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How Muscle Activity Controls Slow Myosin Expression

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Abstract

One of the main gravity-determined functions of the locomotor system is to maintain an upright posture. According to the views developed in the scientific school of Prof. I.B. Kozlovskaya, these functions are provided by the tonic muscular system. Under the term “tonic system” I.B. Kozlovskaya meant all the structures and regulatory mechanisms able to maintain basal mechanical tension (tone) for a long time. In mammals, she assigned to the tonic system the slow-twitch muscle fibers with a predominant expression of the myosin heavy chain beta slow isoform, MYHC I(β), and all the neural mechanisms of their control. It is quite obvious that the muscle’s ability to maintain tonic tension for a long time depends on the intensity of slow-myosin expression. Therefore, it would not be a great exaggeration if we call the slow myosin gene myh7 the true muscle tone gene. In the recent years, it has generally become clear how, against the background of prolonged increased muscle contractile activity, an increase in the expression of the slow MYHC isoform and a decrease in the expression of fast MYHC isoforms are triggered. Far less is known about the mechanisms behind a decrease in the expression of MYHC I(β) caused by a decrease in muscle contractile activity. This phenomenon was observed after exposure to true (spaceflight) weightlessness, after bed-rest hypokinesia and “dry” immersion, and also when using a standard rodent hindlimb suspension (unloading) model. Numerous studies of the myosin phenotypic plasticity are mainly concentrated on the search for the mechanisms that link changes in the expression of myosin genes with the muscle contractile activity pattern. The data discussed in the review indicate that constant expression of slow myosin is controlled by tonic activity and, in turn, is a prerequisite for maintaining such an activity. When this activity is considerably reduced or stopped, the metabolic and mechanical incentives, which trigger the signaling pathways of myh7 gene expression, disappear. Exactly this phenomenon is in the focus of this work.

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REFERENCES

  1. Kozlovskaya IB (2017) Gravitation and tonic muscular system. Aviakosm i Ekol Med 51:1021-1025 (In Russ)

    Google Scholar 

  2. Shchepkin DV, Nabiyev S, Kubasova NA, Bershitskiy SYU, Kopylova GV (2020) Comparison of the functional charactiristics of slow-type and fast-type skeletal muscles. Bull Eksp Biol Med 169:113-119 (In Russ)

    Google Scholar 

  3. Hodgson JA, Roy RR, Higuchi N, Monti RJ, Zhong H, Grossman E, Edgerton VR (2005) Does daily activity level determine muscle phenotype? J Exp Biol 208 (Pt 19):3761-3770 https://doi.org/10.1242/jeb.01825

    Article  PubMed  Google Scholar 

  4. Nasledov GA (1981) Tonic muscular system of vertebrates. Nauka, SpB.

    Google Scholar 

  5. Shenkman BS (2016) From Slow to Fast: Hypogravity-Induced Remodeling of Muscle Fiber Myosin Phenotype. Acta Naturae 8:47-59. https://doi.org/10.32607/20758251-2016-8-4-47-59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Desplanches D, Mayet MH, Ilyina-Kakueva EI, Frutoso J, Flandrois R (1991) Structural and metabolic properties of rat muscle exposed to weightlessness aboard Cosmos 1887. Eur J Appl Physiol Occup Physiol 63:288-292. https://doi.org/10.1007/BF00233864

    Article  CAS  PubMed  Google Scholar 

  7. Shenkman BS, Kozlovskaya IB, Kuznetsov SL, Nemirovskaya TL, Desplanches D (1994) Plasticity of skeletal muscle fibres in space-flown primates. J Gravit Physiol 1:64-66. https://doi.org/10.1023/A:1024473126643

    Article  Google Scholar 

  8. Martin TP, Edgerton VR, Grindeland RE (1988) Influence of spaceflight on rat skeletal muscle. J Appl Physiol 65:2318-2325. https://doi.org/10.1152/jappl.1988.65.5.2318

    Article  CAS  PubMed  Google Scholar 

  9. Ohira Y, Yoshinaga T, Ohara M, Nonaka I, Yoshioka T, Yamashita-Goto K, Shenkman BS, Kozlovskaya IB, Roy RR, Edgerton VR (1999) Myonuclear domain and myosin phenotype in human soleus after bed rest with or without loading. J Appl Physiol 87:1776-1785. https://doi.org/10.1152/jappl.1999.87.5.1776

    Article  CAS  PubMed  Google Scholar 

  10. Shenkman BS, Podlubnaya ZA, Vikhlyantsev IM, Litvinova KS, Udaltsov SN, Nemirovskaya TL (2004) Contractile characteristics and sarcomeric cytoskeletal proteins of human soleus fibers in muscle unloading: role of mechanical stimulation from the support surface. Biophysics 49: 807-815.

