Heterochromatin and ND10 are cell-cycle regulated and phosphorylation-dependent alternate nuclear sites of the transcription repressor Daxx and SWI/SNF protein ATRX

Journal of Cell Science

Volumn 117, Issue 17, 2004, Pages 3807-3820

  Ishov, Alexander M ^a,b   Vladimirova, Olga V ^a   Maul, Gerd G ^a  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

ATRX; Daxx; Heterochromatin; ND10; Nuclear structure; SSRP1

Indexed keywords

CELL PROTEIN; DAXX PROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEIN ATRX; PROTEIN SWI; REPRESSOR PROTEIN; STRUCTURE SPECIFIC RECOGNITION PROTEIN 1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL NUCLEUS; CONTROLLED STUDY; HETEROCHROMATIN; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; TRANSCRIPTION REGULATION;

ANIMALS; ANTIMETABOLITES; BROMODEOXYURIDINE; CARRIER PROTEINS; CELL CYCLE; CELL LINE; CELL NUCLEUS; CELLS, CULTURED; CHROMATIN; DNA HELICASES; G2 PHASE; HETEROCHROMATIN; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RETROVIRIDAE; S PHASE; TIME FACTORS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA;

EID: 4444317361     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01230     Document Type: Article

References (51)

1. Ascoli, C. A. and Maul, G. G. (1991). Idenfification of a novel nuclear domain. J. Cell Biol. 112, 785-795.
2. Berube, N. G., Smeenk, C. A. and Picketts, D. J. (2000). Cell cycle-dependent phosphorylation of the ATRX protein correlates with changes in nuclear matrix and chromatin association. Hum. Mol. Genet. 9, 539-547.
3. Berube, N. G., Jagla, M., Smeenk, C., de Repentigny, Y., Kothary, R. and Picketts, D. J. (2002). Neurodevelopmental defects resulting from ATRX overexpression in transgenic mice. Hum. Mol. Genet. 11, 253-261.
4. Borden, K. L. (2002). Pondering the promyelocytic leukemia protein (PML) puzzle: possible functions for PML nuclear bodies. Mol. Cell. Biol. 22, 5259-5269.
5. Collins, N., Poot, R. A., Kukimoto, I., Garcia-Jimenez, C., Dellaire, G. and Varga-Weisz, P. D. (2002). An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat. Genet. 32, 627-632.
6. Dirks, R. W., Hattinger, C. M., Molenaar, C. and Snaar, S. P. (1999). Synthesis, processing, and transport of RNA within the three-dimensional context of the cell nucleus. Crit. Rev. Eukaryotic Gene Expr. 9, 191-201.
7. Ecsedy, J. A., Michaelson, J. S. and Leder, P. (2003). Homeodomain-interacting protein kinase 1 modulates Daxx localization, phosphorylation, and transcriptional activity. Mol. Cell. Biol. 23, 950-960.
8. Everett, R. D., Earnshaw, W. C., Pluta, A. F., Sternsdorf, T., Ainsztein, A. M., Carmena, M., Ruchaud, S., Hsu, W. and Orr, A. (1999a). A dynamic connection between centromeres and ND10 proteins. J. Cell Sci. 112, 3443-3454.
9. Everett, R. D., Lomonte, P., Sternsdorf, T., van Driel, R. and Orr, A. (1999b). Cell cycle regulation of PML modification and ND10 composition. J. Cell Sci. 112, 4581-4588.
10. Flaus, A. and Owen-Hughes, T. (2001). Mechanisms for ATP-dependent chromatin remodelling. Curr. Opin. Genet. Dev. 11, 148-154.
11. Fuks, F., Hurd, P. J., Wolf, D., Nan, X., Bird, A. P. and Kouzarides, T. (2003). The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278, 4035-4040.
12. Gibbons, R. J., McDowell, T. L., Raman, S., O'Rourke, D. M., Garrick, D., Ayyub, H. and Higgs, D. R. (2000). Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nat. Genet. 24, 368-371.
13. Gibbons, R. J., Pellagatti, A., Garrick, D., Wood, W. G., Malik, N., Ayyub, H., Langford, C., Boultwood, J., Wainscoat, J. S. and Higgs, D. R. (2003). Identification of acquired somatic mutations in the gene encoding chromatin-remodeling factor ATRX in the alpha-thalassemia myelodysplasia syndrome (ATMDS). Nat. Genet. 34, 446-449.
