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Structural Insights into Histone Crotonyl-Lysine Recognition by the AF9 YEATS Domain.

Zhang Q, Zeng L, Zhao C, Ju Y, Konuma T, Zhou MM
Structure 24 1606-12 (2016)
Cited: 41 times
EuropePMC logo PMID: 27545619

Abstract

Histone lysine acylations play an important role in the regulation of gene transcription in chromatin. Unlike histone acetyl-lysine, molecular recognition of a recently identified crotonyl-lysine mark is much less understood. Here, we report that the YEATS domain of AF9 preferentially binds crotonyl-lysine over acetyl-lysine in histone H3. Nuclear magnetic resonance structural analysis reveals that crotonyl-lysine of histone H3 lysine 18 is engulfed deep in an aromatic cage of the YEATS domain where the carbonyl oxygen of crotonyl-lysine forms a hydrogen bond with the backbone amide of protein residue Tyr78. The crotonyl-lysine, through its unique electron-rich double-bond side chain, engages π-π aromatic stacking and extended hydrophobic/aromatic interactions with the YEATS domain compared with acetyl-lysine. Our mutational analysis confirmed key protein residues Phe59 and Tyr78 for crotonyl-lysine recognition. Importantly, our findings present a new structural mechanism of protein-protein interactions mediated by histone lysine crotonylation, and show how the cells interpret acyl-lysine marks in different biological contexts.

Articles - 2ndg mentioned but not cited (2)

  1. Structural Insights into Histone Crotonyl-Lysine Recognition by the AF9 YEATS Domain. Zhang Q, Zeng L, Zhao C, Ju Y, Konuma T, Zhou MM. Structure 24 1606-1612 (2016)
  2. Molecular Recognition of Methacryllysine and Crotonyllysine by the AF9 YEATS Domain. Bilgin N, Moesgaard L, Rahman MM, Türkmen VA, Kongsted J, Mecinović J. Int J Mol Sci 24 7002 (2023)


Reviews citing this publication (13)

  1. Metabolic regulation of gene expression through histone acylations. Sabari BR, Zhang D, Allis CD, Zhao Y. Nat Rev Mol Cell Biol 18 90-101 (2017)
  2. The language of chromatin modification in human cancers. Zhao S, Allis CD, Wang GG. Nat Rev Cancer 21 413-430 (2021)
  3. YEATS Domain-A Histone Acylation Reader in Health and Disease. Zhao D, Li Y, Xiong X, Chen Z, Li H. J Mol Biol 429 1994-2002 (2017)
  4. Functions and mechanisms of lysine crotonylation. Wan J, Liu H, Chu J, Zhang H. J Cell Mol Med 23 7163-7169 (2019)
  5. Metabolism and the Epigenome: A Dynamic Relationship. Haws SA, Leech CM, Denu JM. Trends Biochem Sci 45 731-747 (2020)
  6. Chromatin dynamics and histone modifications in intestinal microbiota-host crosstalk. Fellows R, Varga-Weisz P. Mol Metab 38 100925 (2020)
  7. Protein lysine crotonylation: past, present, perspective. Jiang G, Li C, Lu M, Lu K, Li H. Cell Death Dis 12 703 (2021)
  8. The Regulation and Function of Histone Crotonylation. Ntorla A, Burgoyne JR. Front Cell Dev Biol 9 624914 (2021)
  9. Emerging roles of non-histone protein crotonylation in biomedicine. Hou JY, Zhou L, Li JL, Wang DP, Cao JM. Cell Biosci 11 101 (2021)
  10. Targeting epigenetic protein-protein interactions with small-molecule inhibitors. Linhares BM, Grembecka J, Cierpicki T. Future Med Chem 12 1305-1326 (2020)
  11. Oncometabolites drive tumorigenesis by enhancing protein acylation: from chromosomal remodelling to nonhistone modification. Fu Y, Yu J, Li F, Ge S. J Exp Clin Cancer Res 41 144 (2022)
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Articles citing this publication (26)

