Effects of endurance exercise training on inflammatory circulating progenitor cell content in lean and obese adults

Grace M Niemiro; Jacob M Allen; Lucy J Mailing; Naiman A Khan; Hannah D Holscher; Jeffrey A Woods; Michael De Lisio

doi:10.1113/JP276023

Effects of endurance exercise training on inflammatory circulating progenitor cell content in lean and obese adults

J Physiol. 2018 Jul;596(14):2811-2822. doi: 10.1113/JP276023. Epub 2018 Jun 19.

Authors

Grace M Niemiro¹, Jacob M Allen^{1

2}, Lucy J Mailing^{1

3}, Naiman A Khan^{1

3}, Hannah D Holscher^{1

3

4}, Jeffrey A Woods¹, Michael De Lisio^{1

3

5}

Affiliations

¹ Department of Kinesiology and Community Health, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
² Center for Microbial Pathogenesis, Nationwide Children's Hospital, Columbus, OH, USA.
³ Division of Nutritional Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
⁴ Department of Food Sciences and Human Nutrition, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
⁵ School of Human Kinetics, Brain and Mind Institute, Centre on Neuromuscular Disease, Regenerative Medicine Program, University of Ottawa, Ottawa, ON, Canada.

Abstract

Key points: Chronic inflammation underlies many of the health decrements associated with obesity. Circulating progenitor cells can sense and respond to inflammatory stimuli, increasing the local inflammatory response within tissues. Here we show that 6 weeks of endurance exercise training significantly decreases inflammatory circulating progenitor cells in obese adults. These findings provide novel cellular mechanisms for the beneficial effects of exercise in obese adults.

Abstract: Circulating progenitor cells (CPCs) and subpopulations are normally found in the bone marrow, but can migrate to peripheral tissues to participate in local inflammation and/or remodelling. The purpose of this study was to compare the CPC response, particularly the inflammatory-primed haematopoietic stem and progenitor (HSPC) subpopulation, to a 6 week endurance exercise training (EET) intervention between lean and obese adults. Seventeen healthy weight (age: 23.9 ± 5.4 years, body mass index (BMI): 22.0 ± 2.6 kg m^-2 ) and 10 obese (age: 29.0 ± 8.0 years, BMI: 33.1 ± 6.0 kg m^-2 ) previously sedentary adults participated in an EET. Blood was collected before and after EET for quantification of CPCs and subpopulations via flow cytometry, colony forming unit assays and plasma concentrations of C-X-C motif chemokine 12 (CXCL12), granulocyte-colony stimulating factor (G-CSF), and chemokine (C-C motif) ligand 2 (CCL2). Exercise training reduced the number of circulating HSPCs and adipose tissue-derived mesenchymal stem cells (AT-MSCs). EET increased the colony forming potential of granulocytes and macrophages irrespective of BMI. EET reduced the number of HSPCs expressing the chemokine receptor CCR2 and the pro-inflammatory marker TLR4. EET-induced changes in adipose tissue-derived MSCs and bone marrow-derived MSCs were negatively related to changes in absolute fitness. Our results indicate that EET, regardless of BMI status, decreases CPCs and subpopulations, particularly those primed for contribution to tissue inflammation.

Keywords: Hematopoietic stem cells; Inflammation; Mesenchymal stem cell; Obesity; chemokine c receptor 2.

Publication types

Comparative Study
Research Support, Non-U.S. Gov't

MeSH terms

Adult
Cells, Cultured
Exercise Therapy / methods*
Female
Humans
Inflammation / blood*
Inflammation / etiology
Inflammation / therapy*
Male
Obesity / complications*
Physical Endurance
Stem Cells / cytology*
Stem Cells / metabolism
Thinness / complications*
Young Adult