Resistance training of long duration modulates force and unloaded shortening velocity of single muscle fibres of young women

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Abstract

The aim of the present study was to clarify the impact of long term (1 year) resistance training (RT) on structure and function of single muscle fibres of vastus lateralis in young female subjects. Five young women (age: 25.4 ± 6.2 year) performed exercise sessions at 60% of single subject own repetition maximum (1 RM) 1 h twice a week. Maximum voluntary force was determined pre- and post-RT and was found to significantly increase post-RT ensuring a successful impact of RT on muscle performance in vivo. Needle muscle biopsy samples were obtained both pre- and post-RT and the following determinations were performed: myosin heavy chain isoform (MHC) distribution of the whole muscle samples by SDS–PAGE; cross sectional area (CSA), specific force (Po/CSA) and maximum shortening velocity (Vo) of a large population (n = 358) of single skinned muscle fibres classified on the basis of MHC isoform composition by SDS–PAGE. The results suggest that the long duration of RT can determine a significant increase in specific force (Po/CSA) and unloaded shortening velocity (Vo) of single muscle fibres in female subjects, whereas no muscle fibre hypertrophy and no shift in MHC isoform content was observed.

Introduction

Skeletal muscle structure and function can be affected by a variety of stimuli among which exercise training is one of the most important (Fluck and Hoppeler, 2003). It is generally accepted that skeletal muscle can adapt to resistance training (RT) by both a quantitative mechanism, based on changes in muscle mass and fibre size, and a qualitative mechanism, based on changes in fibre type distribution (Schiaffino and Reggiani, 1996, Bottinelli and Reggiani, 2000, Fluck and Hoppeler, 2003). Human skeletal muscles are, in fact, mixed muscles expressing three main fibre types, namely type 1, 2A and 2X, in variable proportions (Harridge et al., 1996). The latter fibre types are known to have distinctive contractile properties depending on which of the three adult myosin heavy chain (MHC) isoforms they express: MHC-1 (slow), MHC-2A (intermediate) and MHC-2X (fast) (Bottinelli and Reggiani, 2000). There is general consensus that resistance training can determine hypertrophy of single muscle fibres (Schiaffino and Reggiani, 1996, Hortobagyi et al., 2000, Fluck and Hoppeler, 2003, D’Antona et al., 2006) and an increase in the expression of the MHC-2A isoform coupled to a decrease in the expression of MHC-2X (Bottinelli and Reggiani, 2000, Fluck and Hoppeler, 2003, Liu et al., 2003b). However, it has been noted that the above mechanisms might not account for the whole phenomenon of muscle plasticity (Bottinelli, 2001).

Several evidences have suggested that muscle fibres can change their force and shortening velocity independently from a change in size (quantitative mechanism) or in MHC content (qualitative mechanism) (Bottinelli, 2001). In this respect, the first and clearer evidences have been reported in elderly subjects whose muscle fibres showed lower specific force (Po/CSA) and maximum shortening velocity (Vo) than corresponding fibre types of young subjects (Larsson et al., 1997, D’Antona et al., 2003) although contradictory results have been reported (Trappe et al., 2003).

Much less clear is whether muscle fibres can go through changes in Po/CSA and Vo with no change in their MHC isoform content following training, and especially resistance training. No change in Po/CSA and Vo of muscle fibres was observed both in a 12-wk longitudinal study on resistance trained young male subjects (Widrick et al., 2002) and in a cross sectional study comparing sedentary and resistance trained young males (Shoepe et al., 2003). However, very clear changes in Po/CSA were observed in a cross-sectional study on body builders that had been very heavily resistance trained for at least two years (D’Antona et al., 2006) suggesting that the contradictory results might depend on the rather short duration of RT training (12 weeks) of longitudinal studies so far. Moreover, in elderly subjects, Po/CSA and Vo were found to increase following training in males (Trappe et al., 2000b), but not in females (Trappe et al., 2001) suggesting that the impact of training on muscle fibre properties could depend on gender.

The aim of the present study was to clarify the impact of resistance training (RT) on structure and function of single muscle fibres. A very long-term (one year) RT was used to ensure that training duration was not a hindering factor for potential changes in force and velocity of single muscle fibres. Moreover, female subjects were studied to clarify whether the response of force and velocity of single muscle fibres to training could also be observed in females. The results show that prolonged RT can have a clear impact on force and velocity of muscle fibres and that this can occur also in female subjects.

Section snippets

Methods

Five young women were enrolled in the study and subjected to resistance training (RT) for one year. Muscle force was determined in vivo. Structure and function of muscle fibres was determined in vitro using muscle samples obtained by needle biopsy of the vastus lateralis muscle pre- and post-RT.

Muscle force in vivo

Fig. 2 reports the mean values of the maximum voluntary force of the knee extensors for the right and left leg at 90° joint angle pre- and post training for the 5 subjects studied. Statistical analysis (one tailed paired T-test) indicated that force was significantly higher following training both in the right (P = 0.017) and in the left (P = 0.008) leg. The increase was ∼14% and ∼25% for the right and left leg respectively. The increase was statistically significant also at all other joint angles

Discussion

The present work was prompted by the contradictory results obtained studying the effect of resistance training on force and velocity of skeletal muscle fibres. In body builders, that had been very heavily training for at least two years, changes in specific force of muscle fibres were very evident (D’Antona et al., 2006) whereas no change was observed following RT of shorter (12-wk) duration (Widrick et al., 2002). Based on the latter observations, one year RT was used to ensure that duration

Conclusions

The present work indicates that RT can modulate both force and unloaded shortening velocity of muscle fibres independently from a change in size (quantitative mechanism) and in myosin isoform content (qualitative mechanism) and suggests that some of the inconsistencies previously observed in this respect can be due to the duration of training. Moreover, our study on female subjects indicates that gender does not prevent RT adaptations at single muscle fibre level, at least when the duration of

Acknowledgments

This work was supported by the European Union contract Better-Ageing (QLK6-CT2001-00323) and by an Italian Space Agency contract (OSMA).

