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Mutual modulation of gut microbiota and the immune system in type 1 diabetes models

Author

Listed:
  • Estela Rosell-Mases

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida))

  • Alba Santiago

    (Vall d’Hebron Barcelona Hospital Campus)

  • Marta Corral-Pujol

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida))

  • Francisca Yáñez

    (Vall d’Hebron Barcelona Hospital Campus)

  • Encarna Varela

    (Vall d’Hebron Barcelona Hospital Campus)

  • Leire Egia-Mendikute

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida))

  • Berta Arpa

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida))

  • Catalina Cosovanu

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida))

  • Anaïs Panosa

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida))

  • Gerard Serrano-Gómez

    (Vall d’Hebron Barcelona Hospital Campus)

  • Conchi Mora

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida))

  • Joan Verdaguer

    (Universitat de Lleida (UdL) and Institut de Recerca Biomèdica de Lleida (IRBLleida)
    Instituto de Salud Carlos III (ISCIII))

  • Chaysavanh Manichanh

    (Vall d’Hebron Barcelona Hospital Campus
    Instituto de Salud Carlos III (ISCIII))

Abstract

The transgenic 116C-NOD mouse strain exhibits a prevalent Th17 phenotype, and reduced type 1 diabetes (T1D) compared to non-obese diabetic (NOD) mice. A cohousing experiment between both models revealed lower T1D incidence in NOD mice cohoused with 116C-NOD, associated with gut microbiota changes, reduced intestinal permeability, shifts in T and B cell subsets, and a transition from Th1 to Th17 responses. Distinct gut bacterial signatures were linked to T1D in each group. Using a RAG-2−/− genetic background, we found that T cell alterations promoted segmented filamentous bacteria proliferation in young NOD and 116C-NOD, as well as in immunodeficient NOD.RAG-2−/− and 116C-NOD.RAG-2−/− mice across all ages. Bifidobacterium colonization depended on lymphocytes and thrived in a non-diabetogenic environment. Additionally, 116C-NOD B cells in 116C-NOD.RAG-2−/− mice enriched the gut microbiota in Adlercreutzia and reduced intestinal permeability. Collectively, these results indicate reciprocal modulation between gut microbiota and the immune system in rodent T1D models.

Suggested Citation

  • Estela Rosell-Mases & Alba Santiago & Marta Corral-Pujol & Francisca Yáñez & Encarna Varela & Leire Egia-Mendikute & Berta Arpa & Catalina Cosovanu & Anaïs Panosa & Gerard Serrano-Gómez & Conchi Mora , 2023. "Mutual modulation of gut microbiota and the immune system in type 1 diabetes models," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43652-x
    DOI: 10.1038/s41467-023-43652-x
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    1. Himel Mallick & Ali Rahnavard & Lauren J McIver & Siyuan Ma & Yancong Zhang & Long H Nguyen & Timothy L Tickle & George Weingart & Boyu Ren & Emma H Schwager & Suvo Chatterjee & Kelsey N Thompson & Je, 2021. "Multivariable association discovery in population-scale meta-omics studies," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-27, November.
    2. Christopher J. Stewart & Nadim J. Ajami & Jacqueline L. O’Brien & Diane S. Hutchinson & Daniel P. Smith & Matthew C. Wong & Matthew C. Ross & Richard E. Lloyd & HarshaVardhan Doddapaneni & Ginger A. M, 2018. "Temporal development of the gut microbiome in early childhood from the TEDDY study," Nature, Nature, vol. 562(7728), pages 583-588, October.
    3. Li Wen & Ruth E. Ley & Pavel Yu. Volchkov & Peter B. Stranges & Lia Avanesyan & Austin C. Stonebraker & Changyun Hu & F. Susan Wong & Gregory L. Szot & Jeffrey A. Bluestone & Jeffrey I. Gordon & Alexa, 2008. "Innate immunity and intestinal microbiota in the development of Type 1 diabetes," Nature, Nature, vol. 455(7216), pages 1109-1113, October.
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