Influence of Forced Running Loads on the Content of Na + /K + -ATPase Isoforms and Monovalent Cations in Skeletal Muscles of Mice with a Model of Type II Diabetes Mellitus

A. N. Zakharova; Захарова А. Н.; K. G. Milovanova; Милованова К. Г.; A. A. Orlova; Орлова А. А.; E. Yu. Dyakova; Дьякова Е. Ю.; Yu. G. Kalinnikova; Калинникова Ю. Г.; O. V. Kollantay; Коллантай О. В.; I. Yu. Shuvalov; Шувалов И. Ю.; A. V. Chibalin; Чибалин А. В.; L. V. Kapilevich; Капилевич Л. В.

doi:10.31857/S0869813923120142

Influence of Forced Running Loads on the Content of Na⁺/K⁺-ATPase Isoforms and Monovalent Cations in Skeletal Muscles of Mice with a Model of Type II Diabetes Mellitus

Authors: Zakharova A.N.¹, Milovanova K.G.¹, Orlova A.A.¹, Dyakova E.Y.¹, Kalinnikova Y.G.¹, Kollantay O.V.¹, Shuvalov I.Y.¹, Chibalin A.V.¹, Kapilevich L.V.¹
Affiliations:
1. National Research Tomsk State University
Issue: Vol 109, No 12 (2023)
Pages: 1920-1934
Section: ЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИ
URL: https://journals.rcsi.science/0869-8139/article/view/233855
DOI: https://doi.org/10.31857/S0869813923120142
EDN: https://elibrary.ru/CHNRKQ
ID: 233855

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Abstract

The effect of forced running for 1 hour daily for 4 weeks on the content of Na⁺/K⁺-ATPase isoforms and monovalent cations in the skeletal muscles of mice with a model of type II diabetes mellitus (DM-II) was studied. To form a model of the disease, a high-fat diet was used, and physical activity in the form of forced running was carried out for 4 weeks. The content of Na⁺/K⁺-ATPase isoforms and Na⁺ and K⁺ ions in muscle tissue of m. gastrocnemius was determined by Western blotting and atomic absorption spectrophotomery, respectively. It has been shown that the formation of DM-II in mice is accompanied by changes in the content of Na⁺/K⁺-ATPase alpha 1 and 2 isoforms in muscle tissue. The effect of forced running loads on the content of Na⁺/K⁺-ATPase in muscle tissue is significant and primarily differs in age groups. One can also note a certain dependence of the influence of forced running loads on the content of this enzyme on the time of their use. In young animals, changes in the concentrations of monovalent sodium and potassium cations after forced running loads were less pronounced. In aged mice, against the background of forced loads, an increase in the content of sodium and decrease in the content of potassium in muscle tissue was observed. The detected changes in monovalent cations content in the muscle tissue of mice with diabetes mellitus II under the influence of forced running loads may play a role in the implementation of the metabolic effects of physical activity.

