Abstract
External loads applied to skeletal muscle cause increases in the protein translation rate, which leads to muscle hypertrophy. Although some studies have demonstrated that increases in the capacity and efficiency of translation are involved in this process, it remains unclear how these two factors are related to the magnitude of muscle hypertrophy. The present study aimed to clarify the roles played by the capacity and efficiency of translation in muscle hypertrophy. We used an improved synergist ablation in which the magnitude of compensatory hypertrophy could be controlled by partial removal of synergist muscles. Male rats were assigned to four groups in which the plantaris muscle was unilaterally subjected to weak (WK), moderate (MO), middle (MI), and strong (ST) overloading by four types of synergist ablation. Fourteen days after surgery, the weight of the plantaris muscle per body weight increased by 8%, 22%, 32% and 45%, in the WK, MO, MI and ST groups, respectively. Five days after surgery, 18+28S rRNA content (an indicator of translational capacity) increased with increasing overload, with increases of 1.8-fold (MO), 2.2-fold (MI), and 2.5-fold (ST), respectively, relative to non-overloaded muscle (NL) in the WK group. rRNA content showed a strong correlation with relative muscle weight measured 14 days after surgery (r = 0.98). The phosphorylated form of p70S6K (a positive regulator of translational efficiency) showed a marked increase in the MO group, but no further increase was observed with further increase in overload (increases of 22.6-fold (MO), 17.4-fold (MI), and 18.2-fold (ST), respectively, relative to NL in the WK group). These results indicate that increases in ribosome biogenesis at the early phase of overloading are strongly dependent on the amount of overloading, and may play an important role in increasing the translational capacity for further gain of muscular size.
Highlights
In skeletal muscle, it is generally known that the increase of muscle mass subsequent to application of an external load is achieved by the accumulation of increasing of protein synthesis [1]
Our aims were: (i) to establish an animal model of muscle hypertrophy in which the magnitude of hypertrophy can be controlled in a stepwise manner; and (ii) to ascertain if the magnitude of muscle hypertrophy is correlated with ribosome biogenesis and/or p70S6K activation in the early phase of overloading
The relative weight of the plantaris muscle in OL legs was increased significantly compared with non-overloaded muscle (NL) legs (increases of: 7.9 ± 2.4% in WK; 18.7 ± 2.0% in MO; 33.1 ± 3.0% in MO; 50.4 ± 5.3% in ST (P = 0.0004, P = 0.0003, P < 0.0001, P
Summary
It is generally known that the increase of muscle mass subsequent to application of an external load is achieved by the accumulation of increasing of protein synthesis [1]. Among the processes involved in protein synthesis, protein translation has a central role in determining the amount of protein synthesized. To ascertain the part played by translation in overload and/or exercise-induced muscle hypertrophy, contributions of the capacity and efficiency of translation must be considered [2]. Both processes have been thought to be important in the exercise-induced increase in protein synthesis. Most studies have focused on the mechanisms controlling translational efficiency (e.g., ribosome activation through the mammalian target of rapamycin (mTOR) C1 signaling pathway [3,4]) and not on the contribution of “translational capacity”
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