C60 FULLERENE HELPS RESTORE MUSCLE SOLEUS CONTRACTION DYNAMICS AFTER ACHILLOTOMY-INDUCED ATROPHY

Dmytro Nozdrenko, Kateryna Bogutska, Іhor Pampuha, Mykola Petrovsky, Yuriy Prylutskyy


DOI: http://dx.doi.org/10.30970/sbi.1804.791

Abstract


Background. The search for new means that would effectively influence the pathological consequences of muscle immobilization is an urgent priority request of modern biomedicine. Previously, the positive effect of water-soluble C60 fullerenes, as strong antioxidants, was established on the background of muscle ischemia, mechanical muscle injury, and other muscle dysfunctions. These carbon nanoparticles have been shown to reliably protect muscle tissue from damage caused by oxidative stress.
Materials and Methods. The biomechanical parameters of muscle soleus contraction of rats were studied by simulating non-functioning hind limbs using a clinical model – a rupture of the Achilles tendon (achillotomy). Muscle contraction parameters, namely the maximum contraction force and muscle force impulse, were determined on the 15th, 30th, and 45th days after initiation of atrophy using tensometry. As a therapeutic nanoagent, daily oral administration of C60 fullerene aqueous solution at a dose of 1 mg/kg was used throughout the experiment.
Results. Previous registration of muscle soleus contraction force when applying 1 Hz stimulation lasting 1800 s with three pools revealed a decrease in maximal force responses after 15, 30, and 45 days of atrophy. The 45th day after atrophy is considered to be the limit for the fastest recovery of the muscle after immobilization, the further process takes place over several months. In all the tests performed, the therapeutic admini­stration of water-soluble C60 fullerenes (dose 1 mg/kg) an increase in biomechanical parameters was recorded (maximum force of contraction – the change in the form of the “stimulation – force contraction” dependence is a consequence of the development of the pathological process in muscle and the muscle force impulse, which allows assessing the performance of the muscular system after a long-term immobilization), by approximately 29–49±2 % for the maximum contraction force and by 21–37±2 % for the muscle force impulse compared to the atrophy group for 15, 30 and 45 days.
Conclusions. The obtained results indicate the prospects of using water-soluble C60 fullerenes, which can alleviate pathological conditions in the muscular system that arise from skeletal muscle atrophy due to immobilization.


Keywords


muscle soleus, atrophy, C60 fullerene, biomechanical parameters of muscle contraction

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References


Appell, H.-J. (1990). Muscular atrophy following immobilization. Sports Medicine, 10(1), 42-58. doi:10.2165/00007256-199010010-00005
CrossrefPubMedGoogle Scholar

Cao, R. Y., Li, J., Dai, Q., Li, Q., & Yang, J. (2018). Muscle atrophy: present and future. In J. Xiao (Ed.), Muscle atrophy. Advances in experimental medicine and biology (Vol. 1088, pp. 605-624). Singapore: Springer. doi:10.1007/978-981-13-1435-3_29
CrossrefPubMedGoogle Scholar

Cozzoli, A., Capogrosso, R. F., Sblendorio, V. T., Dinardo, M. M., Jagerschmidt, C., Namour, F., Camerino, G. M., & De Luca, A. (2013). (2013). GLPG0492, a novel selective androgen receptor modulator, improves muscle performance in the exercised-mdx mouse model of muscular dystrophy. Pharmacological Research, 72, 9-24. doi:10.1016/j.phrs.2013.03.003
CrossrefPubMedGoogle Scholar

Eswaran, S. V. (2018). Water soluble nanocarbon materials: a panacea for all? Current Science, 114(9), 1846-1850. doi:10.18520/cs/v114/i09/1846-1850
CrossrefGoogle Scholar

Gharbi, N., Pressac, M., Hadchouel, M., Szwarc, H., Wilson, S. R., & Moussa, F. (2005). [60] Fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Letters, 5(12), 2578-2585. doi:10.1021/nl051866b
CrossrefPubMedGoogle Scholar

Goodarzi, S., Da Ros, T., Conde, J., Sefat, F., & Mozafari, M. (2017). Fullerene: biomedical engineers get to revisit an old friend. Materials Today, 20(8), 460-480. doi:10.1016/j.mattod.2017.03.017
CrossrefGoogle Scholar

Grebowski, J., Kazmierska, P., & Krokosz, A. (2013). Fullerenols as a new therapeutic approach in nanomedicine. BioMed Research International, 2013, 751913-751922. doi:10.1155/2013/751913
CrossrefPubMedPMCGoogle Scholar