14. Grignani, F., Gelmetti, V., Fanelli, M., Rogaia, D., de Matteis, S., Ferrara, F. F., Bonci, D., Nervi, C. and Pelicci, P. G. (1999). Formation of PML/RAR alpha high molecular weight nuclear complexes through the PML coiled-coil region is essential for the PML/RAR alpha-mediated retinoic acid response. Oncogene 18, 6313-6321.
15. Hendzel, M. J., Wei, Y., Mancini, M. A., van Houser, A., Ranalli, T., Brinkley, B. R., Bazett-Jones, D. P. and Allis, C. D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360.
16. Hertel, L., de Andrea, M., Bellomo, G., Santoro, P., Landolfo, S. and Gariglio, M. (1999). The HMG protein T160 colocalizes with DNA replication foci and is down-regulated during cell differentiation. Exp. Cell Res. 250, 313-328.
17. Hofmann, H., Sindre, H. and Stamminger, T. (2002). Functional interaction between the pp71 protein of human cytomegalovirus and the PML-interacting protein human Daxx. J. Virol. 76, 5769-5783.
18. Hollenbach, A. D., Sublett, J. E., McPherson, C. J. and Grosveld, G. (1999). The Pax3-FKHR oncoprotein is unresponsive to the Pax3-associated repressor hDaxx. EMBO J. 18, 3702-3711.
19. Hollenbach, A. D., McPherson, C. J., Mientjes, E. J., Iyengar, R. and Grosveld, G. (2002). Daxx and histone deacetylase II associate with chromatin through an interaction with core histones and the chromatin-associated protein Dek. J. Cell Sci. 115, 3319-3330.
20. Ishov, A. M. and Maul, G. G. (1996). The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 134, 815-826.
21. Ishov, A. M., Sotnikov, A. G., Negorev, D., Vladimirova, O. V., Neff, N., Kamitani, T., Yeh, E. T., Strauss, J. F., 3rd and Maul, G. G. (1999). PML is critical for ND10 formation and recruits the PML-interacfing protein Daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147, 221-234.
22. Ishov, A. M., Vladimirova, O. V. and Maul, G. G. (2002). Daxx-mediated accumulation of human cytomegalovirus tegument protein pp71 at ND10 facilitates initiation of viral infection at these nuclear domains. J. Virol. 76, 7705-7712.
23. Kawai, T., Akira, S. and Reed, J. C. (2003). ZIP kinase triggers apoptosis from nuclear PML oncogenic domains. Mol. Cell. Biol. 23, 6174-6186.
24. Klochendler-Yeivin, A., Muchardt, C. and Yaniv, M. (2002). SWI/SNF chromatin remodeling and cancer. Curr. Opin. Genet. Dev. 12, 73-79.
25. Krohn, N. M., Stemmer, C., Fojan, P., Grimm, R. and Grasser, K. D. (2003). Protein kinase CK2 phosphorylates the high mobility group domain protein SSRP1, inducing the recognition of UV-damaged DNA. J. Biol. Chem. 278, 12710-12715.
26. Lehembre, F., Muller, S., Pandolfi, P. P. and Dejean, A. (2001). Regulation of Pax3 transcriptional activity by SUMO-1-modified PML. Oncogene 20, 1-9.
27. Lehming, N., le Saux, A., Schuller, J. and Ptashne, M. (1998). Chromatin components as part of a putative transcriptional repressing complex. Proc. Natl. Acad. Sci. USA 95, 7322-7326.
28. Li, H., Leo, C., Zhu, J., Wu, X., O'Neil, J., Park, E. J. and Chen, J. D. (2000). Sequestration and inhibition of Daxx-mediated transcriptional repression by PML. Mol. Cell. Biol. 20, 1784-1796.
29. McDowell, T. L., Gibbons, R. J., Sutherland, H., O'Rourke, D. M., Bickmore, W. A., Pombo, A., Turley, H., Gatter, K., Picketts, D. J., Buckle, V. J. et al. (1999). 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.
30. Mendez, J. and Stillman, B. (2000). Chromatin association of human origin recognition complex, Cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20, 8602-8612.
31. Michaelson, J. S. (2000). The Daxx enigma. Apoptosis 5, 217-220.
