Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 32, 2010, Pages 14075-14080

  Lewis, Peter W ^a   Elsaesser, Simon J ^a   Noh, Kyung Min ^a   Stadler, Sonja C ^a   Allis, C David ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Epigenetics; ES cell; Heterochromatin; Histone H3.3

Indexed keywords

ALPHA THALASSEMIA X LINKED MENTAL RETARDATION PROTEIN; DAXX PROTEIN; DNA; HISTONE H3; HISTONE H4; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; ATRX PROTEIN, MOUSE; CARRIER PROTEIN; CHAPERONE; DAXX PROTEIN, MOUSE; HELICASE; HISTONE; MULTIPROTEIN COMPLEX; SIGNAL PEPTIDE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CHROMATIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; TELOMERE; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; EMBRYONIC STEM CELL; HETEROCHROMATIN; METABOLISM; MOUSE; NUCLEOSOME; PHYSIOLOGY; PROTEIN BINDING;

ANIMALS; CARRIER PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; EMBRYONIC STEM CELLS; HETEROCHROMATIN; HISTONE CHAPERONES; HISTONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; NUCLEOSOMES; PROTEIN BINDING; TELOMERE;

METAZOA; MURINAE;

EID: 77956282773     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1008850107     Document Type: Article

References (44)

1. Deal RB, Henikoff JG, Henikoff S (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328(5982):1161-1164.
2. Ng RK, Gurdon JB (2008) Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol 10(1):102-109.
3. Ohsawa R, Adkins M, Tyler J (2009) Epigenetic inheritance of an inducibly nucleosome-depleted promoter and its associated transcriptional state in the apparent absence of transcriptional activators. Epigenetics & Chromatin 2:1-11.
4. Elsaesser SJ, Goldberg AD, Allis CD (2010) New functions for an old variant: No substitute for histone H3.3. Curr Opin Genet Dev 20(2):110-117.
5. Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9(6):1191-1200. (Pubitemid 34722299)
6. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116(1):51-61. (Pubitemid 38156183)
7. Verreault A, Kaufman PD, Kobayashi R, Stillman B (1996) Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87(1):95-104.
8. Ray-Gallet D, et al. (2002) HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol Cell 9(5):1091-1100.
9. Goldberg AD, et al. (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140(5):678-691.
10. Wong L, et al. (2009) Histone H3.3 incorporation provides a unique and functionally essential telomeric chromatin in embryonic stem cells. Genome Res 19:404-414.
11. Jin C, et al. (2009) H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet 41(8):941-945.
12. Mito Y, Henikoff JG, Henikoff S (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315(5817):1408-1411. (Pubitemid 46399549)
13. Tang J, et al. (2004) A novel transcription regulatory complex containing death domain-associated protein and the ATR-X syndrome protein. J Biol Chem 279(19):20369-20377.
14. Xue Y, et al. (2003) The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc Natl Acad Sci USA 100(19):10635-10640.
15. Nan X, et al. (2007) Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc Natl Acad Sci USA 104(8):2709-2714. (Pubitemid 46327944)
16. Gibbons RJ, et al. (2000) Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat Genet 24(4):368-371.
17. Wong LH, et al. (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 20(3):351-360.
18. Whitehouse I, et al. (1999) Nucleosome mobilization catalysed by the yeast SWI/SNF complex. Nature 400(6746):784-787.
19. Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT (1997) ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90(1):145-155. (Pubitemid 28009426)
20. Lusser A, Kadonaga JT (2003) Chromatin remodeling by ATP-dependent molecular machines. Bioessays 25(12):1192-1200.
21. Xue Y, et al. (2003) The ATRX syndrome protein forms a chromatin-remodeling complex with Daxx and localizes in promyelocytic leukemia nuclear bodies. Proc Natl Acad Sci USA 100(19):10635-10640.
22. Emelyanov AV, Konev AY, Vershilova E, Fyodorov DV (2010) Protein complex of Drosophila ATRX/XNP and HP1a is required for the formation of pericentric beta-heterochromatin in vivo. J Biol Chem 285(20):15027-15037.
23. Michaelson JS, Bader D, Kuo F, Kozak C, Leder P (1999) Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development. Genes Dev 13(15):1918-1923. (Pubitemid 29407359)
24. Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev In Press.
25. Alexeev AMazin AKowalczykowski SC (2003) Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat Struct Biol 10(3):182-186.
26. Zhang Z, Fan HY, Goldman JA, Kingston RE (2007) Homology-driven chromatin remodeling by human RAD54. Nat Struct Mol Biol 14(5):397-405.
27. Hake SB, et al. (2005) Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes. Proc Natl Acad Sci USA 102(18):6344-6349.
28. Baumann C, Schmidtmann A, Muegge K, De La Fuente R (2008) Association of ATRX with pericentric heterochromatin and the Y chromosome of neonatal mouse spermatogonia. BMC Mol Biol 9(29):1-18.
29. Baumann C, De La Fuente R (2009) ATRX marks the inactive X chromosome (Xi) in somatic cells and during imprinted X chromosome inactivation in trophoblast stem cells. Chromosoma 118(2):209-222.
30. De La Fuente R, Viveiros MM, Wigglesworth K, Eppig JJ (2004) ATRX, a member of the SNF2 family of helicase/ATPases, is required for chromosome alignment and meiotic spindle organization in metaphase II stage mouse oocytes. Dev Biol 272(1):1-14. (Pubitemid 38887280)
31. Ritchie K, et al. (2008) Loss of ATRX leads to chromosome cohesion and congression defects. J Cell Biol 180(2):315-324.
32. Bassett AR, Cooper SE, Ragab A, Travers AA (2008) The chromatin remodelling factor dATRX is involved in heterochromatin formation. PLoS One 3(5):e2099.
33. Schneiderman JI, Sakai A, Goldstein S, Ahmad K (2009) The XNP remodeler targets dynamic chromatin in Drosophila. Proc Natl Acad Sci USA 106(34):14472-14477.
34. Luke B, Lingner J (2009) TERRA: Telomeric repeat-containing RNA. EMBO J 28(17):2503-2510.
35. Zaratiegui M, Irvine DV, Martienssen RA (2007) Noncoding RNAs and gene silencing. Cell 128(4):763-776.
36. Maison C, et al. (2002) Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 30(3):329-334.
37. Cacchione S, Cerone MA, Savino M (1997) In vitro low propensity to form nucleosomes of four telomeric sequences. FEBS Lett 400(1):37-41.
38. Ooi SKT, et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448(7154):714-717.
39. Otani J, et al. (2009) Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep 10(11):1235-1241.
40. Schoeftner S, Blasco MA (2009) A 'higher order' of telomere regulation: Telomere heterochromatin and telomeric RNAs. EMBO J 28(16):2323-2336.
41. Lehnertz B, et al. (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13(14):1192-1200.
42. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T, Blasco MA (2004) Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 36(1):94-99. (Pubitemid 38056214)
43. Jin C, Felsenfeld G (2007) Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21(12):1519-1529.
44. Tamura T, et al. (2009) Inducible deposition of the histone variant H3.3 in interferon-stimulated genes. J Biol Chem 284(18):12217-12225.