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Molecular basis of histone H3K4me3 recognition by ING4.

Palacios A, Muñoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martín-García JM, Luque I, Montoya G, Blanco FJ
J Biol Chem 283 15956-64 (2008)
Cited: 54 times
EuropePMC logo PMID: 18381289

Abstract

The inhibitors of growth (ING) family of tumor suppressors consists of five homologous proteins involved in chromatin remodeling. They form part of different acetylation and deacetylation complexes and are thought to direct them to specific regions of the chromatin, through the recognition of H3K4me3 (trimethylated K4 in the histone 3 tail) by their conserved plant homeodomain (PHD). We have determined the crystal structure of ING4-PHD bound to H3K4me3, which reveals a tight complex stabilized by numerous interactions. NMR shows that there is a reduction in the backbone mobility on the regions of the PHD that participate in the peptide binding, and binding affinities differ depending on histone tail lengths Thermodynamic analysis reveals that the discrimination in favor of methylated lysine is entropy-driven, contrary to what has been described for chromodomains. The molecular basis of H3K4me3 recognition by ING4 differs from that of ING2, which is consistent with their different affinities for methylated histone tails. These differences suggest a distinct role in transcriptional regulation for these two ING family members because of the antagonistic effect of the complexes that they recruit onto chromatin. Our results illustrate the versatility of PHD fingers as readers of the histone code.

Reviews - 2vnf mentioned but not cited (2)

  1. PHD fingers: epigenetic effectors and potential drug targets. Musselman CA, Kutateladze TG. Mol Interv 9 314-323 (2009)
  2. Structural insight into histone recognition by the ING PHD fingers. Champagne KS, Kutateladze TG. Curr Drug Targets 10 432-441 (2009)

Articles - 2vnf mentioned but not cited (4)

  1. Molecular basis of histone H3K4me3 recognition by ING4. Palacios A, Muñoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martín-García JM, Luque I, Montoya G, Blanco FJ. J Biol Chem 283 15956-15964 (2008)
  2. Identification of family-determining residues in PHD fingers. Slama P, Geman D. Nucleic Acids Res 39 1666-1679 (2011)
  3. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
  4. An in silico study of how histone tail conformation affects the binding affinity of ING family proteins. Gül N, Yıldız A. PeerJ 10 e14029 (2022)


Reviews citing this publication (17)

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  2. Handpicking epigenetic marks with PHD fingers. Musselman CA, Kutateladze TG. Nucleic Acids Res 39 9061-9071 (2011)
  3. Structure and function of histone methylation binding proteins. Adams-Cioaba MA, Min J. Biochem Cell Biol 87 93-105 (2009)
  4. Keeping it in the family: diverse histone recognition by conserved structural folds. Yap KL, Zhou MM. Crit Rev Biochem Mol Biol 45 488-505 (2010)
  5. Understanding the interplay between CpG island-associated gene promoters and H3K4 methylation. Hughes AL, Kelley JR, Klose RJ. Biochim Biophys Acta Gene Regul Mech 1863 194567 (2020)
  6. Dynamic interplay between histone H3 modifications and protein interpreters: emerging evidence for a "histone language". Oliver SS, Denu JM. Chembiochem 12 299-307 (2011)
  7. Keep-ING balance: tumor suppression by epigenetic regulation. Tallen G, Riabowol K. FEBS Lett 588 2728-2742 (2014)
  8. Many keys to push: diversifying the 'readership' of plant homeodomain fingers. Li Y, Li H. Acta Biochim Biophys Sin (Shanghai) 44 28-39 (2012)
  9. Cross-talk among epigenetic modifications: lessons from histone arginine methylation. Molina-Serrano D, Schiza V, Kirmizis A. Biochem Soc Trans 41 751-759 (2013)
  10. Reviewing the current classification of inhibitor of growth family proteins. Unoki M, Kumamoto K, Takenoshita S, Harris CC. Cancer Sci 100 1173-1179 (2009)
  11. INGs are potential drug targets for cancer. Zhang R, Jin J, Shi J, Hou Y. J Cancer Res Clin Oncol 143 189-197 (2017)
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  13. Inhibitor of growth-4 mediates chromatin modification and has a suppressive effect on tumorigenesis and innate immunity. Mathema VB, Koh YS. Tumour Biol 33 1-7 (2012)
  14. Systematic analysis of histone modification readout. Nikolov M, Fischle W. Mol Biosyst 9 182-194 (2013)
  15. Inhibitor of growth-4 is a potential target for cancer therapy. Yuan S, Jin J, Shi J, Hou Y. Tumour Biol 37 4275-4279 (2016)
  16. The essential role of tumor suppressor gene ING4 in various human cancers and non-neoplastic disorders. Du Y, Cheng Y, Su G. Biosci Rep 39 BSR20180773 (2019)
  17. BRPF1-KAT6A/KAT6B Complex: Molecular Structure, Biological Function and Human Disease. Zu G, Liu Y, Cao J, Zhao B, Zhang H, You L. Cancers (Basel) 14 4068 (2022)

Articles citing this publication (31)