    Google Scholar 

  11. Desplanches D, Mayet MH, Sempore B, Flandrois R (1987) Structural and functional responses to prolonged hindlimb suspension in rat muscle. J Appl Physiol 63:558-563.

    Article  CAS  Google Scholar 

  12. Templeton GH, Sweeney HL, Timson BF, Padalino M, Dudenhoeffer GA (1988) Changes in fiber composition of soleus muscle during rat hindlimb suspension. J Appl Physiol 65:1191-1195. https://doi.org/10.1152/jappl.1988.65.3.1191

    Article  CAS  PubMed  Google Scholar 

  13. Baldwin KM, Haddad F, Pandorf CE, Roy RR, Edgerton VR (2013) Alterations in muscle mass and contractile phenotype in response to unloading models: role of transcriptional/pretranslational mechanisms. Front Physiol 4:284. https://doi.org/10.3389/fphys.2013.00284

    Article  PubMed  PubMed Central  Google Scholar 

  14. Ranvier L (1873) De quelques faits relatifs a l’histologie et a la physiologie des muscles striaes. Arch Physiol Norm Pathol (Paris) 1:5-15.

    Google Scholar 

  15. Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50:500-509. https://doi.org/10.1002/1097-0029(20000915)50:6<500::AID-JEMT7>3.0.CO;2-7

    Article  CAS  PubMed  Google Scholar 

  16. Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 1447-1531. https://doi.org/10.1152/physrev.00031.2010

  17. Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Musc 1:4. https://doi.org/10.1186/2044-5040-1-4

    Article  CAS  Google Scholar 

  18. Delp MD, Duan C (1996) Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol (1985) 80:261-270. https://doi.org/10.1152/jappl.1996.80.1.261

    Article  CAS  Google Scholar 

  19. Baldwin KM, Valdez V, Schrader LF, Herrick RE (1981) Effect of functional overload on substrate oxidation capacity of skeletal muscle. J Appl Physiol Respir Environ Exerc Physiol 50:1272-1276. https://doi.org/10.1152/jappl.1981.50.6.1272

    Article  CAS  PubMed  Google Scholar 

  20. Conjard A, Peuker H, Pette D (1998) Energy state and myosin heavy chain isoforms in single fibres of normal and transforming rabbit muscles. Pflugers Arch 436 (6):962-969. https://doi.org/10.1007/s004240050730

    Article  CAS  PubMed  Google Scholar 

  21. Ausoni S, Gorza L, Schiaffino S, Gundersen K, Lomo T (1990) Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J Neurosci 10:153-160. https://doi.org/10.1523/JNEUROSCI.10-01-00153.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kubis HP, Scheibe RJ, Meissner JD, Hornung G, Gros G (2002) Fast-to-slow transformation and nuclear import/export kinetics of the transcription factor NFATc1 during electrostimulation of rabbit muscle cells in culture. J Physiol 541:835-847.

    Article  CAS  Google Scholar 

  23. Shishmarev D (2020) Excitation-contraction coupling in skeletal muscle: recent progress and unanswered questions. Biophys Rev 12:143-153. https://doi.org/10.1007/s12551-020-00610-x

    Article  PubMed  PubMed Central  Google Scholar 

  24. Everts ME, Lomo T, Clausen T (1993) Changes in K+, Na+ and calcium contents during in vivo stimulation of rat skeletal muscle. Acta Physiol Scand 147:357-368. https://doi.org/10.1111/j.1748-1716.1993.tb09512.x

    Article  CAS  PubMed  Google Scholar 

  25. Carroll S, Nicotera P, Pette D (1999) Calcium transients in single fibers of low-frequency stimulated fast-twitch muscle of rat. Am J Physiol 277:C1122-C1129. https://doi.org/10.1152/ajpcell.1999.277.6.C1122

    Article  CAS  PubMed  Google Scholar 

  26. Ohlendieck K, Fromming GR, Murray BE, Maguire PB, Leisner E, Traub I, Pette D (1999) Effects of chronic low-frequency stimulation on Ca2+-regulatory membrane proteins in rabbit fast muscle. Pflugers Arch 438:700-708. https://doi.org/10.1007/s004249900115

    Article  CAS  PubMed  Google Scholar 

  27. Casas M, Buvinic S, Jaimovich E (2014) ATP signaling in skeletal muscle: from fiber plasticity to regulation of metabolism. Exerc Sport Sci Rev 42:110-116. https://doi.org/10.1249/JES.0000000000000017

    Article  PubMed  Google Scholar 

  28. Crabtree GR (1999) Generic signals and specific outcomes: signaling through Ca2+, calcineurin, and NF-AT. Cell 96 (5):611-614. https://doi.org/10.1016/s0092-8674(00)80571-1

