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Structural characterization of H3K56Q nucleosomes and nucleosomal arrays.

Watanabe S, Resch M, Lilyestrom W, Clark N, Hansen JC, Peterson C, Luger K
Biochim Biophys Acta 1799 480-6
Cited: 38 times
EuropePMC logo PMID: 20100606

Abstract

The post-translational modification of histones is a key mechanism for the modulation of DNA accessibility. Acetylated lysine 56 in histone H3 is associated with nucleosome assembly during replication and DNA repair, and is thus likely to predominate in regions of chromatin containing nucleosome-free regions. Here we show by X-ray crystallography that mutation of H3 lysine 56 to glutamine (to mimic acetylation) or glutamate (to cause a charge reversal) has no detectable effects on the structure of the nucleosome. At the level of higher order chromatin structure, the K to Q substitution has no effect on the folding of model nucleosomal arrays in cis, regardless of the degree of nucleosome density. In contrast, defects in array-array interactions in trans ('oligomerization') are selectively observed for mutant H3 lysine 56 arrays that contain nucleosome-free regions. Our data suggests that H3K56 acetylation is one of the molecular mechanisms employed to keep chromatin with nucleosome-free regions accessible to the DNA replication and repair machinery.

Reviews - 3kwq mentioned but not cited (1)

  1. Efficient and Innocuous Live-Cell Delivery: Making Membrane Barriers Disappear to Enable Cellular Biochemistry: How Better Cellular Delivery Tools Can Contribute to Precise and Quantitative Cell Biology Assays. Pellois JP. Bioessays 41 e1900031 (2019)

Articles - 3kwq mentioned but not cited (3)

  1. Structural characterization of H3K56Q nucleosomes and nucleosomal arrays. Watanabe S, Resch M, Lilyestrom W, Clark N, Hansen JC, Peterson C, Luger K. Biochim Biophys Acta 1799 480-486 (2010)
  2. Surprising Twists in Nucleosomal DNA with Implication for Higher-order Folding. Todolli S, Young RT, Watkins AS, Bu Sha A, Yager J, Olson WK. J Mol Biol 433 167121 (2021)
  3. Statistical investigation of position-specific deformation pattern of nucleosome DNA based on multiple conformational properties. Yang X, Yan Y. Bioinformation 7 120-124 (2011)


Reviews citing this publication (10)

  1. Histone core modifications regulating nucleosome structure and dynamics. Tessarz P, Kouzarides T. Nat Rev Mol Cell Biol 15 703-708 (2014)
  2. Interpreting the language of histone and DNA modifications. Rothbart SB, Strahl BD. Biochim Biophys Acta 1839 627-643 (2014)
  3. Chromatin higher-order structures and gene regulation. Li G, Reinberg D. Curr Opin Genet Dev 21 175-186 (2011)
  4. Post-translational modifications of histones that influence nucleosome dynamics. Bowman GD, Poirier MG. Chem Rev 115 2274-2295 (2015)
  5. Histone chaperones: modulators of chromatin marks. Avvakumov N, Nourani A, Côté J. Mol Cell 41 502-514 (2011)
  6. Chromatin dynamics: interplay between remodeling enzymes and histone modifications. Swygert SG, Peterson CL. Biochim Biophys Acta 1839 728-736 (2014)
  7. Nucleosome structural studies. Tan S, Davey CA. Curr Opin Struct Biol 21 128-136 (2011)
  8. Revisiting higher-order and large-scale chromatin organization. Bian Q, Belmont AS. Curr Opin Cell Biol 24 359-366 (2012)
  9. Nucleosome-level 3D organization of the genome. Ohno M, Priest DG, Taniguchi Y. Biochem Soc Trans 46 491-501 (2018)
  10. Getting down to the core of histone modifications. Jack AP, Hake SB. Chromosoma 123 355-371 (2014)

Articles citing this publication (24)

