Abstract
Skeletal muscle is made of heterogeneous myofibers with different contractile and metabolic properties. The diverse functionality of myofibers enables skeletal muscle to carry out different tasks from maintaining body posture to performing active movements. In addition to motility, skeletal muscle, which constitutes 40% of body mass, is also a key target of insulin action and performs an essential function in glucose metabolism. Adult skeletal muscle is a highly adaptive organ system and can undergo specific changes in contractile and metabolic properties to meet different functional demands. This plasticity of myofibers reflects a highly coordinated change in gene expression program that is controlled by neural activity. The capacity for on-demand remodeling confers skeletal muscle the remarkable adaptability important for animal survival; its dysregulation, however, could contribute to muscle and metabolic diseases. How neural activity dictates transcriptional programming to modify muscle functionality and diversity is a fundamental issue. Recent studies have identified members of class IIa HDACs as important effectors in both physiological and pathological muscle remodeling. By way of modifying myofiber properties, pharmacological manipulation of IIa HDACs activity could have potential therapeutic utility in the treatment of muscle disorders.
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References
Alderton JM, Steinhardt RA (2000) Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J Biol Chem 275(13):9452–9460
Al-Khalili L et al (2005) Enhanced insulin-stimulated glycogen synthesis in response to insulin, metformin or rosiglitazone is associated with increased mRNA expression of GLUT4 and peroxisomal proliferator activator receptor gamma co-activator 1. Diabetologia 48(6):1173–1179
Aronson D, Dufresne SD, Goodyear LJ (1997) Contractile activity stimulates the c-Jun NH2-terminal kinase pathway in rat skeletal muscle. J Biol Chem 272(41):25636–25640
Backs J et al (2006) CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J Clin Invest 116(7):1853–1864
Bassel-Duby R, Olson EN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75:19–37
Black BL, Olson EN (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol 14:167–196
Bodine SC et al (2001) Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294(5547):1704–1708
Bolger TA et al (2007) The neurodegenerative disease protein ataxin-1 antagonizes the neuronal survival function of myocyte enhancer factor-2. J Biol Chem 282(40):29186–29192
Bottomley MJ et al (2008) Structural and functional analysis of the human HDAC4 catalytic domain reveals a regulatory structural zinc-binding domain. J Biol Chem 283(39):26694–26704
Bradner JE et al (2010) Chemical phylogenetics of histone deacetylases. Nat Chem Biol 6(3):238–243
Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J Physiol 150:417–439
Camargo FD et al (2003) Single hematopoietic stem cells generate skeletal muscle through myeloid intermediates. Nat Med 9(12):1520–1527
Chang S et al (2004) Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol Cell Biol 24(19):8467–8476
Chin ER, Allen DG (1996) The role of elevations in intracellular [Ca2+] in the development of low frequency fatigue in mouse single muscle fibres. J Physiol 491(Pt 3):813–824
Chin ER et al (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12(16):2499–2509
Cohen TJ et al (2007) The histone deacetylase HDAC4 connects neural activity to muscle transcriptional reprogramming. J Biol Chem 282(46):33752–33759
Cohen TJ et al (2009) The deacetylase HDAC4 controls myocyte enhancing factor-2-dependent structural gene expression in response to neural activity. FASEB J 23(1):99–106
Colussi C et al (2008) HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc Natl Acad Sci USA 105(49):19183–19187
Cui SS et al (2003) Valproic acid enhances axonal regeneration and recovery of motor function after sciatic nerve axotomy in adult rats. Brain Res 975(1–2):229–236
Czubryt MP et al (2003) Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc Natl Acad Sci USA 100(4):1711–1716
De Koninck P, Schulman H (1998) Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279(5348):227–230
Deng X et al (2005) Mirk/dyrk1B decreases the nuclear accumulation of class II histone deacetylases during skeletal muscle differentiation. J Biol Chem 280(6):4894–4905
Doble A (1996) The pharmacology and mechanism of action of riluzole. Neurology 47(6(suppl 4)):S233–S241
Esser K et al (1999) The CACC box and myocyte enhancer factor-2 sites within the myosin light chain 2 slow promoter cooperate in regulating nerve-specific transcription in skeletal muscle. J Biol Chem 274(17):12095–12102
Finsterer J (2009) Bulbar and spinal muscular atrophy (Kennedy’s disease): a review. Eur J Neurol 16(5):556–561
Fischle W et al (2002) Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol Cell 9(1):45–57
Gomes MD et al (2001) Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98(25):14440–14445
