DOI QR코드

DOI QR Code

HDAC4 Regulates Muscle Fiber Type-Specific Gene Expression Programs

  • Cohen, Todd J. (Department of Pharmacology and Cancer Biology, Duke University) ;
  • Choi, Moon-Chang (Department of Pharmacology and Cancer Biology, Duke University) ;
  • Kapur, Meghan (Department of Pharmacology and Cancer Biology, Duke University) ;
  • Lira, Vitor A. (Department of Medicine, Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia) ;
  • Yan, Zhen (Department of Medicine, Center for Skeletal Muscle Research at Robert M. Berne Cardiovascular Research Center, University of Virginia) ;
  • Yao, Tso-Pang (Department of Pharmacology and Cancer Biology, Duke University)
  • Received : 2014.10.17
  • Accepted : 2014.12.17
  • Published : 2015.04.30

Abstract

Fiber type-specific programs controlled by the transcription factor MEF2 dictate muscle functionality. Here, we show that HDAC4, a potent MEF2 inhibitor, is predominantly localized to the nuclei in fast/glycolytic fibers in contrast to the sarcoplasm in slow/oxidative fibers. The cytoplasmic localization is associated with HDAC4 hyper-phosphorylation in slow/oxidative-fibers. Genetic reprogramming of fast/glycolytic fibers to oxidative fibers by active CaMKII or calcineurin leads to increased HDAC4 phosphorylation, HDAC4 nuclear export, and an increase in markers associated with oxidative fibers. Indeed, HDAC4 represses the MEF2-dependent, PGC-$1{\alpha}$-mediated oxidative metabolic gene program. Thus differential phosphorylation and localization of HDAC4 contributes to establishing fiber type-specific transcriptional programs.

