Serum Metabolites Associated with Muscle Hypertrophy after 8 Weeks of High- and Low-Load Resistance Training
Abstract
:1. Introduction
2. Material and Methods
2.1. Participants
2.2. Experimental Design
2.3. Nutritional Habits
2.4. Maximum Dynamic Strength
2.5. Training Protocol
2.6. Muscle Activation
2.7. Muscle Thickness
2.8. Blood Sampling
2.9. Sample Preparation for Metabolomics Analysis
2.10. Data Acquisition by NMR and Quantification
2.11. Statistical Analysis
2.11.1. Muscle Thickness, Muscle Activation, and Total Energy Intake of Macronutrients
2.11.2. Metabolic Response
3. Results
3.1. Nutritional Habits
3.2. Maximal Dynamic Strength
3.3. Muscle Activation
3.4. Muscle Hypertrophy
3.5. Metabolic Response
4. Discussion
5. Conclusions
6. Limitations
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Grgic, J.; Schoenfeld, B.J.; Orazem, J.; Sabol, F. Effects of resistance training performed to repetition failure or non-failure on muscular strength and hypertrophy: A systematic review and meta-analysis. J. Sport Health Sci. 2022, 11, 202–211. [Google Scholar] [CrossRef]
- Thiele, D.; Prieske, O.; Chaabene, H.; Granacher, U. Effects of strength training on physical fitness and sport-specific performance in recreational, sub-elite, and elite rowers: A systematic review with meta-analysis. J. Sports Sci. 2020, 38, 1186–1195. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Acosta-Manzano, P.; Rodriguez-Ayllon, M.; Acosta, F.M.; Niederseer, D.; Niebauer, J. Beyond general resistance training. Hypertrophy versus muscular endurance training as therapeutic interventions in adults with type 2 diabetes mellitus: A systematic review and meta-analysis. Obes. Rev. 2020, 21, e13007. [Google Scholar] [CrossRef]
- Delgado-Floody, P.; Alvarez, C.; Lusa Cadore, E.; Flores-Opazo, M.; Caamano-Navarrete, F.; Izquierdo, M. Preventing metabolic syndrome in morbid obesity with resistance training: Reporting interindividual variability. Nutr. Metab. Cardiovasc. Dis. 2019, 29, 1368–1381. [Google Scholar] [CrossRef]
- American College of Sports, M. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med. Sci. Sports Exerc. 2009, 41, 687–708. [Google Scholar] [CrossRef]
- Kraemer, W.J.; Adams, K.; Cafarelli, E.; Dudley, G.A.; Dooly, C.; Feigenbaum, M.S.; Fleck, S.J.; Franklin, B.; Fry, A.C.; Hoffman, J.R.; et al. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med. Sci. Sports Exerc. 2002, 34, 364–380. [Google Scholar] [CrossRef]
- Csapo, R.; Alegre, L.M. Effects of resistance training with moderate vs heavy loads on muscle mass and strength in the elderly: A meta-analysis. Scand. J. Med. Sci. Sports 2016, 26, 995–1006. [Google Scholar] [CrossRef]
- Jenkins, N.D.M.; Miramonti, A.A.; Hill, E.C.; Smith, C.M.; Cochrane-Snyman, K.C.; Housh, T.J.; Cramer, J.T. Greater Neural Adaptations following High- vs. Low-Load Resistance Training. Front. Physiol. 2017, 8, 331. [Google Scholar] [CrossRef] [PubMed]
- Nuzzo, J.L. Narrative Review of Sex Differences in Muscle Strength, Endurance, Activation, Size, Fiber Type, and Strength Training Participation Rates, Preferences, Motivations, Injuries, and Neuromuscular Adaptations. J. Strength Cond. Res. 2022, 00, 1–43. [Google Scholar] [CrossRef]
