A phospho/methyl switch at histone H3 regulates TFIID association with mitotic chromosomes

EMBO Journal

Volumn 29, Issue 23, 2010, Pages 3967-3978

  Varier, Radhika A ^a   Outchkourov, Nikolay S ^a   De Graaf, Petra ^a   Van Schaik, Frederik M A ^a   Ensing, Henk Jan L ^a   Wang, Fangwei ^b   Higgins, Jonathan M G ^b   Kops, Geert J P L ^a   Timmers, Hth Marc ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

haspin; histone methylation; mitosis; PHD; TFIID

Indexed keywords

HISTONE; HOMEODOMAIN PROTEIN; THREONINE; TRANSCRIPTION FACTOR IID;

ARTICLE; BINDING AFFINITY; CHROMATIN; CHROMOSOME; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; METHYLATION; MICROSCOPY; MITOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; CHROMOSOMES; GENE EXPRESSION REGULATION; HISTONES; HUMANS; METHYLATION; MITOSIS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTOR TFIID; TRANSCRIPTIONAL ACTIVATION;

EUKARYOTA;

EID: 78649690139     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.261     Document Type: Article

References (70)

1. Bereczki O, Ujfaludi Z, Pardi N, Nagy Z, Tora L, Boros IM, Balint E (2008) TATA binding protein associated factor 3 (TAF3) interacts with p53 and inhibits its function. BMC Mol Biol 9: 57
2. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas III EJ, Gingeras TR, Schreiber SL, Lander ES (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181
3. Bhattacharya S, Takada S, Jacobson RH (2007) Structural analysis and dimerization potential of the human TAF5 subunit of TFIID. Proc Natl Acad Sci USA 104: 1189-1194
4. Blobel GA, Kadauke S, Wang E, Lau AW, Zuber J, Chou MM, Vakoc CR (2009) A reconfigured pattern of MLL occupancy within mitotic chromatin promotes rapid transcriptional reactivation following mitotic exit. Mol Cell 36: 970-983
5. Christova R, Oelgeschlager T (2002) Association of human TFIID-promoter complexes with silenced mitotic chromatin in vivo. Nat Cell Biol 4: 79-82
6. Dai J, Sultan S, Taylor SS, Higgins JM (2005) The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev 19: 472-488
7. de Graaf P, Mousson F, Geverts B, Scheer E, Tora L, Houtsmuller AB, Timmers HT (2010) Chromatin interaction of TATA-binding protein is dynamically regulated in human cells. J Cell Sci 123: 2663-2671
8. Deato MD, Marr MT, Sottero T, Inouye C, Hu P, Tjian R (2008) MyoD targets TAF3/TRF3 to activate myogenin transcription. Mol Cell 32: 96-105
9. Deato MD, Tjian R (2007) Switching of the core transcription machinery during myogenesis. Genes Dev 21 : 2137-2149
10. Dignam JD, Lebovitz RM, Roeder RG (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11 : 1475-1489
11. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 161: 267-280
12. Dominguez C, Bonvin AM, Winkler GS, van Schaik FM, Timmers HT, Boelens R (2004) Structural model of the UbcH5B/CNOT4 complex revealed by combining NMR, mutagenesis, and docking approaches. Structure 12: 633-644
13. Dreijerink KM, Mulder KW, Winkler GS, Hoppener JW, Lips CJ, Timmers HT (2006) Menin links estrogen receptor activation to histone H3K4 trimethylation. Cancer Res 66: 4929-4935
14. Eswaran J, Patnaik D, Filippakopoulos P, Wang F, Stein RL, Murray JW, Higgins JM, Knapp S (2009) Structure and functional characterization of the atypical human kinase haspin. Proc Natl Acad Sci USA 106: 20198-20203
15. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, Shabanowitz J, Hunt DF, Funabiki H, Allis CD (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438: 1116-1122
16. Fischle W, Wang Y, Allis CD (2003) Binary switches and modification cassettes in histone biology and beyond. Nature 425: 475-479
17. Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y, Minor W, Rastinejad F, Khorasanizadeh S (2005) Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181-1185
18. Gangloff YG, Pointud JC, Thuault S, Carre L, Romier C, Muratoglu S, Brand M, Tora L, Couderc JL, Davidson I (2001) The TFIID components human TAF(II)140 and Drosophila BIP2 (TAF(II)155) are novel metazoan homologues of yeast TAF(II)47 containing a histone fold and a PHD finger. Mol Cell Biol 21 : 5109-5121
