Effects of age and gender on shortening velocity and myosin isoforms in single rat muscle fibres

Degens, Hans, Yu, Fushun, Li, Xiaopeng and Larsson, Lars (1998) Effects of age and gender on shortening velocity and myosin isoforms in single rat muscle fibres. Acta Physiologica Scandinavica, 163 (1). pp. 33-40. ISSN 1748-1716

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Abstract

The maximum velocity of unloaded shortening (V0) and the myosin heavy chain (MyHC) and light chain (MyLC) isoform composition were determined in single fibres from soleus and extensor digitorum longus (EDL) muscles of male and female rats 3–6 and 22–24 months old. In the soleus muscle, the β/slow (type I MyHC) isoform predominated in both young and old animals, irrespective of gender. In the EDL, fibres expressing type IIX MyHC or a combination of IIX and IIB (IIXB) MyHC isoforms were predominant in old rats, while type IIB MyHC fibres predominated in young individuals of both genders. The V0 of soleus fibres expressing the type I MyHC isoform decreased (P < 0.001) by 40% with age in spite of an unchanged MyLC composition. In the EDL, the V0 of fibres expressing IIX, IIXB and IIB MyHC isoforms did not change with age or differ between males and females. In conclusion, similar age-related changes in V0 and MyHC composition were observed in single muscle cells from both male and female rats. The present results demonstrate that the relationship between V0 and MyHC isoform composition at the single fibre level is similar in male and female rats, and that similar qualitative changes take place during ageing in both genders. Motor impairment, such as slowing of muscle movement and increasing muscle weakness, is a prominent feature of ageing. Consequently, many elderly people have difficulties in performing activities of daily life, maintaining postural balance and preventing impending falls. This, together with the age-related decrease in bone strength, which has been suggested to be related to muscle weakness (Madsen et al. 1993), increases the risk of bone fractures in the elderly. The problems may be even greater in women than in men, since men are generally stronger than women at any age (Miller et al. 1993), and consequently women are at greater risk of becoming impaired in certain motor tasks with ageing (Rantanen et al. 1996). The mechanisms underlying these impairments are complex, but alterations within the motor neurone and muscle cell play an important role. An understanding of the age-related changes in skeletal muscle becomes increasingly important in the light of the growing population of elderly people. The maximum velocity of unloaded shortening (V0) is one of the most important design parameters of skeletal muscle, since muscles develop their maximum power at approximately one-third of V0 (Rome et al. 1990). Thus, to generate power optimally over a wide range of movements, it is crucial to be able to recruit muscle fibres with a wide range of V0. The V0 of a muscle is proportional to the myosin adenosine triphosphatase (ATPase) activity (Bárány 1967). The activity of myosin ATPase is determined by the myosin heavy chain (MyHC) isoform composition, and there is a close correlation between V0 and this composition at the single fibre level (Reiser et al. 1985, Greaser et al. 1988, Sweeney et al. 1988, Schluter & Fitts 1994). Ageing has been reported to have different effects in muscles of male and female mammals, including man (Beltran Niclos et al. 1995, Cartee 1995, Phillips et al. 1996). Most studies on the effects of age and gender on skeletal muscle have been focused on differences in maximum force (Miller et al. 1993, Phillips et al. 1996a,b; Rantanan et al. 1996) and muscle size (Cartee 1995). However, the effects of age and gender on the shortening velocity have received less scientific attention and the studies published so far have dealt with changes in the velocity of whole muscle movement (e.g. Beltran Niclos et al. 1995). Measurements of skeletal muscle function in vivo are limited by factors that tend to obscure the behaviour of individual muscle fibres, such as (i) intramuscular differences in fibre orientation, (ii) differences in the mechanical leverage provided by the bony anatomy of the joint, (iii) the elasticity of the muscle and its tendons and, during voluntary contractions, (iv) differences in patterns of motor unit recruitment and (v) activation of antagonistic muscles. In addition, the roles of different fibre types in whole muscle contraction are difficult to evaluate. These confounding factors are circumvented in skinned fibre preparations which allow investigation of the function of the myofilament proteins in a cell with an intact filament lattice under near physiological conditions. In this study the effects of age and gender on the contractile speed and expression of myosin isoforms in skinned single fibres were investigated. On the basis of previous observations indicating that male and female rats exhibited similar age-related changes in the composition of myosin isoforms in both fast- and slow-twitch skeletal muscles (Larsson & Yu 1997), it was hypothesized that V0 and its relation to the MyHC composition of single extensor digitorum longus (EDL) and soleus muscle fibres from female rats would follow the same pattern as that of their male counterparts.