Structural basis for WDR5 interaction (Win) motif recognition in human SET1 family histone methyltransferases

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27275-27289

  Dharmarajan, Venkatasubramanian ^a,c   Lee, Jeong Heon ^b   Patel, Anamika ^c   Skalnik, David G ^b   Cosgrove, Michael S ^c  

^a SYRACUSE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORE COMPLEX; ENERGY DIFFERENCES; HISTONE H3; HISTONE METHYLTRANSFERASES; IN-VITRO; LYMPHOCYTIC LEUKEMIA; MAMMALIAN CELLS; METHYLATION INHIBITORS; METHYLTRANSFERASES; MOTIF RECOGNITION; MOTIF SEQUENCE; NATURALLY OCCURRING; NON-CONSERVED RESIDUES; STRUCTURAL BASIS;

AMINO ACIDS; BINDING ENERGY; GENES; TRANSCRIPTION;

PROTEINS;

ARGININE; BINDING PROTEIN; HISTONE METHYLTRANSFERASE; LYSINE; MIXED LINEAGE LEUKEMIA 1 PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN; PEPTIDE; PROTEIN SET1; UNCLASSIFIED DRUG; WDR5 INTERACTION PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME REGULATION; ENZYME SPECIFICITY; GENETIC CONSERVATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; MAMMAL CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RESIDUE ANALYSIS; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; DNA-BINDING PROTEINS; ENZYME INHIBITORS; HEK293 CELLS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; LEUKEMIA, LYMPHOID; LEUKEMIA, MYELOID; METHYLATION; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NUCLEAR PROTEINS; RETINOL-BINDING PROTEINS, CELLULAR; TRANSCRIPTION FACTORS;

EID: 84864723459     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.364125     Document Type: Article

References (67)

