The Histone-Fold Protein CHRAC14 Influences Chromatin Composition in Response to DNA Damage

Cell Reports

Volumn 7, Issue 2, 2014, Pages 321-330

  Mathew, Veena ^a   Pauleau, Anne Laure ^a   Steffen, Natascha ^b   Bergner, Andrea ^a   Becker, PeterB ^b   Erhardt, Sylvia ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CHRAC14 PROTEIN; HISTONE; HISTONE H3; UNCLASSIFIED DRUG; AUTOANTIGEN; CHRAC-14 PROTEIN, DROSOPHILA; CHROMATIN; DROSOPHILA PROTEIN; NONHISTONE PROTEIN; NUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; CENTROMERE; CHROMATIN; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DROSOPHILA; G2 PHASE CELL CYCLE CHECKPOINT; GENOMIC INSTABILITY; GENOTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; GENETICS; METABOLISM;

ANIMALS; AUTOANTIGENS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; DNA REPAIR; DROSOPHILA; DROSOPHILA PROTEINS; G2 PHASE CELL CYCLE CHECKPOINTS; GENOMIC INSTABILITY; KINETOCHORES; NUCLEOPROTEINS;

EID: 84899655092     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.008     Document Type: Article

References (41)

1. Allshire R.C., Karpen G.H. Epigenetic regulation of centromeric chromatin: old dogs, new tricks?. Nat. Rev. Genet. 2008, 9:923-937.
2. Blower M.D., Daigle T., Kaufman T., Karpen G.H. Drosophila CENP-A mutations cause a BubR1-dependent early mitotic delay without normal localization of kinetochore components. PLoS Genet. 2006, 2:e110.
3. Bolte S., Cordelières F.P. A guided tour into subcellular colocalization analysis in light microscopy. J.Microsc. 2006, 224:213-232.
4. Burger R.M., Peisach J., Horwitz S.B. Stoichiometry of DNA strand scission and aldehyde formation by bleomycin. J.Biol. Chem. 1982, 257:8612-8614.
5. Burrack L.S., Berman J. Neocentromeres and epigenetically inherited features of centromeres. Chromosome Res. 2012, 20:607-619.
6. Celli G.B., Denchi E.L., de Lange T. Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol. 2006, 8:885-890.
7. Cenci G., Siriaco G., Raffa G.D., Kellum R., Gatti M. The Drosophila HOAP protein is required for telomere capping. Nat. Cell Biol. 2003, 5:82-84.
8. Corona D.F., Eberharter A., Budde A., Deuring R., Ferrari S., Varga-Weisz P., Wilm M., Tamkun J., Becker P.B. Two histone fold proteins, CHRAC-14 and CHRAC-16, are developmentally regulated subunits of chromatin accessibility complex (CHRAC). EMBO J. 2000, 19:3049-3059.
9. Eberharter A., Ferrari S., Längst G., Straub T., Imhof A., Varga-Weisz P., Wilm M., Becker P.B. Acf1, the largest subunit of CHRAC, regulates ISWI-induced nucleosome remodelling. EMBO J. 2001, 20:3781-3788.
10. Gao G., Walser J.C., Beaucher M.L., Morciano P., Wesolowska N., Chen J., Rong Y.S. HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner. EMBO J. 2010, 29:819-829.
11. Hartlepp K.F., Fernández-Tornero C., Eberharter A., Grüne T., Müller C.W., Becker P.B. The histone fold subunits of Drosophila CHRAC facilitate nucleosome sliding through dynamic DNA interactions. Mol. Cell. Biol. 2005, 25:9886-9896.
12. Helfricht A., Wiegant W.W., Thijssen P.E., Vertegaal A.C., Luijsterburg M.S., van Attikum H. Remodeling and spacing factor 1 (RSF1) deposits centromere proteins at DNA double-strand breaks to promote non-homologous end-joining. Cell Cycle 2013, 12:3070-3082.
13. Heun P., Erhardt S., Blower M.D., Weiss S., Skora A.D., Karpen G.H. Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell 2006, 10:303-315.
14. Iida T., Araki H. Noncompetitive counteractions of DNA polymerase epsilon and ISW2/yCHRAC for epigenetic inheritance of telomere position effect in Saccharomyces cerevisiae. Mol. Cell. Biol. 2004, 24:217-227.
15. Ito T., Bulger M., Pazin M.J., Kobayashi R., Kadonaga J.T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 1997, 90:145-155.
16. Kops G.J., Weaver B.A., Cleveland D.W. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 2005, 5:773-785.
17. Kukimoto I., Elderkin S., Grimaldi M., Oelgeschläger T., Varga-Weisz P.D. The histone-fold protein complex CHRAC-15/17 enhances nucleosome sliding and assembly mediated by ACF. Mol. Cell 2004, 13:265-277.
