Abstract
Skeletal muscles comprise more than a third of human body mass and critically contribute to regulation of body metabolism. Chronic inactivity reduces metabolic activity and functional capacity of muscles, leading to metabolic and other disorders, reduced life quality and duration. Cellular models based on progenitor cells isolated from human muscle biopsies and then differentiated into mature fibers in vitro can be used to solve a wide range of experimental tasks. The review discusses the aspects of myogenesis dynamics and regulation, which might be important in the development of an adequate cell model. The main function of skeletal muscle is contraction; therefore, electrical stimulation is important for both successful completion of myogenesis and in vitro modeling of major processes induced in the skeletal muscle by acute or regular physical exercise. The review analyzes the drawbacks of such cellular model and possibilities for its optimization, as well as the prospects for its further application to address fundamental aspects of muscle physiology and biochemistry and explore cellular and molecular mechanisms of metabolic diseases.
Similar content being viewed by others
Abbreviations
- AMPK:
-
AMP-activated protein kinase
- EMSC:
-
embryonic muscle stem cell
- GLUT4:
-
insulin-regulated glucose transporter 4
- MYOG:
-
myogenin
- Pax3/Pax7:
-
paired box transcription factors 3/7
- SC:
-
satellite cell
- TNF1:
-
tumor necrosis factor 1
References
DeFronzo, R. A., Gunnarsson, R., Bjorkman, O., Olsson, M., and Wahren, J. (1985) Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus, J. Clin. Invest., 76, 149-155.
Sylow, L., Kleinert, M., Richter, E. A., and Jensen, T. E. (2017) Exercise-stimulated glucose uptake – regulation and implications for glycaemic control, Nat. Rev. Endocrinol., 13, 133-148.
Frayn, K. N. (2003) The glucose-fatty acid cycle: a physiological perspective, Biochem. Soc. Trans., 31, 1115-1119.
Agudelo, L. Z., Femenia, T., Orhan, F., Porsmyr-Palmertz, M., Goiny, M., et al. (2014) Skeletal muscle PGC-1alpha1 modulates kynurenine metabolism and mediates resilience to stress-induced depression, Cell, 159, 33-45.
Pedersen, B. K., and Febbraio, M. A. (2012) Muscles, exercise and obesity: skeletal muscle as a secretory organ, Nat. Rev. Endocrinol., 8, 457-465.
Demontis, F., Piccirillo, R., Goldberg, A. L., and Perrimon, N. (2013) The influence of skeletal muscle on systemic aging and lifespan, Aging Cell, 12, 943-949.
Lanza, I. R., Short, D. K., Short, K. R., Raghavakaimal, S., Basu, R., et al. (2008) Endurance exercise as a countermeasure for aging, Diabetes, 57, 2933-2942.
Vorotnikov, A. V., Stafeev, I. S., Menshikov, M. Y., Shestakova, M. V., and Parfyonova, Y. V. (2019) Latent inflammation and defect in adipocyte renewal as a mechanism of obesity-associated insulin resistance, Biochemistry (Moscow), 84, 1329-1345.
Pillon, N. J., Gabriel, B. M., Dollet, L., Smith, J. A. B., Sardon, P. L., et al. (2020) Transcriptomic profiling of skeletal muscle adaptations to exercise and inactivity, Nat. Commun., 11, 470.
Makhnovskii, P. A., Bokov, R. O., Kolpakov, F. A., and Popov, D. V. (2021) Transcriptomic signatures and upstream regulation in human skeletal muscle adapted to disuse and aerobic exercise, Int. J. Mol. Sci., 22, 1208, https://doi.org/10.3390/ijms22031208.
Schnyder, S., and Handschin, C. (2015) Skeletal muscle as an endocrine organ: PGC-1alpha, myokines and exercise, Bone, 80, 115-125.
Whitham, M., Parker, B. L., Friedrichsen, M., Hingst, J. R., Hjorth, M., et al. (2018) Extracellular vesicles provide a means for tissue crosstalk during exercise, Cell. Metab., 27, 237-251.
Lee, D. C., Brellenthin, A. G., Thompson, P. D., Sui, X., Lee, I. M., and Lavie, C. J. (2017) Running as a key lifestyle medicine for longevity, Prog. Cardiovasc. Dis., 60, 45-55.
