Heterochromatin revisited

Nature Reviews Genetics

Volumn 8, Issue 1, 2007, Pages 35-46

  Grewal, Shiv I S ^a   Jia, Songtao ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; GENOMIC DNA; HISTONE DEACETYLASE; HISTONE H3; LYSINE; PROTEIN SWI;

ACETYLATION; ARABIDOPSIS; CENTROMERE; CHICKEN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SEGREGATION; DNA METHYLATION; DNA REPAIR; EMBRYONIC STEM CELL; EPIGENETICS; EUCHROMATIN; GENE EXPRESSION; GENE SILENCING; GENETIC RECOMBINATION; HETEROCHROMATIN; INTERPHASE; MAMMAL; METHYLATION; MOUSE STRAIN; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SUMOYLATION; TRANSPOSON; UBIQUITINATION; X CHROMOSOME;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; CILIOPHORA; EPIGENESIS, GENETIC; HETEROCHROMATIN; HISTONES; MAMMALS; MODELS, GENETIC; PLANTS; RNA INTERFERENCE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCES POMBE;

EID: 33845755946     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg2008     Document Type: Review

References (152)

1. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260 (1997).
2. Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074-1080 (2001).
3. Goll, M. G. & Bestor, T. H. Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74, 481-514 (2005).
4. Kosak, S. T. & Groudine, M. Gene order and dynamic domains. Science 306, 644-647 (2004).
5. Heitz, E. Das heterochromatin der moose. I Jahrb Wiss Botanik 69, 762-818 (1928) (in German).
6. Huisinga, K. L., Brower-Toland, B. & Elgin, S. C. The contradictory definitions of heterochromatin: transcription and silencing. Chromosoma 115, 110-122 (2006).
7. Weiler, K. S. & Wakimoto, B. T. Heterochromatin and gene expression in Drosophila. Annu. Rev. Genet. 29, 577-605 (1995).
8. Birchler, J. A., Bhadra, M. P. & Bhadra, U. Making noise about silence: repression of repeated genes in animals. Curr. Opin. Genet. Dev. 10, 211-216 (2000).
9. Hall, I. M. & Grewal, S. I. in RNAi: A Guide To Gene Silencing (ed. Hannon, G. J.) 205-232 (Cold Spring Harbor Press, Cold Spring Harbor, 2003).
10. Martens, J. H. et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812 (2005).
11. Boumil, R. M. & Lee, J. T. Forty years of decoding the silence in X-chromosome inactivation. Hum. Mol. Genet. 10, 2225-2232 (2001).
12. Henikoff, S. Heterochromatin function in complex genomes. Biochim. Biophys. Acta. 1470, 1-8 (2000).
13. Allshire, R. C., Nimmo, E. R., Ekwall, K., Javerzat, J. P. & Cranston, G. Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev. 9, 218-233 (1995).
14. Kellum, R. & Alberts, B. M. Heterochromatin protein 1 is required for correct chromosome segregation in Drosophila embryos. J. Cell Sci. 108, 1419-1431 (1995).
15. Csink, A. K. & Henikoff, S. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381, 529-531 (1996).
16. Dernburg, A. F. et al. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell 85, 745-759 (1996).
17. Jia, S., Yamada, T. & Grewal, S. I. Heterochromatin regulates cell type-specific long-range chromatin interactions essential for directed recombination. Cell 119, 469-480 (2004). This paper demonstrated a role for heterochromatin in promoting cell-type-specific, long-range spreading of a protein complex that is involved in promoting recombination.
18. Lu, B. Y., Emtage, P. C., Duyf, B. J., Hilliker, A. J. & Eissenberg, J. C. Heterochromatin protein 1 is required for the normal expression of two heterochromatin genes in Drosophila. Genetics 155, 699-708 (2000).
19. Yasuhara, J. C. & Wakimoto, B. T. Oxymoron no more: the expanding world of heterochromatic genes. Trends Genet. 22, 330-338 (2006).
20. Greil, F. et al. Distinct HP1 and Su(var)3-9 complexes bind to sets of developmentally coexpressed genes depending on chromosomal location. Genes Dev. 17, 2825-2838 (2003).
21. Piacentini, L., Fanti, L., Berloco, M., Perrini, B. & Pimpinelli, S. Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin. J. Cell Biol. 161, 707-714 (2003).
