Passive training improves the recovery of skeletal muscle structure and function in rats with denervated muscle atrophy

doi:10.3969/j.issn.2095-4344.2862

Abstract

Abstract:

BACKGROUND: Inflammatory cells or inflammatory factors participate in the proliferation and differentiation of skeletal muscle satellite cells after denervation injury, and play an important role in the pathological process of skeletal muscle denervation.

OBJECTIVE: To study the effects of passive training on skeletal muscle structure, function and expression of Actin and inflammatory factors in rats with denervated muscle atrophy.

METHODS: Thirty Sprague-Dawley rats were randomly divided into sham operation group, model group and training group. In the model group and the training group, the sciatic nerve was exposed and cut off the sciatic nerve, while the sciatic nerve in the sham operation group was exposed but not cut off. Two months after modeling, rats in the training group underwent passive rehabilitation training with self-made drum for 2 months, and then the degree of muscle atrophy and motor function were evaluated by muscle wet weight ratio and Basso, Beattie and Bresnahan score. The muscle fiber fine structure and cross-sectional area were observed by hematoxylin-eosin staining, and the expression of Actin, tumor necrosis factor-α, interleukin-6 and interleukin-1β in each group was detected by immunohistochemical staining. The study protocol was approved by the Laboratory Animal Welfare Ethics Committee of Shenyang Medical College with the approval No. SYYXY2015010601.

RESULTS AND CONCLUSION: The Basso, Beattie and Bresnahan score of the training group was higher than that of the model group. The wet weight ratio of the training group was higher than that of the model group; however, the cross-sectional area of the muscle fibers was lower than that of the model group (P < 0.001, P < 0.05). The expression of Actin in the training group was higher than that in the model group (P < 0.001), and the expression levels of tumor necrosis factor-α, interleukin-6 and interleukin-1β in the training group were lower than those in the model group (P < 0.001 or P < 0.05). To conclude, passive training can help to recover the muscle structure and function of denervated muscles, reduce the levels of inflammatory factors, prevent further muscle atrophy, and improve skeletal muscle strength.

Key words: passive training, nerve, denervated, skeletal muscle, muscle atrophy, factor, experiment, rat

CLC Number:

Wang Shiyang, Sun Huizhe, Yan Nan, Wang Xiaojie, Zhang Hongxin, Guan Lili, Li Fenjie, Wang Zhengdong. Passive training improves the recovery of skeletal muscle structure and function in rats with denervated muscle atrophy[J]. Chinese Journal of Tissue Engineering Research, 2020, 24(32): 5138-5144.

Figures/Tables 6

References

[1] BOSKOVSKI MT, THOMSON JG. Carpal tunnel syndrome, syndrome of partial thenar atrophy, and W. Russell Brain: a historical perspective. J Hand Surg Am. 2014;39(9): 1822-1829 e1.

[2] JUNQUERA L, GALLEGO L.Images in clinical medicine. Denervation atrophy of the tongue after hypoglossal-nerve injury. N Engl J Med. 2012;367(2):156.

[3] NADERI J, BERNREUTHER C, GRABINSKI N. Plasminogen activator inhibitor type 1 up-regulation is associated with skeletal muscle atrophy and associated fibrosis. Am J Pathol. 2009;175(2):763-771.

[4] AGUERA E, CASTILLA S, LUQUE E.Denervated muscle extract promotes recovery of muscle atrophy through activation of satellite cells. An experimental study. J Sport Health Sci. 2019;8(1):23-31.

[5] GIGER JM, BODELL PW, ZENG M. Rapid muscle atrophy response to unloading: pretranslational processes involving MHC and actin. J Appl Physiol (1985). 2009;107(4): 1204-1212.

[6] WADA E, TANIHATA J, IWAMURA A.Treatment with the anti-IL-6 receptor antibody attenuates muscular dystrophy via promoting skeletal muscle regeneration in dystrophin-/utrophin-deficient mice. Skelet Muscle. 2017; 7(1):23.

[7] WEI J, LIANG BS. PPM1B and P-IKKbeta expression levels correlated inversely with rat gastrocnemius atrophy after denervation. Braz J Med Biol Res.2012;45(8): 711-715.