Yoshida, Y., Jain, S. S., McFarlan, J. T., Snook, L. A., Chabowski, A., and Bonen, A. (2013) Exercise- and training-induced upregulation of skeletal muscle fatty acid oxidation are not solely dependent on mitochondrial machinery and biogenesis, J. Physiol., 591, 4415-4426.
Chambers, T. L., Burnett, T. R., Raue, U., Lee, G. A., Finch, W. H., et al. (2020) Skeletal muscle size, function, and adiposity with lifelong aerobic exercise, J. Appl. Physiol. (1985), 128, 368-378.
Gifford, J. R., Weavil, J. C., and Nelson, A. D. (2016) Symmorphosis in patients with chronic heart failure? J. Appl. Physiol. (1985), 121, 1039.
Kovanen, V., and Suominen, H. (1987) Effects of age and life-time physical training on fibre composition of slow and fast skeletal muscle in rats, Pflugers Arch., 408, 543-551.
Schantz, P. G., and Dhoot, G. K. (1987) Coexistence of slow and fast isoforms of contractile and regulatory proteins in human skeletal muscle fibres induced by endurance training, Acta Physiol. Scand., 131, 147-154.
Schiaffino, S., and Reggiani, C. (2011) Fiber types in mammalian skeletal muscles, Physiol. Rev., 91, 1447-1531.
McCarthy, J. J., Andrews, J. L., McDearmon, E. L., Campbell, K. S., Barber, B. K., et al. (2007) Identification of the circadian transcriptome in adult mouse skeletal muscle, Physiol. Genomics, 31, 86-95.
Miller, B. H., McDearmon, E. L., Panda, S., Hayes, K. R., Zhang, J., et al. (2007) Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation, Proc. Natl. Acad. Sci. USA, 104, 3342-3347.
Perrin, L., Loizides-Mangold, U., Chanon, S., Gobet, C., Hulo, N., et al. (2018) Transcriptomic analyses reveal rhythmic and CLOCK-driven pathways in human skeletal muscle, Elife, 7, e34114, https://doi.org/10.7554/eLife.34114.
Popov, D. V., Makhnovskii, P. A., Shagimardanova, E. I., Gazizova, G. R., Lysenko, E. A., et al. (2019) Contractile activity-specific transcriptome response to acute endurance exercise and training in human skeletal muscle, Am. J. Physiol. Endocrinol. Metab., 316, e605-e614.
Bentzinger, C. F., Wang, Y. X., and Rudnicki, M. A. (2012) Building muscle: molecular regulation of myogenesis, Cold Spring Harb. Perspect. Biol., 4, a008342, https://doi.org/10.1101/cshperspect.a008342.
Chal, J., and Pourquie, O. (2017) Making muscle: skeletal myogenesis in vivo and in vitro, Development, 144, 2104-2122.
Tajbakhsh, S. (2009) Skeletal muscle stem cells in developmental versus regenerative myogenesis, J. Intern. Med., 266, 372-389.
Zammit, P. S. (2017) Function of the myogenic regulatory factors Myf5, MyoD, Myogenin and MRF4 in skeletal muscle, satellite cells and regenerative myogenesis, Semin. Cell Dev. Biol., 72, 19-32.
Asfour, H. A., Allouh, M. Z., and Said, R. S. (2018) Myogenic regulatory factors: the orchestrators of myogenesis after 30 years of discovery, Exp. Biol. Med. (Maywood.), 243, 118-128.
Buckingham, M., and Relaix, F. (2015) PAX3 and PAX7 as upstream regulators of myogenesis, Semin. Cell Dev. Biol., 44, 115-125.
Comai, G., and Tajbakhsh, S. (2014) Molecular and cellular regulation of skeletal myogenesis, Curr. Top. Dev. Biol., 110, 1-73.
Olguin, H. C., and Pisconti, A. (2012) Marking the tempo for myogenesis: Pax7 and the regulation of muscle stem cell fate decisions, J. Cell. Mol. Med., 16, 1013-1025.
Hutcheson, D. A., and Kardon, G. (2009) Genetic manipulations reveal dynamic cell and gene functions: Cre-ating a new view of myogenesis, Cell Cycle, 8, 3675-3678.
Chaillou, T., and Lanner, J. T. (2016) Regulation of myogenesis and skeletal muscle regeneration: effects of oxygen levels on satellite cell activity, FASEB J., 30, 3929-3941.
