The double PHD finger domain of MOZ/MYST3 induces α-helical structure of the histone H3 tail to facilitate acetylation and methylation sampling and modification

Nucleic Acids Research

Volumn 42, Issue 2, 2014, Pages 822-835

  Dreveny, Ingrid ^a   Deeves, Sian E ^a   Fulton, Joel ^a   Yue, Baigong ^a   Messmer, Marie ^a   Bhattacharya, Amit ^a   Collins, Hilary M ^a   Heery, David M ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; DOUBLE PHD FINGER DOMAIN PROTEIN; HISTONE H3; LYSINE ACETYLTRANSFERASE; NUCLEIC ACID BINDING PROTEIN; PROTEIN MOZ; PROTEIN MYST3; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE;

ACETYLATION; AMINO ACID SEQUENCE; GLYCINE; HISTONE ACETYLTRANSFERASES; HISTONES; METHYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84893323422     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt931     Document Type: Article

References (49)

1. Strahl, B.D. and Allis, C.D. (2000) The language of covalent histone modifications. Nature, 403, 41-45.
2. Taverna, S.D., Li, H., Ruthenburg, A.J., Allis, C.D. and Patel, D.J. (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol., 14, 1025-1040.
3. Moriniere, J., Rousseaux, S., Steuerwald, U., Soler-Lopez, M., Curtet, S., Vitte, A.L., Govin, J., Gaucher, J., Sadoul, K., Hart, D.J. et al. (2009) Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature, 461, 664-668.
4. Nady, N., Lemak, A., Walker, J.R., Avvakumov, G.V., Kareta, M.S., Achour, M., Xue, S., Duan, S., Allali-Hassani, A., Zuo, X. et al. (2011) Recognition of multivalent histone states associated with heterochromatin by UHRF1 protein. J. Biol. Chem., 286, 24300-24311.
5. Ruthenburg, A.J., Li, H., Milne, T.A., Dewell, S., McGinty, R.K., Yuen, M., Ueberheide, B., Dou, Y., Muir, T.W., Patel, D.J. et al. (2011) Recognition of a mononucleosomal histone modification pattern by BPTF via Multivalent Interactions. Cell, 145, 692-706.
6. Filippakopoulos, P., Picaud, S., Mangos, M., Keates, T., Lambert, J.P., Barsyte-Lovejoy, D., Felletar, I., Volkmer, R., Muller, S., Pawson, T. et al. (2012) Histone recognition and large-scale structural analysis of the human bromodomain family. Cell, 149, 214-231.
7. Thomas, T., Corcoran, L.M., Gugasyan, R., Dixon, M.P., Brodnicki, T., Nutt, S.L., Metcalf, D. and Voss, A.K. (2006) Monocytic leukemia zinc finger protein is essential for the development of long-term reconstituting hematopoietic stem cells. Genes Dev., 20, 1175-1186.
8. Kitabayashi, I., Aikawa, Y., Nguyen, L.A., Yokoyama, A. and Ohki, M. (2001) Activation of AML1-mediated transcription by MOZ and inhibition by the MOZ-CBP fusion protein. EMBO J., 20, 7184-7196.
9. Pelletier, N., Champagne, N., Stifani, S. and Yang, X.J. (2002) MOZ and MORF histone acetyltransferases interact with the Runt-domain transcription factor Runx2. Oncogene, 21, 2729-2740.
10. Kindle, K.B., Troke, P.J., Collins, H.M., Matsuda, S., Bossi, D., Bellodi, C., Kalkhoven, E., Salomoni, P., Pelicci, P.G., Minucci, S. et al. (2005) MOZ-TIF2 inhibits transcription by nuclear receptors and p53 by impairment of CBP function. Mol. Cell. Biol., 25, 988-1002.
11. Deguchi, K., Ayton, P.M., Carapeti, M., Kutok, J.L., Snyder, C.S., Williams, I.R., Cross, N.C., Glass, C.K., Cleary, M.L. and Gilliland, D.G. (2003) MOZ-TIF2-induced acute myeloid leukemia requires the MOZ nucleosome binding motif and TIF2-mediated recruitment of CBP. Cancer Cell, 3, 259-271.
12. Huntly, B.J., Shigematsu, H., Deguchi, K., Lee, B.H., Mizuno, S., Duclos, N., Rowan, R., Amaral, S., Curley, D., Williams, I.R. et al. (2004) MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell, 6, 587-596.
