Effect of speed endurance training and reduced training volume on running economy and single muscle fiber adaptations in trained runners

Casper Skovgaard, Danny Christiansen, Peter M Christensen, Nicki W Almquist, Martin Thomassen, Jens Bangsbo, Casper Skovgaard, Danny Christiansen, Peter M Christensen, Nicki W Almquist, Martin Thomassen, Jens Bangsbo

Abstract

The aim of the present study was to examine whether improved running economy with a period of speed endurance training and reduced training volume could be related to adaptations in specific muscle fibers. Twenty trained male (n = 14) and female (n = 6) runners (maximum oxygen consumption (VO2 -max): 56.4 ± 4.6 mL/min/kg) completed a 40-day intervention with 10 sessions of speed endurance training (5-10 × 30-sec maximal running) and a reduced (36%) volume of training. Before and after the intervention, a muscle biopsy was obtained at rest, and an incremental running test to exhaustion was performed. In addition, running at 60% vVO2 -max, and a 10-km run was performed in a normal and a muscle slow twitch (ST) glycogen-depleted condition. After compared to before the intervention, expression of mitochondrial uncoupling protein 3 (UCP3) was lower (P < 0.05) and dystrophin was higher (P < 0.05) in ST muscle fibers, and sarcoplasmic reticulum calcium ATPase 1 (SERCA1) was lower (P < 0.05) in fast twitch muscle fibers. Running economy at 60% vVO2 -max (11.6 ± 0.2 km/h) and at v10-km (13.7 ± 0.3 km/h) was ~2% better (P < 0.05) after the intervention in the normal condition, but unchanged in the ST glycogen-depleted condition. Ten kilometer performance was improved (P < 0.01) by 3.2% (43.7 ± 1.0 vs. 45.2 ± 1.2 min) and 3.9% (45.8 ± 1.2 vs. 47.7 ± 1.3 min) in the normal and the ST glycogen-depleted condition, respectively. VO2 -max was the same, but vVO2 -max was 2.0% higher (P < 0.05; 19.3 ± 0.3 vs. 18.9 ± 0.3 km/h) after than before the intervention. Thus, improved running economy with intense training may be related to changes in expression of proteins linked to energy consuming processes in primarily ST muscle fibers.

Keywords: Intense training; muscle fiber type-specific adaptations; muscular adaptations; sprint interval training.

© 2018 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of The Physiological Society and the American Physiological Society.

Figures

Figure 1
Figure 1
Testing before (Pre) and after (Post) 5 blocks/40 days of speed endurance training and reduced training volume in trained runners. Small grey, black and white boxes on the timeline are days with aerobic moderate‐intensity training, speed endurance training and rest days, respectively. INC: incremental test to exhaustion.
Figure 2
Figure 2
Oxygen uptake (A) and running economy (B) at v10‐km before (Pre) and after (Post) 5 blocks/40 days of speed endurance training and reduced training volume in trained runners. Values are means ± SE. ***Post different (P < 0.001) to Pre.
Figure 3
Figure 3
Oxygen uptake (A) and running economy (B) at 60% VO2‐max in depleted and normal conditions before (Pre) and after (Post) 5 blocks/40 days of speed endurance training and reduced training volume in trained runners. Values are means ± SE. *Post different (P < 0.05) to Pre; #difference (P < 0.05) within time‐point.
Figure 4
Figure 4
Protein expression of actin; UCP3, mitochondrial uncoupling protein 3; SERCA1 and 2, sarcoplasmic reticulum calcium ATPase, before (Pre) and after (Post) 5 blocks/40 days of speed endurance training and reduced training volume in trained runners. Values are geometric means ± 95% confidence interval (CI) (Post relative to Pre). *Post different (P < 0.05) from Pre.
Figure 5
Figure 5
ST (A) and FTa (B) single muscle fiber expression of MHCI and II, myosin heavy chain; SERCA1 and 2, sarcoplasmic reticulum calcium ATPase; CS, citrate synthase; UCP3, mitochondrial uncoupling protein 3; and dystrophin, before (Pre) and after (Post) 5 blocks/40 days of speed endurance training and reduced training volume in trained runners. Values are means ± SE (relative to Pre). *Post different (P < 0.05) from Pre.
Figure 6
Figure 6
Time to complete a 10‐km run in depleted and normal conditions before (Pre) and after (Post) 5 blocks/40 days of speed endurance training and reduced training volume in trained runners. Values are means ± SE. **Post different (P < 0.01) to Pre; ###difference (P < 0.001) within time‐point.

