Аннотация
Широко известно, что как в реальных, так и в моделируемых условиях микрогравитации происходит снижение уровня окислительного метаболизма в скелетных мышцах человека и животных. В последние годы стало известно, что одним из последствий снижения уровня окислительного метаболизма в тканях может являться изменение эпигенетического статуса некоторых генов, а также накоплены данные, позволяющие предположить важную роль эпигенетического контроля экспрессии ряда генов в развитии негативных изменений, происходящих с мышцей в условиях реальной или моделируемой микрогравитации. Обзор посвящен анализу и систематизации данных о состоянии окислительного метаболизма и эпигенетического контроля экспрессии генов в скелетных мышцах в условиях функциональной разгрузки, рассмотрению молекулярных взаимосвязей между ключевыми регуляторами окислительного метаболизма и эпигенетическими модификациями и формулированию гипотезы о роли окислительного метаболизма в эпигенетическом блокировании экспрессии ряда генов, определяющих медленный, устойчивый к утомлению фенотип мышечных волокон.
Литература
Memme JM, Slavin M, Moradi N, Hood DA (2021) Mitochondrial Bioenergetics and Turnover during Chronic Muscle Disuse. Int J Mol Sci 22 (10):10.3390/ijms22105179
Romanello V, Sandri M (2021) The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass. Cell Mol Life Sci 78 (4):1305-1328. https://doi.org/10.1007/s00018-020-03662-0
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.
Desplanches D, Mayet MH, Sempore B, Flandrois R (1987) Structural and functional responses to prolonged hindlimb suspension in rat muscle. J Appl Physiol (1985) 63 (2):558-563. https://doi.org/10.1152/jappl.1987.63.2.558
Hirayama Y, Nakanishi R, Maeshige N, Fujino H (2017) Preventive effects of nucleoprotein supplementation combined with intermittent loading on capillary regression induced by hindlimb unloading in rat soleus muscle. Physiol Rep 5 (4):10.14814/phy2.13134.
Fell RD, Steffen JM, Musacchia XJ (1985) Effect of hypokinesia-hypodynamia on rat muscle oxidative capacity and glucose uptake. Am J Physiol 249 (3 Pt 2):R308-R312. https://doi.org/10.1152/ajpregu.1985.249.3.R308
Nagatomo F, Fujino H, Kondo H, Suzuki H, Kouzaki M, Takeda I, Ishihara A (2011) PGC-1alpha and FOXO1 mRNA levels and fiber characteristics of the soleus and plantaris muscles in rats after hindlimb unloading. Histol Histopathol 26 (12):1545-1553. https://doi.org/10.14670/HH-26.1545
Fitts RH, Brimmer CJ, Heywood-Cooksey A, Timmerman RJ (1989) Single muscle fiber enzyme shifts with hindlimb suspension and immobilization. Am J Physiol 256 (5 Pt 1):C1082-C1091. https://doi.org/10.1152/ajpcell.1989.256.5.C1082
Ohira T, Kawano F, Ohira T, Goto K, Ohira Y (2015) Responses of skeletal muscles to gravitational unloading and/or reloading. J Physiol Sci 65 (4):293-310. https://doi.org/10.1007/s12576-015-0375-6
Yajid F, Mercier JG, Mercier BM, Dubouchaud H, Prefaut C (1998) Effects of 4 wk of hindlimb suspension on skeletal muscle mitochondrial respiration in rats. J Appl Physiol (1985) 84 (2):479-485. https://doi.org/10.1152/jappl.1998.84.2.479
Zhang X, Trevino MB, Wang M, Gardell SJ, Ayala JE, Han X, Kelly DP, Goodpaster BH, Vega RB, Coen PM (2018) Impaired Mitochondrial Energetics Characterize Poor Early Recovery of Muscle Mass Following Hind Limb Unloading in Old Mice. J Gerontol A Biol Sci Med Sci 73 (10):1313-1322. https://doi.org/10.1093/gerona/gly051
Шенкман БС, Матвеева ОА, Мазин МГ, Немировская ТЛ, Киселева ЕВ, Козловская ИБ (2003) Пластичность клеточных и тканевых структур m. soleus человека в условиях длительной гипокинезии. Биол мембр 20 (1):77-86. [Shenkman BS, Matveyeva OA, Mazin MG, Nemirovskaya TL, Kiseleva YEV, Kozlovskaya IB (2003) Plasticity of cellular and tissue structures m. human soleus under conditions of prolonged hypokinesia. Biol membr 20 (1):77-86. (In Russ)].
