Rapid epigenetic adaptation to uncontrolled heterochromatin spreading

eLife

Volumn 2015, Issue 4, 2015, Pages

  Wang, Jiyong ^a   Reddy, Bharat D ^a   Jia, Songtao ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; EPE1 PROTEIN; HETEROCHROMATIN PROTEIN 1; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; MESSENGER RNA; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; HETEROCHROMATIN; HISTONE; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; DNA MICROARRAY; ENZYME ACTIVITY; EPISTASIS; EVOLUTIONARY ADAPTATION; GENE; GENE MAPPING; GENE SILENCING; GENETIC ANALYSIS; GROWTH DISORDER; HETEROCHROMATIN; IN VITRO STUDY; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA ISOLATION; TELOMERE HOMEOSTASIS; WESTERN BLOTTING; YEAST; ADAPTATION; BIOLOGICAL MODEL; GENE LOCUS; GENE REPRESSION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; INHERITANCE; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; SCHIZOSACCHAROMYCES;

SCHIZOSACCHAROMYCETACEAE;

ADAPTATION, BIOLOGICAL; BASE SEQUENCE; EPIGENESIS, GENETIC; GENETIC LOCI; HETEROCHROMATIN; HISTONES; INHERITANCE PATTERNS; MODELS, GENETIC; MUTATION; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SUPPRESSION, GENETIC;

EID: 84979854825     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06179     Document Type: Article

References (58)

