Gut bacteria at 6 months of age are associated with immune cell status in 1-year-old children.


Journal

Scandinavian journal of immunology
ISSN: 1365-3083
Titre abrégé: Scand J Immunol
Pays: England
ID NLM: 0323767

Informations de publication

Date de publication:
Apr 2024
Historique:
revised: 27 11 2023
received: 11 05 2023
accepted: 28 11 2023
medline: 15 7 2024
pubmed: 15 7 2024
entrez: 15 7 2024
Statut: ppublish

Résumé

Age-related gut bacterial changes during infancy have been widely studied, but it remains still unknown how these changes are associated with immune cell composition. This study's aim was to explore if the temporal development of gut bacteria during infancy prospectively affects immune cell composition. Faecal bacteria and short-chain fatty acids were analysed from 67 PreventADALL study participants at four timepoints (birth to 12 months) using reduced metagenome sequencing and gas chromatography. Immune cell frequencies were assessed using mass cytometry in whole blood samples at 12 months. The infants clustered into four groups based on immune cell composition: clusters 1 and 2 showed a high relative abundance of naïve cells, cluster 3 exhibited increased abundance of classical- and non-classical monocytes and clusters 3 and 4 had elevated neutrophil levels. At all age groups, we did observe significant associations between the gut microbiota and immune cell clusters; however, these were generally from low abundant species. Only at 6 months of age we observed significant associations between abundant (>8%) species and immune cell clusters. Bifidobacterium adolescentis and Porphyromonadaceae are associated with cluster 1, while Bacteroides fragilis and Bifidobacterium longum are associated with clusters 3 and 4 respectively. These species have been linked to T-cell polarization and maturation. No significant correlations were found between short-chain fatty acids and immune cell composition. Our findings suggest that abundant gut bacteria at 6 months may influence immune cell frequencies at 12 months, highlighting the potential role of gut microbiota in shaping later immune cell composition.

Identifiants

pubmed: 39007947
doi: 10.1111/sji.13346
doi:

Substances chimiques

Fatty Acids, Volatile 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13346

Subventions

Organisme : Arne Ingel's legat
Organisme : Barnestifteslen at Oslo University Hospital
Organisme : Forte
Organisme : Fürst Medical Laboratory, Oslo, Norway
Organisme : Health and Rehabilitation Norway
Organisme : Karolinska Institutet
Organisme : Norges Forskningsråd
Organisme : Norwegian Association of Asthma and Allergy
Organisme : Norwegian Society of Dermatology and Venerology
Organisme : Oslo University Hospital
Organisme : Region Stockholm (ALF-project and individual grants)
Organisme : Roche
Organisme : SFO-V Karolinska Institutet
Organisme : Swedish Asthma and Allergy Association's Research Foundation
Organisme : Swedish Order of Freemasons Foundation Barnhuset
Organisme : Swedish Research council
Organisme : Sykehuset Østfold
Organisme : The Cancer- and Allergy Foundation
Organisme : Delegation of the European Union to Norway, University of Oslo
Organisme : The Foundation for Healthcare and Allergy Research in Sweden - Vårdalstiftelsen
Organisme : The Fridtjof Nansen Institute
Organisme : The Hesselman foundation
Organisme : The Initiative for Clinical Therapy Research
Organisme : The King Gustaf V 80th Birthday Foundation
Organisme : The Kloster foundation
Organisme : The Konsul Th C Bergh's Foundation
Organisme : The Magnus Bergwall foundation
Organisme : The Pediatric Research Foundation at Astrid Lindgren Children's Hospital
Organisme : The Samaritan Foundation for Pediatric research
Organisme : The Sven Jerring Foundation
Organisme : The Swedish Heart-Lung Foundation
Organisme : The Swedish Society of Medicine
Organisme : Thermo-Fisher Uppsala, Sweden
Organisme : Universitetet i Oslo

Informations de copyright

© 2023 The Authors. Scandinavian Journal of Immunology published by John Wiley & Sons Ltd on behalf of The Scandinavian Foundation for Immunology.

