Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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HDAC11 Inhibits Myoblast Differentiation through Repression of MyoD-Dependent Transcription

  • Byun, Sang Kyung (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • An, Tae Hyeon (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Son, Min Jeong (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Lee, Da Som (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Kang, Hyun Sup (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Lee, Eun-Woo (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Han, Baek Soo (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Kim, Won Kon (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Bae, Kwang-Hee (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Oh, Kyoung-Jin (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Lee, Sang Chul (Metabolic Regulation Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
  • Received : 2017.07.05
  • Accepted : 2017.08.10
  • Published : 2017.09.30
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Abstract

Abnormal differentiation of muscle is closely associated with aging (sarcopenia) and diseases such as cancer and type II diabetes. Thus, understanding the mechanisms that regulate muscle differentiation will be useful in the treatment and prevention of these conditions. Protein lysine acetylation and methylation are major post-translational modification mechanisms that regulate key cellular processes. In this study, to elucidate the relationship between myogenic differentiation and protein lysine acetylation/methylation, we performed a PCR array of enzymes related to protein lysine acetylation/methylation during C2C12 myoblast differentiation. Our results indicated that the expression pattern of HDAC11 was substantially increased during myoblast differentiation. Furthermore, ectopic expression of HDAC11 completely inhibited myoblast differentiation, concomitant with reduced expression of key myogenic transcription factors. However, the catalytically inactive mutant of HDAC11 (H142/143A) did not impede myoblast differentiation. In addition, wild-type HDAC11, but not the inactive HDAC11 mutant, suppressed MyoD-induced promoter activities of MEF2C and MYOG (Myogenin), and reduced histone acetylation near the E-boxes, the MyoD binding site, of the MEF2C and MYOG promoters. Collectively, our results indicate that HDAC11 would suppress myoblast differentiation via regulation of MyoD-dependent transcription. These findings suggest that HDAC11 is a novel critical target for controlling myoblast differentiation.

Keywords

References

  1. Ait-Si-Ali, S., Guasconi, V., Fritsch, L., Yahi, H., Sekhri, R., Naguibneva, I., Robin, P., Cabon, F., Polesskaya, A., and Harel-Bellan, A. (2004). A Suv39h-dependent mechanism for silencing S-phase genes in differentiating but not in cycling cells. EMBO J. 23, 605-615. https://doi.org/10.1038/sj.emboj.7600074
  2. Berendse, M., Grounds, M.D., and Lloyd, C.M. (2003). Myoblast structure affects subsequent skeletal myotube morphology and sarcomere assembly. Exp. Cell Res. 291, 435-450. https://doi.org/10.1016/j.yexcr.2003.07.004
  3. Bergstrom, D.A., Penn, B.H., Strand, A., Perry, R.L., Rudnicki, M.A., and Tapscott, S.J. (2002). Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol. Cell. 9, 587-600. https://doi.org/10.1016/S1097-2765(02)00481-1
  4. Braun, T., Buschhausen-Denker, G., Bober, E., Tannich, E., and Arnold, H.H. (1989). A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J. 8, 701-709.
  5. Braun, T., Bober, E., Winter, B., Rosenthal, N., and Arnold, H.H. (1990). Myf-6, a new member of the human gene family of myogenic determination factors: evidence for a gene cluster on chromosome 12. EMBO J. 9, 821-831.
  6. Buchberger, A., Ragge, K., and Arnold, H.H. (1994). The myogenin gene is activated during myocyte differentiation by pre-existing, not newly synthesized transcription factor MEF-2. J. Biol. Chem. 269, 17289-17296.
  7. Burattini, S., Ferri, P., Battistelli, M., Curci, R., Luchetti, F., and Falcieri, E. (2004). C2C12 murine myoblasts as a model of skeletal muscle development: morpho-functional characterization. Eur. J. Histochem. 48, 223-233.
