КАК МЫШЕЧНАЯ АКТИВНОСТЬ КОНТРОЛИРУЕТ ЭКСПРЕССИЮ МЕДЛЕННОГО МИОЗИНА
PDF

Ключевые слова

функциональная разгрузка
экспрессия генов
медленный миозин
скелетная мышца

Как цитировать

Шенкман, Б. С., & Шарло, К. А. (2021). КАК МЫШЕЧНАЯ АКТИВНОСТЬ КОНТРОЛИРУЕТ ЭКСПРЕССИЮ МЕДЛЕННОГО МИОЗИНА. Российский физиологический журнал им. И. М. Сеченова, 107(6-7), 669–694. https://doi.org/10.31857/S086981392106011X

Аннотация

Одной из главных гравитационно-обусловленных функций двигательной системы является поддержание вертикальной стойки. Эти функции по представлениям школы профессора И.Б. Козловской обеспечиваются тонической мышечной системой. Под термином «тоническая система» И.Б. Козловская понимала все структуры и регуляторные механизмы, способные длительное время поддерживать базальное механическое напряжение (тонус). У млекопитающих к тонической системе она относила медленные волокна с преобладающей экспрессией медленной изоформы тяжелых цепей миозина типа I(β) - MyHC I(β) и все контролирующие их нервные механизмы. Понятно, что от интенсивности экспрессии медленного миозина зависит способность мышцы длительно поддерживать тоническое напряжение. Поэтому не будет большим преувеличением, если мы назовем ген медленного миозина myh7 истинным геном мышечного тонуса. В последние годы в целом стало понятно, каким образом на фоне длительной повышенной сократительной активности мышцы запускается повышение экспрессии медленной изоформы тяжелых цепей миозина – MyHC I(β) и снижение экспрессии его быстрых изоформ. Гораздо меньше известно о механизмах снижения экспрессии MyHC I(β) при снижении сократительной активности мышцы. Этот феномен наблюдали после экспозиции в реальной невесомости, после постельной гипокинезии (bedrest), «сухой» иммерсии, а также при использовании стандартной модели вывешивания задних конечностей грызунов. Многочисленные исследования пластичности миозинового фенотипа, как правило, сосредоточены на поисках механизмов, связывающих изменения экспрессии миозиновых генов с характером сократительной активности мышечного волокна. Данные, обсужденные в обзоре, свидетельствуют о том, что постоянная экспрессия медленного миозина контролируется тонической активностью и, в свою очередь, является необходимым условием поддержания такой активности. Когда такая активность значительно снижается или прекращается, то исчезают метаболические и механические стимулы, запускающие сигнальные пути, обеспечивающие экспрессию гена myh7. Именно этот феномен и был предметом обсуждения в настоящей работе.

https://doi.org/10.31857/S086981392106011X
PDF

Литература

Козловская ИБ (2017) Гравитация и позно-тоническая мышечная система. Авиакосм и экол мед 51:1021-1025 [ Kozlovskaya IB (2017) Gravitatsiya i pozno-tonicheskaya myshechnaya sistema. Aviakosm i Ekol Med 51:1021-1025 (In Russ)].

Щепкин ДВ, Набиев С, Кубасова НА, Бершицкий СЮ, Копылова ГВ (2020) Сравнение функциональных характеристик миозина быстрой и медленной скелетных мышц. Бюл эксп биол мед 169:113-119 [Shchepkin DV, Nabiyev S, Kubasova NA, Bershitskiy SYU, Kopylova GV (2020) Sravneniye funktsional'nykh kharakteristik miozina bystroy i medlennoy skeletnykh myshts. Buul Eksp Biol Med 169:113-119 (In Russ)].

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 doi:10.1242/jeb.01825

Наследов ГА (1981) Тоническая мышечная система позвоночных СпБ. Наука [Nasledov GA (1981) Tonicheskaya myshechnaya sistema pozvonochnykh. SpB. Nauka (In Russ)].

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

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. doi: 10.1007/BF00233864

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. doi: /10.1023/A:1024473126643

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

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. doi:10.1152/jappl.1999.87.5.1776

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.

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.

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. doi: 10.1152/jappl.1988.65.3.1191.

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. doi:10.3389/fphys.2013.00284

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.

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

Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev1447-1531. doi:10.1152/physrev.00031.2010

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

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. doi:10.1152/jappl.1996.80.1.261

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. doi:10.1152/jappl.1981.50.6.1272

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. doi:10.1007/s004240050730

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. doi: 10.1523/JNEUROSCI.10-01-00153.1990.

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.