13. Collins, H.M., Kindle, K.B., Matsuda, S., Ryan, C., Troke, P.J., Kalkhoven, E. and Heery, D.M. (2006) MOZ-TIF2 alters cofactor recruitment and histone modification at the RARbeta2 promoter: differential effects of MOZ fusion proteins on CBP-and MOZ-dependent activators. J. Biol. Chem., 281, 17124-17133.
14. Lange, M., Kaynak, B., Forster, U.B., Tonjes, M., Fischer, J.J., Grimm, C., Schlesinger, J., Just, S., Dunkel, I., Krueger, T. et al. (2008) Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev., 22, 2370-2384.
15. Zeng, L., Zhang, Q., Li, S., Plotnikov, A.N., Walsh, M.J. and Zhou, M.M. (2010) Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature, 466, 258-262.
16. Musselman, C.A. and Kutateladze, T.G. (2011) Handpicking epigenetic marks with PHD fingers. Nucleic Acids Res., 39, 9061-9071.
17. Ali, M., Yan, K., Lalonde, M.E., Degerny, C., Rothbart, S.B., Strahl, B.D., Cote, J., Yang, X.J. and Kutateladze, T.G. (2012) Tandem PHD fingers of MORF/MOZ acetyltransferases display selectivity for acetylated histone H3 and are required for the association with chromatin. J. Mol. Biol., 424, 328-338.
18. Qiu, Y., Liu, L., Zhao, C., Han, C., Li, F., Zhang, J., Wang, Y., Li, G., Mei, Y., Wu, M. et al. (2012) Combinatorial readout of unmodified H3R2 and acetylated H3K14 by the tandem PHD finger of MOZ reveals a regulatory mechanism for HOXA9 transcription. Genes Dev., 26, 1376-1391.
19. Sheppard, H.M., Harries, J.C., Hussain, S., Bevan, C. and Heery, D.M. (2001) Analysis of the steroid receptor coactivator 1 (SRC1)-CREB binding protein interaction interface and its importance for the function of SRC1. Mol. Cell. Biol., 21, 39-50.
20. Karmodiya, K., Krebs, A.R., Oulad-Abdelghani, M., Kimura, H. and Tora, L. (2012) H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics, 13, 424.
21. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
22. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
23. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
24. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. III, Snoeyink, J., Richardson, J.S. et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res., 35, W375-W383.
25. Doyon, Y., Cayrou, C., Ullah, M., Landry, A.J., Cote, V., Selleck, W., Lane, W.S., Tan, S., Yang, X.J. and Cote, J. (2006) ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell, 21, 51-64.
26. Voss, A.K., Collin, C., Dixon, M.P. and Thomas, T. (2009) Moz and retinoic acid coordinately regulate H3K9 acetylation, Hox gene expression, and segment identity. Dev Cell, 17, 674-686.
27. Kadoch, C., Hargreaves, D.C., Hodges, C., Elias, L., Ho, L., Ranish, J. and Crabtree, G.R. (2013) Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet., 45, 592-601.
28. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-W549.
29. Johnson, L.M., Fisher-Adams, G. and Grunstein, M. (1992) Identification of a non-basic domain in the histone H4 N-terminus required for repression of the yeast silent mating loci. EMBO J., 11, 2201-2209.
30. Hansen, J.C., Tse, C. and Wolffe, A.P. (1998) Structure and function of the core histone N-termini: more than meets the eye. Biochemistry, 37, 17637-17641.
31. Li, Y. and Li, H. (2012) Many keys to push: diversifying the 'readership' of plant homeodomain fingers. Acta Biochim. Biophys. Sin. (Shanghai), 44, 28-39.
32. Sanchez, R. and Zhou, M.M. (2011) The PHD finger: a versatile epigenome reader. Trends Biochem. Sci., 36, 364-372.
33. Fiedler, M., Sanchez-Barrena, M.J., Nekrasov, M., Mieszczanek, J., Rybin, V., Muller, J., Evans, P. and Bienz, M. (2008) Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex. Mol. Cell, 30, 507-518.
