The RSC chromatin remodeling complex has a crucial role in the complete remodeler set for yeast PHO5 promoter opening

Nucleic Acids Research

Volumn 42, Issue 7, 2014, Pages 4270-4282

  Musladin, Sanja ^a   Krietenstein, Nils ^b   Korber, Philipp ^b   Barbaric, Slobodan ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATASE; TRANSCRIPTION FACTOR GAL4;

ARTICLE; CHD1 GENE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INACTIVATION; GENE INTERACTION; GENETIC VARIABILITY; IN VIVO STUDY; ISW1 GENE; NONHUMAN; PHO5 GENE; PHO8 GENE; PHO84 GENE; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SNF2 GENE; STH1 GENE; TRANSCRIPTION REGULATION;

ACID PHOSPHATASE; ADENOSINE TRIPHOSPHATASES; ALKALINE PHOSPHATASE; CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYCLINS; DNA-BINDING PROTEINS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84897947228     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1395     Document Type: Article

References (69)

1. Tirosh, I. and Barkai, N. (2008) Two strategies for gene regulation by promoter nucleosomes. Genome Res., 18, 1084-1091. (Pubitemid 351931159)
2. Cairns, B.R. (2009) The logic of chromatin architecture and remodelling at promoters. Nature, 461, 193-198.
3. Morse, R.H. (2007) Transcription factor access to promoter elements. J. Cell Biochem., 102, 560-570. (Pubitemid 47557411)
4. Rando, O.J. and Winston, F. (2012) Chromatin and transcription in yeast. Genetics, 190, 351-387.
5. Almer, A., Rudolph, H., Hinnen, A. and Horz, W. (1986) Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J., 5, 2689-2696.
6. Wippo, C.J., Krstulovic, B.S., Ertel, F., Musladin, S., Blaschke, D., Sturzl, S., Yuan, G.C., Horz, W., Korber, P. and Barbaric, S. (2009) Differential cofactor requirements for histone eviction from two nucleosomes at the yeast PHO84 promoter are determined by intrinsic nucleosome stability. Mol. Cell. Biol., 29, 2960-2981.
7. Lam, F.H., Steger, D.J. and O'Shea, E.K. (2008) Chromatin decouples promoter threshold from dynamic range. Nature, 453, 246-250. (Pubitemid 351667976)
8. Barbaric, S., Fascher, K.D. and Horz, W. (1992) Activation of the weakly regulated PHO8 promoter in S cerevisiae: chromatin transition and binding sites for the positive regulator protein Pho4. Nucleic Acids Res., 20, 1031-1038.
9. Fascher, K.D., Schmitz, J. and Horz, W. (1990) Role of trans-activating proteins in the generation of active chromatin at the PHO5 promoter in S cerevisiae. EMBO J., 9, 2523-2528.
10. Oshima, Y., Ogawa, N. and Harashima, S. (1996) Regulation of phosphatase synthesis in saccharomyces cerevisiae-a review. Gene, 179, 171-177. (Pubitemid 26395091)
11. Gregory, P.D., Schmid, A., Zavari, M., Munsterkotter, M. and Horz, W. (1999) Chromatin remodelling at the PHO8 promoter requires SWI-SNF and SAGA at a step subsequent to activator binding. EMBO J., 18, 6407-6414. (Pubitemid 29533244)
12. Barbaric, S., Walker, J., Schmid, A., Svejstrup, J.Q. and Horz, W. (2001) Increasing the rate of chromatin remodeling and gene activation-a novel role for the histone acetyltransferase Gcn5. EMBO J., 20, 4944-4951. (Pubitemid 32848646)
13. Barbaric, S., Luckenbach, T., Schmid, A., Blaschke, D., Horz, W. and Korber, P. (2007) Redundancy of chromatin remodeling pathways for the induction of the yeast PHO5 promoter in vivo. J. Biol. Chem., 282, 27610-27621. (Pubitemid 47529480)
14. Schmid, A., Fascher, K.D. and Horz, W. (1992) Nucleosome disruption at the yeast PHO5 promoter upon PHO5 induction occurs in the absence of DNA replication. Cell, 71, 853-864.
