Histone deacetylase inhibitors in the treatment of muscular dystrophies: Epigenetic drugs for genetic diseases

Molecular Medicine

Volumn 17, Issue 5-6, 2011, Pages 457-465

  Consalvi, Silvia ^a   Saccone, Valentina ^a   Giordani, Lorenzo ^a   Minetti, Giulia ^a,b   Mozzetta, Chiara ^a   Puri, Pier Lorenzo ^a,c  

^a EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^b NOVARTIS PHARMA AG   (Switzerland)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARYLBUTYRIC ACID DERIVATIVE; CAVEOLIN 3; DYSTROBREVIN; DYSTROGLYCAN; DYSTROPHIN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; ENTINOSTAT; FUKUTIN RELATED PROTEIN; GIVINOSTAT; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; NEURONAL NITRIC OXIDE SYNTHASE; SARCOGLYCAN; SYNTROPHIN; TRICHOSTATIN A; VALPROIC ACID; VORINOSTAT;

ARTICLE; CELL SELECTION; CLINICAL TRIAL (TOPIC); COMPLEX FORMATION; DISEASE COURSE; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; GENE THERAPY; GENETIC ANALYSIS; GENETIC REGULATION; HUMAN; INTRACELLULAR SIGNALING; MUSCLE ATROPHY; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; NERVE CELL NETWORK; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SATELLITE CELL; UNSPECIFIED SIDE EFFECT;

ANIMALS; DYSTROPHIN; HISTONE DEACETYLASE INHIBITORS; HUMANS; MICE; MUSCULAR DYSTROPHIES; MUSCULAR DYSTROPHY, DUCHENNE;

EID: 79957948651     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.2119/molmed.2011.00049     Document Type: Article

References (87)