Keywords

References

  1. Akimoto, T., Ribar, T.J., Williams, R.S., and Yan, Z. (2004a). Skeletal muscle adaptation in response to voluntary running in $Ca^{2+}$calmodulin-dependent protein kinase IV-deficient mice. Am. J. Physiol. Cell Physiol. 287, C1311-1319. https://doi.org/10.1152/ajpcell.00248.2004
  2. Akimoto, T., Sorg, B.S., and Yan, Z. (2004b). Real-time imaging of peroxisome proliferator-activated receptor-gamma coactivator-1alpha promoter activity in skeletal muscles of living mice. Am. J. Physiol. Cell Physiol. 287, C790-796. https://doi.org/10.1152/ajpcell.00425.2003
  3. Backs, J., Song, K., Bezprozvannaya, S., Chang, S., and Olson, E.N. (2006). CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J. Clin. Invest. 116, 1853-1864. https://doi.org/10.1172/JCI27438
  4. Bassel-Duby, R., and Olson, E.N. (2006). Signaling pathways in skeletal muscle remodeling. Ann. Rev. Biochem. 75, 19-37. https://doi.org/10.1146/annurev.biochem.75.103004.142622
  5. Black, B.L., and Olson, E.N. (1998). Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 14, 167-196. https://doi.org/10.1146/annurev.cellbio.14.1.167
  6. Chin, E.R., Olson, E.N., Richardson, J.A., Yang, Q., Humphries, C., Shelton, J.M., Wu, H., Zhu, W., Bassel-Duby, R., and Williams, R.S. (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
  7. Choi, M.C., Cohen, T.J., Barrientos, T., Wang, B., Li, M., Simmons, B.J., Yang, J.S., Cox, G.A., Zhao, Y., and Yao, T.P. (2012). A direct HDAC4-MAP kinase crosstalk activates muscle atrophy program. Mol. Cell 47, 122-132. https://doi.org/10.1016/j.molcel.2012.04.025
  8. Cohen, T.J., Waddell, D.S., Barrientos, T., Lu, Z., Feng, G., Cox, G.A., Bodine, S.C., and Yao, T.P. (2007). The histone deacetylase HDAC4 connects neural activity to muscle transcriptional reprogramming. J. Biol. Chem. 282, 33752-33759. https://doi.org/10.1074/jbc.M706268200
  9. Cohen, T.J., Barrientos, T., Hartman, Z.C., Garvey, S.M., Cox, G.A., and Yao, T.P. (2009). The deacetylase HDAC4 controls myocyte enhancing factor-2-dependent structural gene expression in response to neural activity. FASEB J. 23, 99-106. https://doi.org/10.1096/fj.08-115931
  10. Czubryt, M.P., McAnally, J., Fishman, G.I., and Olson, E.N. (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, 1711-1716. https://doi.org/10.1073/pnas.0337639100
  11. Fitzsimons, D.P., Diffee, G.M., Herrick, R.E., and Baldwin, K.M. (1990). Effects of endurance exercise on isomyosin patterns in fast- and slow-twitch skeletal muscles. J. Appl. Physiol. 68, 1950-1955. https://doi.org/10.1152/jappl.1990.68.5.1950
  12. Lin, J., Wu, H., Tarr, P.T., Zhang, C.Y., Wu, Z., Boss, O., Michael, L.F., Puigserver, P., Isotani, E., Olson, E.N., et al. (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
  13. Liu, Y., Randall, W.R., and Schneider, M.F. (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
  14. Marin, P., Andersson, B., Krotkiewski, M., and Bjorntorp, P. (1994). Muscle fiber composition and capillary density in women and men with NIDDM. Diabetes Care 17, 382-386. https://doi.org/10.2337/diacare.17.5.382
  15. McKinsey, T.A., Zhang, C.L., Lu, J., and Olson, E.N. (2000). Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408, 106-111. https://doi.org/10.1038/35040593
  16. McKinsey, T.A., Zhang, C.L., and Olson, E.N. (2002). MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem. Sci. 27, 40-47. https://doi.org/10.1016/S0968-0004(01)02031-X
  17. Minetti, G.C., Colussi, C., Adami, R., Serra, C., Mozzetta, C., Parente, V., Fortuni, S., Straino, S., Sampaolesi, M., Di Padova, M., et al. (2006). Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors. Nat. Med. 12, 1147-1150. https://doi.org/10.1038/nm1479
  18. Naya, F.J., Mercer, B., Shelton, J., Richardson, J.A., Williams, R.S., and Olson, E.N. (2000). Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J. Biol. Chem. 275, 4545-4548. https://doi.org/10.1074/jbc.275.7.4545
  19. Nyholm, B., Qu, Z., Kaal, A., Pedersen, S.B., Gravholt, C.H., Andersen, J.L., Saltin, B., and Schmitz, O. (1997). Evidence of an increased number of type IIb muscle fibers in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes 46, 1822-1828. https://doi.org/10.2337/diab.46.11.1822
  20. Pette, D. (2002). The adaptive potential of skeletal muscle fibers. Can. J. Appl. Physiol. 27, 423-448. https://doi.org/10.1139/h02-023
  21. Potthoff, M.J., Arnold, M.A., McAnally, J., Richardson, J.A., Bassel-Duby, R., and Olson, E.N. (2007a). Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c. Mol. Cell. Biol. 27, 8143-8151. https://doi.org/10.1128/MCB.01187-07
  22. Potthoff, M.J., Wu, H., Arnold, M.A., Shelton, J.M., Backs, J., McAnally, J., Richardson, J.A., Bassel-Duby, R., and Olson, E.N. (2007b). Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers. J. Clin. Invest. 117, 2459-2467. https://doi.org/10.1172/JCI31960
  23. Russell, A.P., Feilchenfeldt, J., Schreiber, S., Praz, M., Crettenand, A., Gobelet, C., Meier, C.A., Bell, D.R., Kralli, A., Giacobino, J.P., et al. (2003). Endurance training in humans leads to fiber typespecific increases in levels of peroxisome proliferator-activated receptor-gamma coactivator-1 and peroxisome proliferatoractivated receptor-alpha in skeletal muscle. Diabetes 52, 2874-2881. https://doi.org/10.2337/diabetes.52.12.2874
  24. Sandri, M., Lin, J., Handschin, C., Yang, W., Arany, Z.P., Lecker, S.H., Goldberg, A.L., and Spiegelman, B.M. (2006). PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc. Natl. Acad. Sci. USA 103, 16260-16265. https://doi.org/10.1073/pnas.0607795103
  25. Schrauwen, P., and Hesselink, M.K. (2004). Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 53, 1412-1417. https://doi.org/10.2337/diabetes.53.6.1412
  26. Spangenburg, E.E., and Booth, F.W. (2003). Molecular regulation of individual skeletal muscle fibre types. Acta Physiol. Scand 178, 413-424. https://doi.org/10.1046/j.1365-201X.2003.01158.x
  27. Terada, S., Goto, M., Kato, M., Kawanaka, K., Shimokawa, T., and Tabata, I. (2002). Effects of low-intensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle. Biochem. Biophys. Res. Commun. 296, 350-354. https://doi.org/10.1016/S0006-291X(02)00881-1
  28. Vega, R.B., Harrison, B.C., Meadows, E., Roberts, C.R., Papst, P.J., Olson, E.N., and McKinsey, T.A. (2004). Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5. Mol. Cell. Biol. 24, 8374-8385. https://doi.org/10.1128/MCB.24.19.8374-8385.2004
  29. Wu, H., Kanatous, S.B., Thurmond, F.A., Gallardo, T., Isotani, E., Bassel-Duby, R., and Williams, R.S. (2002). Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296, 349-352. https://doi.org/10.1126/science.1071163
  30. Wu, H., Naya, F.J., McKinsey, T.A., Mercer, B., Shelton, J.M., Chin, E.R., Simard, A.R., Michel, R.N., Bassel-Duby, R., Olson, E.N., et al. (2000). MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type. EMBO J. 19, 1963-1973. https://doi.org/10.1093/emboj/19.9.1963
  31. Wu, H., Rothermel, B., Kanatous, S., Rosenberg, P., Naya, F.J., Shelton, J.M., Hutcheson, K.A., DiMaio, J.M., Olson, E.N., Bassel-Duby, R., et al. (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
  32. Zhao, X., Ito, A., Kane, C.D., Liao, T.S., Bolger, T.A., Lemrow, S.M., Means, A.R., and Yao, T.P. (2001). The modular nature of histone deacetylase HDAC4 confers phosphorylation-dependent intracellular trafficking. J. Biol. Chem. 276, 35042-35048. https://doi.org/10.1074/jbc.M105086200

