Effect of electrical stimulation-induced resistance exercise on mitochondrial fission and fusion proteins in rat skeletal muscle

Applied Physiology, Nutrition and Metabolism

Volumn 40, Issue 11, 2015, Pages 1137-1142

  Kitaoka, Yu ^a   Ogasawara, Riki ^a   Tamura, Yuki ^a   Fujita, Satoshi ^b   Hatta, Hideo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

Drp1; Fis1; Mfn; Mitochondrial dynamics; Opa1; Resistance exercise; Skeletal muscle

Indexed keywords

DRP1 PROTEIN, RAT; DYNAMIN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; MITOFUSIN 1 PROTEIN, RAT; MITOFUSIN 2 PROTEIN, RAT; OPA1 PROTEIN, RAT; TTC11 PROTEIN, RAT;

ANIMAL; ELECTROSTIMULATION; ENERGY METABOLISM; INNERVATION; METABOLISM; MITOCHONDRIAL DYNAMICS; MUSCLE ISOMETRIC CONTRACTION; MUSCLE MITOCHONDRION; PHOSPHORYLATION; RESISTANCE TRAINING; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; TIME FACTOR;

ANIMALS; DYNAMINS; ELECTRIC STIMULATION; ENERGY METABOLISM; GTP PHOSPHOHYDROLASES; ISOMETRIC CONTRACTION; MEMBRANE PROTEINS; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MUSCLE, SKELETAL; PHOSPHORYLATION; RATS, SPRAGUE-DAWLEY; RESISTANCE TRAINING; TIME FACTORS;

EID: 84945946418     PISSN: 17155312     EISSN: 17155320     Source Type: Journal    
DOI: 10.1139/apnm-2015-0184     Document Type: Article

References (40)