1. Al-Sady, B., Madhani, H.D., and Narlikar, G.J. (2013). Division of labor between the chromodomains of HP1 and Suv39 methylase enables coordination of heterochromatin spread. Mol Cell 51, 80-91.
2. Alper, B.J., Job, G., Yadav, R.K., Shanker, S., Lowe, B.R., and Partridge, J.F. (2013). Sir2 is required for Clr4 to initiate centromeric heterochromatin assembly in fission yeast. Embo J 32, 2321-2335.
3. Aygun, O., Mehta, S., and Grewal, S.I. (2013). HDAC-mediated suppression of histone turnover promotes epigenetic stability of heterochromatin. Nat Struct Mol Biol 20, 547-554.
4. Bannister, A.J., Zegerman, P., Partridge, J.F., Miska, E.A., Thomas, J.O., Allshire, R.C., and Kouzarides, T. (2001). Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124.
5. Cam, H.P., Sugiyama, T., Chen, E.S., Chen, X., FitzGerald, P.C., and Grewal, S.I. (2005). Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 37, 809-819.
6. Castel, S.E., and Martienssen, R.A. (2013). RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nature reviews Genetics 14, 100-112.
7. Cohen, A., and Jia, S. (2014). Noncoding RNAs and the borders of heterochromatin. Wiley Interdiscip Rev RNA.
8. Egan, E.D., Braun, C.R., Gygi, S.P., and Moazed, D. (2014). Post-transcriptional regulation of meiotic genes by a nuclear RNA silencing complex. Rna 20, 867881.
9. Geutjes, E.J., Bajpe, P.K., and Bernards, R. (2012). Targeting the epigenome for treatment of cancer. Oncogene 31, 3827-3844.
10. Gomez, E.B., Espinosa, J.M., and Forsburg, S.L. (2005). Schizosaccharomyces pombe mst2+ encodes a MYST family histone acetyltransferase that negatively regulates telomere silencing. Mol Cell Biol 25, 8887-8903.
11. Grewal, S.I., and Jia, S. (2007). Heterochromatin revisited. Nat Rev Genet 8, 35-46.
12. Grewal, S.I., and Moazed, D. (2003). Heterochromatin and epigenetic control of gene expression. Science 301, 798-802.
13. Gullerova, M., and Proudfoot, N.J. (2008). Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132, 983-995.
14. Hall, I.M., Shankaranarayana, G.D., Noma, K., Ayoub, N., Cohen, A., and Grewal, S.I. . Establishment and maintenance of a heterochromatin domain. Science 297, 2232-2237.
15. Harigaya, Y., Tanaka, H., Yamanaka, S., Tanaka, K., Watanabe, Y., Tsutsumi, C., Chikashige, Y., Hiraoka, Y., Yamashita, A., and Yamamoto, M. (2006). Selective elimination of messenger RNA prevents an incidence of untimely meiosis. Nature 442, 45-50.
16. Heard, E., and Martienssen, R.A. (2014). Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157, 95-109.
17. Hiriart, E., Vavasseur, A., Touat-Todeschini, L., Yamashita, A., Gilquin, B., Lambert, E., Perot, J., Shichino, Y., Nazaret, N., Boyault, C., et al. (2012). Mmi1 RNA surveillance machinery directs RNAi complex RITS to specific meiotic genes in fission yeast. Embo J 31, 2296-2308.
18. Hong, E.J., Villen, J., Gerace, E.L., Gygi, S.P., and Moazed, D. (2005). 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.
19. Horn, P.J., Bastie, J.N., and Peterson, C.L. (2005). A Rik1-associated, cullin-dependent E3 ubiquitin ligase is essential for heterochromatin formation. Genes Dev 19, 1705-1714.
20. Iida, T., Nakayama, J., and Moazed, D. (2008). SiRNA-mediated heterochromatin establishment requires HP1 and is associated with antisense transcription. Mol Cell 31, 178-189.
21. Jia, S., Kobayashi, R., and Grewal, S.I. (2005). Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat Cell Biol 7, 1007-1013.
22. Jia, S., Noma, K., and Grewal, S.I. (2004). RNAi-independent heterochromatin nucleation by the stress-activated ATF/CREB family proteins. Science 304, 19711976.
23. Kagansky, A., Folco, H.D., Almeida, R., Pidoux, A.L., Boukaba, A., Simmer, F., Urano, T., Hamilton, G.L., and Allshire, R.C. (2009). Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science 324, 1716-1719.
24. Kanoh, J., Sadaie, M., Urano, T., and Ishikawa, F. (2005). Telomere binding protein Taz1 establishes Swi6 heterochromatin independently of RNAi at telomeres. Curr Biol 15, 1808-1819.
25. Kim, H.S., Choi, E.S., Shin, J.A., Jang, Y.K., and Park, S.D. (2004). 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.
26. Kreso, A., O'Brien, C.A., van Galen, P., Gan, O.I., Notta, F., Brown, A.M., Ng, K., Ma, J., Wienholds, E., Dunant, C., et al. (2013). Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 339, 543-548.
27. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T. (2001). Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116120.
28. Lee, N.N., Chalamcharla, V.R., Reyes-Turcu, F., Mehta, S., Zofall, M., Balachandran, V., Dhakshnamoorthy, J., Taneja, N., Yamanaka, S., Zhou, M., et al. (2013). Mtr4-like protein coordinates nuclear RNA processing for heterochromatin assembly and for telomere maintenance. Cell 155, 1061-1074.
29. Lejeune, E., and Allshire, R.C. (2011). Common ground: small RNA programming and chromatin modifications. Curr Opin Cell Biol 23, 258-265.
30. Mellone, B.G., Ball, L., Suka, N., Grunstein, M.R., Partridge, J.F., and Allshire, R.C. . Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3. Curr Biol 13, 1748-1757.
31. Moazed, D. (2009). Small RNAs in transcriptional gene silencing and genome defence. Nature 457, 413-420.
