Heterochromatic gene silencing by activator interference and a transcription elongation barrier

Journal of Biological Chemistry

Volumn 288, Issue 40, 2013, Pages 28771-28782

  Johnson, Aaron ^a,b   Wu, Ronghu ^a,d   Peetz, Matthew ^b   Gygi, Steven P ^a   Moazed, Danesh ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUDDING YEASTS; GENE SILENCING; RNA POLYMERASE; TRANSCRIPTIONAL CO-ACTIVATORS;

TRANSCRIPTION; YEAST;

GENETIC ENGINEERING;

FUNGAL PROTEIN; HISTONE DEACETYLASE; NUCLEAR FACTOR; RNA POLYMERASE; RNA POLYMERASE II; SILENT INFORMATION REGULATOR PROTEIN; SILENT INFORMATION REGULATOR PROTEIN 2; SILENT INFORMATION REGULATOR PROTEIN 3; SILENT INFORMATION REGULATOR PROTEIN 4; UNCLASSIFIED DRUG;

ARTICLE; BUDDING; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; CONTROLLED STUDY; FUNGAL GENETICS; GENE DISRUPTION; GENE REPRESSION; GENE SILENCING; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC STABILITY; HETEROCHROMATIN; IN VITRO STUDY; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEOMICS; RNA INTERFERENCE; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; YEAST;

CHROMATIN; CHROMATIN MODIFICATION; GENE SILENCING; HETEROCHROMATIN; SIR PROTEINS; TRANSCRIPTION;

GENE SILENCING; HETEROCHROMATIN; HUMANS; MASS SPECTROMETRY; MODELS, GENETIC; NUCLEOSOMES; PROTEOMICS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; TRANS-ACTIVATORS; TRANSCRIPTION ELONGATION, GENETIC;

EID: 84885146636     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.460071     Document Type: Article

References (43)