1. Dillon, S. C., Zhang, X., Trievel, R. C., and Cheng, X. (2005) The SETdomain protein superfamily: protein lysine methyltransferases. Genome Biol. 6, 227
2. Cosgrove, M. S. (2006) PHinDing a new histone "effector" domain. Structure 14, 1096-1098
3. 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
4. Pray-Grant, M. G., Daniel, J. A., Schieltz, D., Yates, J. R., 3rd, and Grant, P. A. (2005) Chd1 chromodomain links histone H3 methylation with SA-GA- and SLIK-dependent acetylation. Nature 433, 434-438
5. Santos-Rosa, H., Schneider, R., Bernstein, B. E., Karabetsou, N., Morillon, A., Weise, C., Schreiber, S. L., Mellor, J., and Kouzarides, T. (2003) Methylation of histone H3 K4 mediates association of the Isw1p ATPase with chromatin. Mol. Cell 12, 1325-1332
6. Wysocka, J., Swigut, T., Xiao, H., Milne, T. A., Kwon, S. Y., Landry, J., Kauer, M., Tackett, A. J., Chait, B. T., Badenhorst, P., Wu, C., and Allis, C. D. (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442, 86-90
7. Patel, A., Dharmarajan, V., Vought, V. E., and Cosgrove, M. S. (2009) On the mechanism of multiple lysine methylation by the human mixed lineage leukemia protein-1 (MLL1) core complex. J. Biol. Chem. 284, 24242-24256
8. Patel, A., Vought, V. E., Dharmarajan, V., and Cosgrove, M. S. (2011) A novel non-SET domain multi-subunit methyltransferase required for sequential nucleosomal histone H3 methylation by the mixed lineage leukemia protein-1 (MLL1) core complex. J. Biol. Chem. 286, 3359 -3369
9. Briggs, S. D., Bryk, M., Strahl, B. D., Cheung, W. L., Davie, J. K., Dent, S. Y., Winston, F., and Allis, C. D. (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15, 3286-3295
10. Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., Wang, W., Weng, Z., Green, R. D., Crawford, G. E., and Ren, B. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39, 311-318
11. Nislow, C., Ray, E., and Pillus, L. (1997) SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol. Biol. Cell 8, 2421-2436
12. Schneider, J., Wood, A., Lee, J. S., Schuster, R., Dueker, J., Maguire, C., Swanson, S. K., Florens, L., Washburn, M. P., and Shilatifard, A. (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol. Cell 19, 849-856
13. Liu, C. L., Kaplan, T., Kim, M., Buratowski, S., Schreiber, S. L., Friedman, N., and Rando, O. J. (2005) Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3, e328
14. Pokholok, D. K., Harbison, C. T., Levine, S., Cole, M., Hannett, N. M., Lee, T. I., Bell, G. W., Walker, K., Rolfe, P. A., Herbolsheimer, E., Zeitlinger, J., Lewitter, F., Gifford, D. K., and Young, R. A. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122, 517-527
15. 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
16. Lee, J. H., and Skalnik, D.G. (2005) CpG-binding protein (CXXC finger protein 1) is a component of the mammalian Set1 histone H3-Lys4 methyltransferase complex, the analogue of the yeast Set1/COMPASS complex. J. Biol. Chem. 280, 41725-41731
17. Lee, J. H., Tate, C. M., You, J. S., and Skalnik, D. G. (2007) Identification and characterization of the human Set1B histone H3-Lys4 methyltransferase complex. J. Biol. Chem. 282, 13419-13428
18. Miller, T., Krogan, N. J., Dover, J., Erdjument-Bromage, H., Tempst, P., Johnston, M., Greenblatt, J. F., and Shilatifard, A. (2001) COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. U.S.A. 98, 12902-12907
19. Nagy, P. L., Griesenbeck, J., Kornberg, R. D., and Cleary, M. L. (2002) A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc. Natl. Acad. Sci. U.S.A. 99, 90-94
20. Nakamura, T., Mori, T., Tada, S., Krajewski, W., Rozovskaia, T., Wassell, R., Dubois, G., Mazo, A., Croce, C. M., and Canaani, E. (2002) ALL-1 is a histone methyltransferase that assembles a supercomplex of proteins involved in transcriptional regulation. Mol. Cell 10, 1119-1128
21. Roguev, A., Schaft, D., Shevchenko, A., Pijnappel, W. W., Wilm, M., Aasland, R., and Stewart, A. F. (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J. 20, 7137-7148
22. Steward, M. M., Lee, J. S., O'Donovan, A., Wyatt, M., Bernstein, B. E., and Shilatifard, A. (2006) Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes. Nat. Struct. Mol. Biol. 13, 852-854
23. Yokoyama, A., Wang, Z., Wysocka, J., Sanyal, M., Aufiero, D. J., Kitabayashi, I., Herr, W., and Cleary, M. L. (2004) Leukemia proto-oncoprotein MLL forms a SET1-like histone methyltransferase complex with menin to regulate Hox gene expression. Mol. Cell. Biol. 24, 5639 -5649