15. Fascher, K.D., Schmitz, J. and Horz, W. (1993) Structural and functional requirements for the chromatin transition at the PHO5 promoter in Saccharomyces cerevisiae upon PHO5 activation. J. Mol. Biol., 231, 658-667. (Pubitemid 23211305)
16. Clapier, C.R. and Cairns, B.R. (2009) The biology of chromatin remodeling complexes. Annu. Rev. Biochem., 78, 273-304.
17. Eisen, J.A., Sweder, K.S. and Hanawalt, P.C. (1995) Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res., 23, 2715-2723.
18. Flaus, A., Martin, D.M., Barton, G.J. and Owen-Hughes, T. (2006) Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res., 34, 2887-2905. (Pubitemid 44540417)
19. Steger, D.J., Haswell, E.S., Miller, A.L., Wente, S.R. and O'Shea, E.K. (2003) Regulation of chromatin remodeling by inositol polyphosphates. Science, 299, 114-116. (Pubitemid 36042415)
20. Neef, D.W. and Kladde, M.P. (2003) Polyphosphate loss promotes SNF/SWI-and Gcn5-dependent mitotic induction of PHO5. Mol. Cell. Biol., 23, 3788-3797. (Pubitemid 36597459)
21. Dhasarathy, A. and Kladde, M.P. (2005) Promoter occupancy is a major determinant of chromatin remodeling enzyme requirements. Mol. Cell. Biol., 25, 2698-2707. (Pubitemid 40381633)
22. Reinke, H. and Horz, W. (2003) Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol. Cell, 11, 1599-1607. (Pubitemid 36776545)
23. Huang, S. and O'Shea, E.K. (2005) A systematic high-throughput screen of a yeast deletion collection for mutants defective in PHO5 regulation. Genetics, 169, 1859-1871. (Pubitemid 40695603)
24. Boeger, H., Griesenbeck, J., Strattan, J.S. and Kornberg, R.D. (2004) Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Mol. Cell, 14, 667-673. (Pubitemid 38739088)
25. Ehrensberger, A.H. and Kornberg, R.D. (2011) Isolation of an activator-dependent, promoter-specific chromatin remodeling factor. Proc. Natl Acad. Sci. USA, 108, 10115-10120.
26. Ghaemmaghami, S., Huh, W.K., Bower, K., Howson, R.W., Belle, A., Dephoure, N., O'Shea, E.K. and Weissman, J.S. (2003) Global analysis of protein expression in yeast. Nature, 425, 737-741. (Pubitemid 37314318)
27. Cairns, B.R., Lorch, Y., Li, Y., Zhang, M.C., Lacomis, L., Erdjument-Bromage, H., Tempst, P., Du, J., Laurent, B. and Kornberg, R.D. (1996) RSC, an essential, abundant chromatin-remodeling complex. Cell, 87, 1249-1260. (Pubitemid 27010108)
28. Parnell, T.J., Huff, J.T. and Cairns, B.R. (2008) RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. EMBO J., 27, 100-110.
29. Badis, G., Chan, E.T., van Bakel, H., Pena-Castillo, L., Tillo, D., Tsui, K., Carlson, C.D., Gossett, A.J., Hasinoff, M.J., Warren, C.L. et al. (2008) A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell, 32, 878-887.
30. Hartley, P.D. and Madhani, H.D. (2009) Mechanisms that specify promoter nucleosome location and identity. Cell, 137, 445-458.
31. Lorch, Y., Maier-Davis, B. and Kornberg, R.D. (2006) Chromatin remodeling by nucleosome disassembly in vitro. Proc. Natl Acad. Sci. USA, 103, 3090-3093. (Pubitemid 43346429)
32. Boeger, H., Griesenbeck, J., Strattan, J.S. and Kornberg, R.D. (2003) Nucleosomes unfold completely at a transcriptionally active promoter. Mol. Cell, 11, 1587-1598. (Pubitemid 36776544)
33. Korber, P., Luckenbach, T., Blaschke, D. and Horz, W. (2004) Evidence for histone eviction in trans upon induction of the yeast PHO5 promoter. Mol. Cell. Biol., 24, 10965-10974. (Pubitemid 39603150)