    Article  CAS  PubMed  Google Scholar 

  29. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12:2499-2509. https://doi.org/10.1101/gad.12.16.2499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. McCullagh KJ, Calabria E, Pallafacchina G, Ciciliot S, Serrano AL, Argentini C, Kalhovde JM, Lomo T, Schiaffino S (2004) NFAT is a nerve activity sensor in skeletal muscle and controls activity-dependent myosin switching. Proc Natl Acad Sci U S A 101:10590-10595. https://doi.org/10.1073/pnas.0308035101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Tothova J, Blaauw B, Pallafacchina G, Rudolf R, Argentini C, Reggiani C, Schiaffino S (2006) NFATc1 nucleocytoplasmic shuttling is controlled by nerve activity in skeletal muscle. J Cell Sci 119:1604-1611. https://doi.org/10.1242/jcs.02875

    Article  CAS  PubMed  Google Scholar 

  32. Calabria E, Ciciliot S, Moretti I, Garcia M, Picard A, Dyar KA, Pallafacchina G, Tothova J, Schiaffino S, Murgia M (2009) NFAT isoforms control activity-dependent muscle fiber type specification. Proc Natl Acad Sci U S A 106:13335-13340. https://doi.org/10.1073/pnas.0812911106

    Article  PubMed  PubMed Central  Google Scholar 

  33. Eilers W, Jaspers RT, de Haan A, Ferrie C, Valdivieso P, Fluck M (2014) CaMKII content affects contractile, but not mitochondrial, characteristics in regenerating skeletal muscle. BMC Physiol 14:7. https://doi.org/10.1186/s12899-014-0007-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chin ER (2004) The role of calcium and calcium/calmodulin-dependent kinases in skeletal muscle plasticity and mitochondrial biogenesis. Proc Nutr Soc 63:279-286. https://doi.org/10.1079/PNS2004335

    Article  CAS  PubMed  Google Scholar 

  35. Mu X, Brown LD, Liu Y, Schneider MF (2007) Roles of the calcineurin and CaMK signaling pathways in fast-to-slow fiber type transformation of cultured adult mouse skeletal muscle fibers. Physiol Genomics 30:300-312. https://doi.org/10.1152/physiolgenomics.00286.2006

    Article  CAS  PubMed  Google Scholar 

  36. Miska EA, Karlsson C, Langley E, Nielsen SJ, Pines J, Kouzarides T (1999) HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J 18:5099-5107. https://doi.org/10.1093/emboj/18.18.5099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Cohen TJ, Choi MC, Kapur M, Lira VA, Yan Z, Yao TP (2015) HDAC4 regulates muscle fiber type-specific gene expression programs. Mol Cells 38:343-348. https://doi.org/10.14348/molcells.2015.2278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson KA, DiMaio JM, Olson EN, Bassel-Duby R, Williams RS (2001) Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 20:6414-6423. https://doi.org/10.1093/emboj/20.22.6414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li J, Vargas MA, Kapiloff MS, Dodge-Kafka KL (2013) Regulation of MEF2 transcriptional activity by calcineurin/mAKAP complexes. Exp Cell Res 319:447-454. https://doi.org/10.1016/j.yexcr.2012.12.016

    Article  CAS  PubMed  Google Scholar 

  40. Lynch J, Guo L, Gelebart P, Chilibeck K, Xu J, Molkentin JD, Agellon LB, Michalak M (2005) Calreticulin signals upstream of calcineurin and MEF2C in a critical Ca(2+)-dependent signaling cascade. J Cell Biol 170 (1):37-47. https://doi.org/10.1083/jcb.200412156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. McKinsey TA, Zhang CL, Olson EN (2001) Control of muscle development by dueling HATs and HDACs. Curr Opin Genet Dev 11:497-504.

    Article  CAS  Google Scholar 

  42. Grozinger CM, Schreiber SL (2000) Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci U S A 97:7835-7840. https://doi.org/10.1073/pnas.140199597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Liu Y, Randall WR, Schneider MF (2005) Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle. J Cell Biol 168:887-897. https://doi.org/10.1083/jcb.200408128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Zong H, Ren JM, Young LH, Pypaert M, Mu J, Birnbaum MJ, Shulman GI (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99:15983-15987. https://doi.org/10.1073/pnas.252625599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Henriksson J, Salmons S, Chi MY, Hintz CS, Lowry OH (1988) Chronic stimulation of mammalian muscle: changes in metabolite concentrations in individual fibers. Am J Physiol 255 :543-551. https://doi.org/10.1152/ajpcell.1988.255.4.C543

    Article  Google Scholar 

  46. Green HJ, Pette D (1997) Early metabolic adaptations of rabbit fast-twitch muscle to chronic low-frequency stimulation. Eur J Appl Physiol Occup Physiol 75:418-424. https://doi.org/10.1007/s004210050182

