Genome-wide analysis of H3.3 dissociation reveals high nucleosome turnover at distal regulatory regions of embryonic stem cells

详细信息    查看全文

• 作者：Misook Ha (1)
  Daniel C Kraushaar (2)
  Keji Zhao (2)
  
  1. Samsung Advanced Institute of Technology ; Samsung Electronics Corporation ; Yongin-Si ; 446-712 ; Gyeonggi-Do ; South Korea
  2. Systems Biology Center ; National Heart ; Lung ; and Blood Institute ; NIH ; Bethesda ; MD ; 20892 ; USA
  
• 关键词：Histone variant ; H3.3 dissociation ; Nucleosome stability ; Genome ; wide chromatin dynamics
• 刊名：Epigenetics & Chromatin
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：7
• 期：1
• 全文大小：2,334 KB
• 参考文献：1. Goldberg, AD, Banaszynski, LA, Noh, KM, Lewis, PW, Elsaesser, SJ, Stadler, S, Dewell, S, Law, M, Guo, X, Li, X, Wen, D, Chapgier, A, DeKelver, RC, Miller, JC, Lee, YL, Boydston, EA, Holmes, MC, Gregory, PD, Greally, JM, Rafii, S, Yang, C, Scambler, PJ, Garrick, D, Gibbons, RJ, Higgs, DR, Cristea, IM, Urnov, FD, Zheng, D, Allis, CD (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140: pp. 678-691 CrossRef
  2. Jin, C, Felsenfeld, G (2007) Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21: pp. 1519-1529 CrossRef
  3. Ahmad, K, Henikoff, S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9: pp. 1191-1200 CrossRef
  4. McKittrick, E, Gafken, PR, 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: pp. 1525-1530 CrossRef
  5. Ray-Gallet, D, Quivy, JP, Scamps, C, Martini, EM, Lipinski, M, Almouzni, G (2002) HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell 9: pp. 1091-1100 CrossRef
  6. Elsaesser, SJ, Goldberg, AD, Allis, CD (2010) New functions for an old variant: no substitute for histone H3.3. Curr Opin Genet Dev 20: pp. 110-117 CrossRef
  7. Wong, LH, McGhie, JD, Sim, M, Anderson, MA, Ahn, S, Hannan, RD, George, AJ, Morgan, KA, Mann, JR, Choo, KH (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 20: pp. 351-360 CrossRef
  8. Schwartz, BE, Ahmad, K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19: pp. 804-814 CrossRef
  9. Tamura, T, Smith, M, Kanno, T, Dasenbrock, H, Nishiyama, A, Ozato, K (2009) Inducible deposition of the histone variant H3.3 in interferon-stimulated genes. J Biol Chem 284: pp. 12217-12225 CrossRef
  10. Hake, SB, Garcia, BA, Duncan, EM, Kauer, M, Dellaire, G, Shabanowitz, J, Bazett-Jones, DP, Allis, CD, Hunt, DF (2006) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem 281: pp. 559-568 CrossRef
  11. Banaszynski, LA, Wen, D, Dewell, S, Whitcomb, SJ, Lin, M, Diaz, N, Elsasser, SJ, Chapgier, A, Goldberg, AD, Canaani, E, Rafii, S, Zheng, D, Allis, CD (2013) Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 155: pp. 107-120 CrossRef
  12. Santenard, A, Ziegler-Birling, C, Koch, M, Tora, L, Bannister, AJ, Torres-Padilla, ME (2010) Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat Cell Biol 12: pp. 853-862 CrossRef
  13. Kraushaar, DC, 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: pp. R121 CrossRef
  14. Boyer, LA, Plath, K, Zeitlinger, J, Brambrink, T, Medeiros, LA, Lee, TI, Levine, SS, Wernig, M, Tajonar, A, Ray, MK, Bell, GW, Otte, AP, Vidal, M, Gifford, DK, Young, RA, Jaenisch, R (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: pp. 349-353 CrossRef
  15. Mikkelsen, TS, Ku, M, Jaffe, DB, Issac, B, Lieberman, E, Giannoukos, G, Alvarez, P, Brockman, W, Kim, TK, Koche, RP, Lee, W, Mendenhall, E, O鈥橠onovan, A, Presser, A, Russ, C, Xie, X, Meissner, A, Wernig, M, Jaenisch, R, Nusbaum, C, Lander, ES, Bernstein, BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: pp. 553-560 CrossRef
  16. Kraushaar, DC, Zhao, K (2013) The epigenomics of embryonic stem cell differentiation. Int J Biol Sci 9: pp. 1134-1144 CrossRef
