Different continuous training modalities result in distinctive effects on muscle structure, plasticity and function

Pallone,Gabriele; Palmieri,Mattia; Cariati,Ida; Bei,Roberto; Masuelli,Laura; D'arcangelo,Giovanna; Tancredi,Virginia

doi:10.3892/br.2020.1283

Different continuous training modalities result in distinctive effects on muscle structure, plasticity and function

Authors:
- Gabriele Pallone
- Mattia Palmieri
- Ida Cariati
- Roberto Bei
- Laura Masuelli
- Giovanna D'arcangelo
- Virginia Tancredi
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Affiliations: Department of Systems Medicine, University of Rome Tor Vergata, I‑00133 Rome, Italy, Department of Clinical Sciences and Translational Medicine, University of Rome Tor Vergata, I‑00133 Rome, Italy, Department of Experimental Medicine, Sapienza University of Rome, I‑00161 Rome, Italy
Published online on: February 28, 2020 https://doi.org/10.3892/br.2020.1283
Pages: 267-275

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Abstract

The effects of training on muscle structure are dependent on adaptive changes induced by different intensities of physical exercise. Evidence has shown that aerobic training is able to induce adaptive changes to muscle structure based on intensity. The aim of the present study was to investigate the effects of different methods of continuous aerobic training in mice using functional, morphological and biomolecular approaches. The continuous aerobic training methods used in the present study were uniform continuous training (UC), varying continuous training (VC) and progressive continuous training (PC). Mice were made to run 3 times a week for 12 weeks on a motorized RotaRod, following one of the three different training methods at different speeds. The results of the present study demonstrated that the various training methods had different effects on sarcomere length. Ultrastructural analysis demonstrated that UC training resulted in a shortening of sarcomere length, PC training resulted in an elongation of sarcomere length and VC training showed similar sarcomere length when compared with the control sedentary group. Additionally, succinate dehydrogenase complex flavoprotein subunit A levels in muscle tissue following VC training were higher compared with UC and PC training. Overall, the present study showed that varying exercise methods resulted in different types of muscle plasticity, and that the VC protocol resulted in increased coordination and strength endurance in the functional tests, in agreement with the ultrastructural and biochemical profile. These observations support the view that VC training may be more efficient in increasing performance and may thus form the basis of training regimens when an improvement of motor efficiency is required.