Grefte S et al (2007) Skeletal muscle development and regeneration. Stem Cells Dev 16(5):857–868
Gregoire S, Yang XJ (2005) Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors. Mol Cell Biol 25(6):2273–2287
Gregoire S et al (2007) Histone deacetylase 3 interacts with and deacetylates myocyte enhancer factor 2. Mol Cell Biol 27(4):1280–1295
Grimaldi PA (2003) Roles of PPARdelta in the control of muscle development and metabolism. Biochem Soc Trans 31(Pt 6):1130–1132
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 USA 97(14):7835–7840
Grozinger CM, Hassig CA, Schreiber SL (1999) Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc Natl Acad Sci USA 96(9):4868–4873
Guenther MG, Barak O, Lazar MA (2001) The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol 21(18):6091–6101
Gupta MP et al (2008) HDAC4 and PCAF bind to cardiac sarcomeres and play a role in regulating myofilament contractile activity. J Biol Chem 283(15):10135–10146
Haberland M et al (2007) Regulation of HDAC9 gene expression by MEF2 establishes a negative-feedback loop in the transcriptional circuitry of muscle differentiation. Mol Cell Biol 27(2):518–525
Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91(2):534–551
Hennig R, Lomo T (1985) Firing patterns of motor units in normal rats. Nature 314(6007):164–166
Iezzi S et al (2004) Deacetylase inhibitors increase muscle cell size by promoting myoblast recruitment and fusion through induction of follistatin. Dev Cell 6(5):673–684
Koh SD et al (1999) Novel regulation of the A-type K+ current in murine proximal colon by calcium-calmodulin-dependent protein kinase II. J Physiol 517(Pt 1):75–84
Koves TR et al (2005) Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency. J Biol Chem 280(39):33588–33598
Lahm A et al (2007) Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc Natl Acad Sci USA 104(44):17335–17340
Lange S et al (2005) The kinase domain of titin controls muscle gene expression and protein turnover. Science 308(5728):1599–1603
Lee SJ, McPherron AC (2001) Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci USA 98(16):9306–9311
Lemercier C et al (2000) mHDA1/HDAC5 histone deacetylase interacts with and represses MEF2A transcriptional activity. J Biol Chem 275(20):15594–15599
Lilly B et al (1995) Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267(5198):688–693
Lin J et al (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418(6899):797–801
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
Lu J et al (2000a) Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol Cell 6(2):233–244
Lu J et al (2000b) Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc Natl Acad Sci USA 97(8):4070–4075
Marks PA (2007) Discovery and development of SAHA as an anticancer agent. Oncogene 26(9):1351–1356
Matthews SA et al (2006) Essential role for protein kinase D family kinases in the regulation of class II histone deacetylases in B lymphocytes. Mol Cell Biol 26(4):1569–1577
McCampbell A et al (2000) CREB-binding protein sequestration by expanded polyglutamine. Hum Mol Genet 9(14):2197–2202
McGee SL et al (2009) Exercise-induced histone modifications in human skeletal muscle. J Physiol 587(Pt 24):5951–5958
McKinsey TA et al (2000) Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408(6808):106–111
McKinsey TA, Zhang CL, Olson EN (2002) MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci 27(1):40–47
Mejat A et al (2005) Histone deacetylase 9 couples neuronal activity to muscle chromatin acetylation and gene expression. Nat Neurosci 8(3):313–321
Minamiyama M et al (2004) Sodium butyrate ameliorates phenotypic expression in a transgenic mouse model of spinal and bulbar muscular atrophy. Hum Mol Genet 13(11):1183–1192
Minetti GC et al (2006) Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors. Nat Med 12(10):1147–1150
Miska EA et al (1999) HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J 18(18):5099–5107
Molkentin JD et al (1995) Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83(7):1125–1136
Moresi V et al (2010) Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell 143(1):35–45
Murgia M et al (2000) Ras is involved in nerve-activity-dependent regulation of muscle genes. Nat Cell Biol 2(3):142–147
Naya FJ et al (1999) Transcriptional activity of MEF2 during mouse embryogenesis monitored with a MEF2-dependent transgene. Development 126(10):2045–2052
Nucifora FC Jr et al (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291(5512):2423–2428
Pallafacchina G et al (2002) A protein kinase B-dependent and rapamycin-sensitive pathway controls skeletal muscle growth but not fiber type specification. Proc Natl Acad Sci USA 99(14):9213–9218
Pandey UB et al (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447(7146):859–863
Petri S et al (2006) Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 22(1):40–49
Potthoff MJ et al (2007a) Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers. J Clin Invest 117(9):2459–2467
Potthoff MJ et al (2007b) Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c. Mol Cell Biol 27(23):8143–8151