Шенкман Б, Виноградова О, Мазин М, Киселева Е, Белозерова И, Немировская Т, Трушева Т, Тихомиров Е (2003) Физиологическая стоимость физической нагрузки и объем митохондрий рабочих мышц у людей в условиях длительной гипокинезии. Эффекты резистивных локальных нагрузок. Физиология человека 29 (2):75-80. [Shenkman B, Vinogradova O, Mazin M, Kiseleva Ye, Belozerova I, Nemirovskaya T, Trusheva T, Tikhomirov Ye (2003) Physiological cost of physical activity and mitochondrial volume of working muscles in humans under conditions of prolonged hypokinesia. Effects of resistive local load. Human Pysiol 29 (2):75-80.(In Russ)].
Trevino MB, Zhang X, Standley RA, Wang M, Han X, Reis FCG, Periasamy M, Yu G, Kelly DP, Goodpaster BH, Vega RB, Coen PM (2019) Loss of mitochondrial energetics is associated with poor recovery of muscle function but not mass following disuse atrophy. Am J Physiol Endocrinol Metab 317 (5):E899-E910. https://doi.org/10.1152/ajpendo.00161.2019
Lechado ITA, Vitadello M, Traini L, Namuduri AV, Gastaldello S, Gorza L (2018) Sarcolemmal loss of active nNOS (Nos1) is an oxidative stress-dependent, early event driving disuse atrophy. J Pathol 246 (4):433-446. https://doi.org/10.1002/path.5149
Gomez-Cabrera MC, Arc-Chagnaud C, Salvador-Pascual A, Brioche T, Chopard A, Olaso-Gonzalez G, Vina J (2020) Redox modulation of muscle mass and function. Redox Biol 35 101531. https://doi.org/10.1016/j.redox.2020.101531
Max SR (1972) Disuse atrophy of skeletal muscle: loss of functional activity of mitochondria. Biochem Biophys Res Commun 46 (3):1394-1398. https://doi.org/10.1016/s0006-291x(72)80130-x
Larsen S, Lundby AM, Dandanell S, Oberholzer L, Keiser S, Andersen AB, Haider T, Lundby C (2018) Four days of bed rest increases intrinsic mitochondrial respiratory capacity in young healthy males. Physiol Rep 6 (18):e13793. https://doi.org/10.14814/phy2.13793
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 (12):3075-3086. https://doi.org/10.1016/j.bbadis.2017.09.018
Liu J, Peng Y, Cui Z, Wu Z, Qian A, Shang P, Qu L, Li Y, Liu J, Long J (2012) Depressed mitochondrial biogenesis and dynamic remodeling in mouse tibialis anterior and gastrocnemius induced by 4-week hindlimb unloading. IUBMB Life 64 (11):901-910. https://doi.org/10.1002/iub.1087
Standley RA, Distefano G, Trevino MB, Chen E, Narain NR, Greenwood B, Kondakci G, Tolstikov VV, Kiebish MA, Yu G, Qi F, Kelly DP, Vega RB, Coen PM, Goodpaster BH (2020) Skeletal Muscle Energetics and Mitochondrial Function Are Impaired Following 10 Days of Bed Rest in Older Adults. J Gerontol A Biol Sci Med Sci 75 (9):1744-1753. https://doi.org/10.1093/gerona/glaa001
Bilet L, Phielix E, van de Weijer T, Gemmink A, Bosma M, Moonen-Kornips E, Jorgensen JA, Schaart G, Zhang D, Meijer K, Hopman M, Hesselink MKC, Ouwens DM, Shulman GI, Schrauwen-Hinderling VB, Schrauwen P (2020) One-leg inactivity induces a reduction in mitochondrial oxidative capacity, intramyocellular lipid accumulation and reduced insulin signalling upon lipid infusion: a human study with unilateral limb suspension. Diabetologia 63 (6):1211-1222. https://doi.org/10.1007/s00125-020-05128-1
Connor MK, Hood DA (1998) Effect of microgravity on the expression of mitochondrial enzymes in rat cardiac and skeletal muscles. J Appl Physiol (1985) 84 (2):593-598. https://doi.org/10.1152/jappl.1998.84.2.593
Tascher G, Brioche T, Maes P, Chopard A, O'Gorman D, Gauquelin-Koch G, Blanc S, Bertile F (2017) Proteome-wide Adaptations of Mouse Skeletal Muscles during a Full Month in Space. J Proteome Res 16 (7):2623-2638. https://doi.org/10.1021/acs.jproteome.7b00201
Mazin MG, Kiselyova EV, Nemirovskaya TL, Shenkman BS (2000) Ultrastructure of skeletal muscles of rhesus monkeys after spaceflight. J Gravit Physiol 7 (1):S59-S62.
