Limiting the extent of the RDN1 heterochromatin domain by a silencing barrier and Sir2 protein levels in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 29, Issue 10, 2009, Pages 2889-2898

  Biswas, Moumita ^a   Maqani, Nazif ^b   Rai, Ragini ^a   Kumaran, Srikala P ^a   Iyer, Kavitha R ^a   Sendinc, Erdem ^b   Smith, Jeffrey S ^b   Laloraya, Shikha ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED RNA POLYMERASE III; HISTONE ACETYLTRANSFERASE GCN5; RIBOSOME DNA; RNA POLYMERASE II; SIRTUIN 2; SIRTUIN 3; SIRTUIN 4; TRANSFER RNA; CELL CYCLE PROTEIN; COHESINS; GLUTAMINE TRANSFER RNA; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; NONHISTONE PROTEIN; SILENT INFORMATION REGULATOR PROTEIN; SIR2 PROTEIN, S CEREVISIAE; SIRTUIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA FLANKING REGION; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME MECHANISM; GENE; GENE LOCUS; GENE SILENCING; HETEROCHROMATIN; LONG TERMINAL REPEAT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE; TELOMERE; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROARRAY ANALYSIS;

SACCHAROMYCES CEREVISIAE;

CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA, RIBOSOMAL; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; GENOME, FUNGAL; HETEROCHROMATIN; HISTONE ACETYLTRANSFERASES; HISTONE DEACETYLASES; MICROARRAY ANALYSIS; RNA POLYMERASE III; RNA, TRANSFER, GLN; SACCHAROMYCES CEREVISIAE; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SIRTUINS;

EID: 66349126902     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00728-08     Document Type: Article

References (66)