    Article  CAS  PubMed  Google Scholar 

  47. Putman CT, Gallo M, Martins KJ, MacLean IM, Jendral MJ, Gordon T, Syrotuik DG, Dixon WT (2015) Creatine loading elevates the intracellular phosphorylation potential and alters adaptive responses of rat fast-twitch muscle to chronic low-frequency stimulation. Appl Physiol Nutr Metab 40:671-682. https://doi.org/10.1139/apnm-2014-0300

    Article  CAS  PubMed  Google Scholar 

  48. Drenning JA, Lira VA, Simmons CG, Soltow QA, Sellman JE, Criswell DS (2008) Nitric oxide facilitates NFAT-dependent transcription in mouse myotubes. Am J Physiol Cell Physiol 294:C1088-C1095. https://doi.org/10.1152/ajpcell.00523.2007

    Article  CAS  PubMed  Google Scholar 

  49. Reiser PJ, Kline WO, Vaghy PL (1997) Induction of neuronal type nitric oxide synthase in skeletal muscle by chronic electrical stimulation in vivo. J Appl Physiol (1985) 82:1250-1255. https://doi.org/10.1152/jappl.1997.82.4.1250

    Article  CAS  Google Scholar 

  50. Tidball JG, Lavergne E, Lau KS, Spencer MJ, Stull JT, Wehling M (1998) Mechanical loading regulates NOS expression and activity in developing and adult skeletal muscle. Am J Physiol 275:260-266. https://doi.org/10.1152/ajpcell.1998.275.1.C260

    Article  Google Scholar 

  51. Pearson T, McArdle A, Jackson MJ (2015) Nitric oxide availability is increased in contracting skeletal muscle from aged mice, but does not differentially decrease muscle superoxide. Free Radic Biol Med 78: 82-88. https://doi.org/10.1016/j.freeradbiomed.2014.10.505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Shen T, Cseresnyes Z, Liu Y, Randall WR, Schneider MF (2007) Regulation of the nuclear export of the transcription factor NFATc1 by protein kinases after slow fibre type electrical stimulation of adult mouse skeletal muscle fibres. J Physiol 579:535-551. https://doi.org/10.1113/jphysiol.2006.120048

    Article  CAS  PubMed  Google Scholar 

  53. Martins KJ, St-Louis M, Murdoch GK, MacLean IM, McDonald P, Dixon WT, Putman CT, Michel RN (2012) Nitric oxide synthase inhibition prevents activity-induced calcineurin-NFATc1 signalling and fast-to-slow skeletal muscle fibre type conversions. J Physiol 590 (6):1427-1442. https://doi.org/10.1113/jphysiol.2011.223370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, Kelm RJ Jr, Olson EN (2009) A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 17:662-673. https://doi.org/10.1016/j.devcel.2009.10.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. McCarthy JJ, Esser KA, Peterson CA, Dupont-Versteegden EE (2009) Evidence of MyomiR network regulation of beta-myosin heavy chain gene expression during skeletal muscle atrophy. Physiol Genomics 39:219-226. https://doi.org/10.1152/physiolgenomics.00042.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ji J, Tsika GL, Rindt H, Schreiber KL, McCarthy JJ, Kelm RJ Jr, Tsika R (2007) Puralpha and Purbeta collaborate with Sp3 to negatively regulate beta-myosin heavy chain gene expression during skeletal muscle inactivity. Mol Cell Biol 27:1531-1543. https://doi.org/10.1128/MCB.00629-06

    Article  CAS  PubMed  Google Scholar 

  57. Xu M, Chen X, Chen D, Yu B, Li M, He J, Huang Z (2018) MicroRNA-499-5p regulates skeletal myofiber specification via NFATc1/MEF2C pathway and Thrap1/MEF2C axis. Life Sci 215: 236-245. https://doi.org/10.1016/j.lfs.2018.11.020

    Article  CAS  PubMed  Google Scholar 

  58. Huang S, Jin L, Shen J, Shang P, Jiang X, Wang X (2016) Electrical stimulation influences chronic intermittent hypoxia-hypercapnia induction of muscle fibre transformation by regulating the microRNA/Sox6 pathway. Sci Rep 6: 26415. https://doi.org/10.1038/srep26415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Fitts RH, Trappe SW, Costill DL, Gallagher PM, Creer AC, Colloton PA, Peters JR, Romatowski JG, Bain JL, Riley DA (2010) Prolonged space flight-induced alterations in the structure and function of human skeletal muscle fibres. J Physiol 588:3567-3592. https://doi.org/10.1113/jphysiol.2010.188508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Goswami N (2017) Falls and Fall-Prevention in Older Persons: Geriatrics Meets Spaceflight! Front Physiol 8: 603. https://doi.org/10.3389/fphys.2017.00603

    Article  PubMed  PubMed Central  Google Scholar 

  61. Russomano T, Gustavo D, Falcuo F (2008) The Effects of Hypergravity and Microgravity on Biomedical Experiments. Biomed Eng 77. https://doi.org/10.2200/S00105ED1V01Y200801BME018

  62. Shulzhenko EB, Wil-Williams IF (1976) Possibility of long-term water immersion by the “dry” immersion method. Cosm Biol Aviacosm Med 10: 82-84 (In Russ).

