Pulsed electromagnetic fields alleviate streptozotocin‑induced diabetic muscle atrophy

Yang,Jin; Sun,Lijun; Fan,Xiushan; Yin,Bo; Kang,Yiting; An,Shucheng; Tang,Liang

doi:10.3892/mmr.2018.9067

Pulsed electromagnetic fields alleviate streptozotocin‑induced diabetic muscle atrophy

Authors:
- Jin Yang
- Lijun Sun
- Xiushan Fan
- Bo Yin
- Yiting Kang
- Shucheng An
- Liang Tang
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Affiliations: College of Life Sciences, Shaanxi Normal University, Xi'an, Shaanxi 710062, P.R. China, Institute of Sports Biology, Shaanxi Normal University, Xi'an, Shaanxi 710119, P.R. China
Published online on: May 23, 2018 https://doi.org/10.3892/mmr.2018.9067
Pages: 1127-1133

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Abstract

Diabetic muscle atrophy causes a reduction of skeletal muscle size and strength, which affects normal daily activities. However, pulsed electromagnetic fields (PEMFs) can retard the atrophy of type II fibers (ActRIIB) in denervated muscles. Therefore, the purpose of the present study was to determine whether PEMFs can alleviate streptozotocin (STZ)‑induced diabetic muscle atrophy. To do this, 40 Sprague‑Dawley (SD) rats were randomly divided into four groups (n=10 per group): The normal control group (NC; nondiabetic rats without treatment); the diabetic mellitus group (DM; STZ‑induced rats without treatment); the diabetic insulin‑treated group (DT; diabetic rats on insulin treatment, 6‑8 U/d twice a day for 6 weeks) as a positive control; and the diabetic PEMFs therapy group (DP; diabetic rats with PEMFs exposure treatment, 15 Hz, 1.46 mT, 30 min/day for 6 weeks). Body weight, muscle strength, muscle mass and serum insulin level were significantly increased in the DP group compared with the DM group. PEMFs also decreased the blood glucose level and altered the activity of metabolic enzymes. PEMFs significantly increased the cross‑sectional area of muscle fiber. In addition, PEMFs significantly activated protein kinase B (Akt) and mammalian target of rapamycin (mTOR), and inhibited the activity of myostatin (MSTN), ActRIIB and forkhead box protein O1 (FoxO1) compared with the DM group. Thus indicating that the Akt/mTOR and Akt/FoxO1 signaling pathways may be involved in the promotion of STZ‑induced diabetic muscle atrophy by PEMFs. The results of the present study suggested that PEMFs stimulation may alleviate diabetic muscle atrophy in the STZ model, and that this is associated with alterations in multiple signaling pathways in which MSTN may be an integral factor. MSTN‑associated signaling pathways may provide therapeutic targets to attenuate severe diabetic muscle wasting.

