Electrical stimulation delays reinnervation in denervated rat muscle
Clara M. Pinheiro-Dardis PhD
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Search for more papers by this authorBruna T. Erbereli PT
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Search for more papers by this authorDavilene Gigo-Benato PhD
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Search for more papers by this authorPaula A.T.S. Castro PhD
Laboratory of Muscle Plasticity, DFisio, UFSCar, São Carlos, São Paulo, Brazil
Search for more papers by this authorCorresponding Author
Thiago L. Russo PhD
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Correspondence to: T. L. Russo; e-mail: [email protected]Search for more papers by this authorClara M. Pinheiro-Dardis PhD
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Search for more papers by this authorBruna T. Erbereli PT
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Search for more papers by this authorDavilene Gigo-Benato PhD
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Search for more papers by this authorPaula A.T.S. Castro PhD
Laboratory of Muscle Plasticity, DFisio, UFSCar, São Carlos, São Paulo, Brazil
Search for more papers by this authorCorresponding Author
Thiago L. Russo PhD
Fisioterapia Neurológica (LaFiN), Departamento de Fisioterapia, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luis, Km 235, C.P. 676 – CEP: 13565-905, São Carlos, SP, Brazil
Correspondence to: T. L. Russo; e-mail: [email protected]Search for more papers by this authorFunding: This study was supported by FAPESP (2013/21321-6) and CAPES.
Conflicts of Interest: None of the authors has any conflict of interest to disclose.
ABSTRACT
Introduction
It is not clear if electrical stimulation (ES) can affect muscle reinnervation. This study aimed to verify if ES affects neuromuscular recovery after nerve crush injury in rats.
Methods
Denervated muscles were electrically stimulated daily for 6 or 14 days. Neuromuscular performance and excitability, and muscle morphology were determined. Muscle trophism markers (atrogin-1, MuRF-1, and myoD), as well as neuromuscular junction (NMJ) organization (muscle-specific receptor tyrosine kinase [MuSK], cytoplasmic protein downstream of kinase-7 [Dok-7], nicotinic ACh receptor [nAChR], and neural cell adhesion molecule [N-CAM]) were assessed.
Results
ES impaired neuromuscular recovery at day 14 postdenervation. Muscle hypoexcitability was accentuated by ES at 6 and 14 days postdenervation. Although ES reduced the accumulation of atrogin-1, MuRF1, and myoD mRNAs, it increased muscle atrophy. Gene expression of MuSK, Dok-7, nAChR, and the content of N-CAM protein were altered by ES.
Discussion
ES can delay the reinnervation process by modulating factors related to NMJ stability and organization, and inducing dysfunction, hypoexcitability, and muscle atrophy. Muscle Nerve 56: E108–E118, 2017
Supporting Information
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REFERENCES
- 1 Scaakxs D, Kalbermatten DF, Raffoul W, Wiberg M, Kingham PJ. Regenerative cell injection in denervated muscle reduces atrophy and enhances recovery following nerve repair. Muscle Nerve 2013; 47: 691–701.
- 2 Russo TL, Peviani SM, Durigan JLQ, Gigo-Benato D, Delfino GB, Salvini TF. Stretching and electrical stimulation reduce the accumulation of MyoD, myostatin and atrogin-1 in denervated rat skeletal muscle. J Muscle Res Cell Motil 2010; 31: 45–57.
- 3 Wood MD, Kemp SWP, Wrber C, Borschel GH, Gordon T. Outcome measures of peripheral nerve regeneration. Ann Anat 2011; 193: 321–333.
- 4 Malomouzh AI. Non-cholinergic signaling pathways at vertebrate neuromuscular junctions. In: J Cseri. editor. Skeletal muscle: from myogenesis to clinical relations. Kazan: InTech; 2012. 380 p.
- 5 Dow DE, Cederna PS, Hassett CA, Kostrominova TY, Faulkner JA, Dennis RG. Number of contractions to maintain mass and for of a denervated rat muscle. Muscle Nerve 2004; 30: 77–86.
- 6 Gordon T, Amirjani N, Edwards DC, Chan KM. Brief post-surgical electrical stimulation accelerates axon regeneration and muscle reinnervation without affecting the functional measures in carpal tunnel. Exp Neurol 2010; 223: 192–201.
