Age-related changes in metabolic properties of equine skeletal muscle associated with muscle plasticity

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Abstract

The purpose of the present study was to determine the age-related changes in myosin heavy chain (MHC) composition and muscle oxidative and glycolytic capacity in 18 horses ranging in age from two to 30 years. Muscle samples were collected by excisional biopsy of the semimebranosus muscle. MHC expression and the key enzymatic activities were measured.

There was no significant correlation between horse age and the proportions of type-IIA and type-IIX MHC isoforms. The percentage of type-I MHC isoforms decreased with advancing age. Muscle citrate synthase activity decreased, whereas lactate dehydrogenase activity increased with increasing age. Muscle 3-OH acyl CoA dehydrogenase activity did not change with ageing. The results suggest that, similar to humans, the oxidative capacity of equine skeletal muscle decreases with age. The age-related changes in muscle metabolic properties appear to be consistent with an age-related transition in MHC isoforms of equine skeletal muscle that shifts toward more glycolytic isoforms with age.

Introduction

The ageing process typically is responsible for physical impairments such as a reduction in muscle force generating capacity and impaired mobility in mammals. This phenomenon seems to be primarily due to a decrease in the ability of muscle to generate and sustain power output in association with changes in muscular structure and function during ageing (White, 1995; Janssen et al., 2000). A decrease in muscle mass and a loss of motor unit number partially induce the age-related reduction in functional capacity of muscle. The slow (type I) to fast twitch (type II) fibre ratio increases with advancing age. The age-related shift in fibre types appears to be concomitant with a shift in myosin heavy chain (MHC) isoforms with age in horses (Rivero et al., 1997). In humans, the type-I to type-II MHC isoform ratio appears to be greater in aged muscles than in young muscles due to a shift from type-II to type-I MHC isoforms during the ageing process (Welle et al., 2000).

As age increases, the oxidative capacity of human skeletal muscle also declines (Rooyackers et al., 1996; Conley et al., 2000). Evidence of the decreased oxidative capacity is seen in both the rate of mitochondrial protein synthesis and activity of oxidative enzymes such as cytochrome c oxidase and citrate synthase (Rooyackers et al., 1996; Houmard et al., 1998). The reduced oxidative capacity appears to be related to the age-related decrease in aerobic capacity and muscle performance (Houmard et al., 1998; Conley et al., 2000). There is also evidence of diminished glycolytic capacity in aged skeletal muscle (Welle et al., 2000). These age-related adaptations are due to inevitable physiological changes and exacerbated by physical inactivity during the ageing process (Devor and Faulkner, 1999).

Marked ageing process changes in MHC distribution and activity of enzymes indicative of both carbohydrate and fat oxidation in humans and laboratory animals have only been superficially examined in horses (Rivero et al., 1993), and it is not well established whether the changes do occur in the horse, which is naturally athletic species. The majority of previous equine studies in this subject have either focused on trained horses, involve the interaction of training and ageing, or used only horses younger than 10 years of age (Essen et al., 1980; Rivero et al., 1991; Barrey et al., 1999; Roneus and Lindholm, 1991; Roneus, 1993).

Little is known about age-related changes in skeletal muscle characteristics of untrained horses (Rivero et al., 1993). As there is an increase in population of retired and ageing pet horses, it is important to define age-related physiological adaptations in sedentary horses. Therefore, the purpose of the present study was (1) to define the characteristics of muscle of sedentary aged horses, and in particular to characterize the age-related changes in the expression of MHC isoforms and the activity of marker enzymes of energy metabolism and (2) to determine whether that age-related changes in horses would mimic those of humans given the conservation of skeletal muscle structural and function characteristics across a wide range of mammalian species (Charette et al., 1991). Our working hypothesis was that age-related adaptations in the expression of MHC isoforms and marker enzymes of fuel utilization in equine skeletal muscles would be similar to those observed in humans and other mammalian species.

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Animals

In order to define the characteristics of skeletal muscle of ageing horses, 18 horses 2–30 years of age were obtained by either donation to the Veterinary Teaching Hospital, horses from the teaching herd, or in response to a request made to clients of the Equine Ambulatory Service. Upon the approval by the Veterinary Teaching Hospital Executive Committee and the Institutional Laboratory Animal Care and Use Committee (ILACUC) at The Ohio State University, an informed consent was provided to all

Myosin heavy chain composition and total protein concentrations

There was no association between age and muscle protein concentration (Fig. 1). MHC composition was not significantly altered with increasing age from two to 30 years in 18 horses (Fig. 2, Fig. 3, Fig. 4). There was no statistically significant correlation between horse age and the percentages (%) of all these MHC isoforms including type-I, type-IIA, and type-IIX (P=0.07; r=−0.36, 0.2, and −0.03, respectively, n=18). However, visual examination of a scatterplot of the MHC-I data suggested the

Discussion

The results of the present study indicate that the percent of type-I MHC isoforms decreased with advancing horse age. In addition, with increasing age, the activity of muscle CS decreased, whereas the activity of LDH increased. The present findings suggest that age-related changes in equine skeletal muscle may differ from those in humans, particularly the known age-related changes in human type-I MHC isoforms and LDH activity. However, similar to humans, the oxidative capacity (as measured by

Acknowledgements

The authors thank William J. Fink at Ball State University for providing detailed enzymatic analysis protocols and Dr. Marcas M. Bamman at the University of Alabama at Birmingham for support of data presentation at the 2003 FASEB annual meeting. This study was supported by the equine research fund from the College of Veterinary Medicine, Council for Research, at The Ohio State University.

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