Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese Adults

Adipose tissue pathology in obese patients often features impaired adipogenesis, angiogenesis, and chronic low-grade inflammation, all of which are regulated in large part by adipose tissue stromal vascular cells [SVC; i.e., non-adipocyte cells within adipose tissue including preadipocytes, endothel...

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Main Authors: Alison C. Ludzki, Emily M. Krueger, Toree C. Baldwin, Michael W. Schleh, Cara E. Porsche, Benjamin J. Ryan, Lindsey A. Muir, Kanakadurga Singer, Carey N. Lumeng, Jeffrey F. Horowitz
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2020.00903/full
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author Alison C. Ludzki
Emily M. Krueger
Toree C. Baldwin
Michael W. Schleh
Cara E. Porsche
Cara E. Porsche
Benjamin J. Ryan
Lindsey A. Muir
Kanakadurga Singer
Kanakadurga Singer
Kanakadurga Singer
Carey N. Lumeng
Carey N. Lumeng
Carey N. Lumeng
Jeffrey F. Horowitz
author_facet Alison C. Ludzki
Emily M. Krueger
Toree C. Baldwin
Michael W. Schleh
Cara E. Porsche
Cara E. Porsche
Benjamin J. Ryan
Lindsey A. Muir
Kanakadurga Singer
Kanakadurga Singer
Kanakadurga Singer
Carey N. Lumeng
Carey N. Lumeng
Carey N. Lumeng
Jeffrey F. Horowitz
author_sort Alison C. Ludzki
collection DOAJ
description Adipose tissue pathology in obese patients often features impaired adipogenesis, angiogenesis, and chronic low-grade inflammation, all of which are regulated in large part by adipose tissue stromal vascular cells [SVC; i.e., non-adipocyte cells within adipose tissue including preadipocytes, endothelial cells (ECs), and immune cells]. Exercise is known to increase subcutaneous adipose tissue lipolysis, but the impact of exercise on SVCs in adipose tissue has not been explored. The purpose of this study was to assess the effects of a session of exercise on preadipocyte, EC, macrophage, and T cell content in human subcutaneous adipose tissue. We collected abdominal subcutaneous adipose tissue samples from 10 obese adults (BMI 33 ± 3 kg/m2, body fat 41 ± 7%) 12 h after a 60 min acute session of endurance exercise (80 ± 3%HRpeak) vs. no acute exercise session. SVCs were isolated by collagenase digestion and stained for flow cytometry. We found that acute exercise reduced preadipocyte content (38 ± 7 vs. 30 ± 13%SVC; p = 0.04). The reduction was driven by a decrease in CD34hi preadipocytes (18 ± 5 vs. 13 ± 6%SVC; p = 0.002), a subset of preadipocytes that generates high lipolytic rate adipocytes ex vivo. Acute exercise did not alter EC content. Acute exercise also did not change total immune cell, macrophage, or T cell content, and future work should assess the effects of exercise on subpopulations of these cells. We conclude that exercise may rapidly regulate the subcutaneous adipose tissue preadipocyte pool in ways that may help attenuate the high lipolytic rates that are commonly found in obesity.
