Aerobic Plus Resistance Exercise in Obese Older Adults Improves Muscle Protein Synthesis and Preserves Myocellular Quality Despite Weight Loss

Georgia Colleluori, Lina Aguirre, Uma Phadnis, Kenneth Fowler, Reina Armamento-Villareal, Zheng Sun, Lorenzo Brunetti, Jun Hyoung Park, Benny Abraham Kaipparettu, Nagireddy Putluri, Vimlin Auetumrongsawat, Kevin Yarasheski, Clifford Qualls, Dennis T Villareal, Georgia Colleluori, Lina Aguirre, Uma Phadnis, Kenneth Fowler, Reina Armamento-Villareal, Zheng Sun, Lorenzo Brunetti, Jun Hyoung Park, Benny Abraham Kaipparettu, Nagireddy Putluri, Vimlin Auetumrongsawat, Kevin Yarasheski, Clifford Qualls, Dennis T Villareal

Abstract

Anabolic resistance and impaired myocellular quality contribute to age-related sarcopenia, which exacerbates with obesity. Diet-induced muscle mass loss is attenuated by resistance or aerobic plus resistance exercise compared to aerobic exercise in obese elderly. We assessed chronic effects of weight loss plus different exercise modalities on muscle protein synthesis response to feeding and myocellular quality. Obese older adults were randomized to a weight-management program plus aerobic, resistance, or combined aerobic and resistance exercise or to control. Participants underwent vastus lateralis biopsies at baseline and 6 months. Muscle protein synthesis rate increased more in resistance and combined than in control. Autophagy mediators' expression decreased more in combined than in aerobic, which experienced a higher increase in inflammation and mitochondrial regulators' expression. In obese elderly, combined aerobic and resistance exercise is superior to either mode independently for improving muscle protein synthesis and myocellular quality, thereby maintaining muscle mass during weight-loss therapy.

Trial registration: ClinicalTrials.gov NCT01065636.

Keywords: aging; calorie restriction; diet; exercise; lifestyle intervention; muscle protein synthesis; muscle quality; sarcopenia; weight loss.

Conflict of interest statement

DECLARATION OF INTEREST

The authors declare no conflicts of interest.

Published by Elsevier Inc.

Figures

Figure 1. Screening, Randomization, and Follow-up.
Figure 1. Screening, Randomization, and Follow-up.
Study groups included a Control group that participated in neither a weight-management nor an exercise intervention and three exercise groups: a group that participated in aerobic exercise training (Aerobic group), a group that participated in resistance exercise training (Resistance group), and a group that received combined aerobic and resistance exercise training (Combined group); all three exercise groups also participated in a weight-management program.
Figure 2. Muscle Protein Metabolism Studies
Figure 2. Muscle Protein Metabolism Studies
Glucose concentrations (Panel A), insulin concentrations (Panel B), and α-ketoisocaproic acid (KIC) enrichments (Panel C) during the stable isotope infusion in basal (post-absorptive) conditions and mixed meal feeding before and at 6 months of diet-induced weight loss plus different types of exercise interventions in obese older adults. Outline of the protocol (Panel D). Muscle protein synthesis rate during mixed meal feeding before and at 6 months of interventions (Panel E). Muscle protein synthesis rate was calculated using muscle tissue fluid as precursor pool for protein synthesis. Between-group differences in changes from baseline: * p

Figure 3. Gene Expression, Enzyme Activities, and…

Figure 3. Gene Expression, Enzyme Activities, and Metabolites Studies

Gene expression analyses by nanostring (Panel…

Figure 3. Gene Expression, Enzyme Activities, and Metabolites Studies
Gene expression analyses by nanostring (Panel A) and RT-qPCR (Panel B) and protein expression analyses by western blot (Panel C) of representative targets. Fold changes are calculated as the ratio between gene expression or protein levels at 6 months and at baseline. Citrate synthase (Panel D) and Cytochrome c oxidase (Panel E) activities expressed in nmol/min/mg of proteins at baseline and 6 months. Succinate metabolite (Panel F) expressed as normalized intensity at baseline and 6 months. Between-group comparisons in changes from baseline: * p
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Figure 3. Gene Expression, Enzyme Activities, and…
Figure 3. Gene Expression, Enzyme Activities, and Metabolites Studies
Gene expression analyses by nanostring (Panel A) and RT-qPCR (Panel B) and protein expression analyses by western blot (Panel C) of representative targets. Fold changes are calculated as the ratio between gene expression or protein levels at 6 months and at baseline. Citrate synthase (Panel D) and Cytochrome c oxidase (Panel E) activities expressed in nmol/min/mg of proteins at baseline and 6 months. Succinate metabolite (Panel F) expressed as normalized intensity at baseline and 6 months. Between-group comparisons in changes from baseline: * p

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