The ultrastructure of muscle fibers and satellite cells in experimental autoimmune encephalomyelitis after treatment with transcranial magnetic stimulation

References

• Lu DX, Huang SK, Carlson BM. Electron microscopic study of long-term denervated rat skeletal muscle. Anat Rec. 1997;248(3):355–365. doi:10.1002/(SICI)1097-0185(199707)248:3<355:AID-AR8>3.0.CO;2-O.
   PubMedGoogle Scholar
• Borisov AB, Carlson BM. Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat Rec. 2000;258(3):305–318. doi:10.1002/(SICI)1097-0185(20000301)258:3<305::AID-AR10>3.0.CO;2-A.
   PubMedGoogle Scholar
• Borisov AB, Dedkov EI, Carlson BM. Abortive myogenesis in denervated skeletal muscle: differentiative properties of satellite cells, their migration, and block of terminal differentiation. Anat Embryol (Berl). 2005;209(4):269–279. doi:10.1007/s00429-004-0429-7.
   PubMedGoogle Scholar
• de Castro Rodrigues A, Andreo JC, de Mattos Rodrigues SP. Myonuclei and satellite cells in denervated rat muscles: an electron microscopy study. Microsurgery. 2006;26(5):396–398. doi:10.1002/micr.20258.
   PubMed Web of Science ®Google Scholar
• Teixeira NB, Picolo G, Giardini AC, et al. Alterations of peripheral nerve excitability in an experimental autoimmune encephalomyelitis mouse model for multiple sclerosis. J Neuroinflammation. 2020;17(1):266.doi:10.1186/s12974-020-01936-9.
   PubMed Web of Science ®Google Scholar
• Recks MS, Stormanns ER, Bader J, et al. Early axonal damage and progressive myelin pathology define the kinetics of CNS histopathology in a mouse model of multiple sclerosis. Clin Immunol. 2013;149(1):32–45.doi:10.1016/j.clim.2013.06.004.
   PubMed Web of Science ®Google Scholar
• Prinz J, Karacivi A, Stormanns ER, et al. Time-dependent progression of demyelination and axonal pathology in mp4-induced experimental autoimmune encephalomyelitis. PLoS One. 2015;10(12):e0144847.doi:10.1371/journal.pone.0144847.
   PubMed Web of Science ®Google Scholar
• Luque E, Ruz-Caracuel I, Medina FJ, et al. Skeletal muscle findings in experimental autoimmune encephalomyelitis. Pathol Res Pract. 2015;211(7):493–504.doi:10.1016/j.prp.2015.02.004.
   PubMed Web of Science ®Google Scholar
• Muller FL, Song W, Jang YC, et al. Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am J Physiol Regul Integr Comp Physiol. 2007;293(3):R1159–1168.doi:10.1152/ajpregu.00767.2006.
   PubMed Web of Science ®Google Scholar
• Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008;88(4):1243–1276. doi:10.1152/physrev.00031.2007.
   PubMed Web of Science ®Google Scholar
• Wan Q, Yeung SS, Cheung KK, et al. Optimizing electrical stimulation for promoting satellite cell proliferation in muscle disuse atrophy. Am J Phys Med Rehabil. 2016;95(1):28Y38.doi:10.1097/PHM.0000000000000307.
   Web of Science ®Google Scholar
• Agüera E, Castilla S, Luque E, et al. 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. 10.1016/j.jshs.2017.05.007
   PubMed Web of Science ®Google Scholar
• Farup J, Dalgas U, Keytsman C, et al. High intensity training may reverse the fiber type specific decline in myogenic stem cells in multiple sclerosis patients. Front Physiol. 2016;7:193. doi:10.3389/fphys.2016.00193.
   PubMed Web of Science ®Google Scholar
• Chang CW, Lien IN. Tardy effect of neurogenic muscular atrophy by magnetic stimulation. Am J Phys Med Rehabil. 1994;73(4):275–279. doi:10.1097/00002060-199407000-00009.
   PubMed Web of Science ®Google Scholar
• Shimada Y, Sakuraba T, Matsunaga T, et al. Effects of therapeutic magnetic stimulation on acute muscle atrophy in rats after hindlimb suspension. Biomed Res. 2006;27(1):23–27.doi:10.2220/biomedres.27.23.
   PubMed Web of Science ®Google Scholar
• Musarò A, Dobrowolny G, Cambieri C, et al. Neuromuscular magnetic stimulation counteracts muscle decline in ALS patients: results of a randomized, double-blind, controlled study. Sci Rep. 2019;9(1):2837.doi:10.1038/s41598-019-39313-z.
