Top

European Journal of Nutrition

Published in:

01-10-2020 | Atopic Dermatitis | Original Contribution

Bifidobacteria adolescentis regulated immune responses and gut microbial composition to alleviate DNFB-induced atopic dermatitis in mice

Authors: Zhifeng Fang, Lingzhi Li, Jianxian Zhao, Hao Zhang, Yuan-Kun Lee, Wenwei Lu, Wei Chen

Published in: European Journal of Nutrition | Issue 7/2020

Abstract

Purpose

Emerging studies have reported gut microbial composition plays a key role in alleviating AD clinical symptoms during the probiotic intervention, but the correlation among clinical symptoms, immune responses and gut microbial alteration needs to be explored. Therefore, the objective was to investigate the correlation during Bifidobacterium adolescentis intervention in DNFB-induced AD mice.

Methods

The mice were randomly divided into nine groups and fed B. adolescentis for 3 weeks. At the end of the experiment, clinical and immune indicators were assessed. Flow cytometry was performed to explore the effect of B. adolescentis on regulatory T cells in the spleen. V3–V4 region of the 16S ribosomal RNA (rRNA) gene was sequenced to evaluate changes in the gut microbiota.

Results

Bifidobacteria adolescentis treatments reduced ear and skin thickness and suppressed eosinophils and mast cells infiltration. Th1- and Th2-type responses were regulated and the Tregs population was promoted in the spleen by B. adolescentis treatments. Bifidobacteria adolescentis increased the relative abundance of Lactobacillus but decrease Dorea and Pediococcus. Propionic and butyric acids were increased but isovaleric acid was decreased by B. adolescentis treatment. Besides, the functional modules, such as fatty acid biosynthesis, antigen processing and presentation were upregulated by B. adolescentis Ad1 treatment compared to the DNFB group.

Conclusion

Collectively, these results imply that B. adolescentis with the role of immunomodulation promotes Treg differentiation and suppresses Th2 responses, and increases the proportion of Lactobacillus that is positively correlated to increase in propionic acid production, and thus has the potential for AD amelioration.

Available only for authorised users

Leung DY (2000) Atopic dermatitis: new insights and opportunities for therapeutic intervention. J Allergy Clin Immunol 105(5):860–876. https://doi.org/10.1067/mai.2000.106484CrossRefPubMed

Reginald K, Westritschnig K, Werfel T, Heratizadeh A, Novak N, Focke-Tejkl M, Hirschl AM, Leung DYM, Elisyutina O, Fedenko E, Valenta R (2011) Immunoglobulin E antibody reactivity to bacterial antigens in atopic dermatitis patients. Clin Exp Allergy 41(3):357–369. https://doi.org/10.1111/j.1365-2222.2010.03655.xCrossRefPubMed

Leung DY, Bieber T (2003) Atopic dermatitis. Lancet 361(9352):151–160. https://doi.org/10.1016/s0140-6736(03)12193-9CrossRefPubMed

Peng W, Novak N (2015) Pathogenesis of atopic dermatitis. Clin Exp Allergy 45(3):566–574. https://doi.org/10.1111/cea.12495CrossRefPubMed

Leung DY, Boguniewicz M, Howell MD, Nomura I, Hamid QA (2004) New insights into atopic dermatitis. J Clin Investig 113(5):651–657. https://doi.org/10.1172/jci21060CrossRefPubMedPubMedCentral

Liu FT, Goodarzi H, Chen HY (2011) IgE, mast cells, and eosinophils in atopic dermatitis. Clin Rev Allergy Immunol 41(3):298–310. https://doi.org/10.1007/s12016-011-8252-4CrossRefPubMed

Wittig BM, Zeitz M (2003) The gut as an organ of immunology. Int J Colorectal Dis 18(3):181–187. https://doi.org/10.1007/s00384-002-0444-1CrossRefPubMed

Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859–904. https://doi.org/10.1152/physrev.00045.2009CrossRefPubMed

Blacher E, Levy M, Tatirovsky E, Elinav E (2017) Microbiome-modulated metabolites at the interface of host immunity. J Immunol (Baltimore, Md: 1950) 198(2):572–580. https://doi.org/10.4049/jimmunol.1601247CrossRef

10.

Chung H, Kasper DL (2010) Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr Opin Immunol 22(4):455–460. https://doi.org/10.1016/j.coi.2010.06.008CrossRefPubMed

11.

Dzidic M, Abrahamsson TR, Artacho A, Bjorksten B, Collado MC, Mira A, Jenmalm MC (2017) Aberrant IgA responses to the gut microbiota during infancy precede asthma and allergy development. J Allergy Clin Immunol 139(3):1017–1025.e1014. https://doi.org/10.1016/j.jaci.2016.06.047CrossRefPubMed

12.

