Regulation of Set9-Mediated H4K20 Methylation by a PWWP Domain Protein

Molecular Cell

Volumn 33, Issue 4, 2009, Pages 428-437

  Wang, Yu ^a   Reddy, Bharat ^a   Thompson, James ^b   Wang, Hengbin ^c   Noma, Ken ichi ^d   Yates III, John R ^b   Jia, Songtao ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

DNA; PROTEINS

Indexed keywords

BINDING PROTEIN; HISTONE H4; HISTONE METHYLTRANSFERASE; LYSINE; PROTEIN PDP1; SET9 ENZYME; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; GENE MUTATION; HYDROPHOBICITY; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN METHYLATION; YEAST;

AMINO ACID SEQUENCE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; HISTONES; LYSINE; MASS SPECTROMETRY; METHYLATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN METHYLTRANSFERASES; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCETACEAE;

EID: 60549108739     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.02.002     Document Type: Article

References (58)

1. Bahler J., Wu J.Q., Longtine M.S., Shah N.G., McKenzie III A., Steever A.B., Wach A., Philippsen P., and Pringle J.R. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14 (1998) 943-951
2. Berger S.L. The complex language of chromatin regulation during transcription. Nature 447 (2007) 407-412
3. Botuyan M.V., Lee J., Ward I.M., Kim J.E., Thompson J.R., Chen J., and Mer G. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127 (2006) 1361-1373
4. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., and Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298 (2002) 1039-1043
5. Carr A.M., and Casprari T. Checkpoint conrols halting the cell cycle. In: Egel R. (Ed). The Molecular Biology of Schizosaccharomyces pombe (2003), Springer, Berlin 41-56
6. Couture J.F., Collazo E., Brunzelle J.S., and Trievel R.C. Structural and functional analysis of SET8, a histone H4 Lys-20 methyltransferase. Genes Dev. 19 (2005) 1455-1465
7. Czermin B., Melfi R., McCabe D., Seitz V., Imhof A., and Pirrotta V. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111 (2002) 185-196
8. Downs J.A., Nussenzweig M.C., and Nussenzweig A. Chromatin dynamics and the preservation of genetic information. Nature 447 (2007) 951-958
9. Du L.L., Nakamura T.M., Moser B.A., and Russell P. Retention but not recruitment of Crb2 at double-strand breaks requires Rad1 and Rad3 complexes. Mol. Cell. Biol. 23 (2003) 6150-6158
10. Du L.L., Nakamura T.M., and Russell P. Histone modification-dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20 (2006) 1583-1596
11. Eng J., McCormack A., and Yates III J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5 (1994) 976-989
12. Fang J., Feng Q., Ketel C.S., Wang H., Cao R., Xia L., Erdjument-Bromage H., Tempst P., Simon J.A., and Zhang Y. Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr. Biol. 12 (2002) 1086-1099
13. Greeson N.T., Sengupta R., Arida A.R., Jenuwein T., and Sanders S.L. Di-methyl H4 lysine 20 targets the checkpoint protein CRB2 to sites of DNA damage. J. Biol. Chem. 283 (2008) 33168-33174
14. Groth A., Rocha W., Verreault A., and Almouzni G. Chromatin challenges during DNA replication and repair. Cell 128 (2007) 721-733
15. Hong E.J., Villen J., Gerace E.L., Gygi S.P., and Moazed D. A Cullin E3 Ubiquitin Ligase Complex Associates with Rik1 and the Clr4 Histone H3-K9 Methyltransferase and Is Required for RNAi-Mediated Heterochromatin Formation. RNA Biol. 2 (2005) 106-111
16. Horn P.J., Bastie J.N., and Peterson C.L. A Rik1-associated, cullin-dependent E3 ubiquitin ligase is essential for heterochromatin formation. Genes Dev. 19 (2005) 1705-1714
17. Huyen Y., Zgheib O., Ditullio Jr. R.A., Gorgoulis V.G., Zacharatos P., Petty T.J., Sheston E.A., Mellert H.S., Stavridi E.S., and Halazonetis T.D. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432 (2004) 406-411
18. Jia S., Kobayashi R., and Grewal S.I. Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat. Cell Biol. 7 (2005) 1007-1013
19. Julien E., and Herr W. A switch in mitotic histone H4 lysine 20 methylation status is linked to M phase defects upon loss of HCF-1. Mol. Cell 14 (2004) 713-725
20. Karachentsev D., Sarma K., Reinberg D., and Steward R. PR-Set7-dependent methylation of histone H4 Lys 20 functions in repression of gene expression and is essential for mitosis. Genes Dev. 19 (2005) 431-435
21. Kim J., Daniel J., Espejo A., Lake A., Krishna M., Xia L., Zhang Y., and Bedford M.T. Tudor, MBT and chromo domains gauge the degree of lysine methylation. EMBO Rep. 7 (2006) 397-403
22. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
23. Kuzmichev A., Nishioka K., Erdjument-Bromage H., Tempst P., and Reinberg D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 16 (2002) 2893-2905
24. Laue K., Daujat S., Crump J.G., Plaster N., Roehl H.H., Kimmel C.B., Schneider R., and Hammerschmidt M. The multidomain protein Brpf1 binds histones and is required for Hox gene expression and segmental identity. Development 135 (2008) 1935-1946
25. Li B., Carey M., and Workman J.L. The role of chromatin during transcription. Cell 128 (2007) 707-719
26. Litt M.D., Simpson M., Gaszner M., Allis C.D., and Felsenfeld G. Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293 (2001) 2453-2455
27. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 (1997) 251-260
28. Martin C., and Zhang Y. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6 (2005) 838-849
