Dualistic function of Daxx at centromeric and pericentromeric heterochromatin in normal and stress conditions

Nucleus (United States)

Volumn 3, Issue 3, 2012, Pages

  Morozov, Viacheslav M ^a   Gavrilova, Ekaterina V ^a,b,c   Ogryzko, Vasily V ^d   Ishov, Alexander M ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^c INSTITUTE OF CYTOLOGY   (Russian Federation)

^d INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

Centromeres; Daxx; Epigenetic regulation; Heat shock; Heterochromatin; Histone H3.3; ND10; Pericentromeres; PML NBs; Transcription

Indexed keywords

DAXX PROTEIN; HISTONE H3; DAXX PROTEIN, HUMAN; HISTONE; NUCLEAR PROTEIN; RNA; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA;

ARTICLE; CENTROMERE; DNA MODIFICATION; EPIGENETICS; GENOME; HEAT SHOCK; HETEROCHROMATIN; HUMAN; HUMAN CELL; PROTEIN DEPLETION; STRESS; CELL LINE; DRUG ANTAGONISM; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; RNA INTERFERENCE; TEMPERATURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; CENTROMERE; HETEROCHROMATIN; HISTONES; HUMANS; NUCLEAR PROTEINS; RNA; RNA INTERFERENCE; RNA, SMALL INTERFERING; STRESS, PHYSIOLOGICAL; TEMPERATURE;

EID: 84863821039     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.20180     Document Type: Article

References (44)

