Differential Mitochondrial Adaptation of the Slow and Fast Skeletal Muscles by Endurance Running Exercise in Streptozotocin-Induced Diabetic Mice
Language English Country Czech Republic Media print
Document type Journal Article
PubMed
39027954
PubMed Central
PMC11299777
DOI
10.33549/physiolres.935183
PII: 935183
Knihovny.cz E-resources
- MeSH
- Running * physiology MeSH
- Diabetes Mellitus, Experimental * metabolism MeSH
- Physical Endurance physiology MeSH
- Adaptation, Physiological * physiology MeSH
- Physical Conditioning, Animal * physiology MeSH
- Muscle, Skeletal metabolism MeSH
- Blood Glucose metabolism MeSH
- Mice MeSH
- Streptozocin MeSH
- Muscle Fibers, Slow-Twitch metabolism MeSH
- Muscle Fibers, Fast-Twitch metabolism MeSH
- Mitochondria, Muscle * metabolism MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Mice MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Blood Glucose MeSH
- Streptozocin MeSH
The skeletal muscle is the main organ responsible for insulin action, and glucose disposal and metabolism. Endurance and/or resistance training raises the number of mitochondria in diabetic muscles. The details of these adaptations, including mitochondrial adaptations of the slow and fast muscles in diabetes, are unclear. This study aimed to determine whether exercise training in streptozotocin (STZ)-induced mice leads to differential adaptations in the slow and fast muscles, and improving glucose clearance. Eight-week-old mice were randomly distributed into normal control (CON), diabetes (DM), and diabetes and exercise (DM+Ex) groups. In the DM and DM+Ex groups, mice received a freshly prepared STZ (100 mg/kg) intraperitoneal injection on two consecutive days. Two weeks after the injection, the mice in the groups ran on a treadmill for 60 min at 20 m/min for a week and subsequently at 25 m/min for 5 weeks (5 days/week). The analyses indicated that running training at low speed (25 m/min) enhanced mitochondrial enzyme activity and expression of lactate and glucose transporters in the plantaris (low-oxidative) muscle that improved whole-body glucose metabolism in STZ-induced diabetic mice. There were no differences in glucose transporter expression levels in the soleus (high-oxidative) muscle. The endurance running exercise at 20-25 m/min was sufficient to induce mitochondrial adaptation in the low-oxidative muscles, but not in the high-oxidative muscles, of diabetic mice. In conclusion, the present study indicated that running training at 25 m/min improved glucose metabolism by increasing the mitochondrial enzyme activity and glucose transporter 4 and monocarboxylate transporter 4 protein contents in the low-oxidative muscles in STZ-induced diabetic mice.
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Larsen S, Scheede-Bergdahl C, Whitesell T, Boushel R, Bergdahl A. Increased intrinsic mitochondrial respiratory capacity in skeletal muscle from rats with streptozotocin-induced hyperglycemia. Physiol Rep. 2015;3:e12467. doi: 10.14814/phy2.12467. PubMed DOI PMC
Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes. 2002;51:2944–2950. doi: 10.2337/diabetes.51.10.2944. PubMed DOI
Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med. 2004;350:664–671. doi: 10.1056/NEJMoa031314. PubMed DOI PMC
Yasuda K, Nishikawa W, Iwanaka N, Nakamura E, Seino Y, Tsuda K, Ishihara A. Abnormality in fibre type distribution of soleus and plantaris muscles in non-obese diabetic Goto-Kakizaki rats. Clin Exp Pharmacol Physiol. 2002;29:1001–1008. doi: 10.1046/j.1440-1681.2002.03757.x. PubMed DOI
Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes. 2005;54:1926–1933. doi: 10.2337/diabetes.54.7.1926. PubMed DOI