  8. Caretti, G., Di Padova, M., Micales, B., Lyons, G.E., and Sartorelli, V. (2004). The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev. 18, 2627-2638. https://doi.org/10.1101/gad.1241904
  9. Davis, R.L., Weintraub, H., and Lassar, A.B. (1987). Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987-1000. https://doi.org/10.1016/0092-8674(87)90585-X
  10. De la Serna, I.L., Ohkawa, Y., and Imbalzano, A.N. (2006). Chromatin remodelling in mammalian differentiation: lessons from ATPdependent remodellers. Nat. Rev. Genet. 7, 461-473. https://doi.org/10.1038/nrg1882
  11. DeFronzo, R.A., and Tripathy, D. (2009). Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32, S157-S163. https://doi.org/10.2337/dc09-S302
  12. Dodou, E., Xu, S.M., and Black, B.L. (2003). Mef2c is activated directly by myogenicbasic helix-loop-helix proteins during skeletal muscle development in vivo. Mech. Dev. 120, 1021-1032. https://doi.org/10.1016/S0925-4773(03)00178-3
  13. Edmondson, D.G., and Olson, E.N. (1989). A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes Dev. 3, 628-640. https://doi.org/10.1101/gad.3.5.628
  14. Faralli, H., and Dilworth, F.J. (2012). Turning on myogenin in muscle: a paradigm for understanding mechanisms of tissue-specific gene expression. Comp. Funct. Genomics 2012, 836374.
  15. Fu, X., Zhao, J.X., Liang, J., Zhu, M.J., Foretz, M., Viollet, B., and Du, M. (2013). AMP-activated protein kinase mediates myogenin expression and myogenesis via histone deacetylase 5. Am. J. Physiol. Cell Physiol. 305, C887-C895. https://doi.org/10.1152/ajpcell.00124.2013
  16. Gao, L., Cueto, M.A., Asselbergs, F., and Atadja, P. (2002). Cloning and functional characterization of HDAC11, a novel member of the human histone deacetylase family. J. Biol. Chem. 277, 25748-25755. https://doi.org/10.1074/jbc.M111871200
  17. Gerber, A.N., Klesert, T.R., Bergstrom, D.A. and Tapscott, S.J. (1997). Two domains of MyoD mediate transcriptional activation of genes in repressive chromatin: a mechanism for lineage determination in myogenesis. Genes Dev. 11, 436-450. https://doi.org/10.1101/gad.11.4.436
  18. Gossett, L.A., Kelvin, D.J., Sternberg, E.A., and Olson, E.N. (1989). A new myocyte-specific enhancer-binding factor that recognizes a conserved element associated with multiple muscle-specific genes. Mol. Cell. Biol. 9, 5022-5033. https://doi.org/10.1128/MCB.9.11.5022
  19. Guasconi, V., and Puri, P.L. (2009). Chromatin: the interface between extrinsic cues and the epigenetic regulation of muscle regeneration. Trends Cell Biol. 19, 286-294. https://doi.org/10.1016/j.tcb.2009.03.002
  20. Haberland, M., Montgomery, R.L., and Olson, E.N. (2009). The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10, 32-42. https://doi.org/10.1038/nrg2485
  21. Hasty, P., Bradley, A., Morris, J.H., Edmondson, D.G., Venuti, J.M., Olson, E.N., and Klein, W.H. (1993). Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501-506. https://doi.org/10.1038/364501a0
  22. Iezzi, S., Di Padova, M., Serra, C., Caretti, G., Simone, C., Maklan, E., Minetti, G., Zhao, P., Hoffman, E.P., Puri, P.L., et al. (2004). Deacetylase inhibitors increase muscle cell size by promoting myoblast recruitment and fusion through induction of follistatin. Dev. Cell 6, 673-684. https://doi.org/10.1016/S1534-5807(04)00107-8
  23. Karmodiya, K., Krebs, A.R., Oulad-Abdelghani, M., Kimura, H., and Tora, L. (2012). H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics 13, 424. https://doi.org/10.1186/1471-2164-13-424