  17. Meshorer, E, Yellajoshula, D, George, E, Scambler, PJ, Brown, DT, Misteli, T (2006) Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10: pp. 105-116 CrossRef
  18. Dion, MF, Kaplan, T, Kim, M, Buratowski, S, Friedman, N, Rando, OJ (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315: pp. 1405-1408 CrossRef
  19. Deal, RB, Henikoff, JG, Henikoff, S (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328: pp. 1161-1164 CrossRef
  20. Nishiyama, A, Xin, L, Sharov, AA, Thomas, M, Mowrer, G, Meyers, E, Piao, Y, Mehta, S, Yee, S, Nakatake, Y, Stagg, C, Sharova, L, Correa-Cerro, LS, Bassey, U, Hoang, H, Kim, E, Tapnio, R, Qian, Y, Dudekula, D, Zalman, M, Li, M, Falco, G, Yang, HT, Lee, SL, Monti, M, Stanghellini, I, Islam, MN, Nagaraja, R, Goldberg, I, Wang, W (2009) Uncovering early response of gene regulatory networks in ESCs by systematic induction of transcription factors. Cell Stem Cell 5: pp. 420-433 CrossRef
  21. De Santa, F, Barozzi, I, Mietton, F, Ghisletti, S, Polletti, S, Tusi, BK, Muller, H, Ragoussis, J, Wei, CL, Natoli, G (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8: pp. e1000384 CrossRef
  22. Kim, TK, Hemberg, M, Gray, JM, Costa, AM, Bear, DM, Wu, J, Harmin, DA, Laptewicz, M, Barbara-Haley, K, Kuersten, S, Markenscoff-Papadimitriou, E, Kuhl, D, Bito, H, Worley, PF, Kreiman, G, Greenberg, ME (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465: pp. 182-187 CrossRef
  23. Murakami, K, Elmlund, H, Kalisman, N, Bushnell, DA, Adams, CM, Azubel, M, Elmlund, D, Levi-Kalisman, Y, Liu, X, Gibbons, BJ, Levitt, M, Kornberg, RD (2013) Architecture of an RNA polymerase II transcription pre-initiation complex. Science 342: pp. 1238724 CrossRef
  24. Lai, AY, Wade, PA (2011) Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat Rev Cancer 11: pp. 588-596 CrossRef
  25. Kizer, KO, Phatnani, HP, Shibata, Y, Hall, H, Greenleaf, AL, Strahl, BD (2005) A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol 25: pp. 3305-3316 CrossRef
  26. Li, B, Jackson, J, Simon, MD, Fleharty, B, Gogol, M, Seidel, C, Workman, JL, Shilatifard, A (2009) Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J Biol Chem 284: pp. 7970-7976 CrossRef
  27. Yamaguchi, S, Hong, K, Liu, R, Inoue, A, Shen, L, Zhang, K, Zhang, Y (2013) Dynamics of 5-methylcytosine and 5-hydroxymethylcytosine during germ cell reprogramming. Cell Res 23: pp. 329-339 CrossRef
  28. Xu, Y, Wu, F, Tan, L, Kong, L, Xiong, L, Deng, J, Barbera, AJ, Zheng, L, Zhang, H, Huang, S, Min, J, Nicholson, T, Chen, T, Xu, G, Shi, Y, Zhang, K, Shi, YG (2011) Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42: pp. 451-464 CrossRef
  29. Hu, G, Cui, K, Northrup, D, Liu, C, Wang, C, Tang, Q, Ge, K, Levens, D, Crane-Robinson, C, Zhao, K (2013) H2A.Z facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell 12: pp. 180-192 CrossRef
  30. Li, Z, Gadue, P, Chen, K, Jiao, Y, Tuteja, G, Schug, J, Li, W, Kaestner, KH (2012) Foxa2 and H2A.Z mediate nucleosome depletion during embryonic stem cell differentiation. Cell 151: pp. 1608-1616 CrossRef
  31. Blackledge, NP, Zhou, JC, Tolstorukov, MY, Farcas, AM, Park, PJ, Klose, RJ (2010) CpG islands recruit a histone H3 lysine 36 demethylase. Mol Cell 38: pp. 179-190 CrossRef
  32. Kunarso, G, Chia, NY, Jeyakani, J, Hwang, C, Lu, X, Chan, YS, Ng, HH, Bourque, G (2010) Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42: pp. 631-634 CrossRef
  33. Schones, DE, Cui, K, Cuddapah, S, Roh, TY, Barski, A, Wang, Z, Wei, G, Zhao, K (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell 132: pp. 887-898 CrossRef
  34. Ray-Gallet, D, Woolfe, A, Vassias, I, Pellentz, C, Lacoste, N, Puri, A, Schultz, DC, Pchelintsev, NA, Adams, PD, Jansen, LE, Almouzni, G (2011) Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 44: pp. 928-941 CrossRef
