HP1 proteins are essential for a dynamic nuclear response that rescues the function of perturbed heterochromatin in primary human cells

Molecular and Cellular Biology

Volumn 27, Issue 3, 2007, Pages 949-962

  Zhang, Rugang ^a   Liu, Song Tao ^a   Chen, Wei ^a   Bonner, Michael ^a   Pehrson, John ^b   Yen, Timothy J ^a   Adams, Peter D ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHROMOSOME PROTEIN; DNA; HETEROCHROMATIN PROTEIN 1; HISTONE; HISTONE H3; PROTEIN HIRA; PROTEIN MIS12; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; EPIGENETICS; GENETIC CODE; HETEROCHROMATIN; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION;

CELL CYCLE PROTEINS; CELL NUCLEUS; CELLS, CULTURED; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; FIBROBLASTS; HETEROCHROMATIN; HISTONES; HUMANS; HYDROXAMIC ACIDS; MOLECULAR CHAPERONES; PROTEIN TRANSPORT; TRANSCRIPTION FACTORS;

EID: 33846604273     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01639-06     Document Type: Article

References (74)

1. Ahmad, K., and S. Henikoff. 2002. The histone variant h3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9:1191-1200.
2. Arlett, C. F., and S. A. Harcourt. 1980. Survey of radiosensitivity in a variety of human cell strains. Cancer Res. 40:926-932.
3. Bannister, A. J., P. Zegerman, J. F. Partridge, E. A. Miska, J. O. Thomas, R. C. Allshire, and T. Kouzarides. 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120-124.
4. Blackwell, C., K. A. Martin, A. Greenall, A. Pidoux, R. C. Allshire, and S. K. Whitehall. 2004. The Schizosaccharomyces pombe HIRA-like protein Hip1 is required for the periodic expression of histone genes and contributes to the function of complex centromeres. Mol. Cell. Biol. 24:4309-4320.
5. Bosch, A., and P. Suau. 1995. Changes in core histone variant composition in differentiating neurons: the roles of differential turnover and synthesis rates. Eur. J. Cell Biol. 68:220-225.
6. Brown, D. T., S. E. Wellman, and D. B. Sittman. 1985. Changes in the levels of three different classes of histone mRNA during murine erythroleukemia cell differentiation. Mol. Cell. Biol. 5:2879-2886.
7. Cheutin, T., A. J. McNairn, T. Jenuwein, D. M. Gilbert, P. B. Singh, and T. Misteli. 2003. Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299:721-725.
8. Cimini, D., M. Mattiuzzo, L. Torosantucci, and F. Degrassi. 2003. Histone hyperacetylation in mitosis prevents sister chromatid separation and produces chromosome segregation defects. Mol. Biol. Cell 14:3821-3833.
9. Costanzi, C., and J. R. Pehrson. 2001. MACROH2A2, a new member of the MARCOH2A core histone family. J. Biol. Chem. 276:21776-21784.
10. Earnshaw, W., B. Bordwell, C. Marino, and N. Rothfield. 1986. Three human chromosomal autoantigens are recognized by sera from patients with anticentromere antibodies. J. Clin. Investig. 77:426-430.
11. Gilchrist, S., N. Gilbert, P. Perry, and W. A. Bickmore. 2004. Nuclear organization of centromeric domains is not perturbed by inhibition of histone deacetylases. Chromosome Res. 12:505-516.
12. Greenall, A., E. S. Williams, K. A. Martin, J. M. Palmer, J. Gray, C. Liu, and S. K. Whitehall. 2006. Hip3 interacts with the HIRA proteins Hip1 and Slm9 and is required for transcriptional silencing and accurate chromosome segregation. J. Biol. Chem. 281:8732-8739.
13. Grove, G. W., and A. Zweidler. 1984. Regulation of nucleosomal core histone variant levels in differentiating murine erythroleukemia cells. Biochemistry 23:4436-4443.
14. Hake, S. B., B. A. Garcia, E. M. Duncan, M. Kauer, G. Dellaire, J. Shabanowitz, D. P. Bazett-Jones, C. D. Allis, and D. F. Hunt. 2006. Expression patterns and posttranslational modifications associated with mammalian histone H3 variants. J. Biol. Chem. 281:559-568.
15. Hall, C., D. M. Nelson, X. Ye, K. Baker, J. A. DeCaprio, S. Seeholzer, M. Lipinski, and P. D. Adams. 2001. HIRA, the human homologue of yeast Hir1p and Hir2p, is a novel cyclin-cdk2 substrate whose expression blocks S-phase progression. Mol. Cell. Biol. 21:1854-1865.
16. Horowitz-Scherer, R. A., and C. L. Woodcock. 2006. Organization of interphase chromatin. Chromosoma 115:1-14.
17. Ito, A., C. H. Lai, X. Zhao, S. Saito, M. H. Hamilton, E. Appella, and T. P. Yao. 2001. p300/CBP-mediated p53 acetylation is commonly induced by p53-activating agents and inhibited by MDM2. EMBO J. 20:1331-1340.
18. Jacobs, S. A., S. D. Taverna, Y. Zhang, S. D. Briggs, J. Li, J. C. Eissenberg, C. D. Allis, and S. Khorasanizadeh. 2001. Specificity of the HP1 chromo domain for the methylated N terminus of histone H3. EMBO J. 20:5232-5241.
