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Molecular basis of histone tail recognition by human TIP5 PHD finger and bromodomain of the chromatin remodeling complex NoRC.

<div class='caption-title'>Domain Organization of Human Chromatin Associated Proteins Containing PHD Zinc Fingers Adjacent to BRDs</div>
<div class='caption-title'>Structures of TIP5 and BAZ2B PHD Zinc Fingers in Free State and in Complex with H3K4 Peptide</div>
<div class='caption-title'>Structures of TIP5 and BAZ2B BRDs in the Free State and in Complex with H3 and H4 Peptides</div>
Tallant C, Valentini E, Fedorov O, Overvoorde L, Ferguson FM, Filippakopoulos P, Svergun DI, Knapp S, Ciulli A
OpenAccess logo Structure 23 80-92 (2015)
Related entries: 4q6f, 4qbm, 4qc1, 4qc3, 4qf2, 4qf3

Cited: 44 times
EuropePMC logo PMID: 25533489

Abstract

Binding of the chromatin remodeling complex NoRC to RNA complementary to the rDNA promoter mediates transcriptional repression. TIP5, the largest subunit of NoRC, is involved in recruitment to rDNA by interactions with promoter-bound TTF-I, pRNA, and acetylation of H4K16. TIP5 domains that recognize posttranslational modifications on histones are essential for recruitment of NoRC to chromatin, but how these reader modules recognize site-specific histone tails has remained elusive. Here, we report crystal structures of PHD zinc finger and bromodomains from human TIP5 and BAZ2B in free form and bound to H3 and/or H4 histones. PHD finger functions as an independent structural module in recognizing unmodified H3 histone tails, and the bromodomain prefers H3 and H4 acetylation marks followed by a key basic residue, KacXXR. Further low-resolution analyses of PHD-bromodomain modules provide molecular insights into their trans histone tail recognition, required for nucleosome recruitment and transcriptional repression of the NoRC complex.

Articles - 4lz2 mentioned but not cited (1)

  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)


Reviews citing this publication (16)

