Solution structure of the Pdp1 PWWP domain reveals its unique binding sites for methylated H4K20 and DNA

Biochemical Journal

Volumn 442, Issue 3, 2012, Pages 527-538

  Qiu, Yu ^a   Zhang, Wen ^a   Zhao, Chen ^a   Wang, Yan ^a   Wang, Weiwei ^a   Zhang, Jiahai ^a   Zhang, Zhiyong ^a   Li, Guohong ^b   Shi, Yunyu ^a   Tu, Xiaoming ^a   Wu, Jihui ^a  

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

^b INSTITUTE OF BIOPHYSICS   (China)

Author keywords

DNA binding; Histone methylation; Nucleosome; Pdp1; PWWP domain; Schizosaccharomyces pombe; Set9

Indexed keywords

BINDING PROTEIN; CELL PROTEIN; DNA; DOUBLE STRANDED DNA; HISTONE H4; LYSINE; LYSINE DERIVATIVE; METHYLLYSINE; METHYLTRANSFERASE; PDP1 PROTEIN; SET9 PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; HISTONE METHYLATION; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOSOME; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; DNA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HISTONES; LYSINE; METHYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SOLUTIONS;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 84863230348     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111885     Document Type: Article

References (45)

1. Allis, C., Jenuwein, T. and Reinberg, D. (2007) Epigenetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor
2. Kouzarides, T. (2007) SnapShot: histone-modifying enzymes. Cell 128, 802
3. Wang, Y. and Jia, S. (2009) Degrees make all the difference: the multifunctionality of histone H4 lysine 20 methylation. Epigenetics 4, 273-276
4. Houston, S. I., McManus, K. J., Adams, M. M., Sims, J. K., Carpenter, P. B., Hendzel, M. J. and Rice, J. C. (2008) Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J. Biol. Chem. 283, 19478-19488
5. Kalakonda, N., Fischle, W., Boccuni, P., Gurvich, N., Hoya-Arias, R., Zhao, X., Miyata, Y., Macgrogan, D., Zhang, J., Sims, J. K. et al. (2008) Histone H4 lysine 20 monomethylation promotes transcriptional repression by L3MBTL1. Oncogene 27, 4293-4304 (Pubitemid 352009998)
6. Oda, H., Okamoto, I., Murphy, N., Chu, J., Price, S. M., Shen, M. M., Torres-Padilla, M. E., Heard, E. and Reinberg, D. (2009) Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol. Cell. Biol. 29, 2278-2295
7. Rice, J. C., Nishioka, K., Sarma, K., Steward, R., Reinberg, D. and Allis, C. D. (2002) Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev. 16, 2225-2230 (Pubitemid 35013085)
8. Sims, J. K., Houston, S. I., Magazinnik, T. and Rice, J. C. (2006) A trans-tail histone code defined by monomethylated H4 Lys-20 and H3 Lys-9 demarcates distinct regions of silent chromatin. J. Biol. Chem. 281, 12760-12766 (Pubitemid 43855367)
9. Sims, J. K. and Rice, J. C. (2008) PR-Set7 establishes a repressive trans-tail histone code that regulates differentiation. Mol. Cell. Biol. 28, 4459-4468 (Pubitemid 351977746)
10. Trojer, P., Li, G., Sims, III, R. J., Vaquero, A., Kalakonda, N., Boccuni, P., Lee, D., Erdjument-Bromage, H., Tempst, P., Nimer, S. D. et al. (2007) L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129, 915-928 (Pubitemid 46802701)
11. Botuyan, M. V., Lee, J., Ward, I. M., Kim, J. E., Thompson, J. R., Chen, J. and Mer, G. (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361-1373 (Pubitemid 44960409)
12. Sanders, S. L., Portoso, M., Mata, J., Bahler, J., Allshire, R. C. and Kouzarides, T. (2004) Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119, 603-614 (Pubitemid 39535749)
13. Schotta, G., Lachner, M., Sarma, K., Ebert, A., Sengupta, R., Reuter, G., Reinberg, D. and Jenuwein, T. (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18, 1251-1262 (Pubitemid 38720593)
14. Couture, J. F., Collazo, E., Brunzelle, J. S. and Trievel, R. C. (2005) Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase. Genes Dev. 19, 1455-1465 (Pubitemid 41003012)
15. Fang, J., Feng, Q., Ketel, C. S., Wang, H., Cao, R., Xia, L., Erdjument-Bromage, H., Tempst, P., Simon, J. A. and Zhang, Y. (2002) Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr. Biol. 12, 1086-1099 (Pubitemid 34766930)
16. Nishioka, K., Rice, J. C., Sarma, K., Erdjument-Bromage, H., Werner, J., Wang, Y., Chuikov, S., Valenzuela, P., Tempst, P., Steward, R. et al. (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9, 1201-1213 (Pubitemid 34722300)
17. Xiao, B., Jing, C., Kelly, G., Walker, P. A., Muskett, F. W., Frenkiel, T. A., Martin, S. R., Sarma, K., Reinberg, D., Gamblin, S. J. et al. (2005) Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev. 19, 1444-1454 (Pubitemid 41003011)
18. Zhang, K., Mosch, K., Fischle, W. and Grewal, S. I. (2008) Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat. Struct. Mol. Biol. 15, 381-388 (Pubitemid 351483395)
