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

Animals Bifidobacterium adolescentis Dermatitis, Atopic / therapy Dinitrofluorobenzene Disease Models, Animal Gastrointestinal Microbiome Immunity Mice
Atopic dermatitis Bifidobacterium adolescentis Gut microbiota Immune responses Short-chain fatty acids

Journal

European journal of nutrition
ISSN: 1436-6215
Titre abrégé: Eur J Nutr
Pays: Germany
ID NLM: 100888704

Informations de publication

Date de publication:
Oct 2020
Historique:
received: 03 09 2019
accepted: 11 11 2019
pubmed: 2 12 2019
medline: 24 6 2021
entrez: 2 12 2019
Statut: ppublish

Résumé

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. 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. 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. 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.

Identifiants

DOI: 10.1007/s00394-019-02145-8 PMID: 31786642
pubmed: 31786642
doi: 10.1007/s00394-019-02145-8
pii: 10.1007/s00394-019-02145-8
doi:

Substances chimiques

Dinitrofluorobenzene D241E059U6

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3069-3081

Subventions

Organisme : National Natural Science Foundation of China
ID : 31820103010
Organisme : National Natural Science Foundation of China
ID : 31771953
Organisme : National Natural Science Foundation of China
ID : 31871774
Organisme : National first-class discipline program of Food Science and Technology
ID : JUFSTR20180102
Organisme : Fundamental Research Funds for the Central Universities
ID : JUSRP51903B

Commentaires et corrections

Type : ErratumIn

Références

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.2000.106484
doi: 10.1067/mai.2000.106484 pubmed: 10808164
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.x
doi: 10.1111/j.1365-2222.2010.03655.x pubmed: 21155910
Leung DY, Bieber T (2003) Atopic dermatitis. Lancet 361(9352):151–160. https://doi.org/10.1016/s0140-6736(03)12193-9
doi: 10.1016/s0140-6736(03)12193-9 pubmed: 12531593
Peng W, Novak N (2015) Pathogenesis of atopic dermatitis. Clin Exp Allergy 45(3):566–574. https://doi.org/10.1111/cea.12495
doi: 10.1111/cea.12495 pubmed: 25610977
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/jci21060
doi: 10.1172/jci21060 pubmed: 14991059 pmcid: 351324
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/s12016-011-8252-4
doi: 10.1007/s12016-011-8252-4 pubmed: 21249468
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/s00384-002-0444-1
doi: 10.1007/s00384-002-0444-1 pubmed: 12673481
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.00045.2009
doi: 10.1152/physrev.00045.2009 pubmed: 20664075 pmcid: 20664075
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.1601247
doi: 10.4049/jimmunol.1601247
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.2010.06.008
doi: 10.1016/j.coi.2010.06.008 pubmed: 20656465
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.2016.06.047
doi: 10.1016/j.jaci.2016.06.047 pubmed: 27531072
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.12522
doi: 10.1111/pai.12522 pubmed: 26663491
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.2003.105
doi: 10.1067/mai.2003.105
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.2018.01905
doi: 10.3389/fimmu.2018.01905 pubmed: 6102352 pmcid: 6102352
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.2017.3647
doi: 10.1001/jamadermatol.2017.3647 pubmed: 29117309
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.0147809
doi: 10.1371/journal.pone.0147809 pubmed: 26840903 pmcid: 4739579
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/ijms18020318
doi: 10.3390/ijms18020318 pubmed: 29295552 pmcid: 5796053
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.2016.12.022
doi: 10.1016/j.jid.2016.12.022 pubmed: 28340682
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.2017.07.853
doi: 10.1016/j.jid.2017.07.853 pubmed: 29054595
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.2019.01.060
doi: 10.1016/j.envres.2019.01.060 pubmed: 30743242
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.2676
doi: 10.1038/nbt.2676 pubmed: 3819121 pmcid: 3819121
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.6b02305
doi: 10.1021/acs.jafc.6b02305 pubmed: 27438677
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
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.2012.01.002
doi: 10.1016/j.it.2012.01.002 pubmed: 22305714 pmcid: 3319498
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.1200936
doi: 10.4049/jimmunol.1200936 pubmed: 23125413
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.2014.488
doi: 10.1038/jid.2014.488 pubmed: 25405323
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/srep44385
doi: 10.1038/srep44385 pubmed: 28290517 pmcid: 5349591
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.2011.04.060
doi: 10.1016/j.jaci.2011.04.060 pubmed: 21782228
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.x
doi: 10.1111/j.1398-9995.2007.01462.x pubmed: 17711557
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.00261-11
doi: 10.1128/mBio.00261-11 pubmed: 23131829 pmcid: 3509431
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/10.1099/00207713-52-2-423
doi: 10.1099/00207713-52-2-423 pubmed: 11931151
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.2011.06.072
doi: 10.1053/j.gastro.2011.06.072 pubmed: 21741921
Nishimura T (1986) Antimicrobial chemotherapy of infections due to Pseudomonas aeruginosa. Pediatrics Int. https://doi.org/10.1111/j.1442-200X.1986.tb00750.x
doi: 10.1111/j.1442-200X.1986.tb00750.x
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.2016.05.041
doi: 10.1016/j.cell.2016.05.041
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.1241165
doi: 10.1126/science.1241165 pubmed: 23828891
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.2017.11.045
doi: 10.1016/j.jaci.2017.11.045

