Muscle damaging eccentric exercise attenuates disuse-induced declines in daily myofibrillar protein synthesis and transiently prevents muscle atrophy in healthy men.

Tom S O Jameson,Doaa R Abdelrahman,Andrew J Murton,Benjamin T Wall,Sean P Kilroe,Marlou L Dirks,Francis B Stephens,Jonathan Fulford

doi:10.1152/ajpendo.00294.2021

Abstract

Short-term disuse leads to muscle loss driven by lowered daily myofibrillar protein synthesis (MyoPS). However, disuse commonly results from muscle damage, and its influence on muscle deconditioning during disuse is unknown. Twenty-one males [20 ± 1 yr, BMI = 24 ± 1 kg·m-2 (± SE)] underwent 7 days of unilateral leg immobilization immediately preceded by 300 bilateral, maximal, muscle-damaging eccentric quadriceps contractions (DAM; subjects n = 10) or no exercise (CON; subjects n = 11). Participants ingested deuterated water and underwent temporal bilateral thigh MRI scans and vastus lateralis muscle biopsies of immobilized (IMM) and nonimmobilized (N-IMM) legs. N-IMM quadriceps muscle volume remained unchanged throughout both groups. IMM quadriceps muscle volume declined after 2 days by 1.7 ± 0.5% in CON (P = 0.031; and by 1.3 ± 0.6% when corrected to N-IMM; P = 0.06) but did not change in DAM, and declined equivalently in CON [by 6.4 ± 1.1% (5.0 ± 1.6% when corrected to N-IMM)] and DAM [by 2.6 ± 1.8% (4.0 ± 1.9% when corrected to N-IMM)] after 7 days. Immobilization began to decrease MyoPS compared with N-IMM in both groups after 2 days (P = 0.109), albeit with higher MyoPS rates in DAM compared with CON (P = 0.035). Frank suppression of MyoPS was observed between days 2 and 7 in CON (IMM = 1.04 ± 0.12, N-IMM = 1.86 ± 0.10%·day-1; P = 0.002) but not DAM (IMM = 1.49 ± 0.29, N-IMM = 1.90 ± 0.30%·day-1; P > 0.05). Declines in MyoPS and quadriceps volume after 7 days correlated positively in CON (r2=0.403; P = 0.035) but negatively in DAM (r2=0.483; P = 0.037). Quadriceps strength declined following immobilization in both groups, but to a greater extent in DAM. Prior muscle-damaging eccentric exercise increases MyoPS and prevents loss of quadriceps muscle volume after 2 (but not 7) days of disuse.NEW & NOTEWORTHY We investigated the impact of prior muscle-damaging eccentric exercise on disuse-induced muscle deconditioning. Two and 7 days of muscle disuse per se lowered quadriceps muscle volume in association with lowered daily myofibrillar protein synthesis (MyoPS). Prior eccentric exercise prevented the decline in muscle volume after 2 days and attenuated the decline in MyoPS after 2 and 7 days. These data indicate eccentric exercise increases MyoPS and transiently prevents quadriceps muscle atrophy during muscle disuse.

Highlights

A short-term period of rehabilitative physical inactivity or complete limb immobilization is often prescribed following acute musculoskeletal injury to facilitate healing and prevent further injury [1]
We have recently reported that these acute metabolic perturbations translate to reduced daily myofibrillar protein synthesis (MyoPS) rates measured under free-living conditions during 2–7 days of limb immobilization in healthy men [16, 24], with the extent of the decline positively correlating with the loss of muscle mass [24]
We assessed the temporal modulation of short-term (2 and 7 days) “uncomplicated” muscle disuse deconditioning by the presence of prior muscle damage in young healthy males; a novel paradigm to experimentally model more clinically relevant “complicated” muscle disuse

Summary

Introduction

A short-term period of rehabilitative physical inactivity or complete limb immobilization is often prescribed following acute musculoskeletal injury (e.g., sports injuries) to facilitate healing and prevent further injury [1]. Experimental physical inactivity is commonly modeled in the laboratory by subjecting healthy, uninjured individuals to acute (e.g., 1– 14 days) muscle disuse via limb immobilization Uncomplicated human muscle disuse atrophy can largely be explained by declines in myofibrillar protein synthesis (MyoPS) rates. We have recently reported that these acute metabolic perturbations translate to reduced daily MyoPS rates measured under free-living conditions during 2–7 days of limb immobilization in healthy men [16, 24], with the extent of the decline positively correlating with the loss of muscle mass [24]

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