Références

Henrick BM, Rodriguez L, Lakshmikanth T, et al. Bifidobacteria‐mediated immune system imprinting early in life. Cell. 2021;184(15):3884‐3898.e11.
Wiertsema SP, van Bergenhenegouwen J, Garssen J, Knippels LMJ. The interplay between the gut microbiome and the immune system in the context of infectious diseases throughout life and the role of nutrition in optimizing treatment strategies. Nutrients. 2021;13(3):886.
Vatanen T, Kostic AD, d'Hennezel E, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016;165(4):842‐853.
Arrieta M‐C, Stiemsma LT, Dimitriu PA, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015;7(307):307ra152.
Kelly D, Coutts AGP. Early nutrition and the development of immune function in the neonate. Proc Nutr Soc. 2000;59(2):177‐185.
von Mutius E, Smits HH. Primary prevention of asthma: from risk and protective factors to targeted strategies for prevention. Lancet. 2020;396(10254):854‐866.
Matamoros S, Gras‐Leguen C, le Vacon F, Potel G, de la Cochetiere MF. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol. 2013;21(4):167‐173.
Shao Y, Forster SC, Tsaliki E, et al. Stunted microbiota and opportunistic pathogen colonization in caesarean‐section birth. Nature. 2019;574:117‐121.
Bäckhed F, Roswall J, Peng Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690‐703.
Gotoh A, Katoh T, Sakanaka M, et al. Sharing of human milk oligosaccharides degradants within bifidobacterial communities in faecal cultures supplemented with Bifidobacterium bifidum. Sci Rep. 2018;8(1):13958.
Moore RE, Townsend SD. Temporal development of the infant gut microbiome. Open Biol. 2019;9(9):190128.
Nilsen M, Madelen Saunders C, Leena Angell I, et al. Butyrate levels in the transition from an infant‐ to an adult‐like gut microbiota correlate with bacterial networks associated with Eubacterium Rectale and Ruminococcus Gnavus. Genes. 2020;11(11):1245.
Corrêa‐Oliveira R, Fachi JL, Vieira A, Sato FT, Vinolo MAR. Regulation of immune cell function by short‐chain fatty acids. Clin Transl Immunol. 2016;5(4):e73.
Roy CC, Kien CL, Bouthillier L, Levy E. Short‐chain fatty acids: ready for prime time? Nutr Clin Pract. 2006;21(4):351‐366.
Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T‐cell generation. Nature. 2013;504(7480):451‐455.
Trompette A, Gollwitzer ES, Yadava K, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med. 2014;20(2):159‐166.
Park J, Kim M, Kang SG, et al. Short‐chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR‐S6K pathway. Mucosal Immunol. 2015;8(1):80‐93.
den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short‐chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54(9):2325‐2340.
Skjerven HO, Rehbinder EM, Vettukattil R, et al. Skin emollient and early complementary feeding to prevent infant atopic dermatitis (PreventADALL): a factorial, multicentre, cluster‐randomised trial. Lancet. 2020;395(10228):951‐961.
Lødrup Carlsen KC, Rehbinder EM, Skjerven HO, et al. Preventing atopic dermatitis and ALLergies in children—the PreventADALL study. Allergy. 2018;73(10):2063‐2070.
Nilsen M, Lokmic A, Angell IL, et al. Fecal microbiota nutrient utilization potential suggests mucins as drivers for initial gut colonization of mother‐child shared bacteria. Appl Environ Microbiol. 2021;87:AEM.02201‐20.
Hiseni P, Rudi K, Wilson RC, Hegge FT, Snipen L. HumGut: a comprehensive human gut prokaryotic genomes collection filtered by metagenome data. Microbiome. 2021;9(1):165.
Mikes J, Olin A, Lakshmikanth T, Chen Y, Brodin P. Automated cell processing for mass cytometry experiments. Methods Mol Biol. 2019;1989:111‐123.
Chen Y, Lakshmikanth T, Mikes J, Brodin P. Single‐cell classification using learned cell phenotypes. bioRxiv, 2020. doi:10.1101/2020.07.22.216002
Naeem S, Aishan W. Study and implementing K‐mean clustering algorithm on English text and techniques to find the optimal value of K. Int J Comput Appl. 2018;975(8887):7‐14.
Tibshirani R, Walther G, Hastie T. Estimating the number of clusters in a data set via the gap statistic. J R Stat Soc Series B Stat Methodology. 2001;63(2):411‐423.
Kaufman L, Rousseeuw PJ. Finding Groups in Data: an Introduction to Cluster Analysis. Wiley; 1990.
Kassambara A, Mundt F. factoextra: extract and visualise the results of multivariate data analyses. R. Package version 1.0.7. 2020.
De Cáceres M, Jansen F, Dell N. indicspecies: relationship between species and groups of sites. R. Package version 1.7.9. 2020.
Ouwehand AC, Isolauri E, He F, Hashimoto H, Benno Y, Salminen S. Differences in Bifidobacterium flora composition in allergic and healthy infants. J Allergy Clin Immunol. 2001;108(1):144‐145.
Tan TG, Sefik E, Geva‐Zatorsky N, et al. Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice. Proc Natl Acad Sci USA. 2016;113(50):E8141‐E8150.
Ruiz L, Delgado S, Ruas‐Madiedo P, Sánchez B, Margolles A. Bifidobacteria and their molecular communication with the immune system. Front Microbiol. 2017;8:2345.
Ang QY, Alexander M, Newman JC, et al. Ketogenic diets Alter the gut microbiome resulting in decreased intestinal Th17 cells. Cell. 2020;181(6):1263‐1275.e16.
Garidou L, Pomié C, Klopp P, et al. The gut microbiota regulates intestinal CD4 T cells expressing RORγt and controls metabolic disease. Cell Metab. 2015;22(1):100‐112.
Takahashi S, Fukuda M, Mitani A, et al. Follicular dendritic cell‐secreted protein is decreased in experimental periodontitis concurrently with the increase of interleukin‐17 expression and the Rankl/Opg mRNA ratio. J Periodontal Res. 2014;49(3):390‐397.
Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev. 2008;223(1):87‐113.
Oboki K, Ohno T, Saito H, Nakae S. Th17 and allergy. Allergol Int. 2008;57(2):121‐134.
Ramakrishna C, Kujawski M, Chu H, Li L, Mazmanian SK, Cantin EM. Bacteroides fragilis polysaccharide a induces IL‐10 secreting B and T cells that prevent viral encephalitis. Nat Commun. 2019;10(1):2153.
Troy EB, Kasper DL. Beneficial effects of Bacteroides fragilis polysaccharides on the immune system. Front Biosci (Landmark Ed). 2010;15:25‐34.
Kjer‐Nielsen L, Patel O, Corbett AJ, et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 2012;491(7426):717‐723.
Hossain KS, Amarasena S, Mayengbam S. B vitamins and their roles in gut health. Microorganisms. 2022;10(6):1168.
Lukiw WJ. Bacteroides fragilis lipopolysaccharide and inflammatory signaling in Alzheimer's disease. Front Microbiol. 2016;7:1544.

