Combinatorial readout of unmodified H3R2 and acetylated H3K14 by the tandem PHD finger of MOZ reveals a regulatory mechanism for HOXA9 transcription

Genes and Development

Volumn 26, Issue 12, 2012, Pages 1376-1391

  Qiu, Yu ^a,b   Liu, Lei ^a,b   Zhao, Chen ^a,b   Han, Chuanchun ^a,b   Li, Fudong ^a,b   Zhang, Jiahai ^a,b   Wang, Yan ^c   Li, Guohong ^c   Mei, Yide ^a,b   Wu, Mian ^a,b   Wu, Jihui ^a,b   Shi, Yunyu ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

Author keywords

H3K14ac; H3r2me0; Histone acetyltransferase; HOXA9; MOZ; PHD finger

Indexed keywords

H3K14AC PROTEIN; H3R2 PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE MOZ; MESSENGER RNA; NUCLEAR PROTEIN; PHD12 PROTEIN; TRANSCRIPTION FACTOR HOXA9; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CRYSTAL STRUCTURE; HISTONE ACETYLATION; HUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION;

ACETYLATION; AMINO ACID SEQUENCE; ARGININE; GENE EXPRESSION REGULATION; HISTONE ACETYLTRANSFERASES; HISTONES; HOMEODOMAIN PROTEINS; HUMANS; LYSINE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TRANSCRIPTION, GENETIC;

EID: 84862612318     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.188359.112     Document Type: Article

References (61)