34. Boeger, H., Griesenbeck, J. and Kornberg, R.D. (2008) Nucleosome retention and the stochastic nature of promoter chromatin remodeling for transcription. Cell, 133, 716-726. (Pubitemid 351636300)
35. Cairns, B.R. (2007) Chromatin remodeling: insights and intrigue from single-molecule studies. Nat. Struct. Mol. Biol., 14, 989-996. (Pubitemid 350060341)
36. Lorch, Y., Griesenbeck, J., Boeger, H., Maier-Davis, B. and Kornberg, R.D. (2011) Selective removal of promoter nucleosomes by the RSC chromatin-remodeling complex. Nat. Struct. Mol. Biol., 18, 881-885.
37. Auesukaree, C., Homma, T., Tochio, H., Shirakawa, M., Kaneko, Y. and Harashima, S. (2004) Intracellular phosphate serves as a signal for the regulation of the PHO pathway in Saccharomyces cerevisiae. J. Biol. Chem., 279, 17289-17294. (Pubitemid 38560488)
38. Thomas, M.R. and O'Shea, E.K. (2005) An intracellular phosphate buffer filters transient fluctuations in extracellular phosphate levels. Proc. Natl Acad. Sci. USA, 102, 9565-9570. (Pubitemid 40981721)
39. Gaudreau, L., Schmid, A., Blaschke, D., Ptashne, M. and Horz, W. (1997) RNA polymerase II holoenzyme recruitment is sufficient to remodel chromatin at the yeast PHO5 promoter. Cell, 89, 55-62. (Pubitemid 27180585)
40. Amberg, D.C., Burke, D.J. and Strathern, J.N. (2005) Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
41. Korber, P., Barbaric, S., Luckenbach, T., Schmid, A., Schermer, U.J., Blaschke, D. and Horz, W. (2006) The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters. J. Biol. Chem., 281, 5539-5545. (Pubitemid 43847649)
42. Straka, C. and Horz, W. (1991) A functional role for nucleosomes in the repression of a yeast promoter. EMBO J., 10, 361-368. (Pubitemid 21905486)
43. Ertinger, G. (1998) Rolle der Transkriptionsfaktoren bei der Offnung der Chromatinstruktur am PHO5-Promoter in Saccharomyces cerevisiae. Ph.D Thesis. Universitat Munchen.
44. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
45. Carroll, A.S., Bishop, A.C., DeRisi, J.L., Shokat, K.M. and O'Shea, E.K. (2001) Chemical inhibition of the Pho85 cyclin-dependent kinase reveals a role in the environmental stress response. Proc. Natl Acad. Sci. USA, 98, 12578-12583. (Pubitemid 33019988)
46. Haguenauer-Tsapis, R. and Hinnen, A. (1984) A deletion that includes the signal peptidase cleavage site impairs processing, glycosylation, and secretion of cell surface yeast acid phosphatase. Mol. Cell. Biol., 4, 2668-2675. (Pubitemid 15113605)
47. Barbaric, S., Kozulic, B., Ries, B. and Mildner, P. (1980) Purification and evidence for heterogeneity of acid phosphatase from Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun., 95, 404-409.
48. Svaren, J., Venter, U. and Horz, W. (1995) In vivo analysis of nucleosome structure and transcription factor binding in Saccharomyces cerevisiae. Methods Mol. Genet., 6, 153-167.
49. Gregory, P.D. and Horz, W. (1999) Mapping chromatin structure in yeast. Methods Enzymol., 304, 365-376. (Pubitemid 29268893)
50. Gregory, P.D., Barbaric, S. and Horz, W. (1999) Restriction nucleases as probes for chromatin structure. Methods Mol. Biol., 119, 417-425.
51. Dohmen, R.J., Wu, P. and Varshavsky, A. (1994) Heat-inducible degron: a method for constructing temperature-sensitive mutants. Science, 263, 1273-1276. (Pubitemid 24107546)
52. Ertel, F., Dirac-Svejstrup, A.B., Hertel, C.B., Blaschke, D., Svejstrup, J.Q. and Korber, P. (2010) In vitro reconstitution of PHO5 promoter chromatin remodeling points to a role for activator-nucleosome competition in vivo. Mol. Cell. Biol., 30, 4060-4076.