19. Garcia BA, Barber CM, Hake SB, Ptak C, Turner FB, Busby SA, Shabanowitz J, Moran RG, Allis CD, Hunt DF (2005) Modifications of human histone H3 variants during mitosis. Biochemistry 44: 13202-13213
20. Garske AL, Oliver SS, Wagner EK, Musselman CA, LeRoy G, Garcia BA, Kutateladze TG, Denu JM (2010) Combinatorial profiling of chromatin binding modules reveals multisite discrimination. Nat Chem Biol 6: 283-290
21. Gilfillan S, Stelzer G, Piaia E, Hofmann MG, Meisterernst M (2005) Efficient binding of NC2.TATA-binding protein to DNA in the absence of TATA. J Biol Chem 280: 6222-6230
22. Gottesfeld JM, Forbes DJ (1997) Mitotic repression of the transcrip-tional machinery. Trends Biochem Sci 22: 197-202
23. 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
24. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88
25. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, van Meel J, Rieder CL, Peters JM (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 161: 281-294
26. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318
27. Heix J, Vente A, Voit R, Budde A, Michaelidis TM, Grummt I (1998) Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B-mediated phos-phorylation. EMBO J 17: 7373-7381
28. Higgins JM (2010) Haspin: a newly discovered regulator of mitotic chromosome behavior. Chromosoma 119: 137-147
29. Hirota T, Lipp JJ, Toh BH, Peters JM (2005) Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438: 1176-1180
30. 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
31. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, Hayes DN, Shanmugam KS, Bhattacharjee A, Biondi CA, Kay GF, Hayward NK, Hess JL, Meyerson M (2004) Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell 13: 587-597
32. Jacobson RH, Ladurner AG, King DS, Tjian R (2000) Structure and function of a human TAFII250 double bromodomain module. Science 288: 1422-1425
33. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293: 1074-1080
34. Kaelin Jr WG, Krek W, Sellers WR, DeCaprio JA, Ajchenbaum F, Fuchs CS, Chittenden T, Li Y, Farnham PJ, Blanar MA, Livingston DM, Flemington EK (1992) Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell 70: 351-364
35. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, Funabiki H (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase aurora B. Science (e-pub ahead of print)
36. Kieffer-Kwon P, Martianov I, Davidson I (2004) Cell-specific nu-cleolar localization of TBP-related factor 2. Mol Biol Cell 15: 4356-4368
37. 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
38. Kornberg RD, Lorch Y (1999) Chromatin-modifying and -remodeling complexes. Curr Opin Genet Dev 9: 148-151
39. Kouskouti A, Talianidis I (2005) Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBO J 24: 347-357
40. Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SG, Green MR, Goodman RH (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370: 223-226
41. Lan F, Collins RE, De Cegli R, Alpatov R, Horton JR, Shi X, Gozani O, Cheng X, Shi Y (2007) Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448: 718-722
42. Leresche A, Wolf VJ, Gottesfeld JM (1996) Repression of RNA polymerase II and III transcription during M phase of the cell cycle. Exp Cell Res 229: 282-288
43. Markaki Y, Christogianni A, Politou AS, Georgatos SD (2009) Phosphorylation of histone H3 at Thr3 is part of a combinatorial pattern that marks and configures mitotic chromatin. J Cell Sci 122: 2809-2819
44. Matthews AG, Kuo AJ, Ramon-Maiques S, Han S, Champagne KS, Ivanov D, Gallardo M, Carney D, Cheung P, Ciccone DN, Walter KL, Utz PJ, Shi Y, Kutateladze TG, Yang W, Gozani O, Oettinger MA (2007) RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 450: 1106-1110
45. Muller F, Demeny MA, Tora L (2007) New problems in RNA polymerase II transcription initiation: matching the diversity of core promoters with a variety of promoter recognition factors. J Biol Chem 282: 14685-14689
46. Org T, Chignola F, Hetenyi C, Gaetani M, Rebane A, Liiv I, Maran U, Mollica L, Bottomley MJ, Musco G, Peterson P (2008) The autoimmune regulator PHD finger binds to non-methylated his-tone H3K4 to activate gene expression. EMBO Rep 9: 370-376