  24. Krishnan, M., Singh, A.B., Smith, J.J., Sharma, A., Chen, X., Eschrich, S., Yeatman, T.J., Beauchamp, R.D., and Dhawan, P. (2010). HDAC inhibitors regulate claudin-1 expression in colon cancer cells through modulation of mRNA stability. Oncogene 29, 305-312. https://doi.org/10.1038/onc.2009.324
  25. Lassar, A.B., Skapek, S.X., and Novitch, B. (1994). Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr. Opin. Cell Biol. 6, 788-794. https://doi.org/10.1016/0955-0674(94)90046-9
  26. Lee, D.S., Choi, H., Han, B.S., Kim, W.K., Lee, S.C., Oh, K-J., and Bae, K-H. (2016). c-Jun regulates adipocyte differentiation via the KLF15- mediated mode. Biochem. Biophys. Res. Commun. 469, 552-558. https://doi.org/10.1016/j.bbrc.2015.12.035
  27. Liu, H., Hu, Q., D'Ercole, J., and Ye, P. (2009). Histone deacetylase 11 regulates oligodendrocyte-specific gene expression and cell development in OL-1 oligodendroglia cells. Glia 57, 1-12. https://doi.org/10.1002/glia.20729
  28. Lu, J., McKinsey, T.A., Zhang, C.L., and Olson, E.N. (2000). Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II histone deacetylases. Mol. Cell 6, 233-244. https://doi.org/10.1016/S1097-2765(00)00025-3
  29. Mal, A.K. (2006). Histone methyltransferase Suv39h1 represses MyoD-stimulated myogenic differentiation. EMBO J. 25, 3323-3334. https://doi.org/10.1038/sj.emboj.7601229
  30. Mal, A., and Harter, M.L. (2003). MyoD is functionally linked to the silencing of a muscle -specific regulatory gene prior to skeletal myogenesis. Proc. Natl. Acad. Sci. USA. 100, 1735-1739. https://doi.org/10.1073/pnas.0437843100
  31. Mal, A., Sturniolo, M., Schiltz, R.L., Ghosh, M.K., and Harter, M.L. (2001). A role for histone deacetylase HDAC1 in modulating the transcriptional activity of MyoD: inhibition of the myogenic program. EMBO J. 20, 1739-1753. https://doi.org/10.1093/emboj/20.7.1739
  32. Martin, J.F., Schwarz, J.J., and Olson, E.N. (1993). Myocyte enhancer factor (MEF) 2C: a tissue-restricted member of the MEF-2 family of transcription factors. Proc. Natl. Acad. Sci. USA. 90, 5282-5286. https://doi.org/10.1073/pnas.90.11.5282
  33. McDermott, J.C., Cardoso, M.C., Yu, Y.T., Andres, V., Leifer, D., Krainc, D., Lipton, S.A., and Nadal-Ginard, B. (1993). hMEF2C gene encodes skeletal muscle- and brain-specific transcription factors. Mol. Cell. Biol. 13, 2564-2577. https://doi.org/10.1128/MCB.13.4.2564
  34. McKinsey, T.A., Zhang, C.L., and Olson, E.N. (2002). Signaling chromatin to make muscle. Curr. Opin. Cell Biol. 14, 763-772. https://doi.org/10.1016/S0955-0674(02)00389-7
  35. Molkentin, J.D., Black, B.L., Martin, J.F., and Olson, E.N. (1995). Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83, 1125-1136. https://doi.org/10.1016/0092-8674(95)90139-6
  36. Nabeshima, Y., Hanaoka, K., Hayasaka, M., Esumi, E., Li, S., Nonaka, I., and Nabeshima, Y. (1993). Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532-535. https://doi.org/10.1038/364532a0
  37. Oh, K.J., Park, J., Kim, S.S., Oh, H., Choi, C.S., Koo, S.H. (2012). TCF7L2 modulates glucose homeostasis by regulating CREB- and FoxO1-dependent transcriptional pathway in the liver. PLOS Genet. 8, e1002986. https://doi.org/10.1371/journal.pgen.1002986
  38. Olson, E.N., and Klein, W.H. (1994). bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8, 1-8. https://doi.org/10.1101/gad.8.1.1
  39. Olson, E.N., Perry, M., and Schulz, R.A. (1995). Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev. Biol. 172, 2-14. https://doi.org/10.1006/dbio.1995.0002
  40. Pasini, D., Hansen, K.H., Christensen, J., Agger, K., Cloos, P.A., and Helin, K. (2008). Coordinated regulation of transcriptional repression by the RBP2 H3K4 demethylase and polycomb-repressive complex 2. Genes Dev. 22, 1345-1355. https://doi.org/10.1101/gad.470008