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1	Costill DL, Daniels J, Evans W, Fink W, Krahenbuhl G and Saltin B: Skeletal muscle enzymes and fiber composition in male and female track athletes. J Appl Physiol. 40:149–154. 1976.PubMed/NCBI View Article : Google Scholar
2	Harber M and Trappe S: Single muscle fiber contractile properties of young competitive distance runners. J Appl Physiol (1985). 105:629–636. 2008.PubMed/NCBI View Article : Google Scholar
3	Coyle EF: Integration of the physiological factors determining endurance performance ability. Exerc Sport Sci Rev. 23:25–63. 1995.PubMed/NCBI
4	Hawley JA: Adaptations of skeletal muscle to prolonged, intense endurance training. Clin Exp Pharmacol Physiol. 29:218–222. 2002.PubMed/NCBI View Article : Google Scholar
5	Fitts RH, McDonald KS and Schluter JM: The determinants of skeletal muscle force and power: Their adaptability with changes in activity pattern. J Biomech. 1:111–122. 1991.PubMed/NCBI View Article : Google Scholar
6	Fitts RH and Widrick JJ: Muscle mechanics: Adaptations with exercise-training. Exerc Sport Sci Rev. 24:427–473. 1996.PubMed/NCBI
7	Goldspink G: Malleability of the motor system: A comparative approach. J Exp Biol. 115:375–391. 1985.PubMed/NCBI
8	Hegarty PV and Hooper AC: Sarcomere length and fibre diameter distributions in four different mouse skeletal muscles. J Anat. 110:249–257. 1971.PubMed/NCBI
9	Widrick JJ, Stelzer JE, Shoepe TC and Garner DP: Functional properties of human muscle fibers after short-term resistance exercise training. Am J Physiol Regul Integr Comp Physiol. 283:R408–R416. 2002.PubMed/NCBI View Article : Google Scholar
10	Fitts RH: New insights on sarcoplasmic reticulum calcium regulation in muscle fatigue. J Appl Physiol (1985). 111:345–346. 2011.PubMed/NCBI View Article : Google Scholar
11	Groennebaek T and Vissing K: Impact of resistance training on skeletal muscle mitochondrial biogenesis, content, and function. Front Physiol. 8(713)2017.PubMed/NCBI View Article : Google Scholar
12	Holloszy JO and Coyle EF: Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol Respir Environ Exerc Physiol. 56:831–838. 1984.PubMed/NCBI View Article : Google Scholar
13	Hood DA: Contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol (1985). 90:1137–1157. 2001.PubMed/NCBI View Article : Google Scholar
14	Schantz PG: Plasticity of human skeletal muscle with special reference to effects of physical training on enzyme levels of the NADH shuttles and phenotypic expression of slow and fast myofibrillar proteins. Acta Physiol Scand Suppl. 558:1–62. 1986.PubMed/NCBI
15	Lundberg TR, Fernandez-Gonzalo R, Gustafsson T and Tesch PA: Aerobic exercise does not compromise muscle hypertrophy response to short-term resistance training. J Appl Physiol (1985). 114:81–89. 2013.PubMed/NCBI View Article : Google Scholar
16	Konopka AR and Harber MP: Skeletal muscle hypertrophy after aerobic exercise training. Exerc Sport Sci Rev. 42:53–61. 2014.PubMed/NCBI View Article : Google Scholar
17	Tjønna AE, Lee SJ, Rognmo Ø, Stølen TO, Bye A, Haram PM, Loennechen JP, Al-Share QY, Skogvoll E, Slørdahl SA, et al: Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome: A pilot study. Circulation. 118:346–354. 2008.PubMed/NCBI View Article : Google Scholar
18	Wisløff U, Støylen A, Loennechen JP, Bruvold M, Rognmo Ø, Haram PM, Tjønna AE, Helgerud J, Slørdahl SA, Lee SJ, et al: Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: A randomized study. Circulation. 115:3086–3094. 2007.PubMed/NCBI View Article : Google Scholar
19	Alansare A, Alford K, Lee S, Church T and Jung HC: The effects of high-intensity interval training vs. Moderate-Intensity continuous training on heart rate variability in physically inactive adults. Int J Environ Res Public Health. 15(E1508)2018.PubMed/NCBI View Article : Google Scholar
20	Gaitán JM, Eichner NZM, Gilbertson NM, Heiston EM, Weltman A and Malin SK: Two weeks of interval training enhances fat oxidation during exercise in obese adults with prediabetes. J Sports Sci Med. 18:636–644. 2019.PubMed/NCBI
21	D'Arcangelo G, Triossi T, Buglione A, Melchiorri G and Tancredi V: Modulation of synaptic plasticity by short-term aerobic exercise in adult mice. Behav Brain Res. 332:59–63. 2017.PubMed/NCBI View Article : Google Scholar
22	Louhimies S: Directive 86/609/EEC on the protection of animals used for experimental and other scientific purposes. Altern Lab Anim. 2:217–219. 2002.PubMed/NCBI View Article : Google Scholar
23	D'Arcangelo G, Grossi D, Racaniello M, Cardinale A, Zaratti A, Rufini S, Cutarelli A, Tancredi V, Merlo D and Frank C: Miglustat reverts the impairment of synaptic plasticity in a mouse model of NPC disease. Neural Plast. 2016(3830424)2016.PubMed/NCBI View Article : Google Scholar
24	Masuelli L, Focaccetti C, Cereda V, Lista F, Vitolo D, Trono P, Gallo P, Amici A, Monaci P, Mattei M, et al: Gene-Specific inhibition of breast carcinoma in BALB-neuT mice by active immunization with rat neu or human ErbB receptors. Int J Oncol. 30:381–392. 2007.PubMed/NCBI
25	Ballesta García I, Rubio Arias JÁ, Ramos Campo DJ, Martínez González-Moro I and Carrasco Poyatos M: High-Intensity interval training dosage for heart failure and coronary artery disease cardiac rehabilitation. A systematic review and meta-analysis. Rev Esp Cardiol (Engl Ed). 72:233–243. 2019.PubMed/NCBI View Article : Google Scholar
26	Ballesta-García I, Martínez González-Moro I, Rubio-Arias JÁ and Carrasco-Poyatos M: High-Intensity interval circuit training versus moderate-intensity continuous training on functional ability and body mass index in middle-aged and older women: A randomized controlled trial. Int J Environ Res Public Health. 16(E4205)2019.PubMed/NCBI View Article : Google Scholar
27	Mannella CA: Structural diversity of mitochondria: Functional implications. Ann NY Acad Sci. 1147:171–179. 2008.PubMed/NCBI View Article : Google Scholar
28	Gordon AM, Huxley AF and Julian FJ: The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol. 184:170–192. 1966.PubMed/NCBI View Article : Google Scholar
29	Herzog W and Leonard TR: Force enhancement following stretching of skeletal muscle: A new mechanism. J Exp Biol. 205:1275–1283. 2002.PubMed/NCBI
30	Riis S, Christensen B, Nellemann B, Møller AB, Husted AS, Pedersen SB, Schwartz TW, Jørgensen JOL and Jessen N: Molecular adaptations in human subcutaneous adipose tissue after ten weeks of endurance exercise training in healthy males. J Appl Physiol (1985). 126:569–577. 2019.PubMed/NCBI View Article : Google Scholar
31	Cochran AJ, Percival ME, Tricarico S, Little JP, Cermak N, Gillen JB, Tarnopolsky MA and Gibala MJ: Intermittent and continuous high-intensity exercise training induce similar acute but different chronic muscle adaptations. Exp Physiol. 99:782–791. 2014.PubMed/NCBI View Article : Google Scholar
32	Aisbett B, Condo D, Zacharewicz E and Lamon S: The impact of shiftwork on skeletal muscle health. Nutrients. 9(E248)2017.PubMed/NCBI View Article : Google Scholar
33	Dobbins M, Husson H, DeCorby K and LaRocca RL: School-Based physical activity programs for promoting physical activity and fitness in children and adolescents aged 6 to 18. Cochrane Database Syst Rev. 2(CD007651)2013.PubMed/NCBI View Article : Google Scholar