ATRX ADD domain links an atypical histone methylation recognition mechanism to human mental-retardation syndrome

Nature Structural and Molecular Biology

Volumn 18, Issue 7, 2011, Pages 769-776

  Iwase, Shigeki ^a   Xiang, Bin ^b,c   Ghosh, Sharmistha ^d   Ren, Ting ^a   Lewis, Peter W ^e   Cochrane, Jesse C ^f   Allis, C David ^e   Picketts, David J ^g   Patel, Dinshaw J ^h   Li, Haitao ^b,c   Shi, Yang ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b TSINGHUA UNIVERSITY   (China)

^c Tsinghua University   (China)

^d HARVARD MEDICAL SCHOOL   (United States)

^e ROCKEFELLER UNIVERSITY   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^h MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; HISTONE H3; LYSINE; NUCLEAR PROTEIN; PROTEIN ATRX ADD; UNCLASSIFIED DRUG;

ALPHA THALASSEMIA; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CRYSTAL STRUCTURE; HETEROCHROMATIN; HISTONE METHYLATION; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; X LINKED MENTAL RETARDATION;

AMINO ACID SEQUENCE; BINDING SITES; DNA HELICASES; HETEROCHROMATIN; HISTONES; HUMANS; INTELLECTUAL DISABILITY; METHYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 79960050537     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2062     Document Type: Article

References (55)

