Exercise counteracts the effects of short-term overfeeding and reduced physical activity independent of energy imbalance in healthy young men

Abstract

Physical activity can affect many aspects of metabolism but it is unclear to what extent this relies on manipulation of energy balance. Twenty-six active men age 25 ± 7 years (mean ± SD) were randomly assigned either to consume 50% more energy than normal by over-consuming their habitual diet for 7 days whilst simultaneously restricting their physical activity below 4000 steps day(-1) to induce an energy surplus (SUR group; n = 14) or to the same regimen but with 45 min of daily treadmill running at 70% of maximum oxygen uptake (SUR+EX group; n = 12). Critically, the SUR+EX group received additional dietary energy intake to account for the energy expended by exercise, thus maintaining a matched energy surplus. At baseline and follow-up, fasted blood samples and abdominal subcutaneous adipose tissue biopsies were obtained and oral glucose tolerance tests conducted. Insulinaemic responses to a standard glucose load increased 2-fold from baseline to follow-up in the SUR group (17 ± 16 nmol (120 min) l(-1); P = 0.002) whereas there was no change in the SUR+EX group (1 ± 6 nmol (120 min) l(-1)). Seven of 17 genes within adipose tissue were differentially expressed in the SUR group; expression of SREBP-1c, FAS and GLUT4 was significantly up-regulated and expression of PDK4, IRS2, HSL and visfatin was significantly down-regulated (P ≤ 0.05). The pAMPK/AMPK protein ratio in adipose tissue was significantly down-regulated in the SUR group (P = 0.005). Vigorous-intensity exercise counteracted most of the effects of short-term overfeeding and under-activity at the whole-body level and in adipose tissue, even in the face of a standardised energy surplus.

Figures

Figure 1. Schematic representation of the achieved energy surplus induced by the overfeeding and restricted physical activity model in SUR group (n= 13) and SUR+EX group (n= 12)

Energy intake estimated from diet analysis (PRO, protein; CHO, carbohydrate; EtOH, energy from Alcohol). RMR estimated from indirect calorimetry. DIT was calculated post-intervention as 8.3% of energy intake; this was done by calculating the specific DIT associated with each macronutrient before the overall DIT was determined. PAEE was based on step count and indirect calorimetry (exercise, EX). Energy surplus was calculated as the difference between energy intake and energy expenditure. Values are means ± CI.

Figure 2. Serum insulin 2 h iAUC (A) and plasma glucose 2 h iAUC (B) in response to the OGTT before and after a week of overfeeding and reduced physical activity

Means ± CI are shown. In A, *denotes a day × group interaction (P= 0.002) and # denotes values different pre–post within SUR group (P= 0.001).

Figure 3. Relative gene expression of several key genes measured in adipose tissue at baseline and follow-up for the SUR group (n= 10) and the SUR+EX group (n= 12)

Dashed line represents no change. Data normalised to PPIA, baseline and internal calibrator. Sufficient RNA could not be obtained from some smaller biopsies to carry out gene expression analysis on those samples; as a result n= 10 in the SUR group and n= 12 in the SUR+EX group. Any change scores that were over 3 SDs from the mean (n= 14) were excluded from this figure but were included in the statistical analysis which used the logged values. Samples outside the detectable limit (Ct > 35; n= 46) were excluded from the analysis. Leptin (SUR+EX, n= 10), SREBP-1c (SUR, n= 9), PDK4 (SUR, n= 8), FAS (SUR, n= 9), TNFa (SUR, n= 9; SUR+EX, n= 9), IRS2 (SUR+EX, n= 11), HSL (SUR+EX, n= 11), visfatin (SUR+EX, n= 11), IL-18 (SUR, n= 6; SUR+EX, n= 7), IL-6 (SUR, n= 3; SUR+EX, n= 6), AMPK (SUR+EX, n= 11), apelin (SUR, n= 4, SUR+EX, n= 6). Values are means ± SEM. *P≤ 0.05 day × group interaction. #P≤ 0.05 baseline vs. follow-up. †Main effect of day (i.e.: Day 1 vs. Day 8, both groups; P≤ 0.05).

Figure 4. Mean fold change in the expression of several key proteins measured in adipose tissue at baseline and follow-up for the SUR group (n= 7) and the SUR+EX group (n= 8)

Data normalised to GAPDH. Values are means ± CI. *P≤ 0.05 day × group interaction. #P≤ 0.05 baseline vs. follow-up. †Main effect of day (i.e.: Day 1 vs. Day 8, both groups; P≤ 0.05). Representative blots for each protein are shown in Supplemental Fig. S2, available online.