   PubMedGoogle Scholar
• Suzuki K, Ito T, Okada Y, et al. preventive effects of repetitive peripheral magnetic stimulation on muscle atrophy in the paretic lower limb of acute stroke patients: a pilot study. Prog Rehabil Med 2020;5:20200008. 10.2490/prm.20200008
   PubMedGoogle Scholar
• Peña-Toledo MA, Luque E, Ruz-Caracuel I, et al. Transcranial magnetic stimulation improves muscle involvement in experimental autoimmune encephalomyelitis. Int J Mol Sci. 2021;22(16):8589.doi:10.3390/ijms22168589.
   PubMed Web of Science ®Google Scholar
• Medina-Fernandez FJ, Escribano BM, Luque E, et al. Comparative of transcranial magnetic stimulation and other treatments in experimental autoimmune encephalomyelitis. Brain Res Bull. 2018;137:128–145. doi:10.1016/j.brainresbull.2017.11.018.
   Web of Science ®Google Scholar
• Desaki J, Nishida N. Fine structural study of the regeneration of muscle fibers in the rat soleus muscle during aging. J Electron Microsc (Tokyo). 2011;60(2):191–200. doi:10.1093/jmicro/dfr003.
   PubMedGoogle Scholar
• Dubowitz V, Sewry CA, Oldfords A. Muscle Biopsy: A Practical Approach. 5th ed ed. London, UK: Elsevier; 2021:140–182.
   Google Scholar
• Lawson-Smith MJ, McGeachie JK. The identification of myogenic cells in skeletal muscle, with emphasis on the use of tritiated thymidine autoradiography and desmin antibodies. J Anat. 1998;192(Pt 2):161–171. doi:10.1046/j.1469-7580.1998.19220161.x.
   PubMedGoogle Scholar
• Marzani B, Pansarasa O, Marzatico F. “Oxidative stress” and muscle aging: influence of age, sex, fiber composition and function. Basic Appl Myol. 2004;14:37–44.
   Google Scholar
• Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev. 2008;88(4):1243–1276. doi:10.1152/physrev.00031.2007.
   PubMed Web of Science ®Google Scholar
• Siu PM, Alway SE. Response and adaptation of skeletal muscle to denervation stress: the role of apoptosis in muscle loss. Front Biosci. 2009;14(2):432–452. doi:10.2741/3253. Landmark Ed.
   Google Scholar
• Dirks A, Leeuwenburgh C. Apoptosis in skeletal muscle with aging. Am J Physiol Regul Integr Comp Physiol. 2002;282(2):R519–527. doi:10.1152/ajpregu.00458.2001.
   PubMed Web of Science ®Google Scholar
• Tews DS, Goebel HH, Schneider I, et al. DNA-fragmentation and expression of apoptosis-related proteins in experimentally denervated and reinnervated rat facial muscle. Neuropathol Appl Neurobiol. 1997;23(2):141–149. doi:10.1111/j.1365-2990.1997.tb01196.x.
   PubMed Web of Science ®Google Scholar
• Schwartz LM. Skeletal muscles do not undergo apoptosis during either atrophy or programmed cell death-revisiting the myonuclear domain hypothesis. Front Physiol. 2019;9:1887. doi:10.3389/fphys.2018.01887.
   PubMed Web of Science ®Google Scholar
• D’Emilio A, Biagiotti L, Burattini S, et al. Morphological and biochemical patterns in skeletal muscle apoptosis. Histol Histopathol. 2010;25(1):21–32.doi:10.14670/HH-25.21.
   PubMed Web of Science ®Google Scholar
• Jejurikar SS, Marcelo CL, WM K Jr. Skeletal muscle denervation increases satellite cell susceptibility to apoptosis. Plast Reconstr Surg. 2002;110(1):160–168. doi:10.1097/00006534-200207000-00027.
   PubMed Web of Science ®Google Scholar
• Jejurikar SS, WM K Jr. Satellite cell depletion in degenerative skeletal muscle. Apoptosis. 2003;8(6):573–578. doi:10.1023/A:1026127307457.
   PubMed Web of Science ®Google Scholar
• Nakae Y, Stoward PJ, Shono M, et al. Most apoptotic cells in mdx diaphragm muscle contain accumulated lipofuscin. Histochem Cell Biol. 2001;115(3):205–214.doi:10.1007/s004180100250.
   PubMed Web of Science ®Google Scholar
• O’Leary MF, Vainshtein A, Carter HN, et al. Denervation-induced mitochondrial dysfunction and autophagy in skeletal muscle of apoptosis-deficient animals. Am J Physiol Cell Physiol. 2012;303(4):C447–54.doi:10.1152/ajpcell.00451.2011.