  35. Mavrich, TN, Jiang, C, Ioshikhes, IP, Li, X, Venters, BJ, Zanton, SJ, Tomsho, LP, Qi, J, Glaser, RL, Schuster, SC, Gilmour, DS, Albert, I, Pugh, BF (2008) Nucleosome organization in the Drosophila genome. Nature 453: pp. 358-362 CrossRef
  36. Kaplan, N, Moore, IK, Fondufe-Mittendorf, Y, Gossett, AJ, Tillo, D, Field, Y, LeProust, EM, Hughes, TR, Lieb, JD, Widom, J, Segal, E (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: pp. 362-366 CrossRef
  37. Radman-Livaja, M, Rando, OJ (2010) Nucleosome positioning: how is it established, and why does it matter?. Dev Biol 339: pp. 258-266 CrossRef
  38. Huang, C, Zhu, B (2014) H3.3 turnover: a mechanism to poise chromatin for transcription, or a response to open chromatin?. Bioessays 36: pp. 579-584 CrossRef
  39. Shogren-Knaak, M, Ishii, H, Sun, JM, Pazin, MJ, Davie, JR, Peterson, CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311: pp. 844-847 CrossRef
  40. Svaren, J, Horz, W (1997) Transcription factors vs nucleosomes: regulation of the PHO5 promoter in yeast. Trends Biochem Sci 22: pp. 93-97 CrossRef
  41. Boeger, H, Griesenbeck, J, Strattan, JS, Kornberg, RD (2004) Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol Cell 14: pp. 667-673 CrossRef
  42. Zaret, KS, Caravaca, JM, Tulin, A, Sekiya, T (2010) Nuclear mobility and mitotic chromosome binding: similarities between pioneer transcription factor FoxA and linker histone H1. Cold Spring Harb Symp Quant Biol 75: pp. 219-226 CrossRef
  43. Ballare, C, Castellano, G, Gaveglia, L, Althammer, S, Gonzalez-Vallinas, J, Eyras, E, Le Dily, F, Zaurin, R, Soronellas, D, Vicent, GP, Beato, M (2013) Nucleosome-driven transcription factor binding and gene regulation. Mol Cell 49: pp. 67-79
  44. Huang, C, Zhang, Z, Xu, M, Li, Y, Li, Z, Ma, Y, Cai, T, Zhu, B (2013) H3.3鈥揌4 tetramer splitting events feature cell-type specific enhancers. PLoS Genet 9: pp. e1003558 CrossRef
  45. Kraushaar, DC, Yamaguchi, Y, Wang, L (2010) Heparan sulfate is required for embryonic stem cells to exit from self-renewal. J Biol Chem 285: pp. 5907-5916 CrossRef
  46. Shechter, D, Dormann, HL, Allis, CD, Hake, SB (2007) Extraction, purification and analysis of histones. Nat Protoc 2: pp. 1445-1457 CrossRef
  47. Barski, A, Cuddapah, S, Cui, K, Roh, TY, Schones, DE, Wang, Z, Wei, G, Chepelev, I, Zhao, K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: pp. 823-837 CrossRef
  48. Chen, X, Xu, H, Yuan, P, Fang, F, Huss, M, Vega, VB, Wong, E, Orlov, YL, Zhang, W, Jiang, J, Loh, YH, Yeo, HC, Yeo, ZX, Narang, V, Govindarajan, KR, Leong, B, Shahab, A, Ruan, Y, Bourque, G, Sung, WK, Clarke, ND, Wei, CL, Ng, HH (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: pp. 1106-1117 CrossRef
  49. Ku, M, Koche, RP, Rheinbay, E, Mendenhall, EM, Endoh, M, Mikkelsen, TS, Presser, A, Nusbaum, C, Xie, X, Chi, AS, Adli, M, Kasif, S, Ptaszek, LM, Cowan, CA, Lander, ES, Koseki, H, Bernstein, BE (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4: pp. e1000242 CrossRef
  50. Kagey, MH, Newman, JJ, Bilodeau, S, Zhan, Y, Orlando, DA, van Berkum, NL, Ebmeier, CC, Goossens, J, Rahl, PB, Levine, SS, Taatjes, DJ, Dekker, J, Young, RA (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: pp. 430-435 CrossRef
  51. Whyte, WA, Bilodeau, S, Orlando, DA, Hoke, HA, Frampton, GM, Foster, CT, Cowley, SM, Young, RA (2012) Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482: pp. 221-225
  52. Stadler, MB, Murr, R, Burger, L, Ivanek, R, Lienert, F, Scholer, A, van Nimwegen, E, Wirbelauer, C, Oakeley, EJ, Gaidatzis, D, Tiwari, VK, Schubeler, D (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: pp. 490-495
  