1. Berger SL. 2007. The complex language of chromatin regulation during transcription. Nature 447: 407-412.
2. Borrow J, Stanton VP Jr, Andresen JM, Becher R, Behm FG, Chaganti RS, Civin CI, Disteche C, Dube I, Frischauf AM, et al. 1996. The translocation t(8;16)(p11;p13) of acute mye-loid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nat Genet 14: 33-41.
3. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, et al. 1998. Crystallography and NMR system: A new software suite for macromolecular structure determination. Acta Crys-tallogr 54: 905-921.
4. Carapeti M, Aguiar RC, Goldman JM, Cross NC. 1998. A novel fusion between MOZ and the nuclear receptor coactivator TIF2 in acute myeloid leukemia. Blood 91: 3127-3133.
5. Chaffanet M, Gressin L, Preudhomme C, Soenen-Cornu V, Birnbaum D, Pebusque MJ. 2000. MOZ is fused to p300 in an acute monocytic leukemia with t(8;22). Genes Chromosomes Cancer 28: 138-144.
6. Champagne KS, Saksouk N, Pena PV, Johnson K, Ullah M, Yang XJ, Cote J, Kutateladze TG. 2008. The crystal structure of the ING5 PHD finger in complex with an H3K4me3 histone peptide. Proteins 72: 1371-1376.
7. Clore GM, Gronenborn AM. 1994. Multidimensional hetero-nuclear nuclear magnetic resonance of proteins. Methods Enzymol 239: 349-363.
8. Collaborative Computational Project, Number 4. 1994. The Ccp4 suite: Programs for protein crystallography. Acta Crys-tallogr D Biol Crystallogr 50: 760-763.
9. Crump JG, Swartz ME, Eberhart JK, Kimmel CB. 2006. Moz-dependent Hox expression controls segment-specific fate maps of skeletal precursors in the face. Development 133: 2661-2669.
10. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. 1995. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biol NMR 6: 277-293.
11. Dhalluin C, Carlson JE, Zeng L, He C, Aggarwal AK, Zhou MM. 1999. Structure and ligand of a histone acetyltransferase bromodomain. Nature 399: 491-496.
12. Downs JA, Nussenzweig MC, Nussenzweig A. 2007. Chromatin dynamics and the preservation of genetic information. Nature 447: 951-958.
13. Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, Lane WS, Tan S, Yang XJ, Cote J. 2006. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 21: 51-64.
14. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
15. Groth A, Rocha W, Verreault A, Almouzni G. 2007. Chromatin challenges during DNA replication and repair. Cell 128: 721-733.
16. Guccione E, Bassi C, Casadio F, Martinato F, Cesaroni M, Schuchlautz H, Luscher B, Amati B. 2007. Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449: 933-937.
17. Holbert MA, Sikorski T, Carten J, Snowflack D, Hodawadekar S, Marmorstein R. 2007. The human monocytic leukemia zinc finger histone acetyltransferase domain contains DNA-bind-ing activity implicated in chromatin targeting. J Biol Chem 282: 36603-36613.
18. Holm L, Rosenstrom P. 2010. Dali server: Conservation mapping in 3D. Nucleic Acids Res 38: W545-W549. doi: 10.1093/ nar/gkq366.
19. Horton JR, Upadhyay AK, Qi HH, Zhang X, Shi Y, Cheng X. 2010. Enzymatic and structural insights for substrate specificity of a family of jumonji histone lysine demethylases. Nat Struct Mol Biol 17: 38-43.
20. Iberg AN, Espejo A, Cheng D, Kim D, Michaud-Levesque J, Richard S, Bedford MT. 2008. Arginine methylation of the histone H3 tail impedes effector binding. J Biol Chem 283: 3006-3010.
21. Katsumoto T, Aikawa Y, Iwama A, Ueda S, Ichikawa H, Ochiya T, Kitabayashi I. 2006. MOZ is essential for maintenance of hematopoietic stem cells. Genes Dev 20: 1321-1330.
22. Kirmizis A, Santos-Rosa H, Penkett CJ, Singer MA, Vermeulen M, Mann M, Bahler J, Green RD, Kouzarides T. 2007. Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 449: 928-932.
23. Kitabayashi I, Aikawa Y, Nguyen LA, Yokoyama A, Ohki M. 2001. Activation of AML1-mediated transcription by MOZ and inhibition by the MOZ-CBP fusion protein. EMBO J 20: 7184-7196.
24. Kornberg RD, Lorch Y. 1999. Twenty-five years of the nucleo-some, fundamental particle of the eukaryote chromosome. Cell 98: 285-294.
25. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
26. Lange M, Kaynak B, Forster UB, Tonjes M, Fischer JJ, 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.
27. Langer G, Cohen SX, Lamzin VS, Perrakis A. 2008. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3: 1171-1179.
28. Laue K, Daujat S, Crump JG, Plaster N, Roehl HH, Tubingen Screen C, Kimmel CB, Schneider R, Hammerschmidt M. 2008. The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development 135: 1935-1946.
29. Liu CL, Kaplan T, Kim M, Buratowski S, Schreiber SL, Friedman N, Rando OJ. 2005. Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol 3: e328. doi: 10.1371/ journal.pbio.0030328.
30. Luger K, Rechsteiner TJ, Richmond TJ. 1999. Preparation of nu-cleosome core particle from recombinant histones. Methods Enzymol 304: 3-19.
31. Mansfield RE, Musselman CA, Kwan AH, Oliver SS, Garske AL, Davrazou F, Denu JM, Kutateladze TG, Mackay JP. 2011. Plant homeodomain (PHD) fingers of CHD4 are histone H3-binding modules with preference for unmodified H3K4 and methylated H3K9. J Biol Chem 286: 11779-11791.