1. Bach, D., Pich, S., Soriano, F.X., Vega, N., Baumgartner, B., Oriola, J., et al. 2003. Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism. A novel regulatory mechanism altered in obesity. J. Biol. Chem. 278: 17190–17197. PMID:12598526.
2. Bonen, A., Tonouchi, M., Miskovic, D., Heddle, C., Heikkila, J.J., and Halestrap, A.P. 2000. Isoform-specific regulation of the lactate transporters MCT1 and MCT4 by contractile activity. Am. J. Physiol. Endocrinol. Metab. 279: E1131–E1138.PMID:11052969.
3. Burgomaster, K.A., Howarth, K.R., Phillips, S.M., Rakobowchuk, M., Macdonald, M.J., McGee, S.L., and Gibala, M.J. 2008. Similar metabolic adaptations during exercise after low volume sprint interval and traditional endurance training in humans. J. Physiol. 586: 151–160. doi:10.1113/jphysiol. 2007.142109. PMID:17991697.
4. Cartoni, R., Léger, B., Hock, M.B., Praz, M., Crettenand, A., Pich, S., et al. 2005. Mitofusins 1/2 and ERRα expression are increased in human skeletal muscle after physical exercise. J. Physiol. 567: 349–358. doi:10.1113/jphysiol.2005. 092031. PMID:15961417.
5. Chen, H., Chomyn, A., and Chan, D.C. 2005. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280: 26185–26192. doi:10.1074/jbc.M503062200. PMID:15899901.
6. Chen, H., Vermulst, M., Wang, Y.E., Chomyn, A., Prolla, T.A., McCaffery, J.M., and Chan, D.C. 2010. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell, 141: 280–289. doi: 10.1016/j.cell.2010.02.026. PMID:20403324.
7. Ding, H., Jiang, N., Liu, H., Liu, X., Liu, D., Zhao, F., et al. 2010. Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle. Biochim. Biophys. Acta, Gen. Subj. 1800: 250–256. doi:10. 1016/j.bbagen.2009.08.007.
8. Duvezin-Caubet, S., Jagasia, R., Wagener, J., Hofmann, S., Trifunovic, A., Hansson, A., et al. 2006. Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J. Biol. Chem. 281: 37972–37979. doi:10.1074/jbc.M606059200. PMID:17003040.
9. Enoki, T., Yoshida, Y., Lally, J., Hatta, H., and Bonen, A. 2006. Testosterone increases lactate transport, monocarboxylate transporter (MCT) 1 and MCT4 in rat skeletal muscle. J. Physiol. 577: 433–443. doi:10.1113/jphysiol.2006. 115436. PMID:16959859.
10. Fan, X., Hussien, R., and Brooks, G.A. 2010. H2O2-induced mitochondrial fragmentation in C2C12 myocytes. Free Radic. Biol. Med. 49: 1646–1654. doi:10.1016/j.freeradbiomed.2010.08.024. PMID:20801212.
11. Fealy, C.E., Mulya, A., Lai, N., and Kirwan, J.P. 2014. Exercise training decreases activation of the mitochondrial fission protein dynamin-related protein-1 in insulin-resistant human skeletal muscle. J. Appl. Physiol. 117: 239–245. doi: 10.1152/japplphysiol.01064.2013.
12. Green, H., Dahly, A., Shoemaker, K., Goreham, C., Bombardier, E., and Ball-Burnett, M. 1999a. Serial effects of high-resistance and prolonged endurance training on Na+-K+ pump concentration and enzymatic activities in human vastus lateralis. Acta Physiol. Scand. 165: 177–184. doi:10.1046/j.1365-201x.1999.00484.x. PMID:10090329.
13. Green, H., Goreham, C., Ouyang, J., Ball-Burnett, M., and Ranney, D. 1999b. Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am. J. Physiol. 276: R591–R596. PMID:9950941.
14. Hoshino, D., Yoshida, Y., Kitaoka, Y., Hatta, H., and Bonen, A. 2013. Highintensity interval training increases intrinsic rates of mitochondrial fatty acid oxidation in rat red and white skeletal muscle. Appl. Physiol. Nutr. Metab. 38: 326–333. doi:10.1139/apnm-2012-0257. PMID:23537026.
15. Iqbal, S., Ostojic, O., Singh, K., Joseph, A.-M., and Hood, D.A. 2013. Expression of mitochondrial fission and fusion regulatory proteins in skeletal muscle during chronic use and disuse. Muscle Nerve, 48: 963–970. doi:10.1002/mus.23838. PMID:23494933.
16. Ishihara, N., Fujita, Y., Oka, T., and Mihara, K. 2006. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25: 2966–2977. doi:10.1038/sj.emboj.7601184. PMID:16778770.
17. Jamart, C., Naslain, D., Gilson, H., and Francaux, M. 2013. Higher activation of autophagy in skeletal muscle of mice during endurance exercise in the fasted state. Am. J. Physiol. Endocrinol. Metab. 305: E964–E974. doi:10.152/ajpendo.00270.2013. PMID:23964069.
18. Juel, C., Holten, M.K., and Dela, F. 2004. Effects of strength training on muscle lactate release and MCT1 and MCT4 content in healthy and type 2 diabetic humans. J. Physiol. 556: 297–304. doi:10.1113/jphysiol.2003.058222. PMID: 14724187.
19. Karlsson, H.K.R., Nilsson, P.-A., Nilsson, J., Chibalin, A.V., Zierath, J.R., and Blomstrand, E. 2004. Branched-chain amino acids increase p70S6k phosphorylation in human skeletal muscle after resistance exercise. Am. J. Physiol. Endocrinol. Metab. 287: E1–E7. doi:10.1152/ajpendo.00430.2003. PMID:14998784.
20. Kashatus, J.A., Nascimento, A., Myers, L.J., Sher, A., Byrne, F.L., Hoehn, K.L., et al. 2015. Erk2 phosphorylation of Drp1 promotes mitochondrial fission and MAPK-driven tumor growth. Mol. Cell, 57: 537–551. doi:10.1016/j.molcel.2015. 01.002.