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  2. DNA binding drives the association of BRG1/hBRM bromodomains with nucleosomes. Morrison EA, Sanchez JC, Ronan JL, Farrell DP, Varzavand K, Johnson JK, Gu BX, Crabtree GR, Musselman CA. Nat Commun 8 16080 (2017)
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  4. 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)
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  6. Selective Targeting of Bromodomains of the Bromodomain-PHD Fingers Family Impairs Osteoclast Differentiation. Meier JC, Tallant C, Fedorov O, Witwicka H, Hwang SY, van Stiphout RG, Lambert JP, Rogers C, Yapp C, Gerstenberger BS, Fedele V, Savitsky P, Heidenreich D, Daniels DL, Owen DR, Fish PV, Igoe NM, Bayle ED, Haendler B, Oppermann UCT, Buffa F, Brennan PE, Müller S, Gingras AC, Odgren PR, Birnbaum MJ, Knapp S. ACS Chem Biol 12 2619-2630 (2017)
  7. BAZ2A-mediated repression via H3K14ac-marked enhancers promotes prostate cancer stem cells. Peña-Hernández R, Aprigliano R, Carina Frommel S, Pietrzak K, Steiger S, Roganowicz M, Lerra L, Bizzarro J, Santoro R. EMBO Rep 22 e53014 (2021)
  8. Hepatitis Delta Virus histone mimicry drives the recruitment of chromatin remodelers for viral RNA replication. Abeywickrama-Samarakoon N, Cortay JC, Sureau C, Müller S, Alfaiate D, Guerrieri F, Chaikuad A, Schröder M, Merle P, Levrero M, Dény P. Nat Commun 11 419 (2020)
  9. Targeting Ligandable Pockets on Plant Homeodomain (PHD) Zinc Finger Domains by a Fragment-Based Approach. Amato A, Lucas X, Bortoluzzi A, Wright D, Ciulli A. ACS Chem Biol 13 915-921 (2018)
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  11. The Master Regulator Protein BAZ2B Can Reprogram Human Hematopoietic Lineage-Committed Progenitors into a Multipotent State. Arumugam K, Shin W, Schiavone V, Vlahos L, Tu X, Carnevali D, Kesner J, Paull EO, Romo N, Subramaniam P, Worley J, Tan X, Califano A, Cosma MP. Cell Rep 33 108474 (2020)
  12. The transcription factor 7 like 2‑binding protein TIP5 activates β‑catenin/transcription factor signaling in hepatocellular carcinoma. Li C, Wu W, Ding H, Li Q, Xie K. Mol Med Rep 17 7645-7651 (2018)
  13. A histone-mimicking interdomain linker in a multidomain protein modulates multivalent histone binding. Kostrhon S, Kontaxis G, Kaufmann T, Schirghuber E, Kubicek S, Konrat R, Slade D. J Biol Chem 292 17643-17657 (2017)
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  15. Inhibitor of Growth 4 (ING4) is a positive regulator of rRNA synthesis. Trinh DA, Shirakawa R, Kimura T, Sakata N, Goto K, Horiuchi H. Sci Rep 9 17235 (2019)
  16. LINC00885 promotes cervical cancer progression through sponging miR-3150b-3p and upregulating BAZ2A. Liu Y, Chen J, Zhou L, Yin C. Biol Direct 17 4 (2022)
  17. Structural Analysis of Small-Molecule Binding to the BAZ2A and BAZ2B Bromodomains. Dalle Vedove A, Spiliotopoulos D, D'Agostino VG, Marchand JR, Unzue A, Nevado C, Lolli G, Caflisch A. ChemMedChem 13 1479-1487 (2018)
  18. Coordination of Di-Acetylated Histone Ligands by the ATAD2 Bromodomain. Evans CM, Phillips M, Malone KL, Tonelli M, Cornilescu G, Cornilescu C, Holton SJ, Gorjánácz M, Wang L, Carlson S, Gay JC, Nix JC, Demeler B, Markley JL, Glass KC. Int J Mol Sci 22 9128 (2021)
  19. The BRPF1 bromodomain is a molecular reader of di-acetyllysine. Obi JO, Lubula MY, Cornilescu G, Henrickson A, McGuire K, Evans CM, Phillips M, Boyson SP, Demeler B, Markley JL, Glass KC. Curr Res Struct Biol 2 104-115 (2020)
  20. Focused conformational sampling in proteins. Bacci M, Langini C, Vymětal J, Caflisch A, Vitalis A. J Chem Phys 147 195102 (2017)
  21. Identification of a Bromodomain-like Region in 15-Lipoxygenase-1 Explains Its Nuclear Localization. Chen D, Xiao Z, Guo H, Gogishvili D, Setroikromo R, van der Wouden PE, Dekker FJ. Angew Chem Int Ed Engl 60 21875-21883 (2021)
  22. Structural basis of the TAM domain of BAZ2A in binding to DNA or RNA independent of methylation status. Chen S, Zhou M, Dong A, Loppnau P, Wang M, Min J, Liu K. J Biol Chem 297 101351 (2021)
  23. Binding specificity and function of the SWI/SNF subunit SMARCA4 bromodomain interaction with acetylated histone H3K14. Enríquez P, Krajewski K, Strahl BD, Rothbart SB, Dowen RH, Rose RB. J Biol Chem 297 101145 (2021)
  24. Elucidation of binding preferences of YEATS domains to site-specific acetylated nucleosome core particles. Kikuchi M, Morita S, Goto M, Wakamori M, Katsura K, Hanada K, Shirouzu M, Umehara T. J Biol Chem 298 102164 (2022)
  25. Biochemical and cellular insights into the Baz2B protein, a non-catalytic subunit of the chromatin remodeling complex. Breindl M, Spitzer D, Gerasimaitė R, Kairys V, Schubert T, Henfling R, Schwartz U, Lukinavičius G, Manelytė L. Nucleic Acids Res 52 337-354 (2024)
  26. Computed Protein-Protein Enthalpy Signatures as a Tool for Identifying Conformation Sampling Problems. Çınaroğlu SS, Biggin PC. J Chem Inf Model 63 6095-6108 (2023)
  27. Crystal structure of the BAZ2B TAM domain. Feng Y, Chen S, Zhou M, Zhang J, Min J, Liu K. Heliyon 8 e09873 (2022)


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