  1. Characterization of histone acylations links chromatin modifications with metabolism. Simithy J, Sidoli S, Yuan ZF, Coradin M, Bhanu NV, Marchione DM, Klein BJ, Bazilevsky GA, McCullough CE, Magin RS, Kutateladze TG, Snyder NW, Marmorstein R, Garcia BA. Nat Commun 8 1141 (2017)
  2. Structure-guided development of YEATS domain inhibitors by targeting π-π-π stacking. Li X, Li XM, Jiang Y, Liu Z, Cui Y, Fung KY, van der Beelen SHE, Tian G, Wan L, Shi X, Allis CD, Li H, Li Y, Li XD. Nat Chem Biol 14 1140-1149 (2018)
  3. First comprehensive proteome analysis of lysine crotonylation in seedling leaves of Nicotiana tabacum. Sun H, Liu X, Li F, Li W, Zhang J, Xiao Z, Shen L, Li Y, Wang F, Yang J. Sci Rep 7 3013 (2017)
  4. Identification of the YEATS domain of GAS41 as a pH-dependent reader of histone succinylation. Wang Y, Jin J, Chung MWH, Feng L, Sun H, Hao Q. Proc Natl Acad Sci U S A 115 2365-2370 (2018)
  5. Gcn5 and Esa1 function as histone crotonyltransferases to regulate crotonylation-dependent transcription. Kollenstart L, de Groot AJL, Janssen GMC, Cheng X, Vreeken K, Martino F, Côté J, van Veelen PA, van Attikum H. J Biol Chem 294 20122-20134 (2019)
  6. Quantitative Crotonylome Analysis Expands the Roles of p300 in the Regulation of Lysine Crotonylation Pathway. Huang H, Wang DL, Zhao Y. Proteomics 18 e1700230 (2018)
  7. Recognition of Histone H3K14 Acylation by MORF. Klein BJ, Simithy J, Wang X, Ahn J, Andrews FH, Zhang Y, Côté J, Shi X, Garcia BA, Kutateladze TG. Structure 25 650-654.e2 (2017)
  8. Structural insights into the π-π-π stacking mechanism and DNA-binding activity of the YEATS domain. Klein BJ, Vann KR, Andrews FH, Wang WW, Zhang J, Zhang Y, Beloglazkina AA, Mi W, Li Y, Li H, Shi X, Kutateladze AG, Strahl BD, Liu WR, Kutateladze TG. Nat Commun 9 4574 (2018)
  9. Yaf9 subunit of the NuA4 and SWR1 complexes targets histone H3K27ac through its YEATS domain. Klein BJ, Ahmad S, Vann KR, Andrews FH, Mayo ZA, Bourriquen G, Bridgers JB, Zhang J, Strahl BD, Côté J, Kutateladze TG. Nucleic Acids Res 46 421-430 (2018)
  10. YEATS domain: Linking histone crotonylation to gene regulation. Li Y, Zhao D, Chen Z, Li H. Transcription 8 9-14 (2017)
  11. GAS41 Recognizes Diacetylated Histone H3 through a Bivalent Binding Mode. Cho HJ, Li H, Linhares BM, Kim E, Ndoj J, Miao H, Grembecka J, Cierpicki T. ACS Chem Biol 13 2739-2746 (2018)
  12. Histone benzoylation serves as an epigenetic mark for DPF and YEATS family proteins. Ren X, Zhou Y, Xue Z, Hao N, Li Y, Guo X, Wang D, Shi X, Li H. Nucleic Acids Res 49 114-126 (2021)
  13. The Response of Rhodotorula mucilaginosa to Patulin Based on Lysine Crotonylation. Yang Q, Li Y, Apaliya MT, Zheng X, Serwah BNA, Zhang X, Zhang H. Front Microbiol 9 2025 (2018)
  14. Discovery of Selective Small-Molecule Inhibitors for the ENL YEATS Domain. Ma XR, Xu L, Xu S, Klein BJ, Wang H, Das S, Li K, Yang KS, Sohail S, Chapman A, Kutateladze TG, Shi X, Liu WR, Wen H. J Med Chem 64 10997-11013 (2021)
  15. Structural Insights into Interaction Mechanisms of Alternative Piperazine-urea YEATS Domain Binders in MLLT1. Ni X, Heidenreich D, Christott T, Bennett J, Moustakim M, Brennan PE, Fedorov O, Knapp S, Chaikuad A. ACS Med Chem Lett 10 1661-1666 (2019)
  16. More Than π-π-π Stacking: Contribution of Amide-π and CH-π Interactions to Crotonyllysine Binding by the AF9 YEATS Domain. Krone MW, Travis CR, Lee GY, Eckvahl HJ, Houk KN, Waters ML. J Am Chem Soc 142 17048-17056 (2020)
  17. Establishment and function of chromatin modification at enhancers. Tafessu A, Banaszynski LA. Open Biol 10 200255 (2020)
  18. Histone lysine methacrylation is a dynamic post-translational modification regulated by HAT1 and SIRT2. Delaney K, Tan M, Zhu Z, Gao J, Dai L, Kim S, Ding J, He M, Halabelian L, Yang L, Nagarajan P, Parthun MR, Lee S, Khochbin S, Zheng YG, Zhao Y. Cell Discov 7 122 (2021)
  19. re-TAMD: exploring interactions between H3 peptide and YEATS domain using enhanced sampling. Lamothe G, Malliavin TE. BMC Struct Biol 18 4 (2018)
  20. Evaluation of acyllysine isostere interactions with the aromatic pocket of the AF9 YEATS domain. Travis CR, Francis DY, Williams DC, Waters ML. Protein Sci 32 e4533 (2023)
  21. Recognition of acetylated histone by Yaf9 regulates metabolic cycling of transcription initiation and chromatin regulatory factors. Zhang J, Gundu A, Strahl BD. Genes Dev 35 1678-1692 (2021)
  22. 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)
  23. Fragment-Based Discovery of AF9 YEATS Domain Inhibitors. Liu Y, Jin R, Lu H, Bian K, Wang R, Wang L, Gao R, Zhang J, Wu J, Yao X, Liu X, Liu D, Wang X, Zhang Z, Ruan K. Int J Mol Sci 23 3893 (2022)
  24. Lysine crotonylation is widespread on proteins of diverse functions and localizations in Toxoplasma gondii. Li FC, Nie LB, Elsheikha HM, Yin FY, Zhu XQ. Parasitol Res 120 1617-1626 (2021)
  25. GAS41 promotes H2A.Z deposition through recognition of the N terminus of histone H3 by the YEATS domain. Kikuchi M, Takase S, Konuma T, Noritsugu K, Sekine S, Ikegami T, Ito A, Umehara T. Proc Natl Acad Sci U S A 120 e2304103120 (2023)
  26. Histone Readers and Their Roles in Cancer. Wen H, Shi X. Cancer Treat Res 190 245-272 (2023)


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