Histone chaperone Anp32e removes H2A.Z from DNA double-strand breaks and promotes nucleosome reorganization and DNA repair

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

Volumn 112, Issue 24, 2015, Pages 7507-7512

  Gursoy Yuzugullu, Ozge ^a   Ayrapetov, Marina K ^a   Price, Brendan D ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anp32e; DSB repair; Genome instability; H2A.Z; NHEJ

Indexed keywords

CHAPERONE; HISTONE CHAPERONE ANP32E; HISTONE H2AZ; HISTONE H4; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; ANP32E PROTEIN, HUMAN; CARRIER PROTEIN; HISTONE; HISTONE H2A.F-Z; NUCLEAR PROTEIN; NUCLEOSOME; PHOSPHOPROTEIN; RBBP8 PROTEIN, HUMAN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HISTONE ACETYLATION; HOMOLOGOUS RECOMBINATION; HUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN CONFORMATION; ACETYLATION; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MOLECULAR GENETICS; PROTEIN DOMAIN;

ACETYLATION; AMINO ACID SEQUENCE; CARRIER PROTEINS; CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA REPAIR; HEK293 CELLS; HELA CELLS; HISTONE CHAPERONES; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; NUCLEOSOMES; PHOSPHOPROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84935852240     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504868112     Document Type: Article

References (51)