47. Orphanides G, Lagrange T, Reinberg D (1996) The general transcription factors of RNA polymerase II. Genes Dev 10 : 2657-2683
48. Palacios A, Munoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martin-Garcia JM, Luque I, Montoya G, Blanco FJ (2008) Molecular basis of histone H3K4me3 recognition by ING4. J Biol Chem 283: 15956-15964
49. Pijnappel WP, Kolkman A, Baltissen MP, Heck AJ, Timmers HM (2009) Quantitative mass spectrometry of TATA binding protein-containing complexes and subunit phosphorylations during the cell cycle. Proteome Sci 7: 46
50. Polioudaki H, Markaki Y, Kourmouli N, Dialynas G, Theodoropoulos PA, Singh PB, Georgatos SD (2004) Mitotic phosphorylation of histone H3 at threonine 3. FEBS Lett 560: 39-44
51. Prigent C, Dimitrov S (2003) Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 116: 3677-3685
52. Ramon-Maiques S, Kuo AJ, Carney D, Matthews AG, Oettinger MA, Gozani O, Yang W (2007) The plant homeodomain finger of RAG2 recognizes histone H3 methylated at both lysine-4 and arginine-2. Proc Natl Acad Sci USA 104: 18993-18998
53. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599
54. Saksouk N, Avvakumov N, Champagne KS, Hung T, Doyon Y, Cayrou C, Paquet E, Ullah M, Landry AJ, Cote V, Yang XJ, Gozani O, Kutateladze TG, Cote J (2009) HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol Cell 33: 257-265
55. Segil N, Guermah M, Hoffmann A, Roeder RG, Heintz N (1996) Mitotic regulation of TFIID: inhibition of activator-dependent transcription and changes in subcellular localization. Genes Dev 10: 2389-2400
56. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns BR, Ayer DE, Kutateladze TG, Shi Y, Cote J, Chua KF et al (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442: 96-99
57. Soutoglou E, Demeny MA, Scheer E, Fienga G, Sassone-Corsi P, Tora L (2005) The nuclear import of TAF10 is regulated by one of its three histone fold domain-containing interaction partners. Mol Cell Biol 25: 4092-4104
58. Stokes DG, Perry RP (1995) DNA-binding and chromatin localization properties of CHD1. Mol Cell Biol 15: 2745-2753
59. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45
60. Thomas MC, Chiang CM (2006) The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41 : 105-178
61. Van Der Knaap JA, Borst JW, Van Der Vliet PC, Gentz R, Timmers HT (1997) Cloning of the cDNA for the TATA-binding protein-associated factorII170 subunit of transcription factor B-TFIID reveals homology to global transcription regulators in yeast and Drosophila. Proc Natl Acad Sci USA 94: 11827-11832
62. Van Ingen H, Van Schaik FM, Wienk H, Ballering J, Rehmann H, Dechesne AC, Kruijzer JA, Liskamp RM, Timmers HT, Boelens R (2008) Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. Structure 16: 1245-1256
63. Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, Varier RA, Baltissen MP, Stunnenberg HG, Mann M, Timmers HT (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131: 58-69
64. Verrijzer CP, Tjian R (1996) TAFs mediate transcriptional activation and promoter selectivity. Trends Biochem Sci 21: 338-342
65. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, Stukenberg PT, Gorbsky GJ, Higgins JM (2010) Histone H3 Thr-3 phosphor-ylation by haspin positions aurora B at Centromeres in mitosis. Science (e-pub ahead of print)
66. Wen H, Li J, Song T, Lu M, Kan PY, Lee MG, Sha B, Shi X (2010) Recognition of histone H3K4 trimethylation by the plant home-odomain of PHF2 modulates histone demethylation. J Biol Chem 285: 9322-9326
67. Workman JL, Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 67: 545-579
68. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J, Kauer M, Tackett AJ, Chait BT, Badenhorst P, Wu C, Allis CD (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86-90
69. Xing H, Vanderford NL, Sarge KD (2008) The TBP-PP2A mitotic complex bookmarks genes by preventing condensin action. Nat Cell Biol 10: 1318-1323
70. Yokoyama A, Wang Z, Wysocka J, Sanyal M, Aufiero DJ, Kitabayashi I, Herr W, Cleary ML (2004) Leukemia proto-onco-protein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol Cell Biol 24: 5639-5649