19. Wang, Y., Reddy, B., Thompson, J., Wang, H., Noma, K., Yates, III, J. R. and Jia, S. (2009) Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Mol. Cell 33, 428-437
20. Izumoto, Y., Kuroda, T., Harada, H., Kishimoto, T. and Nakamura, H. (1997) Hepatoma-derived growth factor belongs to a gene family in mice showing significant homology in the amino terminus. Biochem. Biophys. Res. Commun. 238, 26-32 (Pubitemid 27453267)
21. Stec, I., Wright, T. J., van Ommen, G. J., de Boer, P. A., van Haeringen, A., Moorman, A. F., Altherr, M. R. and den Dunnen, J. T. (1998) WHSC1, a 90 kb SET domain-containing gene, expressed in early development and homologous to a Drosophila dysmorphy gene maps in the Wolf-Hirschhorn syndrome critical region and is fused to IgH in t(4;14) multiple myeloma. Hum. Mol. Genet. 7, 1071-1082 (Pubitemid 28306870)
22. Qiu, C., Sawada, K., Zhang, X. and Cheng, X. (2002) The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds. Nat. Struct. Biol. 9, 217-224 (Pubitemid 34171315)
23. Lukasik, S. M., Cierpicki, T., Borloz, M., Grembecka, J., Everett, A. and Bushweller, J. H. (2006) High resolution structure of the HDGF PWWP domain: a potential DNA binding domain. Protein Sci. 15, 314-323 (Pubitemid 43145003)
24. Vezzoli, A., Bonadies, N., Allen, M. D., Freund, S. M., Santiveri, C. M., Kvinlaug, B. T., Huntly, B. J., Gottgens, B. and Bycroft, M. (2010) Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat. Struct. Mol. Biol. 17, 617-619
25. Dhayalan, A., Rajavelu, A., Rathert, P., Tamas, R., Jurkowska, R. Z., Ragozin, S. and Jeltsch, A. (2010) The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 285, 26114-26120
26. Clore, G. M. and Gronenborn, A. M. (1994) Multidimensional heteronuclear nuclear magnetic resonance of proteins. Methods Enzymol. 239, 349-363
27. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
28. Shen, Y., Delaglio, F., Cornilescu, G. and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
29. Brunger, 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. et al. (1998) Crystallography &NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 54, 905-921
30. Koradi, R., Billeter, M. and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55, 29-32
31. Shen, W., Xu, C., Huang, W., Zhang, J., Carlson, J. E., Tu, X., Wu, J. and Shi, Y. (2007) Solution structure of human Brg1 bromodomain and its specific binding to acetylated histone tails. Biochemistry 46, 2100-2110 (Pubitemid 46355321)
32. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D. and Kay, L. E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33, 5984-6003 (Pubitemid 24184605)
33. Liu, Y., Huang, H., Zhou, B. O., Wang, S. S., Hu, Y., Li, X., Liu, J., Zang, J., Niu, L., Wu, J. et al. (2010) Structural analysis of Rtt106p reveals a DNA binding role required for heterochromatin silencing. J. Biol. Chem. 285, 4251-4262
34. Simon, M. D., Chu, F., Racki, L. R., de la Cruz, C. C., Burlingame, A. L., Panning, B., Narlikar, G. J. and Shokat, K. M. (2007) The site-specific installation of methyl-lysine analogs into recombinant histones. Cell 128, 1003-1012 (Pubitemid 46341408)
35. Luger, K., Rechsteiner, T. J. and Richmond, T. J. (1999) Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119, 1-16
36. Keeney, J. B. and Boeke, J. D. (1994) Efficient targeted integration at leu1-32 and ura4-294 in Schizosaccharomyces pombe. Genetics 136, 849-856 (Pubitemid 24085636)
37. Gietz, R. D., Schiestl, R. H., Willems, A. R. and Woods, R. A. (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11, 355-360
38. Matsuo, Y., Asakawa, K., Toda, T. and Katayama, S. (2006) A rapid method for protein extraction from fission yeast. Biosci. Biotechnol. Biochem. 70, 1992-1994 (Pubitemid 44285439)
39. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)
40. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138 (Pubitemid 23288916)
41. Wu, H., Zeng, H., Lam, R., Tempel, W., Amaya, M. F., Xu, C., Dombrovski, L., Qiu, W., Wang, Y. and Min, J. (2011) Structural and histone binding ability characterizations of human PWWP domains. PLoS ONE 6, e18919
42. Slater, L. M., Allen, M. D. and Bycroft, M. (2003) Structural variation in PWWP domains. J. Mol. Biol. 330, 571-576 (Pubitemid 36808688)
43. Lee, J., Thompson, J. R., Botuyan, M. V. and Mer, G. (2008) Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A-tudor. Nat. Struct. Mol. Biol. 15, 109-111
44. Pena, P. V., Davrazou, F., Shi, X., Walter, K. L., Verkhusha, V. V., Gozani, O., Zhao, R. and Kutateladze, T. G. (2006) Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442, 100-103 (Pubitemid 44064217)
45. Jacobs, S. A. and Khorasanizadeh, S. (2002) Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail. Science 295, 2080-2083 (Pubitemid 34229471)