24. Cao, F., Chen, Y., Cierpicki, T., Liu, Y., Basrur, V., Lei, M., and Dou, Y. (2010) An Ash2L/RbBP5 heterodimer stimulates the MLL1 methyltransferase activity through coordinated substrate interactions with the MLL1 SET domain. PLoS One 5, e14102
25. Takahashi, Y. H., Westfield, G. H., Oleskie, A. N., Trievel, R. C., Shilatifard, A., and Skiniotis, G. (2011) Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proc. Natl. Acad. Sci. U.S.A. 108, 20526-20531
26. Dou, Y., Milne, T. A., Ruthenburg, A. J., Lee, S., Lee, J. W., Verdine, G. L., Allis, C. D., and Roeder, R. G. (2006) Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat. Struct. Mol. Biol. 13, 713-719
27. Glaser, S., Schaft, J., Lubitz, S., Vintersten, K., van der Hoeven, F., Tufteland, K. R., Aasland, R., Anastassiadis, K., Ang, S. L., and Stewart, A. F. (2006) Multiple epigenetic maintenance factors implicated by the loss of Mll2 in mouse development. Development 133, 1423-1432
28. Hughes, C. M., Rozenblatt-Rosen, O., Milne, T. A., Copeland, T. D., Levine, S. S., Lee, J. C., Hayes, D. N., Shanmugam, K. S., Bhattacharjee, A., Biondi, C. A., Kay, G. F., Hayward, N. K., Hess, J. L., and Meyerson, M. (2004) Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol. Cell 13, 587-597
29. Milne, T. A., Briggs, S. D., Brock, H. W., Martin, M. E., Gibbs, D., Allis, C. D., and Hess, J. L. (2002) MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol. Cell 10, 1107-1117
30. Prasad, R., Zhadanov, A. B., Sedkov, Y., Bullrich, F., Druck, T., Rallapalli, R., Yano, T., Alder, H., Croce, C. M., Huebner, K., Mazo, A., and Canaani, E. (1997) Structure and expression pattern of human ALR, a novel gene with strong homology to ALL-1 involved in acute leukemia and to Drosophila trithorax. Oncogene 15, 549-560
31. Wysocka, J., Myers, M. P., Laherty, C. D., Eisenman, R. N., and Herr, W. (2003) Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3-K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev. 17, 896-911
32. Cho, Y. W., Hong, T., Hong, S., Guo, H., Yu, H., Kim, D., Guszczynski, T., Dressler, G. R., Copeland, T. D., Kalkum, M., and Ge, K. (2007) PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J. Biol. Chem. 282, 20395-20406
33. Wang, P., Lin, C., Smith, E. R., Guo, H., Sanderson, B. W., Wu, M., Gogol, M., Alexander, T., Seidel, C., Wiedemann, L. M., Ge, K., Krumlauf, R., and Shilatifard, A. (2009) Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol. Cell. Biol. 29, 6074-6085
34. Wysocka, J., Swigut, T., Milne, T. A., Dou, Y., Zhang, X., Burlingame, A. L., Roeder, R. G., Brivanlou, A. H., and Allis, C. D. (2005) WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121, 859-872
35. Patel, A., Dharmarajan, V., and Cosgrove, M. S. (2008) Structure ofWDR5 bound to mixed lineage leukemia protein-1 peptide. J. Biol. Chem. 283, 32158-32161
36. Patel, A., Vought, V. E., Dharmarajan, V., and Cosgrove, M. S. (2008) A conserved arginine-containing motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein-1 core complex. J. Biol. Chem. 283, 32162-32175
37. Dorigo, B., Schalch, T., Kulangara, A., Duda, S., Schroeder, R. R., and Richmond, T. J. (2004) Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science 306, 1571-1573
38. Paulussen, A. D., Stegmann, A. P., Blok, M. J., Tserpelis, D., Posma-Velter, C., Detisch, Y., Smeets, E. E., Wagemans, A., Schrander, J. J., van den Boogaard, M. J., van der Smagt, J., van Haeringen, A., Stolte-Dijkstra, I., Kerstjens-Frederikse, W. S., Mancini, G. M., Wessels, M. W., Hennekam, R. C., Vreeburg, M., Geraedts, J., de Ravel, T., Fryns, J. P., Smeets, H. J., Devriendt, K., and Schrander-Stumpel, C. T. (2011) MLL2 mutation spectrum in 45 patients with Kabuki syndrome. Hum. Mutat. 32, E2018-E2025
39. Dharmarajan, V., and Cosgrove, M. S. (2011) in Acute Leukemia-The Scientist's Perspective and Challenge (Antica, M., ed) pp. 157-204, InTech, Rijeka, Croatia
40. Huntsman, D. G., Chin, S. F., Muleris, M., Batley, S. J., Collins, V. P., Wiedemann, L. M., Aparicio, S., and Caldas, C. (1999) MLL2, the second human homolog of the Drosophila trithorax gene, maps to 19q13.1 and is amplified in solid tumor cell lines. Oncogene 18, 7975-7984