- Jenkins, N.D.; Housh, T.J.; Buckner, S.L.; Bergstrom, H.C.; Cochrane, K.C.; Hill, E.C.; Smith, C.M.; Schmidt, R.J.; Johnson, G.O.; Cramer, J.T. Neuromuscular Adaptations After 2 and 4 Weeks of 80% Versus 30% 1 Repetition Maximum Resistance Training to Failure. J. Strength Cond. Res. 2016, 30, 2174–2185. [Google Scholar] [CrossRef]
- Mitchell, C.J.; Churchward-Venne, T.A.; West, D.W.; Burd, N.A.; Breen, L.; Baker, S.K.; Phillips, S.M. Resistance exercise load does not determine training-mediated hypertrophic gains in young men. J. Appl. Physiol. (1985) 2012, 113, 71–77. [Google Scholar] [CrossRef] [Green Version]
- Nobrega, S.R.; Ugrinowitsch, C.; Pintanel, L.; Barcelos, C.; Libardi, C.A. Effect of Resistance Training to Muscle Failure vs. Volitional Interruption at High- and Low-Intensities on Muscle Mass and Strength. J. Strength Cond. Res. 2018, 32, 162–169. [Google Scholar] [CrossRef] [PubMed]
- Jenkins, N.D.; Housh, T.J.; Bergstrom, H.C.; Cochrane, K.C.; Hill, E.C.; Smith, C.M.; Johnson, G.O.; Schmidt, R.J.; Cramer, J.T. Muscle activation during three sets to failure at 80 vs. 30% 1RM resistance exercise. Eur. J. Appl. Physiol. 2015, 115, 2335–2347. [Google Scholar] [CrossRef] [PubMed]
- Schoenfeld, B.J.; Contreras, B.; Willardson, J.M.; Fontana, F.; Tiryaki-Sonmez, G. Muscle activation during low- versus high-load resistance training in well-trained men. Eur. J. Appl. Physiol. 2014, 114, 2491–2497. [Google Scholar] [CrossRef]
- Burd, N.A.; Mitchell, C.J.; Churchward-Venne, T.A.; Phillips, S.M. Bigger weights may not beget bigger muscles: Evidence from acute muscle protein synthetic responses after resistance exercise. Appl. Physiol. Nutr. Metab. 2012, 37, 551–554. [Google Scholar] [CrossRef] [PubMed]
- Ozaki, H.; Loenneke, J.P.; Buckner, S.L.; Abe, T. Muscle growth across a variety of exercise modalities and intensities: Contributions of mechanical and metabolic stimuli. Med. Hypotheses 2016, 88, 22–26. [Google Scholar] [CrossRef]
- Nalbandian, M.; Takeda, M. Lactate as a Signaling Molecule That Regulates Exercise-Induced Adaptations. Biology 2016, 5, 38. [Google Scholar] [CrossRef] [Green Version]
- Shad, B.J.; Smeuninx, B.; Atherton, P.J.; Breen, L. The mechanistic and ergogenic effects of phosphatidic acid in skeletal muscle. Appl. Physiol. Nutr. Metab. 2015, 40, 1233–1241. [Google Scholar] [CrossRef] [Green Version]
- Wackerhage, H.; Schoenfeld, B.J.; Hamilton, D.L.; Lehti, M.; Hulmi, J.J. Stimuli and sensors that initiate skeletal muscle hypertrophy following resistance exercise. J. Appl. Physiol. (1985) 2019, 126, 30–43. [Google Scholar] [CrossRef]
- Morville, T.; Sahl, R.E.; Moritz, T.; Helge, J.W.; Clemmensen, C. Plasma Metabolome Profiling of Resistance Exercise and Endurance Exercise in Humans. Cell Rep. 2020, 33, 108554. [Google Scholar] [CrossRef]
- Gehlert, S.; Weinisch, P.; Romisch-Margl, W.; Jaspers, R.T.; Artati, A.; Adamski, J.; Dyar, K.A.; Aussieker, T.; Jacko, D.; Bloch, W.; et al. Effects of Acute and Chronic Resistance Exercise on the Skeletal Muscle Metabolome. Metabolites 2022, 12, 445. [Google Scholar] [CrossRef]