- 7 Russo TL, Peviani SM, Durigan JLQ, Salvini TF. Electrical stimulation increases matrix metalloproteinase -2 gene expression but does not change its activity in denervated rat muscle. Muscle Nerve 2008; 37: 45–57.
- 8 Gigo-Benato D, Russo TL, Geuna S, Domingues NRSR, Salvini TF, Parizotto NA. Electrical stimulation impairs early functional recovery and accentuates skeletal muscle atrophy after sciatic nerve crush injury in rats. Muscle Nerve 2010; 41: 685–693.
- 9 Dow DE, Cederna PS, Hasset CA, Dennis RG, Faulkner JA. Electrical stimulation prior to delayed reinnervation does not enhance recovery in muscles of rats. Restor Neurol Neurosci 2007; 25: 601–610.
- 10 Willand MP, Chiang CD, Zhang JJ, Kemp SWP, Borschel GH, Gordon T. Daily Electrical muscle stimulation enhances functional recovery following nerve transection and repair in rats. Neurorehabil Neural Repair 2015; 29: 690–700.
- 11 Sinis N, Horn F, Genchev B, Skouras E, Merkel D, Angelova SK, et al. Electrical stimulation of paralyzed vibrissal muscles reduces endplate reinnervation and does not promote motor recovery after facial nerve repair in rats. Ann Anat 2009; 191: 356–370.
- 12 Tam SL, Gordon T. Neuromuscular activity impairs axonal sprouting in partially denervated muscles by inhibiting bridge formation of perisynaptic schwann cells. J Neurobiol 2003; 57: 221–234.
- 13 Salmons S, Ashley Z, Sutherland H, Russold MF, Li F, Jarvis JC. Functional electrical stimulation of denervated muscle: basic issues. Artif Organs 2005; 29: 199–201.
- 14 Changeux JP, Edelstein SJ. Allosteric receptors after 30 years review. Neuron 1998; 21: 959–980.
- 15
Lindstrom JM. Acetylcholine receptors and myasthenia. Muscle Nerve 2000; 23: 453–477.
10.1002/(SICI)1097-4598(200004)23:4<453::AID-MUS3>3.0.CO;2-O CAS PubMed Web of Science® Google Scholar
- 16 Ma J, Shen J, Garrett JP, Lee CA, Zhongyu L, Elsaidi GA, et al. Gene expression of myogenic regulatory factors, nicotinic acetylcholine receptor subunits, and GAP-43 in skeletal muscle following denervation in a rat model. J Orthop Res 2007; 25: 1498–1505.
- 17 DeChiara TM, Bowen DC, Valenzuela DM, Simmons MV, Poueymirou WT, Thomas S, et al. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 1996; 85: 501–512.
- 18 Okada K, Inoue A, Okada M, Murata Y, Kakuta S, Jigami T, et al. The muscle protein DoK-7 is essential for neuromuscular synaptogenesis. Science 2006; 312: 1802–1805.
- 19 Polo-Parada L, Bose CM, Landmesser LT. Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions. Neuron 2001; 32: 815–828.
- 20 Vitureira N, Letellier M, White IJ, Goda Y. Differential control of presynaptic efficacy by postsynaptic N-cadherin and β-catenin. Nat Neurosci 2012; 15: 81–89.
- 21 Chipman PH, Schachner M, Rafuse VF. Presynaptic NCAM is required for motor neurons to functionally expand their peripheral field of innervation in partially denervated muscles. J Neurosci 2014; 34: 10497–10510.
- 22 Enriquez-Barreto L, Palazzetti C, Brennaman LH, Maness PF, Fairén A. Neural cell adhesion molecule, NCAM, regulates thalamocortical axon pathfinding and the organization of the cortical somatosensory representation in mouse. Front Mol Neurosci 2012; 5: 76.
- 23 Chattopadhyaya B, Baho E, Huang ZJ, Schachner M, Di Cristo G. Neural cell adhesion molecule-mediated Fyn activation promotes GABAergic synapse maturation in postnatal mouse cortex. J Neurosci 2013; 33: 5957–5968.
- 24 Jackman RW, Kandarian SC. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol 2004; 287: C834–C843.
- 25 Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, et al. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 2001; 294: 1704–1708.
- 26 Bodine SC. Disuse-induced muscle wasting. Int J Biochem Cell Biol 2013; 45: 2200–2208.