Wagatsuma, A., and Sakuma, K. (2013) Mitochondria as a potential regulator of myogenesis, Sci. World J., 2013, 593267.
Costamagna, D., Costelli, P., Sampaolesi, M., and Penna, F. (2015) Role of inflammation in muscle homeostasis and myogenesis, Mediators Inflamm., 2015, 805172.
Ge, Y., and Chen, J. (2012) Mammalian target of rapamycin (mTOR) signaling network in skeletal myogenesis, J. Biol. Chem., 287, 43928-43935.
Furuichi, Y., Kawabata, Y., Aoki, M., Mita, Y., Fujii, N. L., and Manabe, Y. (2021) Excess glucose impedes the proliferation of skeletal muscle satellite cells under adherent culture conditions, Front. Cell. Dev. Biol., 9, 640399.
Grabiec, K., Gajewska, M., Milewska, M., Blaszczyk, M., and Grzelkowska-Kowalczyk, K. (2014) The influence of high glucose and high insulin on mechanisms controlling cell cycle progression and arrest in mouse C2C12 myoblasts: the comparison with IGF-I effect, J. Endocrinol. Invest., 37, 233-245.
Luo, W., Ai, L., Wang, B. F., and Zhou, Y. (2019) High glucose inhibits myogenesis and induces insulin resistance by down-regulating AKT signaling, Biomed. Pharmacother., 120, 109498.
Hunt, L. C., Xu, B., Finkelstein, D., Fan, Y., Carroll, P. A., et al. (2015) The glucose-sensing transcription factor MLX promotes myogenesis via myokine signaling, Genes Dev., 29, 2475-2489.
Fulco, M., Cen, Y., Zhao, P., Hoffman, E. P., McBurney, M. W., Sauve, A. A., and Sartorelli, V. (2008) Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt, Dev. Cell, 14, 661-673.
Elkalaf, M., Andel, M., and Trnka, J. (2013) Low glucose but not galactose enhances oxidative mitochondrial metabolism in C2C12 myoblasts and myotubes, PLoS One, 8, e70772.
Costford, S. R., Crawford, S. A., Dent, R., McPherson, R., and Harper, M. E. (2009) Increased susceptibility to oxidative damage in post-diabetic human myotubes, Diabetologia, 52, 2405-2415.
Aguer, C., Gambarotta, D., Mailloux, R. J., Moffat, C., Dent, R., et al. (2011) Galactose enhances oxidative metabolism and reveals mitochondrial dysfunction in human primary muscle cells, PLoS One, 6, e28536.
Krauss, R. S., Joseph, G. A., and Goel, A. J. (2017) Keep your friends close: cell–cell contact and skeletal myogenesis, Cold Spring Harb. Perspect. Biol., 9, a029298.
Aas, V., Torbla, S., Andersen, M. H., Jensen, J., and Rustan, A. C. (2002) Electrical stimulation improves insulin responses in a human skeletal muscle cell model of hyperglycemia, Ann. N. Y. Acad. Sci., 967, 506-515.
Carter, S., and Solomon, T. P. J. (2019) In vitro experimental models for examining the skeletal muscle cell biology of exercise: the possibilities, challenges and future developments, Pflugers Arch., 471, 413-429.
Nikolic, N., Gorgens, S. W., Thoresen, G. H., Aas, V., Eckel, J., and Eckardt, K. (2017) Electrical pulse stimulation of cultured skeletal muscle cells as a model for in vitro exercise – possibilities and limitations, Acta Physiol. (Oxf), 220, 310-331.
Nikolic, N., and Aas, V. (2019) Electrical pulse stimulation of primary human skeletal muscle cells, Methods Mol. Biol., 1889, 17-24.
Valdes, J. A., Gaggero, E., Hidalgo, J., Leal, N., Jaimovich, E., and Carrasco, M. A. (2008) NFAT activation by membrane potential follows a calcium pathway distinct from other activity-related transcription factors in skeletal muscle cells, Am. J. Physiol. Cell Physiol., 294, C715-C725.
Sidorenko, S., Klimanova, E., Milovanova, K., Lopina, O. D., Kapilevich, L. V., et al. (2018) Transcriptomic changes in C2C12 myotubes triggered by electrical stimulation: role of Ca(2+)i-mediated and Ca(2+)i-independent signaling and elevated [Na(+)]i/[K(+)]i ratio, Cell Calcium, 76, 72-86.