- Suga, T.; Okita, K.; Morita, N.; Yokota, T.; Hirabayashi, K.; Horiuchi, M.; Takada, S.; Takahashi, T.; Omokawa, M.; Kinugawa, S.; et al. Intramuscular metabolism during low-intensity resistance exercise with blood flow restriction. J. Appl. Physiol. (1985) 2009, 106, 1119–1124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suga, T.; Okita, K.; Takada, S.; Omokawa, M.; Kadoguchi, T.; Yokota, T.; Hirabayashi, K.; Takahashi, M.; Morita, N.; Horiuchi, M.; et al. Effect of multiple set on intramuscular metabolic stress during low-intensity resistance exercise with blood flow restriction. Eur. J. Appl. Physiol. 2012, 112, 3915–3920. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Valerio, D.F.; Berton, R.; Conceicao, M.S.; Canevarolo, R.R.; Chacon-Mikahil, M.P.T.; Cavaglieri, C.R.; Meirelles, G.V.; Zeri, A.C.; Libardi, C.A. Early metabolic response after resistance exercise with blood flow restriction in well-trained men: A metabolomics approach. Appl. Physiol. Nutr. Metab. 2018, 43, 240–246. [Google Scholar] [CrossRef] [Green Version]
- Berton, R.; Conceicao, M.S.; Libardi, C.A.; Canevarolo, R.R.; Gaspari, A.F.; Chacon-Mikahil, M.P.; Zeri, A.C.; Cavaglieri, C.R. Metabolic time-course response after resistance exercise: A metabolomics approach. J. Sports Sci. 2017, 35, 1211–1218. [Google Scholar] [CrossRef]
- Fiehn, O.; Kopka, J.; Dormann, P.; Altmann, T.; Trethewey, R.N.; Willmitzer, L. Metabolite profiling for plant functional genomics. Nat. Biotechnol. 2000, 18, 1157–1161. [Google Scholar] [CrossRef]
- Brown, L.E.; Weir, J. ASEP Procedures recommendation I: Accurate assessment of muscular strength and power. J. Exerc. Physiol. Online 2001, 4, 1–21. [Google Scholar]
- Schoenfeld, B.J.; Peterson, M.D.; Ogborn, D.; Contreras, B.; Sonmez, G.T. Effects of Low- vs. High-Load Resistance Training on Muscle Strength and Hypertrophy in Well-Trained Men. J. Strength Cond. Res. 2015, 29, 2954–2963. [Google Scholar] [CrossRef] [Green Version]
- Ren, S.; Hinzman, A.A.; Kang, E.L.; Szczesniak, R.D.; Lu, L.J. Computational and statistical analysis of metabolomics data. Metabolomics 2015, 11, 1492–1513. [Google Scholar] [CrossRef]
- Vigotsky, A.D.; Halperin, I.; Lehman, G.J.; Trajano, G.S.; Vieira, T.M. Interpreting Signal Amplitudes in Surface Electromyography Studies in Sport and Rehabilitation Sciences. Front. Physiol. 2017, 8, 985. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dos Anjos, F.V.; Pinto, T.P.; Gazzoni, M.; Vieira, T.M. The Spatial Distribution of Ankle Muscles Activity Discriminates Aged from Young Subjects during Standing. Front. Hum. Neurosci. 2017, 11, 190. [Google Scholar] [CrossRef] [Green Version]
- Person, R.S. Rhythmic activity of a group of human motoneurones during voluntary contraction of a muscle. Electroencephalogr. Clin. Neurophysiol. 1974, 36, 585–595. [Google Scholar] [CrossRef]
- Dankel, S.J.; Mattocks, K.T.; Jessee, M.B.; Buckner, S.L.; Mouser, J.G.; Loenneke, J.P. Do metabolites that are produced during resistance exercise enhance muscle hypertrophy? Eur. J. Appl. Physiol. 2017, 117, 2125–2135. [Google Scholar] [CrossRef]
- Fallentin, N.; Jorgensen, K.; Simonsen, E.B. Motor unit recruitment during prolonged isometric contractions. Eur. J. Appl. Physiol. Occup. Physiol. 1993, 67, 335–341. [Google Scholar] [CrossRef]
- Fuglevand, A.J.; Zackowski, K.M.; Huey, K.A.; Enoka, R.M. Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J. Physiol. 1993, 460, 549–572. [Google Scholar] [CrossRef] [PubMed]
- Schoenfeld, B.J. Potential mechanisms for a role of metabolic stress in hypertrophic adaptations to resistance training. Sports Med. 2013, 43, 179–194. [Google Scholar] [CrossRef]
