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Structural insights into acetylated-histone H4 recognition by the bromodomain-PHD finger module of human transcriptional coactivator CBP.

Plotnikov AN, Yang S, Zhou TJ, Rusinova E, Frasca A, Zhou MM
Structure 22 353-60 (2014)
Cited: 30 times
EuropePMC logo PMID: 24361270

Abstract

Bromodomain functions as the acetyl-lysine binding domains to regulate gene transcription in chromatin. Bromodomains are rapidly emerging as new epigenetic drug targets for human diseases. However, owing to their transient nature and modest affinity, histone-binding selectivity of bromodomains has remained mostly elusive. Here, we report high-resolution crystal structures of the bromodomain-PHD tandem module of human transcriptional coactivator CBP bound to lysine-acetylated histone H4 peptides. The structures reveal that the PHD finger serves a structural role in the tandem module and that the bromodomain prefers lysine-acetylated motifs comprising a hydrophobic or aromatic residue at -2 and a lysine or arginine at -3 or -4 position from the acetylated lysine. Our study further provides structural insights into distinct modes of singly and diacetylated histone H4 recognition by the bromodomains of CBP and BRD4 that function differently as a transcriptional coactivator and chromatin organizer, respectively, explaining their distinct roles in control of gene expression in chromatin.

Reviews - 4n4f mentioned but not cited (2)

  1. Partners in crime: The role of tandem modules in gene transcription. Sharma R, Zhou MM. Protein Sci 24 1347-1359 (2015)
  2. Chemistry towards Biology-Instruct: Snapshot. Hricovíni M, Owens RJ, Bak A, Kozik V, Musiał W, Pierattelli R, Májeková M, Rodríguez Y, Musioł R, Slodek A, Štarha P, Piętak K, Słota D, Florkiewicz W, Sobczak-Kupiec A, Jampílek J. Int J Mol Sci 23 14815 (2022)

Articles - 4n4f mentioned but not cited (4)

  1. Structural insights into acetylated-histone H4 recognition by the bromodomain-PHD finger module of human transcriptional coactivator CBP. Plotnikov AN, Yang S, Zhou TJ, Rusinova E, Frasca A, Zhou MM. Structure 22 353-360 (2014)
  2. Intrinsic protein disorder in histone lysine methylation. Lazar T, Schad E, Szabo B, Horvath T, Meszaros A, Tompa P, Tantos A. Biol Direct 11 30 (2016)
  3. Identification of dual histone modification-binding protein interaction by combining mass spectrometry and isothermal titration calorimetric analysis. Chen P, Guo Z, Chen C, Tian S, Bai X, Zhai G, Ma Z, Wu H, Zhang K. J Adv Res 22 35-46 (2020)
  4. A new structural arrangement in proteins involving lysine NH3+ group and carbonyl. Rogacheva ON, Izmailov SA, Slipchenko LV, Skrynnikov NR. Sci Rep 7 16402 (2017)


Reviews citing this publication (6)

  1. Role of Intrinsic Protein Disorder in the Function and Interactions of the Transcriptional Coactivators CREB-binding Protein (CBP) and p300. Dyson HJ, Wright PE. J Biol Chem 291 6714-6722 (2016)
  2. The many lives of KATs - detectors, integrators and modulators of the cellular environment. Sheikh BN, Akhtar A. Nat Rev Genet 20 7-23 (2019)
  3. Selectivity on-target of bromodomain chemical probes by structure-guided medicinal chemistry and chemical biology. Galdeano C, Ciulli A. Future Med Chem 8 1655-1680 (2016)
  4. The Role of CREBBP/EP300 and Its Therapeutic Implications in Hematological Malignancies. Zhu Y, Wang Z, Li Y, Peng H, Liu J, Zhang J, Xiao X. Cancers (Basel) 15 1219 (2023)
  5. Binding Mode of Acetylated Histones to Bromodomains: Variations on a Common Motif. Marchand JR, Caflisch A. ChemMedChem 10 1327-1333 (2015)
  6. Histone acetylation dynamics in repair of DNA double-strand breaks. Aricthota S, Rana PP, Haldar D. Front Genet 13 926577 (2022)

Articles citing this publication (18)