22. Cryderman, D. E. et al. Role of Drosophila HP1 in euchromatic gene expression. Dev. Dyn. 232, 767-774 (2005).
23. Vakoc, C. R., Mandat, S. A., Olenchock, B. A. & Blobel, G. A. Histone H3 lysine 9 methylation and HP1γ are associated with transcription elongation through mammalian chromatin. Mol. Cell 19, 381-391 (2005).
24. Zofall, M. & Grewal, S. I. Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol. Cell 22, 681-692 (2006).
25. Maison, C. & Almouzni, G. HP1 and the dynamics of heterochromatin maintenance. Nature Rev. Mol. Cell Biol. 5, 296-304 (2004).
26. Hiragami, K. & Festenstein, R. Heterochromatin protein 1: a pervasive controlling influence. Cell. Mol. Life Sci. 62, 2711-2726 (2005).
27. Cheutin, T. et al. Maintenance of stable heterochromatin domains by dynamic HP1 binding. Science 299, 721-725 (2003).
28. Festenstein, R. et al. Modulation of heterochromatin protein 1 dynamics in primary mammalian cells. Science 299, 719-721 (2003). References 27 and 28 demonstrated that the heterochromatin protein HP1 is highly dynamic, even in heterochromatin domains, which are generally perceived to be highly stable.
29. Cheutin, T., Gorski, S. A., May, K. M., Singh, P. B. & Misteli, T. In vivo dynamics of Swi6 in yeast: evidence for a stochastic model of heterochromatin. Mol. Cell. Biol. 24, 3157-3167 (2004).
30. Grunstein, M. Yeast heterochromatin: regulation of its assembly and inheritance by histones. Cell 93, 325-328 (1998).
31. Nakayama, J., Rice, J. C., Strahl, B. D., Allis, C. D. & Grewal, S. I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292, 110-113 (2001). This paper demonstrated that methylation of H3K9 is crucial for recruitment of Swi6/HP1 to heterochromatic loci.
32. Litt, M. D., Simpson, M., Gaszner, M., Allis, C. D. & Felsenfeld, G. Correlation between histone lysine methylation and developmental changes at the chicken β-globin locus. Science 293, 2453-2455 (2001).
33. Noma, K., Allis, C. D. & Grewal, S. I. Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293, 1150-1155 (2001).
34. Cam, H. P. et al. Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nature Genet. 37, 809-819 (2005).
35. Martin, C. & Zhang, Y. The diverse functions of histone lysine methylation. Nature Rev. Mol. Cell Biol. 6, 838-849 (2005).
36. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. & Jenuwein, T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120 (2001).
37. Bannister, A. J. et al. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124 (2001). References 36 and 37 demonstrated that the chromodomain of HP1 binds with high affinity to H3K9me.
38. Schotta, G. et al. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21, 1121-1131 (2002).
39. Rea, S. et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-539 (2000). This paper showed that mammalian SUV39H1 and its fission yeast homologue Clr4 are histone H3K9-specific methyltranscferases, and identified the SET domain as the catalytic motif.
40. Hall, I. M. et al. Establishment and maintenance of a heterochromatin domain. Science 297, 2232-2237 (2002). This paper established a link between RNAi and heterochromatin assembly in fission yeast, and showed that heterochromatin assembly that is nucleated at a repeat element can spread in a manner that is dependent upon Swi6/HP1.
41. Brasher, S. V. et al. The structure of mouse HP1 suggests a unique mode of single peptide recognition by the shadow chromo domain dimer. EMBO J. 19, 1587-1597 (2000).
42. Cowieson, N. P., Partridge, J. F., Allshire, R. C. & McLaughlin, P. J. Dimerisation of a chromo shadow domain and distinctions from the chromodomain as revealed by structural analysis. Curr. Biol. 10, 517-525 (2000).
43. Smothers, J. F. & Henikoff, S. The HP1 chromo shadow domain binds a consensus peptide pentamer. Curr. Biol. 10, 27-30 (2000).
44. Lechner, M. S., Schultz, D. C., Negorev, D., Maul, G. G. & Rauscher, F. J., 3rd. The mammalian heterochromatin protein 1 binds diverse nuclear proteins through a common motif that targets the chromoshadow domain. Biochem. Biophys. Res. Commun. 331, 929-937 (2005).