41. FitzGerald, K. T., and Diaz, M. O. (1999) MLL2: a new mammalian member of the trx/MLL family of genes. Genomics 59, 187-192
42. Caligiuri, M. A., Schichman, S. A., Strout, M. P., Mro'zek, K., Baer, M. R., Frankel, S. R., Barcos, M., Herzig, G. P., Croce, C. M., and Bloomfield, C. D. (1994) Molecular rearrangement of the ALL-1 gene in acute myeloid leukemia without cytogenetic evidence of 11q23 chromosomal translocations. Cancer Res. 54, 370-373
43. Quentmeier, H., Reinhardt, J., Zaborski, M., and Drexler, H. G. (2003) MLL partial tandem duplications in acute leukemia cell lines. Leukemia 17, 980-981
44. Schichman, S. A., Caligiuri, M. A., Gu, Y., Strout, M. P., Canaani, E., Bloomfield, C. D., and Croce, C. M. (1994) ALL-1 partial duplication in acute leukemia. Proc. Natl. Acad. Sci. U.S.A. 91, 6236-6239
45. Dorrance, A. M., Liu, S., Chong, A., Pulley, B., Nemer, D., Guimond, M., Yuan, W., Chang, D., Whitman, S. P., Marcucci, G., and Caligiuri, M. A. (2008) The Mll partial tandem duplication: differential, tissue-specific activity in the presence or absence of the wild-type allele. Blood 112, 2508-2511
46. Dorrance, A. M., Liu, S., Yuan, W., Becknell, B., Arnoczky, K. J., Guimond, M., Strout, M. P., Feng, L., Nakamura, T., Yu, L., Rush, L. J., Weinstein, M., Leone, G., Wu, L., Ferketich, A., Whitman, S. P., Marcucci, G., and Caligiuri, M. A. (2006) Mll partial tandem duplication induces aberrant Hox expression in vivo via specific epigenetic alterations. J. Clin. Investig. 116, 2707-2716
47. Whitman, S. P., Liu, S., Vukosavljevic, T., Rush, L. J., Yu, L., Liu, C., Klisovic, M. I., Maharry, K., Guimond, M., Strout, M. P., Becknell, B., Dorrance, A., Klisovic, R. B., Plass, C., Bloomfield, C. D., Marcucci, G., and Caligiuri, M. A. (2005) The MLL partial tandem duplication: evidence for recessive gain-of-function in acute myeloid leukemia identifies a novel patient subgroup for molecular-targeted therapy. Blood 106, 345-352
48. Zhang, P., Lee, H., Brunzelle, J. S., and Couture, J. F. (2012) The plasticity of WDR5 peptide-binding cleft enables the binding of the SET1 family of histone methyltransferases. Nucleic Acids Res. 40, 4237-4246
49. Cheng, Y., and Prusoff, W. H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108
50. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
51. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
52. Vagin, A., and Teplyakov, A (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025
53. Ruthenburg, A. J., Wang, W., Graybosch, D. M., Li, H., Allis, C. D., Patel, D. J., and Verdine, G. L. (2006) Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex. Nat. Struct. Mol. Biol. 13, 704-712
54. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
55. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119
56. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
57. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
58. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
59. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New York
60. Karatas, H., Townsend, E. C., Bernard, D., Dou, Y., and Wang, S. (2010) Analysis of the binding of mixed lineage leukemia 1 (MLL1) and histone 3 peptides to WD repeat domain 5 (WDR5) for the design of inhibitors of the MLL1-WDR5 interaction. J. Med. Chem. 53, 5179-5185
61. Song, J. J., and Kingston, R. E. (2008) WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. J. Biol. Chem., 283, 35258-35264
62. Couture, J. F., Collazo, E., and Trievel, R. C. (2006) Molecular recognition of histone H3 by the WD40 protein WDR5. Nat. Struct. Mol. Biol. 13, 698-703
63. Han, Z., Guo, L., Wang, H., Shen, Y., Deng, X. W., and Chai, J. (2006) Structural basis for the specific recognition of methylated histone H3 lysine 4 by the WD-40 protein WDR5. Mol. Cell 22, 137-144
64. Schuetz, A., Allali-Hassani, A., Martín, F., Loppnau, P., Vedadi, M., Bochkarev, A., Plotnikov, A. N., Arrowsmith, C. H., and Min, J. (2006) Structural basis for molecular recognition and presentation of histone H3 by WDR5. EMBO J. 25, 4245-4252
65. Cosgrove, M. S., and Patel, A. (2010) Mixed lineage leukemia: a structure- function perspective of the MLL1 protein. FEBS J. 277, 1832- 1842
66. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
67. Henikoff, S., and Henikoff, J. G. (1992) Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. U.S.A. 89, 10915-10919