    CAS  Google Scholar 

  63. Morey-Holton ER, Globus RK (2002) Hindlimb unloading rodent model: technical aspects. J Appl Physiol 92:1367-1377. https://doi.org/10.1152/japplphysiol.00969.2001

    Article  PubMed  Google Scholar 

  64. Ilin EA, Novikov VE (1980) Stand for modelling the physiological effects of weightlessness in laboratory experiments with rats. Kosm Biol Aviakosm Med 14:79-80.

    CAS  PubMed  Google Scholar 

  65. Alford EK, Roy RR, Hodgson JA, Edgerton VR (1987) Electromyography of rat soleus, medial gastrocnemius, and tibialis anterior during hind limb suspension. Exp Neurol 96 (3):635-649. https://doi.org/10.1016/0014-4886(87)90225-1

    Article  CAS  PubMed  Google Scholar 

  66. Fitts RH, Riley DR, Widrick JJ (2001) Functional and structural adaptations of skeletal muscle to microgravity. J Exp Biol 204:3201-3208.

    Article  CAS  Google Scholar 

  67. Shenkman BS, Nemirovskaya TL (2008) Calcium-dependent signaling mechanisms and soleus fiber remodeling under gravitational unloading. J Muscle Res Cell Motil 29:221-230. https://doi.org/10.1007/s10974-008-9164-7

    Article  CAS  PubMed  Google Scholar 

  68. Gazenko OG, Grigoriev AI, Kozlovskaya IB (1987) Mechanisms of acute and chronic effects of microgravity. Physiologist 30 (1 Suppl):S1-S5.

    CAS  PubMed  Google Scholar 

  69. Kozlovskaya IB, Shenkman BS (2019) Cellular Responses of Human Postural Muscle to Dry Immersion. Front Physiol 10:187. https://doi.org/10.3389/fphys.2019.00187

    Article  PubMed  PubMed Central  Google Scholar 

  70. Kawano F (2004) The mechanisms underlying neuromuscular changes in microgravity environment. Biol Sci Space 18 (3):104-105.

    PubMed  Google Scholar 

  71. De-Doncker L, Kasri M, Picquet F, Falempin M (2005) Physiologically adaptive changes of the L5 afferent neurogram and of the rat soleus EMG activity during 14 days of hindlimb unloading and recovery. J Exp Biol 208:4585-4592. https://doi.org/10.1242/jeb.01931

    Article  CAS  PubMed  Google Scholar 

  72. Giger JM, Bodell PW, Zeng M, Baldwin KM, Haddad F (2009) Rapid muscle atrophy response to unloading: pretranslational processes involving MYHC and actin. J Appl Physiol (1985):1204-1212. https://doi.org/10.1152/japplphysiol.00344.2009

  73. Vilchinskaya NA, Mochalova EP, Nemirovskaya TL, Mirzoev TM, Turtikova OV, Shenkman BS (2017) Rapid decline in MyHC I(beta) mRNA expression in rat soleus during hindlimb unloading is associated with AMPK dephosphorylation. J Physiol 595:7123-7134. https://doi.org/10.1113/JP275184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Desaphy JF, Pierno S, Liantonio A, De Luca A, Didonna MP, Frigeri A, Nicchia GP, Svelto M, Camerino C, Zallone A, Camerino DC (2005) Recovery of the soleus muscle after short- and long-term disuse induced by hindlimb unloading: effects on the electrical properties and myosin heavy chain profile. Neurobiol Dis 18:356-365. https://doi.org/10.1016/j.nbd.2004.09.016

    Article  CAS  PubMed  Google Scholar 

  75. Lomonosova YN, Turtikova OV, Shenkman BS (2016) Reduced expression of MyHC slow isoform in rat soleus during unloading is accompanied by alterations of endogenous inhibitors of calcineurin/NFAT signaling pathway. J Muscle Res Cell Motil 37:7-16. https://doi.org/10.1007/s10974-015-9428-y

    Article  CAS  PubMed  Google Scholar 

  76. Stevens L, Gohlsch B, Mounier Y, Pette D (1999) Changes in myosin heavy chain mRNA and protein isoforms in single fibers of unloaded rat soleus muscle. FEBS Letters 463:15-18. https://doi.org/10.1016/s0014-5793(99)01596-3