- 27 Bodine SC, Baehr LM. Skeletal muscle atrophy and the E3 ubiquitin ligases MuRF1 and MAFbx/atrogin-1. Am J Physiol Endocrinol Metab 2014; 307: E469–E484.
- 28 Russo TL, França C, Castro C, Salvini TF. Alterations of chronaxie, rheobase and accommodation in denervated skeletal muscle submitted to electrical stimulation. Rev Bras Fisioter 2004; 8: 169–175.
- 29 Cummigs J. Electrical stimulation in denervated muscle. In: M Gersh, editor Electrotheraphy in rehabilitation, 3rd ed. New York: Churchill Livingstone; 1990. p 269–290.
- 30 Kostrominova TY, Dow DE, Dennis RG, Miller RA, Faulkner JA. Comparison of gene expression of 2-mo denervated, 2-mo stimulated-denervated and control rat skeletal muscles. Physiol Genomics 2005; 22: 227–243.
- 31 Pinheiro-Dardis CM, Russo TL. Electrical stimulation based on chronaxie increases fibrosis and modulates TWEAK/Fn14, TGF-β/myostatin and MMP pathways in denervated muscles. Am J Phys Med Rehabil 2016. [Epub ahead of print].
- 32 Ramirez C, Russo TL, Sandoval MC, Dentillo AA, Silva-Couto MA, Durigan JLQ, et al. Joint inflammation alters gene and protein expression and leads to atrophy in the tibialis anterior muscle in rats. Am J Phys Med Rehabil 2011; 90: 930–939.
- 33 Adams CM, Suneja M, Dudley-Javoroski S, Shields RK. Altered mRNA expression after long-term soleus electrical stimulation training in humans with paralysis. Muscle Nerve 2011; 43: 65–75.
- 34 Fujita N, Murakami S, Fujino H. The combined effect of electrical stimulation and hugh-load isometric contraction on protein degradation pathways in muscle atrophy induced by hindlimb unloading. J Biomed Biotechnol 2011; 2011: 401493.
- 35 Dow DE, Carlson BM, Hassetta CA, Dennis RG, Faulkner JA. Electrical stimulation of denervated muscles of rats maintains mass and force, but not recovery following grafting. Restor Neurol Neurosci 2006; 24: 41–54.
- 36 Tomori K, Ohta Y, Nishizawa T, Tamaki H, Takekura H. Low-intensity electrical stimulation ameliorates disruption of transverse tubules and neuromuscular junctional architecture in denervated rat skeletal muscle fibers. J Muscle Res Cell Motil 2010; 31: 195–205.
- 37 Pieber K, Herceg M, Paternostro-Sluga T, Schuhfried O. Optimizing stimulation parameter in functional electrical stimulation of denervated muscles: a cross-sectional study. J Neuroeng Rehabil 2015; 12: 51.
- 38 Geuna S, Raimondo S, Ronchi G, Di Scipio F, Tos P, Czaja K, et al. Chapter 3: histology of the peripheral nerve and changes occurring during nerve regeneration. Int Rev Neurobiol 2009; 87: 27–46.
- 39 Willand MP, Holmes MB, Bain JR, Fahnestock M, De Bruin H. Electrical muscle stimulation after immediate nerve repair reduces muscle atrophy without affecting reinnervation. Muscle Nerve 2013; 48: 219–225.
- 40 Elzinga K, Tyreman N, Ladak A, Savaryn B, Olson J, Gordon T. Brief electrical stimulation improves nerve regeneration after delayed. Exp Neurol 2015; 269: 142–153.
- 41 Assis DCM, Lima EM, Goes BT, Cavalcanti JZ, Paixão AB, Vaniier-Santos MA, et al. The parameters o transcutaneous electrical nerve stimulation are critical to its regenerative effects when applied just after a sciatic crush lesion in mice. Biomed Res Int 2014; 2014: 1–8.
- 42 Tintignac LA, Brenner H-R, Ruegg MA. Mechanisms regulating neuromuscular junction development and function and causes of muscle wasting. Physiol Rev 2015; 95: 809–852.
- 43 Perez-Garcia MJ, Burden SJ. Increasing MuSK activity delays denervation and improves motor function in ALS mice. Cell Rep 2012; 2: 497–502.
- 44 Zhang HL, Peng HB. Mechanism of acetylcholine receptor cluster formation induced by DC electric field. PLoS One 2011; 6: e26805.