IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43652-x.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43652-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43652-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Shuqin Zeng & Alexandre Almeida & Shiping Li & Junjie Ying & Hua Wang & Yi Qu & R. Paul Ross & Catherine Stanton & Zhemin Zhou & Xiaoyu Niu & Dezhi Mu & Shaopu Wang, 2024. "A metagenomic catalog of the early-life human gut virome," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Ruairi C. Robertson & Thaddeus J. Edens & Lynnea Carr & Kuda Mutasa & Ethan K. Gough & Ceri Evans & Hyun Min Geum & Iman Baharmand & Sandeep K. Gill & Robert Ntozini & Laura E. Smith & Bernard Chasekw, 2023. "The gut microbiome and early-life growth in a population with high prevalence of stunting," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Courtney Hoskinson & Darlene L. Y. Dai & Kate L. Bel & Allan B. Becker & Theo J. Moraes & Piushkumar J. Mandhane & B. Brett Finlay & Elinor Simons & Anita L. Kozyrskyj & Meghan B. Azad & Padmaja Subba, 2023. "Delayed gut microbiota maturation in the first year of life is a hallmark of pediatric allergic disease," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Li Zhang & Karen R. Jonscher & Zuyuan Zhang & Yi Xiong & Ryan S. Mueller & Jacob E. Friedman & Chongle Pan, 2022. "Islet autoantibody seroconversion in type-1 diabetes is associated with metagenome-assembled genomes in infant gut microbiomes," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Manish Boolchandani & Kevin S. Blake & Drake H. Tilley & Miguel M. Cabada & Drew J. Schwartz & Sanket Patel & Maria Luisa Morales & Rina Meza & Giselle Soto & Sandra D. Isidean & Chad K. Porter & Mark, 2022. "Impact of international travel and diarrhea on gut microbiome and resistome dynamics," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    6. Fanette Fontaine & Sondra Turjeman & Karel Callens & Omry Koren, 2023. "The intersection of undernutrition, microbiome, and child development in the first years of life," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    7. Shinji Fukuda & Yumiko Nakanishi & Eisuke Chikayama & Hiroshi Ohno & Tsuneo Hino & Jun Kikuchi, 2009. "Evaluation and Characterization of Bacterial Metabolic Dynamics with a Novel Profiling Technique, Real-Time Metabolotyping," PLOS ONE, Public Library of Science, vol. 4(3), pages 1-10, March.
    8. Bo Tang & Li Tang & Shengpeng Li & Shuang Liu & Jialin He & Pan Li & Sumin Wang & Min Yang & Longhui Zhang & Yuanyuan Lei & Dianji Tu & Xuefeng Tang & Hua Hu & Qin Ouyang & Xia Chen & Shiming Yang, 2023. "Gut microbiota alters host bile acid metabolism to contribute to intrahepatic cholestasis of pregnancy," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Lingling Wang & Haobin Yao & Daniel C. Morgan & Kam Shing Lau & Suet Yi Leung & Joshua W. K. Ho & Wai K. Leung, 2023. "Altered human gut virome in patients undergoing antibiotics therapy for Helicobacter pylori," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    10. Alice Risely & Kerstin Wilhelm & Tim Clutton-Brock & Marta B. Manser & Simone Sommer, 2021. "Diurnal oscillations in gut bacterial load and composition eclipse seasonal and lifetime dynamics in wild meerkats," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    11. Suzanne L. Ishaq & Emily F. Wissel & Patricia G. Wolf & Laura Grieneisen & Erin M. Eggleston & Gwynne Mhuireach & Michael Friedman & Anne Lichtenwalner & Jessica Otero Machuca & Katherine Weatherford , 2022. "Designing the Microbes and Social Equity Symposium: A Novel Interdisciplinary Virtual Research Conference Based on Achieving Group-Directed Outputs," Challenges, MDPI, vol. 13(2), pages 1-20, July.
    12. Carolina Alves Costa Silva & Gianmarco Piccinno & Déborah Suissa & Mélanie Bourgin & Gerty Schreibelt & Sylvère Durand & Roxanne Birebent & Marine Fidelle & Cissé Sow & Fanny Aprahamian & Paolo Manghi, 2024. "Influence of microbiota-associated metabolic reprogramming on clinical outcome in patients with melanoma from the randomized adjuvant dendritic cell-based MIND-DC trial," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Justine Tanoey & Christina Baechle & Hermann Brenner & Andreas Deckert & Julia Fricke & Kathrin Günther & André Karch & Thomas Keil & Alexander Kluttig & Michael Leitzmann & Rafael Mikolajczyk & Nadia, 2022. "Birth Order, Caesarean Section, or Daycare Attendance in Relation to Child- and Adult-Onset Type 1 Diabetes: Results from the German National Cohort," IJERPH, MDPI, vol. 19(17), pages 1-14, August.
    14. Yue Clare Lou & Benjamin E. Rubin & Marie C. Schoelmerich & Kaden S. DiMarco & Adair L. Borges & Rachel Rovinsky & Leo Song & Jennifer A. Doudna & Jillian F. Banfield, 2023. "Infant microbiome cultivation and metagenomic analysis reveal Bifidobacterium 2’-fucosyllactose utilization can be facilitated by coexisting species," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Thomas A. Auchtung & Christopher J. Stewart & Daniel P. Smith & Eric W. Triplett & Daniel Agardh & William A. Hagopian & Anette G. Ziegler & Marian J. Rewers & Jin-Xiong She & Jorma Toppari & Åke Lern, 2022. "Temporal changes in gastrointestinal fungi and the risk of autoimmunity during early childhood: the TEDDY study," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    16. Xiaoxiao Yuan & Ruirui Wang & Bing Han & ChengJun Sun & Ruimin Chen & Haiyan Wei & Linqi Chen & Hongwei Du & Guimei Li & Yu Yang & Xiaojuan Chen & Lanwei Cui & Zhenran Xu & Junfen Fu & Jin Wu & Wei Gu, 2022. "Functional and metabolic alterations of gut microbiota in children with new-onset type 1 diabetes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    17. M. Büttner & J. Ostner & C. L. Müller & F. J. Theis & B. Schubert, 2021. "scCODA is a Bayesian model for compositional single-cell data analysis," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    18. Seong Beom An & Bo-Gie Yang & Gyeonghui Jang & Do-Yeon Kim & Jiyoung Kim & Sung-Man Oh & Nahyun Oh & Sanghee Lee & Ji-Yeong Moon & Jeong-Ah Kim & Ji-Hyun Kim & Yoo-Jeong Song & Hye-Won Hyun & Jisoo Ki, 2022. "Combined IgE neutralization and Bifidobacterium longum supplementation reduces the allergic response in models of food allergy," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    19. Diletta Maria Francesca Ingrosso & Maria Teresa Quarta & Alessia Quarta & Francesco Chiarelli, 2023. "Prevention of Type 1 Diabetes in Children: A Worthy Challenge?," IJERPH, MDPI, vol. 20(11), pages 1-15, May.
    20. Jake Lin & Elaheh Moradi & Karoliina Salenius & Suvi Lehtipuro & Tomi Häkkinen & Jutta E. Laiho & Sami Oikarinen & Sofia Randelin & Hemang M. Parikh & Jeffrey P. Krischer & Jorma Toppari & Åke Lernmar, 2023. "Distinct transcriptomic profiles in children prior to the appearance of type 1 diabetes-linked islet autoantibodies and following enterovirus infection," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43652-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.