Shenkman BS, Nemirovskaya TL, Belozerova IN, Mazin MG, Matveeva OA (2002) Mitochondrial adaptations in skeletal muscle cells in mammals exposed to gravitational unloading. J Gravit Physiol 9 (1):159-162.
Desplanches D, Kayar SR, Sempore B, Flandrois R, Hoppeler H (1990) Rat soleus muscle ultrastructure after hindlimb suspension. J Appl Physiol (1985) 69 (2):504-508. https://doi.org/10.1152/jappl.1990.69.2.504
Shenkman BS (2020) How Postural Muscle Senses Disuse? Early Signs and Signals. Int J Mol Sci 21 (14):10.3390/ijms21145037.
Ingalls CP, Warren GL, Armstrong RB (1999) Intracellular Ca2+ transients in mouse soleus muscle after hindlimb unloading and reloading. J Appl Physiol (1985) 87 (1):386-390. https://doi.org/10.1152/jappl.1999.87.1.386
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 (23):7123-7134. https://doi.org/10.1113/JP275184
Kravtsova VV, Matchkov VV, Bouzinova EV, Vasiliev AN, Razgovorova IA, Heiny JA, Krivoi, II (2015) Isoform-specific Na,K-ATPase alterations precede disuse-induced atrophy of rat soleus muscle. Biomed Res Int 2015 (720172. https://doi.org/10.1155/2015/720172
Krivoi, II, Kravtsova VV, Altaeva EG, Kubasov IV, Prokof'ev AV, Drabkina TM, Nikol'skii EE, Shenkman BS (2008) [Decrease in the electrogenic contribution of Na,K-ATPase and resting membrane potential as a possible mechanism of calcium ion accumulation in filaments of the rat musculus soleus subjected to the short-term gravity unloading]. Biofizika 53 (6):1051-1057.
Henriksen EJ, Tischler ME (1988) Time course of the response of carbohydrate metabolism to unloading of the soleus. Metabolism 37 (3):201-208.
Vilchinskaya NA, Mirzoev TM, Lomonosova YN, Kozlovskaya IB, Shenkman BS (2015) Human muscle signaling responses to 3-day head-out dry immersion. J Musculoskelet Neuronal Interact 15 (3):286-293.
Zaripova KA, Kalashnikova EP, Kostrominova TY,Shenkman BS, Nemirovskaya TL (2021) Role of Pannexin 1 ATP-Permeable Channels in the Regulation of Signaling Pathways during Skeletal Muscle Unloading. Int J Mol Sci 22(19):10444. https://doi.org/10.3390/ijms221910444
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 (5):471-476.