1. HenikoffS. Conspiracy of silence among repeated transgenes. Bioessays 1998; 20:532-5; PMID:9723001; h t t p://d x. d o i. o r g/1 0. 1 0 0 2/(S I C I) 1 5 2 1-1878(199807)20:7<532::AID-BIES3>3.0. CO;2-M.
2. Warburton PE, Haaf T, Gosden J, Lawson D, Willard HF. Characterization of a chromosome-specific chimpanzee alpha satellite subset: evolutionary relationship to subsets on human chromosomes. Genomics 1996; 33:220-8; PMID:8660971; http://dx.doi.org/10.1006/geno.1996.0187.
3. Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, et al. Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 2007; 17:1146-60; PMID:17623812; http://dx.doi. org/10.1101/gr.6022807.
4. Bergmann JH, Rodríguez MG, Martins NM, Kimura H, Kelly DA, Masumoto H, et al. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 2011; 30:328-40; PMID:21157429; http://dx.doi.org/10.1038/emboj.2010.329.
5. Choo KH. Centromere DNA dynamics: latent centromeres and neocentromere formation. Am J Hum Genet 1997; 61:1225-33; PMID:9399915; http://dx.doi.org/10.1086/301657.
6. Moyzis RK, Albright KL, Bartholdi MF, Cram LS, Deaven LL, Hildebrand CE, et al. Human chromosome-specific repetitive DNA sequences: novel markers for genetic analysis. Chromosoma 1987; 95:375-86; PMID:3677921; http://dx.doi.org/10.1007/BF00333988.
7. Jolly C, Metz A, Govin J, Vigneron M, Turner BM, Khochbin S, et al. Stress-induced transcription of satellite III repeats. J Cell Biol 2004; 164:25-33; PMID:14699086; http://dx.doi.org/10.1083/jcb.200306104.
8. Eymery A, Souchier C, Vourc'h C, Jolly C. Heat shock factor 1 binds to and transcribes satellite II and III sequences at several pericentromeric regions in heat-shocked cells. Exp Cell Res 2010; 316:1845-55; PMID:20152833; http://dx.doi.org/10.1016/j. yexcr.2010.02.002.
9. Lindsay CR, Giovinazzi S, Ishov AM. Daxx is a predominately nuclear protein that does not translocate to the cytoplasm in response to cell stress. Cell Cycle 2009; 8:1544-51; PMID:19372739; http://dx.doi. org/10.4161/cc.8.10.8379.
10. Lindsay CR, Morozov VM, Ishov AM. PML NBs (ND10) and Daxx: from nuclear structure to protein function. Front Biosci 2008; 13:7132-42; PMID:18508722; http://dx.doi.org/10.2741/3216.
11. Ishov AM, Sotnikov AG, Negorev D, Vladimirova OV, NeffN, Kamitani T, et al. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J Cell Biol 1999; 147:221-34; PMID:10525530; http://dx.doi.org/10.1083/jcb.147.2.221.
12. Maul GG, Negorev D, Bell P, Ishov AM. Review: properties and assembly mechanisms of ND10, PML bodies or PODs. J Struct Biol 2000; 129:278-87; PMID:10806078; http://dx.doi.org/10.1006/jsbi.2000.4239.
13. Negorev D, Maul GG. Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene 2001; 20:7234-42; PMID:11704851; http://dx.doi. org/10.1038/sj.onc.1204764.
14. Pluta AF, Earnshaw WC, Goldberg IG. Interphasespecific association of intrinsic centromere protein CENP-C with HDaxx, a death domain-binding protein implicated in Fas-mediated cell death. J Cell Sci 1998; 111:2029-41; PMID:9645950.
15. Ishov AM, Vladimirova OV, Maul GG. Heterochromatin and ND10 are cell cycle regulated and phosphorylation-dependent alternate nuclear sites of the transcription repressor Daxx and SWI/SNF protein ATRX. J Cell Sci 2004; 117:3807-20; PMID:15252119; http://dx.doi.org/10.1242/jcs.01230.
16. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010; 140:678-91; PMID:20211137; http://dx.doi.org/10.1016/j.cell.2010.01.003.
17. 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 2010; 24:1253-65; PMID:20504901; http://dx.doi.org/10.1101/gad.566910.
18. Hake SB, Allis CD. Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis". Proc Natl Acad Sci USA 2006; 103:6428-35; PMID:16571659; http://dx.doi. org/10.1073/pnas.0600803103.
19. Elsaesser SJ, Goldberg AD, Allis CD. New functions for an old variant: no substitute for histone H3.3. Curr Opin Genet Dev 2010; 20:110-7; PMID:20153629; http://dx.doi.org/10.1016/j.gde.2010.01.003.
20. Szenker E, Ray-Gallet D, Almouzni G. The double face of the histone variant H3.3. Cell Res 2011; 21:421-34; PMID:21263457; http://dx.doi.org/10.1038/cr.2011.14.
21. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004; 116:51-61; PMID:14718166; http://dx.doi.org/10.1016/S0092-8674(03)01064-X.
22. Maul GG, Yu E, Ishov AM, Epstein AL. Nuclear domain 10 (ND10) associated proteins are also present in nuclear bodies and redistribute to hundreds of nuclear sites after stress. J Cell Biochem 1995; 59:498-513; PMID:8749719; http://dx.doi.org/10.1002/jcb.240590410.