Keywords

monovalent cations, Na⁺/K⁺-ATPasa, muscles, running load, diabetes mellitus

References

Groop LC, Eriksson JG (1992) The etiology and pathogenesis of non-insulin-dependent diabetes. Ann Med 24(6): 483–489. https://doi.org/10.1002/dmr.5610090503
Fujimaki S, Kuwabara T (2017) Diabetes-induced dysfunction of mitochondria and stem cells in skeletal muscle and the nervous system. Int J Mol Sci 18(10): 2147. https://doi.org/10.3390/ijms18102147
Højlund K (2014) Metabolism and insulin signaling in common metabolic disorders and inherited insulin resistance. Dan Med J 61(7): B4890.
Nagy C, Einwallner E (2018) Study of In vivo glucose metabolism in high-fat diet-fed mice using oral glucose tolerance test (OGTT) and insulin tolerance test (ITT). J Vis Exp 7(131): 1–12. https://doi.org/10.3791/56672
Huh JY (2018) The role of exercise-induced myokines in regulating metabolism. Arch Pharm Res 41(1): 14–29. https://doi.org/10.1007/s12272-017-0994-y
Zakharova AN, Milovanova KG, Orlova, AA, Dyakova EY, Kalinnikova JG, Kollantay OV, Shuvalov IY, Chibalin AV, Kapilevich LV (2023) Effects of Treadmill Running at Different Light Cycles in Mice with Metabolic Disorders. Int J Mol Sci 24: 15132. https://doi.org/10.3390/ijms242015132
Winzell MS, Ahren B (2004) The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 53(3): S215–S219. https://doi.org/10.2337/diabetes.53.suppl_3.s215
Meneilly GS (2001) Pathophysiology of diabetes in the elderly. In: Diabetes in old age. John Wiley & Sons. 155–164. https://doi.org/10.1002/0470842326.ch2
Brandt C, Pedersen BK (2010) The role of exercise-induced myokines in muscle homeostasis and the defense against chronic diseases. J Biomed Biotechnol 520258. https://doi.org/10.1155/2010/520258
Hansen JS, Zhao X, Irmler M, Liu X, Hoene M, Scheler M, Li Y, Beckers J, Hrabĕ de Angelis M, Häring HU, Pedersen BK, Lehmann R, Xu G, Plomgaard P, Weigert C (2015) Type 2 diabetes alters metabolic and transcriptional signatures of glucose and amino acid metabolism during exercise and recovery. Diabetologia 58(8): 1845–1854. https://doi.org/10.1007/s00125-015-3584-x
Karstoft K, Pedersen BK (2016) Exercise and type 2 diabetes: focus on metabolism and inflammation. Immunol Cell Biol 94: 146–150. https://doi.org/10.1038/icb.2015.101
Kapilevich L, Zakharova A, Kabachkova A, Kironenko T, Milovanova K, Orlov S (2017) Different impact of physical activity on plasma myokines content in athletes and untrained volunteers. FEBS J 284(1): 370–373.
Kapilevich LV, Zakharova AN, Kabachkova AV, Kironenko TA, Orlov SN (2017) Dynamic and static exercises differentially affect plasma cytokine content in elite endurance- and strength-trained athletes and untrained volunteers. Front Physiol 30(8): 35. https://doi.org/10.3389/fphys.2017.00035
Jurkat-Rott K, Fauler M, Lehmann-Horn F (2006) Ion channels and ion transporters of the transverse tubular system of skeletal muscle. J Muscle Res Cell Motil 27: 275–290. https://doi.org/10.1007/s10974-006-9088-z
Sejersted OM, Sjogaard G (2000) Dynamics and consequences of potassium shifts in skeletal muscle and heart during exercise. Physiol Rev 80: 1411–1481. https://doi.org/10.1152/physrev.2000.80.4.1411
McDonough AA, Thompson CB, Youn JH (2002) Skeletal muscle regulates extracellular potassium. Am J Physiol Ren Physiol 282: F967–F974. https://doi.org/10.1152/ajprenal.00360.2001
McKenna MJ, Bangsbo J, Renaud JM (2008) Muscle K+, Na+, and Cl– -disturbances and Na-K pump inactivation: implications for fatigue. J Appl Phys 104: 288–295. https://doi.org/10.1152/japplphysiol.01037.2007
Murphy KT, Nielsen OB, Clausen T (2008) Analysis of exerciseinduced Na+-K+ exchange in rat skeletal muscle. Exp Physiol 93: 1249–1262. https://doi.org/10.1113/expphysiol.2008.042457
Cairns SP, Lindinger MI (2008) Do multiple ionic interactions contribute to skeletal muscle fatigue? J Physiol 586: 4039–4054. https://doi.org/10.1113/jphysiol.2008.155424
Orlov SN, Koltsova SV, Kapilevich LV, Gusakova SV, Dulin NO (2015) KCC1 and NKCC2: The pathogenetic role of cation-chloride cotransporters in hypertension. Genes & Diseas 2: 186–196. https://doi.org/10.1016/j.gendis.2015.02.007
