Impact of resistance exercise on ribosome biogenesis is acutely regulated by post-exercise recovery strategies.

Matthew P. G. Barnett,Llion A. Roberts,David Cameron-Smith,James F. Markworth,Truls Raastad,Vandré C. Figueiredo,Jonathan M. Peake,Jeff S. Coombes

doi:10.14814/phy2.12670

Abstract

Muscle hypertrophy occurs following increased protein synthesis, which requires activation of the ribosomal complex. Additionally, increased translational capacity via elevated ribosomal RNA (rRNA) synthesis has also been implicated in resistance training-induced skeletal muscle hypertrophy. The time course of ribosome biogenesis following resistance exercise (RE) and the impact exerted by differing recovery strategies remains unknown. In the present study, the activation of transcriptional regulators, the expression levels of pre-rRNA, and mature rRNA components were measured through 48h after a single-bout RE. In addition, the effects of either low-intensity cycling (active recovery, ACT) or a cold-water immersion (CWI) recovery strategy were compared. Nine male subjects performed two bouts of high-load RE randomized to be followed by 10min of either ACT or CWI. Muscle biopsies were collected before RE and at 2, 24, and 48h after RE. RE increased the phosphorylation of the p38-MNK1-eIF4E axis, an effect only evident with ACT recovery. Downstream, cyclin D1 protein, total eIF4E, upstream binding factor 1 (UBF1), and c-Myc proteins were all increased only after RE with ACT. This corresponded with elevated abundance of the pre-rRNAs (45S, ITS-28S, ITS-5.8S, and ETS-18S) from 24h after RE with ACT. In conclusion, coordinated upstream signaling and activation of transcriptional factors stimulated pre-rRNA expression after RE. CWI, as a recovery strategy, markedly blunted these events, suggesting that suppressed ribosome biogenesis may be one factor contributing to the impaired hypertrophic response observed when CWI is used regularly after exercise.

Highlights

Resistance exercise (RE) training results in marked structural and contractile adaptations within skeletal muscle
Ribosome biogenesis has recently been implicated in muscle hypertrophy induced by RE (Figueiredo et al 2015)
A single bout of high-load RE activated multiple cellular signaling events that enable the activation of transcriptional factors involved in the recruitment of polymerase I (Pol I), the initiation of ribosome biogenesis and increased pre-ribosomal RNA (rRNA) expression

Summary

Introduction

Resistance exercise (RE) training results in marked structural and contractile adaptations within skeletal muscle. This complex tissue remodeling is dependent upon increased protein synthesis to enable muscle fiber hypertrophy. The first and rate-limiting step of ribosome biogenesis is transcription of the rDNA into the precursor 45S rRNA (Panov et al 2001). This requires various transcriptional factors such as upstream binding factor (UBF) and transcription initiation factor IA (TIF-IA) to bind to the rDNA promoter and induce the synthesis of the prerRNA by the dedicated RNA polymerase I (Pol I) (Moss et al 2007). Together with 80+ ribosomal proteins by RNA polymerase II and 5S rRNA transcribed by rRNA polymerase III, these mature rRNAs eventually form the large and small subunits of the ribosome (Henras et al 2015)

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Results

Conclusion