Incorporation of histone H3.1 suppresses the lineage potential of skeletal muscle

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 775-786

  Harada, Akihito ^a   Maehara, Kazumitsu ^a   Sato, Yuko ^b,c   Konno, Daijiro ^d   Tachibana, Taro ^e   Kimura, Hiroshi ^b,c   Ohkawa, Yasuyuki ^a,c  

^a KYUSHU UNIVERSITY   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d RIKEN   (Japan)

^e Osaka Prefecture University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE;

ANIMAL; CELL LINE; CELL LINEAGE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHYLATION; MOUSE; MUSCLE DEVELOPMENT; PROMOTER REGION; SKELETAL MUSCLE;

ANIMALS; CELL LINE; CELL LINEAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; METHYLATION; MICE; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; PROMOTER REGIONS, GENETIC;

EID: 84941095996     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1346     Document Type: Article

References (59)

1. Strahl, B.D., Allis, C.D. (2000) The language of covalent histone modifications. Nature, 403, 41-45.
2. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jorgensen, H.F., John, R.M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M. et al. (2006) Chromatin signatures of pluripotent cell lines. Nat. Cell Biol., 8, 532-538.
3. Bernstein, B.E., Mikkelsen, T.S., Xie, X.H., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125, 315-326.
4. Mikkelsen, T.S., Ku, M.C., Jaffe, D.B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.K., Koche, R.P. et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature, 448, 553-560.
5. Ahmad, K., Henikoff, S. (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell, 9, 1191-1200.
6. Goldberg, A.D., Banaszynski, L.A., Noh, K.M., Lewis, P.W., Elsaesser, S.J., Stadler, S., Dewell, S., Law, M., Guo, X.Y., Li, X. et al. (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell, 140, 678-691.
7. Ng, R.K., Gurdon, J.B. (2008) Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat. Cell Biol., 10, U102-U183.
8. McKittrick, E., Gaften, P.R., Ahmad, K., Henikoff, S. (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. U.S.A., 101, 1525-1530.
9. Loyola, A., Bonaldi, T., Roche, D., Imhof, A., Almouzni, G. (2006) PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell, 24, 309-316.
10. Loyola, A., Almouzni, G. (2007) Marking histone H3 variants: how, when and why? Trends Biochem. Sci., 32, 425-433.
11. Schwartzentruber, J., Korshunov, A., Liu, X.Y., Jones, D.T.W., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A.M., Quang, D.A.K., Tonjes, M. et al. (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature, 482, 226-231.
12. Santenard, A., Ziegler-Birling, C., Koch, M., Tora, L., Bannister, A.J., Torres-Padilla, M.E. (2010) Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat. Cell Biol., 12, 853-862.
13. Harada, A., Okada, S., Konno, D., Odawara, J., Yoshimi, T., Yoshimura, S., Kumamaru, H., Saiwai, H., Tsubota, T., Kurumizaka, H. et al. (2012) Chd2 interacts with H3.3 to determine myogenic cell fate. EMBO J., 31, 2994-3007.
14. Asp, P., Blum, R., Vethantham, V., Parisi, F., Micsinai, M., Cheng, J., Bowman, C., Kluger, Y., Dynlacht, B.D. (2011) Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc. Natl. Acad. Sci. U.S.A., 108, E149-E158.
15. Caretti, G., Di Padova, M., Micales, B., Lyons, G.E., Sartorelli, V. (2004) The Polycomb EA2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Gene Dev., 18, 2627-2638.
16. Juan, A.H., Derfoul, A., Feng, X.S., Ryall, J.G., Dell'Orso, S., Pasut, A., Zare, H., Simone, J.M., Rudnicki, M.A., Sartorelli, V. (2011) Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Gene Dev., 25, 789-794.
17. Woodhouse, S., Pugazhendhi, D., Brien, P., Pell, J.M. (2013) Ezh2 maintains a key phase of muscle satellite cell expansion but does not regulate terminal differentiation. J. Cell Sci., 126, 565-579.
18. Seenundun, S., Rampalli, S., Liu, Q.C., Aziz, A., Palii, C., Hong, S.H., Blais, A., Brand, M., Ge, K., Dilworth, F.J. (2010) UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. EMBO J., 29, 1401-1411.