Smolyaninova LV, Koltsova SV, Sidorenko SV, Orlov SN (2017) Augmented gene expression triggered by Na+,K+-ATPase inhibition: Role of -mediated and – independent excitation-transcription coupling. Cell Calcium 68: 5–13. https://doi.org/10.1016/j.ceca.2017.10.00210.1016/j.ceca.2017.10.002
Sidorenko S, Klimanova E, Milovanova K, Lopina OD, Kapilevich LV, Chibalin AV, Orlov SN (2018) Transcriptomic changes in C2C12 myotubes triggered by electrical stimulation: Role of -mediated and -independent signaling and elevated [Na+]i/[K+]i ratio. Cell Calcium 76: 72–86. https://doi.org/10.1016/j.ceca.2018.09.00710.1016/j.ceca.2018.09.007
Kapilevich LV, Kironenko TA, Zaharova AN (2015) Skeletal muscle as an endicrine organ: role of [Na+]i/[K+]i-mediated excitation-transcription coupling. Genes & Diseas 2: 328–336. https://doi.org/10.1016/j.gendis.2015.10.001
Lauritzen HP, Brandauer J, Schjerling P (2013) Contraction and AICAR stimulate IL-6 vesicle depletion from skeletal muscle fibers in vivo. Diabetes 62: 3081–3092. https://doi.org/10.2337/db12-1261
Jannot MF, Dufayet De La Tour DT, Coste P (2002) Na/K ATPase activity in Diabetic Patient Metabolism. Diabetes mellitus 51(3): 284–291.
Shamansurova ZM, Mukhamedova FA, Tsoi AG, Tashmanova AB, Alieva AV, Akhrarova NA (2009) Abnormal Na-K-ATPase activity in erythrocytes from patients with diabetes mellitus. Diabetes mellitus 12(2): 55–57. https://doi.org/10.14341/2072-0351-5399
Chistyakova OV, Sukhov IB, Dobretsov MG, Kubasov IV (2020) Study of Na/K-ATPase activity in the myocardium of rats under experimental conditions of prediabetes and diabetes mellitus. J Evol Biochem Physiol 56(2): 166–168. https://doi.org/10.1134/S0022093020020118
Kapilevich LV, Milovanova KG, Sidorenko SV, Fedorov DA, Kironenko TA, Zakharova AN, Dyakova EYu, Orlov SN (2020) Influence of dynamic and static loads on the content of sodium and potassium in mouse skeletal muscles. Bull Exp Biol Med 169(1): 4–7. https://doi.org/10.1007/s10517-020-04811-y
Klimanova EA, Sidorenko SV, Tverskoi AM, Shiyan AA, Smolyaninova LV, Kapilevich LV, Gusakova SV, Maksimov GV, Lopina OD, Orlov SN (2019) Search for Intracellular Sensors Involved in the Functioning of Monovalent Cations as Secondary Messengers. Biochemistry (Moscow) 84(11): 1280–1295. https://doi.org/10.1134/S0006297919110063
Shiyan AA, Sidorenko SV, Fedorov D, Klimanova EA, Smolyaninova LV, Kapilevich LV, Grygorczyk R, Orlov SN (2019) Elevation of intracellular Na+ contributes to expression of early response genes triggered by endothelial cell shrinkage. Cell Physiol Biochem 53(4): 638–647. https://doi.org/10.33594/000000162
Smolyaninova LV, Shiyan AA, Kapilevich LV, Lopachev AV, Fedorova TN, Klementieva TS, Moskovtsev AA, Kubatiev AA, Orlov SN (2019) Transcriptomic changes triggered by ouabain in rat cerebellum granule cells: Role of α3- and α1-Na+,K+-ATPase-mediated signaling. PLoS One 14(9): e0222767. https://doi.org/10.1371/journal.pone.0222767
Kapilevich LV, Zakharova AN, Dyakova EYu, Kalinnikova JG, Chibalin AV (2019) Mice experimental model of diabetes mellitus type ii based on high fat diet. Bull Siber Med 18(3): 53–61. https://doi.org/10.20538/1682-0363-2019-3-53-61
Zakharova AN, Kalinnikova Y, Negodenko ES, Orlova AA, Kapilevich LV (2020) Experimental simulation of cyclic training loads. Teor Prakt Fizich Kult 10: 26–27.
Clausen T (2013) Quantification of Na, K pumps and their transport rate in skeletal muscle: Functional significance. J General Physiol 142(4): 327–345. https://doi.org/10.1085/jgp.201310980
Raue U, Trappe TA, Estrem ST, Qian H-R, Helvering LM, Smith RC, Trappe S (2012) Transcriptomic signature of resistance exercise adaptations: mixed muscle and fiber type specific profiles in young and old adults. J Appl Physiol 112: 1625–1636. https://doi.org/10.1152/japplphysiol.00435.2011
McKenna MJ, Bangsbo J, Renaud JM (2008) Muscle K+, Na+, and Cl– disturbances and Na+-K+ pump inactivation: implications for fatigue. J Appl Phys 104: 288–295. https://doi.org/10.1152/japplphysiol.01037.2007
Koltsova SV, Trushina Y, Haloui M, Akimova OA, Tremblay J, Hamet P, Orlov SN (2012) Ubiquitous [Na+]i/[K+]i-sensitive transcriptome in mammalian cells: evidence for [Ca2+]i-independent excitation-transcription coupling. PLoS One 7: e38032. https://doi.org/10.1371/journal.pone.0038032