32. Moazed, D. (2011). Mechanisms for the inheritance of chromatin states. Cell 146, 510518.
33. Motamedi, M.R., Hong, E.J., Li, X., Gerber, S., Denison, C., Gygi, S., and Moazed, D. (2008). HP1 proteins form distinct complexes and mediate heterochromatic gene silencing by nonoverlapping mechanisms. Mol Cell 32, 778-790.
34. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D., and Grewal, S.I. (2001). Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292, 110-113.
35. Noma, K., Cam, H.P., Maraia, R.J., and Grewal, S.I. (2006). A role for TFIIIC transcription factor complex in genome organization. Cell 125, 859-872.
36. Nugent, R.L., Johnsson, A., Fleharty, B., Gogol, M., Xue-Franzen, Y., Seidel, C., Wright, A.P., and Forsburg, S.L. (2010). Expression profiling of S. pombe acetyltransferase mutants identifies redundant pathways of gene regulation. BMC Genomics 11, 59.
37. Ragunathan, K., Jih, G., and Moazed, D. (2014). Epigenetic inheritance uncoupled from sequence-specific recruitment. Science.
38. Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B.D., Sun, Z.W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C.P., Allis, C.D., et al. (2000). Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-599.
39. Reddy, B.D., Wang, Y., Niu, L., Higuchi, E.C., Marguerat, S.B., Bahler, J., Smith, G.R., and Jia, S. (2011). Elimination of a specific histone H3K14 acetyltransferase complex bypasses the RNAi pathway to regulate pericentric heterochromatin functions. Genes Dev 25, 214-219.
40. Roguev, A., Bandyopadhyay, S., Zofall, M., Zhang, K., Fischer, T., Collins, S.R., Qu, H., Shales, M., Park, H.O., Hayles, J., et al. (2008). Conservation and rewiring of functional modules revealed by an epistasis map in fission yeast. Science 322, 405-410.
41. Rusche, L.N., Kirchmaier, A.L., and Rine, J. (2003). The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72, 481-516.
42. Ryan, C.J., Roguev, A., Patrick, K., Xu, J., Jahari, H., Tong, Z., Beltrao, P., Shales, M., Qu, H., Collins, S.R., et al. (2012). Hierarchical modularity and the evolution of genetic interactomes across species. Mol Cell 46, 691-704.
43. Sharma, S.V., Lee, D.Y., Li, B., Quinlan, M.P., Takahashi, F., Maheswaran, S., McDermott, U., Azizian, N., Zou, L., Fischbach, M.A., et al. (2010). A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69-80.
44. Sugiyama, T., Cam, H.P., Sugiyama, R., Noma, K., Zofall, M., Kobayashi, R., and Grewal, S.I. (2007). SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128, 491-504.
45. Tadeo, X., Wang, J., Kallgren, S.P., Liu, J., Reddy, B.D., Qiao, F., and Jia, S. (2013). Elimination of shelterin components bypasses RNAi for pericentric heterochromatin assembly. Genes Dev 27, 2489-2499.
46. Talbert, P.B., and Henikoff, S. (2006). Spreading of silent chromatin: inaction at a distance. Nature reviews Genetics 7, 793-803.
47. Tashiro, S., Asano, T., Kanoh, J., and Ishikawa, F. (2013). Transcription-induced chromatin association of RNA surveillance factors mediates facultative heterochromatin formation in fission yeast. Genes Cells 18, 327-339.
48. Trewick, S.C., Minc, E., Antonelli, R., Urano, T., and Allshire, R.C. (2007). The JmjC domain protein Epe1 prevents unregulated assembly and disassembly of heterochromatin. Embo J 26, 4670-4682.
49. Tsukada, Y., Fang, J., Erdjument-Bromage, H., Warren, M.E., Borchers, C.H., Tempst, P., and Zhang, Y. (2006). Histone demethylation by a family of JmjC domain- containing proteins. Nature 439, 811-816.
50. Wang, J., Lawry, S.T., Cohen, A.L., and Jia, S. (2014). Chromosome boundary elements and regulation of heterochromatin spreading. Cell Mol Life Sci 71, 4841-4852.
51. Wang, J., Tadeo, X., Hou, H., Andrews, S., Moresco, J.J., Yates, J.R., 3rd, Nagy, P.L., and Jia, S. (2015). Tls1 regulates splicing of shelterin components to control telomeric heterochromatin assembly and telomere length. Nucleic Acids Res 42, 11419-11432.
52. Wang, J., Tadeo, X., Hou, H., Tu, P.G., Thompson, J., Yates, J.R., 3rd, and Jia, S. (2013). Epe1 recruits BET family bromodomain protein Bdf2 to establish heterochromatin boundaries. Genes Dev 27, 1886-1902.
53. Wang, Y., Kallgren, S.P., Reddy, B.D., Kuntz, K., Lopez-Maury, L., Thompson, J., Watt, S., Ma, C., Hou, H., Shi, Y., et al. (2012). Histone H3 lysine 14 acetylation is required for activation of a DNA damage checkpoint in fission yeast. J Biol Chem 287, 4386-4393.
54. Watt, S., Mata, J., Lopez-Maury, L., Marguerat, S., Burns, G., and Bahler, J. (2008). Urg1: a uracil-regulatable promoter system for fission yeast with short induction and repression times. PLoS One 3, e1428.
55. Yamanaka, S., Mehta, S., Reyes-Turcu, F.E., Zhuang, F., Fuchs, R.T., Rong, Y., Robb, G.B., and Grewal, S.I. (2013). RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493, 557-560.
56. Zhang, K., Mosch, K., Fischle, W., and Grewal, S.I. (2008). Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat Struct Mol Biol 15, 381-388.
57. Zofall, M., and Grewal, S.I. (2006). Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol Cell 22, 681-692.
58. Zofall, M., Yamanaka, S., Reyes-Turcu, F.E., Zhang, K., Rubin, C., and Grewal, S.I. (2012). RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science 335, 96-100.