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1	Atkinson MA and Eisenbarth GS: Type 1 diabetes: New perspectives on disease pathogenesis and treatment. Lancet. 358:221–229. 2001. View Article : Google Scholar : PubMed/NCBI
2	Andersen H, Gjerstad MD and Jakobsen J: Atrophy of foot muscles: A measure of diabetic neuropathy. Diabetes Care. 27:2382–2385. 2004. View Article : Google Scholar : PubMed/NCBI
3	Fritzsche K, Blüher M, Schering S, Buchwalow IB, Kern M, Linke A, Oberbach A, Adams V and Punkt K: Metabolic profile and nitric oxide synthase expression of skeletal muscle fibers are altered in patients with type 1 diabetes. Exp Clin Endocrinol Diabetes. 116:606–613. 2008. View Article : Google Scholar : PubMed/NCBI
4	Krause MP, Riddell MC, Gordon CS, Imam SA, Cafarelli E and Hawke TJ: Diabetic myopathy differs between Ins2Akita+/- and streptozotocin-induced Type 1 diabetic models. J Appl Physiol (1985). 106:1650–1659. 2009. View Article : Google Scholar : PubMed/NCBI
5	Jakobsen J and Reske-Nielsen E: Diffuse muscle fiber atrophy in newly diagnosed diabetes. Clin Neuropathol. 5:73–77. 1986.PubMed/NCBI
6	Riddell MC and Iscoe KE: Physical activity, sport, and pediatric diabetes. Pediatr Diabetes. 7:60–70. 2006. View Article : Google Scholar : PubMed/NCBI
7	Hulmi JJ, Silvennoinen M, Lehti M, Kivelä R and Kainulainen H: Altered REDD1, myostatin, and Akt/mTOR/FoxO/MAPK signaling in streptozotocin-induced diabetic muscle atrophy. Am J Physiol Endocrinol Metab. 302:E307–E315. 2012. View Article : Google Scholar : PubMed/NCBI
8	Tang L, Liu CT, Wang XD, Luo K, Zhang DD, Chi AP, Zhang J and Sun LJ: A prepared anti-MSTN polyclonal antibody reverses insulin resistance of diet-induced obese rats via regulation of PI3K/Akt/mTOR&FoxO1 signal pathways. Biotechnol Lett. 36:2417–2423. 2014. View Article : Google Scholar : PubMed/NCBI
9	McPherron AC, Lawler AM and Lee SJ: Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 387:83–90. 1997. View Article : Google Scholar : PubMed/NCBI
10	Glass DJ: PI3 kinase regulation of skeletal muscle hypertrophy and atrophy. Curr Top Microbiol Immunol. 346:267–278. 2010.PubMed/NCBI
11	Chang CW and Lien IN: Tardy effect of neurogenic muscular atrophy by magnetic stimulation. Am J Phys Med Rehabil. 73:275–279. 1994. View Article : Google Scholar : PubMed/NCBI
12	Livingstone SJ, Levin D, Looker HC, Lindsay RS, Wild SH, Joss N, Leese G, Leslie P, McCrimmon RJ, Metcalfe W, et al: Estimated life expectancy in a Scottish cohort with type 1 diabetes, 2008–2010. JAMA. 313:37–44. 2015. View Article : Google Scholar : PubMed/NCBI
13	Xu H, Zhang J, Lei Y, Han Z, Rong D, Yu Q, Zhao M and Tian J: Low frequency pulsed electromagnetic field promotes C2C12 myoblasts proliferation via activation of MAPK/ERK pathway. Biochem Biophys Res Commun. 479:97–102. 2016. View Article : Google Scholar : PubMed/NCBI
14	Liu M, Lee C, Laron D, Zhang N, Waldorff EI, Ryaby JT, Feeley B and Liu X: Role of pulsed electromagnetic fields (PEMF) on tenocytes and myoblasts-potential application for treating rotator cuff tears. J Orthop Res. 35:956–964. 2017. View Article : Google Scholar : PubMed/NCBI
15	Tucker JJ, Cirone JM, Morris TR, Nuss CA, Huegel J, Waldorff EI, Zhang N, Ryaby JT and Soslowsky LJ: Pulsed electromagnetic field therapy improves tendon-to-bone healing in a rat rotator cuff repair model. J Orthop Res. 35:902–909. 2017. View Article : Google Scholar : PubMed/NCBI
16	Fricke O, Seewi O, Semler O, Tutlewski B, Stabrey A and Schoenau E: The influence of auxology and long-term glycemic control on muscle function in children and adolescents with type 1 diabetes mellitus. J Musculoskelet Neuronal Interact. 8:188–195. 2008.PubMed/NCBI
17	Junod A, Lambert AE, Stauffacher W and Renold AE: Diabetogenic action of streptozotocin: Relationship of dose to metabolic response. J Clin Invest. 48:2129–2139. 1969. View Article : Google Scholar : PubMed/NCBI
18	Li RJ, Qiu SD, Tian H and Zhou SW: Diabetes induced by multiple low doses of STZ can be spontaneously recovered in adult mice. Dongwuxue Yanjiu. 34:238–243. 2013.(In Chinese). PubMed/NCBI
19	Tsai CC, Chan P, Chen LJ, Chang CK, Liu Z and Lin JW: Merit of ginseng in the treatment of heart failure in type 1-like diabetic rats. Biomed Res Int. 2014:4841612014. View Article : Google Scholar : PubMed/NCBI
20	Lewis MI, Fournier M, Wang H, Storer TW, Casaburi R and Kopple JD: Effect of endurance and/or strength training on muscle fiber size, oxidative capacity, and capillarity in hemodialysis patients. J Appl Physiol (1985). 119:865–871. 2015. View Article : Google Scholar : PubMed/NCBI