1. Allard, S., R. T. Utley, J. Savard, A. Clarke, P. Grant, C. J. Brandl, L. Pillus, J. L. Workman, and J. Cote. 1999. NuA4, an essential transcription adaptor/histone acetyl transferase complex containing Esa1p and the ATM-related co-factor Tra1p. EMBO J. 18:5108-5119.
2. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1993. Current protocols in molecular biology. Greene Publishing Associates, New York, NY.
3. Bi, X., M. Braunstein, G. J. Shei, and J. R. Broach. 1999. The yeast HML I silencer defines a heterochromatin domain boundary by directional establishment of silencing. Proc. Natl. Acad. Sci. USA 96:11934-11939.
4. Bi, X., and J. R. Broach. 2001. Chromatin boundaries in Saccharomyces cerevisiae. Curr. Opin. Genet. Dev. 11:199-204.
5. Bi, X. 2002. Domains of gene silencing near the left end of chromosome III in Saccharomyces cerevisiae. Genetics 160:1401- 1407.
6. Bi, X., Q. Yu, J. J. Sandmeier, and Y. Zou. 2004. Formation of boundaries of transcriptionally silent chromatin by nucleosome-excluding structures. Mol. Cell. Biol. 24:2118-2131.
7. Blat, Y., and N. Kleckner. 1999. Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249-259.
8. Briggs, S. D., M. Bryk, B. D. Strahl, W. L. Cheung, J. K. Davie, S. Y. Dent., F. Winston, and C. D. Allis. 2001. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15:3286-3295.
9. Bryk, M., M. Banerjee, M. Murphy, K. E. Knudsen, D. J. Garfinkel, and M. J. Curcio. 1997. Transcriptional silencing of Ty1 elements in the RDN1 locus of yeast. Genes Dev. 11:255-269.
10. Buck, S. W., J. J. Sandmeier, and J. S. Smith. 2002. RNA polymerase I propagates unidirectional spreading of rDNA silent chromatin. Cell 111: 1003-1014.
11. Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
12. Cioci, F., L. Vu, K. Eliason, M. Oakes, I. N. Siddiqi, and M. Nomura. 2003. Silencing in yeast rDNA chromatin: reciprocal relationship in gene expression between RNA polymerase I and II. Mol. Cell 12:135-145.
13. Clarke, A. S., E. Samal, and L. Pillus. 2006. Distinct roles for the essential MYST family HAT Esa1p in transcriptional silencing. Mol. Biol. Cell 17: 1744-1757.
14. Donze, D., C. R. Adams, J. Rine, and R. T. Kamakaka. 1999. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev. 13: 698-708.
15. Donze, D., and R. T. Kamakaka. 2001. RNA polymerase III and RNA polymerase II promoter complexes are heterochromatin barriers in Saccharomyces cerevisiae. EMBO J. 20:520-531.
16. Donze, D., and R. T. Kamakaka. 2002. Braking the silence: how heterochromatin gene repression is stopped in its tracks. Bioessays 24:344-349.
17. Dror, V., and F. Winston. 2004. The Swi/Snf chromatin remodeling complex is required for ribosomal DNA and telomeric silencing in Saccharomyces cerevisiae. Mol. Cell. Biol. 24:8227-8235.
18. Dubey, R. N., and M. R. Gartenberg. 2007. A tDNA establishes cohesion of a neighboring silent chromatin domain. Genes Dev. 21:2150-2160.
19. Ehrenhofer-Murray, A. E., D. H. Rivier, and J. Rine. 1997. The role of Sas2, an acetyltransferase homologue of Saccharomyces cerevisiae, in silencing and ORC function. Genetics 145:923-934.
20. Ferrari, R., C. Rivetti, J. Acker, and G. Dieci. 2004. Distinct roles of transcription factors TFIIIB and TFIIIC in RNA polymerase III transcription reinitiation. Proc. Natl. Acad. Sci. USA 101:13442-13447.
21. Fritze, C. E., K. Verschueren, R. Strich, and R. E. Esposito. 1997. Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA. EMBO J. 16:6495-6509.
22. Gotta, M., S. Strahl-Bolsinger, H. Renauld, T. Laroche, B. K. Kennedy, M. Grunstein, and S. M. Gasser. 1997. Localization of Sir2p: the nucleolus as a compartment for silent information regulators. EMBO J. 16:3243-3255.
23. Howe, L., D. Auston, P. Grant, S. John, R. G. Cook, J. L. Workman, and L. Pillus. 2001. Histone H3 specific acetyltransferases are essential for cell cycle progression. Genes Dev. 15:3144-3154.
24. Hull, M. W., Erickson J., M. Johnston, and D. R. Engelke. 1994. tRNA genes as transcriptional repressor elements. Mol. Cell. Biol. 14:1266-1277.
25. Ishii, K., G. Arib, C. Lin, G. Van Houwe, and U. K. Laemmli. 2002. Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 109: 551-562.
26. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293:1074-1080.
27. Kennedy, B. K., M. Gotta, D. A. Sinclair, K. Mills, D. S. McNabb, M. Murthy, S. M. Pak, T. Laroche, S. M. Gasser, and L. Guarente. 1997. Redistribution of silencing proteins from telomeres to the nucleolus is associated with extension of life span in S. cerevisiae. Cell 89:381-391.
28. Kimura, A., T. Umehara, and M. Horikoshi. 2002. Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat. Genet. 32:370-377.
29. Koshland, D. E., and V. Guacci. 2000. Sister chromatid cohesion: the beginning of a long and beautiful relationship. Curr. Opin. Cell Biol. 12:297-301.
30. Tyr locus: transcription of the mutant genes in vitro. Cell 22:415-425.
31. 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.
32. Laloraya, S., V. Guacci, and D. Koshland. 2000. Chromosomal addresses of the cohesin component Mcd1p. J. Cell Biol. 151:1047-1056.
33. Lau, A., B. Blitzblau., and S. P. Bell. 2002. Cell-cycle control of the establishment of mating-type silencing in S. cerevisiae. Genes Dev. 16:2935-2945.
34. Meijsing, S. H., and A. E. Ehrenhofer-Murray. 2001. The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae. Genes Dev. 15:3169-3182.