- Takada, S.; Okita, K.; Suga, T.; Omokawa, M.; Kadoguchi, T.; Sato, T.; Takahashi, M.; Yokota, T.; Hirabayashi, K.; Morita, N.; et al. Low-intensity exercise can increase muscle mass and strength proportionally to enhanced metabolic stress under ischemic conditions. J. Appl. Physiol. (1985) 2012, 113, 199–205. [Google Scholar] [CrossRef] [Green Version]
- Brunelli, D.T.; Finardi, E.A.R.; Bonfante, I.L.P.; Gaspari, A.F.; Sardeli, A.V.; Souza, T.M.F.; Chacon-Mikahil, M.P.T.; Cavaglieri, C.R. Acute low- compared to high-load resistance training to failure results in greater energy expenditure during exercise in healthy young men. PLoS ONE 2019, 14, e0224801. [Google Scholar] [CrossRef]
- Fry, A.C. The role of resistance exercise intensity on muscle fibre adaptations. Sports Med. 2004, 34, 663–679. [Google Scholar] [CrossRef]
- Schiaffino, S.; Reggiani, C. Fiber types in mammalian skeletal muscles. Physiol. Rev. 2011, 91, 1447–1531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adams, G.R.; Bamman, M.M. Characterization and regulation of mechanical loading-induced compensatory muscle hypertrophy. Compr. Physiol. 2012, 2, 2829–2870. [Google Scholar] [CrossRef]
- Cooper, A.J.; Shurubor, Y.I.; Dorai, T.; Pinto, J.T.; Isakova, E.P.; Deryabina, Y.I.; Denton, T.T.; Krasnikov, B.F. omega-Amidase: An underappreciated, but important enzyme in L-glutamine and L-asparagine metabolism; relevance to sulfur and nitrogen metabolism, tumor biology and hyperammonemic diseases. Amino. Acids. 2016, 48, 1–20. [Google Scholar] [CrossRef]
- Baumgartner, M.R.; Almashanu, S.; Suormala, T.; Obie, C.; Cole, R.N.; Packman, S.; Baumgartner, E.R.; Valle, D. The molecular basis of human 3-methylcrotonyl-CoA carboxylase deficiency. J. Clin. Investig. 2001, 107, 495–504. [Google Scholar] [CrossRef] [Green Version]
- Longo, N.; Frigeni, M.; Pasquali, M. Carnitine transport and fatty acid oxidation. Biochim. Biophys. Acta 2016, 1863, 2422–2435. [Google Scholar] [CrossRef]
- Evans, M.; Cogan, K.E.; Egan, B. Metabolism of ketone bodies during exercise and training: Physiological basis for exogenous supplementation. J. Physiol. 2017, 595, 2857–2871. [Google Scholar] [CrossRef] [Green Version]
- Tinsley, G.M.; Willoughby, D.S. Fat-Free Mass Changes During Ketogenic Diets and the Potential Role of Resistance Training. Int. J. Sport Nutr. Exerc. Metab. 2016, 26, 78–92. [Google Scholar] [CrossRef]
- Winder, W.W.; Baldwin, K.M.; Holloszy, J.O. Enzymes involved in ketone utilization in different types of muscle: Adaptation to exercise. Eur. J. Biochem. 1974, 47, 461–467. [Google Scholar] [CrossRef]
- Volek, J.S.; Duncan, N.D.; Mazzetti, S.A.; Staron, R.S.; Putukian, M.; Gomez, A.L.; Pearson, D.R.; Fink, W.J.; Kraemer, W.J. Performance and muscle fiber adaptations to creatine supplementation and heavy resistance training. Med. Sci. Sports Exerc. 1999, 31, 1147–1156. [Google Scholar] [CrossRef]
- Louis, M.; Poortmans, J.R.; Francaux, M.; Hultman, E.; Berre, J.; Boisseau, N.; Young, V.R.; Smith, K.; Meier-Augenstein, W.; Babraj, J.A.; et al. Creatine supplementation has no effect on human muscle protein turnover at rest in the postabsorptive or fed states. Am. J. Physiol. Endocrinol. Metab. 2003, 284, E764–E770. [Google Scholar] [CrossRef] [Green Version]
- Safdar, A.; Yardley, N.J.; Snow, R.; Melov, S.; Tarnopolsky, M.A. Global and targeted gene expression and protein content in skeletal muscle of young men following short-term creatine monohydrate supplementation. Physiol. Genom. 2008, 32, 219–228. [Google Scholar] [CrossRef]