  1. A histone acetylation switch regulates H2A.Z deposition by the SWR-C remodeling enzyme. Watanabe S, Radman-Livaja M, Rando OJ, Peterson CL. Science 340 195-199 (2013)
  2. Preparation of fully synthetic histone H3 reveals that acetyl-lysine 56 facilitates protein binding within nucleosomes. Shimko JC, North JA, Bruns AN, Poirier MG, Ottesen JJ. J Mol Biol 408 187-204 (2011)
  3. Activator-dependent p300 acetylation of chromatin in vitro: enhancement of transcription by disruption of repressive nucleosome-nucleosome interactions. Szerlong HJ, Prenni JE, Nyborg JK, Hansen JC. J Biol Chem 285 31954-31964 (2010)
  4. Comprehensive structural analysis of mutant nucleosomes containing lysine to glutamine (KQ) substitutions in the H3 and H4 histone-fold domains. Iwasaki W, Tachiwana H, Kawaguchi K, Shibata T, Kagawa W, Kurumizaka H. Biochemistry 50 7822-7832 (2011)
  5. Multisite Substrate Recognition in Asf1-Dependent Acetylation of Histone H3 K56 by Rtt109. Zhang L, Serra-Cardona A, Zhou H, Wang M, Yang N, Zhang Z, Xu RM. Cell 174 818-830.e11 (2018)
  6. In Vitro Chromatin Assembly: Strategies and Quality Control. Muthurajan U, Mattiroli F, Bergeron S, Zhou K, Gu Y, Chakravarthy S, Dyer P, Irving T, Luger K. Methods Enzymol 573 3-41 (2016)
  7. Hyper-Acetylation of Histone H3K56 Limits Break-Induced Replication by Inhibiting Extensive Repair Synthesis. Che J, Smith S, Kim YJ, Shim EY, Myung K, Lee SE. PLoS Genet 11 e1004990 (2015)
  8. Distinct transcriptional roles for Histone H3-K56 acetylation during the cell cycle in Yeast. Topal S, Vasseur P, Radman-Livaja M, Peterson CL. Nat Commun 10 4372 (2019)
  9. An evolutionarily 'young' lysine residue in histone H3 attenuates transcriptional output in Saccharomyces cerevisiae. Hyland EM, Molina H, Poorey K, Jie C, Xie Z, Dai J, Qian J, Bekiranov S, Auble DT, Pandey A, Boeke JD. Genes Dev 25 1306-1319 (2011)
  10. Nucleosome conformational variability in solution and in interphase nuclei evidenced by cryo-electron microscopy of vitreous sections. Eltsov M, Grewe D, Lemercier N, Frangakis A, Livolant F, Leforestier A. Nucleic Acids Res 46 9189-9200 (2018)
  11. Regulation of chromatin assembly/disassembly by Rtt109p, a histone H3 Lys56-specific acetyltransferase, in vivo. Durairaj G, Chaurasia P, Lahudkar S, Malik S, Shukla A, Bhaumik SR. J Biol Chem 285 30472-30479 (2010)
  12. Dynamics of the higher-order structure of chromatin. Chen P, Li G. Protein Cell 1 967-971 (2010)
  13. Establishment and Maintenance of Chromatin Architecture Are Promoted Independently of Transcription by the Histone Chaperone FACT and H3-K56 Acetylation in Saccharomyces cerevisiae. McCullough LL, Pham TH, Parnell TJ, Connell Z, Chandrasekharan MB, Stillman DJ, Formosa T. Genetics 211 877-892 (2019)
  14. DNA sequence influences hexasome orientation to regulate DNA accessibility. Brehove M, Shatoff E, Donovan BT, Jipa CM, Bundschuh R, Poirier MG. Nucleic Acids Res 47 5617-5633 (2019)
  15. Structural dynamics of nucleosome mediated by acetylations at H3K56 and H3K115,122. Rajagopalan M, Balasubramanian S, Ioshikhes I, Ramaswamy A. Eur Biophys J 46 471-484 (2017)
  16. Regulation of plant architecture by a new histone acetyltransferase targeting gene bodies. Yang X, Yan J, Zhang Z, Lin T, Xin T, Wang B, Wang S, Zhao J, Zhang Z, Lucas WJ, Li G, Huang S. Nat Plants 6 809-822 (2020)
  17. Structural insight into the recognition of acetylated histone H3K56ac mediated by the bromodomain of CREB-binding protein. Xu L, Cheng A, Huang M, Zhang J, Jiang Y, Wang C, Li F, Bao H, Gao J, Wang N, Liu J, Wu J, Wong CCL, Ruan K. FEBS J 284 3422-3436 (2017)
  18. Chemical and biological tools for the preparation of modified histone proteins. Howard CJ, Yu RR, Gardner ML, Shimko JC, Ottesen JJ. Top Curr Chem 363 193-226 (2015)
  19. Histone H3 Lysine 56 Acetylation Enhances AP Endonuclease 1-Mediated Repair of AP Sites in Nucleosome Core Particles. Rodriguez Y, Horton JK, Wilson SH. Biochemistry 58 3646-3655 (2019)
  20. Molecular dynamics simulations reveal how H3K56 acetylation impacts nucleosome structure to promote DNA exposure for lesion sensing. Fu I, Geacintov NE, Broyde S. DNA Repair (Amst) 107 103201 (2021)
  21. The convergent chemical synthesis of histone H3 protein for site-specific acetylation at Lys56 and ubiquitination at Lys122. Qi YK, He QQ, Ai HS, Guo J, Li JB. Chem Commun (Camb) 53 4148-4151 (2017)
  22. News Chromatin: a ubiquitin crowbar opens chromatin. Peterson CL. Nat Chem Biol 7 68-69 (2011)
  23. Deacetylation of H4 lysine16 affects acetylation of lysine residues in histone H3 and H4 and promotes transcription of constitutive genes. Ray A, Khan P, Nag Chaudhuri R. Epigenetics 16 597-617 (2021)
  24. RNA Polymerase II Dependent Crosstalk between H4K16 Deacetylation and H3K56 Acetylation Promotes Transcription of Constitutively Expressed Genes. Khan P, Singha P, Nag Chaudhuri R. Mol Cell Biol 43 596-610 (2023)


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