Compositional and structural analysis of selected chromosomal domains from Saccharomyces cerevisiae

Nucleic Acids Research

Volumn 42, Issue 1, 2014, Pages

  Hamperl, Stephan ^a   Brown, Christopher R ^b   Garea, Ana Villar ^a   Perez Fernandez, Jorge ^a   Bruckmann, Astrid ^a   Huber, Katharina ^a   Wittner, Manuel ^a   Babl, Virginia ^a   Stoeckl, Ulrike ^a   Deutzmann, Rainer ^a   Boeger, Hinrich ^b   Tschochner, Herbert ^a   Milkereit, Philipp ^a   Griesenbeck, Joachim ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; DNA DIRECTED RNA POLYMERASE III; RIBOSOME DNA; RNA POLYMERASE II;

ARTICLE; AUTONOMOUS REPLICATION SEQUENCE; BIOCHEMICAL COMPOSITION; CHROMATIN STRUCTURE; CHROMOSOMAL DOMAIN; CHROMOSOMAL PARAMETERS; CONTROLLED STUDY; ELECTRON MICROSCOPY; FUNGAL GENE; FUNGAL GENOME; GENE CLUSTER; GENE DOSAGE; GENE ISOLATION; GENE LOCUS; GENOME ANALYSIS; HISTONE MODIFICATION; MASS SPECTROMETRY; NONHUMAN; NUCLEOSOME; PHO5 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; PROTEOMICS; RNA GENE; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

EID: 84891793959     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt891     Document Type: Article

References (90)