    Article  CAS  PubMed  Google Scholar 

  77. Stevens L, Sultan KR, Peuker H, Gohlsch B, Mounier Y, Pette D (1999) Time-dependent changes in myosin heavy chain mRNA and protein isoforms in unloaded soleus muscle of rat. Am J Physiol 277: 1044-1049. https://doi.org/10.1152/ajpcell.1999.277.6.C1044

    Article  Google Scholar 

  78. Lomonosova YN, Kalamkarov GR, Bugrova AE, Shevchenko TF, Kartashkina NL, Lysenko EA, Shvets VI, Nemirovskaya TL (2011) Protective effect of L-Arginine administration on proteins of unloaded m. soleus. Biochemistry (Mosc) 76 (5):571-580. https://doi.org/10.1134/S0006297911050075

    Article  CAS  Google Scholar 

  79. Mirzoev T, Tyganov S, Vilchinskaya N, Lomonosova Y, Shenkman B (2016) Key Markers of mTORC1-Dependent and mTORC1-Independent Signaling Pathways Regulating Protein Synthesis in Rat Soleus Muscle During Early Stages of Hindlimb Unloading. Cell Physiol Biochem 39:1011-1020. https://doi.org/10.1159/000447808

    Article  CAS  PubMed  Google Scholar 

  80. Ohira Y, Yasui W, Kariya F, Wakatsuki T, Nakamura K, Asakura T, Edgerton VR (1994) Metabolic adaptation of skeletal muscles to gravitational unloading. Acta Astronaut 33:113-117. https://doi.org/10.1016/0094-5765(94)90115-5

    Article  CAS  PubMed  Google Scholar 

  81. McBride A, Ghilagaber S, Nikolaev A, Hardie DG (2009) The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor. Cell Metab 9:23-34. https://doi.org/10.1016/j.cmet.2008.11.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Henriksen EJ, Tischler ME (1988) Time course of the response of carbohydrate metabolism to unloading of the soleus. Metabolism 37:201-208. https://doi.org/10.1016/0026-0495(88)90096-0

    Article  CAS  PubMed  Google Scholar 

  83. Wakatsuki T, Ohira Y, Yasui W, Nakamura K, Asakura T, Ohno H, Yamamoto M (1994) Responses of contractile properties in rat soleus to high-energy phosphates and/or unloading. Jpn J Physiol 44:193-204 https://doi.org/10.2170/jjphysiol.44.193

    Article  CAS  PubMed  Google Scholar 

  84. Matoba T Watabe Y, Ohira Y (1993) β-Guanidinopropionic acid suppresses suspension-induced changes in myosin expression in rat skeletal muscle. Med Sci Sports Exerc 25:157.

    Article  Google Scholar 

  85. Sharlo K, Paramonova I, Turtikova O, Tyganov S, Shenkman B (2019) Plantar mechanical stimulation prevents calcineurin-NFATc1 inactivation and slow-to-fast fiber type shift in rat soleus muscle under hindlimb unloading. J Appl Physiol 126:1769-1781. https://doi.org/10.1152/japplphysiol.00029.2019

    Article  CAS  PubMed  Google Scholar 

  86. Paramonova II, Sharlo KA, Vilchinskaya NA, Shenkman BS (2020) The Time Course of Muscle Nuclear Content of Transcription Factors Regulating the MyHC I(β) Expression in the Rat Soleus Muscle under Gravitational Unloading. Biol Membr 37:126-133. https://doi.org/10.31857/S0233475520020097

    Article  CAS  Google Scholar 

  87. Ingalls CP, Wenke JC, Armstrong RB (2001) Time course changes in [Ca2+]i, force, and protein content in hindlimb-suspended mouse soleus muscles. Aviat Space Environ Med 72:471-476.

    CAS  PubMed  Google Scholar 

  88. Sharlo K, Paramonova I, Turtikova O, Tyganov S, Shenkman B (2019) Plantar mechanical stimulation prevents calcineurin/NFATc1 inactivation and slow-to-fast fiber-type shift in rat soleus muscle under hindlimb unloading. J Appl Physiol 126:1769-1781. https://doi.org/10.1152/japplphysiol.00029.2019

    Article  CAS  PubMed  Google Scholar 

  89. Sharlo KA, Paramonova, II, Lvova ID, Vilchinskaya NA, Bugrova AE, Shevchenko TF, Kalamkarov GR, Shenkman BS (2020) NO-Dependent Mechanisms of Myosin Heavy Chain Transcription Regulation in Rat Soleus Muscle After 7-Days Hindlimb Unloading. Front Physiol 11:814. https://doi.org/10.3389/fphys.2020.00814