19. Kastan, M. B., and J. Bartek. 2004. Cell-cycle checkpoints and cancer. Nature 432:316-323.
20. Kaufman, P. D., J. L. Cohen, and M. A. Osley. 1998. Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol. Cell. Biol. 18:4793-4806.
21. Krawitz, D. C., T. Kama, and P. D. Kaufman. 2002. Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol. Cell. Biol. 22:614-625.
22. Krimer, D. B., G. Cheng, and A. I. Skoultchi. 1993. Induction of H3.3 replacement histone mRNAs during the precommitment period of murine erythroleukemia cell differentiation. Nucleic Acids Res. 21:2873-2879.
23. Kuo, M. H., J. E. Brownell, R. E. Sobel, T. A. Ranalli, R. G. Cook, D. G. Edmondson, S. Y. Roth, and C. D. Allis. 1996. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 383:269-272.
24. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein. 2001. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116-120.
25. Laird, P. W. 2005. Cancerepigenetics. Hum. Mol. Genet. 14:(Spec. No. 1)R65-R76.
26. Lechner, M. S., G. E. Begg, D. W. Speicher, and F. J. Rauscher III. 2000. Molecular determinants for targeting heterochromatin protein 1-mediated gene silencing: direct chromoshadow domain-KAP-1 corepressor interaction is essential. Mol. Cell. Biol. 20:6449-6465.
27. Li, M. J., M. C. Peakman, E. I. Golub, G. Reddy, D. C. Ward, C. M. Radding, and N. Maizels. 1996. Rad51 expression and localization in B cells carrying out class switch recombination. Proc. Natl. Acad. Sci. USA 93:10222-10227.
28. Loppin, B., E. Bonnefoy, C. Anselme, A. Laurencon, T. L. Karr, and P. Couble. 2005. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386-1390.
29. Loyola, A., and G. Almouzni. 2004. Bromodomains in living cells participate in deciphering the histone code. Trends Cell Biol. 14:279-281.
30. Loyola, A., T. Bonaldi, D. Roche, A. Imhof, and G. Almouzni. 2006. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24:309-316.
31. Maiato, H., J. DeLuca, E. D. Salmon, and W. C. Earnshaw. 2004. The dynamic kinetochore-microtubule interface. J. Cell Sci. 117:5461-5477.
32. Maison, C., D. Bailly, A. H. Peters, J. P. Quivy, D. Roche, A. Taddei, M. Lachner, T. Jenuwein, and G. Almouzni. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329-334.
33. Maser, R. S., K. J. Monsen, B. E. Nelms, and J. H. Petrini. 1997. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell. Biol. 17:6087-6096.
34. McKittrick, E., P. R. Gafken, K. Ahmad, and S. Henikoff. 2004. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 101:1525-1530.
35. Minc, E., Y. Allory, H. J. Worman, J. C. Courvalin, and B. Buendia. 1999. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108:220-234.
36. Mito, Y., J. G. Henikoff, and S. Henikoff. 2005. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 37:1090-1097.
37. Muchardt, C., M. Guilleme, J. S. Seeler, D. Trouche, A. Dejean, and M. Yaniv. 2002. Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1α. EMBO Rep. 3:975-981.
38. Narita, M., S. Nunez, E. Heard, A. W. Lin, S. A. Hearn, D. L. Spector, G. J. Hannon, and S. W. Lowe. 2003. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113:703-716.
39. Nielsen, S. J., R. Schneider, U. M. Bauer, A. J. Bannister, A. Morrison, D. O'Carroll, R. Firestein, M. Cleary, T. Jenuwein, R. E. Herrera, and T. Kouzarides. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412:561-565.
40. Obuse, C., O. Iwasaki, T. Kiyomitsu, G. Goshima, Y. Toyoda, and M. Yanagida. 2004. A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nat. Cell Biol. 6:1135-1141.
41. Ogawa, H., K. Ishiguro, S. Gaubatz, D. M. Livingston, and Y. Nakatani. 2002. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in GO cells. Science 296:1132-1136.
42. Ooi, S. L., J. R. Priess, and S. Henikoff. 2006. Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans. PLoS Genet. 2:e97.
43. Orlando, V., H. Strutt, and R. Paro. 1997. Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205-214.
44. Pantazis, P., and W. M. Bonner. 1984. Specific alterations in the pattern of histone-3 synthesis during conversion of human leukemic cells to terminally differentiated cells in culture. Differentiation 28:186-190.
45. Peart, M. J., G. K. Smyth, R. K. van Laar, D. D. Bowtell, V. M. Richon, P. A. Marks, A. J. Holloway, and R. W. Johnstone. 2005. Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc. Natl. Acad. Sci. USA 102:3697-3702.
46. Phelps-Durr, T. L., J. Thomas, P. Vahab, and M. C. Timmermans. 2005. Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17:2886-2898.
