UTX demethylase activity is required for satellite cell-mediated muscle regeneration

Journal of Clinical Investigation

Volumn 126, Issue 4, 2016, Pages 1555-1565

  Faralli, Hervé ^a,b   Wang, Chaochen ^c   Nakka, Kiran ^a,b   Benyoucef, Aissa ^a,b   Sebastian, Soji ^a,f   Zhuang, Lenan ^c   Chu, Alphonse ^a,b   Palii, Carmen G ^a,b   Liu, Chengyu ^d   Camellato, Brendan ^a,e   Brand, Marjorie ^a,b,e   Ge, Kai ^c   Dilworth, F Jeffrey ^a,b,e  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e UNIVERSITY OF OTTAWA   (Canada)

^f CANADIAN NUCLEAR LABORATORIES   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEMETHYLASE; HISTONE DEMETHYLASE UTX; HISTONE H3; LYSINE; MYOGENIN; UNCLASSIFIED DRUG; HISTONE; MYOG PROTEIN, MOUSE; UTX PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE; GENE EXPRESSION; HISTONE DEMETHYLATION; IN VIVO STUDY; INFLAMMATORY CELL; MALE; MOUSE; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SKELETAL MUSCLE SATELLITE CELL; STEM CELL; UTX GENE; ANIMAL; BIOSYNTHESIS; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUSCLE FIBRIL; PHYSIOLOGY; REGENERATION;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; HISTONE DEMETHYLASES; HISTONES; MALE; MICE; MICE, KNOCKOUT; MYOFIBRILS; MYOGENIN; REGENERATION; SATELLITE CELLS, SKELETAL MUSCLE;

EID: 84964670056     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI83239     Document Type: Article

References (55)