32. Martin DG, Grimes DE, Baetz K, Howe L. 2006. Methylation of histone H3 mediates the association of the NuA3 histone acetyltransferase with chromatin. Mol Cell Biol 26: 3018-3028.
33. Miller CT, Maves L, Kimmel CB. 2004. moz regulates Hox expression and pharyngeal segmental identity in zebrafish. Development 131: 2443-2461.
34. Mishima Y, Miyagi S, Saraya A, Negishi M, Endoh M, Endo TA, Toyoda T, Shinga J, Katsumoto T, Chiba T, et al. 2011. The Hbo1-Brd1/Brpf2 complex is responsible for global acetyla-tion of H3K14 and required for fetal liver erythropoiesis. Blood 118: 2443-2453.
35. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
36. Narlikar GJ, Fan HY, Kingston RE. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475-487.
37. Owen DJ, Ornaghi P, Yang JC, Lowe N, Evans PR, Ballario P, Neuhaus D, Filetici P, Travers AA. 2000. The structural basis for the recognition of acetylated histone H4 by the bromo-domain of histone acetyltransferase gcn5p. EMBO J 19: 6141-6149.
38. Paggetti J, Largeot A, Aucagne R, Jacquel A, Lagrange B, Yang XJ, Solary E, Bastie JN, Delva L. 2010. Crosstalk between leukemia-associated proteins MOZ and MLL regulates HOX gene expression in human cord blood CD34+ cells. Oncogene 29: 5019-5031.
39. Palacios A, Garcia P, Padro D, Lopez-Hernandez E, Martin I, Blanco FJ. 2006. Solution structure and NMR characterization of the binding to methylated histone tails of the plant homeodomain finger of the tumour suppressor ING4. FEBS Lett 580: 6903-6908.
40. Pelletier N, Champagne N, Stifani S, Yang XJ. 2002. MOZ and MORF histone acetyltransferases interact with the Runt-domain transcription factor Runx2. Oncogene 21: 2729-2740.
41. Pena PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, Zhao R, Kutateladze TG. 2006. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442: 100-103.
42. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, et al. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527.
43. Qin S, Jin L, Zhang J, Liu L, Ji P, Wu M, Wu J, 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.
44. Rosaleny LE, Ruiz-Garcia AB, Garcia-Martinez J, Perez-Ortin JE, Tordera V. 2007. The Sas3p and Gcn5p histone acetyltrans-ferases are recruited to similar genes. Genome Biol 8: R119. doi: 10.1186/gb-2007-8-6-r119.
45. Ruthenburg AJ, Allis CD, Wysocka J. 2007a. Methylation of lysine 4 on histone H3: Intricacy of writing and reading a single epigenetic mark. Mol Cell 25: 15-30.
46. Ruthenburg AJ, Li H, Patel DJ, Allis CD. 2007b. Multivalent engagement of chromatin modifications by linked binding modules. Natl Rev 8: 983-994.
47. Saksouk N, Avvakumov N, Champagne KS, Hung T, Doyon Y, Cayrou C, Paquet E, Ullah M, Landry AJ, Cote V, et al. 2009. HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol Cell 33: 257-265.
48. Sheldrick GM. 2008. A short history of SHELX. Acta Crystallogr A 64: 112-122.
49. +: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biol NMR 44: 213-223.
50. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, et al. 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442: 96-99.
51. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait BT, et al. 2006. Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 24: 785-796.
52. Thomas T, Corcoran LM, Gugasyan R, Dixon MP, Brodnicki T, Nutt SL, Metcalf D, Voss AK. 2006. Monocytic leukemia zinc finger protein is essential for the development of long-term reconstituting hematopoietic stem cells. Genes Dev 20: 1175-1186.
53. Ullah M, Pelletier N, Xiao L, Zhao SP, Wang K, Degerny C, Tahmasebi S, Cayrou C, Doyon Y, Goh SL, et al. 2008. Molecular architecture of quartet MOZ/MORF histone acetyltransferase complexes. Mol Cell Biol 28: 6828-6843.
54. Vezzoli A, Bonadies N, Allen MD, Freund SM, Santiveri CM, Kvinlaug BT, Huntly BJ, Gottgens B, Bycroft M. 2010. Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol 17: 617-619.
55. Voss AK, Collin C, Dixon MP, Thomas T. 2009. Moz and retinoic acid coordinately regulate H3K9 acetylation, Hox gene expression, and segment identity. Dev Cell 17: 674-686.
56. Wang GG, Allis CD, Chi P. 2007. Chromatin remodeling and cancer, part I: Covalent histone modifications. Trends Mol Med 13: 363-372.
57. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, et al. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903.
58. Weber C, Wider G, von Freyberg B, Traber R, Braun W, Widmer H, Wuthrich K. 1991. The NMR structure of cyclosporin A bound to cyclophilin in aqueous solution. Biochemistry 30: 6563-6574.
59. Yang XJ, Ullah M. 2007. MOZ and MORF, two large MYSTic HATs in normal and cancer stem cells. Oncogene 26: 5408-5419.
60. Zeng L, Zhou MM. 2002. Bromodomain: An acetyl-lysine binding domain. FEBS Lett 513: 124-128.
61. Zeng L, Zhang Q, Li S, Plotnikov AN, Walsh MJ, Zhou MM. 2010. Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466: 258-262.