[8] HILLEN BK, YAMAGUCHI GT, ABBAS JJ, et al. Joint-specific changes in locomotor complexity in the absence of muscle atrophy following incomplete spinal cord injury. J Neuroeng Rehabil. 2013;10:97.

[9] MA W, ZHANG R, HUANG Z, et al. PQQ ameliorates skeletal muscle atrophy, mitophagy and fiber type transition induced by denervation via inhibition of the inflammatory signaling pathways. Ann Transl Med.2019;7(18): 440.

[10] JIANG GL, GU YD, ZHANG LY. Randomized, double-blind, and placebo-controlled trial of clenbuterol in denervated muscle atrophy. ISRN Pharm. 2011;2011:981254.

[11] HORII N, UCHIDA M, HASEGAWA N. Resistance training prevents muscle fibrosis and atrophy via down-regulation of C1q-induced Wnt signaling in senescent mice. FASEB J. 2018;32(7):3547-3559.

[12] HUANG Z, FANG Q, MA W. Skeletal Muscle Atrophy Was Alleviated by Salidroside Through Suppressing Oxidative Stress and Inflammation During Denervation. Front Pharmacol. 2019;10:997.

[13] WENG J, WANG YH, LI M, et al. GSK3β inhibitor promotes myelination and mitigates muscle atrophy after peripheral nerve injury. Neural Regen Res. 2018;13(2):324-330.

[14] 李枚原,薛成斌,韦中亚.大鼠失神经支配后比目鱼肌和趾长伸肌超微结构变化的实验研究[J].交通医学,2011,25(2):107-109.

[15] 董进,柯棠山,刘坤祥.大鼠失神经不同时相的骨骼肌形态和MyoD表达变化[J].现代医药卫生. 2015,36(8):1124-6+30.

[16] SZCZEPANOWSKA J, BOROVIKOV YS, JAKUBIEC-PUKA A. Effects of denervation and muscle inactivity on the organization of F-actin. Muscle Nerve. 1998;21(3):309-317.

[17] RILEY DA, BAIN JL, THOMPSON JL. Disproportionate loss of thin filaments in human soleus muscle after 17-day bed rest. Muscle Nerve. 1998;21(10):1280-1289.

[18] TAMAKI H, YOTANI K, OGITA F. Electrical Stimulation of Denervated Rat Skeletal Muscle Ameliorates Bone Fragility and Muscle Loss in Early-Stage Disuse Musculoskeletal Atrophy. Calcif Tissue Int. 2017;100(4):420-430.

[19] THEILEN NT, JEREMIC N, WEBER GJ. Exercise preconditioning diminishes skeletal muscle atrophy after hindlimb suspension in mice. J Appl Physiol (1985). 2018; 125(4):999-1010.

[20] NAKAGAWA K, TAMAKI H, HAYAO K. Electrical Stimulation of Denervated Rat Skeletal Muscle Retards Capillary and Muscle Loss in Early Stages of Disuse Atrophy. Biomed Res Int. 2017;2017:5695217.

[21] FINNI T, HODGSON JA, LAI AM. Mapping of movement in the isometrically contracting human soleus muscle reveals details of its structural and functional complexity. J Appl Physiol (1985). 2003;95(5):2128-2133.

[22] HADDAD F, ZALDIVAR F, COOPER DM. IL-6-induced skeletal muscle atrophy. J Appl Physiol (1985). 2005;98(3): 911-917.

[23] MA W, ZHANG R, HUANG Z. PQQ ameliorates skeletal muscle atrophy, mitophagy and fiber type transition induced by denervation via inhibition of the inflammatory signaling pathways. Ann Transl Med. 2019;7(18):440.

[24] WU C, TANG L, NI X. Salidroside Attenuates Denervation-Induced Skeletal Muscle Atrophy Through Negative Regulation of Pro-inflammatory Cytokine. Front Physiol. 2019;10:665.

[25] AL-NASSAN S, FUJITA N, KONDO H. Chronic Exercise Training Down-Regulates TNF-alpha and Atrogin-1/MAFbx in Mouse Gastrocnemius Muscle Atrophy Induced by Hindlimb Unloading. Acta Histochem Cytochem. 2012;45(6):343-349.