23. Nefkens I, Negorev DG, Ishov AM, Michaelson JS, Yeh ET, Tanguay RM, et al. Heat shock and Cd2+ exposure regulate PML and Daxx release from ND10 by independent mechanisms that modify the induction of heat-shock proteins 70 and 25 differently. J Cell Sci 2003; 116:513-24; PMID:12508112; http://dx.doi. org/10.1242/jcs.00253.
24. Hollenbach AD, Sublett JE, McPherson CJ, Grosveld G. The Pax3-FKHR oncoprotein is unresponsive to the Pax3-associated repressor hDaxx. EMBO J 1999; 18:3702-11; PMID:10393185; http://dx.doi. org/10.1093/emboj/18.13.3702.
25. Morozov VM, Massoll NA, Vladimirova OV, Maul GG, Ishov AM. Regulation of c-met expression by transcription repressor Daxx. Oncogene 2008; 27:2177-86; PMID:17952115; http://dx.doi.org/10.1038/sj.onc.1210865.
26. Boellmann F, Guettouche T, Guo Y, Fenna M, Mnayer L, Voellmy R. DAXX interacts with heat shock factor 1 during stress activation and enhances its transcriptional activity. Proc Natl Acad Sci USA 2004; 101:4100-5; PMID:15016915; http://dx.doi.org/10.1073/pnas.0304768101.
27. Nakatani Y, Ogryzko V. Immunoaffinity purification of mammalian protein complexes. Methods Enzymol 2003; 370:430-44; PMID:14712665; http://dx.doi. org/10.1016/S0076-6879(03)70037-8.
28. Sullivan BA, Karpen GH. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 2004; 11:1076-83; PMID:15475964; http://dx.doi.org/10.1038/nsmb845.
29. Velichko AK, Kantidze OL, Razin SV. HP1α is not necessary for the structural maintenance of centromeric heterochromatin. Epigenetics 2011; 6:380-7; PMID:20962594; http://dx.doi.org/10.4161/epi.6.3.13866.
30. Eymery A, Callanan M, Vourc'h C. The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int J Dev Biol 2009; 53:259-68; PMID:19412885; http://dx.doi.org/10.1387/ijdb.082673ae.
31. Campos EI, Reinberg D. New chaps in the histone chaperone arena. Genes Dev 2010; 24:1334-8; PMID:20595228; http://dx.doi.org/10.1101/gad.1946810.
32. Grewal SI. RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 2010; 20:134-41; PMID:20207534; http://dx.doi. org/10.1016/j.gde.2010.02.003.
33. Rizzi N, Denegri M, Chiodi I, Corioni M, Valgardsdottir R, Cobianchi F, et al. Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock. Mol Biol Cell 2004; 15:543-51; PMID:14617804; http://dx.doi.org/10.1091/mbc.E03-07-0487.
34. Biamonti G, Vourc'h C. Nuclear stress bodies. Cold Spring Harb Perspect Biol 2010; 2:695; PMID:20516127; http://dx.doi.org/10.1101/cshperspect. a000695.
35. Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, Kandels-Lewis S, et al. Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 2008; 14:507-22; PMID:18410728; http://dx.doi.org/10.1016/j.devcel.2008.02.001.
36. Jiao Y, Shi C, Edil BH, de Wilde RF, Klimstra DS, Maitra A, et al. DAXX/ATRX, MEN1 and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011; 331:1199-203; PMID:21252315; http://dx.doi.org/10.1126/science.1200609.
37. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, PfaffE, Jacob K, et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 2012; 482:226-31; PMID:22286061; http://dx.doi.org/10.1038/nature10833.
38. Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, et al. Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 2011; 331:593-6; PMID:21233348; http://dx.doi.org/10.1126/science.1200801.
39. Eymery A, Horard B, El Atifi-Borel M, Fourel G, Berger F, Vitte AL, et al. A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 2009; 37:6340-54; PMID:19720732; http://dx.doi.org/10.1093/nar/gkp639.
40. Lindsay CR, Scholz A, Morozov VM, Ishov AM. Daxx shortens mitotic arrest caused by paclitaxel. Cell Cycle 2007; 6:1200-4; PMID:17471023; http://dx.doi.org/10.4161/cc.6.10.4244.
41. Blower MD, Sullivan BA, Karpen GH. Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2002; 2:319-30; PMID:11879637; http://dx.doi.org/10.1016/S1534-5807(02)00135-1.
42. Zinchuk V, Zinchuk O, Okada T. Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem 2007; 40:101-11; PMID:17898874; http://dx.doi. org/10.1267/ahc.07002.
43. Crusselle-Davis VJ, Zhou Z, Anantharaman A, Moghimi B, Dodev T, Huang S, et al. Recruitment of coregulator complexes to the beta-globin gene locus by TFII-I and upstream stimulatory factor. FEBS J 2007; 274:6065-73; PMID:17970752; http://dx.doi. org/10.1111/j.1742-4658.2007.06128.x.
44. Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C, Cmarko D, et al. Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res 2002; 276:10-23; PMID:11978004; http://dx.doi. org/10.1006/excr.2002.5513.