Sciancalepore, M., Coslovich, T., Lorenzon, P., Ziraldo, G., and Taccola, G. (2015) Extracellular stimulation with human “noisy” electromyographic patterns facilitates myotube activity, J. Muscle Res. Cell Motil., 36, 349-357.
Fujita, H., Nedachi, T., and Kanzaki, M. (2007) Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes, Exp. Cell Res., 313, 1853-1865.
Nikolic, N., Bakke, S. S., Kase, E. T., Rudberg, I., Flo, H., et al. (2012) Electrical pulse stimulation of cultured human skeletal muscle cells as an in vitro model of exercise, PLoS One, 7, e33203.
Lambernd, S., Taube, A., Schober, A., Platzbecker, B., Gorgens, S. W., et al. (2012) Contractile activity of human skeletal muscle cells prevents insulin resistance by inhibiting pro-inflammatory signalling pathways, Diabetologia, 55, 1128-1139.
Brown, A. E., Jones, D. E., Walker, M., and Newton, J. L. (2015) Abnormalities of AMPK activation and glucose uptake in cultured skeletal muscle cells from individuals with chronic fatigue syndrome, PLoS One, 10, e0122982.
Li, Z., Yue, Y., Hu, F., Zhang, C., Ma, X., et al. (2018) Electrical pulse stimulation induces GLUT4 translocation in C2C12 myotubes that depends on Rab8A, Rab13, and Rab14, Am. J. Physiol. Endocrinol. Metab., 314, E478-E493.
Chen, W., Nyasha, M. R., Koide, M., Tsuchiya, M., Suzuki, N., et al. (2019) In vitro exercise model using contractile human and mouse hybrid myotubes, Sci. Rep., 9, 11914.
Son, Y. H., Lee, S. M., Lee, S. H., Yoon, J. H., Kang, J. S., et al. (2019) Comparative molecular analysis of endurance exercise in vivo with electrically stimulated in vitro myotube contraction, J. Appl. Physiol., 127, 1742-1753.
Hartwig, S., Raschke, S., Knebel, B., Scheler, M., Irmler, M., et al. (2014) Secretome profiling of primary human skeletal muscle cells, Biochim. Biophys. Acta, 1844, 1011-1017.
Raschke, S., Eckardt, K., Bjorklund, H. K., Jensen, J., and Eckel, J. (2013) Identification and validation of novel contraction-regulated myokines released from primary human skeletal muscle cells, PLoS One, 8, e62008.
Feng, H., Kang, C., Dickman, J. R., Koenig, R., Awoyinka, I., et al. (2013) Training-induced mitochondrial adaptation: role of peroxisome proliferator-activated receptor gamma coactivator-1alpha, nuclear factor-kappaB and beta-blockade, Exp. Physiol., 98, 784-795.
Burch, N., Arnold, A. S., Item, F., Summermatter, S., Brochmann Santana, S. G., et al. (2010) Electric pulse stimulation of cultured murine muscle cells reproduces gene expression changes of trained mouse muscle, PLoS One, 5, e10970.
Silveira, L. R., Pilegaard, H., Kusuhara, K., Curi, R., and Hellsten, Y. (2006) The contraction induced increase in gene expression of peroxisome proliferator-activated receptor (PPAR)-gamma coactivator 1alpha (PGC-1alpha), mitochondrial uncoupling protein 3 (UCP3) and hexokinase II (HKII) in primary rat skeletal muscle cells is dependent on reactive oxygen species, Biochim. Biophys. Acta, 1763, 969-976.
Beiter, T., Hudemann, J., Burgstahler, C., Niess, A. M., and Munz, B. (2018) Effects of extracellular orotic acid on acute contraction-induced adaptation patterns in C2C12 cells, Mol. Cell Biochem., 448, 251-263.
Abdelmoez, A. M., Sardon, P. L., Smith, J. A. B., Gabriel, B. M., Savikj, M., et al. (2020) Comparative profiling of skeletal muscle models reveals heterogeneity of transcriptome and metabolism, Am. J. Physiol. Cell Physiol., 318, C615-C626.
Feng, Y. Z., Nikolic, N., Bakke, S. S., Kase, E. T., Guderud, K., et al. (2015) Myotubes from lean and severely obese subjects with and without type 2 diabetes respond differently to an in vitro model of exercise, Am. J. Physiol. Cell Physiol., 308, C548-C556.