Yokota T, Kinugawa S, Hirabayashi K, Matsushima S, Inoue N, Ohta Y, Hamaguchi S, et al. Oxidative stress in skeletal muscle impairs mitochondrial respiration and limits exercise capacity in type 2 diabetic mice. Am J Physiol Heart Circ Physiol. 2009;297:H1069–H1077. doi: 10.1152/ajpheart.00267.2009. PubMed DOI
Colberg SR, Sigal RJ, Yardley JE, Riddell MC, Dunstan DW, Dempsey PC, Horton ES, et al. Physical activity/exercise and diabetes: A position statement of the American Diabetes Association. Diabetes Care. 2016;39:2065–2079. doi: 10.2337/dc16-1728. PubMed DOI PMC
Hall KE, McDonald MW, Grisé KN, Campos OA, Noble EG, Melling CW. The role of resistance and aerobic exercise training on insulin sensitivity measures in STZ-induced Type 1 diabetic rodents. Metabolism. 2013;62:1485–1494. doi: 10.1016/j.metabol.2013.05.012. PubMed DOI
King AJ. The use of animal models in diabetes research. Br J Pharmacol. 2012;166:877–894. doi: 10.1111/j.1476-5381.2012.01911.x. PubMed DOI PMC
Bonen A, Miskovic D, Tonouchi M, Lemieux K, Wilson MC, Marette A, Halestrap AP. Abundance and subcellular distribution of MCT1 and MCT4 in heart and fast-twitch skeletal muscles. Am J Physiol Endocrinol Metab. 2000;278:E1067–E1077. doi: 10.1152/ajpendo.2000.278.6.E1067. PubMed DOI
Juel C, Halestrap AP. Lactate transport in skeletal muscle-role and regulation of the monocarboxylate transporter. J Physiol. 1999;517:633–642. doi: 10.1111/j.1469-7793.1999.0633s.x. PubMed DOI PMC
McCullagh KJ, Poole RC, Halestrap AP, O’Brien M, Bonen A. Role of the lactate transporter (MCT1) in skeletal muscles. Am J Physiol. 1996;271:E143–E150. doi: 10.1152/ajpendo.1996.271.1.E143. PubMed DOI
Enoki T, Yoshida Y, Hatta H, Bonen A. Exercise training alleviates MCT1 and MCT4 reductions in heart and skeletal muscles of STZ-induced diabetic rats. J Appl Physiol. 2003;94:2433–2438. doi: 10.1152/japplphysiol.01155.2002. PubMed DOI
Nakamoto I, Ishihara A. Effects of voluntary running exercise on skeletal muscle properties in nonobese rats with type 2 diabetes. Physiol Res. 2020;69:73–84. doi: 10.33549/physiolres.934178. PubMed DOI PMC
Ferrannini E. The theoretical bases of indirect calorimetry: a review. Metabolism. 1988;37:287–301. doi: 10.1016/0026-0495(88)90110-2. PubMed DOI
Tadaishi M, Miura S, Kai Y, Kano Y, Oishi Y, Ezaki O. Skeletal muscle-specific expression of PGC-1alpha-b, an exercise-responsive isoform, increases exercise capacity and peak oxygen uptake. PLoS One. 2011;6:e28290. doi: 10.1371/journal.pone.0028290. PubMed DOI PMC
Weir JB. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol. 1949;109:1–9. doi: 10.1113/jphysiol.1949.sp004363. PubMed DOI PMC
Lo S, Russell JC, Taylor AW. Determination of glycogen in small tissue samples. J Appl Physiol. 1970;28:234–236. doi: 10.1152/jappl.1970.28.2.234. PubMed DOI
Takahashi Y, Matsunaga Y, Banjo M, Takahashi K, Sato Y, Seike K, Nakano S, et al. Effects of nutrient intake timing on post-exercise glycogen accumulation and its related signaling pathways in mouse skeletal muscle. Nutrients. 2019;11:2555. doi: 10.3390/nu11112555. PubMed DOI PMC
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 (Tokyo) 2014;60:413–419. doi: 10.3177/jnsv.60.413. PubMed DOI
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. doi: 10.1007/s12576-013-0290-7. PubMed DOI PMC
Takahashi K, Kitaoka Y, Matsunaga Y, Hatta H. Effect of post-exercise lactate administration on glycogen repletion and signaling activation in different types of mouse skeletal muscle. Curr Res Physiol. 2020;3:34–43. doi: 10.1016/j.crphys.2020.07.002. PubMed DOI PMC
Kitaoka Y, Tamura Y, Takahashi K, Terada K, Takemasa T, Hatta H. Effects of Nrf2 deficiency on mitochondrial oxidative stress in aged skeletal muscle. Physiol Rep. 2019;7:e13998. doi: 10.14814/phy2.13998. PubMed DOI PMC
Srere PA. Citrate synthase. Methods Enzymol. 1969;13:3–11. doi: 10.1016/0076-6879(69)13005-0. DOI