32. Michaelson, J. S. and Leder, P. (2003). RNAi reveals anti-apoptotic and transcriptionally repressive activities of Daxx. J. Cell Sci. 116, 345-352.
33. Michaelson, J. S., Bader, D., Kuo, F., Kozak, C. and Leder, P. (1999). Loss of Daxx, a promiscuously interacting protein, results in extensive apoptosis in early mouse development. Genes Dev. 13, 1918-1923.
34. Moen, P. T., Jr, Johnson, C. V., Byron, M., Shopland, L. S., de la Serna, I. L., Imbalzano, A. N. and Lawrence, J. B. (2004). Repositioning of muscle-specific genes relative to the periphery of SC-35 domains during skeletal myogenesis. Mol. Biol. Cell 15, 197-206.
35. Morgenstern, J. P. and Land, H. (1990). Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596.
36. Nakayasu, H. and Berezney, R. (1989). Mapping replicational sites in the eucaryotic cell nucleus. J. Cell Biol. 108, 1-11.
37. 2+ 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. 116, 513-524.
38. Negorev, D. and Maul, G. G. (2001). Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene 20, 7234-7242.
39. Orphanides, G., Wu, W. H., Lane, W. S., Hampsey, M. and Reinberg, D. (1999). The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400, 284-288.
40. Picketts, D. J., Higgs, D. R., Bachoo, S., Blake, D. J., Quarrell, O. W. and Gibbons, R. J. (1996). ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome. Hum. Mol. Genet. 5, 1899-1907.
41. Seeler, J. S., Marchio, A., Sitterlin, D., Transy, C. and Dejean, A. (1998). Interaction of SP100 with HP1 proteins: a link between the promyelocytic leukemia-associated nuclear bodies and the chromatin compartment. Proc. Natl. Acad. Sci. USA 95, 7316-7321.
42. Shopland, L. S., Johnson, C. V., Byron, M., McNeil, J. and Lawrence, J. B. (2003). Clustering of multiple specific genes and gene-rich R-bands around SC-35 domains: evidence for local euchromatic neighborhoods. J. Cell Biol. 162, 981-990.
43. Sutherland, H. G., Mumford, G. K., Newton, K., Ford, L. V., Farrall, R., Dellaire, G., Caceres, J. F. and Bickmore, W. A. (2001). Large-scale identification of mammalian proteins localized to nuclear sub-compartments. Hum. Mol. Genet. 10, 1995-2011.
44. Tang, Q. and Maul, G. G. (2003). Mouse cytomegalovirus immediate-early protein 1 binds with host cell repressors to relieve suppressive effects on viral transcription and replication during lytic infection. J. Virol. 77, 1357-1367.
45. Torii, S., Egan, D. A., Evans, R. A. and Reed, J. C. (1999). Human Daxx regulates Fas-induced apoptosis from nuclear PML oncogenic domains (PODs). EMBO J. 18, 6037-6049.
46. Tsukamoto, T., Hashiguchi, N., Janicki, S. M., Tumbar, T., Belmont, A. S. and Spector, D. L. (2000). Visualization of gene activity in living cells. Nat. Cell Biol. 2, 871-878.
47. Xue, Y., Gibbons, R., Yan, Z., Yang, D., McDowell, T. L., Sechi, S., Qin, J., Zhou, S., Higgs, D. and Wang, W. (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, 10635-10640.
48. Yang, X., Khosravi-Far, R., Chang, H. Y. and Baltimore, D. (1997). Daxx, a novel Fas-binding protein that activates JNK and apoptosis. Cell 89, 1067-1076.
49. Yarnell, A. T., Oh, S., Reinberg, D. and Lippard, S. J. (2001). Interaction of FACT, SSRP1, and the high mobility group (HMG) domain of SSRP1 with DNA damaged by the anticancer drug cisplatin. J. Biol. Chem. 276, 25736-25741.
50. Zeittin, S. G., Barber, C. M., Allis, C. D., Sullivan, K. F. and Sullivan, K. (2001). Differential regulation of CENP-A and histone H3 phosphorylation in G2/M. J. Cell Sci. 114, 653-661.
51. Zhao, T., Heyduk, T. and Eissenberg, J. C. (2001). Phosphorylation site mutations in heterochromatin protein 1 (HP1) reduce or eliminate silencing activity. J. Biol. Chem. 276, 9512-9518.