Auteurs

Morten Nilsen (M)

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.

Unni Cecilie Nygaard (UC)

Section for Immunology, Department of Method Development and Analytics, Norwegian Institute of Public Health, Oslo, Norway.

Petter Brodin (P)

Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
Pediatric Rheumatology, Karolinska University Hospital, Solna, Sweden.

Karin Cecilie Lødrup Carlsen (KCL)

Division of Paediatric and Adolescent Medicine, Oslo University Hospital, Oslo, Norway.
Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Cecilie Fredheim (C)

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.

Guttorm Haugen (G)

Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Division of Obstetrics and Gynaecology, Oslo University Hospital, Oslo, Norway.

Gunilla Hedlin (G)

Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
Astrid Lindgren Children's Hospital, Karolinska University Hospital, Stockholm, Sweden.

Christine Monceyron Jonassen (CM)

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.
Genetic Unit, Centre for Laboratory Medicine, Østfold Hospital Trust, Kalnes, Norway.

Unni Lise Albertsdottir Jonsmoen (ULA)

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.

Tadepally Lakshmikanth (T)

Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.

Björn Nordlund (B)

Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
Astrid Lindgren Children's Hospital, Karolinska University Hospital, Stockholm, Sweden.

Axel Olin (A)

Human Evolutionary Genetics, Institut Pasteur, Paris, France.

Eva Maria Rehbinder (EM)

Department of Dermatology and Vaenorology, Oslo University Hospital, Oslo, Norway.

Håvard O Skjerven (HO)

Division of Paediatric and Adolescent Medicine, Oslo University Hospital, Oslo, Norway.
Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Lars Snipen (L)

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.

Anne Cathrine Staff (AC)

Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Division of Obstetrics and Gynaecology, Oslo University Hospital, Oslo, Norway.

Cilla Söderhäll (C)

Department of Women's and Children's Health, Karolinska Institutet, Stockholm, Sweden.
Astrid Lindgren Children's Hospital, Karolinska University Hospital, Stockholm, Sweden.

Riyas Vettukattil (R)

Division of Paediatric and Adolescent Medicine, Oslo University Hospital, Oslo, Norway.
Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Knut Rudi (K)

Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway.

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