Hodgson, J. A., Roy, R. R., Higuchi, N., Monti, R. J., Zhong, H., Grossman, E., & Edgerton V. R. (2005). Does daily activity level determine muscle phenotype? The Journal of Experimental Biology, 208(1), 3761-3770. doi:10.1242/jeb.01825
CrossrefPubMedGoogle Scholar

Jamart, C., Raymackers, J., Li An, G., Deldicque, L., & Francaux, M. (2011). Prevention of muscle disuse atrophy by MG132 proteasome inhibitor. Muscle Nerve, 43(5), 708-716. doi:10.1002/mus.21949
CrossrefPubMedGoogle Scholar

Jørgensen, S. L., Kierkegaard-Brøchner, S., Bohn, M. B., Høgsholt, M., Aagaard, P., & Mechlenburg, I. (2023). Effects of blood-flow restricted exercise versus conventional resistance training in musculoskeletal disorders - a systematic review and meta-analysis. BMC Sports Science, Medicine and Rehabilitation, 15(1), 141. doi:10.1186/s13102-023-00750-z
CrossrefPubMedPMCGoogle Scholar

Jozsa, L., Thöring, J., Järvinen, M., Kannus, P., Lehto, M., & Kvist, M. (1988). Quantitative alterations in intramuscular connective tissue following immobilization: an experimental study in the rat calf muscles. Experimental & Molecular Pathology, 49(2), 267-278. doi:10.1016/0014-4800(88)90039-1
CrossrefPubMedGoogle Scholar

Nozdrenko, D., Abramchuk, O., Prylutska, S., Vygovska, O., Soroca, V., Bogutska, K., Khrapatyi, S., Prylutskyy, Y., Scharff, P., & Ritter, U. (2021a). Analysis of biomechanical parameters of muscle soleus contraction and blood biochemical parameters in rat with chronic glyphosate intoxication and therapeutic use of C60 fullerene. International Journal of Molecular Sciences, 22(9), 4977. doi:10.3390/ijms22094977
CrossrefPubMedPMCGoogle Scholar

Nozdrenko, D., Matvienko, T., Vygovska, O., Bogutska, K., Motuziuk, O., Nurishchenko, N., Prylutskyy, Y., Scharff, P., & Ritter, U. (2021b). Protective effect of water-soluble C60 fullerene nanoparticles on the ischemia-reperfusion injury of the muscle soleus in rats. International Journal of Molecular Sciences, 22(13), 6812. doi:10.3390/ijms22136812
CrossrefPubMedPMCGoogle Scholar

Nozdrenko, D., Matvienko, T., Vygovska, O., Soroca, V., Bogutska, K., Zholos, A., Scharff, P., Ritter, U., & Prylutskyy, Y. (2022). Post-traumatic recovery of muscle soleus in rats is improved via synergistic effect of C60 fullerene and TRPM8 agonist menthol. Applied Nanoscience, 12(3), 467-478. doi:10.1007/s13204-021-01703-z
CrossrefGoogle Scholar

Ohira, Y., Yoshinaga, T., Nomura, T., Kawano, F., Ishihara, A., Nonaka, I., Roy, R. R., & Edgerton, V. R. (2002). Gravitational unloading effects on muscle fiber size, phenotype and myonuclear number. Advances in Space Research, 30(4), 777-781. doi:10.1016/s0273-1177(02)00395-2
CrossrefPubMedGoogle Scholar

Paddon-Jones, D., Sheffield-Moore, M., Cree, M. G., Hewlings, S. J., Aarsland, A., Wolfe, R. R., & Ferrando, A. A. (2006). Atrophy and impaired muscle protein synthesis during prolonged inactivity and stress. The Journal of Clinical Endocrinology & Metabolism, 91(12), 4836-4841. doi:10.1210/jc.2006-0651
CrossrefPubMedGoogle Scholar

Prilutski, Yu. I., Durov, S. S., Yashchuk, V. N., Ogul'chansky, T. Yu., Pogorelov, V. E., Astashkin, Yu. A., Buzaneva, E. V., Kirghisov, Yu. D., Andrievsky, G. V., & Scharff, P. (1999). Theoretical predictions and experimental studies of self-organization C60 nanoparticles in water solution and on the support. In A. Châtelain, J. M. Bonard (Eds.), The European Physical Journal D: Atomic, molecular and optical physics (pp. 341-343). Berlin: Heidelberg. doi:10.1007/978-3-642-88188-6_65
CrossrefGoogle Scholar

Prylutskyy, Y. I., Vereshchaka, I. V., Maznychenko, A. V., Bulgakova, N. V., Gonchar, O. O., Kyzyma, O. A., Ritter, U., Scharff, P., Tomiak, T., Nozdrenko, D. M., Mishchenko, I. V., & Kostyukov, A. I. (2017). С60 fullerene as promising therapeutic agent for correcting and preventing skeletal muscle fatigue. Journal of Nanobiotechnology, 15(1), 8. doi:10.1186/s12951-016-0246-1
CrossrefPubMedPMCGoogle Scholar