35. Michel, A. H., B. Kornmann, K. Dubrana, and D. Shore. 2005. Spontaneous rDNA copy number variation modulates Sir2 levels and epigenetic gene silencing. Genes Dev. 19:1199-1210.
36. Morris, S. A., B. Rao, B. A. Garcia, S. B. Hake, R. L. Diaz, J. Shabanowitz, D. F. Hunt, C. D. Allis, J. D. Lieb, and B. D. Strahl. 2007. Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J. Biol. Chem. 282:7632-7640.
37. Newman, A., R. C. Ogden, and J. Abelson. 1983. tRNA gene transcription in yeast: effects of specified base substitutions in the intragenic promoter. Cell 35:117-125.
38. Noma, K., H. P. Cam, R. J. Maraia, and S. I. Grewal. 2006. A role for TFIIIC transcription factor complex in genome organization. Cell 125:859-872.
39. Oki, M., L. Valenzuela, T. Chiba, T. Ito, and R. T. Kamakaka. 2004. Barrier proteins remodel and modify chromatin to restrict silenced domains. Mol. Cell. Biol. 24:1956-1967.
40. Oki, M., and R. T. Kamakaka. 2005. Barrier function at HMR. Mol. Cell 19:707-716.
41. Osada, S., A. Sutton, N. Muster, C. E. Brown, J. R. Yates III, R. Sternglanz, and J. L. Workman. 2001. The yeast SAS (something about silencing) protein complex contains a MYST-type putative acetyltransferase and functions with chromatin assembly factor Asf1. Genes Dev. 15:3155-3168.
42. Parelho, V., S. Hadjur, M. Spivakov, M. Leleu, S. Sauer, H. C. Gregson, A. Jarmuz, C. Canzonetta, Z. Webster, T. Nesterova, B. S. Cobb, K. Yokomori, N. Dillon, L. Aragon, A. G. Fisher, and M. Merkenschlager. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422-433.
43. Scott, K. C., S. L. Merrett, and H. F. Willard. 2006. A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr. Biol. 16:119-129.
44. Shia, W. J., S. Osada, L. Florens, S. K. Swanson, M. P. Washburn, and J. L. Workman. 2005. Characterization of the yeast trimeric-SAS acetyltransferase complex. J. Biol. Chem. 280:11987-11994.
45. Shou, W., J. H. Seol, A. Shevchenko, C. Baskerville, D. Moazed, Z. W. Chen, J. Jang, A. Shevchenko, H. Charbonneau, and R. J. Deshaies. 1999. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 97:233-244.
46. Thr gene upstream of STE6 is a barrier to repression in MATα cells and exerts a potential tRNA position effect in MATa cells. Nucleic Acids Res. 32:5206-5213.
47. Simms, T. A., S. L. Dugas, J. C. Gremillion, M. E. Ibos, M. N. Dandurand, T. T. Toliver, D. J. Edwards, and D. Donze. 2008. TFIIIC binding sites function as both heterochromatin barriers and chromatin insulators in Saccharomyces cerevisiae. Eukaryot. Cell 7:2078-2086.
48. Sinclair, D. A., and L. Guarente. 1997. Extrachromosomal rDNA circles - a cause of aging in yeast. Cell 91:1033-1042.
49. Smith, J. S., and J. D. Boeke. 1997. An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 11:241-254.
50. Smith, J. S., C. B. Brachmann, L. Pillus, and J. D. Boeke. 1998. Distribution of a limited Sir2 protein pool regulates the strength of yeast rDNA silencing and is modulated by Sir4p. Genetics 149:1205-1219.
51. Storici, F., L. K. Lewis, and M. A. Resnick. 2001. In vivo site-directed mutagenesis using oligonucleotides. Nat. Biotechnol. 19:773-776.
52. Straight, A. F., W. Shou, G. J. Dowd, C. W. Turck, R. J. Deshaies, A. D. Johnson, and D. Moazed. 1999. Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell 97:245-256.
53. Strunnikov, A. V., V. L. Larionov, and D. Koshland. 1993. SMC1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J. Cell Biol. 123:1635-1648.
54. Suka, N., K. Luo, and M. Grunstein. 2002. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat. Genet. 32:378-383.
55. Sutton, A., W. J. Shia, D. Band, P. D. Kaufman, S. Osada, J. L. Workman, and R. Sternglanz. 2003. Sas4 and Sas5 are required for the histone acetyltransferase activity of Sas2 in the SAS complex. J. Biol. Chem. 278:16887-16892.
56. Takahashi, H., J. M. McCaffery, R. A. Irizarry, and J. D. Boeke. 2006. Nucleocytosolic acetyl-coenzyme a synthetase is required for histone acetylation and global transcription. Mol. Cell 23:207-217.
57. Takechi, S., and T. Nakayama. 1999. Sas3 is a histone acetyl transferase and requires a zinc finger motif. Biochem. Biophys. Res. Commun. 266:405-410.
58. Tanaka, T., M. P. Cosma, K. Wirth, and K. Nasmyth. 1999. Identification of cohesin association sites at centromeres and along chromosome arms. Cell 98:847-858.
59. Turner, B. M. 1993. Decoding the nucleosome. Cell 75:5-8.
60. Valenzuela, L., and R. T. Kamakaka. 2006. Chromatin insulators. Annu. Rev. Genet. 40:107-138.
61. Wendt, K. S., K. Yoshida, T. Itoh, M. Bando, B. Koch, E. Schirghuber, S. Tsutsumi, G. Nagae, K. Ishihara, T. Mishiro, K. Yahata, F. Imamoto, H. Aburatani, M. Nakao, N. Imamoto, K. Maeshima, K. Shirahige, and J. M. Peters. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796-801.
62. West, A., S. Huang, M. Gaszner, M. Litt, and G. Felsenfeld. 2004. Recruitment of histone modifications by USF proteins at a vertebrate barrier element. Mol. Cell 16:453-463.
63. Xu, E. Y., S. Kim, K. Replogle, J. Rine, and D. H. Rivier. 1999. Identification of SAS4 and SAS5, two genes that regulate silencing in Saccharomyces cerevisiae. Genetics 153:13-23.
64. Xu, E. Y., S. Kim, and D. H. Rivier. 1999. SAS4 and SAS5 are locus-specific regulators of silencing in Saccharomyces cerevisiae. Genetics 153:25-33.
65. Zhang, W., J. R. Bone, D. G. Edmondson, B. M. Turner, and S. Y. Roth. 1998. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J. 17:3155-3167.
66. Zhou, J., and S. L. Berger. 2004. Good fences make good neighbors: barrier elements and genomic regulation. Mol. Cell 16:500-502.