Chen CC, Chen KJ, Kong MS, Chang HJ, Huang JL (2016) Alterations in the gut microbiotas of children with food sensitization in early life. Pediatr Allergy Immunol 27(3):254–262. https://doi.org/10.1111/pai.12522CrossRefPubMed

13.

Watanabe S, Narisawa Y, Arase S, Okamatsu H, Ikenaga T, Tajiri Y, Kumemura M (2003) Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol 111(3):587–591. https://doi.org/10.1067/mai.2003.105CrossRefPubMed

14.

Kwon MS, Lim SK, Jang JY, Lee J, Park HK, Kim N, Yun M, Shin MY, Jo HE, Oh YJ, Roh SW, Choi HJ (2018) Lactobacillus sakei WIKIM30 ameliorates atopic dermatitis-like skin lesions by inducing regulatory T cells and altering gut microbiota structure in mice. Front Immunol 9:1905. https://doi.org/10.3389/fimmu.2018.01905CrossRefPubMedPubMedCentral

15.

Navarro-Lopez V, Ramirez-Bosca A, Ramon-Vidal D, Ruzafa-Costas B, Genoves-Martinez S, Chenoll-Cuadros E, Carrion-Gutierrez M, Horga de la Parte J, Prieto-Merino D, Codoner-Cortes FM (2018) Effect of oral administration of a mixture of probiotic strains on SCORAD index and use of topical steroids in young patients with moderate atopic dermatitis: a randomized clinical trial. JAMA Dermatol 154(1):37–43. https://doi.org/10.1001/jamadermatol.2017.3647CrossRefPubMed

16.

Hevia A, Milani C, López P, Donado CD, Cuervo A, González S, Suárez A, Turroni F, Gueimonde M, Ventura M (2016) Allergic patients with long-term asthma display low levels of Bifidobacterium adolescentis. PLoS ONE 11(2):e0147809. https://doi.org/10.1371/journal.pone.0147809CrossRefPubMedPubMedCentral

17.

Wang L, Hu L, Xu Q, Yin B, Fang D, Wang G, Zhao J, Zhang H, Chen W (2017) Bifidobacterium adolescentis exerts strain-specific effects on constipation induced by loperamide in BALB/c mice. Int J Mol Sci. https://doi.org/10.3390/ijms18020318CrossRefPubMedPubMedCentral

18.

Egawa G, Honda T, Kabashima K (2017) SCFAs control skin immune responses via increasing Tregs. J Invest Dermatol 137(4):800–801. https://doi.org/10.1016/j.jid.2016.12.022CrossRefPubMed

19.

Sasso O, Summa M, Armirotti A, Pontis S, De Mei C, Piomelli D (2018) The N-acylethanolamine acid amidase inhibitor ARN077 suppresses inflammation and pruritus in a mouse model of allergic dermatitis. J Invest Dermatol 138(3):562–569. https://doi.org/10.1016/j.jid.2017.07.853CrossRefPubMed

20.

Zhai Q, Cen S, Jiang J, Zhao J, Zhang H, Chen W (2019) Disturbance of trace element and gut microbiota profiles as indicators of autism spectrum disorder: a pilot study of Chinese children. Environ Res 171:501–509. https://doi.org/10.1016/j.envres.2019.01.060CrossRefPubMed

21.

Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. https://doi.org/10.1038/nbt.2676CrossRefPubMedPubMedCentral

22.

Mao B, Li D, Ai C, Zhao J, Zhang H, Chen W (2016) Lactulose differently modulates the composition of luminal and mucosal microbiota in C57BL/6J mice. J Agric Food Chem 64(31):6240–6247. https://doi.org/10.1021/acs.jafc.6b02305CrossRefPubMed

23.

Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Paper presented at the Third International conference on weblogs and social media, San Jose, California, USA, 17–20, May, 2009

24.

Ding Y, Xu J, Bromberg JS (2012) Regulatory T cell migration during an immune response. Trends Immunol 33(4):174–180. https://doi.org/10.1016/j.it.2012.01.002CrossRefPubMedPubMedCentral

25.

Schmitt EG, Haribhai D, Williams JB, Aggarwal P, Shuang J, Charbonnier LM, Ke Y, Lorier R, Turner A, Ziegelbauer J (2012) IL-10 produced by iTreg cells controls colitis and pathogenic ex-iTreg cells during immunotherapy. J Immunol 189(12):5638–5648. https://doi.org/10.4049/jimmunol.1200936CrossRefPubMed

26.

Han SC, Koo DH, Kang NJ, Yoon WJ, Kang GJ, Kang HK, Yoo ES (2015) Docosahexaenoic acid alleviates atopic dermatitis by generating Tregs and IL-10/TGF-beta-modified macrophages via a TGF-beta-dependent mechanism. J Invest Dermatol 135(6):1556–1564. https://doi.org/10.1038/jid.2014.488CrossRefPubMed

27.