References

    1. Bangsbo, J. 2015. Performance in sports ‐ with specific emphasis on the effect of intensified training. Scand. J. Med. Sci. Sport 25:88–99.
    1. Bangsbo, J. , Gunnarsson T. P., Wendell J., Nybo L., and Thomassen M.. 2009. Reduced volume and increased training intensity elevate muscle Na+‐K+ pump 2‐subunit expression as well as short‐ and long‐term work capacity in humans. J. Appl. Physiol. 107:1771–1780.
    1. Barclay, C. J. , Constable J. K., and Gibbs C. L.. 1993. Energetics of fast‐ and slow‐twitch muscles of the mouse. J. Physiol. 472:61–80.
    1. Berchtold, M. W. , Brinkmeier H., and Müntener M.. 2000. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 80:1215–1265.
    1. Bergstrom, J. 1962. Muscle electrolytes in man. Scand. J. Clin. Lab. Investig. 68:1–110.
    1. Bickham, D. C. , Bentley D. J., Le Rossignol P. F., and Cameron‐Smith D.. 2006. The effects of short‐term sprint training on MCT expression in moderately endurance‐trained runners. Eur. J. Appl. Physiol. 96:636–643.
    1. Boss, O. , Hagen T., and Lowell B. B.. 2000. Uncoupling proteins 2 and 3: potential regulators of mitochondrial energy metabolism. Diabetes 49:143–156.
    1. Chopard, A. , Arrighi N., Carnino A., and Marini J. F.. 2005. Changes in dysferlin, proteins from dystrophin glycoprotein complex, costameres, and cytoskeleton in human soleus and vastus lateralis muscles after a long‐term bedrest with or without exercise. FASEB J. 19:1722–1724.
    1. Christensen, P. M. , Gunnarsson T. P., Thomassen M., Wilkerson D. P., Nielsen J. J., and Bangsbo J.. 2015. Unchanged content of oxidative enzymes in fast‐twitch muscle fibers and kinetics after intensified training in trained cyclists. Physiol. Rep. 3:e12428.
    1. Clausen, T. , Van Hardeveld C., Everts M. E., Van H. C., and Everts M. E.. 1991. Significance of cation transport in control of energy metabolism and thermogenesis. Physiol. Rev. 71:733–774.
    1. Crow, M. T. , and Kushmerick M. J.. 1982. Chemical energetics of slow‐ and fast‐twitch muscles of the mouse. J. Gen. Physiol. 79:147–166.
    1. Delbono, O. , and Meissner G.. 1996. Sarcoplasmic reticulum Ca2+ release in rat slow‐ and fast‐twitch muscles. J. Membr. Biol. 151:123–130.
    1. Egan, B. , and Zierath J. R.. 2013. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 17:162–184.
    1. Egan, B. , Carson B. P., Garcia‐Roves P. M., Chibalin A. V., Sarsfield F. M., Barron N., et al. 2010. Exercise intensity‐dependent regulation of peroxisome proliferator‐activated receptor coactivator‐1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J. Physiol. 588:1779–1790.
    1. Froemming, G. R. , Murray B. E., Harmon S., Pette D., and Ohlendieck K.. 2000. Comparative analysis of the isoform expression pattern of Ca2+‐regulatory membrane proteins in fast‐twitch, slow‐twitch, cardiac, neonatal and chronic low‐frequency stimulated muscle fibers. Biochim. Biophys. Acta – Biomembr. 1466:151–168.
    1. Gollnick, P. D. , Piehl K., and Saltin B.. 1974. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J. Physiol. 241:45–57.
    1. Gong, D. W. , He Y., Karas M., and Reitman M.. 1997. Uncoupling protein‐3 is a mediator of thermogenesis regulated by thyroid hormone, b3‐adrenergic agonists, and leptin. J. Biol. Chem. 272:24129–24132.
    1. Green, H. J. , Burnett M., Kollias H., Ouyang J., Smith I., and Tupling S.. 2011. Malleability of human skeletal muscle sarcoplasmic reticulum to short‐term training. Appl. Physiol. Nutr. Metab. 36:904–912.
    1. Gunnarsson, T. P. , Christensen P. M., Holse K., Christiansen D., and Bangsbo J.. 2012. Effect of additional speed endurance training on performance and muscle adaptations. Med. Sci. Sports Exerc. 44:1942–1948.
    1. He, Z. H. , Bottinelli R., Pellegrino M. A., Ferenczi M. A., and Reggiani C.. 2000. ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys. J . 79:945–961.
    1. Howley, E. T. , Bassett D. R., and Welch H. G.. 1995. Criteria for maximal oxygen uptake: review and commentary. Med. Sci. Sports Exerc. 27:1292–1301.
    1. Hughes, D. C. , Wallace M. A., and Baar K.. 2015. Effects of aging, exercise, and disease on force transfer in skeletal muscle. Am. J. Physiol. – Endocrinol. Metab. 309:E1–E10.
    1. Iaia, F. M. , and Bangsbo J.. 2010. Speed endurance training is a powerful stimulus for physiological adaptations and performance improvements of athletes. Scand. J. Med. Sci. Sport 20:11–23.
    1. Iaia, F. M. , Thomassen M., Kolding H., Gunnarsson T., Wendell J., Rostgaard T., et al. 2008. Reduced volume but increased training intensity elevates muscle Na+‐K+ pump alpha1‐subunit and NHE1 expression as well as short‐term work capacity in humans. J. Appl. Physiol. 106:73–80.
