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Multiomics reveals persistence of obesity-associated immune cell phenotypes in adipose tissue during weight loss and weight regain in mice

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  • Matthew A. Cottam

    (Vanderbilt University School of Medicine)

  • Heather L. Caslin

    (Vanderbilt University School of Medicine)

  • Nathan C. Winn

    (Vanderbilt University School of Medicine)

  • Alyssa H. Hasty

    (Vanderbilt University School of Medicine
    VA Tennessee Valley Healthcare System)

Abstract

Within adipose tissue (AT), immune cells and parenchymal cells closely interact creating a complex microenvironment. In obesity, immune cell derived inflammation contributes to insulin resistance and glucose intolerance. Diet-induced weight loss improves glucose tolerance; however, weight regain further exacerbates the impairment in glucose homeostasis observed with obesity. To interrogate the immunometabolic adaptations that occur in AT during murine weight loss and weight regain, we utilized cellular indexing of transcriptomes and epitopes by sequencing (CITEseq) in male mice. Obesity-induced imprinting of AT immune cells persisted through weight-loss and progressively worsened with weight regain, ultimately leading to impaired recovery of type 2 regulatory cells, activation of antigen presenting cells, T cell exhaustion, and enhanced lipid handling in macrophages in weight cycled mice. This work provides critical groundwork for understanding the immunological causes of weight cycling-accelerated metabolic disease. For further discovery, we provide an open-access web portal of diet-induced AT immune cell imprinting: https://hastylab.shinyapps.io/MAIseq .

Suggested Citation

  • Matthew A. Cottam & Heather L. Caslin & Nathan C. Winn & Alyssa H. Hasty, 2022. "Multiomics reveals persistence of obesity-associated immune cell phenotypes in adipose tissue during weight loss and weight regain in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30646-4
    DOI: 10.1038/s41467-022-30646-4
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    2. Sang Mun Han & Eun Seo Park & Jeu Park & Hahn Nahmgoong & Yoon Ha Choi & Jiyoung Oh & Kyung Min Yim & Won Taek Lee & Yun Kyung Lee & Yong Geun Jeon & Kyung Cheul Shin & Jin Young Huh & Sung Hee Choi &, 2023. "Unique adipose tissue invariant natural killer T cell subpopulations control adipocyte turnover in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Laurent L’homme & Benan Pelin Sermikli & Joel T. Haas & Sébastien Fleury & Sandrine Quemener & Valentine Guinot & Emelie Barreby & Nathalie Esser & Robert Caiazzo & Hélène Verkindt & Benjamin Legendre, 2024. "Adipose tissue macrophage infiltration and hepatocyte stress increase GDF-15 throughout development of obesity to MASH," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Alexander Piening & Emily Ebert & Carter Gottlieb & Niloufar Khojandi & Lindsey M. Kuehm & Stella G. Hoft & Kelly D. Pyles & Kyle S. McCommis & Richard J. DiPaolo & Stephen T. Ferris & Elise Alspach &, 2024. "Obesity-related T cell dysfunction impairs immunosurveillance and increases cancer risk," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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