45. Yamada, T., Fischle, W., Sugiyama, T., Allis, C. D. & Grewal, S. I. The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol. Cell 20, 173-185 (2005).
46. Zhang, C. L., McKinsey, T. A. & Olson, E. N. Association of class II histone deacetylases with heterochromatin protein 1: potential role for histone methylation in control of muscle differentiation. Mol. Cell. Biol. 22, 7302-7312 (2002).
47. Wysocka, J. et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 422, 86-90 (2006).
48. Pray-Grant, M. G., Daniel, J. A., Schieltz, D., Yates, J. R., 3rd & Grant, P. A. Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433, 434-438 (2005).
49. Carrozza, M. J. et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123, 581-592 (2005).
50. Joshi, A. A. & Struhl, K. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 20, 971-978 (2005).
51. Keogh, M. C. et al. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123, 593-605 (2005).
52. Nielsen, S. J. et al. Rb targets histone H3 methylation and HP1 to promoters. Nature 412, 561-565 (2001).
53. Schultz, D., Ayyanathan, K., Negorev, D., Maul, G. & Rauscher, F. R. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16, 1855-1869 (2002).
54. Dorer, D. R. & Henikoff, S. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77, 993-1002 (1994).
55. Selker, E. U. Repeat-induced gene silencing in fungi. Adv. Genet. 46, 439-450 (2002).
56. Luff, B., Pawlowski, L. & Bender, J. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3, 505-511 (1999).
57. Matzke, M. A. & Birchler, J. A. RNAi-mediated pathways in the nucleus. Nature Rev. Genet. 6, 24-35 (2005).
58. Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811 (1998). This groundbreaking study revealed an unexpected role of dsRNA in controlling gene expression.
59. Meister, G. & Tuschl, T. Mechanisms of gene silencing by double-stranded RNA. Nature 431, 343-349 (2004).
60. Cox, D. N. et al. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12, 3715-3727 (1998).
61. Klar, A. J. Developmental choices in mating-type interconversion in fission yeast. Trends Genet. 8, 208-213 (1992).
62. Grewal, S. I., Bonaduce, M. J. & Klar, A. J. Histone deacetylase homologs regulate epigenetic inheritance of transcriptional silencing and chromosome segregation in fission yeast. Genetics 150, 563-576 (1998).
63. Volpe, T. A. et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833-1837 (2002). This paper demonstrated that the RNAi machinery is required for transcriptional silencing and heterochromatin formation at the centromeres in fission yeast.
64. Mochizuki, K., Fine, N. A., Fujisawa, T. & Gorovsky, M. A. Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell 110, 689-699 (2002). This paper showed that the RNAi machinery is required for programmed elimination of DNA sequences in Tetrahymena thermophila, a process that involves heterochromatin formation at the eliminated DNA.
65. Taverna, S. D., Coyne, R. S. & Allis, C. D. Methylation of histone H3 at lysine 9 targets programmed DNA elimination in tetrahymena. Cell 110, 701-711 (2002).
66. Pal-Bhadra, M. et al. Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303, 669-672 (2004). This study demonstrated that the RNAi machinery is required for silencing and heterochromatin formation in D. melanogaster.
67. Zilberman, D., Cao, X. & Jacobsen, S. E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716-719 (2003). These authors established that the RNAi machinery is required for heterochromatic gene silencing and control of transposable elements in A. thaliana.
68. Kanellopoulou, C. et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489-501 (2005).
69. Fukagawa, T. et al. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nature Cell Biol. 6, 784-791 (2004).
70. Grishok, A., Sinskey, J. L. & Sharp, P. A. Transcriptional silencing of a transgene by RNAi in the soma of C. elegans. Genes Dev. 19, 683-696 (2005).
71. Reinhart, B. J. & Bartel, D. P. Small RNAs correspond to centromere heterochromatic repeats. Science 297, 1831 (2002).
72. Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, e104 (2004).
73. Lippman, Z. et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471-476 (2004).
74. Aravin, A. A. et al. The small RNA profile during Drosophila melanogaster development. Dev. Cell 5, 337-350 (2003).
75. Djupedal, I. et al. RNA Pol II subunit Rpb7 promotes centromeric transcription and RNAi-directed chromatin silencing. Genes Dev. 19, 2301-2306 (2005).