19. De la Serna, I.L., Carlson, K.A., Hill, D.A., Guidi, C.J., Stephenson, R.O., Sif, S., Kingston, R.E., Imbalzano, A.N. (2000) Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene. Mol. Cell. Biol., 20, 2839-2851.
20. Kawakami, K., Noda, T. (2004) Transposition of the Tol2 element, an Ac-like element from the Japanese medaka fish Oryzias latipes, in mouse embryonic stem cells. Genetics, 166, 895-899.
21. Kawakami, K., Takeda, H., Kawakami, N., Kobayashi, M., Matsuda, N., Mishina, M. (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell, 7, 133-144.
22. Urasaki, A., Morvan, G., Kawakami, K. (2006) Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics, 174, 639-649.
23. Kimura, H., Takizawa, N., Allemand, E., Hori, T., Iborra, F.J., Nozaki, N., Muraki, M., Hagiwara, M., Krainer, A.R., Fukagawa, T. et al. (2006) A novel histone exchange factor, protein phosphatase 2C gamma mediates the exchange and dephosphorylation of H2A-H2B. J. Cell Biol., 175, 389-400.
24. Nozawa, R.S., Nagao, K., Masuda, H.T., Iwasaki, O., Hirota, T., Nozaki, N., Kimura, H., Obuse, C. (2010) Human POGZ modulates dissociation of HP1 alpha from mitotic chromosome arms through Aurora B activation. Nat. Cell Biol., 12, 719-727.
25. Ohkawa, Y., Marfella, C.G.A., Imbalzano, A.N. (2006) Skeletal muscle specification by myogenin and Mef2D via the SWI/SNF ATPase Brg1. EMBO J., 25, 490-501.
26. Kimura, H., Hayashi-Takanaka, Y., Goto, Y., Takizawa, N., Nozaki, N. (2008) The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Struct. Funct., 33, 61-73.
27. Hayashi-Takanaka, Y., Yamagata, K., Wakayama, T., Stasevich, T.J., Kainuma, T., Tsurimoto, T., Tachibana, M., Shinkai, Y., Kurumizaka, H., Nozaki, N. et al. (2011) Tracking epigenetic histone modifications in single cells using Fab-based live endogenous modification labeling. Nucleic Acids Res., 39, 6475-6488.
28. Langmead, B., Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods, 9, 357-359.
29. Shen, Y., Yue, F., McCleary, D.F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V.V. et al. (2012) A map of the cis-regulatory sequences in the mouse genome. Nature, 488, 116-120.
30. Taher, L., Collette, N.M., Murugesh, D., Maxwell, E., Ovcharenko, I., Loots, G.G. (2011) Global gene expression analysis of murine limb development. PLoS One, 6, e28358.
31. Xiao, S.J., Zhang, C., Zou, Q., Ji, Z.L. (2010) TiSGeD: a database for tissue-specific genes. Bioinformatics, 26, 1273-1275.
32. Odawara, J., Harada, A., Yoshimi, T., Maehara, K., Tachibana, T., Okada, S., Akashi, K., Ohkawa, Y. (2011) The classification of mRNA expression levels by the phosphorylation state of RNAPII CTD based on a combined genome-wide approach. BMC Genomics, 12, 516.
33. Brand, M., Rampalli, S., Chaturvedi, C.P., Dilworth, F.J. (2008) Analysis of epigenetic modifications of chromatin at specific gene loci by native chromatin immunoprecipitation of nucleosomes isolated using hydroxyapatite chromatography. Nat. Protoc., 3, 398-409.
34. Banaszynski, L.A., Wen, D.C., Dewell, S., Whitcomb, S.J., Lin, M.Y., Diaz, N., Elsasser, S.J., Chapgier, A., Goldberg, A.D., Canaani, E. et al. (2013) Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell, 155, 107-120.
35. Daury, L., Chailleux, C., Bonvallet, J., Trouche, D. (2006) Histone H3.3 deposition at E2F-regulated genes is linked to transcription. EMBO Rep., 7, 66-71.
36. Jin, C.Y., Zang, C.Z., Wei, G., Cui, K.R., Peng, W.Q., Zhao, K.J., Felsenfeld, G. (2009) H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat. Genet., 41, 941-945.
37. Jin, C.Y., Felsenfeld, G. (2007) Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Gene Dev., 21, 1519-1529.
38. Huang, C., Zhang, Z.Q., Xu, M., Li, Y.F., Li, Z., Ma, Y.T., Cai, T., Zhu, B. (2013) H3.3-H4 tetramer splitting events feature cell-type specific enhancers. PLoS Genet., 9, e1003558.
39. Kraushaar, D.C., Jin, W., Maunakea, A., Abraham, B., Ha, M., Zhao, K. (2013) Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol., 14, R121.