1. Dalkilic I, Kunkel LM. (2003) Muscular dystrophies: genes to pathogenesis. Curr. Opin. Genet. Dev. 13:231-8.
2. Hoffman EP, Brown RH Jr, Kunkel LM. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 51:919-28.
3. Ervasti JM. (2007) Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochim. Biophys. Acta. 1772:108-17.
4. Mendell JR, Boué DR, Martin PT. (2006) The congenital muscular dystrophies: recent advances and molecular insights. Pediatr. Dev. Pathol. 9427-43.
5. Davies KE, Nowak KJ. (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat. Rev. Mol. Cell. Biol. 7:762-73.
6. Batchelor CL, Winder SJ. (2006) Sparks, signals and shock absorbers: how dystrophin loss causes muscular dystrophy. Trends Cell. Biol. 16:198-205.
7. Kuang S, Rudnicki MA. (2008) The emerging biology of satellite cells and their therapeutic potential. Trends Mol. Med. 14:82-91.
8. Engvall E, Wewer UM. (2003) The new frontier in muscular dystrophy research: booster genes. FASEB J. 17:1579-84.
9. Mozzetta C, Minetti G, Puri PL. (2009) Regenerative pharmacology in the treatment of genetic diseases: the paradigm of muscular dystrophy. Int. J. Biochem. Cell Biol. 41:701-10.
10. Shi X, Garry DJ. (2006) Muscle stem cells in development, regeneration, and disease. Genes. Dev. 20:1692-708.
11. Péault B, et al. (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol. Ther. 15:867-77.
12. Gopinath SD, Rando TA. (2008) Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell. 7:590-8.
13. Sacco A, et al. (2010) Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell. 143:1059-71.
14. Conboy IM, et al. (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature. 433:760-4.
15. Jaskelioff M, et al. (2011) Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature. 469:102-6.
16. Ferrari G, et al. (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 279:1528-30.
17. Gussoni E, et al. (1999) Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 401:390-4.
18. LaBarge MA, Blau HM. (2002) Biological progression from adult bone marrow to mononucle-ate muscle stem cell to multinucleate muscle fiber in response to injury. Cell. 111:589-601.
19. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA. (2002) Myogenic specification of side population cells in skeletal muscle. J. Cell Biol. 159:123-34.
20. Minasi MG, et al. (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development. 129:2773-83.
21. Young HE, et al. (2001) Human reserve pluripo-tent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat. Rec. 264:51-62.
22. Sherwood RI, et al. (2004) Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell. 119:543-54.
23. Mitchell KJ, et al. (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat. Cell Biol. 12:257-66.
24. Joe AW, et al. (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12:153-63.
25. Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K. (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 12:143-52.
26. Rodeheffer MS. (2010) Tipping the scale: muscle versus fat. Nat. Cell Biol. 12:102-4.
27. Guasconi V, Puri PL. (2009) Chromatin: the interface between extrinsic cues and the epigenetic regulation of muscle regeneration. Trends Cell Biol. 19:286-94.
28. Palacios D, et al. (2010) TNF/p38±/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell. 7:455-629.
29. Acharyya S, et al. (2010) TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methyla-tion mediated repression: implications in duchenne muscular dystrophy. PLoS One. 5:e12479.
30. Wehling M, Spencer MJ, Tidball JG. (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol. 155:123-31.
31. Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A. (2008) S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature. 455:411-5.
32. Colussi C, et al. (2009) HDAC2 blockade by nitric oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc. Natl. Acad. Sci. U. S. A. 106:1679.
33. Minetti GC, et al. (2006) Functional and morphological recovery of dystrophic muscles in mice treated with deacetylase inhibitors. Nat. Med. 12:1147-50.
34. Lee SJ. (2004) Regulation of muscle mass by myostatin. Annu. Rev. Cell Dev. Biol. 20:61-86.
35. Tsuchida K. (2008)Targeting myostatin for therapies against muscle-wasting disorders. Curr. Opin. Drug Discov. Devel. 11:487-94.
36. Bogdanovich S, Perkins KJ, Krag TO, Whittemore LA, Khurana TS. (2005) Myostatin propeptide-mediated amelioration of dystrophic pathophysi-ology. FASEB J. 19:543-9.
37. Bogdanovich S, et al. (2002) Functional improvement of dystrophic muscle by myostatin blockade. Nature. 420:418-21.
38. Nakatani M, et al. (2008) Transgenic expression of a myostatin inhibitor derived from follistatin increases skeletal muscle mass and ameliorates dys-trophic pathology in mdx mice. FASEB J. 22:477-87.
39. Haidet AM, et al. (2008) Long-term enhancement of skeletal muscle mass and strength by single gene administration of myostatin inhibitors. Proc. Natl. Acad. Sci. U. S. A.105:4318-22.
40. Wagner KR, Lechtzin N, Judge DP. (2007) Current treatment of adult Duchenne muscular dystrophy. Biochim. Biophys. Acta. 1772:229-37.
41. Rodino-Klapac LR, et al. (2009) Inhibition of myostatin with emphasis on follistatin as a therapy for muscle disease. Muscle Nerve. 39:283-96.
42. Iezzi S, Cossu G, Nervi C, Sartorelli V, Puri PL. (2002) Stage-specific modulation of skeletal myo-genesis by inhibitors of nuclear deacetylases. Proc. Natl. Acad. Sci. U. S. A. 99:7757-62.
43. Iezzi S, et al. (2004) Deacetylase inhibitors increase muscle cell size by promoting myoblast recruitment and fusion through induction of fol-listatin. Dev. Cell. 6:673-84.
44. Pisconti A, et al. (2006) Follistatin induction by nitric oxide through cyclic GMP: a tightly regulated signaling pathway that controls myoblast fusion. J. Cell Biol. 172:233-44.
45. Puri PL, Sartorelli V. (2000) Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. J. Cell Physiol. 185:155-73.
