Six Homeoproteins and a linc-RNA at the Fast MYH Locus Lock Fast Myofiber Terminal Phenotype

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Adult skeletal muscles are classified into fast-type and slow-type, which display different resistance to muscle atrophy and metabolic protection against obesity. We identify in this manuscript a new mechanism controlling in vivo adult muscle fiber-type specification implicating a long intergenic non-coding RNA, linc-MYH. We demonstrate a three-element genetic partnership, where an enhancer under the control of the myogenic homeoprotein Six1 functions as a regulatory hub to control fibre phenotype. In this partnership, the enhancer controls positively the expression of both the adjacent fast myosin heavy chain (MYH) gene cluster and of linc-MYH. linc-MYH is present only in adult fast type skeletal myofibers and controls their phenotype by suppressing slow-type gene expression. The regulation of linc-MYH could provide a lead for new therapeutic approaches or drug development.

Vyšlo v časopise: Six Homeoproteins and a linc-RNA at the Fast MYH Locus Lock Fast Myofiber Terminal Phenotype. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004386
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004386

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Zdroje

1. GundersenK (2011) Excitation-transcription coupling in skeletal muscle: the molecular pathways of exercise. Biol Rev Camb Philos Soc 86: 564–600.

2. SchiaffinoS, ReggianiC (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 91: 1447–1531.

3. BraunT, GautelM (2011) Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis. Nat Rev Mol Cell Biol 12: 349–361.

4. GreisingSM, GranseeHM, MantillaCB, SieckGC (2012) Systems biology of skeletal muscle: fiber type as an organizing principle. Wiley Interdiscip Rev Syst Biol Med 4: 457–473.

5. ShragerJB, DesjardinsPR, BurkmanJM, KonigSK, StewartSK, et al. (2000) Human skeletal myosin heavy chain genes are tightly linked in the order embryonic-IIa-IId/x-ILb-perinatal-extraocular. J Muscle Res Cell Motil 21: 345–355.

6. PalstraR-J, de LaatW, GrosveldF (2008) Beta-globin regulation and long-range interactions. Adv Genet 61: 107–142.

7. GrifoneR, DemignonJ, HoubronC, SouilE, NiroC, et al. (2005) Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 132: 2235–2249.

8. RelaixF, DemignonJ, LaclefC, PujolJ, SantoliniM, et al. (2013) Six Homeoproteins Directly Activate Myod Expression in the Gene Regulatory Networks That Control Early Myogenesis. PLoS Genet 9: e1003425.

9. RichardA-F, DemignonJ, SakakibaraI, PujolJ, FavierM, et al. (2011) Genesis of muscle fiber-type diversity during mouse embryogenesis relies on Six1 and Six4 gene expression. Dev Biol 359: 303–320.

10. NiroC, DemignonJ, VincentS, LiuY, GiordaniJ, et al. (2010) Six1 and Six4 gene expression is necessary to activate the fast-type muscle gene program in the mouse primary myotome. Dev Biol 338: 168–182.

11. GrifoneR, LaclefC, LopezS, DemignonJ, GuidottiJ, et al. (2004) Six1 and Eya1 Expression Can Reprogram Adult Muscle from the Slow-Twitch Phenotype into the Fast-Twitch Phenotype. Mol Cell Biol 24: 6253–6267.

12. LaclefC, HamardG, DemignonJ, SouilE, HoubronC, et al. (2003) Altered myogenesis in Six1-deficient mice. Development 130: 2239–2252.

13. MercerTR, MattickJS (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20: 300–307.

14. LeeJT (2012) Epigenetic Regulation by Long Noncoding RNAs. Science (80-) 338: 1435–1439.

15. GuttmanM, RinnJL (2012) Modular regulatory principles of large non-coding RNAs. Nature 482: 339–346.

16. CesanaM, CacchiarelliD, LegniniI, SantiniT, SthandierO, et al. (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147: 358–369.

17. RinnJL, ChangHY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81: 145–166.

18. CabiancaDS, CasaV, BodegaB, XynosA, GinelliE, et al. (2012) A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149: 819–831.

19. WangKC, YangYW, LiuB, SanyalA, Corces-ZimmermanR, et al. (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120–124.

20. YangL, LinC, LiuW, ZhangJ, Ohgi Ka, et al. (2011) ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 147: 773–788.

21. TsaiM-C, ManorO, WanY, MosammaparastN, WangJK, et al. (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689–693.

22. RinnJL, KerteszM, WangJK, SquazzoSL, XuX, et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311–1323.

23. MartianovI, RamadassA, Serra BarrosA, ChowN, AkoulitchevA (2007) Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445: 666–670.

24. SchmitzK-M, MayerC, PostepskaA, GrummtI (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 24: 2264–2269.

25. MiniouP, TizianoD, FrugierT, RoblotN, Le MeurM, et al. (1999) Gene targeting restricted to mouse striated muscle lineage. Nucleic Acids Res 27: e27.

26. Le GrandF, GrifoneR, MourikisP, HoubronC, GigaudC, et al. (2012) Six1 regulates stem cell repair potential and self-renewal during skeletal muscle regeneration. J Cell Biol 198: 815–832.

27. Bassel-DubyR, OlsonEN (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75: 19–37.

28. AnC-I, DongY, HagiwaraN (2011) Genome-wide mapping of Sox6 binding sites in skeletal muscle reveals both direct and indirect regulation of muscle terminal differentiation by Sox6. BMC Dev Biol 11: 59.

29. PotthoffMJ, WuH, ArnoldMA, SheltonJM, BacksJ, et al. (2007) Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers. J Clin Invest 117: 2459–2467.

30. QuiatD, Voelker Ka, PeiJ, Grishin NV, GrangeRW, et al. (2011) Concerted regulation of myofiber-specific gene expression and muscle performance by the transcriptional repressor Sox6. Proc Natl Acad Sci U S A 108: 10196–10201.

31. FaticaA, BozzoniI (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15: 7–21.

32. ToyoshimaC, IwasawaS, OgawaH, HirataA, TsuedaJ, et al. (2013) Crystal structures of the calcium pump and sarcolipin in the Mg2+-bound E1 state. Nature 495: 260–264.

33. WintherA-ML, BublitzM, KarlsenJL, MøllerJV, HansenJB, et al. (2013) The sarcolipin-bound calcium pump stabilizes calcium sites exposed to the cytoplasm. Nature 495: 265–269.

34. LiuY, ChuA, ChakrounI, IslamU, BlaisA (2010) Cooperation between myogenic regulatory factors and SIX family transcription factors is important for myoblast differentiation. Nucleic Acids Res 38: 6857–6871.

35. Van RooijE, QuiatD, JohnsonBa, SutherlandLB, QiX, et al. (2009) A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 17: 662–673.

36. HagègeH, KlousP, BraemC, SplinterE, DekkerJ, et al. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2: 1722–1733.

37. JoanneP, HourdéC, OchalaJ, CaudéranY, MedjaF, et al. (2012) Impaired adaptive response to mechanical overloading in dystrophic skeletal muscle. PLoS One 7: e35346.

38. GiordaniJ, BajardL, DemignonJ, DaubasP, BuckinghamM, et al. (2007) Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs. Proc Natl Acad Sci U S A 104: 11310–11315.

39. RouaultH, SantoliniM, SchweisguthF, HakimV (2014) Imogene: identification of motifs and cis-regulatory modules underlying gene co-regulation. Nucleic Acids Res doi: 10.1093/nar/gku209

40. GruberAR, LorenzR, BernhartSH, NeuböckR, HofackerIL (2008) The Vienna RNA websuite. Nucleic Acids Res 36: W70–4.