76. Kato, H. et al. RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science 309, 467-469 (2005). References 75 and 76 showed that mutations in RNA Pol II subunits affect RNAi-mediated heterochromatin assembly at fission yeast centromeres.
77. Partridge, J. F., Scott, K. S., Bannister, A. J., Kouzarides, T. & Allshire, R. C. cis-acting DNA from fission yeast centromeres mediates histone H3 methylation and recruitment of silencing factors and cohesin to an ectopic site. Curr. Biol. 12, 1652-1660 (2002).
78. Grewal, S. I. & Klar, A. J. A recombinationally repressed region between mat2 and mat3 loci shares homology to centromeric repeats and regulates directionality of mating-type switching in fission yeast. Genetics 146, 1221-1238 (1997).
79. Noma, K. et al. RITS acts in cis to promote RNA interference-mediated transcriptional and posttranscriptional silencing. Nature Genet. 36, 1174-1180 (2004).
80. Jia, S., Noma, K. & Grewal, S. I. RNAi-independent heterochromatin nucleation by the stress-activated ATF/CREB family proteins. Science 304, 1971-1976 (2004).
81. Kim, H. S., Choi, E. S., Shin, J. A., Jang, Y. K. & Park, S. D. Regulation of Swi6/HP1-dependent heterochromatin assembly by cooperation of components of the mitogen-activated protein kinase pathway and a histone deacetylase Clr6. J. Biol. Chem. 279, 42850-42859 (2004).
82. Kanoh, J., Sadaie, M., Urano, T. & Ishikawa, F. Telomere binding protein Taz1 establishes Swi6 heterochromatin independently of RNAi at telomeres. Curr. Biol. 15, 1808-1819 (2005).
83. Hansen, K. R., Ibarra, P. T. & Thon, G. Evolutionary-conserved telomere-linked helicase genes of fission yeast are repressed by silencing factors, RNAi components and the telomere-binding protein Taz1. Nucl. Acids Res. 34, 78-88 (2006).
84. Nakagawa, H. et al. Fission yeast CENP-B homologs nucleate centromeric heterochromatin by promoting heterochromatin-specific histone tail modifications. Genes Dev. 16, 1766-1778 (2002).
85. Gonzalo, S. & Blasco, M. A. Role of Rb family in the epigenetic definition of chromatin. Cell Cycle 4, 752-755 (2005).
86. Verdel, A. et al. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303, 672-676 (2004). This paper reported the identification of the RITS complex, which is involved in RNAi-mediated heterochromatin assembly and silencing in fission yeast.
87. Petrie, V. J., Wuitschick, J. D., Givens, C. D., Kosinski, A. M. & Partridge, J. F. RNA interference (RNAi)-dependent and RNAi-independent association of the Chp1 chromodomain protein with distinct heterochromatic loci in fission yeast. Mol. Cell. Biol. 25, 2331-2346 (2005).
88. Sugiyama, T., Cam, H., Verdel, A., Moazed, D. & Grewal, S. I. RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc. Natl Acad. Sci. USA 102, 152-157 (2005).
89. Buhler, M., Verdel, A. & Moazed, D. Tethering RITS to a nascent transcript initiates RNAi- and heterochromatin-dependent gene silencing. Cell 125, 873-886 (2006).
90. Motamedi, M. R. et al. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119, 789-802 (2004).
91. Irvine, D. V. et al. Argonaute slicing is required for heterochromatic silencing and spreading. Science 313, 1134-1137 (2006).
92. Zofall, M. & Grewal, S. I. RNAi-mediated heterochromatin assembly in fission yeast. Cold Spring Harb. Symp. Quant. Biol. (in the press).
93. Jia, S., Kobayashi, R. & Grewal, S. I. Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nature Cell Biol. 7, 1007-1013 (2005).
94. Horn, P. J., Bastie, J. N. & Peterson, C. L. A Rik1-associated, cullin-dependent E3 ubiquitin ligase is essential for heterochromatin formation. Genes Dev. 19, 1705-1714 (2005).
95. Hong, E. E., Villen, J., Gerace, E. L., Gygi, S. P. & Moazed, D. A Cullin E3 ubiquitin ligase complex associates with Rik1 and the Clr4 histone H3-K9 methyltransferase and is required for RNAi-mediated heterochromatin formation. RNA Biol. 2, 106-111 (2005).