53. Campsteijn, C., Wijnands-Collin, A.M. and Logie, C. (2007) Reverse genetic analysis of the yeast RSC chromatin remodeler reveals a role for RSC3 and SNF5 homolog 1 in ploidy maintenance. PloS Genet., 3, e92.
54. Tsuchiya, E., Uno, M., Kiguchi, A., Masuoka, K., Kanemori, Y., Okabe, S. and Mikayawa, T. (1992) The Saccharomyces cerevisiae NPS1 gene, a novel CDC gene which encodes a 160 kDa nuclear protein involved in G2 phase control. EMBO J., 11, 4017-4026.
55. Du, J., Nasir, I., Benton, B.K., Kladde, M.P. and Laurent, B.C. (1998) Sth1p, a Saccharomyces cerevisiae Snf2p/Swi2p homolog, is an essential ATPase in RSC and differs from Snf/Swi in its interactions with histones and chromatin-associated proteins. Genetics, 150, 987-1005. (Pubitemid 28510029)
56. Pondugula, S., Neef, D.W., Voth, W.P., Darst, R.P., Dhasarathy, A., Reynolds, M.M., Takahata, S., Stillman, D.J. and Kladde, M.P. (2009) Coupling phosphate homeostasis to cell cycle-specific transcription: mitotic activation of Saccharomyces cerevisiae PHO5 by Mcm1 and Forkhead proteins. Mol. Cell. Biol., 29, 4891-4905.
57. Madden, S.L., Creasy, C.L., Srinivas, V., Fawcett, W. and Bergman, L.W. (1988) Structure and expression of the PHO80 gene of Saccharomyces cerevisiae. Nucleic Acids Res., 16, 2625-2637.
58. Kaffman, A., Herskowitz, I., Tjian, R. and O'Shea, E.K. (1994) Phosphorylation of the transcription factor Pho4 by a cyclin-CDK complex, Pho80-Pho85. Science, 263, 1153-1156. (Pubitemid 24105964)
59. O'Neill, E.M., Kaffman, A., Jolly, E.R. and O'Shea, E.K. (1996) Regulation of Pho4 nuclear localization by the Pho80-Pho85 cyclin-CDK complex. Science, 271, 209-212.
60. Adkins, M.W., Howar, S.R. and Tyler, J.K. (2004) Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell, 14, 657-666. (Pubitemid 38739087)
61. Floer, M., Wang, X., Prabhu, V., Berrozpe, G., Narayan, S., Spagna, D., Alvarez, D., Kendall, J., Krasnitz, A., Stepansky, A. et al. (2010) A RSC/nucleosome complex determines chromatin architecture and facilitates activator binding. Cell, 141, 407-418.
62. Hota, S.K. and Bartholomew, B. (2011) Diversity of operation in ATP-dependent chromatin remodelers. Biochim. Biophys. Acta, 1809, 476-487.
63. Ryan, D.P. and Owen-Hughes, T. (2011) Snf2-family proteins: chromatin remodellers for any occasion. Curr. Opin. Chem. Biol., 15, 649-656.
64. Venters, B.J. and Pugh, B.F. (2009) A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res., 19, 360-371.
65. Wippo, C.J., Israel, L., Watanabe, S., Hochheimer, A., Peterson, C.L. and Korber, P. (2011) The RSC chromatin remodelling enzyme has a unique role in directing the accurate positioning of nucleosomes. EMBO J., 30, 1277-1288.
66. Ogawa, N., Saitoh, H., Miura, K., Magbanua, J.P.V., Bunya, M., Harashima, S. and Oshima, Y. (1995) Structure and distribution of specific cis-elements for transcriptional regulation of PHO84 in Saccharomyces cerevisiae. Mol. Gen. Genet., 249, 406-416. (Pubitemid 26019051)
67. Rudolph, H. and Hinnen, A. (1987) The yeast PHO5 promoter: phosphate-control elements and sequences mediating mRNA start-site selection. Proc. Natl Acad. Sci. USA, 84, 1340-1344. (Pubitemid 17027349)
68. Hertel, C.B., Langst, G., Horz, W. and Korber, P. (2005) Nucleosome stability at the yeast PHO5 and PHO8 promoters correlates with differential cofactor requirements for chromatin opening. Mol. Cell. Biol., 25, 10755-10767. (Pubitemid 41747121)
69. Partensky, P.D. and Narlikar, G.J. (2009) Chromatin remodelers act globally, sequence positions nucleosomes locally. J. Mol. Biol., 391, 12-25.