Zachariassen LF, Krych L, Engkilde K, Nielsen DS, Kot W, Hansen CH, Hansen AK (2017) Sensitivity to oxazolone induced dermatitis is transferable with gut microbiota in mice. Sci Rep 7:44385. https://doi.org/10.1038/srep44385CrossRefPubMedPubMedCentral

28.

Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Muller G, Stokholm J, Smith B, Krogfelt KA (2011) Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol 128(3):646–652. https://doi.org/10.1016/j.jaci.2011.04.060CrossRefPubMed

29.

Penders J, Stobberingh EE, van den Brandt PA, Thijs C (2007) The role of the intestinal microbiota in the development of atopic disorders. Allergy 62(11):1223–1236. https://doi.org/10.1111/j.1398-9995.2007.01462.xCrossRefPubMed

30.

Williams BL, Hornig M, Parekh T, Lipkin WI (2012) Application of novel PCR-based methods for detection, quantitation, and phylogenetic characterization of Sutterella species in intestinal biopsy samples from children with autism and gastrointestinal disturbances. MBio. https://doi.org/10.1128/mBio.00261-11CrossRefPubMedPubMedCentral

31.

Taras D, Simmering R, Collins MD, Lawson PA, Blaut M (2002) Reclassification of Eubacterium formicigenerans Holdeman and Moore 1974 as Dorea formicigenerans gen. nov., comb. nov., and description of Dorea longicatena sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 52(Pt 2):423–428. https://doi.org/10.1099/00207713-52-2-423CrossRefPubMed

32.

Saulnier DM, Riehle K, Mistretta TA, Diaz MA, Mandal D, Raza S, Weidler EM, Qin X, Coarfa C, Milosavljevic A, Petrosino JF, Highlander S, Gibbs R, Lynch SV, Shulman RJ, Versalovic J (2011) Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology 141(5):1782–1791. https://doi.org/10.1053/j.gastro.2011.06.072CrossRefPubMed

33.

Nishimura T (1986) Antimicrobial chemotherapy of infections due to Pseudomonas aeruginosa. Pediatrics Int. https://doi.org/10.1111/j.1442-200X.1986.tb00750.xCrossRef

34.

Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F (2016) From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165(6):1332–1345. https://doi.org/10.1016/j.cell.2016.05.041CrossRefPubMed

35.

Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341(6145):569–573. https://doi.org/10.1126/science.1241165CrossRefPubMed

36.

Lee MJ, Kang MJ, Lee SY, Lee E, Kim K, Won S, Suh DI, Kim KW, Sheen YH, Ahn K, Kim BS, Hong SJ (2018) Perturbations of gut microbiome genes in infants with atopic dermatitis according to feeding type. J Allergy Clin Immunol 141(4):1310–1319. https://doi.org/10.1016/j.jaci.2017.11.045CrossRefPubMed

Title: Bifidobacteria adolescentis regulated immune responses and gut microbial composition to alleviate DNFB-induced atopic dermatitis in mice
Authors: Zhifeng Fang
Lingzhi Li
Jianxian Zhao
Hao Zhang
Yuan-Kun Lee
Wenwei Lu
Wei Chen
Publication date: 01-10-2020
Publisher: Springer Berlin Heidelberg
Keywords: Atopic Dermatitis
Respiratory Microbiota
Published in: European Journal of Nutrition / Issue 7/2020
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI: https://doi.org/10.1007/s00394-019-02145-8

ACC 2024 Congress Coverage

Cardiology Video

Highlights from the ACC 2024 Congress

Watch now

Watch official videos from the ACC congress summarizing key highlights from the last year in heart failure, cardiomyopathies, valvular disease, pulmonary vascular disease, and pediatric cardiology.

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

ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Bifidobacteria adolescentis regulated immune responses and gut microbial composition to alleviate DNFB-induced atopic dermatitis in mice

Abstract

Purpose

Methods

Results

Conclusion

ACC 2024 Congress Coverage

Highlights from the ACC 2024 Congress

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

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 7/2020

A nutrient-wide association study for risk of prostate cancer in the European Prospective Investigation into Cancer and Nutrition and the Netherlands Cohort Study

Egg yolk augments type 2 immunity by activating innate cells

The ‘Seal’ of Sir Shackleton

Prebiotic effect of inulin-type fructans on faecal microbiota and short-chain fatty acids in type 2 diabetes: a randomised controlled trial

Correction to: Prebiotic effect of inulin‑type fructans on faecal microbiota and short‑chain fatty acids in type 2 diabetes: a randomised controlled trial

Associations between dietary flavonoids and retinal microvasculature in older adults

ACC 2024 Congress Coverage

Highlights from the ACC 2024 Congress

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

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page