21. Kitaoka, Y., Takahashi, Y., Machida, M., Takeda, K., Takemasa, T., and Hatta, H. 2014. Effect of AMPK activation on monocarboxylate transporter (MCT)1 and MCT4 in denervated muscle. J. Physiol. Sci. 64: 59–64. doi:10.1007/s12576-013-0290-7. PMID:24081524.
22. Lira, V.A., Okutsu, M., Zhang, M., Greene, N.P., Laker, R.C., Breen, D.S., et al. 2013. Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. FASEB J. 27: 4184–4193. doi:10.1096/fj.13-228486. PMID:23825228.
23. Meeusen, S., DeVay, R., Block, J., Cassidy-Stone, A., Wayson, S., McCaffery, J.M., and Nunnari, J. 2006. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell, 127: 383–395. doi:10.1016/j.cell.2006.09.021. PMID:17055438.
24. Moore, D.R., Atherton, P.J., Rennie, M.J., Tarnopolsky, M.A., and Phillips, S.M. 2011. Resistance exercise enhances mTOR and MAPK signalling in human muscle over that seen at rest after bolus protein ingestion. Acta Physiol. 201: 365–372. doi:10.1111/j.1748-1716.2010.02187.x.
25. Ogasawara, R., Kobayashi, K., Tsutaki, A., Lee, K., Abe, T., Fujita, S., et al. 2013. mTOR signaling response to resistance exercise is altered by chronic resistance training and detraining in skeletal muscle. J. Appl. Physiol. 114: 934–940. doi:10.1152/japplphysiol.01161.2012.
26. Ogasawara, R., Sato, K., Matsutani, K., Nakazato, K., and Fujita, S. 2014. The order of concurrent endurance and resistance exercise modifies mTOR signalling and protein synthesis in rat skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 306: E1155–E1162. doi:10.1152/ajpendo.00647.2013. PMID:24691029.
27. Ogborn, D.I., McKay, B.R., Crane, J.D., Safdar, A., Akhtar, M., Parise, G., and Tamopolsky, M.A. 2015. Effects of age and unaccustomed resistance exercise on mitochondrial transcript and protein abundance in skeletal muscle of men. Am. J. Physiol. Regul. Integr. Comp. Physiol. 308: R734–R741. doi:10.1152/ajpregu.00005.2014. PMID:25695287.
28. Parone, P.A., Da Cruz, S., Tondera, D., Mattenberger, Y., James, D.I., Maechler, P., et al. 2008. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoSOne,3: e3257. doi:10.1371/journal. pone.0003257. PMID:18806874.
29. Perry, C.G.R., Heigenhauser, G.J.F., Bonen, A., and Spriet, L.L. 2008. Highintensity aerobic interval training increases fat and carbohydrate metabolic capacities in human skeletal muscle. Appl. Physiol. Nutr. Metab. 33: 1112–1123. doi:10.1139/H08-097. PMID:19088769.
30. Perry, C.G.R., Lally, J., Holloway, G.P., Heigenhauser, G.J., Bonen, A., and Spriet, L.L. 2010. Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J. Physiol. 588: 4795–4810. doi:10.1113/jphysiol.2010.199448. PMID: 20921196.
31. Pesta, D., Hoppel, F., Macek, C., Messner, H., Faulhaber, M., Kobel, C., et al. 2011. Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301: R1078–R1087. doi:10.1152/ajpregu.00285.2011. PMID:21775647.
32. Picard, M., Gentil, B.J., McManus, M.J., White, K., St Louis, K., Gartside, S.E., et al. 2013. Acute exercise remodels mitochondrial membrane interactions in mouse skeletal muscle. J. Appl. Physiol. 115: 1562–1571. doi:10.1152/ japplphysiol.00819.2013.
33. Picard, M., Azuelos, I., Jung, B., Giordano, C., Matecki, S., Hussain, S., et al. 2015. Mechanical ventilation triggers abnormal mitochondrial dynamics and morphology in the diaphragm. J. Appl. Physiol. 118: 1161–1171. doi:10.1152/japplphysiol.00873.2014.
34. Porter, C., Reidy, P.T., Bhattarai, N., Sidossis, L.S., and Rasmussen, B.B. 2014. Resistance Exercise Training Alters Mitochondrial Function in Human Skeletal Muscle. Med Sci Sports Exerc. doi:10.1249/MSS.0000000000000605.
35. Romanello, V., Guadagnin, E., Gomes, L., Roder, I., Sandri, C., Petersen, Y., et al. 2010. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J. 29: 1774–1785. doi:10.1038/emboj.2010.60. PMID:20400940.
36. Salvadego, D., Domenis, R., Lazzer, S., Porcelli, S., Rittweger, J., Rizzo, G., et al. 2013. Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training. J. Appl. Physiol. 114: 1527–1535. doi:10.1152/japplphysiol.00883.2012.
37. Serasinghe, M.N., Wieder, S.Y., Renault, T.T., Elkholi, R., Asciolla, J.J., Yao, J.L., et al. 2015. Mitochondrial division is requisite to RAS-induced transformation and targeted by oncogenic MAPK pathway inhibitors. Mol. Cell, 57: 521–536. doi:10.1016/j.molcel.2015.01.003.
38. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., and Mihara, K. 2007. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282: 11521–11529. doi:10.1074/jbc.M607279200. PMID:17301055.
39. Tesch, P.A., Thorsson, A., and Colliander, E.B. 1990. Effects of eccentric and concentric resistance training on skeletal muscle substrates, enzyme activities and capillary supply. Acta Physiol. Scand. 140: 575–580. doi:10.1111/j.1748-1716.1990.tb09035.x. PMID:2082717.
40. Wang, X., Li, H., Zheng, A., Yang, L., Liu, J., Chen, C., et al. 2014. Mitochondrial dysfunction-associated OPA1 cleavage contributes to muscle degeneration: preventative effect of hydroxytyrosol acetate. Cell Death Dis. 5: e1521. doi:10.1038/cddis.2014.473. PMID:25393477.