18. Kusch T., Florens L., Macdonald W.H., Swanson S.K., Glaser R.L., Yates J.R., Abmayr S.M., Washburn M.P., Workman J.L. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 2004, 306:2084-2087.
19. Lan L., Ui A., Nakajima S., Hatakeyama K., Hoshi M., Watanabe R., Janicki S.M., Ogiwara H., Kohno T., Kanno S., Yasui A. The ACF1 complex is required for DNA double-strand break repair in human cells. Mol. Cell 2010, 40:976-987.
20. Li Y., Pursell Z.F., Linn S. Identification and cloning of two histone fold motif-containing subunits of HeLa DNA polymerase epsilon. J.Biol. Chem. 2000, 275:23247-23252.
21. Madigan J.P., Chotkowski H.L., Glaser R.L. DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. Nucleic Acids Res. 2002, 30:3698-3705.
22. Morel F., Renoux M., Lachaume P., Alziari S. Bleomycin-induced double-strand breaks in mitochondrial DNA of Drosophila cells are repaired. Mutat. Res. 2008, 637:111-117.
23. Moreno-Moreno O., Torras-Llort M., Azorín F. Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res. 2006, 34:6247-6255.
24. Moreno-Moreno O., Medina-Giró S., Torras-Llort M., Azorín F. The F box protein partner of paired regulates stability of Drosophila centromeric histone H3, CenH3(CID). Curr. Biol. 2011, 21:1488-1493.
25. Nakayama M., Maruyama S., Kanda H., Ohkita N., Nakano K., Ito F., Kawasaki K. Relationships of Drosophila melanogaster RECQ5/QE to cell-cycle progression and DNA damage. FEBS Lett. 2006, 580:6938-6942.
26. Nishino T., Takeuchi K., Gascoigne K.E., Suzuki A., Hori T., Oyama T., Morikawa K., Cheeseman I.M., Fukagawa T. CENP-T-W-S-X forms aunique centromeric chromatin structure with a histone-like fold. Cell 2012, 148:487-501.
27. Olive P.L., Banáth J.P. The comet assay: a method to measure DNA damage in individual cells. Nat. Protoc. 2006, 1:23-29.
28. Osley M.A., Tsukuda T., Nickoloff J.A. ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat. Res. 2007, 618:65-80.
29. Poot R.A., Dellaire G., Hülsmann B.B., Grimaldi M.A., Corona D.F., Becker P.B., Bickmore W.A., Varga-Weisz P.D. HuCHRAC, a human ISWI chromatin remodelling complex contains hACF1 and two novel histone-fold proteins. EMBO J. 2000, 19:3377-3387.
30. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J.Biol. Chem. 1998, 273:5858-5868.
31. Sánchez-Molina S., Mortusewicz O., Bieber B., Auer S., Eckey M., Leonhardt H., Friedl A.A., Becker P.B. Role for hACF1 in the G2/M damage checkpoint. Nucleic Acids Res. 2011, 39:8445-8456.
32. Schuh M., Lehner C.F., Heidmann S. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 2007, 17:237-243.
33. Schwartz J.L. Monofunctional alkylating agent-induced S-phase-dependent DNA damage. Mutat. Res. 1989, 216:111-118.
34. Soria G., Polo S.E., Almouzni G. Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol. Cell 2012, 46:722-734.
35. Stellfox M.E., Bailey A.O., Foltz D.R. Putting CENP-A in its place. Cell. Mol. Life Sci. 2013, 70:387-406.
36. Suganuma T., Gutiérrez J.L., Li B., Florens L., Swanson S.K., Washburn M.P., Abmayr S.M., Workman J.L. ATAC is a double histone acetyltransferase complex that stimulates nucleosome sliding. Nat. Struct. Mol. Biol. 2008, 15:364-372.
37. Sullivan B., Karpen G. Centromere identity in Drosophila is not determined invivo by replication timing. J.Cell Biol. 2001, 154:683-690.
38. Tercero J.A., Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 2001, 412:553-557.
39. Varga-Weisz P.D., Wilm M., Bonte E., Dumas K., Mann M., Becker P.B. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 1997, 388:598-602.
40. Zeitlin S.G., Patel S., Kavli B., Slupphaug G. Xenopus CENP-A assembly into chromatin requires base excision repair proteins. DNA Repair (Amst.) 2005, 4:760-772.
41. Zeitlin S.G., Baker N.M., Chapados B.R., Soutoglou E., Wang J.Y., Berns M.W., Cleveland D.W. Double-strand DNA breaks recruit the centromeric histone CENP-A. Proc. Natl. Acad. Sci. USA 2009, 106:15762-15767.