47. Pina, B., and P. Suau. 1987. Changes in histones H2A and H3 variant composition in differentiating and mature rat brain cortical neurons. Dev. Biol. 123:51-58.
48. 2 checkpoint in normal cells that is defective in tumor cells. Mol. Biol. Cell 11:2069-2083.
49. Rangasamy, D., I. Greaves, and D. J. Tremethick. 2004. RNA interference demonstrates a novel role for H2A.Z in chromosome segregation. Nat. Struct. Mol. Biol. 11:650-655.
50. Richards, E. J., and S. C. Elgin. 2002. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108:489-500.
51. Robbins, A. R., S. A. Jablonski, T. J. Yen, K. Yoda, R. Robey, S. E. Bates, and D. L. Sackett. 2005. Inhibitors of histonedeacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 4:717-726.
52. Rogakou, E. P., and K. E. Sekeri-Pataryas. 1999. Histone variants of H2A and H3 families are regulated during in vitro aging in the same manner as during differentiation. Exp. Gerontol. 34:741-754.
53. Roopra, A., R. Qazi, B. Schoenike, T. J. Daley, and J. F. Morrison. 2004. Localized domains of G9a-mediated histone methylation are required for silencing of neuronal genes. Mol. Cell 14:727-738.
54. Rudd, M. K., and H. F. Willard. 2004. Analysis of the centromeric regions of the human genome assembly. Trends Genet. 20:529-533.
55. Saffery, R., D. V. Irvine, B. Griffiths, P. Kalitsis, L. Wordeman, and K. H. Choo. 2000. Human centromeres and neocentromeres show identical distribution patterns of >20 functionally important kinetochore-associated proteins. Hum. Mol. Genet. 9:175-185.
56. Scheppach, W., and F. Weiler. 2004. The butyrate story: old wine in new bottles? Curr. Opin. Clin. Nutr. Metab. Care 7:563-567.
57. Schwartz, B. E., and K. Ahmad. 2005. Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev. 19:804-814.
58. Scully, R., J. Chen, R. L. Ochs, K. Keegan, M. Hoekstra, J. Feunteun, and D. M. Livingston. 1997. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90:425-435.
59. Sharp, J. A., E. T. Fouts, D. C. Krawitz, and P. D. Kaufman. 2001. Yeast histone deposition protein Asf1p requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol. 11:463-473.
60. Sharp, J. A., A. A. Franco, M. A. Osley, P. D. Kaufman, D. C. Krawitz, T. Kama, E. T. Fouts, and J. L. Cohen. 2002. Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in Saccharomyces cerevisiae. Genes Dev. 16:85-100.
61. Sobel, R. E., R. G. Cook, C. A. Perry, A. T. Annunziato, and C. D. Allis. 1995. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. USA 92:1237-1241.
62. Taddei, A., C. Maison, D. Roche, and G. Almouzni. 2001. Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat. Cell Biol. 3:114-120.
63. Tagami, H., D. Ray-Gallet, G. Almouzni, and Y. Nakatani. 2004. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:51-61.
64. Tse, C., T. Sera, A. P. Wolffe, and J. C. Hansen. 1998. Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol. Cell. Biol. 18:4629-4638.
65. Urban, M. K., and A. Zweidler. 1983. Changes in nucleosomal core histone variants during chicken development and maturation. Dev. Biol. 95:421-428.
66. Vakoc, C. R., S. A. Mandat, B. A. Olenchock, and G. A. Blobel. 2005. Histone H3 lysine 9 methylation and HP1γ are associated with transcription elongation through mammalian chromatin. Mol. Cell 19:381-391.
67. Vaziri, H., S. K. Dessain, E. Ng Eaton, S. I. Imai, R. A. Frye, T. K. Pandita, L. Guarente, and R. A. Weinberg. 2001. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107:149-159.
68. Wang, Y., W. Fischle, W. Cheung, S. Jacobs, S. Khorasanizadeh, and C. D. Allis. 2004. Beyond the double helix: writing and reading the histone code. Novartis Found. Symp. 259:3-21, 163-169.
69. Weichselbaum, R. R., J. Nove, and J. B. Little. 1980. X-ray sensitivity of fifty-three human diploid fibroblast cell strains from patients with characterized genetic disorders. Cancer Res. 40:920-925.
70. Wirbelauer, C., O. Bell, and D. Schubeler. 2005. Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev. 19:1761-1766.
71. Wunsch, A. M., and J. Lough. 1987. Modulation of histone H3 variant synthesis during the myoblast-myotube transition of chicken myogenesis. Dev. Biol. 119:94-99.
72. Reference deleted.
73. 2 phases by trichostatin A. Exp. Cell Res. 177:122-131.
74. Zhang, R., M. V. Poustovoitov, X. Ye, H. A. Santos, W. Chen, S. M. Daganzo, J. P. Erzberger, I. G. Serebriiskii, A. A. Canutescu, R. L. Dunbrack, J. R. Pehrson, J. M. Berger, P. D. Kaufman, and P. D. Adams. 2005. Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASFIa and HIRA. Dev. Cell 8:19-30.