Relationship between calcium circulation-related factors and muscle strength in rat sciatic nerve injury model

Document Type : Original Article

Authors

Department of Forensic Medicine, Xuzhou Medical University, Xuzhou, Jiangsu, P. R. China

Abstract

Objective(s): The purpose of this study is to investigate the indication function of the calcium circulation-related factors on the damage to muscle strength and contraction function after nerve injury. The target factors include ryanodine receptor (RyR), inositol-1,4,5-triphosphate receptor (IP3R), phospholamban (PLN), cryptocalcitonin (CASQ), ATPase and troponin C (TNNC).
Materials and Methods: Sprague-Dawley (SD) rats were randomly divided into sham-operated group (SO), sciatic nerve injury group (SNI) and sciatic nerve disconnection group (SNT). Sciatic nerve function index and stretching test were used to examine the changes to muscle strength; bilateral gastrocnemius muscles were extracted after execution for gastrocnemius wet weight ratio test. HE staining slides and average cross-sectional area of muscle fibers were acquired to analyze the muscle atrophy. The transcription level of the factors was also measured.
Results: Sciatic nerve damage in SNI group was significantly higher than that in SO group in the 6 weeks, but there was no significant difference between SNT and SO groups fallowing sciatic nerve damage. Sciatic nerve function in SNT group was worse than that in SNI group. The average cross-sectional area of gastrocnemius muscle fibers in SNI and SNT groups was significantly reduced compared to that in SO group. The transcriptional levels of RyR, PLN, CASQ, ATPase and TNNC in SNI and SNT groups were significantly different from those in SO group.
Conclusion: Calcium circulation-related factors could be used as potential indicators for assessment of damages to muscle strength.