[26] HE Q, QIU J, DAI M. MicroRNA-351 inhibits denervation-induced muscle atrophy by targeting TRAF6. Exp Ther Med. 2016;12(6):4029-4034.

[27] ZHOU L, HUANG Y, XIE H. Buyang Huanwu Tang improves denervation-dependent muscle atrophy by increasing ANGPTL4, and increases NF-kappaB and MURF1 levels. Mol Med Rep. 2018;17(3):3674-3680.

[28] OBERBACH A, LEHMANN S, KIRSCH K. Long-term exercise training decreases interleukin-6 (IL-6) serum levels in subjects with impaired glucose tolerance: effect of the -174G/C variant in IL-6 gene. Eur J Endocrinol. 2008;159(2): 129-136.

[29] MAMMEN AL, SARTORELLI V. IL-6 Blockade as a Therapeutic Approach for Duchenne Muscular Dystrophy. EBioMedicine. 2015;2(4):274-275.

[30] MIYAGI MY, SEELAENDER M, CASTOLDI A. Long-term aerobic exercise protects against cisplatin-induced nephrotoxicity by modulating the expression of IL-6 and HO-1. PLoS One. 2014;9(10):e108543.

[31] MADARO L, PASSAFARO M, SALA D. Denervation-activated STAT3-IL-6 signalling in fibro-adipogenic progenitors promotes myofibres atrophy and fibrosis. Nat Cell Biol. 2018; 20(8):917-927.

[32] SISHI BJ, ENGELBRECHT AM. Tumor necrosis factor alpha (TNF-alpha) inactivates the PI3-kinase/PKB pathway and induces atrophy and apoptosis in L6 myotubes. Cytokine. 2011;54(2):173-184.

[33] KERN H, HOFER C, LOEFLER S. Atrophy, ultra-structural disorders, severe atrophy and degeneration of denervated human muscle in SCI and Aging. Implications for their recovery by Functional Electrical Stimulation, updated 2017. Neurol Res. 2017;39(7):660-666.

[34] IMASAKA K I, TOMITA Y, NISHIJIMA T, et al. Pectoral Muscle Atrophy After Axillary Artery Cannulation for Aortic Arch Surgery . Semin Thorac Cardiovasc Surg.2019; 31(3): 414-21.

[35] HAMANO N, YAMAMOTO A, SHITARA H, et al. Does successful rotator cuff repair improve muscle atrophy and fatty infiltration of the rotator cuff? A retrospective magnetic resonance imaging study performed shortly after surgery as a reference. J Shoulder Elbow Surg.2017;26(6): 967-974.

[36] RUVEN C, LI W, LI H, et al. Transplantation of Embryonic Spinal Cord Derived Cells Helps to Prevent Muscle Atrophy after Peripheral Nerve Injury. Int J Mol Sci.2017;18(3):

[37] GU S, SHEN Y, XU W, et al. Application of fetal neural stem cells transplantation in delaying denervated muscle atrophy in rats with peripheral nerve injury. Microsurgery.2010;30(4): 266-274.

[38] ZHANG PX, HAN N, KOU YH, et al. Tissue engineering for the repair of peripheral nerve injury. Neural Regen Res. 2019; 14(1):51-58.

[39] MOIMAS S, NOVATI F, RONCHI G, et al. Effect of vascular endothelial growth factor gene therapy on post-traumatic peripheral nerve regeneration and denervation-related muscle atrophy. Gene Ther.2013; 20(10): 1014-1021.

[40] SCHAKMAN O, THISSEN J P. Gene therapy with anabolic growth factors to prevent muscle atrophy. Curr Opin Clin Nutr Metab Care.2006; 9(3): 207-13.

[41] ITOH Y, MURAKAMI T, MORI T, et al. Training at non-damaging intensities facilitates recovery from muscle atrophy. Muscle Nerve.2017; 55(2): 243-253.

[42] PANISSET M G, GALEA M P, EL-ANSARY D. Does early exercise attenuate muscle atrophy or bone loss after spinal cord injury?. Spinal Cord.2016;54(2): 84-92.

[43] RABELO M, DE MOURA JUCA R V B, LIMA L A O, et al. Overview of FES-Assisted Cycling Approaches and Their Benefits on Functional Rehabilitation and Muscle Atrophy. Adv Exp Med Biol.2018;1088:561-583.