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spelling doaj.art-d07f41fb589b4cd1b8d4d8a8ee71bc612022-12-21T17:17:32ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-07-011110.3389/fphys.2020.00903560263Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese AdultsAlison C. Ludzki0Emily M. Krueger1Toree C. Baldwin2Michael W. Schleh3Cara E. Porsche4Cara E. Porsche5Benjamin J. Ryan6Lindsey A. Muir7Kanakadurga Singer8Kanakadurga Singer9Kanakadurga Singer10Carey N. Lumeng11Carey N. Lumeng12Carey N. Lumeng13Jeffrey F. Horowitz14Substrate Metabolism Laboratory, School of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesSubstrate Metabolism Laboratory, School of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesSubstrate Metabolism Laboratory, School of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesSubstrate Metabolism Laboratory, School of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesDepartment of Pediatrics, Medical School, University of Michigan, Ann Arbor, MI, United StatesGraduate Program in Immunology, Medical School, University of Michigan, Ann Arbor, MI, United StatesSubstrate Metabolism Laboratory, School of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesDepartment of Computational Medicine and Bioinformatics, Medical School, University of Michigan, Ann Arbor, MI, United StatesDepartment of Pediatrics, Medical School, University of Michigan, Ann Arbor, MI, United StatesGraduate Program in Immunology, Medical School, University of Michigan, Ann Arbor, MI, United StatesDepartment of Molecular and Integrative Physiology, Medical School, University of Michigan, Ann Arbor, MI, United StatesDepartment of Pediatrics, Medical School, University of Michigan, Ann Arbor, MI, United StatesGraduate Program in Immunology, Medical School, University of Michigan, Ann Arbor, MI, United StatesDepartment of Molecular and Integrative Physiology, Medical School, University of Michigan, Ann Arbor, MI, United StatesSubstrate Metabolism Laboratory, School of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesAdipose tissue pathology in obese patients often features impaired adipogenesis, angiogenesis, and chronic low-grade inflammation, all of which are regulated in large part by adipose tissue stromal vascular cells [SVC; i.e., non-adipocyte cells within adipose tissue including preadipocytes, endothelial cells (ECs), and immune cells]. Exercise is known to increase subcutaneous adipose tissue lipolysis, but the impact of exercise on SVCs in adipose tissue has not been explored. The purpose of this study was to assess the effects of a session of exercise on preadipocyte, EC, macrophage, and T cell content in human subcutaneous adipose tissue. We collected abdominal subcutaneous adipose tissue samples from 10 obese adults (BMI 33 ± 3 kg/m2, body fat 41 ± 7%) 12 h after a 60 min acute session of endurance exercise (80 ± 3%HRpeak) vs. no acute exercise session. SVCs were isolated by collagenase digestion and stained for flow cytometry. We found that acute exercise reduced preadipocyte content (38 ± 7 vs. 30 ± 13%SVC; p = 0.04). The reduction was driven by a decrease in CD34hi preadipocytes (18 ± 5 vs. 13 ± 6%SVC; p = 0.002), a subset of preadipocytes that generates high lipolytic rate adipocytes ex vivo. Acute exercise did not alter EC content. Acute exercise also did not change total immune cell, macrophage, or T cell content, and future work should assess the effects of exercise on subpopulations of these cells. We conclude that exercise may rapidly regulate the subcutaneous adipose tissue preadipocyte pool in ways that may help attenuate the high lipolytic rates that are commonly found in obesity.https://www.frontiersin.org/article/10.3389/fphys.2020.00903/fullpreadipocytesexerciseobesitymacrophagesendothelial cellsT cells
spellingShingle Alison C. Ludzki
Emily M. Krueger
Toree C. Baldwin
Michael W. Schleh
Cara E. Porsche
Cara E. Porsche
Benjamin J. Ryan
Lindsey A. Muir
Kanakadurga Singer
Kanakadurga Singer
Kanakadurga Singer
Carey N. Lumeng
Carey N. Lumeng
Carey N. Lumeng
Jeffrey F. Horowitz
Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese Adults
Frontiers in Physiology
preadipocytes
exercise
obesity
macrophages
endothelial cells
T cells
title Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese Adults
title_full Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese Adults
title_fullStr Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese Adults
title_full_unstemmed Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese Adults
title_short Acute Aerobic Exercise Remodels the Adipose Tissue Progenitor Cell Phenotype in Obese Adults
title_sort acute aerobic exercise remodels the adipose tissue progenitor cell phenotype in obese adults
topic preadipocytes
exercise
obesity
macrophages
endothelial cells
T cells
url https://www.frontiersin.org/article/10.3389/fphys.2020.00903/full
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