96. Thon, G. et al. The Clr7 and Clr8 directionality factors and the Pcu4 cullin mediate heterochromatin formation in the fission yeast Schizosaccharomyces pombe. Genetics 171, 1583-1595 (2005).
97. Neuwald, A. F. & Poleksic, A. PSI-BLAST searches using hidden markov models of structural repeats: prediction of an unusual sliding DNA clamp and of β-propellers in UV-damaged DNA-binding protein. Nucleic Acids Res. 28, 3570-3580 (2000).
98. Gaszner, M. & Felsenfeld, G. Insulators: exploiting transcriptional and epigenetic mechanisms. Nature Rev. Genet. 7, 703-713 (2006).
99. Labrador, M. & Corces, V. G. Setting the boundaries of chromatin domains and nuclear organization. Cell 111, 151-154 (2002).
100. Bi, X. & Broach, J. R. Chromosomal boundaries in S. cerevisiae. Curr. Opin. Genet. Dev. 11, 199-204 (2001).
101. Oki, M. & Kamakaka, R. T. Barrier function at HMR. Mol. Cell 19, 707-716 (2005).
102. Thon, G., Bjerling, P., Bunner, C. M. & Verhein-Hansen, J. Expression-state boundaries in the mating-type region of fission yeast. Genetics 161, 611-622 (2002).
103. Noma, K., Cam, H. P., Maraia, R. J. & Grewal, S. I. A role for TFIIIC transcription factor complex in genome organization. Cell 125, 859-872 (2006).
104. Yusufzai, T. M., Tagami, H., Nakatani, Y. & Felsenfeld, G. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol. Cell 13, 291-298 (2004).
105. Ishii, K., Arib, G., Lin, C., Van Houwe, G. & Laemmli, U. K. Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 109, 551-562 (2002).
106. Scott, K. C., Merrett, S. L. & Willard, H. F. A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr. Biol. 16, 119-129 (2006).
107. Partridge, J. F., Borgstrom, B. & Allshire, R. C. Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev. 14, 783-791 (2000).
108. Shogren-Knaak, M. et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844-847 (2006).
109. Tamaru, H. & Selker, E. U. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414, 277-283 (2001).
110. Chan, S. W., Henderson, I. R. & Jacobsen, S. E. Gardening the genome: DNA methylation in Arabidopsis thaliana. Nature Rev. Genet. 6, 351-360 (2005).
111. Ohki, I. et al. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 105, 487-497 (2001).
112. Bird, A. P. & Wolffe, A. P. Methylation-induced repression-belts, braces, and chromatin. Cell 99, 451-454 (1999).
113. Murchison, E. P., Partridge, J. F., Tam, O. H., Cheloufi, S. & Hannon, G. J. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl Acad. Sci. USA 102, 12135-12140 (2005).
114. Haussecker, D. & Proudfoot, N. J. Dicer-dependent turnover of intergenic transcripts from the human β-globin gene cluster. Mol. Cell. Biol. 25, 9724-9733 (2005).
115. Sigova, A., Rhind, N. & Zamore, P. D. A single Argonaute protein mediates both transcriptional and posttranscriptional silencing in Schizosaccharomyces pombe. Genes Dev. 18, 2359-2367 (2004).
116. Maison, C. et al. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nature Genet. 30, 329-334 (2002).
117. Muchardt, C. et al. Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1α. EMBO Rep. 3, 975-981 (2002).
118. Seum, C., Delattre, M., Spierer, A. & Spierer, P. Ectopic HP1 promotes chromosome loops and variegated silencing in Drosophila. EMBO J. 20, 812-818 (2001).
119. Li, Y., Danzer, J. R., Alvarez, P., Belmont, A. S. & Wallrath, L. L. Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development 130, 1817-1824 (2003).
120. Hall, I. M., Noma, K. & Grewal, S. I. RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc. Natl Acad. Sci. USA 100, 193-198 (2003).
121. Grimaud, C. et al. RNAi components are required for nuclear clustering of Polycomb group response elements. Cell 124, 957-971 (2006).
122. Pal-Bhadra, M., Bhadra, U. & Birchler, J. A. Interrelationship of RNA interference and transcriptional gene silencing in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 69, 433-438 (2004).
123. Lei, E. P. & Corces, V. G. RNA interference machinery influences the nuclear organization of a chromatin insulator. Nature Genet. 38, 936-941 (2006).