40. Yang, J.H., Song, Y., Seol, J.H., Park, J.Y., Yang, Y.J., Han, J.W., Youn, H.D., Cho, E.J. (2011) Myogenic transcriptional activation of MyoD mediated by replication-independent histone deposition. Proc. Natl. Acad. Sci. U.S.A., 108, 85-90.
41. Jullien, J., Astrand, C., Szenker, E., Garrett, N., Almouzni, G., Gurdon, J.B. (2012) HIRA dependent H3.3 deposition is required for transcriptional reprogramming following nuclear transfer to Xenopus oocytes. Epigenetics Chromatin, 5, 17.
42. Szenker, E., Lacoste, N., Almouzni, G. (2012) A developmental requirement for HIRA-dependent H3.3 deposition revealed at gastrulation in xenopus. Cell Rep., 1, 730-740.
43. Pchelintsev, N.A., McBryan, T., Rai, T.S., van Tuyn, J., Ray-Gallet, D., Almouzni, G., Adams, P.D. (2013) Placing the HIRA histone chaperone complex in the chromatin landscape. Cell Rep, 3, 1012-1019.
44. Drane, P., Ouararhni, K., Depaux, A., Shuaib, M., Hamiche, A. (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Gene Dev., 24, 1253-1265.
45. Delbarre, E., Ivanauskiene, K., Kuntziger, T., Collas, P. (2013) DAXX-dependent supply of soluble (H3.3-H4) dimers to PML bodies pending deposition into chromatin. Genome Res., 23, 440-451.
46. Lassar, A.B., Paterson, B.M., Weintraub, H. (1986) Transfection of a dna locus that mediates the conversion of 10T1/2 fibroblasts to myoblasts. Cell, 47, 649-656.
47. Elsasser, S.J., Huang, H.D., Lewis, P.W., Chin, J.W., Allis, C.D., Patel, D.J. (2012) DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature, 491, 560-565.
48. Liu, C.P., Xiong, C.Y., Wang, M.Z., Yu, Z.L., Yang, N., Chen, P., Zhang, Z.G., Li, G.H., Xu, R.M. (2012) Structure of the variant histone H3.3-H4 heterodimer in complex with its chaperone DAXX. Nat. Struct. Mol. Biol., 19, 1287-1292.
49. Song, Y., Seol, J.H., Yang, J.H., Kim, H.J., Han, J.W., Youn, H.D., Cho, E.J. (2013) Dissecting the roles of the histone chaperones reveals the evolutionary conserved mechanism of transcription-coupled deposition of H3.3. Nucleic Acids Res., 41, 5199-5209.
50. Wirbelauer, C., Bell, O., Schubeler, D. (2005) Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Gene Dev., 19, 1761-1766.
51. Delbarre, E., Jacobsen, B.M., Reiner, A.H., Sorensen, A.L., Kuntziger, T., Collas, P. (2010) Chromatin environment of histone variant H3.3 revealed by quantitative imaging and genome-scale chromatin and DNA immunoprecipitation. Mol. Biol. Cell, 21, 1872-1884.
52. Voigt, P., LeRoy, G., Drury, W.J., Zee, B.M., Son, J., Beck, D.B., Young, N.L., Garcia, B.A., Reinberg, D. (2012) Asymmetrically modified nucleosomes. Cell, 151, 181-193.
53. Issaeva, I., Zonis, Y., Rozovskaia, T., Orlovsky, K., Croce, C.M., Nakamura, T., Mazo, A., Eisenbach, L., Canaani, E. (2007) Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol. Cell. Biol., 27, 1889-1903.
54. Klose, R.J., Yan, Q., Tothova, Z., Yamane, K., Erdjument-Bromage, H., Tempst, P., Gilliland, D.G., Zhang, Y., Kaelin, W.G. (2007) The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell, 128, 889-900.
55. Pasini, D., Hansen, K.H., Christensen, J., Agger, K., Cloos, P.A.C., Helin, K. (2008) Coordinated regulation of transcriptional repression by the RBP2 H3K4 demethylase and polycomb-repressive complex 2. Gene Dev., 22, 1345-1355.
56. Hake, S.B., Allis, C.D. (2006) Histone H3 variants and their potential role in indexing mammalian genomes: The 'H3 barcode hypothesis'. Proc. Natl. Acad. Sci. U.S.A., 103, 6428-6435.
57. Lewis, P.W., Elsaesser, S.J., Noh, K.M., Stadler, S.C., Allis, C.D. (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. U.S.A., 107, 14075-14080.
58. Zhu, J., Adli, M., Zou, J.Y., Verstappen, G., Coyne, M., Zhang, X.L., Durham, T., Miri, M., Deshpande, V., De Jager, P.L. et al. (2013) Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell, 152, 642-654.
59. Vastenhouw, N.L., Zhang, Y., Woods, I.G., Imam, F., Regev, A., Liu, X.S., Rinn, J., Schier, A.F. (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature, 464, 922-926.