Shenkman BS, Nemirovskaya TL (2008) Calcium-dependent signaling mechanisms and soleus fiber remodeling under gravitational unloading. J Muscle Res Cell Motil 29 (6-8):221-230. https://doi.org/10.1007/s10974-008-9164-7
Li A, Yi J, Li X, Zhou J (2020) Physiological Ca(2+) Transients Versus Pathological Steady-State Ca(2+) Elevation, Who Flips the ROS Coin in Skeletal Muscle Mitochondria. Front Physiol 11 595800. https://doi.org/10.3389/fphys.2020.595800
Karam C, Yi J, Xiao Y, Dhakal K, Zhang L, Li X, Manno C, Xu J, Li K, Cheng H, Ma J, Zhou J (2017) Absence of physiological Ca(2+) transients is an initial trigger for mitochondrial dysfunction in skeletal muscle following denervation. Skelet Muscle 7 (1):6. https://doi.org/10.1186/s13395-017-0123-0
Andersson DC, Betzenhauser MJ, Reiken S, Meli AC, Umanskaya A, Xie W, Shiomi T, Zalk R, Lacampagne A, Marks AR (2011) Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab 14 (2):196-207. https://doi.org/10.1016/j.cmet.2011.05.014
Matecki S, Dridi H, Jung B, Saint N, Reiken SR, Scheuermann V, Mrozek S, Santulli G, Umanskaya A, Petrof BJ, Jaber S, Marks AR, Lacampagne A (2016) Leaky ryanodine receptors contribute to diaphragmatic weakness during mechanical ventilation. Proc Natl Acad Sci U S A 113 (32):9069-9074. https://doi.org/10.1073/pnas.1609707113
Sharlo K, Lvova I, Turtikova O, Tyganov S, Kalashnikov V, Shenkman B (2022) Plantar stimulation prevents the decreases in fatigue resistance and mitochondrial biogenesis in rat m soleus under 7 days of hindlimb suspension. Arch Biochem Biophys 718 (142):109-150. https://doi.org/10.1016/j.abb.2022.109150
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
Agnetti G, Herrmann H, Cohen S (2021) New roles for desmin in the maintenance of muscle homeostasis. FEBS J 10.1111/febs.15864.
Milner DJ, Mavroidis M, Weisleder N, Capetanaki Y (2000) Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J Cell Biol 150 (6):1283-1298. https://doi.org/10.1083/jcb.150.6.1283
Petrova IO, Tyganov SA, Mirzoev TM, Tsaturyan AK, Kozlovskaya IB, Shenkman BS (2018) Early Desmall es, Cyrillicline in Rat Soleus Passive Tension with Hindlimb Unloading: Inactivation of Cross-bridges or Activation of Calpains? Dokl Biochem Biophys 481 (1):205-207. https://doi.org/10.1134/S1607672918040075
Миpзоев ТМ, Веcелова ОМ, Лаpина ИМ, Шенкман БС, Огнева ИВ (2012) Паpаметpы клеточного дыxания волокон и cодеpжание деcмина в камбаловидной мышце кpыcы на pанниx этапаx гpавитационной pазгpузки. Биофизика 57 (3):509-514. [Mirzoyev TM, Vecelova OM, Larina IM, Shenkman BS, Ogneva IV (2012) Parameters of cellular respiration of fibers and the content of desmin in the rat soleus muscle at the early stage of gravitational unloading. Biofizika 57 (3):509-514. (In Russ)].
Hyatt HW, Ozdemir M, Yoshihara T, Nguyen BL, Deminice R, Powers SK (2021) Calpains play an essential role in mechanical ventilation-induced diaphragmatic weakness and mitochondrial dysfunction. Redox Biol 38 101802. https://doi.org/10.1016/j.redox.2020.101802
Herzig S, Shaw RJ (2018) AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 19 (2):121-135. https://doi.org/10.1038/nrm.2017.95
Adams GR, Haddad F, Baldwin KM (1994) Interaction of chronic creatine depletion and muscle unloading: effects on postural locomotor muscles. J Appl Physiol (1985) 77 (3):1198-1205. https://doi.org/10.1152/jappl.1994.77.3.1198
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 (3):1011-1020. https://doi.org/10.1159/000447808
