 2011 to 2014
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits