Oral Lactate Administration Additively Enhances Endurance Training-Induced Increase in Cytochrome C Oxidase Activity in Mouse Soleus Muscle
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Experimental Design
2.2.1. Four-Week Experiment
2.2.2. Single Bout Experiment
2.3. Analytical Methods
2.3.1. Mitochondrial Enzyme Activity
2.3.2. Western Blotting
2.4. Statistical Analysis
3. Results
3.1. Four-Week Experiment
3.1.1. Blood Lactate Level after Lactate Ingestion
3.1.2. Body and Muscle Weights, and Energy Intake
3.1.3. Mitochondrial Enzyme Activity Following 4-week Lactate Ingestion
3.1.4. MCT Protein Contents Following 4-Week Lactate Ingestion
3.2. Single Bout Experiment
Phosphorylation State of Protein Associated with Mitochondrial Adaptations
4. Discussion
4.1. Mitochondrial Enzyme Activity Following Oral Lactate Administration
4.2. Oral Lactate Administration and MCT Protein Contents
4.3. Effects of Metabolic Alkalosis
4.4. Ingestion Volume and Future Perspective
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Davies, K.J.; Packer, L.; Brooks, G.A. Biochemical adaptation of mitochondria, muscle, and whole-animal respiration to endurance training. Arch. Biochem. Biophys. 1981, 209, 539–554. [Google Scholar] [CrossRef]
- Fitts, R.H.; Booth, F.W.; Winder, W.W.; Holloszy, J.O. Skeletal muscle respiratory capacity, endurance, and glycogen utilization. Am. J. Physiol. 1975, 228, 1029–1033. [Google Scholar] [CrossRef] [Green Version]
- Hawley, J.A. Exercise as a therapeutic intervention for the prevention and treatment of insulin resistance. Diabetes Metab. Res. Rev. 2004, 20, 383–393. [Google Scholar] [CrossRef]
- Da Cruz, S.; Parone, P.A.; Lopes, V.S.; Lillo, C.; McAlonis-Downes, M.; Lee, S.K.; Vetto, A.P.; Petrosyan, S.; Marsala, M.; Murphy, A.N.; et al. Elevated PGC-1alpha activity sustains mitochondrial biogenesis and muscle function without extending survival in a mouse model of inherited ALS. Cell Metab. 2012, 15, 778–786. [Google Scholar] [CrossRef] [Green Version]
- Handschin, C.; Kobayashi, Y.M.; Chin, S.; Seale, P.; Campbell, K.P.; Spiegelman, B.M. PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev. 2007, 21, 770–783. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holloszy, J.O.; Coyle, E.F. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 1984, 56, 831–838. [Google Scholar] [CrossRef]
- Stutts, W.C. Physical activity determinants in adults. Perceived benefits, barriers, and self efficacy. AAOHN J. 2002, 50, 499–507. [Google Scholar] [CrossRef] [PubMed]
- Trost, S.G.; Owen, N.; Bauman, A.E.; Sallis, J.F.; Brown, W. Correlates of adults’ participation in physical activity: Review and update. Med. Sci. Sports Exerc. 2002, 34, 1996–2001. [Google Scholar] [CrossRef] [PubMed]
- Kimm, S.Y.; Glynn, N.W.; McMahon, R.P.; Voorhees, C.C.; Striegel-Moore, R.H.; Daniels, S.R. Self-perceived barriers to activity participation among sedentary adolescent girls. Med. Sci. Sports Exerc. 2006, 38, 534–540. [Google Scholar] [CrossRef]
- Brooks, G.A. The Science and Translation of Lactate Shuttle Theory. Cell Metab. 2018, 27, 757–785. [Google Scholar] [CrossRef] [PubMed]
- Ferguson, B.S.; Rogatzki, M.J.; Goodwin, M.L.; Kane, D.A.; Rightmire, Z.; Gladden, L.B. Lactate metabolism: Historical context, prior misinterpretations, and current understanding. Eur. J. Appl. Physiol. 2018, 118, 691–728. [Google Scholar] [CrossRef] [PubMed]
- Gladden, L.B. Lactate metabolism: A new paradigm for the third millennium. J. Physiol. 2004, 558, 5–30. [Google Scholar] [CrossRef] [PubMed]
- Fahey, T.D.; Larsen, J.D.; Brooks, G.A.; Colvin, W.; Henderson, S.; Lary, D. The effects of ingesting polylactate or glucose polymer drinks during prolonged exercise. Int. J. Sport Nutr. 1991, 1, 249–256. [Google Scholar] [CrossRef] [PubMed]
- Swensen, T.; Crater, G.; Bassett, D.R., Jr.; Howley, E.T. Adding polylactate to a glucose polymer solution does not improve endurance. Int. J. Sports Med. 1994, 15, 430–434. [Google Scholar] [CrossRef]
- Bryner, R.W.; Hornsby, W.G.; Chetlin, R.; Ullrich, I.H.; Yeater, R.A. Effect of lactate consumption on exercise performance. J. Sports Med. Phys. Fitness. 1998, 38, 116–123. [Google Scholar] [CrossRef]
- Northgraves, M.J.; Peart, D.J.; Jordan, C.A.; Vince, R.V. Effect of lactate supplementation and sodium bicarbonate on 40-km cycling time trial performance. J. Strength Cond. Res. 2014, 28, 273–280. [Google Scholar] [CrossRef] [Green Version]
- Azevedo, J.L.; Tietz, E.; Two-Feathers, T.; Paull, J.; Chapman, K. Lactate, fructose and glucose oxidation profiles in sports drinks and the effect on exercise performance. PLoS ONE. 2007, 2, e927. [Google Scholar] [CrossRef]
- Kitaoka, Y.; Takeda, K.; Tamura, Y.; Hatta, H. Lactate administration increases mRNA expression of PGC-1alpha and UCP3 in mouse skeletal muscle. Appl. Physiol. Nutr. Metab. 2016, 41, 695–698. [Google Scholar] [CrossRef] [Green Version]
- Hashimoto, T.; Hussien, R.; Oommen, S.; Gohil, K.; Brooks, G.A. Lactate sensitive transcription factor network in L6 cells: Activation of MCT1 and mitochondrial biogenesis. FASEB J. 2007, 21, 2602–2612. [Google Scholar] [CrossRef]
- Takahashi, K.; Kitaoka, Y.; Matsunaga, Y.; Hatta, H. Effects of lactate administration on mitochondrial enzyme activity and monocarboxylate transporters in mouse skeletal muscle. Physiol. Rep. 2019, 7, e14224. [Google Scholar] [CrossRef]
- Egan, B.; Zierath, J.R. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab. 2013, 17, 162–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Srere, P.A. Citrate synthase. Methods Enzymol. 1969, 13, 3–11. [Google Scholar] [CrossRef]
- Spinazzi, M.; Casarin, A.; Pertegato, V.; Salviati, L.; Angelini, C. Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat. Protoc. 2012, 7, 1235–1246. [Google Scholar] [CrossRef] [PubMed]
- Bonen, A.; Miskovic, D.; Tonouchi, M.; Lemieux, K.; Wilson, M.C.; Marette, A.; Halestrap, A.P. Abundance and subcellular distribution of MCT1 and MCT4 in heart and fast-twitch skeletal muscles. Am. J. Physiol. Endocrinol. Metab. 2000, 278, E1067–E1077. [Google Scholar] [CrossRef]
- Yamada, T.; Ivarsson, N.; Hernandez, A.; Fahlstrom, A.; Cheng, A.J.; Zhang, S.J.; Bruton, J.D.; Ulfhake, B.; Westerblad, H. Impaired mitochondrial respiration and decreased fatigue resistance followed by severe muscle weakness in skeletal muscle of mitochondrial DNA mutator mice. J. Physiol. 2012, 590, 6187–6197. [Google Scholar] [CrossRef] [Green Version]
- Cho, Y.; Hazen, B.C.; Gandra, P.G.; Ward, S.R.; Schenk, S.; Russell, A.P.; Kralli, A. Perm1 enhances mitochondrial biogenesis, oxidative capacity, and fatigue resistance in adult skeletal muscle. FASEB J. 2016, 30, 674–687. [Google Scholar] [CrossRef] [Green Version]
- Dimmer, K.S.; Friedrich, B.; Lang, F.; Deitmer, J.W.; Broer, S. The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem. J. 2000, 350 Pt 1, 219–227. [Google Scholar] [CrossRef]
- Wilson, M.C.; Jackson, V.N.; Heddle, C.; Price, N.T.; Pilegaard, H.; Juel, C.; Bonen, A.; Montgomery, I.; Hutter, O.F.; Halestrap, A.P. Lactic acid efflux from white skeletal muscle is catalyzed by the monocarboxylate transporter isoform MCT3. J. Biol. Chem. 1998, 273, 15920–15926. [Google Scholar] [CrossRef] [Green Version]
- Kitaoka, Y.; Mukai, K.; Takahashi, K.; Ohmura, H.; Hatta, H. Effect of lactate administration on exercise-induced PGC-1α mRNA expression in Thoroughbreds. Comp. Exerc. Physiol. 2020, in press. [Google Scholar]
- Kawai, M.; Minami, Y.; Sayama, Y.; Kuwano, A.; Hiraga, A.; Miyata, H. Muscle fiber population and biochemical properties of whole body muscles in Thoroughbred horses. Anat. Rec. 2009, 292, 1663–1669. [Google Scholar] [CrossRef]
- Denies, M.S.; Johnson, J.; Maliphol, A.B.; Bruno, M.; Kim, A.; Rizvi, A.; Rustici, K.; Medler, S. Diet-induced obesity alters skeletal muscle fiber types of male but not female mice. Physiol. Rep. 2014, 2, e00204. [Google Scholar] [CrossRef] [PubMed]
- Augusto, V.; Padovani, C.R.; Campos, G.E.R. Skeletal muscle fiber types in C57BL6J mice. J. Morphol. Sci. 2017, 21, 0. [Google Scholar]
- Tobina, T.; Yoshioka, K.; Hirata, A.; Mori, S.; Kiyonaga, A.; Tanaka, H. Peroxisomal proliferator-activated receptor gamma co-activator-1 alpha gene expression increases above the lactate threshold in human skeletal muscle. J. Sports Med. Phys. Fitness. 2011, 51, 683–688. [Google Scholar] [PubMed]
- Goodwin, M.L.; Harris, J.E.; Hernandez, A.; Gladden, L.B. Blood lactate measurements and analysis during exercise: A guide for clinicians. J. Diabetes Sci. Technol. 2007, 1, 558–569. [Google Scholar] [CrossRef] [Green Version]
- Costill, D.L.; Daniels, J.; Evans, W.; Fink, W.; Krahenbuhl, G.; Saltin, B. Skeletal muscle enzymes and fiber composition in male and female track athletes. J. Appl. Physiol. 1976, 40, 149–154. [Google Scholar] [CrossRef]
- Gollnick, P.D.; Armstrong, R.B.; Saltin, B.; Saubert, C.W.t.; Sembrowich, W.L.; Shepherd, R.E. Effect of training on enzyme activity and fiber composition of human skeletal muscle. J. Appl. Physiol. 1973, 34, 107–111. [Google Scholar] [CrossRef] [Green Version]
- Percival, M.E.; Martin, B.J.; Gillen, J.B.; Skelly, L.E.; MacInnis, M.J.; Green, A.E.; Tarnopolsky, M.A.; Gibala, M.J. Sodium bicarbonate ingestion augments the increase in PGC-1alpha mRNA expression during recovery from intense interval exercise in human skeletal muscle. J. Appl. Physiol. 2015, 119, 1303–1312. [Google Scholar] [CrossRef] [Green Version]
- Hoshino, D.; Tamura, Y.; Masuda, H.; Matsunaga, Y.; Hatta, H. Effects of decreased lactate accumulation after dichloroacetate administration on exercise training-induced mitochondrial adaptations in mouse skeletal muscle. Physiol. Rep. 2015, 3, e12555. [Google Scholar] [CrossRef]
- Cai, T.-Q.; Ren, N.; Jin, L.; Cheng, K.; Kash, S.; Chen, R.; Wright, S.D.; Taggart, A.K.P.; Waters, M.G. Role of GPR81 in lactate-mediated reduction of adipose lipolysis. Biochem. Biophys. Res. Commun. 2008, 377, 987–991. [Google Scholar] [CrossRef]
- Ohno, Y.; Oyama, A.; Kaneko, H.; Egawa, T.; Yokoyama, S.; Sugiura, T.; Ohira, Y.; Yoshioka, T.; Goto, K. Lactate increases myotube diameter via activation of MEK/ERK pathway in C2C12 cells. Acta Physiologica 2018, 223, e13042. [Google Scholar] [CrossRef]
- Takahashi, H.; Alves, C.R.; Stanford, K.I.; Middelbeek, R.J.; Nigro, P.; Ryan, R.E.; Xue, R.; Sakaguchi, M.; Lynes, M.D.; So, K. TGF-β2 is an exercise-induced adipokine that regulates glucose and fatty acid metabolism. Nat. Metab. 2019, 1, 291. [Google Scholar] [CrossRef] [PubMed]
- Jeanson, Y.; Ribas, F.; Galinier, A.; Arnaud, E.; Ducos, M.; Andre, M.; Chenouard, V.; Villarroya, F.; Casteilla, L.; Carriere, A. Lactate induces FGF21 expression in adipocytes through a p38-MAPK pathway. Biochem. J. 2016, 473, 685–692. [Google Scholar] [CrossRef] [PubMed]
- Schiffer, T.; Schulte, S.; Sperlich, B.; Achtzehn, S.; Fricke, H.; Struder, H.K. Lactate infusion at rest increases BDNF blood concentration in humans. Neurosci. Lett. 2011, 488, 234–237. [Google Scholar] [CrossRef] [PubMed]
- Larsen, S.; Nielsen, J.; Hansen, C.N.; Nielsen, L.B.; Wibrand, F.; Stride, N.; Schroder, H.D.; Boushel, R.; Helge, J.W.; Dela, F.; et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J. Physiol. 2012, 590, 3349–3360. [Google Scholar] [CrossRef]
- Jacobs, R.A.; Fluck, D.; Bonne, T.C.; Burgi, S.; Christensen, P.M.; Toigo, M.; Lundby, C. Improvements in exercise performance with high-intensity interval training coincide with an increase in skeletal muscle mitochondrial content and function. J. Appl. Physiol. 2013, 115, 785–793. [Google Scholar] [CrossRef] [Green Version]
- Granata, C.; Jamnick, N.A.; Bishop, D.J. Training-Induced Changes in Mitochondrial Content and Respiratory Function in Human Skeletal Muscle. Sports Med. 2018, 48, 1809–1828. [Google Scholar] [CrossRef]
- Granata, C.; Oliveira, R.S.; Little, J.P.; Renner, K.; Bishop, D.J. Mitochondrial adaptations to high-volume exercise training are rapidly reversed after a reduction in training volume in human skeletal muscle. FASEB J. 2016, 30, 3413–3423. [Google Scholar] [CrossRef] [Green Version]
- Granata, C.; Oliveira, R.S.F.; Little, J.P.; Renner, K.; Bishop, D.J. Training intensity modulates changes in PGC-1α and p53 protein content and mitochondrial respiration, but not markers of mitochondrial content in human skeletal muscle. FASEB J. 2016, 30, 959–970. [Google Scholar] [CrossRef] [Green Version]
- Jacobs, R.A.; Lundby, C. Mitochondria express enhanced quality as well as quantity in association with aerobic fitness across recreationally active individuals up to elite athletes. J. Appl. Physiol. 2013, 114, 344–350. [Google Scholar] [CrossRef] [Green Version]
- Montero, D.; Cathomen, A.; Jacobs, R.A.; Fluck, D.; de Leur, J.; Keiser, S.; Bonne, T.; Kirk, N.; Lundby, A.K.; Lundby, C. Haematological rather than skeletal muscle adaptations contribute to the increase in peak oxygen uptake induced by moderate endurance training. J. Physiol. 2015, 593, 4677–4688. [Google Scholar] [CrossRef]
- Kitaoka, Y.; Watanabe, D.; Nonaka, Y.; Yagishita, K.; Kano, Y.; Hoshino, D. Effects of clenbuterol administration on mitochondrial morphology and its regulatory proteins in rat skeletal muscle. Physiol. Rep. 2019, 7, e14266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iqbal, S.; Ostojic, O.; Singh, K.; Joseph, A.M.; Hood, D.A. Expression of mitochondrial fission and fusion regulatory proteins in skeletal muscle during chronic use and disuse. Muscle Nerve 2013, 48, 963–970. [Google Scholar] [CrossRef] [PubMed]
- Pilegaard, H.; Domino, K.; Noland, T.; Juel, C.; Hellsten, Y.; Halestrap, A.P.; Bangsbo, J. Effect of high-intensity exercise training on lactate/H+ transport capacity in human skeletal muscle. Am. J. Physiol. 1999, 276, E255–E261. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kitaoka, Y.; Masuda, H.; Mukai, K.; Hiraga, A.; Takemasa, T.; Hatta, H. Effect of training and detraining on monocarboxylate transporter (MCT) 1 and MCT4 in Thoroughbred horses. Exp. Physiol. 2011, 96, 348–355. [Google Scholar] [CrossRef] [PubMed]
- Perry, C.G.; Heigenhauser, G.J.; Bonen, A.; Spriet, L.L. High-intensity aerobic interval training increases fat and carbohydrate metabolic capacities in human skeletal muscle. Appl. Physiol. Nutr. Metab. 2008, 33, 1112–1123. [Google Scholar] [CrossRef]
- Hoshino, D.; Hanawa, T.; Takahashi, Y.; Masuda, H.; Kato, M.; Hatta, H. Chronic post-exercise lactate administration with endurance training increases glycogen concentration and monocarboxylate transporter 1 protein in mouse white muscle. J. Nutr. Sci. Vitaminol. 2014, 60, 413–419. [Google Scholar] [CrossRef] [Green Version]
- Mazzeo, R.S.; Brooks, G.A.; Schoeller, D.A.; Budinger, T.F. Disposal of blood [1-13C]lactate in humans during rest and exercise. J. Appl. Physiol. 1986, 60, 232–241. [Google Scholar] [CrossRef]
- McLane, J.A.; Holloszy, J.O. Glycogen synthesis from lactate in the three types of skeletal muscle. J. Biol. Chem. 1979, 254, 6548–6553. [Google Scholar]
- Kitaoka, Y.; Takahashi, Y.; Machida, M.; Takeda, K.; Takemasa, T.; Hatta, H. Effect of AMPK activation on monocarboxylate transporter (MCT)1 and MCT4 in denervated muscle. J. Physiol. Sci. 2014, 64, 59–64. [Google Scholar] [CrossRef]
- Furugen, A.; Kobayashi, M.; Narumi, K.; Watanabe, M.; Otake, S.; Itagaki, S.; Iseki, K. AMP-activated protein kinase regulates the expression of monocarboxylate transporter 4 in skeletal muscle. Life Sci. 2011, 88, 163–168. [Google Scholar] [CrossRef] [Green Version]
- Thomas, C.; Bishop, D.J.; Lambert, K.; Mercier, J.; Brooks, G.A. Effects of acute and chronic exercise on sarcolemmal MCT1 and MCT4 contents in human skeletal muscles: Current status. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 302, R1–R14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Montfoort, M.C.; Van Dieren, L.; Hopkins, W.G.; Shearman, J.P. Effects of ingestion of bicarbonate, citrate, lactate, and chloride on sprint running. Med. Sci. Sports. Exerc. 2004, 36, 1239–1243. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bishop, D.J.; Thomas, C.; Moore-Morris, T.; Tonkonogi, M.; Sahlin, K.; Mercier, J. Sodium bicarbonate ingestion prior to training improves mitochondrial adaptations in rats. Am. J. Physiol. Endocrinol. Metab. 2010, 299, E225–E233. [Google Scholar] [CrossRef] [PubMed]
- Hashimoto, T.; Yokokawa, T.; Narusawa, R.; Okada, Y.; Kawaguchi, R.; Higashida, K. A lactate-based compound containing caffeine in addition to voluntary running exercise decreases subcutaneous fat mass and improves glucose metabolism in obese rats. J. Funct. Foods. 2019, 56, 84–91. [Google Scholar] [CrossRef]
S+S (n = 8) | L+S (n = 9) | S+T (n = 8) | L+T (n = 8) | |
---|---|---|---|---|
Initial body weight (g) | 36.7 ± 0.5 | 36.4 ± 0.6 | 36.8 ± 0.4 | 36.4 ± 0.9 |
Final body weight (g) | 40.6 ± 0.8 | 40.5 ± 0.5 | 41.2 ± 0.5 | 40.6 ± 0.7 |
Plantaris muscle (mg) | 40.0 ± 1.3 | 41.7 ± 1.4 | 40.3 ± 1.6 | 41.3 ± 1.5 |
Soleus muscle (mg) | 17.6 ± 0.6 | 16.8 ± 1.1 | 19.0 ± 0.8 | 18.6 ± 0.9 |
Energy intake (kcal/day) | 18.2 ± 0.5 | 17.9 ± 0.5 | 18.8 ± 0.3 | 18.0 ± 0.5 |
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Takahashi, K.; Kitaoka, Y.; Yamamoto, K.; Matsunaga, Y.; Hatta, H. Oral Lactate Administration Additively Enhances Endurance Training-Induced Increase in Cytochrome C Oxidase Activity in Mouse Soleus Muscle. Nutrients 2020, 12, 770. https://doi.org/10.3390/nu12030770
Takahashi K, Kitaoka Y, Yamamoto K, Matsunaga Y, Hatta H. Oral Lactate Administration Additively Enhances Endurance Training-Induced Increase in Cytochrome C Oxidase Activity in Mouse Soleus Muscle. Nutrients. 2020; 12(3):770. https://doi.org/10.3390/nu12030770
Chicago/Turabian StyleTakahashi, Kenya, Yu Kitaoka, Ken Yamamoto, Yutaka Matsunaga, and Hideo Hatta. 2020. "Oral Lactate Administration Additively Enhances Endurance Training-Induced Increase in Cytochrome C Oxidase Activity in Mouse Soleus Muscle" Nutrients 12, no. 3: 770. https://doi.org/10.3390/nu12030770
APA StyleTakahashi, K., Kitaoka, Y., Yamamoto, K., Matsunaga, Y., & Hatta, H. (2020). Oral Lactate Administration Additively Enhances Endurance Training-Induced Increase in Cytochrome C Oxidase Activity in Mouse Soleus Muscle. Nutrients, 12(3), 770. https://doi.org/10.3390/nu12030770