1. Li, H. et al. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442, 91-95 (2006). (Pubitemid 44064215)
2. Wysocka, J. et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442, 86-90 (2006). (Pubitemid 44064214)
3. Shi, X. et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442, 96-99 (2006). (Pubitemid 44064216)
4. Peña, P.V. et al. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442, 100-103 (2006). (Pubitemid 44064217)
5. Bannister, A.J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124 (2001). (Pubitemid 32225848)
6. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120 (2001). (Pubitemid 32225847)
7. Berger, S.L. The complex language of chromatin regulation during transcription. Nature 447, 407-412 (2007). (Pubitemid 46816746)
8. van Bokhoven, H. & Kramer, J.M. Disruption of the epigenetic code: an emerging mechanism in mental retardation. Neurobiol. Dis. 39, 3-12 (2010).
9. Iwase, S. & Shi, Y. Histone and DNA modifications in mental retardation. Prog. Drug Res. 67, 147-173 (2011).
10. Ropers, H.H. & Hamel, B.C. X-linked mental retardation. Nat. Rev. Genet. 6, 46-57 (2005). (Pubitemid 39657897)
11. Gibbons, R.J., Picketts, D.J., Villard, L. & Higgs, D.R. Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell 80, 837-845 (1995).
12. Gibbons, R. Alpha thalassaemia-mental retardation, X linked. Orphanet J. Rare Dis. 1, 15 (2006).
13. Gibbons, R.J. et al. Mutations in the chromatin-associated protein ATRX. Hum. Mutat. 29, 796-802 (2008). (Pubitemid 351794130)
14. Tang, J. et al. A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J. Biol. Chem. 279, 20369-20377 (2004). (Pubitemid 38623483)
15. Ooi, S.K. et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717 (2007). (Pubitemid 47236857)
16. Otani, J. et al. Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep. 10, 1235-1241 (2009).
17. Zhang, Y. et al. Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res. 38, 4246-4253 (2010).
18. Goldberg, A.D. et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691 (2010).
19. McDowell, T.L. et al. Localization of a putative transcriptional regulator (ATRX) at pericentromeric heterochromatin and the short arms of acrocentric chromosomes. Proc. Natl. Acad. Sci. USA 96, 13983-13988 (1999).
20. Allshire, R.C. & Karpen, G.H. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9, 923-937 (2008). (Pubitemid 50329068)
21. Pidoux, A.L. & Allshire, R.C. The role of heterochromatin in centromere function. Phil. Trans. R. Soc. Lond. B 360, 569-579 (2005). (Pubitemid 41529654)
22. Sullivan, B.A. & Karpen, G.H. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat. Struct. Mol. Biol. 11, 1076-1083 (2004). (Pubitemid 39453336)
23. Martens, J.H. et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812 (2005). (Pubitemid 40396109)
24. Rea, S. et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-599 (2000). (Pubitemid 30641039)
25. O'Carroll, D. et al. Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Mol. Cell. Biol. 20, 9423-9433 (2000). (Pubitemid 32246126)
26. Rice, J.C. et al. Histone methyltransferases direct different degrees of methylation to define distinct chromatin domains. Mol. Cell 12, 1591-1598 (2003). (Pubitemid 38037025)
27. Nan, X. et al. Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc. Natl. Acad. Sci. USA 104, 2709-2714 (2007). (Pubitemid 46327944)
28. Lechner, M.S., Schultz, D.C., Negorev, D., Maul, G.G. & Rauscher, F.J. III. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem. Biophys. Res. Commun. 331, 929-937 (2005). (Pubitemid 40692450)
29. Bérubé, N.G., Smeenk, C.A. & Picketts, D.J. Cell cycle-dependent phosphorylation of the ATRX protein correlates with changes in nuclear matrix and chromatin association. Hum. Mol. Genet. 9, 539-547 (2000). (Pubitemid 30154012)
30. Xue, Y. et al. The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc. Natl. Acad. Sci. USA 100, 10635-10640 (2003). (Pubitemid 37140081)
31. Taverna, S.D., Li, H., Ruthenburg, A.J., Allis, C.D. & Patel, D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 14, 1025-1040 (2007). (Pubitemid 350060344)
32. Maurer-Stroh, S. et al. The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci. 28, 69-74 (2003). (Pubitemid 36165134)
33. Collins, R.E. et al. The ankyrin repeats of G9a and GLP histone methyltransferases are mono- and dimethyllysine binding modules. Nat. Struct. Mol. Biol. 15, 245-250 (2008). (Pubitemid 351654039)
34. Jacobs, S.A. et al. Specificity of the HP1 chromo domain for the methylated N-terminus of histone H3. EMBO J. 20, 5232-5241 (2001). (Pubitemid 32910917)
35. Schalch, T. et al. High-affinity binding of Chp1 chromodomain to K9 methylated histone H3 is required to establish centromeric heterochromatin. Mol. Cell 34, 36-46 (2009).
36. Fischle, W. et al. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev. 17, 1870-1881 (2003). (Pubitemid 36944564)
37. Argentaro, A. et al. Structural consequences of disease-causing mutations in the ATRX-DNMT3-DNMT3L (ADD) domain of the chromatin-associated protein ATRX. Proc. Natl. Acad. Sci. USA 104, 11939-11944 (2007). (Pubitemid 47185609)
38. Allshire, R.C., Nimmo, E.R., Ekwall, K., Javerzat, J.P. & Cranston, G. Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev. 9, 218-233 (1995).
39. Guenatri, M., Bailly, D., Maison, C. & Almouzni, G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 166, 493-505 (2004). (Pubitemid 39097169)
40. Ritchie, K. et al. Loss of ATRX leads to chromosome cohesion and congression defects. J. Cell Biol. 180, 315-324 (2008). (Pubitemid 351185918)
41. Bérubé, N.G. et al. The chromatin-remodeling protein ATRX is critical for neuronal survival during corticogenesis. J. Clin. Invest. 115, 258-267 (2005). (Pubitemid 40385468)
42. Chen, T. et al. Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat. Genet. 39, 391-396 (2007). (Pubitemid 46328497)
43. Ha, G.H. et al. Mitotic catastrophe is the predominant response to histone acetyltransferase depletion. Cell Death Differ. 16, 483-497 (2009).
44. Wong, L.H. et al. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 20, 351-360 (2010).
45. Lewis, P.W., Elsaesser, S.J., Noh, K.M., Stadler, S.C. & Allis, C.D. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. USA 107, 14075-14080 (2010).
46. Drané, P., Ouararhni, K., Depaux, A., Shuaib, M. & Hamiche, A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 24, 1253-1265 (2010).
47. Zeng, L. et al. Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466, 258-262 (2010).
48. Tsai, W.-W. TRIM24 links recognition of a non-canonical histone signature to breast cancer. Nature 468, 927-932 (2010).
49. Schnitzler, G.R. Isolation of histones and nucleosome cores from mammalian cells. Curr. Protoc. Mol. Biol. 21, 21.5.1-21.5.12 (2001).
50. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
51. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
52. Vagin, A. & Teplyakov, A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (1997). (Pubitemid 127485985)
53. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
54. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)
55. Iwase, S. et al. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128, 1077-1088 (2007). (Pubitemid 46437259)