Park, S., Turner, K. D., Zheng, D., Brault, J. J., Zou, K., et al. (2019) Electrical pulse stimulation induces differential responses in insulin action in myotubes from severely obese individuals, J. Physiol., 597, 449-466.
Lund, J., Rustan, A. C., Lovsletten, N. G., Mudry, J. M., Langleite, T. M., et al. (2017) Exercise in vivo marks human myotubes in vitro: training-induced increase in lipid metabolism, PLoS One, 12, e0175441.
Gaster, M. (2019) The diabetic phenotype is preserved in myotubes established from type 2 diabetic subjects: a critical appraisal, APMIS, 127, 3-26.
Nilsson, E., and Ling, C. (2017) DNA methylation links genetics, fetal environment, and an unhealthy lifestyle to the development of type 2 diabetes, Clin. Epigenetics, 9, 105.
Varemo, L., Henriksen, T. I., Scheele, C., Broholm, C., Pedersen, M., et al. (2017) Type 2 diabetes and obesity induce similar transcriptional reprogramming in human myocytes, Genome Med., 9, 47.
Turner, D. C., Gorski, P. P., Maasar, M. F., Seaborne, R. A., Baumert, P., et al. (2020) DNA methylation across the genome in aged human skeletal muscle tissue and muscle-derived cells: the role of HOX genes and physical activity, Sci. Rep., 10, 15360.
Hawley, J. A., Hargreaves, M., Joyner, M. J., and Zierath, J. R. (2014) Integrative biology of exercise, Cell, 159, 738-749.
Tothova, J., Blaauw, B., Pallafacchina, G., Rudolf, R., Argentini, C., et al. (2006) NFATc1 nucleocytoplasmic shuttling is controlled by nerve activity in skeletal muscle, J. Cell Sci., 119, 1604-1611.
Ehlers, M. L., Celona, B., and Black, B. L. (2014) NFATc1 controls skeletal muscle fiber type and is a negative regulator of MyoD activity, Cell Rep., 8, 1639-1648.
Wojtaszewski, J. F., Mourtzakis, M., Hillig, T., Saltin, B., and Pilegaard, H. (2002) Dissociation of AMPK activity and ACCbeta phosphorylation in human muscle during prolonged exercise, Biochem. Biophys. Res. Commun., 298, 309-316.
Popov, D. V. (2018) Adaptation of skeletal muscles to contractile activity of varying duration and intensity: the role of PGC1a, Biochemistry (Moscow), 83, 613-628.
Popov, D. V., Makhnovskii, P. A., Kurochkina, N. S., Lysenko, E. A., Vepkhvadze, T. F., and Vinogradova, O. L. (2018) Intensity-dependent gene expression after aerobic exercise in endurance-trained skeletal muscle, Biol. Sport, 35, 277-289.
Tarum, J., Folkesson, M., Atherton, P. J., and Kadi, F. (2017) Electrical pulse stimulation: an in vitro exercise model for the induction of human skeletal muscle cell hypertrophy. A proof-of-concept study, Exp. Physiol., 102, 1405-1413.
Valero-Breton, M., Warnier, G., Castro-Sepulveda, M., Deldicque, L., and Zbinden-Foncea, H. (2020) Acute and chronic effects of high frequency electric pulse stimulation on the Akt/mTOR pathway in human primary myotubes, Front. Bioeng. Biotechnol., 8, 565679.
Humphrey, S. J., Yang, G., Yang, P., Fazakerley, D. J., Stockli, J., et al. (2013) Dynamic adipocyte phosphoproteome reveals that Akt directly regulates mTORC2, Cell Metab., 17, 1009-1020.
Humphrey, S. J., Azimifar, S. B., and Mann, M. (2015) High-throughput phosphoproteomics reveals in vivo insulin signaling dynamics, Nat. Biotechnol., 33, 990-995.
Sacco, F., Humphrey, S. J., Cox, J., Mischnik, M., Schulte, A., et al. (2016) Glucose-regulated and drug-perturbed phosphoproteome reveals molecular mechanisms controlling insulin secretion, Nat. Commun., 7, 13250.
Li, J., Li, Q., Tang, J., Xia, F., Wu, J., and Zeng, R. (2015) Quantitative Phosphoproteomics revealed glucose-stimulated responses of islet associated with insulin secretion, J. Proteome Res., 14, 4635-4646.