Auteurs

Zhifeng Fang (Z)

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.

Lingzhi Li (L)

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.

Jianxian Zhao (J)

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
(Yangzhou) Institute of Food Biotechnology, Jiangnan University, Yangzhou, 225004, China.

Hao Zhang (H)

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, 214122, Jiangsu, China.
Wuxi Translational Medicine Research Center and Jiangsu Translational Medicine Research Institut Wuxi Branch, Wuxi, 214122, Jiangsu, China.
(Yangzhou) Institute of Food Biotechnology, Jiangnan University, Yangzhou, 225004, China.

Yuan-Kun Lee (YK)

Department of Microbiology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore.

Wenwei Lu (W)

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China. luwenwei@jiangnan.edu.cn.
School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China. luwenwei@jiangnan.edu.cn.
National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, 214122, Jiangsu, China. luwenwei@jiangnan.edu.cn.
(Yangzhou) Institute of Food Biotechnology, Jiangnan University, Yangzhou, 225004, China. luwenwei@jiangnan.edu.cn.

Wei Chen (W)

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China.
National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, 214122, Jiangsu, China.
Beijing Innovation Centre of Food Nutrition and Human Health, Beijing Technology and Business University (BTBU), Beijing, 100048, China.

Articles similaires

Evaluating the efficacy of telesurgery with dual console SSI Mantra Surgical Robotic System: experiment on animal model and clinical trials.

Sudhir Prem Srivastava, Vishwajyoti Pascual Srivastava, Avinesh Singh et al.
1.00
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell

FBXO22 inhibits colitis and colorectal carcinogenesis by regulating the degradation of the S2448-phosphorylated form of mTOR.

Minle Li, Xuan Chen, Pengfei Qu et al.
1.00
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Use of organic material provided by an automatic enrichment device by weaner pigs and its influence on tail lesions.

Philipp Heseker, Jeanette Probst, Stefanie Ammer et al.
1.00
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Bifidobacteria adolescentis regulated immune...
questionsmedicales.fr › Bactéries › Bactéries à Gram positif › Bâtonnets à Gram positif › Bâtonnets asporogènes à Gram positif › Bâtonnets asporogènes irréguliers à Gram positif › Actinobacteria › Bifidobacterium › Bifidobacterium adolescentis › Bifidobacteria adolescentis regulated immune...
questionsmedicales.fr › Maladies du système immunitaire › Hypersensibilité › Hypersensibilité immédiate › Eczéma atopique › Bifidobacteria adolescentis regulated immune...
questionsmedicales.fr › Composés chimiques organiques › Composés nitrés › Nitrobenzènes › Dinitrobenzènes › 1-Fluoro-2,4-dinitro-benzène › Bifidobacteria adolescentis regulated immune...
questionsmedicales.fr › Techniques d'investigation › Modèles théoriques › Modèles biologiques › Modèles animaux de maladie humaine › Bifidobacteria adolescentis regulated immune...
questionsmedicales.fr › Environnement et santé publique › Environnement › Écosystème › Biodiversité › Biote › Microbiote › Microbiome gastro-intestinal › Bifidobacteria adolescentis regulated immune...
questionsmedicales.fr › Phénomènes du système immunitaire › Immunité › Bifidobacteria adolescentis regulated immune...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Bifidobacteria adolescentis regulated immune...