1. Kornberg, R.D. and Lorch, Y. (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell, 98, 285-294
2. Rando, O.J. (2012) Combinatorial complexity in chromatin structure and function: Revisiting the histone code. Curr. Opin. Genet. Dev., 22, 148-155
3. Collas, P. (2010) The current state of chromatin immunoprecipitation. Mol. Biotechnol., 45, 87-100
4. Ansari, A. and Gartenberg, M.R. (1999) Persistence of an alternate chromatin structure at silenced loci in vitro. Proc. Natl Acad. Sci. USA, 96, 343-348
5. Boffa, L.C., Carpaneto, E.M. and Allfrey, V.G. (1995) Isolation of active genes containing CAG repeats by DNA strand invasion by a peptide nucleic acid. Proc. Natl Acad. Sci. USA, 92, 1901-1905
6. Ghirlando, R. and Felsenfeld, G. (2008) Hydrodynamic studies on defined heterochromatin fragments support a 30-nm fiber having six nucleosomes per turn. J. Mol. Biol., 376, 1417-1425
7. Griesenbeck, J., Boeger, H., Strattan, J.S. and Kornberg, R.D. (2003) Affinity purification of specific chromatin segments from chromosomal loci in yeast. Mol. Cell. Biol., 23, 9275-9282
8. Higashinakagawa, T., Wahn, H. and Reeder, R.H. (1977) Isolation of ribosomal gene chromatin. Dev. Biol., 55, 375-386
9. Simpson, R.T., Ducker, C.E., Diller, J.D. and Ruan, C. (2004) Purification of native, defined chromatin segments. Methods Enzymol., 375, 158-170
10. Workman, J.L. and Langmore, J.P. (1985) Nucleoprotein hybridization: A method for isolating specific genes as high molecular weight chromatin. Biochemistry, 24, 7486-7497
11. Zhang, X.Y. and Hörz, W. (1982) Analysis of highly purified satellite DNA containing chromatin from the mouse. Nucleic Acids Res., 10, 1481-1494
12. Antäo, J.M., Mason, J.M., Dé jardin, J. and Kingston, R.E. (2012) Protein landscape at Drosophila melanogaster telomere-Associated sequence repeats. Mol. Cell. Biol., 32, 2170-2182
13. Dé jardin, J. and Kingston, R.E. (2009) Purification of proteins associated with specific genomic Loci. Cell, 136, 175-186
14. Byrum, S.D., Raman, A., Taverna, S.D. and Tackett, A.J. (2012) ChAP-MS: A method for identification of proteins and histone posttranslational modifications at a single genomic locus. Cell Rep., 2, 198-205
15. Akiyoshi, B., Nelson, C.R., Ranish, J.A. and Biggins, S. (2009) Quantitative proteomic analysis of purified yeast kinetochores identifies a PP1 regulatory subunit. Genes Dev., 23, 2887-2899
16. Unnikrishnan, A., Gafken, P.R. and Tsukiyama, T. (2010) Dynamic changes in histone acetylation regulate origins of DNA replication. Nat. Struct. Mol. Biol., 17, 430-437
17. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Seraphin, B. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotech., 17, 1030-1032
18. Hamperl, S., Wittner, M., Babl, V., Perez-Fernandez, J., Tschochner, H. and Griesenbeck, J. (2013) Chromatin states at ribosomal DNA loci. Biochim. Biophys. Acta, 1829, 405-417
19. Longtine, M.S., McKenzie, A. III, Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J.R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast, 14, 953-961
20. Green, M.R., Sambrook, J. and Cold Spring Harbor Laboratory (2012) Molecular Cloning: A Laboratory Manual (Fourth Edition): Three-Volume Set 0004 ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y
21. Reiter, A., Hamperl, S., Seitz, H., Merkl, P., Perez-Fernandez, J., Williams, L., Gerber, J., Németh, A., Lé ger, I., Gadal, O. et al. (2012) The Reb1-homologue Ydr026c/Nsi1 is required for efficient RNA polymerase I termination in yeast. EMBO J., 31, 3480-3493
22. Gietz, R.D. and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene, 74, 527-534
23. Wai, H.H., Vu, L., Oakes, M. and Nomura, M. (2000) Complete deletion of yeast chromosomal rDNA repeats and integration of a new rDNA repeat: Use of rDNA deletion strains for functional analysis of rDNA promoter elements in vivo. Nucleic Acids Res., 28, 3524-3534
24. Griesenbeck, J., Boeger, H., Strattan, J.S. and Kornberg, R.D. (2004) Purification of defined chromosomal domains. Methods Enzymol., 375, 170-178
25. Wai, H., Johzuka, K., Vu, L., Eliason, K., Kobayashi, T., Horiuchi, T. and Nomura, M. (2001) Yeast RNA polymerase I enhancer is dispensable for transcription of the chromosomal rRNA gene and cell growth, and its apparent transcription enhancement from ectopic promoters requires Fob1 protein. Mol. Cell. Biol., 21, 5541-5553
26. Merz, K., Hondele, M., Goetze, H., Gmelch, K., Stoeckl, U. and Griesenbeck, J. (2008) Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev., 22, 1190-1204
27. Mumberg, D., Müller, R. and Funk, M. (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene, 156, 119-122
28. Oeffinger, M., Wei, K.E., Rogers, R., DeGrasse, J.A., Chait, B.T., Aitchison, J.D. and Rout, M.P. (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods, 4, 951-956
29. Jakob, S., Ohmayer, U., Neueder, A., Hierlmeier, T., Perez- Fernandez, J., Hochmuth, E., Deutzmann, R., Griesenbeck, J., Tschochner, H. and Milkereit, P. (2012) Interrelationships between yeast ribosomal protein assembly events and transient ribosome biogenesis factors interactions in early pre-ribosomes. PLoS ONE, 7, e32552
30. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354
31. Villar-Garea, A., Israel, L. and Imhof, A. (2008) Analysis of histone modifications by mass spectrometry. Curr. Protoc. Protein Sci., Chapter 14, Unit 14.10
32. Strohalm, M., Hassman, M., Kosata, B. and Kodícek, M. (2008) mMass data miner: An open source alternative for mass spectrometric data analysis. Rapid Commun. Mass Spectrom., 22, 905-908
33. Strohalm, M., Kavan, D., Nová k, P., Volný, M. and Havlícek, V. (2010) mMass 3: A cross-platform software environment for precise analysis of mass spectrometric data. Anal. Chem., 82, 4648-4651
34. Wessel, D. and Flügge, U.I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem., 138, 141-143
35. Goetze, H., Wittner, M., Hamperl, S., Hondele, M., Merz, K., Stoeckl, U. and Griesenbeck, J. (2010) Alternative chromatin structures of the 35S rRNA genes in saccharomyces cerevisiae provide a molecular basis for the selective recruitment of RNA polymerases I and II. Mol. Cell. Biol., 30, 2028-2045
36. Sogo, J.M. and Thoma, F. (1989) Electron microscopy of chromatin. Methods Enzymol., 170, 142-165
37. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 9, 671-675
38. Li, C., Mueller, J.E. and Bryk, M. (2006) Sir2 represses endogenous polymerase II transcription units in the ribosomal DNA nontranscribed spacer. Mol. Biol. Cell, 17, 3848-3859
39. Cesarini, E., Mariotti, F.R., Cioci, F. and Camilloni, G. (2010) RNA polymerase I transcription silences noncoding RNAs at the ribosomal DNA locus in Saccharomyces cerevisiae. Eukaryotic Cell, 9, 325-335
40. Li, Q., Zhou, H., Wurtele, H., Davies, B., Horazdovsky, B., Verreault, A. and Zhang, Z. (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell, 134, 244-255
41. Clemente-Ruiz, M., Gonzá lez-Prieto, R. and Prado, F. (2011) Histone H3K56 acetylation, CAF1, and Rtt106 coordinate nucleosome assembly and stability of advancing replication forks. PLoS Genet., 7, e1002376
42. Ng, H.H., Ciccone, D.N., Morshead, K.B., Oettinger, M.A. and Struhl, K. (2003) Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: A potential mechanism for position-effect variegation. Proc. Natl Acad. Sci. USA, 100, 1820-1825
43. Vannini, A. and Cramer, P. (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol. Cell, 45, 439-446
44. Lue, N.F. and Kornberg, R.D. (1993) A possible role for the yeast TATA-element-binding protein in DNA replication. Proc. Natl Acad. Sci. USA, 90, 8018-8022
45. Stagljar, I., Hübscher, U. and Barberis, A. (1999) Activation of DNA replication in yeast by recruitment of the RNA polymerase II transcription complex. Biol. Chem., 380, 525-530
46. Ross, P.L., Huang, Y.N., Marchese, J.N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S. et al. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics, 3, 1154-1169
47. Freidkin, I. and Katcoff, D.J. (2001) Specific distribution of the Saccharomyces cerevisiae linker histone homolog HHO1p in the chromatin. Nucleic Acids Res., 29, 4043-4051
48. Levy, A., Eyal, M., Hershkovits, G., Salmon-Divon, M., Klutstein, M. and Katcoff, D.J. (2008) Yeast linker histone Hho1p is required for efficient RNA polymerase I processivity and transcriptional silencing at the ribosomal DNA. Proc. Natl Acad. Sci. USA, 105, 11703-11708
49. Costa, A. and Onesti, S. (2008) The MCM complex: (just) a replicative helicasëBiochem. Soc. Trans., 36, 136-140
50. Conrad-Webb, H. and Butow, R.A. (1995) A polymerase switch in the synthesis of rRNA in Saccharomyces cerevisiae. Mol. Cell. Biol., 15, 2420-2428
51. Mayán, M.D. (2013) RNAP-II transcribes two small RNAs at the promoter and terminator regions of the RNAP-I gene in Saccharomyces cerevisiae. Yeast, 30, 25-32
52. Siddiqi, I.N., Dodd, J.A., Vu, L., Eliason, K., Oakes, M.L., Keener, J., Moore, R., Young, M.K. and Nomura, M. (2001) Transcription of chromosomal rRNA genes by both RNA polymerase I and II in yeast uaf30 mutants lacking the 30 kDa subunit of transcription factor UAF. EMBO J., 20, 4512-4521
53. Smith, J.S. and Boeke, J.D. (1997) An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev., 11, 241-254
54. Vu, L., Siddiqi, I., Lee, B.S., Josaitis, C.A. and Nomura, M. (1999) RNA polymerase switch in transcription of yeast rDNA: Role of transcription factor UAF (upstream activation factor) in silencing rDNA transcription by RNA polymerase II. Proc. Natl Acad. Sci. USA, 96, 4390-4395
55. Mougey, E.B., O'Reilly, M., Osheim, Y., Miller, O.L. Jr, Beyer, A. and Sollner-Webb, B. (1993) The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. Genes Dev., 7, 1609-1619
56. Osheim, Y.N., French, S.L., Keck, K.M., Champion, E.A., Spasov, K., Dragon, F., Baserga, S.J. and Beyer, A.L. (2004) Pre-18S Ribosomal RNA Is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol. Cell, 16, 943-954
57. Wery, M., Ruidant, S., Schillewaert, S., Leporé, N. and Lafontaine, D.L.J. (2009) The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA, 15, 406-419