    Article  PubMed  PubMed Central  Google Scholar 

  90. Dyar KA, Ciciliot S, Tagliazucchi GM, Pallafacchina G, Tothova J, Argentini C, Agatea L, Abraham R, Ahdesmaki M, Forcato M, Bicciato S, Schiaffino S, Blaauw B (2015) The calcineurin-NFAT pathway controls activity-dependent circadian gene expression in slow skeletal muscle. Mol Metab 4:823-833. https://doi.org/10.1016/j.molmet.2015.09.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Shenkman BS (2020) How Postural Muscle Senses Disuse? Early Signs and Signals. Int J Mol Sci 21(14):5037. https://doi.org/10.3390/ijms1145037

    Article  CAS  PubMed Central  Google Scholar 

  92. Ingalls CP, Warren GL, Armstrong RB (1999) Intracellular Ca2+ transients in mouse soleus muscle after hindlimb unloading and reloading. J Appl Physiol (1985) 87:386-390. https://doi.org/10.1152/jappl.1999.87.1.386

    Article  CAS  Google Scholar 

  93. Arutyunyan RS Kozlovskaya IB, Nasledov GA, Nemirovskaya TL, Radzyukevitch TL, Shenkman BS (1995) The contraction of unweighted fast and slow rat muscles in calcium-free solution. Basic Appl Myol 5:169-175.

    Google Scholar 

  94. Lvova ID, Sharlo KA, Paramonova II, Shenkman BS (2021) Transient activation of slow myosin expression after 3 days of rat hindlimb unloading is caused by calcium ions accumulation. Aviakosm Ekol Med. In Press.

  95. Sharlo KA, Mochalova EP, Belova SP, Lvova ID, Nemirovskaya TL, Shenkman BS (2020) The role of MAP-kinase p38 in the m. soleus slow myosin mRNA transcription regulation during short-term functional unloading. Archiv Biochem Biophys 695:108-622. https://doi.org/10.1016/j.abb.2020.108622

    Article  CAS  Google Scholar 

  96. Wright DC, Geiger PC, Han DH, Jones TE, Holloszy JO (2007) Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J Biol Chem 282:18793-18799. https://doi.org/10.1074/jbc.M611252200

    Article  CAS  PubMed  Google Scholar 

  97. Sharlo KA, Paramonova II, Lvova ID, Mochalova EP, Kalashnikov VE, Vilchinskaya NA, Tyganov SA, Konstantinova TS, Shevchenko TF, Kalamkarov GR, Shenkman BS (2021) Plantar Mechanical Stimulation Maintains Slow Myosin Expression in Disused Rat Soleus Muscle via NO-Dependent Signaling. Int J Mol Sci 22:10. https://doi.org/10.3390/ijms22031372

    Article  CAS  Google Scholar 

  98. Mukhina AM, Altayeva EG, Nemirovskaya TL, Shenkman BS (2006) Role of L-type Ca channels in Ca2+ accumulation and changes in distribution of myosin heavy chain and SERCA isoforms in rat M. soleus under gravitational unloading. Russ J Pysiol 92 (11):1285-1295 (In Russ).

    CAS  Google Scholar 

  99. Xia L, Cheung KK, Yeung SS, Yeung EW (2016) The involvement of transient receptor potential canonical type 1 in skeletal muscle regrowth after unloading-induced atrophy. J Physiol 594:3111-3126. https://doi.org/10.1113/JP271705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Dupont-Versteegden EE, Knox M, Gurley CM, Houle JD, Peterson CA (2002) Maintenance of muscle mass is not dependent on the calcineurin-NFAT pathway. Am J Physiol Cell Physiol 282:1387-1395. https://doi.org/10.1152/ajpcell.00424.2001

    Article  Google Scholar 

  101. Shen T, Liu Y, Contreras M, Hernandez-Ochoa EO, Randall WR, Schneider MF (2010) DNA binding sites target nuclear NFATc1 to heterochromatin regions in adult skeletal muscle fibers. Histochem Cell Biol 134:387-402. https://doi.org/10.1007/s00418-010-0744-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Meissner JD, Freund R, Krone D, Umeda PK, Chang KC, Gros G, Scheibe RJ (2011) Extracellular signal-regulated kinase 1/2-mediated phosphorylation of p300 enhances myosin heavy chain I/beta gene expression via acetylation of nuclear factor of activated T cells c1. Nucleic Acids Res 39:5907-5925. https://doi.org/10.1093/nar/gkr162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Chen YJ, Wang YN, Chang WC (2007) ERK2-mediated C-terminal serine phosphorylation of p300 is vital to the regulation of epidermal growth factor-induced keratin 16 gene expression. J Biol Chem 282:27215-27228. https://doi.org/10.1074/jbc.M700264200