124. Gasser, S. M. Positions of potential: nuclear organization and gene expression. Cell 104, 639-642 (2001).
125. Heard, E. Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr. Opin. Genet. Dev. 15, 482-489 (2005).
126. Ayoub, N. et al. A novel JmjC domain protein modulates heterochromatization in fission yeast. Mol. Cell. Biol. 23, 4356-4370 (2003).
127. Peters, A. H. et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337 (2001).
128. Karpen, G. H., Le, M. H. & Le, H. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273, 118-122 (1996).
129. Bernard, P. et al. Requirement of heterochromatin for cohesion at centromeres. Science 294, 2539-2542 (2001).
130. Nonaka, N. et al. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nature Cell Biol. 4, 89-93 (2002). References 129 and 130 showed that Swi6/HP1 preferentially recruit cohesin to heterochromatic loci including pericentric regions, which is essential for proper chromosome segregation.
131. Ekwall, K. The roles of histone modifications and small RNA in centromere function. Chromosome Res. 12, 535-542 (2004).
132. Pidoux, A. L. & Allshire, R. C. Kinetochore and heterochromatin domains of the fission yeast centromere. Chromosome Res. 12, 521-534 (2004).
133. Obuse, C. et al. A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nature Cell Biol. 6, 1135-1141 (2004).
134. Ainsztein, A. M., Kandels-Lewis, S. E., Mackay, A. M. & Earnshaw, W. C. INCENP centromere and spindle targeting: identification of essential conserved motifs and involvement of heterochromatin protein HP1. J. Cell Biol. 143, 1763-1774 (1998).
135. Pinsky, B. A. & Biggins, S. The spindle checkpoint: tension versus attachment. Trends Cell Biol. 15, 486-493 (2005).
136. Pak, D. T. et al. Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91, 311-323 (1997).
137. Murzina, N., Verreault, A., Laue, E. & Stillman, B. Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol. Cell 4, 529-540 (1999).
138. Bailis, J. M., Bernard, P., Antonelli, R., Allshire, R. C. & Forsburg, S. L. Hsk1-Dfp1 is required for heterochromatin-mediated cohesion at centromeres. Nature Cell Biol. 5, 1111-1116 (2003).
139. Klose, R. J. et al. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442, 312-316 (2006).
140. Fodor, B. D. et al. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev. 20, 1557-1562 (2006).
141. Whetstine, J. R. et al. Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125, 467-481 (2006).
142. Fischle, W. et al. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438, 1116-1122 (2005).
143. Hirota, T., Lipp, J. J., Toh, B. H. & Peters, J. M. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438, 1176-1180 (2005). References 142 and 143 showed that the association of HP1 with H3K9me can be regulated by the phosphorylation of adjacent serine 10 residue.
144. Eissenberg, J. C., Ge, Y. W. & Hartnett, T. Increased phosphorylation of HP1, a heterochromatin-associated protein of Drosophila, is correlated with heterochromatin assembly. J. Biol. Chem. 269, 21315-21321 (1994).
145. Lomberk, G., Bensi, D., Fernandez-Zapico, M. E. & Urrutia, R. Evidence for the existence of an HP1-mediated subcode within the histone code. Nature Cell Biol. 8, 407-415 (2006).
146. Shin, J. A. et al. SUMO modification is involved in the maintenance of heterochromatin stability in fission yeast. Mol. Cell 19, 817-828 (2005).
147. Minc, E., Allory, Y., Worman, H. J., Courvalin, J. C. & Buendia, B. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108, 220-234 (1999).
148. Moazed, D. Common themes in mechanisms of gene silencing. Mol. Cell 8, 489-498 (2001).
149. Orban, T. I. & Izaurralde, E. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 11, 459-469 (2005).
150. Freitag, M., Hickey, P. C., Khlafallah, T. K., Read, N. D. & Selker, E. U. HP1 is essential for DNA methylation in Neurospora. Mol. Cell 13, 427-434 (2004). This paper showed that the HP1 homologue of N. crassa is required for DNA methylation at the relics of transposons.
151. Alleman, M. et al. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442, 295-298 (2006).
152. Mandell, J. G., Goodrich, K. J., Bahler, J. & Cech, T. R. Expression of a RecQ helicase homolog affects progression through crisis in fission yeast lacking telomerase. J. Biol. Chem. 280, 5249-5257 (2005).