• 刊物主题：Animal Genetics and Genomics; Human Genetics; Plant Genetics & Genomics; Cell Biology;
• 出版者：BioMed Central
• ISSN：1756-8935

文摘

Background The histone variant H3.3 plays a critical role in maintaining the pluripotency of embryonic stem cells (ESCs) by regulating gene expression programs important for lineage specification. H3.3 is deposited by various chaperones at regulatory sites, gene bodies, and certain heterochromatic sites such as telomeres and centromeres. Using Tet-inhibited expression of epitope-tagged H3.3 combined with ChIP-Seq we undertook genome-wide measurements of H3.3 dissociation rates across the ESC genome and examined the relationship between H3.3-nucleosome turnover and ESC-specific transcription factors, chromatin modifiers, and epigenetic marks. Results Our comprehensive analysis of H3.3 dissociation rates revealed distinct H3.3 dissociation dynamics at various functional chromatin domains. At transcription start sites, H3.3 dissociates rapidly with the highest rate at nucleosome-depleted regions (NDRs) just upstream of Pol II binding, followed by low H3.3 dissociation rates across gene bodies. H3.3 turnover at transcription start sites, gene bodies, and transcription end sites was positively correlated with transcriptional activity. H3.3 is found decorated with various histone modifications that regulate transcription and maintain chromatin integrity. We find greatly varying H3.3 dissociation rates across various histone modification domains: high dissociation rates at active histone marks and low dissociation rates at heterochromatic marks. Well- defined zones of high H3.3-nucleosome turnover were detected at binding sites of ESC-specific pluripotency factors and chromatin remodelers, suggesting an important role for H3.3 in facilitating protein binding. Among transcription factor binding sites we detected higher H3.3 turnover at distal cis-acting sites compared to proximal genic transcription factor binding sites. Our results imply that fast H3.3 dissociation is a hallmark of interactions between DNA and transcriptional regulators. Conclusion Our study demonstrates that H3.3 turnover and nucleosome stability vary greatly across the chromatin landscape of embryonic stem cells. The presence of high H3.3 turnover at RNA Pol II binding sites at extragenic regions as well as at transcription start and end sites of genes, suggests a specific role for H3.3 in transcriptional initiation and termination. On the other hand, the presence of well-defined zones of high H3.3 dissociation at transcription factor and chromatin remodeler binding sites point to a broader role in facilitating accessibility.