Gupta RC, Misulis KE, Dettbarn WD (1989) Activity dependent characteristics of fast and slow muscle: biochemical and histochemical considerations. Neurochem Res 14 (7):647-655. https://doi.org/10.1007/BF00964874
Tyganov SA, Mochalova EP, Belova SP, Sharlo KA, Rozhkov SV, Vilchinskaya NA, Paramonova II, Mirzoev TM, Shenkman BS (2019) Effects of Plantar Mechanical Stimulation on Anabolic and Catabolic Signaling in Rat Postural Muscle Under Short-Term Simulated Gravitational Unloading. Front Physiol 10:1252. https://doi.org/10.3389/fphys.2019.01252
Rosa-Caldwell ME, Brown JL, Perry RA Jr, Shimkus KL, Shirazi-Fard Y, Brown LA, Hogan HA, Fluckey JD, Washington TA, Wiggs MP, Greene NP (2020) Regulation of mitochondrial quality following repeated bouts of hindlimb unloading. Appl Physiol Nutr Metab 45 (3):264-274. https://doi.org/10.1139/apnm-2019-0218
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
Theilen NT, Jeremic N, Weber GJ, Tyagi SC (2018) Exercise preconditioning diminishes skeletal muscle atrophy after hindlimb suspension in mice. J Appl Physiol (1985) 125 (4):999-1010. https://doi.org/10.1152/japplphysiol.00137.2018
Qi Z, Zhang Y, Guo W, Ji L, Ding S (2012) Increased insulin sensitivity and distorted mitochondrial adaptations during muscle unloading. Int J Mol Sci 13 (12):16971-16985. https://doi.org/10.3390/ijms131216971
Kang C, Ji LL (2013) Muscle immobilization and remobilization downregulates PGC-1alpha signaling and the mitochondrial biogenesis pathway. J Appl Physiol (1985) 115 (11):1618-1625. https://doi.org/10.1152/japplphysiol.01354.2012
Gambara G, Salanova M, Ciciliot S, Furlan S, Gutsmann M, Schiffl G, Ungethuem U, Volpe P, Gunga HC, Blottner D (2017) Gene Expression Profiling in Slow-Type Calf Soleus Muscle of 30 Days Space-Flown Mice. PLoS One 12 (1):e0169314. https://doi.org/10.1371/journal.pone.0169314
Buso A, Comelli M, Picco R, Isola M, Magnesa B, Pisot R, Rittweger J, Salvadego D, Simunic B, Grassi B, Mavelli I (2019) Mitochondrial Adaptations in Elderly and Young Men Skeletal Muscle Following 2 Weeks of Bed Rest and Rehabilitation. Front Physiol 10:474. https://doi.org/10.3389/fphys.2019.00474
Fernandez-Gonzalo R, Irimia JM, Cusso R, Gustafsson T, Linne A, Tesch PA (2014) Flywheel resistance exercise to maintain muscle oxidative potential during unloading. Aviat Space Environ Med 85 (7):694-699. https://doi.org/10.3357/asem.3856.2014
Rittweger J, Albracht K, Fluck M, Ruoss S, Brocca L, Longa E, Moriggi M, Seynnes O, Di Giulio I, Tenori L, Vignoli A, Capri M, Gelfi C, Luchinat C, Francheschi C, Bottinelli R, Cerretelli P, Narici M (2018) Sarcolab pilot study into skeletal muscle's adaptation to long-term spaceflight. NPJ Microgravity 4:18. https://doi.org/10.1038/s41526-018-0052-1
Wagatsuma A, Kotake N, Kawachi T, Shiozuka M, Yamada S, Matsuda R (2011) Mitochondrial adaptations in skeletal muscle to hindlimb unloading. Mol Cell Biochem 350 (1-2):1-11. https://doi.org/10.1007/s11010-010-0677-1
Kenny HC, Tascher G, Ziemianin A, Rudwill F, Zahariev A, Chery I, Gauquelin-Koch G, Barielle MP, Heer M, Blanc S, O'Gorman DJ, Bertile F (2020) Effectiveness of Resistive Vibration Exercise and Whey Protein Supplementation Plus Alkaline Salt on the Skeletal Muscle Proteome Following 21 Days of Bed Rest in Healthy Males. J Proteome Res 19 (8):3438-3451. https://doi.org/10.1021/acs.jproteome.0c00256
Cho Y, Hazen BC, Gandra PG, Ward SR, Schenk S, Russell AP, Kralli A (2016) Perm1 enhances mitochondrial biogenesis, oxidative capacity, and fatigue resistance in adult skeletal muscle. FASEB J 30 (2):674-687. https://doi.org/10.1096/fj.15-276360