Tang, J. S., Li, Q. R., Li, J. M., Wu, J. R., and Zeng, R. (2017) Systematic synergy of glucose and GLP-1 to stimulate insulin secretion revealed by quantitative phosphoproteomics, Sci. Rep., 7, 1018.
Hoffman, N. J., Parker, B. L., Chaudhuri, R., Fisher-Wellman, K. H., Kleinert, M., et al. (2015) Global phosphoproteomic analysis of human skeletal muscle reveals a network of exercise-regulated kinases and AMPK substrates, Cell Metab., 22, 922-935.
Needham, E. J., Humphrey, S. J., Cooke, K. C., Fazakerley, D. J., Duan, X., et al. (2019) Phosphoproteomics of acute cell stressors targeting exercise signaling networks reveal drug interactions regulating protein secretion, Cell Rep., 29, 1524-1538.
Denes, L. T., Riley, L. A., Mijares, J. R., Arboleda, J. D., McKee, K., et al. (2019) Culturing C2C12 myotubes on micromolded gelatin hydrogels accelerates myotube maturation, Skelet. Muscle, 9, 17.
Hoshino, D., Kawata, K., Kunida, K., Hatano, A., Yugi, K., et al. (2020) Trans-omic analysis reveals ROS-dependent pentose phosphate pathway activation after high-frequency electrical stimulation in C2C12 myotubes, iScience, 23, 101558.
Stefanetti, R. J., Lamon, S., Wallace, M., Vendelbo, M. H., Russell, A. P., and Vissing, K. (2015) Regulation of ubiquitin proteasome pathway molecular markers in response to endurance and resistance exercise and training, Pflugers Arch., 467, 1523-1537.
Pagano, A. F., Py, G., Bernardi, H., Candau, R. B., and Sanchez, A. M. (2014) Autophagy and protein turnover signaling in slow-twitch muscle during exercise, Med. Sci. Sports Exerc., 46, 1314-1325.
Wilkinson, S. B., Phillips, S. M., Atherton, P. J., Patel, R., Yarasheski, K. E., et al. (2008) Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle, J. Physiol., 586, 3701-3717.
Donges, C. E., Burd, N. A., Duffield, R., Smith, G. C., West, D. W., et al. (2012) Concurrent resistance and aerobic exercise stimulates both myofibrillar and mitochondrial protein synthesis in sedentary middle-aged men, J. Appl. Physiol. (1985), 112, 1992-2001.
Di Donato, D. M., West, D. W., Churchward-Venne, T. A., Breen, L., et al. (2014) Influence of aerobic exercise intensity on myofibrillar and mitochondrial protein synthesis in young men during early and late postexercise recovery, Am. J. Physiol Endocrinol. Metab., 306, E1025-E1032.
Midrio, M. (2006) The denervated muscle: facts and hypotheses. A historical review, Eur. J. Appl. Physiol., 98, 1-21.
Salmons, S., and Sreter, F. A. (1976) Significance of impulse activity in the transformation of skeletal muscle type, Nature, 263, 30-34.
Ferrari, M. B., Podugu, S., and Eskew, J. D. (2006) Assembling the myofibril: coordinating contractile cable construction with calcium, Cell Biochem. Biophys., 45, 317-337.
Nedachi, T., Fujita, H., and Kanzaki, M. (2008) Contractile C2C12 myotube model for studying exercise-inducible responses in skeletal muscle, Am. J. Physiol. Endocrinol. Metab., 295, E1191-E1204.
Khodabukus, A., Madden, L., Prabhu, N. K., Koves, T. R., Jackman, C. P., et al. (2019) Electrical stimulation increases hypertrophy and metabolic flux in tissue-engineered human skeletal muscle, Biomaterials, 198, 259-269.
Park, H., Bhalla, R., Saigal, R., Radisic, M., Watson, N., et al. (2008) Effects of electrical stimulation in C2C12 muscle constructs, J. Tissue Eng. Regen. Med., 2, 279-287.
Shimizu, K., Fujita, H., and Nagamori, E. (2009) Alignment of skeletal muscle myoblasts and myotubes using linear micropatterned surfaces ground with abrasives, Biotechnol. Bioeng., 103, 631-638.