Ito M, Kondo Y, Nakatani A, Hayashi K, Naruse A. Characterization of low dose streptozotocin-induced progressive diabetes in mice. Environ Toxicol Pharmacol. 2001;9:71–78. doi: 10.1016/S1382-6689(00)00064-8. PubMed DOI
Tandon S, Ayis S, Hopkins D, Harding S, Stadler M. The impact of pharmacological and lifestyle interventions on body weight in people with type 1 diabetes: A systematic review and meta-analysis. Diabetes Obes Metab. 2021;23:350–362. doi: 10.1111/dom.14221. PubMed DOI
Choi HM, Kim HR, Kim EK, Byun YS, Won YS, Yoon WK, Kim HC, et al. An age-dependent alteration of the respiratory exchange ratio in the db/db mouse. Lab Anim Res. 2015;31:1–6. doi: 10.5625/lar.2015.31.1.1. PubMed DOI PMC
Hirsch KR, Greenwalt CE, Cabre HE, Gould LM, Brewer GJ, Blue MNM, Ferrando AA, et al. Metabolic effects of high-intensity interval training and essential amino acids. Eur J Appl Physiol. 2021;121:3297–3311. doi: 10.1007/s00421-021-04792-4. PubMed DOI
Goodpaster BH, Katsiaras A, Kelley DE. Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity. Diabetes. 2003;52:2191–2197. doi: 10.2337/diabetes.52.9.2191. PubMed DOI
Matsunaga Y, Sakata Y, Yago T, Nakamura H, Shimizu T, Takeda Y. Effects of glucose with casein peptide supplementation on post-exercise muscle glycogen resynthesis in C57BL/6J mice. Nutrients. 2018;10:753. doi: 10.3390/nu10060753. PubMed DOI PMC
Miyamoto L, Toyoda T, Hayashi T, Yonemitsu S, Nakano M, Tanaka S, Ebihara K, et al. Effect of acute activation of 5′-AMP-activated protein kinase on glycogen regulation in isolated rat skeletal muscle. J Appl Physiol. 2007;102:1007–1013. doi: 10.1152/japplphysiol.01034.2006. PubMed DOI
Takahashi Y, Matsunaga Y, Yoshida H, Shinya T, Sakaguchi R, Hatta H. High carbohydrate diet increased glucose transporter protein levels in jejunum but did not lead to enhanced post-exercise skeletal muscle glycogen recovery. Nutrients. 2021;13:2140. doi: 10.3390/nu13072140. PubMed DOI PMC
Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, Schroder HD, et al. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol. 2012;590:3349–3360. doi: 10.1113/jphysiol.2012.230185. PubMed DOI PMC
Ljubicic V, Hood DA. Specific attenuation of protein kinase phosphorylation in muscle with a high mitochondrial content. Am J Physiol Endocrinol Metab. 2009;297:E749–E758. doi: 10.1152/ajpendo.00130.2009. PubMed DOI
Matsunaga Y, Tamura Y, Takahashi Y, Masuda H, Hoshino D, Kitaoka Y, Saito N, et al. Pre-exercise casein peptide supplementation enhances endurance training-induced mitochondrial enzyme activity in slow twitch muscle, but not fast twitch muscle of high fat diet-fed mice. J Phys Fit Sports Med. 2015;4:377–384. doi: 10.7600/jpfsm.4.377. DOI
Takahashi Y, Hijikata K, Seike K, Nakano S, Banjo M, Sato Y, Takahashi K, et al. Effects of royal jelly administration on endurance training-induced mitochondrial adaptations in skeletal muscle. Nutrients. 2018;10:1735. doi: 10.3390/nu10111735. PubMed DOI PMC
Nikooie R, Rajabi H, Gharakhanlu R, Atabi F, Omidfar K, Aveseh M, Larijani B. Exercise-induced changes of MCT1 in cardiac and skeletal muscles of diabetic rats induced by high-fat diet and STZ. J Physiol Biochem. 2013;69:865–877. doi: 10.1007/s13105-013-0263-6. PubMed DOI
Harmer AR, Chisholm DJ, McKenna MJ, Hunter SK, Ruell PA, Naylor JM, Maxwell LJ, et al. Sprint training increases muscle oxidative metabolism during high-intensity exercise in patients with type 1 diabetes. Diabetes Care. 2008;31:2097–2102. doi: 10.2337/dc08-0329. PubMed DOI PMC
Bonen A. The expression of lactate transporters (MCT1 and MCT4) in heart and muscle. Eur J Appl Physiol. 2001;86:6–11. doi: 10.1007/s004210100516. PubMed DOI
Armstrong RB, Gollnick PD, Ianuzzo CD. Histochemical properties of skeletal muscle fibers in streptozotocin-diabetic rats. Cell Tissue Res. 1975;162:387–394. doi: 10.1007/BF00220185. PubMed DOI