Lvova ID, Sharlo KA, Rozhkov SV, Mirzoev TM, Shenkman BS (2021) The Role of Glycogen Synthase Kinase 3 Activity in the Regulation of Mitochondrial Biogenesis in Rat Postural Muscle under Hindlimb Unloading. Biochemistry (Moscow) Suppl SerA: Membr Cell Biol 16 (372-377. https://doi.org/ 10.31857/S0233475521060074
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 (1-2):7-16. https://doi.org/10.1007/s10974-015-9428-y
Leermakers PA, Kneppers AEM, Schols A, Kelders M, de Theije CC, Verdijk LB, van Loon LJC, Langen RCJ, Gosker HR (2019) Skeletal muscle unloading results in increased mitophagy and decreased mitochondrial biogenesis regulation. Muscle Nerve 60 (6):769-778. https://doi.org/10.1002/mus.26702
Rosa-Caldwell ME, Lim S, Haynie WS, Brown JL, Lee DE, Dunlap KR, Jansen LT, Washington TA, Wiggs MP, Greene NP (2021) Mitochondrial aberrations during the progression of disuse atrophy differentially affect male and female mice. J Cachexia Sarcopenia Muscle 12 (6):2056-2068. https://doi.org/10.1002/jcsm.12809
Kang C, Ji LL (2016) PGC-1alpha overexpression via local transfection attenuates mitophagy pathway in muscle disuse atrophy. Free Radic Biol Med 93:32-40. https://doi.org/10.1016/j.freeradbiomed.2015.12.032
Drake JC, Wilson RJ, Laker RC, Guan Y, Spaulding HR, Nichenko AS, Shen W, Shang H, Dorn MV, Huang K, Zhang M, Bandara AB, Brisendine MH, Kashatus JA, Sharma PR, Young A, Gautam J, Cao R, Wallrabe H, Chang PA, Wong M, Desjardins EM, Hawley SA, Christ GJ, Kashatus DF, Miller CL, Wolf MJ, Periasamy A, Steinberg GR, Hardie DG, Yan Z (2021) Mitochondria-localized AMPK responds to local energetics and contributes to exercise and energetic stress-induced mitophagy. Proc Natl Acad Sci U S A 118 (37):10.1073/pnas.2025932118
Kang C, Yeo D, Ji LL (2016) Muscle immobilization activates mitophagy and disrupts mitochondrial dynamics in mice. Acta Physiol (Oxf) 218 (3):188-197. https://doi.org/10.1111/apha.12690
Standley RA, Distefano G, Pereira SL, Tian M, Kelly OJ, Coen PM, Deutz NEP, Wolfe RR, Goodpaster BH (2017) Effects of beta-hydroxy-beta-methylbutyrate on skeletal muscle mitochondrial content and dynamics, and lipids after 10 days of bed rest in older adults. J Appl Physiol (1985) 123 (5):1092-1100. https://doi.org/10.1152/japplphysiol.00192.2017
Zorzano A (2009) Regulation of mitofusin-2 expression in skeletal muscle. Appl Physiol Nutr Metab 34 (3):433-439. https://doi.org/10.1139/H09-049
Gowher H, Jeltsch A (2018) Mammalian DNA methyltransferases: new discoveries and open questions. Biochem Soc Trans 46 (5):1191-1202. https://doi.org/10.1042/BST20170574
Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324 (5929):930-935. https://doi.org/10.1126/science.1170116
Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333 (6047):1300-1303. https://doi.org/10.1126/science.1210597
An J, Rao A, Ko M (2017) TET family dioxygenases and DNA demethylation in stem cells and cancers. Exp Mol Med 49 (4):e323. https://doi.org/10.1038/emm.2017.5
Bird A, Taggart M, Frommer M, Miller OJ, Macleod D (1985) A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell 40 (1):91-99. https://doi.org/10.1016/0092-8674(85)90312-5
Saxonov S, Berg P, Brutlag DL (2006) A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci U S A 103 (5):1412-1417. https://doi.org/10.1073/pnas.0510310103
Moore LD, Le T, Fan G (2013) DNA methylation and its basic function. Neuropsychopharmacology 38 (1):23-38. https://doi.org/10.1038/npp.2012.112
Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T (2000) DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24 (1):88-91. https://doi.org/10.1038/71750