29. Maurer-Stroh S., Dickens N.J., Hughes-Davies L., Kouzarides T., Eisenhaber F., and Ponting C.P. The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci. 28 (2003) 69-74
30. Morris S.A., Shibata Y., Noma K., Tsukamoto Y., Warren E., Temple B., Grewal S.I., and Strahl B.D. Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryot. Cell 4 (2005) 1446-1454
31. Muller J., Hart C.M., Francis N.J., Vargas M.L., Sengupta A., Wild B., Miller E.L., O'Connor M.B., Kingston R.E., and Simon J.A. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111 (2002) 197-208
32. Nakamura T.M., Du L.L., Redon C., and Russell P. Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol. Cell. Biol. 24 (2004) 6215-6230
33. Nakayama J., Rice J.C., Strahl B.D., Allis C.D., and Grewal S.I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292 (2001) 110-113
34. Nameki N., Tochio N., Koshiba S., Inoue M., Yabuki T., Aoki M., Seki E., Matsuda T., Fujikura Y., Saito M., et al. Solution structure of the PWWP domain of the hepatoma-derived growth factor family. Protein Sci. 14 (2005) 756-764
35. Nishioka K., Rice J.C., Sarma K., Erdjument-Bromage H., Werner J., Wang Y., Chuikov S., Valenzuela P., Tempst P., Steward R., et al. PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9 (2002) 1201-1213
36. Noma K., Allis C.D., and Grewal S.I. Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293 (2001) 1150-1155
37. Noma K., and Grewal S.I. Histone H3 lysine 4 methylation is mediated by Set1 and promotes maintenance of active chromatin states in fission yeast. Proc. Natl. Acad. Sci. USA 99 Suppl 4 (2002) 16438-16445
38. Qiu C., Sawada K., Zhang X., and Cheng X. The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds. Nat. Struct. Biol. 9 (2002) 217-224
39. Rayasam G.V., Wendling O., Angrand P.O., Mark M., Niederreither K., Song L., Lerouge T., Hager G.L., Chambon P., and Losson R. NSD1 is essential for early post-implantation development and has a catalytically active SET domain. EMBO J. 22 (2003) 3153-3163
40. Rice J.C., Nishioka K., Sarma K., Steward R., Reinberg D., and Allis C.D. Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev. 16 (2002) 2225-2230
41. Rouse J., and Jackson S.P. Interfaces between the detection, signaling, and repair of DNA damage. Science 297 (2002) 547-551
42. Ruthenburg A.J., Allis C.D., and Wysocka J. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25 (2007) 15-30
43. Saka Y., Esashi F., Matsusaka T., Mochida S., and Yanagida M. Damage and replication checkpoint control in fission yeast is ensured by interactions of Crb2, a protein with BRCT motif, with Cut5 and Chk1. Genes Dev. 11 (1997) 3387-3400
44. Sakaguchi A., and Steward R. Aberrant monomethylation of histone H4 lysine 20 activates the DNA damage checkpoint in Drosophila melanogaster. J. Cell Biol. 176 (2007) 155-162
45. Sanders S.L., Portoso M., Mata J., Bahler J., Allshire R.C., and Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119 (2004) 603-614
46. Schotta G., Lachner M., Sarma K., Ebert A., Sengupta R., Reuter G., Reinberg D., and Jenuwein T. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18 (2004) 1251-1262
47. Schotta G., Sengupta R., Kubicek S., Malin S., Kauer M., Callen E., Celeste A., Pagani M., Opravil S., De La Rosa-Velazquez I.A., et al. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 22 (2008) 2048-2061
48. Shi X., Kachirskaia I., Walter K.L., Kuo J.H., Lake A., Davrazou F., Chan S.M., Martin D.G., Fingerman I.M., Briggs S.D., et al. Proteome-wide analysis in Saccharomyces cerevisiae identifies several PHD fingers as novel direct and selective binding modules of histone H3 methylated at either lysine 4 or lysine 36. J. Biol. Chem. 282 (2007) 2450-2455
49. Slater L.M., Allen M.D., and Bycroft M. Structural variation in PWWP domains. J. Mol. Biol. 330 (2003) 571-576
50. Stec I., Nagl S.B., van Ommen G.J., and den Dunnen J.T. The PWWP domain: a potential protein-protein interaction domain in nuclear proteins influencing differentiation?. FEBS Lett. 473 (2000) 1-5
51. Walworth N.C., and Bernards R. rad-dependent response of the chk1-encoded protein kinase at the DNA damage checkpoint. Science 271 (1996) 353-356
52. Wang H., An W., Cao R., Xia L., Erdjument-Bromage H., Chatton B., Tempst P., Roeder R.G., and Zhang Y. mAM facilitates conversion by ESET of dimethyl to trimethyl lysine 9 of histone H3 to cause transcriptional repression. Mol. Cell 12 (2003) 475-487
53. Washburn M.P., Wolters D., and Yates III J.R. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19 (2001) 242-247
54. Wysocka J., Swigut T., Milne T.A., Dou Y., Zhang X., Burlingame A.L., Roeder R.G., Brivanlou A.H., and Allis C.D. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121 (2005) 859-872
55. 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., and Wilson J.R. Specificity and mechanism of the histone methyltransferase Pr-Set7. Genes Dev. 19 (2005) 1444-1454
56. Yang H., Pesavento J.J., Starnes T.W., Cryderman D.E., Wallrath L.L., Kelleher N.L., and Mizzen C.A. Preferential dimethylation of histone H4 lysine 20 by Suv4-20. J. Biol. Chem. 283 (2008) 12085-12092
57. Zhang K., Mosch K., Fischle W., and Grewal S.I. Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat. Struct. Mol. Biol. 15 (2008) 381-388
58. Zhou B.B., and Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 408 (2000) 433-439