Cited by

  1. Disruption of ATP-sensitive potassium channel function in skeletal muscles promotes production and secretion of musclin vol.471, pp.1, 2016, https://doi.org/10.1016/j.bbrc.2016.01.166
  2. G9a inhibits MEF2C activity to control sarcomere assembly vol.6, pp.1, 2016, https://doi.org/10.1038/srep34163
  3. Trichostatin A, a histone deacetylase inhibitor, modulates unloaded-induced skeletal muscle atrophy vol.119, pp.4, 2015, https://doi.org/10.1152/japplphysiol.01031.2014
  4. Expression of carbonic anhydrase III and skeletal muscle remodeling following selective denervation vol.16, pp.6, 2017, https://doi.org/10.3892/mmr.2017.7644
  5. Rapid decline in MyHC I(β) mRNA expression in rat soleus during hindlimb unloading is associated with AMPK dephosphorylation vol.595, pp.23, 2017, https://doi.org/10.1113/JP275184
  6. ) vol.313, pp.1, 2017, https://doi.org/10.1152/ajpregu.00378.2016
  7. AMP-Activated Protein Kinase as a Key Trigger for the Disuse-Induced Skeletal Muscle Remodeling vol.19, pp.11, 2018, https://doi.org/10.3390/ijms19113558
  8. The effects of obesity on skeletal muscle contractile function vol.221, pp.13, 2018, https://doi.org/10.1242/jeb.163840
  9. Proteomic and microRNA Transcriptome Analysis revealed the microRNA-SmyD1 network regulation in Skeletal Muscle Fibers performance of Chinese perch vol.7, pp.None, 2015, https://doi.org/10.1038/s41598-017-16718-2
  10. АМФ-АКТИВИРУЕМАЯ ПРОТЕИНКИНАЗА - ПУСКОВОЕ ЗВЕНО ГИПОГРАВИТАЦИОННОЙ ПЕРЕСТРОЙКИ ПОСТУРАЛЬНОЙ МЫШЦЫ, "Росс vol.104, pp.8, 2015, https://doi.org/10.7868/s0869813918070031
  11. Lysine Acetylation Goes Global: From Epigenetics to Metabolism and Therapeutics vol.118, pp.3, 2015, https://doi.org/10.1021/acs.chemrev.7b00181
  12. Histone deacetylase activity mediates thermal plasticity in zebrafish ( Danio rerio ) vol.9, pp.None, 2015, https://doi.org/10.1038/s41598-019-44726-x
  13. HDAC4 gene silencing alleviates epilepsy by inhibition of GABA in a rat model vol.15, pp.None, 2015, https://doi.org/10.2147/ndt.s181669
  14. MEF-2 isoforms' (A-D) roles in development and tumorigenesis vol.10, pp.28, 2015, https://doi.org/10.18632/oncotarget.26763
  15. HDAC4 Controls Muscle Homeostasis through Deacetylation of Myosin Heavy Chain, PGC-1α, and Hsc70 vol.29, pp.3, 2015, https://doi.org/10.1016/j.celrep.2019.09.023
  16. Epigenetic mechanisms related to cognitive decline during aging vol.98, pp.2, 2015, https://doi.org/10.1002/jnr.24436
  17. The role of histone deacetylase 4 during chondrocyte hypertrophy and endochondral bone development vol.9, pp.2, 2015, https://doi.org/10.1302/2046-3758.92.bjr-2019-0172.r1
  18. The Time Course of Muscle Nuclear Content of Transcription Factors Regulating the MyHC I(β) Expression in the Rat Soleus Muscle under Gravitational Unloading vol.14, pp.3, 2020, https://doi.org/10.1134/s1990747820020099
  19. Role of CaMKII and sarcolipin in muscle adaptations to strength training with different levels of fatigue in the set vol.31, pp.1, 2015, https://doi.org/10.1111/sms.13828
  20. HDAC11 is a novel regulator of fatty acid oxidative metabolism in skeletal muscle vol.288, pp.3, 2015, https://doi.org/10.1111/febs.15456
  21. HDAC4 Knockdown Alleviates Denervation-Induced Muscle Atrophy by Inhibiting Myogenin-Dependent Atrogene Activation vol.15, pp.None, 2015, https://doi.org/10.3389/fncel.2021.663384
  22. HDAC4 Is Indispensable for Reduced Slow Myosin Expression at the Early Stage of Hindlimb Unloading in Rat Soleus Muscle vol.14, pp.11, 2021, https://doi.org/10.3390/ph14111167