Titcombe P, Murray R, Hewitt M, Antoun E, Cooper C, Inskip HM, Holbrook JD, Godfrey KM, Lillycrop K, Hanson M, Barton SJ (2021) Human non-CpG methylation patterns display both tissue-specific and inter-individual differences suggestive of underlying function. Epigenetics 1-12. https://doi.org/10.1080/15592294.2021.1950990
Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329 (5990):444-448. https://doi.org/10.1126/science.1190485
A FCL (2020) Mitochondrial metabolism and DNA methylation: a review of the interaction between two genomes. Clin Epigenetics 12 (1):182. https://doi.org/10.1186/s13148-020-00976-5
Salminen A, Kauppinen A, Hiltunen M, Kaarniranta K (2014) Krebs cycle intermediates regulate DNA and histone methylation: epigenetic impact on the aging process. Ageing Res Rev 16:45-65. https://doi.org/10.1016/j.arr.2014.05.004
Yang Q, Liang X, Sun X, Zhang L, Fu X, Rogers CJ, Berim A, Zhang S, Wang S, Wang B, Foretz M, Viollet B, Gang DR, Rodgers BD, Zhu MJ, Du M (2016) AMPK/alpha-Ketoglutarate Axis Dynamically Mediates DNA Demethylation in the Prdm16 Promoter and Brown Adipogenesis. Cell Metab 24 (4):542-554. https://doi.org/10.1016/j.cmet.2016.08.010
Wu D, Hu D, Chen H, Shi G, Fetahu IS, Wu F, Rabidou K, Fang R, Tan L, Xu S, Liu H, Argueta C, Zhang L, Mao F, Yan G, Chen J, Dong Z, Lv R, Xu Y, Wang M, Ye Y, Zhang S, Duquette D, Geng S, Yin C, Lian CG, Murphy GF, Adler GK, Garg R, Lynch L, Yang P, Li Y, Lan F, Fan J, Shi Y, Shi YG (2018) Glucose-regulated phosphorylation of TET2 by AMPK reveals a pathway linking diabetes to cancer. Nature 559 (7715):637-641. https://doi.org/10.1038/s41586-018-0350-5
Zhang T, Guan X, Choi UL, Dong Q, Lam MMT, Zeng J, Xiong J, Wang X, Poon TCW, Zhang H, Zhang X, Wang H, Xie R, Zhu B, Li G (2019) Phosphorylation of TET2 by AMPK is indispensable in myogenic differentiation. Epigen Chromatin 12 (1):32. https://doi.org/10.1186/s13072-019-0281-x
Matuleviciute R, Cunha PP, Johnson RS, Foskolou IP (2021) Oxygen regulation of TET enzymes. FEBS J 288 (24):7143-7161. https://doi.org/10.1111/febs.15695
Zhong T, Men Y, Lu L, Geng T, Zhou J, Mitsuhashi A, Shozu M, Maihle NJ, Carmichael GG, Taylor HS, Huang Y (2017) Metformin alters DNA methylation genome-wide via the H19/SAHH axis. Oncogene 36 (17):2345-2354. https://doi.org/10.1038/onc.2016.391
Marin TL, Gongol B, Zhang F, Martin M, Johnson DA, Xiao H, Wang Y, Subramaniam S, Chien S, Shyy JY (2017) AMPK promotes mitochondrial biogenesis and function by phosphorylating the epigenetic factors DNMT1, RBBP7, and HAT1. Sci Signal 10 (464):eaaf 7478. https://doi.org/10.1126/scisignal.aaf7478
Cao K, Lv W, Wang X, Dong S, Liu X, Yang T, Xu J, Zeng M, Zou X, Zhao D, Ma Q, Lin M, Long J, Zang W, Gao F, Feng Z, Liu J (2021) Hypermethylation of Hepatic Mitochondrial ND6 Provokes Systemic Insulin Resistance. Adv Sci (Weinh) 8 (11):2004507. https://doi.org/10.1002/advs.202004507
Furukawa T, Tanimoto K, Fukazawa T, Imura T, Kawahara Y, Yuge L (2018) Simulated microgravity attenuates myogenic differentiation via epigenetic regulations. NPJ Microgravity 4:11. https://doi.org/10.1038/s41526-018-0045-0
Tomiga Y, Ito A, Sudo M, Ando S, Eshima H, Sakai K, Nakashima S, Uehara Y, Tanaka H, Soejima H, Higaki Y (2019) One week, but not 12 hours, of cast immobilization alters promotor DNA methylation patterns in the nNOS gene in mouse skeletal muscle. J Physiol 597 (21):5145-5159. https://doi.org/10.1113/JP277019
