IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48935-5.html
   My bibliography  Save this article

Obesity-associated microbiomes instigate visceral adipose tissue inflammation by recruitment of distinct neutrophils

Author

Listed:
  • Dharti Shantaram

    (Wexner Medical Center at The Ohio State University)

  • Rebecca Hoyd

    (Pelotonia Institute for Immuno-Oncology at The Ohio State University Comprehensive Cancer Center–Arthur G. James Cancer Hospital and Richard J. Solove Research Institute)

  • Alecia M. Blaszczak

    (Wexner Medical Center at The Ohio State University)

  • Linda Antwi

    (Pelotonia Institute for Immuno-Oncology at The Ohio State University Comprehensive Cancer Center–Arthur G. James Cancer Hospital and Richard J. Solove Research Institute)

  • Anahita Jalilvand

    (Wexner Medical Center at The Ohio State University)

  • Valerie P. Wright

    (Wexner Medical Center at The Ohio State University)

  • Joey Liu

    (Wexner Medical Center at The Ohio State University)

  • Alan J. Smith

    (Wexner Medical Center at The Ohio State University)

  • David Bradley

    (Wexner Medical Center at The Ohio State University)

  • William Lafuse

    (The Ohio State University)

  • YunZhou Liu

    (Pelotonia Institute for Immuno-Oncology at The Ohio State University Comprehensive Cancer Center–Arthur G. James Cancer Hospital and Richard J. Solove Research Institute)

  • Nyelia F. Williams

    (Pelotonia Institute for Immuno-Oncology at The Ohio State University Comprehensive Cancer Center–Arthur G. James Cancer Hospital and Richard J. Solove Research Institute)

  • Owen Snyder

    (Pelotonia Institute for Immuno-Oncology at The Ohio State University Comprehensive Cancer Center–Arthur G. James Cancer Hospital and Richard J. Solove Research Institute)

  • Caroline Wheeler

    (Pelotonia Institute for Immuno-Oncology at The Ohio State University Comprehensive Cancer Center–Arthur G. James Cancer Hospital and Richard J. Solove Research Institute)

  • Bradley Needleman

    (The Ohio State University)

  • Stacy Brethauer

    (The Ohio State University)

  • Sabrena Noria

    (The Ohio State University)

  • David Renton

    (The Ohio State University)

  • Kyle A. Perry

    (The Ohio State University)

  • Prabha Nagareddy

    (Cardiovascular Section University of Oklahoma Health Sciences Center (OUHSC))

  • Daniel Wozniak

    (The Ohio State University)

  • Sahil Mahajan

    (The Ohio State University)

  • Pranav S. J. B. Rana

    (The Ohio State University)

  • Maciej Pietrzak

    (The Ohio State University)

  • Larry S. Schlesinger

    (Texas Biomedical Research Institute)

  • Daniel J. Spakowicz

    (Pelotonia Institute for Immuno-Oncology at The Ohio State University Comprehensive Cancer Center–Arthur G. James Cancer Hospital and Richard J. Solove Research Institute)

  • Willa A. Hsueh

    (Wexner Medical Center at The Ohio State University)

Abstract

Neutrophils are increasingly implicated in chronic inflammation and metabolic disorders. Here, we show that visceral adipose tissue (VAT) from individuals with obesity contains more neutrophils than in those without obesity and is associated with a distinct bacterial community. Exploring the mechanism, we gavaged microbiome-depleted mice with stool from patients with and without obesity during high-fat or normal diet administration. Only mice receiving high-fat diet and stool from subjects with obesity show enrichment of VAT neutrophils, suggesting donor microbiome and recipient diet determine VAT neutrophilia. A rise in pro-inflammatory CD4+ Th1 cells and a drop in immunoregulatory T cells in VAT only follows if there is a transient spike in neutrophils. Human VAT neutrophils exhibit a distinct gene expression pattern that is found in different human tissues, including tumors. VAT neutrophils and bacteria may be a novel therapeutic target for treating inflammatory-driven complications of obesity, including insulin resistance and colon cancer.