1. Grewal, S. I., and Moazed, D. (2003) Heterochromatin and epigenetic control of gene expression. Science 301, 798-802
2. Reifsnyder, C., Lowell, J., Clarke, A., and Pillus, L. (1996) Yeast SAS silencing genes and human genes associated with AML and HIV-1 Tat interactions are homologous with acetyltransferases. Nat. Genet. 14, 42-49
3. Johnson, A., Li, G., Sikorski, T. W., Buratowski, S., Woodcock, C. L., and Moazed, D. (2009) Reconstitution of heterochromatin-dependent transcriptional gene silencing. Mol. Cell 35, 769-781
4. Bühler, M., and Moazed, D. (2007) Transcription and RNAi in heterochromatic gene silencing. Nat. Struct. Mol. Biol. 14, 1041-1048
5. 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
6. Rusché, L. N., Kirchmaier, A. L., and Rine, J. (2002) Ordered nucleation and spreading of silenced chromatin in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 2207-2222
7. Hoppe, G. J., Tanny, J. C., Rudner, A. D., Gerber, S. A., Danaie, S., Gygi, S. P., and Moazed, D. (2002) Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation. Mol. Cell. Biol. 22, 4167-4180
8. Rudner, A. D., Hall, B. E., Ellenberger, T., and Moazed, D. (2005) A nonhistone protein-protein interaction required for assembly of the SIR complex and silent chromatin. Mol. Cell. Biol. 25, 4514-4528
9. Liou, G. G., Tanny, J. C., Kruger, R. G., Walz, T., and Moazed, D. (2005) Assembly of the SIR complex and its regulation byO-acetyl-ADP-ribose, a product of NAD-dependent histone deacetylation. Cell 121, 515-527
10. Hecht, A., Laroche, T., Strahl-Bolsinger, S., Gasser, S. M., and Grunstein, M. (1995) Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80, 583-592
11. Chen, L., and Widom, J. (2005) Mechanism of transcriptional silencing in yeast. Cell 120, 37-48
12. Gao, L., and Gross, D. S. (2008) Sir2 silences gene transcription by targeting the transition between RNA polymerase II initiation and elongation. Mol. Cell. Biol. 28, 3979-3994
13. Sekinger, E. A., and Gross, D. S. (2001) Silenced chromatin is permissive to activator binding and PIC recruitment. Cell 105, 403-414
14. Fitzgerald, D. P., and Bender, W. (2001) Polycomb group repression reduces DNA accessibility. Mol. Cell. Biol. 21, 6585-6597
15. Dellino, G. I., Schwartz, Y. B., Farkas, G., McCabe, D., Elgin, S. C., and Pirrotta, V. (2004) Polycomb silencing blocks transcription initiation. Mol. Cell 13, 887-893
16. King, I. F., Francis, N. J., and Kingston, R. E. (2002) Native and recombinant polycomb group complexes establish a selective block to template accessibility to repress transcription in vitro. Mol. Cell. Biol. 22, 7919-7928
17. Margueron, R., Li, G., Sarma, K., Blais, A., Zavadil, J., Woodcock, C. L., Dynlacht, B. D., and Reinberg, D. (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell 32, 503-518
18. Francis, N. J., Kingston, R. E., and Woodcock, C. L. (2004) Chromatin compaction by a polycomb group protein complex. Science 306, 1574-1577
19. Sawadogo, M., and Roeder, R. G. (1985) Factors involved in specific transcription by human RNA polymerase II: analysis by a rapid and quantitative in vitro assay. Proc. Natl. Acad. Sci. U.S.A. 82, 4394-4398
20. Woontner, M., Wade, P. A., Bonner, J., and Jaehning, J. A. (1991) Transcriptional activation in an improved whole-cell extract from Saccharomyces cerevisiae. Mol. Cell. Biol. 11, 4555-4560
21. Kong, S. E., Banks, C. A., Shilatifard, A., Conaway, J. W., and Conaway, R. C. (2005) ELL-associated factors 1 and 2 are positive regulators of RNA polymerase II elongation factor ELL. Proc. Natl. Acad. Sci. U.S.A. 102, 10094-10098
22. Carey, M., Li, B., and Workman, J. L. (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol. Cell 24, 481-487
23. Keogh, M. C., Cho, E. J., Podolny, V., and Buratowski, S. (2002) Kin28 is found within TFIIH and a Kin28-Ccl1-Tfb3 trimer complex with differential sensitivities to T-loop phosphorylation. Mol. Cell. Biol. 22, 1288-1297
24. Yates, J. R., 3rd, Eng, J. K., McCormack, A. L., and Schieltz, D. (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436
25. Elias, J. E., and Gygi, S. P. (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat. Methods 4, 207-214
26. Huttlin, E. L., Jedrychowski, M. P., Elias, J. E., Goswami, T., Rad, R., Beausoleil, S. A., Villén, J., Haas, W., Sowa, M. E., and Gygi, S. P. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189
27. Bhaumik, S. R. (2011) Distinct regulatory mechanisms of eukaryotic transcriptional activation by SAGA and TFIID. Biochim. Biophys. Acta 1809, 97-108
28. Sikorski, T. W., Joo, Y. J., Ficarro, S. B., Askenazi, M., Buratowski, S., and Marto, J. A. (2012) Proteomic analysis demonstrates activator-and chromatin-specific recruitment to promoters. J. Biol. Chem. 287, 35397-35408
29. Bondarenko, V. A., Steele, L. M., Ujvári, A., Gaykalova, D. A., Kulaeva, O. I., Polikanov, Y. S., Luse, D. S., and Studitsky, V. M. (2006) Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol. Cell 24, 469-479
30. Bühler, M. (2009) RNA turnover and chromatin-dependent gene silencing. Chromosoma 118, 141-151
31. Trojer, P., and Reinberg, D. (2007) Facultative heterochromatin: is there a distinctive molecular signature? Mol. Cell 28, 1-13
32. Chen, L., and Widom, J. (2004) Molecular basis of transcriptional silencing in budding yeast. Biochem. Cell Biol. 82, 413-418
33. Kitada, T., Kuryan, B. G., Tran, N. N., Song, C., Xue, Y., Carey, M., and Grunstein, M. (2012) Mechanism for epigenetic variegation of gene expression at yeast telomeric heterochromatin. Genes Dev. 26, 2443-2455
34. Lehmann, L., Ferrari, R., Vashisht, A. A., Wohlschlegel, J. A., Kurdistani, S. K., and Carey, M. (2012) Polycomb repressive complex 1 (PRC1) disas-sembles RNA polymerase II preinitiation complexes. J. Biol. Chem. 287, 35784-35794
35. Sinha, M., Watanabe, S., Johnson, A., Moazed, D., and Peterson, C. L. (2009) Recombinational repair within heterochromatin requires ATP-dependent chromatin remodeling. Cell 138, 1109-1121
36. Wong, K. H., and Struhl, K. (2011) The Cyc8-Tup1 complex inhibits transcription primarily by masking the activation domain of the recruiting protein. Genes Dev. 25, 2525-2539
37. Loo, S., and Rine, J. (1994) Silencers and domains of generalized repression. Science 264, 1768-1771
38. van Leeuwen, F., Gafken, P. R., and Gottschling, D. E. (2002) Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 109, 745-756
39. Martino, F., Kueng, S., Robinson, P., Tsai-Pflugfelder, M., van Leeuwen, F., Ziegler, M., Cubizolles, F., Cockell, M. M., Rhodes, D., and Gasser, S. M. (2009) Reconstitution of yeast silent chromatin: multiple contact sites and O-AADPR binding load SIR complexes onto nucleosomes in vitro. Mol. Cell 33, 323-334
40. Armache, K. J., Garlick, J. D., Canzio, D., Narlikar, G. J., and Kingston, R. E. (2011) Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science 334, 977-982
41. Wang, F., Li, G., Altaf, M., Lu, C., Currie, M. A., Johnson, A., and Moazed, D. (2013) Heterochromatin protein Sir3 induces contacts between the amino terminus of histone H4 and nucleosomal DNA. Proc. Natl. Acad. Sci. U.S.A. 110, 8495-8500
42. Ku, M., Koche, R. P., Rheinbay, E., Mendenhall, E. M., Endoh, M., Mikkelsen, T. S., Presser, A., Nusbaum, C., Xie, X., Chi, A. S., Adli, M., Kasif, S., Ptaszek, L. M., Cowan, C. A., Lander, E. S., Koseki, H., and Bernstein, B. E. (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242
43. Li, G., and Widom, J. (2004) Nucleosomes facilitate their own invasion. Nat. Struct. Mol. Biol. 11, 763-769