Rajan I et al (2009) Loss of the putative catalytic domain of HDAC4 leads to reduced thermal nociception and seizures while allowing normal bone development. PLoS One 4(8):e6612
Robbins SL, Kumar V, Cotran RS (2010) Robbins and Cotran pathologic basis of disease, 8th edn. Saunders, Elsevier, Philadelphia, PA, xiv, 1450 p
Rouaux C et al (2007) Sodium valproate exerts neuroprotective effects in vivo through CREB-binding protein-dependent mechanisms but does not improve survival in an amyotrophic lateral sclerosis mouse model. J Neurosci 27(21):5535–5545
Ryu H et al (2005) Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J Neurochem 93(5):1087–1098
Sandri M et al (2006) PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103(44):16260–16265
Shen T et al (2006) Parallel mechanisms for resting nucleo-cytoplasmic shuttling and activity dependent translocation provide dual control of transcriptional regulators HDAC and NFAT in skeletal muscle fiber type plasticity. J Muscle Res Cell Motil 27(5–7):405–411
Shi H et al (2008) Modulation of skeletal muscle fiber type by mitogen-activated protein kinase signaling. FASEB J 22(8):2990–3000
Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178(4):413–424
Sparrow DB et al (1999) MEF-2 function is modified by a novel co-repressor, MITR. EMBO J 18(18):5085–5098
Sugai F et al (2004) Benefit of valproic acid in suppressing disease progression of ALS model mice. Eur J Neurosci 20(11):3179–3183
Tang H, Goldman D (2006) Activity-dependent gene regulation in skeletal muscle is mediated by a histone deacetylase (HDAC)-Dach2-myogenin signal transduction cascade. Proc Natl Acad Sci USA 103(45):16977–16982
Vadivelu SK et al (2004) Muscle regeneration and myogenic differentiation defects in mice lacking TIS7. Mol Cell Biol 24(8):3514–3525
van der Linden AM, Nolan KM, Sengupta P (2007) KIN-29 SIK regulates chemoreceptor gene expression via an MEF2 transcription factor and a class II HDAC. EMBO J 26(2):358–370
Vega RB et al (2004) Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119(4):555–566
Verdin E, Dequiedt F, Kasler HG (2003) Class II histone deacetylases: versatile regulators. Trends Genet 19(5):286–293
Vietor I et al (2005) TIS7 regulation of the beta-catenin/Tcf-4 target gene osteopontin (OPN) is histone deacetylase-dependent. J Biol Chem 280(48):39795–39801
Wang AH, Yang XJ (2001) Histone deacetylase 4 possesses intrinsic nuclear import and export signals. Mol Cell Biol 21(17):5992–6005
Wang AH et al (1999) HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol Cell Biol 19(11):7816–7827
Wang AH et al (2000) Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol Cell Biol 20(18):6904–6912
Welle S et al (2003) Gene expression profile of aging in human muscle. Physiol Genomics 14(2):149–159
Wen YD et al (2000) The histone deacetylase-3 complex contains nuclear receptor corepressors. Proc Natl Acad Sci USA 97(13):7202–7207
Williams AH et al (2009) MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 326(5959):1549–1554
Wu H et al (2000) MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type. EMBO J 19(9):1963–1973
Wu H et al (2001) Activation of MEF2 by muscle activity is mediated through a calcineurin-dependent pathway. EMBO J 20(22):6414–6423
Wu H et al (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296(5566):349–352
Yoon HG et al (2003) Purification and functional characterization of the human N-CoR complex: the roles of HDAC3, TBL1 and TBLR1. EMBO J 22(6):1336–1346
Zhang CL et al (2001a) Association of COOH-terminal-binding protein (CtBP) and MEF2-interacting transcription repressor (MITR) contributes to transcriptional repression of the MEF2 transcription factor. J Biol Chem 276(1):35–39
Zhang CL, McKinsey TA, Olson EN (2001b) The transcriptional corepressor MITR is a signal-responsive inhibitor of myogenesis. Proc Natl Acad Sci USA 98(13):7354–7359
Zhang CL, McKinsey TA, Olson EN (2002a) Association of class II histone deacetylases with heterochromatin protein 1: potential role for histone methylation in control of muscle differentiation. Mol Cell Biol 22(20):7302–7312
Zhang CL et al (2002b) Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110(4):479–488
Zhao X et al (2001) The modular nature of histone deacetylase HDAC4 confers phosphorylation-dependent intracellular trafficking. J Biol Chem 276(37):35042–35048
Zhao X et al (2005) Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylase-mediated lysine modifications. Mol Cell Biol 25(19):8456–8464
Acknowledgment
We thank Drs. T. Barrientos for comments and M.C. Choi for sharing unpublished data. This work was supported by National Institute of Health (AR055613).
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Simmons, B.J., Cohen, T.J., Bedlack, R., Yao, TP. (2011). HDACs in Skeletal Muscle Remodeling and Neuromuscular Disease. In: Yao, TP., Seto, E. (eds) Histone Deacetylases: the Biology and Clinical Implication. Handbook of Experimental Pharmacology, vol 206. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21631-2_5
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