1. Ciccia A, Elledge SJ (2010) The DNA damage response: Making it safe to play with knives. Mol Cell 40(2):179-204.
2. Bonner WM, et al. (2008) GammaH2AX and cancer. Nat Rev Cancer 8(12):957-967.
3. Matsuoka S, et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316(5828):1160-1166.
4. Mattiroli F, et al. (2012) RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150(6):1182-1195.
5. Xu Y, et al. (2010) The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J Cell Biol 191(1):31-43.
6. Fradet-Turcotte A, et al. (2013) 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499(7456):50-54.
7. Jackson SP, Durocher D (2013) Regulation of DNA damage responses by ubiquitin and SUMO. Mol Cell 49(5):795-807.
8. Fnu S, et al. (2011) Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc Natl Acad Sci USA 108(2):540-545.
9. Pai CC, et al. (2014) A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice. Nat Commun 5:4091.
10. Ayrapetov MK, Gursoy-Yuzugullu O, Xu C, Xu Y, Price BD (2014) DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc Natl Acad Sci USA 111(25):9169-9174.
11. Sun Y, et al. (2009) Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat Cell Biol 11(11):1376-1382.
12. Sun Y, Jiang X, Chen S, Fernandes N, Price BD (2005) A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci USA 102(37):13182-13187.
13. Xu Y, et al. (2012) Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol Cell 48(5):723-733.
14. Murr R, et al. (2006) Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 8(1):91-99.
15. Downs JA, et al. (2004) Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 16(6):979-990.
16. Price BD, D'Andrea AD (2013) Chromatin remodeling at DNA double-strand breaks. Cell 152(6):1344-1354.
17. Nishibuchi I, et al. (2014) Reorganization of damaged chromatin by the exchange of histone variant H2A.Z-2. Int J Radiat Oncol Biol Phys 89(4):736-744.
18. Morillo-Huesca M, Clemente-Ruiz M, Andújar E, Prado F (2010) The SWR1 histone replacement complex causes genetic instability and genome-wide transcription misregulation in the absence of H2A.Z. PLoS ONE 5(8):e12143.
19. Papamichos-Chronakis M, Watanabe S, Rando OJ, Peterson CL (2011) Global regulation of H2A.Z localization by the INO80 chromatin-remodeling enzyme is essential for genome integrity. Cell 144(2):200-213.
20. Obri A, et al. (2014) ANP32E is a histone chaperone that removes H2A.Z from chromatin. Nature 505(7485):648-653.
21. Mao Z, et al. (2014) Anp32e, a higher eukaryotic histone chaperone directs preferential recognition for H2A.Z. Cell Res 24(4):389-399.
22. Wyrick JJ, Kyriss MN, Davis WB (2012) Ascending the nucleosome face: Recognition and function of structured domains in the histone H2A-H2B dimer. Biochim Biophys Acta 1819(8):892-901.
23. Potoyan DA, Papoian GA (2012) Regulation of the H4 tail binding and folding landscapes via Lys-16 acetylation. Proc Natl Acad Sci USA 109(44):17857-17862.
24. Sinha D, Shogren-Knaak MA (2010) Role of direct interactions between the histone H4 Tail and the H2A core in long range nucleosome contacts. J Biol Chem 285(22):16572-16581.
25. Zhou J, Fan JY, Rangasamy D, Tremethick DJ (2007) The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat Struct Mol Biol 14(11):1070-1076.
26. Shogren-Knaak M, et al. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311(5762):844-847.
27. Kalashnikova AA, Porter-Goff ME, Muthurajan UM, Luger K, Hansen JC (2013) The role of the nucleosome acidic patch in modulating higher order chromatin structure. J R Soc Interface 10(82):20121022.
28. Luger K, Dechassa ML, Tremethick DJ (2012) New insights into nucleosome and chromatin structure: An ordered state or a disordered affair? Nat Rev Mol Cell Biol 13(7):436-447.
29. Zlatanova J, Thakar A (2008) H2A.Z: View from the top. Structure 16(2):166-179.
30. Barbera AJ, et al. (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311(5762):856-861.
31. Chodaparambil JV, et al. (2007) A charged and contoured surface on the nucleosome regulates chromatin compaction. Nat Struct Mol Biol 14(11):1105-1107.
32. Bennardo N, Cheng A, Huang N, Stark JM (2008) Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 4(6):e1000110.
33. Lee-Theilen M, Matthews AJ, Kelly D, Zheng S, Chaudhuri J (2011) CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat Struct Mol Biol 18(1):75-79.
34. Weber CM, Henikoff JG, Henikoff S (2010) H2A.Z nucleosomes enriched over active genes are homotypic. Nat Struct Mol Biol 17(12):1500-1507.
35. Henikoff S, Henikoff JG, Sakai A, Loeb GB, Ahmad K (2009) Genome-wide profiling of salt fractions maps physical properties of chromatin. Genome Res 19(3):460-469.
36. Jin C, Felsenfeld G (2007) Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21(12):1519-1529.
37. Zhang H, Roberts DN, Cairns BR (2005) Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123(2):219-231.
38. Park YJ, Dyer PN, Tremethick DJ, Luger K (2004) A new fluorescence resonance energy transfer approach demonstrates that the histone variant H2AZ stabilizes the histone octamer within the nucleosome. J Biol Chem 279(23):24274-24282.
39. Fan JY, Rangasamy D, Luger K, Tremethick DJ (2004) H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol Cell 16(4):655-661.
40. Chou DM, et al. (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc Natl Acad Sci USA 107(43):18475-18480.
41. Luijsterburg MS, et al. (2009) Heterochromatin protein 1 is recruited to various types of DNA damage. J Cell Biol 185(4):577-586.
42. Baldeyron C, Soria G, Roche D, Cook AJ, Almouzni G (2011) HP1alpha recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J Cell Biol 193(1):81-95.
43. Goldstein M, Derheimer FA, Tait-Mulder J, Kastan MB (2013) Nucleolin mediates nucleosome disruption critical for DNA double-strand break repair. Proc Natl Acad Sci USA 110(42):16874-16879.
44. Chen H, Symington LS (2013) Overcoming the chromatin barrier to end resection. Cell Res 23(3):317-319.
45. Adkins NL, Niu H, Sung P, Peterson CL (2013) Nucleosome dynamics regulates DNA processing. Nat Struct Mol Biol 20(7):836-842.
46. Choi J, Heo K, An W (2009) Cooperative action of TIP48 and TIP49 in H2A.Z exchange catalyzed by acetylation of nucleosomal H2A. Nucleic Acids Res 37(18):5993-6007.
47. Conaway RC, Conaway JW (2009) The INO80 chromatin remodeling complex in transcription, replication and repair. Trends Biochem Sci 34(2):71-77.
48. Tang J, et al. (2013) Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 20(3):317-325.
49. Kalocsay M, Hiller NJ, Jentsch S (2009) Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 33(3):335-343.
50. Horigome C, et al. (2014) SWR1 and INO80 chromatin remodelers contribute to DNA double-strand break perinuclear anchorage site choice. Mol Cell 55(4):626-639.
51. Lemaître C, et al. (2014) Nuclear position dictates DNA repair pathway choice. Genes Dev 28(22):2450-2463.