   PubMed Web of Science ®Google Scholar
• Carpenter S, Karpati G. Pathology of Skeletal Muscle. 2nd. New York: Oxford University Press; 2001.
   Google Scholar
• De Bleecker JL, Ertl BB, Engel AG. Patterns of abnormal protein expression in target formations and unstructured cores. Neuromuscul Disord. 1996;6(5):339–349. doi:10.1016/0960-8966(96)00369-0.
   PubMed Web of Science ®Google Scholar
• Song T, Sadayappan S. Featured characteristics and pivotal roles of satellite cells in skeletal muscle regeneration. J Muscle Res Cell Motil. 2020; 41(4):341–353. doi:10.1007/s10974-019-09553-7.
   PubMed Web of Science ®Google Scholar
• Schiaffino S, Reggiani C, Akimoto T, et al. Molecular mechanisms of skeletal muscle hypertrophy. J Neuromuscul Dis. 2021;8(2):169–183.doi:10.3233/JND-200568.
   PubMedGoogle Scholar
• Rajasekaran NS, Shelar SB, Jones DP, et al. Reductive stress impairs myogenic differentiation. Redox Biol. 2020;34:101492. doi:10.1016/j.redox.2020.101492.
   PubMed Web of Science ®Google Scholar
• Le Moal E, Pialoux V, Juban G, et al. Redox control of skeletal muscle regeneration. Antioxid Redox Signal. 2017;27(5):276–310.doi:10.1089/ars.2016.6782.
   PubMed Web of Science ®Google Scholar
• Xing H, Zhou M, Assinck P, et al. Electrical stimulation influences satellite cell differentiation after sciatic nerve crush injury in rats. Muscle Nerve. 2015;51(3):400–411.doi:10.1002/mus.24322.
   PubMed Web of Science ®Google Scholar
• Wan Q, Yeung SS, Cheung KK, et al. Optimizing electrical stimulation for promoting satellite cell proliferation in muscle disuse atrophy. Am J Phys Med Rehabil. 2016;95(1):28–38.doi:10.1097/PHM.0000000000000307.
   PubMed Web of Science ®Google Scholar
• Stern-Straeter J, Bonaterra GA, Kassner SS, et al. Impact of static magnetic fields on human myoblast cell cultures. Int J Mol Med. 2011;28(6):907–917. doi:10.3892/ijmm.2011.777.
   PubMed Web of Science ®Google Scholar
• Mueller CE, Birk R, Kramer B, et al. Influence of static magnetic fields on human myoblast/mesenchymal stem cell co‑cultures. Mol Med Rep. 2018;17(3):3813–3820.doi:10.3892/mmr.2017.8334.
   PubMed Web of Science ®Google Scholar
• Bi J, Jing H, Zhou C, et al. Regulation of skeletal myogenesis in C2C12 cells through modulation of Pax7, MyoD, and myogenin via different low-frequency electromagnetic field energies. Technol Health Care. 2022;30(S1):371–382.doi:10.3233/THC-THC228034.
   PubMedGoogle Scholar
• Jimena I, Tasset I, Lopez-Martos R, et al. Effects of magnetic stimulation on oxidative stress and skeletal muscle regeneration induced by mepivacaine in rat. Med Chem. 2009;5(1):44–49.doi:10.2174/157340609787049217.
   PubMed Web of Science ®Google Scholar
• Filippin LI, Cuevas MJ, Lima E, et al. Nitric oxide regulates the repair of injured skeletal muscle. Nitric Oxide. 2011;24(1):43–49.doi:10.1016/j.niox.2010.11.003.
   PubMed Web of Science ®Google Scholar
• Medina-Fernandez FJ, Escribano BM, Agüera E, et al. Effects of transcranial magnetic stimulation on oxidative stress in experimental autoimmune encephalomyelitis. Free Radic Res. 2017;51(5):460–469.doi:10.1080/10715762.2017.1324955.
   PubMed Web of Science ®Google Scholar
• Túnez I, Drucker-Colín R, Jimena I, et al. Transcranial magnetic stimulation attenuates cell loss and oxidative damage in the striatum induced in the 3-nitropropionic model of Huntington’s disease. J Neurochem. 2006;97(3):619–630. doi:10.1111/j.1471-4159.2006.03724.x.
   PubMed Web of Science ®Google Scholar
• Mori F, Ljoka C, Magni E, et al. Transcranial magnetic stimulation primes the effects of exercise therapy in multiple sclerosis. J Neurol. 2011;258(7):1281–1287.doi:10.1007/s00415-011-5924-1.
   PubMed Web of Science ®Google Scholar