Keywords


1. Enger M, Skjaker SA, Nordsletten L, Pripp AH, Melhuus K, Moosmayer S, Brox JI. Sports-related acute shoulder injuries in an urban population. BMJ Open Sport Exerc Med 2019; 5: e000551.
2.Steinbacher P, Eckl P. Impact of oxidative stress on exercising skeletal muscle. Biomolecules 2015; 5: 356-377.
3.Miller MS, Bedrin NG, Ades PA, Palmer M, Toth MJ. Molecular determinants of force production in human skeletal muscle fibers: effects of myosin isoform expression and cross-sectional area. Am J Physiol Cell Physiol 2015; 308: C473.
4. Setiyowati YD, Wang ST, Chen HM. Thermotherapy combined with therapeutic exercise improves muscle strength and depression in patients with ischemic stroke. Rehabil Nurs 2019;44:254-262.
5. Mentiplay BF, Tan D, Williams G, Adair B, Pua YH, Bower KJ, et al Assessment of isometric muscle strength and rate of torque development with hand-held dynamometry: Test-retest reliability and relationship with gait velocity after stroke. Journal of biomechanics 2018; 75: 171-175.
6. Frontera W R, Ochala J. Skeletal Muscle: A brief review of structure and function. Calcif Tissue Int 2015; 96: 183-195.
7. Berry DB, Regner B, Galinsky V, Ward SR, Frank LR. Relationships between tissue microstructure and the diffusion tensor in simulated skeletal muscle. Magn Reson Med 2018; 80:317-329.
8.Gong H, Liu L, Jiang CL. Progress in the study of C2C12 cell contraction model and its contractile function. Chin J Sport Med 2015; 34: 78-81.
9. Nozdrenko DM, Miroshnychenko MS, Soroca VM, Korchins ka LV, Zavodovskiy DO. The effect of chlorpyrifos upon ATPase activity of sarcoplasmic reticulum and biomechanics of skeleta l muscle contraction. Ukr Biochem J 2016;88:82-88.
10. Emril DR, Wibowo S, Meliala L, Susilowati R. Cytidine 5’-diphosphocholine administration prevents peripheral neuropathic pain after sciatic nerve crush injury in rats. J Pain Res 2016;9:287-291.
11. Wiberg R, Jonsson S, Novikova LN, Kingham PJ. Investigation of the expression of myogenic transcription factors, microRNAs and muscle-specific E3 ubiquitin ligases in the medial gastrocnemius and soleus muscles following peripheral nerve injury. PLoS One 2015;10:e0142699.
12. Kaczmarek D, Łochyński D, Everaert I, Pawlak M, Derave W, Celichowski J. Role of histidyl dipeptides in contractile function of fast and slow motor units in rat skeletal muscle. J Appl Physiol (1985) 2016;121:164-172.
13. Romero NB. Centronuclear myopathies: a widening concept. Neuromuscular Disorders Nmd 2010; 20: 223-228.
14. Béatrice Chabi, Ljubicic V, Menzies KJ, Huang, JH, Saleem A, Hood DA. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 2007; 7: 2-12.
15. Rassier, Dilson E. Sarcomere mechanics in striated muscles: from molecules to sarcomeres to cells. American journal of physiology. Cell physiology 2017; 313: C134-C145.
16. Järvilehto Matti, Mänttäri Satu. Comparative analysis of mouse skeletal muscle fibre type composition and contractile responses to calcium channel blocker. BMC Physiology 2005; 5: 4.
17. Jayasinghe ID, Munro M, Baddeley D, Launikonis BS, Soeller C. Observation of the molecular organization of calcium release sites in fast- and slow-twitch skeletal muscle with nanoscale imaging. J R Soc Interface 2014;11: pii: 20140570.
18. Barone V, Randazzo D, Del Re V, Sorrentino V, Rossi D. Organization of junctional sarcoplasmic reticulum proteins in skeletal muscle fibers. J Muscle Res Cell Motil 2015; 36: 501-515.
19. Allard B. From excitation to intracellular Ca2+movements in skeletal muscle: Basic aspects and related clinical disorders. Neuromuscul Disord 2018; 28: 394-401.
20. Díaz-Vegas AR, Cordova A, Valladares D, Llanos P, Hidalgo C, Gherardi G, et al. Mitochondrial calcium increase induced by RyR1 and IP3R channel activation after membrane depolarization regulates skeletal muscle metabolism. Front Physiol 2018;9:791.
21. Renganathan M. Caloric restriction prevents age-related decline in skeletal muscle dihydropyridine receptor and ryanodine receptor expression. FEBS letters 1998; 434: 346-350.
22. Thomas MM, Vigna C, Betik AC, Tupling AR, Hepple RT. Initiating treadmill training in late middle age offers modest adaptations in Ca2+ handling but enhances oxidative damage in senescent rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 2010; 298: R1269.
23. Green HJ, Klug GA, Reichmann H, Seedorf U, Wiehrer W, Pette D. Exercise-induced fibre type transitions with regard to myosin, parvalbumin, and sarcoplasmic reticulum in muscles of the rat. Pflügers Arch 1984; 400: 432-438.
24. Periasamy M, Maurya SK, Sahoo SK, Singh S, Sahoo SK, Reis FCG, Bal NC. Role of SERCA pump in muscle thermogenesis and metabolism. Compr Physiol 2017;7:879-890.
25. Hamm NC, Stammers AN, Susser SE, Hlynsky MW, Kimber DE, Kehler DS, et al. The regulation of sarco(endo)plasmic reticulum calcium-ATPases (SERCA). Can J Physiol  Pharmacol 2015; 93: 843-854.
26. Periasamy M, Maurya SK, Sahoo SK, Singh S, Reis FCG, Bal NC. Role of SERCA pump in muscle thermogenesis and metabolism. Compr Physiol2017; 7: 879-890.
27. Fajardo VA, Eric B, Chris V, Tahira D, Darin B, Daniel G, et al. Co-expression of SERCA isoforms, phospholamban and sarcolipin in human skeletal muscle fibers. PLoS ONE 2013; 8: e84304.
28. Asahi M, Kurzydlowski K, Tada M, Maclennan DH. Sarcolipin inhibits polymerization of phospholamban to induce superinhibition of Sarco(endo)plasmic reticulum Ca2+-ATPases (SERCAs). Journal of Biological Chemistry 2002; 277: 26725-26728.
29. Komatsu M, Nakada T, Kawaqishi H, Kato H, Yamada M. Increase in phospholamban content in mouse skeletal muscle after denervation. J Muscle Res Cell Motil 2018; 39: 163-173.
30. Lewis KM, Munske GR, Byrd SS, Kang J, Cho HJ, Ríos E, et al. Characterization of post-translational modifications to calsequestrins of cardiac and skeletal muscle. Int J Mol Sci 2016;17: pii: E1539.
31. Boncompagni S, Protasi F, Franzini-Armstrong C. Sequential stages in the age-dependent gradual formation and accumulation of tubular aggregates in fast twitch muscle fibers: SERCA and calsequestrin involvement. Age (Dordr) 2012;34:27-41.
32. Shen X, Cannell MB, Ward ML. Effect of SR load and pH regulatory mechanisms on stretch-dependent Ca(2+) entry during the slow force response. J Mol Cell Cardiol 2013; 63:37-46.
33. Paolini C, Quarta M, D’Onofrio L, Reggiani C, Protasi F. Differential effect of calsequestrin ablation on structure and function of fast and slow skeletal muscle fibers. J Biomed Biotechnol 2011;2011:634075.
34. Hunter RB, Mitchell-Felton H, Essig DA, Kandarian, SC. Expression of endoplasmic reticulum stress proteins during skeletal muscle disuse atrophy. AJP Cell Physiology 2001; 281: C1285-C1290.
35. Zhang H, Audira G, Li Y, Xian W, Varikkodan MM, Hsiao CD. Comparative study the expression of calcium cycling genes in Bombay duck (Harpadon nehereus) and beltfish (Trichiurus lepturus) with different swimming activities. Genom Data 2017;12:58-61.
36. Gergely J. Professor Ebashi’s impact on the study of the regulation of striated muscle contraction. Mol Cell Biochem 1999; 190: 5-8.
37. Germinario E, Esposito A, Megighian A, Midrio M, Danieli-Betto D. Early changes of type 2B fibers after denervation of rat EDL skeletal muscle. J Appl Physiol 2002; 92: 2045-2052.
38. Leeuw T, Kapp M, Pette D. Role of innervation for development and maintenance of troponin subunit isoform patterns in fast- and slow-twitch muscles of the rabbit. Differentiation 1994; 55: 193-201.
39. Ruegg DG, Kakebeeke TH, Gabriel JP, Bennefeld M. Conduction velocity of nerve and muscle fiber action potentials after a space mission or a bed rest. Clin Neurophysiol 2003; 114: 86-93.
40. Tieland M, Trouwborst I, Clark B C. Skeletal muscle performance and ageing. Journal Cachexia Sarcopenia Muscle 2018; 9:3-19.
41. Ruegg DG, Kakebeeke TH, Gabriel JP, Bennefeld M. Effects of ageing on single muscle fibre contractile function following short-term immobilisation. J Physiol 2011; 589: 4745-4757.
42. Manzano R, Toivonen JM, Calvo AC, Muñoz MJ, Zaragoza P, Osta R. Housekeeping gene expression in myogenic cell cultures from neurodegeneration and denervation animal models. Biochem Biophys Res Commun 2011; 407: 0-763.
43. Nakao R, Yamamoto S, Yasumoto Y, Kadota K, Oishi K. Impact of denervation-induced muscle atrophy on housekeeping gene expression in mice. Muscle Nerve 2015; 51: 276-281.