58. Hierlmeier, T., Merl, J., Sauert, M., Perez-Fernandez, J., Schultz, P., Bruckmann, A., Hamperl, S., Ohmayer, U., Rachel, R., Jacob, A. et al. (2013) Rrp5p, Noc1p and Noc2p form a protein module which is part of early large ribosomal subunit precursors in S. cerevisiae. Nucleic Acids Res., 41, 1191-1210
59. Jones, H.S., Kawauchi, J., Braglia, P., Alen, C.M., Kent, N.A. and Proudfoot, N.J. (2007) RNA polymerase I in yeast transcribes dynamic nucleosomal rDNA. Nat. Struct. Mol. Biol., 14, 123-130
60. Mueller, J.E. and Bryk, M. (2007) Isw1 acts independently of the Isw1a and Isw1b complexes in regulating transcriptional silencing at the ribosomal DNA locus in Saccharomyces cerevisiae. J. Mol. Biol., 371, 1-10
61. Schmid, M., Durussel, T. and Laemmli, U.K. (2004) ChIC and ChEC: Genomic mapping of chromatin proteins. Mol. Cell, 16, 147-157
62. Todd, R.B. and Andrianopoulos, A. (1997) Evolution of a fungal regulatory gene family: The Zn(II)2Cys6 binuclear cluster DNA binding motif. Fungal Genet. Biol., 21, 388-405
63. 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
64. Zhu, C., Byers, K.J.R.P., McCord, R.P., Shi, Z., Berger, M.F., Newburger, D.E., Saulrieta, K., Smith, Z., Shah, M.V., Radhakrishnan, M. et al. (2009) High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res., 19, 556-566
65. Kuzuhara, T. and Horikoshi, M. (2004) A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing. Nat. Struct. Mol. Biol., 11, 275-283
66. Cech, T. and Pardue, M.L. (1977) Cross-linking of DNA with trimethylpsoralen is a probe for chromatin structure. Cell, 11, 631-640
67. Cech, T., Potter, D. and Pardue, M.L. (1977) Electron microscopy of DNA cross-linked with trimethylpsoralen: A probe for chromatin structure. Biochemistry, 16, 5313-5321
68. 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
69. French, S.L., Osheim, Y.N., Schneider, D.A., Sikes, M.L., Fernandez, C.F., Copela, L.A., Misra, V.A., Nomura, M., Wolin, S.L. and Beyer, A.L. (2008) Visual analysis of the yeast 5S rRNA gene transcriptome: Regulation and role of La protein. Mol. Cell. Biol., 28, 4576-4587
70. Yoshida, K., Ogawa, N. and Oshima, Y. (1989) Function of the PHO regulatory genes for repressible acid phosphatase synthesis in Saccharomyces cerevisiae. Mol. Gen. Genet., 217, 40-46
71. 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
72. Almer, A., Rudolph, H., Hinnen, A. and Hörz, 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
73. 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
74. Adkins, M.W., Williams, S.K., Linger, J. and Tyler, J.K. (2007) Chromatin disassembly from the PHO5 promoter is essential for the recruitment of the general transcription machinery and coactivators. Mol. Cell. Biol., 27, 6372-6382
75. Brown, C.R., Mao, C., Falkovskaia, E., Law, J.K. and Boeger, H. (2011) In vivo role for the chromatin-remodeling enzyme SWI/SNF in the removal of promoter nucleosomes by disassembly rather than sliding. J. Biol. Chem., 286, 40556-40565
76. Dhasarathy, A. and Kladde, M.P. (2005) Promoter occupancy is a major determinant of chromatin remodeling enzyme requirements. Mol. Cell. Biol., 25, 2698-2707
77. 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
78. Mao, C., Brown, C.R., Griesenbeck, J. and Boeger, H. (2011) Occlusion of regulatory sequences by promoter nucleosomes in vivo. PLoS ONE, 6, e17521
79. Nogi, Y., Vu, L. and Nomura, M. (1991) An approach for isolation of mutants defective in 35S ribosomal RNA synthesis in Saccharomyces cerevisiae. Proc. Natl, Acd. Sci. USA, 88, 7026-7030
80. Fath, S., Milkereit, P., Podtelejnikov, A.V., Bischler, N., Schultz, P., Bier, M., Mann, M. and Tschochner, H. (2000) Association of yeast RNA polymerase I with a nucleolar substructure active in rRNA synthesis and processing. J. Cell Biol., 149, 575-590
81. Kobayashi, T. and Ganley, A.R.D. (2005) Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science, 309, 1581-1584
82. Poole, A.M., Kobayashi, T and Ganley, A.R.D. (2012) A positive role for yeast extrachromosomal rDNA circles? Bioessays, 34, 725-729
83. Cioci, F., Vu, L., Eliason, K., Oakes, M., Siddiqi, I.N. and Nomura, M. (2003) Silencing in yeast rDNA chromatin: Reciprocal relationship in gene expression between RNA polymerase I and II. Mol. Cell, 12, 135-145
84. 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
85. 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
86. 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
87. Huh, W-K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S. and O'Shea, E.K. (2003) Global analysis of protein localization in budding yeast. Nature, 425, 686-691
88. Nogi, Y., Yano, R., Dodd, J., Carles, C. and Nomura, M. (1993) Gene RRN4 in Saccharomyces cerevisiae encodes the A12.2 subunit of RNA polymerase I and Is essential only at high temperatures. Mol. Cell. Biol., 13, 114-122
89. Sengstag, C. and Hinnen, A. (1987) The sequence of the Saccharomyces cerevisiae gene PH02 codes for a regulatory protein with unusual aminoacid composition. Nucl. Acids Res., 15, 233-246
90. Buhler, J.M., Huet, J., Davies, K.E., Sentenac, A. and Fromageot, P. (1980) Immunological studies of yeast nuclear RNA polymerases at the subunit level. J. Biol. Chem., 255, 9949-9954