    1. Iaia, F. M. , Hellsten Y., Nielsen J. J., Fernstrom M., Sahlin K., Bangsbo J., et al. 2009. Four weeks of speed endurance training reduces energy expenditure during exercise and maintains muscle oxidative capacity despite a reduction in training volume. J. Appl. Physiol. 106:73–80.
    1. Jansson, E. , and Kaijser L.. 1977. Muscle adaptation to extreme endurance training in man. Acta Physiol. Scand. 100:315–324.
    1. Joyner, M. J. , and Coyle E. F.. 2008. Endurance exercise performance: the physiology of champions. J. Physiol. 586:35–44.
    1. Krustrup, P. , Soderlund K., Mohr M., and Bangsbo J.. 2004. Slow‐twitch fiber glycogen depletion elevates moderate‐exercise fast‐twitch fiber activity and O2 uptake. Med. Sci. Sports Exerc. 36:973–982.
    1. Krustrup, P. , Secher N. H., Relu M. U., Hellsten Y., Soderlund K., and Bangsbo J.. 2008. Neuromuscular blockade of slow twitch muscle fibres elevates muscle oxygen uptake and energy turnover during submaximal exercise in humans. J. Physiol. 586:6037–6048.
    1. Lowry, O. H. , and Passonneau J. V.. 1972. A flexible system of enzymatic analysis. P. 237 Academic, New York.
    1. Majerczak, J. , Karasinski J., and Zoladz J. A.. 2008. Training induced decrease in oxygen cost of cycling is accompanied by down‐regulation of serca expression in human vastus lateralis muscle. J. Physiol. Pharmacol. 59:589–602.
    1. Majerczak, J. , Korostynski M., Nieckarz Z., Szkutnik Z., Duda K., and Zoladz J. A.. 2012. Endurance training decreases the non‐linearity in the oxygen uptake‐power output relationship in humans. Exp. Physiol. 97:386–399.
    1. Mogensen, M. , Bagger M., Pedersen P. K., Fernström M., and Sahlin K.. 2006. Cycling efficiency in humans is related to low UCP3 content and to type I fibres but not to mitochondrial efficiency. J. Physiol. 571:669–681.
    1. Murphy, R. M. 2011. Enhanced technique to measure proteins in single segments of human skeletal muscle fibers: fiber‐type dependence of AMPK‐α1 and ‐β1. J Appl Physiol. 110:820–825.
    1. Nordsborg, N. B. , Lundby C., Leick L., and Pilegaard H.. 2010. Relative workload determines exercise‐induced increases in PGC‐1α mRNA. Med. Sci. Sports Exerc. 42:1477–1484.
    1. Prins, K. W. , Humston J. L., Mehta A., Tate V., Ralston E., and Ervasti J. M.. 2009. Dystrophin is a microtubule‐associated protein. J. Cell Biol. 186:363–369.
    1. Russell, A. P. , Somm E., Praz M., Crettenand A., Hartley O., Melotti A., et al. 2003a. UCP3 protein regulation in human skeletal muscle fibre types I, IIa and IIx is dependent on exercise intensity. J. Physiol. 550:855–861.
    1. Russell, A. P. , Wadley G., Hesselink M. K. C., Schaart G., Lo S., Léger B., et al. 2003b. UCP3 protein expression is lower in type I, IIa and IIx muscle fiber types of endurance‐trained compared to untrained subjects. Pflugers Arch. Eur. J. Physiol. 445:563–569.
    1. Rybakova, I. N. , Patel J. R., and Ervasti J. M.. 2000. The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J. Cell Biol. 150:1209–1214.
    1. Saunders, P. U. , Pyne D. B., Telford R. D., and Hawley J. A.. 2004. Factors affecting running economy in trained distance runners. Sport Med. 34:465–485.
    1. Schiaffino, S. , and Reggiani C.. 2011. Fiber types in mammalian skeletal muscles. Physiol. Rev. 91:1447–1531.
    1. Skovgaard, C. , Christensen P. M., Larsen S., Andersen T., Thomassen M., and Bangsbo J.. 2014. Concurrent speed endurance and resistance training improves performance, running economy, and muscle NHE1 in moderately trained runners. J. Appl. Physiol. 117:1097–1109.
    1. Skovgaard, C. , Brandt N., Pilegaard H., and Bangsbo J.. 2016. Combined speed endurance and endurance exercise amplify the exercise‐induced PGC‐1α and PDK4 mRNA response in trained human muscle. Physiol. Rep. 4:e12864.
    1. Smith, I. C. , Bombardier E., Vigna C., and Tupling A. R.. 2013. ATP consumption by sarcoplasmic reticulum Ca2+ pumps accounts for 40–50% of resting metabolic rate in mouse fast and slow twitch skeletal muscle. PLoS ONE 8:1–11.
    1. Vøllestad, N. K. , and Blom P. C.. 1985. Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiol. Scand. 125:395–405.
    1. Walsh, B. , Howlett R. A., Stary C. M., Kindig C. A., and Hogan M. C.. 2006. Measurement of activation energy and oxidative phosphorylation onset kinetics in isolated muscle fibers in the absence of cross‐bridge cycling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290:R1707–R1713.

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