Huang, N. F., Lee, R. J., and Li, S. (2010) Engineering of aligned skeletal muscle by micropatterning, Am. J. Transl. Res., 2, 43-55.
Huang, N. F., Thakar, R. G., Wong, M., Kim, D., Lee, R. J., and Li, S. (2004) Tissue engineering of muscle on micropatterned polymer films, Conf. Proc. IEEE Eng. Med. Biol. Soc., 2004, 4966-4969.
Huang, N. F., Patel, S., Thakar, R. G., Wu, J., Hsiao, B. S., et al. (2006) Myotube assembly on nanofibrous and micropatterned polymers, Nano Lett., 6, 537-542.
Bukatin, A. S., Mukhin, I. S., Malyshev, E. I., Kukhtevich, I. V., Evstrapov, A. A., and Dubina, M. V. (2016) Fabrication of high-aspect-ratio microstructures in polymer microfluid chips for in vitro single cell analysis, Tech. Phys., 61, 1566-1571.
Suh, G. C., Bettadapur, A., Santoso, J. W., and McCain, M. L. (2017) Fabrication of micromolded gelatin hydrogels for long-term culture of aligned skeletal myotubes, Methods Mol. Biol., 1668, 147-163.
Bettadapur, A., Suh, G. C., Geisse, N. A., Wang, E. R., Hua, C., et al. (2016) Prolonged culture of aligned skeletal myotubes on micromolded gelatin hydrogels, Sci. Rep., 6, 28855.
Cooper, S. T., Maxwell, A. L., Kizana, E., Ghoddusi, M., Hardeman, E. C., et al. (2004) C2C12 co-culture on a fibroblast substratum enables sustained survival of contractile, highly differentiated myotubes with peripheral nuclei and adult fast myosin expression, Cell Motil. Cytoskelet., 58, 200-211.
Lautaoja, J. H., Pekkala, S., Pasternack, A., Laitinen, M., Ritvos, O., and Hulmi, J. J. (2020) Differentiation of murine C2C12 myoblasts strongly reduces the effects of myostatin on intracellular signaling, Biomolecules, 10, 695, https://doi.org/10.3390/biom10050695.
Pekkala, S., Keskitalo, A., Kettunen, E., Lensu, S., Nykanen, N., et al. (2019) Blocking activin receptor ligands is not sufficient to rescue cancer-associated gut microbiota-a role for gut microbial flagellin in colorectal cancer and cachexia? Cancers. (Basel), 11, 1799, https://doi.org/10.3390/cancers11111799.
Pandurangan, M., Jeong, D., Amna, T., Van, B. H., and Hwang, I. (2012) Co-culture of C2C12 and 3T3-L1 preadipocyte cells alters the gene expression of calpains, caspases and heat shock proteins, In vitro Cell Dev. Biol. Anim., 48, 577-582.
Pandurangan, M., and Hwang, I. (2014) Application of cell co-culture system to study fat and muscle cells, Appl. Microbiol. Biotechnol., 98, 7359-7364.
Takegahara, Y., Yamanouchi, K., Nakamura, K., Nakano, S., and Nishihara, M. (2014) Myotube formation is affected by adipogenic lineage cells in a cell-to-cell contact-independent manner, Exp. Cell Res., 324, 105-114.
Collins, K. H., Herzog, W., MacDonald, G. Z., Reimer, R. A., Rios, J. L., et al. (2018) Obesity, metabolic syndrome, and musculoskeletal disease: common inflammatory pathways suggest a central role for loss of muscle integrity, Front. Physiol., 9, 112.
Stafeev, I., Podkuychenko, N., Michurina, S., Sklyanik, I., Panevina, A., et al. (2019) Low proliferative potential of adipose-derived stromal cells associates with hypertrophy and inflammation in subcutaneous and omental adipose tissue of patients with type 2 diabetes mellitus, J. Diabetes Complicat., 33, 148-159.
Funding
This work was supported by the Russian Foundation for Basic Research (project no. 20-015-00415).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare no conflict of interest. This article does not contain any studies with human participants or animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Vepkhvadze, T.F., Vorotnikov, A.V. & Popov, D.V. Electrical Stimulation of Cultured Myotubes in vitro as a Model of Skeletal Muscle Activity: Current State and Future Prospects. Biochemistry Moscow 86, 597–610 (2021). https://doi.org/10.1134/S0006297921050084
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297921050084