1. Steffen PA, Ringrose L. What are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory. Nat Rev Mol Cell Biol. 2014;15(5):340-356.
2. Ringrose L, Paro R. Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annu Rev Genet. 2004;38(1):413-443.
3. Barski A, et al. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823-837.
4. Bernstein BE, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125(2):315-326.
5. Cao R, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298(5595):1039-1043.
6. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell. 2002;111(2):185-196.
7. Muller J, et al. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell. 2002;111(2):197-208.
8. Pengelly AR, Copur O, Jackle H, Herzig A, Muller J. A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science. 2013;339(6120):698-699.
9. Hansen KH, et al. A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol. 2008;10(11):1291-1300.
10. Gaydos LJ, Wang W, Strome S. Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science. 2014;345(6203):1515-1518.
11. Lan F, et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature. 2007;449(7163):689-694.
12. Agger K, et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature. 2007;449(7163):731-734.
13. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, Ge K. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci U S A. 2007;104(47):18439-18444.
14. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell. 2007;130(6):1083-1094.
15. Lee MG, et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science. 2007;318(5849):447-450.
16. Greenfield A, et al. The UTX gene escapes X inactivation in mice and humans. Hum Mol Genet. 1998;7(4):737-742.
17. Shpargel KB, Sengoku T, Yokoyama S, Magnuson T. UTX and UTY demonstrate histone demethylase-independent function in mouse embryonic development. PLoS Genet. 2012;8(9):e1002964.
18. Sen GL, Webster DE, Barragan DI, Chang HY, Khavari PA. Control of differentiation in a self-renewing mammalian tissue by the histone demethylase JMJD3. Genes Dev. 2008;22(14):1865-1870.
19. Seenundun S, et al. UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. EMBO J. 2010;29(8):1401-1411.
20. Mansour AA, et al. The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming. Nature. 2012;488(7411):409-413.
21. van Haaften G, et al. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat Genet. 2009;41(5):521-523.
22. Copur O, Müller J. The histone H3-K27 demethylase Utx regulates HOX gene expression in Drosophila in a temporally restricted manner. Development. 2013;140(16):3478-3485.
23. Vandamme J, Lettier G, Sidoli S, Di Schiavi E, Norregaard Jensen O, Salcini AE. The C. elegans H3K27 demethylase UTX-1 is essential for normal development, independent of its enzymatic activity. PLoS Genet. 2012;8(5):e1002647.
24. Shpargel KB, Starmer J, Yee D, Pohlers M, Magnuson T. KDM6 demethylase independent loss of histone H3 lysine 27 trimethylation during early embryonic development. PLoS Genet. 2014;10(8):e1004507.
25. Miller SA, Mohn SE, Weinmann AS. Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol Cell. 2010;40(4):594-605.
26. Wang C, et al. UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity. Proc Natl Acad Sci U S A. 2012;109(38):15324-15329.
27. Thieme S, et al. The histone demethylase UTX regulates stem cell migration and hematopoiesis. Blood. 2013;121(13):2462-2473.
28. Bentzinger CF, Wang YX, von Maltzahn J, Rudnicki MA. The emerging biology of muscle stem cells: implications for cell-based therapies. Bioessays. 2013;35(3):231-241.
29. Aziz A, Sebastian S, Dilworth FJ. The origin and fate of muscle satellite cells. Stem Cell Rev. 2012;8(2):609-622.
30. Liu QC, et al. Comparative expression profiling identifies differential roles for Myogenin and p38alpha MAPK signaling in myogenesis. J Mol Cell Biol. 2012;4(6):386-397.
31. Singh K, Dilworth FJ. Differential modulation of cell cycle progression distinguishes members of the myogenic regulatory factor family of transcription factors. FEBS J. 2013;280(17):3991-4003.
32. Lepper C, Conway SJ, Fan CM. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature. 2009;460(7255):627-631.
33. Welstead GG, et al. X-linked H3K27me3 demethylase Utx is required for embryonic development in a sex-specific manner. Proc Natl Acad Sci U S A. 2012;109(32):13004-13009.
34. Kruidenier L, et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature. 2012;488(7411):404-408.
35. Cho YW, et al. PTIP associates with MLL3-and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem. 2007;282(28):20395-20406.
36. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR. Muscle satellite cells adopt divergent fates: A mechanism for self-renewal? J Cell Biol. 2004;166(3):347-357.
37. Siegel AL, Kuhlmann PK, Cornelison DD. Muscle satellite cell proliferation and association: new insights from myofiber time-lapse imaging. Skelet Muscle. 2011;1(1):7.
38. Juan AH, et al. Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev. 2011;25(8):789-794.
39. Woodhouse S, Pugazhendhi D, Brien P, Pell JM. Ezh2 maintains a key phase of muscle satellite cell expansion but does not regulate terminal differentiation. J Cell Sci. 2013;126(pt 2):565-579.
40. Blum R, Vethantham V, Bowman C, Rudnicki M, Dynlacht BD. Genome-wide identification of enhancers in skeletal muscle: The role of MyoD1. Genes Dev. 2012;26(24):2763-2779.
41. Chakroun I, et al. Genome-wide association between Six4, MyoD, and the histone demethylase Utx during myogenesis. FASEB J. 2015;29(11):4738-4755.
42. Wang AH, et al. The histone chaperone Spt6 coordinates histone H3K27 demethylation and myogenesis. EMBO J. 2013;32(8):1075-1086.
43. Faralli H, Dilworth FJ. Chaperoning RNA Polymerase II through repressive chromatin. EMBO J. 2013;32(8):1067-1068.
44. Liu L, et al. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 2013;4(1):189-204.
45. Judson RN, Zhang RH, Rossi FM. Tissue-resident mesenchymal stem/progenitor cells in skeletal muscle: collaborators or saboteurs? FEBS J. 2013;280(17):4100-4108.
46. Saclier M, Cuvellier S, Magnan M, Mounier R, Chazaud B. Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration. FEBS J. 2013;280(17):4118-4130.
47. Shefer G, Van de Mark DP, Richardson JB, Yablonka-Reuveni Z. Satellite-cell pool size does matter: defining the myogenic potency of aging skeletal muscle. Dev Biol. 2006;294(1):50-66.
48. Brand M, Rampalli S, Chaturvedi CP, Dilworth FJ. Analysis of epigenetic modifications of chromatin at specific gene loci by native chromatin immunoprecipitation (N-ChIP) of nucleosomes isolated using hydroxyapatite chromatography. Nat Protoc. 2008;3(3):398-409.
49. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-1760.
50. Shen L, Shao N, Liu X, Nestler E. ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics. 2014;15:284.
51. Trapnell C, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562-578.
52. Langmead B, Salzberg SL. Fast gappedread alignment with Bowtie 2. Nat Methods. 2012;9(4):357-359.
53. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105-1111.
54. Anders S, Pyl PT, Huber W. HTSeq - a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166-169.
55. Robinson MD, McCarthy DJ, Smyth GK. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139-140.