- Parise, G.; Mihic, S.; MacLennan, D.; Yarasheski, K.E.; Tarnopolsky, M.A. Effects of acute creatine monohydrate supplementation on leucine kinetics and mixed-muscle protein synthesis. J. Appl. Physiol. (1985) 2001, 91, 1041–1047. [Google Scholar] [CrossRef] [Green Version]
- Crossland, H.; Smith, K.; Atherton, P.J.; Wilkinson, D.J. A novel stable isotope tracer method to simultaneously quantify skeletal muscle protein synthesis and breakdown. Metabol. Open 2020, 5, 100022. [Google Scholar] [CrossRef]
- Fischman, A.J.; Yu, Y.M.; Livni, E.; Babich, J.W.; Young, V.R.; Alpert, N.M.; Tompkins, R.G. Muscle protein synthesis by positron-emission tomography with L-[methyl-11C]methionine in adult humans. Proc. Natl. Acad. Sci. USA 1998, 95, 12793–12798. [Google Scholar] [CrossRef] [Green Version]
- Moran, A.; Toffolo, G.; Schiavon, M.; Vella, A.; Klaus, K.; Cobelli, C.; Nair, K.S. A novel triple-tracer approach to assess postprandial protein turnover. Am. J. Physiol. Endocrinol. Metab. 2018, 315, E469–E477. [Google Scholar] [CrossRef]
- Vendelbo, M.H.; Moller, A.B.; Christensen, B.; Nellemann, B.; Clasen, B.F.; Nair, K.S.; Jorgensen, J.O.; Jessen, N.; Moller, N. Fasting increases human skeletal muscle net phenylalanine release and this is associated with decreased mTOR signaling. PLoS ONE 2014, 9, e102031. [Google Scholar] [CrossRef] [Green Version]
- Gu, X.; Orozco, J.M.; Saxton, R.A.; Condon, K.J.; Liu, G.Y.; Krawczyk, P.A.; Scaria, S.M.; Harper, J.W.; Gygi, S.P.; Sabatini, D.M. SAMTOR is an S-adenosylmethionine sensor for the mTORC1 pathway. Science 2017, 358, 813–818. [Google Scholar] [CrossRef] [Green Version]
- Villa, E.; Sahu, U.; O’Hara, B.P.; Ali, E.S.; Helmin, K.A.; Asara, J.M.; Gao, P.; Singer, B.D.; Ben-Sahra, I. mTORC1 stimulates cell growth through SAM synthesis and m(6)A mRNA-dependent control of protein synthesis. Mol. Cell 2021, 81, 2076–2093e2079. [Google Scholar] [CrossRef]
- Kaya, M.; Moriwaki, Y.; Ka, T.; Inokuchi, T.; Yamamoto, A.; Takahashi, S.; Tsutsumi, Z.; Tsuzita, J.; Oku, Y.; Yamamoto, T. Plasma concentrations and urinary excretion of purine bases (uric acid, hypoxanthine, and xanthine) and oxypurinol after rigorous exercise. Metabolism 2006, 55, 103–107. [Google Scholar] [CrossRef]
- Fulle, S.; Protasi, F.; Di Tano, G.; Pietrangelo, T.; Beltramin, A.; Boncompagni, S.; Vecchiet, L.; Fano, G. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp. Gerontol. 2004, 39, 17–24. [Google Scholar] [CrossRef]
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Valério, D.F.; Castro, A.; Gáspari, A.; Barroso, R. Serum Metabolites Associated with Muscle Hypertrophy after 8 Weeks of High- and Low-Load Resistance Training. Metabolites 2023, 13, 335. https://doi.org/10.3390/metabo13030335
Valério DF, Castro A, Gáspari A, Barroso R. Serum Metabolites Associated with Muscle Hypertrophy after 8 Weeks of High- and Low-Load Resistance Training. Metabolites. 2023; 13(3):335. https://doi.org/10.3390/metabo13030335
Chicago/Turabian StyleValério, Denis F., Alex Castro, Arthur Gáspari, and Renato Barroso. 2023. "Serum Metabolites Associated with Muscle Hypertrophy after 8 Weeks of High- and Low-Load Resistance Training" Metabolites 13, no. 3: 335. https://doi.org/10.3390/metabo13030335