  1. Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Southall SM, Wong PS, Odho Z, Roe SM, Wilson JR. Mol Cell 33 181-191 (2009)
  2. ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, Simon MD, Kutateladze TG, Gozani O. Mol Cell 33 248-256 (2009)
  3. Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Lee WY, Lee D, Chung WI, Kwon CS. Plant J 58 511-524 (2009)
  4. Citrullination of inhibitor of growth 4 (ING4) by peptidylarginine deminase 4 (PAD4) disrupts the interaction between ING4 and p53. Guo Q, Fast W. J Biol Chem 286 17069-17078 (2011)
  5. The solution structure of the first PHD finger of autoimmune regulator in complex with non-modified histone H3 tail reveals the antagonistic role of H3R2 methylation. Chignola F, Gaetani M, Rebane A, Org T, Mollica L, Zucchelli C, Spitaleri A, Mannella V, Peterson P, Musco G. Nucleic Acids Res 37 2951-2961 (2009)
  6. A phospho/methyl switch at histone H3 regulates TFIID association with mitotic chromosomes. Varier RA, Outchkourov NS, de Graaf P, van Schaik FM, Ensing HJ, Wang F, Higgins JM, Kops GJ, Timmers HT. EMBO J 29 3967-3978 (2010)
  7. Exploring PHD fingers and H3K4me0 interactions with molecular dynamics simulations and binding free energy calculations: AIRE-PHD1, a comparative study. Spiliotopoulos D, Spitaleri A, Musco G. PLoS One 7 e46902 (2012)
  8. Structure of p15(PAF)-PCNA complex and implications for clamp sliding during DNA replication and repair. De Biasio A, de Opakua AI, Mortuza GB, Molina R, Cordeiro TN, Castillo F, Villate M, Merino N, Delgado S, Gil-Cartón D, Luque I, Diercks T, Bernadó P, Montoya G, Blanco FJ. Nat Commun 6 6439 (2015)
  9. Inhibitor of growth-4 promotes IkappaB promoter activation to suppress NF-kappaB signaling and innate immunity. Coles AH, Gannon H, Cerny A, Kurt-Jones E, Jones SN. Proc Natl Acad Sci U S A 107 11423-11428 (2010)
  10. Druggability of methyl-lysine binding sites. Santiago C, Nguyen K, Schapira M. J Comput Aided Mol Des 25 1171-1178 (2011)
  11. The PHD finger of human UHRF1 reveals a new subgroup of unmethylated histone H3 tail readers. Lallous N, Legrand P, McEwen AG, Ramón-Maiques S, Samama JP, Birck C. PLoS One 6 e27599 (2011)
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  13. Negative regulation of NF-κB by the ING4 tumor suppressor in breast cancer. Byron SA, Min E, Thal TS, Hostetter G, Watanabe AT, Azorsa DO, Little TH, Tapia C, Kim S. PLoS One 7 e46823 (2012)
  14. A dominant mutant allele of the ING4 tumor suppressor found in human cancer cells exacerbates MYC-initiated mouse mammary tumorigenesis. Kim S, Welm AL, Bishop JM. Cancer Res 70 5155-5162 (2010)
  15. The dimeric structure and the bivalent recognition of H3K4me3 by the tumor suppressor ING4 suggests a mechanism for enhanced targeting of the HBO1 complex to chromatin. Palacios A, Moreno A, Oliveira BL, Rivera T, Prieto J, García P, Fernández-Fernández MR, Bernadó P, Palmero I, Blanco FJ. J Mol Biol 396 1117-1127 (2010)
  16. Transient induction of ING4 by Myc drives prostate epithelial cell differentiation and its disruption drives prostate tumorigenesis. Berger PL, Frank SB, Schulz VV, Nollet EA, Edick MJ, Holly B, Chang TT, Hostetter G, Kim S, Miranti CK. Cancer Res 74 3357-3368 (2014)
  17. Deletion of the inhibitor of growth 4 (ING4) tumor suppressor gene is prevalent in human epidermal growth factor 2 (HER2)-positive breast cancer. Tapia C, Zlobec I, Schneider S, Kilic E, Güth U, Bubendorf L, Kim S. Hum Pathol 42 983-990 (2011)
  18. Crystal structure of inhibitor of growth 4 (ING4) dimerization domain reveals functional organization of ING family of chromatin-binding proteins. Culurgioni S, Muñoz IG, Moreno A, Palacios A, Villate M, Palmero I, Montoya G, Blanco FJ. J Biol Chem 287 10876-10884 (2012)
  19. Proliferating cell nuclear antigen (PCNA) interactions in solution studied by NMR. De Biasio A, Campos-Olivas R, Sánchez R, López-Alonso JP, Pantoja-Uceda D, Merino N, Villate M, Martin-Garcia JM, Castillo F, Luque I, Blanco FJ. PLoS One 7 e48390 (2012)
  20. The H3K4me3/2 histone demethylase RBR-2 controls axon guidance by repressing the actin-remodeling gene wsp-1. Mariani L, Lussi YC, Vandamme J, Riveiro A, Salcini AE. Development 143 851-863 (2016)
  21. ING Genes Work as Tumor Suppressor Genes in the Carcinogenesis of Head and Neck Squamous Cell Carcinoma. Li X, Kikuchi K, Takano Y. J Oncol 2011 963614 (2011)
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  23. Functional impact of cancer-associated mutations in the tumor suppressor protein ING4. Moreno A, Palacios A, Orgaz JL, Jimenez B, Blanco FJ, Palmero I. Carcinogenesis 31 1932-1938 (2010)
  24. Cation-π interactions of methylated ammonium ions: a quantum mechanical study. Rapp C, Goldberger E, Tishbi N, Kirshenbaum R. Proteins 82 1494-1502 (2014)
  25. Rapamycin-upregulated miR-29b promotes mTORC1-hyperactive cell growth in TSC2-deficient cells by downregulating tumor suppressor retinoic acid receptor β (RARβ). Liu HJ, Lam HC, Baglini CV, Nijmeh J, Cottrill AA, Chan SY, Henske EP. Oncogene 38 7367-7383 (2019)
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  28. High level of H3K4 tri-methylation modification predicts poor prognosis in esophageal cancer. Ye XD, Qiu BQ, Xiong D, Pei X, Jie N, Xu H, Zhu SQ, Long X, Xu Z, Wu HB, Xu JJ, Huang YS, Wu YB. J Cancer 11 3256-3263 (2020)
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