Rong, Z., Yang, Z., Zhang, C., Pu, R., Chen, C., Xu, J., & Fei, L. (2023). Bioinformatics analysis of paravertebral muscles atrophy in adult degenerative scoliosis. Journal of Muscle Research and Cell Motility, 44(4), 287-297. doi:10.1007/s10974-023-09650-8
CrossrefPubMedPMCGoogle Scholar

Rüegg, M. A., & Glass, D. J. (2011). Molecular mechanisms and treatment options for muscle wasting diseases. Annual Review of Pharmacology and Toxicology, 51(1), 373-395. doi:10.1146/annurev-pharmtox-010510-100537
CrossrefPubMedGoogle Scholar

Ryan, J. J., Bateman, H. R., Stover, A., Gomez, G., Norton, S. K., Zhao, W., Schwartz, L. B., Lenk, R., & Kepley, C. L. (2007). Fullerene nanomaterials inhibit the allergic response. Journal of Immunology, 179(1), 665-672. doi:10.4049/jimmunol.179.1.665
CrossrefPubMedGoogle Scholar

Sayed, R. K. A., Hibbert, J. E., Jorgenson, K. W., & Hornberger, T. A. (2023). The structural adaptations that mediate disuse-induced atrophy of skeletal muscle. Cells, 12(24), 2811. doi:10.3390/cells12242811
CrossrefPubMedPMCGoogle Scholar

Scharff, P., Carta-Abelmann, L., Siegmund, C., Matyshevska, O. P., Prylutska, S. V., Koval, T. V., Golub, A. A., Yashchuk, V. M., Kushnir, K. M., & Prylutskyy, Yu. I. (2004). Effect of X-ray and UV irradiation of the C60 fullerene aqueous solution on biological samples. Carbon, 42(5-6), 1199-1201. doi:10.1016/j.carbon.2003.12.055
CrossrefGoogle Scholar

Shally, A., & McDonagh, B. (2020). The redox environment and mitochondrial dysfunction in age-related skeletal muscle atrophy. Biogerontology, 21(4), 461-473. doi:10.1007/s10522-020-09879-7
CrossrefPubMedGoogle Scholar

Thomason, D. B., & Booth, F. W. (1990). Atrophy of the soleus muscle by hindlimb unweighting. Journal of Applied Physiology, 68(1), 1-12. doi:10.1152/jappl.1990.68.1.1
CrossrefPubMedGoogle Scholar

Tidball, J. G. (2005). Inflammatory processes in muscle injury and repair. American journal of physiology. Regulatory, integrative and comparative physiology, 288(2), R345-R353. doi:10.1152/ajpregu.00454.2004
CrossrefPubMedGoogle Scholar

Tidball, J. G., & Villalta S. A. (2010). Regulatory interactions between muscle and the immune system during muscle regeneration. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 298(5), R1173-R1187. doi:10.1152/ajpregu.00735.2009
CrossrefPubMedPMCGoogle Scholar

Tischler, M. E., & Slentz, M. (1995). Impact of weightlessness on muscle function. ASGSB Bulletin: Publication of the American Society for Gravitational and Space Biology, 8(2), 73-81.
Google Scholar

Vereshchaka, I. V., Bulgakova, N. V., Maznychenko, A. V., Gonchar, O. O., Prylutskyy, Yu. I., Ritter, U., Moska, W., Tomiak, T., Nozdrenko, D. M., Mishchenko, I. V., & Kostyukov, A. I. (2018). C60 fullerenes diminish the muscle fatigue in rats comparable to N-acetylcysteine or β-alanine. Frontiers in Physiology, 9, 517. doi:10.3389/fphys.2018.00517
CrossrefPubMedPMCGoogle Scholar

Yoshihara, T., Takaragawa, M., Dobashi, S., & Naito, H. (2022). Losartan treatment attenuates hindlimb unloading-induced atrophy in the soleus muscle of female rats via canonical TGF-β signaling. Journal of Physiological Sciences, 72, 6. doi:10.1186/s12576-022-00830-8
CrossrefPubMedPMCGoogle Scholar

Zuccaro, E., Marchioretti, C., Pirazzini, M., & Pennuto, M. (2023). Introduction to the special issue "Skeletal muscle atrophy: mechanisms at a cellular level". Cells, 12(3), 502. doi:10.3390/cells12030502
CrossrefPubMedPMCGoogle Scholar


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