21	Eprintsev AT, Falaleeva MI, Lyashchenko MS, Gataullinaa MO and Kompantseva EI: Isoformes of malate dehydrogenase from rhodovulum steppense A-20s grown chemotrophically under aerobic condtions. Prikl Biokhim Mikrobiol. 52:168–173. 2016.PubMed/NCBI
22	Chen V and Ianuzzo CD: Metabolic alterations in skeletal muscle of chronically streptozotocin-diabetic rats. Arch Biochem Biophys. 217:131–138. 1982. View Article : Google Scholar : PubMed/NCBI
23	Ianuzzo CD and Armstrong RB: Phosphofructokinase and succinate dehydrogenase activities of normal and diabetic rat skeletal muscle. Horm Metab Res. 8:244–245. 1976. View Article : Google Scholar : PubMed/NCBI
24	Cai F: Studies of enzyme histochemistry and ultrastructure of the myocardium in rats with streptozotocin-induced diabetes. Zhonghua Yi Xue Za Zhi. 69276–278. (20)1989.(In Chinese). PubMed/NCBI
25	Jia Q, Ma S, Liu X, Li S, Wang Y, Gao Q and Yang R: Effects of hydrogen sulfide on contraction capacity of diaphragm from type 1 diabetic rats. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 41:496–501. 2016.(In Chinese). PubMed/NCBI
26	Lee SJ: Sprinting without myostatin: A genetic determinant of athletic prowess. Trends Genet. 23:475–477. 2007. View Article : Google Scholar : PubMed/NCBI
27	Rebbapragada A, Benchabane H, Wrana JL, Celeste AJ and Attisano L: Myostatin signals through a transforming growth factor beta-like signaling pathway to block adipogenesis. Mol Cell Biol. 23:7230–7242. 2003. View Article : Google Scholar : PubMed/NCBI
28	Lee SJ: Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol. 20:61–86. 2004. View Article : Google Scholar : PubMed/NCBI
29	Jeong J, Conboy MJ and Conboy IM: Pharmacological inhibition of myostatin/TGF-β receptor/pSmad3 signaling rescues muscle regenerative responses in mouse model of type 1 diabetes. Acta Pharmacol Sin. 34:1052–1060. 2013. View Article : Google Scholar : PubMed/NCBI
30	Sriram S, Subramanian S, Juvvuna PK, McFarlane C, Salerno MS, Kambadur R and Sharma M: Myostatin induces DNA damage in skeletal muscle of streptozotocin-induced type 1 diabetic mice. J Biol Chem. 289:5784–5798. 2014. View Article : Google Scholar : PubMed/NCBI
31	Glass DJ: Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol. 37:1974–1984. 2005. View Article : Google Scholar : PubMed/NCBI
32	Leger B, Cartoni R, Praz M, Lamon S, Dériaz O, Crettenand A, Gobelet C, Rohmer P, Konzelmann M, Luthi F and Russell AP: Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol. 576:923–933. 2006. View Article : Google Scholar : PubMed/NCBI
33	Dang K, Li YZ, Gong LC, Xue W, Wang HP, Goswami N and Gao YF: Stable atrogin-1 (Fbxo32) and MuRF1 (Trim63) gene expression is involved in the protective mechanism in soleus muscle of hibernating Daurian ground squirrels (Spermophilus dauricus). Biol Open. 5:62–71. 2016. View Article : Google Scholar : PubMed/NCBI
34	Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ and Yancopoulos GD: Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol. 3:1014–1019. 2001. View Article : Google Scholar : PubMed/NCBI
35	Hoffman EP and Nader GA: Balancing muscle hypertrophy and atrophy. Nat Med. 10:584–585. 2004. View Article : Google Scholar : PubMed/NCBI
36	Rodriguez J, Vernus B, Chelh I, Cassar-Malek I, Gabillard JC, Sassi Hadj A, Seiliez I, Picard B and Bonnieu A: Myostatin and the skeletal muscle atrophy and hypertrophy signaling pathways. Cell Mol Life Sci. 71:4361–4371. 2014. View Article : Google Scholar : PubMed/NCBI
37	Kamei Y, Miura S, Suzuki M, Kai Y, Mizukami J, Taniguchi T, Mochida K, Hata T, Matsuda J, Aburatani H, et al: Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem. 279:41114–41123. 2004. View Article : Google Scholar : PubMed/NCBI
38	Bonaldo P and Sandri M: Cellular and molecular mechanisms of muscle atrophy. Dis Model Mech. 6:25–39. 2013. View Article : Google Scholar : PubMed/NCBI
39	Zhang J, Zhuang P, Wang Y, Song L, Zhang M, Lu Z, Zhang L, Wang J, Alemu PN, Zhang Y, et al: Reversal of muscle atrophy by Zhimu-Huangbai herb-pair via Akt/mTOR/FoxO3 signal pathway in streptozotocin-induced diabetic mice. PLoS One. 9:e1009182014. View Article : Google Scholar : PubMed/NCBI
40	Patterson TE, Sakai Y, Grabiner MD, Ibiwoye M, Midura RJ, Zborowski M and Wolfman A: Exposure of murine cells to pulsed electromagnetic fields rapidly activates the mTOR signaling pathway. Bioelectromagnetics. 27:535–544. 2006. View Article : Google Scholar : PubMed/NCBI