  1. Molecular basis of histone tail recognition by human TIP5 PHD finger and bromodomain of the chromatin remodeling complex NoRC. Tallant C, Valentini E, Fedorov O, Overvoorde L, Ferguson FM, Filippakopoulos P, Svergun DI, Knapp S, Ciulli A. Structure 23 80-92 (2015)
  2. The ZZ domain of p300 mediates specificity of the adjacent HAT domain for histone H3. Zhang Y, Xue Y, Shi J, Ahn J, Mi W, Ali M, Wang X, Klein BJ, Wen H, Li W, Shi X, Kutateladze TG. Nat Struct Mol Biol 25 841-849 (2018)
  3. Role of the CBP catalytic core in intramolecular SUMOylation and control of histone H3 acetylation. Park S, Stanfield RL, Martinez-Yamout MA, Dyson HJ, Wilson IA, Wright PE. Proc Natl Acad Sci U S A 114 E5335-E5342 (2017)
  4. Just a Flexible Linker? The Structural and Dynamic Properties of CBP-ID4 Revealed by NMR Spectroscopy. Piai A, Calçada EO, Tarenzi T, Grande AD, Varadi M, Tompa P, Felli IC, Pierattelli R. Biophys J 110 372-381 (2016)
  5. TRIM66 reads unmodified H3R2K4 and H3K56ac to respond to DNA damage in embryonic stem cells. Chen J, Wang Z, Guo X, Li F, Wei Q, Chen X, Gong D, Xu Y, Chen W, Liu Y, Kang J, Shi Y. Nat Commun 10 4273 (2019)
  6. Structural basis of molecular recognition of helical histone H3 tail by PHD finger domains. Bortoluzzi A, Amato A, Lucas X, Blank M, Ciulli A. Biochem J 474 1633-1651 (2017)
  7. Combinatorial regulation of a signal-dependent activator by phosphorylation and acetylation. Paz JC, Park S, Phillips N, Matsumura S, Tsai WW, Kasper L, Brindle PK, Zhang G, Zhou MM, Wright PE, Montminy M. Proc Natl Acad Sci U S A 111 17116-17121 (2014)
  8. Crosstalk between DNA methylation and histone acetylation triggers GDNF high transcription in glioblastoma cells. Zhang B, Gu X, Han X, Gao Q, Liu J, Guo T, Gao D. Clin Epigenetics 12 47 (2020)
  9. Synergistic Modification Induced Specific Recognition between Histone and TRIM24 via Fluctuation Correlation Network Analysis. Zhang J, Luo H, Liu H, Ye W, Luo R, Chen HF. Sci Rep 6 24587 (2016)
  10. Identification of Chemoresistance-Associated Key Genes and Pathways in High-Grade Serous Ovarian Cancer by Bioinformatics Analyses. Wu Y, Xia L, Guo Q, Zhu J, Deng Y, Wu X. Cancer Manag Res 12 5213-5223 (2020)
  11. Epigenetic mechanisms to propagate histone acetylation by p300/CBP. Kikuchi M, Morita S, Wakamori M, Sato S, Uchikubo-Kamo T, Suzuki T, Dohmae N, Shirouzu M, Umehara T. Nat Commun 14 4103 (2023)
  12. Epigenetic modifications promote the expression of the orphan nuclear receptor NR0B1 in human lung adenocarcinoma cells. Lu Y, Liu Y, Liao S, Tu W, Shen Y, Yan Y, Tao D, Lu Y, Ma Y, Yang Y, Zhang S. Oncotarget 7 43162-43176 (2016)
  13. Functional domains of SP110 that modulate its transcriptional regulatory function and cellular translocation. Leu JS, Chang SY, Mu CY, Chen ML, Yan BS. J Biomed Sci 25 34 (2018)
  14. Development of Dimethylisoxazole-Attached Imidazo[1,2-a]pyridines as Potent and Selective CBP/P300 Inhibitors. Muthengi A, Wimalasena VK, Yosief HO, Bikowitz MJ, Sigua LH, Wang T, Li D, Gaieb Z, Dhawan G, Liu S, Erickson J, Amaro RE, Schönbrunn E, Qi J, Zhang W. J Med Chem 64 5787-5801 (2021)
  15. Molecular and functional characterization of an evolutionarily conserved CREB-binding protein in the Lymnaea CNS. Hatakeyama D, Sunada H, Totani Y, Watanabe T, Felletár I, Fitchett A, Eravci M, Anagnostopoulou A, Miki R, Okada A, Abe N, Kuzuhara T, Kemenes I, Ito E, Kemenes G. FASEB J 36 e22593 (2022)
  16. 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)
  17. Discovery of novel CBP bromodomain inhibitors through TR-FRET-based high-throughput screening. Zhang FC, Sun ZY, Liao LP, Zuo Y, Zhang D, Wang J, Chen YT, Xiao SH, Jiang H, Lu T, Xu P, Yue LY, Du DH, Zhang H, Liu CP, Luo C. Acta Pharmacol Sin 41 286-292 (2020)
  18. Discovery of an EP300 Inhibitor using Structure-based Virtual Screening and Bioactivity Evaluation. Pan D, Huang Y, Jiang D, Zhang Y, Wu M, Han M, Jin X. Curr Pharm Des 30 1985-1994 (2024)


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