46. Palacios D, Puri PL. (2006) The epigenetic network regulating muscle development and regeneration. J. Cell Physiol. 207:1-11.
47. Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF. (2006) Myogenic factors that regulate expression of muscle-specific microRNAs. Proc. Natl. Acad. Sci. U. S. A. 103:8721-6.
48. McKinsey TA, Zhang CL, Olson EN. (2001) Control of muscle development by dueling HATs and HDACs. Curr. Opin. Genet. Dev. 11:497-504.
49. Puri PL, et al. (2001) Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol. Cell. 8:885-97.
50. Mal A, Sturniolo M, Schiltz RL, Ghosh MK, Har-ter ML. (2001) A role for histone deacetylase HDAC1 in modulating the transcriptional activity of MyoD: inhibition of the myogenic program. EMBO J. 20:1739-53.
51. McKinsey TA, Zhang CL, Olson EN. (2000) Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc. Natl. Acad. Sci. U. S. A. 97:14400-5.
52. Lu J, McKinsey TA, Zhang CL, Olson EN. (2000) Regulation of skeletal myogenesis by association of the MEF2 transcription factor with class II his-tone deacetylases. Mol. Cell. 6:233-244.
53. Sartorelli V, et al. (1999) Acetylation of MyoD directed by PCAF is necessary for the execution of the muscle program. Mol. Cell. 4:725-734.
54. Ma K, Chan JK, Zhu G, Wu Z. (2005) Myocyte enhancer factor 2 acetylation by p300 enhances its DNA binding activity, transcriptional activity, and myogenic differentiation. Mol. Cell. Biol. 25:3575-3582.
55. Angelelli C, et al. (2008) Differentiation-dependent lysine 4 acetylation enhances MEF2C binding to DNA in skeletal muscle cells. Nucleic Acids Res. 36:915-928.
56. Greco S, et al. (2009) Common micro-RNA signature in skeletal muscle damage and regeneration induced by Duchenne muscular dystrophy and acute ischemia. FASEB J. 23:3335-3346.
57. Eisenberg I, et al. (2007) Distinctive patterns of microRNA expression in primary muscular disorders. Proc. Natl. Acad. Sci. U. S. A. 104:17016-17021.
58. Williams AH, Liu N, van Rooij E, Olson EN. (2009) MicroRNA control of muscle development and disease. Curr. Opin. Cell Biol. 21:461-469.
59. Chen JF, et al. (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38:228-233.
60. Eisenberg I, Alexander MS, Kunkel LM. (2009) miRNAS in normal and diseased skeletal muscle. J. Cell. Mol. Med. 13:2-11.
61. Rosenberg MI, Georges SA, Asawachaicharn A, Analau E, Tapscott SJ. (2006) MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J. Cell Biol. 175:77-85.
62. Liu N, et al. (2007) An intragenic MEF2-depen-dent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc. Natl. Acad. Sci. U. S. A. 104:20844-20849.
63. Mallappa C, et al. (2010) Myogenic microRNA expression requires ATP-dependent chromatin remodeling enzyme function. Mol. Cell. Biol. 30:3176-3186.
64. Cacchiarelli D, et al. (2010) MicroRNAs involved in molecular circuitries relevant for the Duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway. Cell Metab. 12:341-51.
65. Colussi C, et al. (2009) Nitric oxide deficiency determines global chromatin changes in Duchenne muscular dystrophy. FASEB J. 23:2131-2141.
66. Sun Y, et al. (2010) Mammalian target of ra-pamycin regulates miRNA-1 and follistatin in skeletal myogenesis. J. Cell Biol. 28:189:1157-1169.
67. Brunelli S, et al. (2007) Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proc. Natl. Acad. Sci. U. S. A. 104:264-269.
68. Zammit PS, Partridge TA. (2002) Sizing up muscular dystrophy. Nat. Med. 8:1355-6.
69. Aoki F, Kojima I. (2007) Therapeutic potential of follistatin to promote tissue regeneration and prevent tissue fibrosis. Endocr. J. 54:849-854.
70. Colussi C, et al. (2010). Proteomic profile of differentially expressed plasma proteins from dys-trophic mice and following suberoylainide hydroxamic acid treatment. Proteomics Clin. Appl. 4:71-83.
71. Nebbioso A, et al. (2009) Selective class II HDAC inhibitors impair myogenesis by modulating the stability and activity of HDAC-MEF2 complexes. EMBO Rep. 10:776-782.
72. Vojinovic J, Damjanov N. (2011) HDAC inhibition in rheumatoid arthritis and juvenile idio-pathic arthritis. Mol. Med. 17:397-403.
73. Elaut G, Rogiers V, Vanhaecke T. (2007) The pharmaceutical potential of histone deacetylase inhibitors. Curr. Pharm. Des. 13:2584-2620.
74. Barker N, Bartfeld S, Clevers H. (2010) Tissue-resident adult stem cell populations of rapidly self-renewing organs. Cell Stem Cell. 7:656-670.
75. Duvic M, Vu J. (2007) Vorinostat: a new oral his-tone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert. Opin. Investig. Drugs. 16:1111-1120.
76. Ware CB, et al. (2009). Histone deacetylase inhibition elicits an evolutionarily conserved self-renewal program in embryonic stem cells. Cell Stem Cell. 4: 359-369.
77. Liang J, et al. (2008) Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol. 10:731-739.
78. Menegola E, Di Renzo F, Broccia ML, Giavini E. (2006) Inhibition of histone deacetylase as a new mechanism of teratogenesis. Birth Defects Res. C Embryo Today. 78:345-353.
79. Edgar R, Domrachev M, Lash AE. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207-210.
80. Bernstein BE, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 125:315-326.
81. Azuara V, et al. (2006) Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8:532-538.
82. Lee MG, et al. (2006) Functional interplay between histone demethylase and deacetylase enzymes. Mol. Cell. Biol. 26:6395-6402.
83. Boyer LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature. 441:349-353.
84. Mohn F, et al. (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell. 30:755-766.
85. Karantzali E, et al. (2008) Histone deacetylase inhibition accelerates the early events of stem cell differentiation: transcriptomic and epigenetic analysis. Genome Biol. 9:R65.
86. Wang Z, et al. (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell. 138:1019-1031.
87. Mozzetta C, et al. (2011) Selective control of Pax7 expression by TNF-activated p38±/polycomb repressive complex 2 (PRC2) signaling during muscle satellite cell differentiation. Cell Cycle. 10:191-198.