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

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. doi:10.1111/j.1748-1716.1993.tb09512.x

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. doi:10.1152/ajpcell.1999.277.6.C1122

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. doi:10.1007/s004249900115

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. doi:10.1249/JES.0000000000000017

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

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. doi:10.1101/gad.12.16.2499.

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. doi:10.1073/pnas.0308035101

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. doi:10.1242/jcs.02875

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. doi:10.1073/pnas.0812911106

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. doi:10.1186/s12899-014-0007-z

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. doi:10.1079/PNS2004335

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. doi:10.1152/physiolgenomics.00286.2006

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. doi:10.1093/emboj/18.18.5099

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. doi:10.14348/molcells.2015.2278

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. doi:10.1093/emboj/20.22.6414

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. doi:10.1016/j.yexcr.2012.12.016

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. doi:10.1083/jcb.200412156

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

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. doi:10.1073/pnas.140199597

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. doi:10.1083/jcb.200408128

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. doi:10.1073/pnas.252625599

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. doi:10.1152/ajpcell.1988.255.4.C543

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. doi:10.1007/s004210050182

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. doi:10.1139/apnm-2014-0300

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. doi:10.1152/ajpcell.00523.2007

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. doi:10.1152/jappl.1997.82.4.1250

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. doi: 10.1152/ajpcell.1998.275.1.C260

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. doi:10.1016/j.freeradbiomed.2014.10.505

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 Pysiol 579:535-551. doi:10.1113/jphysiol.2006.120048

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. doi:10.1113/jphysiol.2011.223370

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. doi:10.1016/j.devcel.2009.10.013

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. doi:10.1152/physiolgenomics.00042.2009

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. doi:10.1128/MCB.00629-06

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. doi:10.1016/j.lfs.2018.11.020

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. doi:10.1038/srep26415

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. doi:10.1113/jphysiol.2010.188508

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

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

Шульженко ЕБ, Виль-Вильямс ИФ (1976) Возможность проведения длительной водной иммерсии методом «сухого» погружения. Косм биол авиакосм мед 10: 82-84 [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)].

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

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.

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. doi: /10.1016/0014-4886(87)90225-1

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

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

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

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

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

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. doi:10.1242/jeb.01931

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

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. doi:10.1113/JP275184

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. doi:10.1016/j.nbd.2004.09.016

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. doi:10.1007/s10974-015-9428-y

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. doi: 10.1016/s0014-5793(99)01596-3.

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. doi:10.1152/ajpcell.1999.277.6.C1044

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. doi:10.1134/S0006297911050075

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. doi:10.1159/000447808

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. doi: /10.1016/0094-5765(94)90115-5

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. doi:10.1016/j.cmet.2008.11.008

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

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 doi: 10.2170/jjphysiol.44.193

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.

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. doi:10.1152/japplphysiol.00029.2019

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. doi: 10.31857/S0233475520020097

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.

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. JAppl Physiol 126:1769-1781. doi: 10.1152/japplphysiol.00029.2019

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. doi:10.3389/fphys.2020.00814

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. doi:10.1016/j.molmet.2015.09.004

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

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. doi:10.1152/jappl.1999.87.1.386

Arutyunyan R S Kozlovskaya I B, Nasledov G A, Nemirovskaya T L, Radzyukevitch T L, Shenkman B S (1995) The contraction of unweighted fast and slow rat muscles in calcium-free solution. Basic Appl Myol 5:169-175.

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.

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. doi:10.1016/j.abb.2020.108622

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. doi:10.1074/jbc.M611252200

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. doi:3390/ijms22031372

Мухина АМ, Алтаева ЭГ, Немировская ТЛ, Шенкман БС (2006) Роль кальциевых каналов L-типа в накоплении Са2+ в волокнах m. soleus крысы и изменении соотношения изоформ миозина и SERCA при гравитационной разгрузке. Рос физиол журн 92:1285-1295. [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)].

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. doi:10.1113/JP271705

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. doi:10.1152/ajpcell.00424.2001

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. doi:10.1007/s00418-010-0744-4

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. doi:10.1093/nar/gkr162

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. doi:10.1074/jbc.M700264200

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. doi:10.1152/ajpcell.00075.2009

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

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. doi:10.1074/jbc.C000304200

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. doi:

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.

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

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

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. doi:10.15252/emmm.201606372

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. doi:10.1074/jbc.M704817200

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. doi:10.1038/nature00904

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. doi:https://doi.org/10.1134/S1990747818010099

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. doi:10.1016/j.bbadis.2017.09.018

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. doi:10.1016/j.bbamcr.2019.118610