34. Flanagan, J.F., Mi, L.Z., Chruszcz, M., Cymborowski, M., Clines, K.L., Kim, Y., Minor, W., Rastinejad, F. and Khorasanizadeh, S. (2005) Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature, 438, 1181-1185.
35. Arita, K., Isogai, S., Oda, T., Unoki, M., Sugita, K., Sekiyama, N., Kuwata, K., Hamamoto, R., Tochio, H., Sato, M. et al. (2012) Recognition of modification status on a histone H3 tail by linked histone reader modules of the epigenetic regulator UHRF1. Proc. Natl Acad. Sci. USA, 109, 12950-12955.
36. Chakraborty, S., Sinha, K.K., Senyuk, V. and Nucifora, G. (2003) SUV39H1 interacts with AML1 and abrogates AML1 transactivity. AML1 is methylated in vivo. Oncogene, 22, 5229-5237.
37. Sturm, D., Witt, H., Hovestadt, V., Khuong-Quang, D.A., Jones, D.T., Konermann, C., Pfaff, E., Tonjes, M., Sill, M., Bender, S. et al. (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell, 22, 425-437.
38. Schwartzentruber, J., Korshunov, A., Liu, X.Y., Jones, D.T., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A.M., Quang, D.A., Tonjes, M. et al. (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature, 482, 226-231.
39. Karmodiya, K., Krebs, A.R., Oulad-Abdelghani, M., Kimura, H. and Tora, L. (2012) H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics, 13, 424.
40. Wysocka, J., Swigut, T., Xiao, H., Milne, T.A., Kwon, S.Y., Landry, J., Kauer, M., Tackett, A.J., Chait, B.T., Badenhorst, P. et al. (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature, 442, 86-90.
41. Dou, Y., Milne, T.A., Tackett, A.J., Smith, E.R., Fukuda, A., Wysocka, J., Allis, C.D., Chait, B.T., Hess, J.L. and Roeder, R.G. (2005) Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell, 121, 873-885.
42. Ullah, M., Pelletier, N., Xiao, L., Zhao, S.P., Wang, K., Degerny, C., Tahmasebi, S., Cayrou, C., Doyon, Y., Goh, S.L. et al. (2008) Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes. Mol. Cell. Biol., 28, 6828-6843.
43. Laue, K., Daujat, S., Crump, J.G., Plaster, N., Roehl, H.H., Kimmel, C.B., Schneider, R. and Hammerschmidt, M. (2008) The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development, 135, 1935-1946.
44. Zuber, J., Shi, J., Wang, E., Rappaport, A.R., Herrmann, H., Sison, E.A., Magoon, D., Qi, J., Blatt, K., Wunderlich, M. et al. (2011) RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature, 478, 524-528.
45. Qin, S., Jin, L., Zhang, J., Liu, L., Ji, P., Wu, M., Wu, J. and Shi, Y. (2011) Recognition of unmodified histone H3 by the first PHD finger of bromodomain-PHD finger protein 2 provides insights into the regulation of histone acetyltransferases monocytic leukemic zinc-finger protein (MOZ) and MOZ-related factor (MORF). J. Biol. Chem., 286, 36944-36955.
46. Lan, F., Collins, R.E., De Cegli, R., Alpatov, R., Horton, J.R., Shi, X., Gozani, O., Cheng, X. and Shi, Y. (2007) Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature, 448, 718-722.
47. Champagne, K.S., Saksouk, N., Pena, P.V., Johnson, K., Ullah, M., Yang, X.J., Cote, J. and Kutateladze, T.G. (2008) The crystal structure of the ING5 PHD finger in complex with an H3K4me3 histone peptide. Proteins, 72, 1371-1376.
48. Harris, W.J., Huang, X., Lynch, J.T., Spencer, G.J., Hitchin, J.R., Li, Y., Ciceri, F., Blaser, J.G., Greystoke, B.F., Jordan, A.M. et al. (2012) The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell, 21, 473-487.
49. Dawson, M.A., Prinjha, R.K., Dittmann, A., Giotopoulos, G., Bantscheff, M., Chan, W.I., Robson, S.C., Chung, C.W., Hopf, C., Savitski, M.M. et al. (2011) Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature, 478, 529-533.