Orietta Pansarasa received her degree in Biological Sciences from the University of Pavia, Italy, in 1996 and her Ph.D. degree in Neurobiology from the University of Catania, Italy, in 2001. After graduating, she worked as a Post Doc at the Department of Physiological and Pharmacological Cellular-Molecular Sciences, Pharmacology and Pharmacological Biotechnologies Unit, University of Pavia (2001–2003). She studied the role of reactive oxygen species during aging of central nervous system in

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  • Cited by (0)

    Orietta Pansarasa received her degree in Biological Sciences from the University of Pavia, Italy, in 1996 and her Ph.D. degree in Neurobiology from the University of Catania, Italy, in 2001. After graduating, she worked as a Post Doc at the Department of Physiological and Pharmacological Cellular-Molecular Sciences, Pharmacology and Pharmacological Biotechnologies Unit, University of Pavia (2001–2003). She studied the role of reactive oxygen species during aging of central nervous system in rats and of muscular system in human. She also studied the effects of neuromuscular aging and of hypothalamic-pituitary-gonadal axis alterations on the main antioxidant defence systems. Since 2003 she works as a Post Doc at the Department of Experimental Medicine, Human Physiology Unit, University of Pavia. She studied different aspects of skeletal muscle physiology. Her interest is particularly focussed on the adaptations of functional and biochemical parameters of muscular system during aging, physical training and muscular dystrophy (evaluation of the efficacy of new genetic and cellular therapies). At the moment she is applying the proteomic approach to the analysis of skeletal muscle adapatations.

    Chiara Rinaldi received her B.S. degree in 2003 and her Ph.D. degree in Physiology and Neurosciences in 2008 from the University of Pavia, Italy. She spent the year before graduating (2007) at the University of California, Irvine, USA, to expand her insight in molecular biology aspects. Her researches were maily focus on plasticity and functionality of muscular tissue in both health and disease conditions, in particular during exercise training and muscular dystrophy. Since July 2008 she has a postdoc position at the University of California, Los Angeles, USA, where she is studying the immunological mechanisms underlying the sarcopenic muscle condition.

    Valeria Parente received her degree in Biological Sciences from University of Insubria, Varese (Italy) in 1999 and her PhD in Physiology from the University of Pavia (Italy) in 2002. After graduating, in 2000, she was abroad for collaboration with MRC Toxicology Unit at University of Leicester (UK). She was a post doc in the Laboratory of Human Physiology, Department of Experimental Medicine at University of Pavia. Now she is postdoctoral researcher in the Laboratory of Vascular Biology and Gene Therapy at Centro Cardiologico Monzino, Milan. Her research interests are focused on skeletal muscle adapations, on stem cell research, stem cell and gene therapy, and on regeneration of skeletal and cardiac muscle.

    Danilo Miotti received his MD degree from the University of Pavia, Italy, in 1988, Specialization in Anaesthesia and Intensive Care from the University of Pavia, Italy, in 1992, Post Graduate Diploma in Thermography from Billerica, Massachussets (USA) in 1992, Post Graduate Diploma in Algological Science from ISAL (Algological Science Italian Institute) in 1994, Specialization in Physiopathology and Pain Therapy from University of Verona in 2001. He is director of Palliative Care and Pain Therapy Operative Unit at Salvatore Maugeri Foundation IRCCS of Pavia. He devoted most of his clinical and research activity in cancer pain, CRPS (Complex Regional Pain Syndrome), neuropathic pain, low back pain, quality of life, Spinal cord stimulation and intrathecal pain therapy.

    Paolo Capodaglio received his M.D. degree from the University of Pavia, Italy, in 1988 and his specialization in Physical Medicine and Rehabilitation (PMR) from the same University in 1991. After graduating, he started working as a PMR specialist in an Institute for clinical care and research (Fondazione Maugeri IRCCS) with clinical and research interests. He was abroad for long and short visits (1992 University of Dusseldorf, 1995-1996 National Institute of Occupational Health, Copenhagen, Danemark) and thereafter developed collaborations with several foreign laboratories. At present, he is Head of the PMR Unit and the Laboratory for Research in Biomechanics and Rehabilitation at the Istituto Auxologico Italiano IRCCS in Verbania-Piancavallo, Italy and contract professor of PMR in the Medical School of the University of Brescia, Italy. He devoted most of his research to the functional evaluation in ageing and pathological conditions (spinal cord injuries, musculoskeletal disorders, obesity) and is reviewer for several indexed papers.

    Roberto Bottinelli received his M.D. degree from the University of Pavia, Italy, in 1981 and his Ph.D. degree in Physiology from the same University in 1989. Shortly after graduating, he was abroad for two long visits (1982–1983 University of Washington, Seattle, USA and 1986–1987 University of St. Andrews, Scotland) and thereafter developed collaborations with several foreign laboratories. He is full professor of Physiology in the Medical School of the University of Pavia. He devoted most of his research to muscle physiology and in particular to the cellular and molecular mechanisms underlying the very large structural and functional heterogeneity and plasticity of skeletal muscle in health (ageing, disuse, exercise training) and disease (muscular dystrophy and respiratory diseases). Since 2000 he has been responsible of the laboratory of Muscle Biophysics of the Department of Experimental Medicine of the University of Pavia. He is in the editorial board of the Journal of Physiology (London) and of the European Journal of Applied Physiology. He is the director of the Specialization School in Sport Medicine of the Faculty and the Head of the Department of Experimental Medicine of the University of Pavia.

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