Suggested Citation

  • Dharti Shantaram & Rebecca Hoyd & Alecia M. Blaszczak & Linda Antwi & Anahita Jalilvand & Valerie P. Wright & Joey Liu & Alan J. Smith & David Bradley & William Lafuse & YunZhou Liu & Nyelia F. Willia, 2024. "Obesity-associated microbiomes instigate visceral adipose tissue inflammation by recruitment of distinct neutrophils," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48935-5
    DOI: 10.1038/s41467-024-48935-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48935-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48935-5?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. Justin I. Odegaard & Roberto R. Ricardo-Gonzalez & Matthew H. Goforth & Christine R. Morel & Vidya Subramanian & Lata Mukundan & Alex Red Eagle & Divya Vats & Frank Brombacher & Anthony W. Ferrante & , 2007. "Macrophage-specific PPARγ controls alternative activation and improves insulin resistance," Nature, Nature, vol. 447(7148), pages 1116-1120, June.
    2. Ivan Vujkovic-Cvijin & Jack Sklar & Lingjing Jiang & Loki Natarajan & Rob Knight & Yasmine Belkaid, 2020. "Host variables confound gut microbiota studies of human disease," Nature, Nature, vol. 587(7834), pages 448-454, November.
    3. David Bradley & Alan J. Smith & Alecia Blaszczak & Dharti Shantaram & Stephen M. Bergin & Anahita Jalilvand & Valerie Wright & Kathleen L. Wyne & Revati S. Dewal & Lisa A. Baer & Katherine R. Wright &, 2022. "Interferon gamma mediates the reduction of adipose tissue regulatory T cells in human obesity," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    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. Alexandra M. Cheney & Stephanann M. Costello & Nicholas V. Pinkham & Annie Waldum & Susan C. Broadaway & Maria Cotrina-Vidal & Marc Mergy & Brian Tripet & Douglas J. Kominsky & Heather M. Grifka-Walk , 2023. "Gut microbiome dysbiosis drives metabolic dysfunction in Familial dysautonomia," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Cameron Martino & Livia S. Zaramela & Bei Gao & Mallory Embree & Janna Tarasova & Seth J. Parker & Yanhan Wang & Huikuan Chu & Peng Chen & Kuei-Chuan Lee & Daniela Domingos Galzerani & Jivani M. Genga, 2022. "Acetate reprograms gut microbiota during alcohol consumption," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Braden T Tierney & Yingxuan Tan & Zhen Yang & Bing Shui & Michaela J Walker & Benjamin M Kent & Aleksandar D Kostic & Chirag J Patel, 2022. "Systematically assessing microbiome–disease associations identifies drivers of inconsistency in metagenomic research," PLOS Biology, Public Library of Science, vol. 20(3), pages 1-18, March.
    4. Lixiang Zhai & Haitao Xiao & Chengyuan Lin & Hoi Leong Xavier Wong & Yan Y. Lam & Mengxue Gong & Guojun Wu & Ziwan Ning & Chunhua Huang & Yijing Zhang & Chao Yang & Jingyuan Luo & Lu Zhang & Ling Zhao, 2023. "Gut microbiota-derived tryptamine and phenethylamine impair insulin sensitivity in metabolic syndrome and irritable bowel syndrome," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Yiming Lu & Aiqing Yang & Cheng Quan & Yingwei Pan & Haoyun Zhang & Yuanfeng Li & Chengming Gao & Hao Lu & Xueting Wang & Pengbo Cao & Hongxia Chen & Shichun Lu & Gangqiao Zhou, 2022. "A single-cell atlas of the multicellular ecosystem of primary and metastatic hepatocellular carcinoma," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. 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.
    7. Louise Grahnemo & Maria Nethander & Eivind Coward & Maiken Elvestad Gabrielsen & Satya Sree & Jean-Marc Billod & Klara Sjögren & Lars Engstrand & Koen F. Dekkers & Tove Fall & Arnulf Langhammer & Kris, 2023. "Identification of three bacterial species associated with increased appendicular lean mass: the HUNT study," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    8. Yolanda Y. Huang & Morgan N. Price & Allison Hung & Omree Gal-Oz & Surya Tripathi & Christopher W. Smith & Davian Ho & Héloïse Carion & Adam M. Deutschbauer & Adam P. Arkin, 2024. "Barcoded overexpression screens in gut Bacteroidales identify genes with roles in carbon utilization and stress resistance," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    9. Randall H. Friedline & Hye Lim Noh & Sujin Suk & Mahaa Albusharif & Sezin Dagdeviren & Suchaorn Saengnipanthkul & Bukyung Kim & Allison M. Kim & Lauren H. Kim & Lauren A. Tauer & Natalie M. Baez Torre, 2024. "IFNγ-IL12 axis regulates intercellular crosstalk in metabolic dysfunction-associated steatotic liver disease," Nature Communications, Nature, vol. 15(1), pages 1-18, 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:15:y:2024:i:1:d:10.1038_s41467-024-48935-5. 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.