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

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. Williams, Owen Snyder, Caroline Wheeler, Bradley Needleman, Stacy Brethauer, Sabrena Noria, David Renton, Kyle A. Perry, Prabha Nagareddy, Daniel Wozniak, Sahil Mahajan, Pranav S. J. B. Rana, Maciej Pietrzak, Larry S. Schlesinger, Daniel J. Spakowicz () and Willa A. Hsueh ()
Additional contact information
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

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-48935-5

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