Alibegovic AC, Sonne MP, Hojbjerre L, Bork-Jensen J, Jacobsen S, Nilsson E, Faerch K, Hiscock N, Mortensen B, Friedrichsen M, Stallknecht B, Dela F, Vaag A (2010) Insulin resistance induced by physical inactivity is associated with multiple transcriptional changes in skeletal muscle in young men. Am J Physiol Endocrinol Metab 299 (5):E752-E763. https://doi.org/10.1152/ajpendo.00590.2009
Begue G, Raue U, Jemiolo B, Trappe S (2017) DNA methylation assessment from human slow- and fast-twitch skeletal muscle fibers. J Appl Physiol (1985) 122 (4):952-967. https://doi.org/10.1152/japplphysiol.00867.2016
Rye PT, Frick LE, Ozbal CC, Lamarr WA (2011) Advances in label-free screening approaches for studying histone acetyltransferases. J Biomol Screen 16 (10):1186-1195. https://doi.org/10.1177/1087057111418653
Graff J, Tsai LH (2013) Histone acetylation: molecular mnemonics on the chromatin. Nat Rev Neurosci 14 (2):97-111. https://doi.org/10.1038/nrn3427
Sun XJ, Man N, Tan Y, Nimer SD, Wang L (2015) The Role of Histone Acetyltransferases in Normal and Malignant Hematopoiesis. Front Oncol 5:108. https://doi.org/10.3389/fonc.2015.00108
Tian H, Liu S, Ren J, Lee JKW, Wang R, Chen P (2020) Role of Histone Deacetylases in Skeletal Muscle Physiology and Systemic Energy Homeostasis: Implications for Metabolic Diseases and Therapy. Front Physiol 11:949. https://doi.org/10.3389/fphys.2020.00949
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 (6):887-897. https://doi.org/10.1083/jcb.200408128
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.
Shimazu T, Hirschey MD, Newman J, He W, Shirakawa K, Le Moan N, Grueter CA, Lim H, Saunders LR, Stevens RD, Newgard CB, Farese RV, Jr., de Cabo R, Ulrich S, Akassoglou K, Verdin E (2013) Suppression of oxidative stress by beta-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 339 (6116):211-214. https://doi.org/10.1126/science.1227166
Ruderman NB, Xu XJ, Nelson L, Cacicedo JM, Saha AK, Lan F, Ido Y (2010) AMPK and SIRT1: a long-standing partnership? Am J Physiol Endocrinol Metab 298 (4):E751-E760. https://doi.org/10.1152/ajpendo.00745.2009
Chen J, Wang Y, Hamed M, Lacroix N, Li Q (2015) Molecular Basis for the Regulation of Transcriptional Coactivator p300 in Myogenic Differentiation. Sci Rep 5:13727. https://doi.org/10.1038/srep13727
Poizat C, Puri PL, Bai Y, Kedes L (2005) Phosphorylation-dependent degradation of p300 by doxorubicin-activated p38 mitogen-activated protein kinase in cardiac cells. Mol Cell Biol 25 (7):2673-2687. https://doi.org/10.1128/MCB.25.7.2673-2687.2005
Galdieri L, Gatla H, Vancurova I, Vancura A (2016) Activation of AMP-activated Protein Kinase by Metformin Induces Protein Acetylation in Prostate and Ovarian Cancer Cells. J Biol Chem 291 (48):25154-25166. https://doi.org/10.1074/jbc.M116.742247
Paramonova II, Vilchinskaya NA, Shenkman BS (2021) HDAC4 Is Indispensable for Reduced Slow Myosin Expression at the Early Stage of Hindlimb Unloading in Rat Soleus Muscle. Pharmaceuticals (Basel) 14 (11):10.3390/ph14111167.
Yoshihara T, Machida S, Kurosaka Y, Kakigi R, Sugiura T, Naito H (2016) Immobilization induces nuclear accumulation of HDAC4 in rat skeletal muscle. J Physiol Sci 66 (4):337-343. https://doi.org/10.1007/s12576-015-0432-1
Mochalova EP, Belova SP, Mirzoev TM, Shenkman BS, Nemirovskaya TL (2019) Atrogin-1/MAFbx mRNA expression is regulated by histone deacetylase 1 in rat soleus muscle under hindlimb unloading. Sci Rep 9 (1):10263. https://doi.org/10.1038/s41598-019-46753-0
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. (3):10.3390/ijms22031372
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 (1):C6-C16. https://doi.org/10.1152/ajpcell.00075.2009