  41. Pollock, R., and Treisman, R. (1991). Human SRF-related proteins: DNA-binding properties and potential regulatory targets. Genes Dev. 5, 2327-2341. https://doi.org/10.1101/gad.5.12a.2327
  42. Puri, P.L., and Sartorelli, V. (2000). Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J. Cell. Physiol. 185, 155-173. https://doi.org/10.1002/1097-4652(200011)185:2<155::AID-JCP1>3.0.CO;2-Z
  43. Rajendran, P., Williams, D.E., Ho, E., and Dashwood, R.H. (2011). Metabolism as a key to histone deacetylase inhibition. Crit. Rev. Biochem. Mol. Biol. 46, 181-199. https://doi.org/10.3109/10409238.2011.557713
  44. Rhodes, S.J., and Konieczny, S.F. (1989). Identification of MRF4: a new member of the muscle regulatory factor gene family. Genes Dev. 3, 2050-2061. https://doi.org/10.1101/gad.3.12b.2050
  45. Rudnicki, M.A., Braun, T., Hinuma, S., and Jaenisch, R. (1992). Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383-390. https://doi.org/10.1016/0092-8674(92)90508-A
  46. Rudnicki, M.A., Schnegelsberg, P.N., Stead, R.H., Braun, T., Arnold, H.H. and Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359. https://doi.org/10.1016/0092-8674(93)90621-V
  47. Sabourin, L.A., and Rudnicki, M.A. (2000). The molecular regulation of myogenesis. Clin. Genet. 57, 16-25.
  48. Srivastava, S., Bhowmick, K., Chatterjee, S., Basha, J., Kundu, T.K., and Dhar, S.K. (2014). Histone H3K9 acetylation level modulates gene expression and may affect parasite growth in human malaria parasite Plasmodium falciparum. FEBS J. 281, 5265-5278. https://doi.org/10.1111/febs.13067
  49. Thangapandian, S., John, S., Lee, Y., Kim, S., and Lee, K.W. (2011). Dynamic structure-based pharmacophore model development: a new and effective addition in the histone deacetylase 8 (HDAC8) inhibitor discovery. Int. J. Mol. Sci. 12, 9440-9462. https://doi.org/10.3390/ijms12129440
  50. Thangapandian, S., John, S., and Lee, K.W. (2012). Molecular dynamics simulation study explaining inhibitor selectivity in different class of histone deacetylases. J. Biomol. Struct. Dyn. 29, 677-698. https://doi.org/10.1080/07391102.2012.10507409
  51. Voelter-Mahlknecht, S., Ho, A.D., and Mahlknecht, U. (2005). Chromosomal organization and localization of the novel class IV human histone deacetylase 11 gene. Int. J. Mol. Med. 16, 589-598.
  52. Wang, D.Z., Valdez, M.R., McAnally, J., Richardson, J., and Olson, E.N. (2001). The Mef2c gene is a direct transcriptional target of myogenic bHLH and MEF2 proteins during skeletal muscle development. Development 128, 4623-4633.
  53. Weintraub, H., Davis, R., Lockshon, D., and Lassar, A. (1990). MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation. Proc. Natl. Acad. Sci. USA 87, 5623-5627. https://doi.org/10.1073/pnas.87.15.5623
  54. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, T.K., Turner, D., Rupp, R., Hollenberg, S., et al. (1991). The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251, 761-766. https://doi.org/10.1126/science.1846704
  55. Xu, Q., and Wu Z. (2000). The insulin-like growth factorphosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcomaderived RD cells. J. Biol. Chem. 275, 36750-36757. https://doi.org/10.1074/jbc.M005030200
  56. Yu, Y.T., Breitbart, R.E., Smoot, L.B., Lee, Y., Mahdavi, V., and Nadal- Ginard, B. (1992). Human myocyte-specific enhancer factor 2 comprises a group of tissue-restricted MADS box transcription factors. Genes Dev. 6, 1783-1798. https://doi.org/10.1101/gad.6.9.1783

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