    Article  CAS  PubMed  Google Scholar 

  104. Pandorf CE, Haddad F, Wright C, Bodell PW, Baldwin KM (2009) Differential epigenetic modifications of histones at the myosin heavy chain genes in fast and slow skeletal muscle fibers and in response to muscle unloading. Am J Physiol Cell Physiol 297:6-16. https://doi.org/10.1152/ajpcell.00075.2009

    Article  CAS  Google Scholar 

  105. Martin M, Kettmann R, Dequiedt F (2007) Class IIa histone deacetylases: regulating the regulators. Oncogene 26:5450-5467. https://doi.org/10.1038/sj.onc.1210613

    Article  CAS  PubMed  Google Scholar 

  106. Youn HD, Grozinger CM, Liu JO (2000) Calcium regulates transcriptional repression of myocyte enhancer factor 2 by histone deacetylase 4. J Biol Chem 275:22563-22567. https://doi.org/10.1074/jbc.C000304200

    Article  CAS  PubMed  Google Scholar 

  107. McKinsey TA, Zhang CL, Olson EN (2001) Identification of a signal-responsive nuclear export sequence in class II histone deacetylases. Mol Cell Biol 21 (18):6312-6321.

    Article  CAS  Google Scholar 

  108. Lu J, McKinsey TA, Zhang CL, Olson EN (2000) Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol Cell 6:233-244.

    Article  CAS  Google Scholar 

  109. Socco S, Bovee RC, Palczewski MB, Hickok JR, Thomas DD (2017) Epigenetics: The third pillar of nitric oxide signaling. Pharmacol Res 52-58. https://doi.org/10.1016/j.phrs.2017.04.011

  110. Nott A, Riccio A (2009) Nitric oxide-mediated epigenetic mechanisms in developing neurons. Cell Cycle 8:725-730. https://doi.org/10.4161/cc.8.5.7805

    Article  CAS  PubMed  Google Scholar 

  111. Liu J, Liang X, Zhou D, Lai L, Xiao L, Liu L, Fu T, Kong Y, Zhou Q, Vega RB, Zhu MS, Kelly DP, Gao X, Gan Z (2016) Coupling of mitochondrial function and skeletal muscle fiber type by a miR-499/Fnip1/AMPK circuit. EMBO Mol Med 8:1212-1228. https://doi.org/10.15252/emmm.201606372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Handschin C, Chin S, Li P, Liu F, Maratos-Flier E, Lebrasseur NK, Yan Z, Spiegelman BM (2007) Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals. J Biol Chem 282:30014-30021. https://doi.org/10.1074/jbc.M704817200

    Article  CAS  PubMed  Google Scholar 

  113. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418 :797-801. https://doi.org/10.1038/nature00904

    Article  CAS  PubMed  Google Scholar 

  114. Sharlo K, Lomonosova Y, Turtikova O, Mitrofanova O, Kalamkarov G, Bugrova A, Shevchenko T, Shenkman B (2018) The Role of GSK-3β Phosphorylation in the Regulation of Slow Myosin Expression in Soleus Muscle during Functional Unloading. Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology 12:85-91. https://doi.org/10.1134/S1990747818010099

    Article  Google Scholar 

  115. Theeuwes WF, Gosker HR, Langen RCJ, Verhees KJP, Pansters NAM, Schols A, Remels AHV (2017) Inactivation of glycogen synthase kinase-3beta (GSK-3beta) enhances skeletal muscle oxidative metabolism. Biochim Biophys Acta Mol Basis Dis 1863:3075-3086. https://doi.org/10.1016/j.bbadis.2017.09.018

    Article  CAS  PubMed  Google Scholar 

  116. Theeuwes WF, Gosker HR, Schols A, Langen RCJ, Remels AHV (2020) Regulation of PGC-1alpha expression by a GSK-3beta-TFEB signaling axis in skeletal muscle. Biochim Biophys Acta Mol Cell Res 1867:118610. https://doi.org/10.1016/j.bbamcr.2019.118610

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the Russian Science Foundation, grant No. 18-15-00107.

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  1. Institute of Biomedical Problems, Russian Academy of Sciences, Moscow, Russia

    B. S. Shenkman & K. A. Sharlo

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  1. B. S. Shenkman
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The authors equally contributed to the writing of this review.

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Translated by A. Polyanovsky

Russian Text © The Author(s), 2021, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2021, Vol. 107, Nos. 6–7, pp. 669–694https://doi.org/10.31857/S086981392106011X.

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Shenkman, B.S., Sharlo, K.A. How Muscle Activity Controls Slow Myosin Expression. J Evol Biochem Phys 57, 605–625 (2021). https://doi.org/10.1134/S002209302103011X

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