Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA

EMBO Journal

Volumn 16, Issue 21, 1997, Pages 6495-6509

  Fritze, Christian E ^a,b   Verschueren, Kristin ^a,c   Strich, Randy ^a,d   Esposito, Rochelle Easton ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c Celgen   (Belgium)

^d FOX CHASE CANCER CENTER   (United States)

Author keywords

Chromatin; rDNA; Silencing; Sir2

Indexed keywords

METHYLTRANSFERASE; MICROCOCCAL NUCLEASE; RIBOSOME DNA; RIBOSOME RNA; SPACER DNA;

ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA RECOMBINATION; FUNGAL GENETICS; GENE FUNCTION; GENE LOCUS; GENE MAPPING; MEIOSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; REGULATOR GENE; REPRESSOR GENE; SILENCER GENE; TELOMERE; TRANSCRIPTION TERMINATION; YEAST;

CHROMATIN; CHROMOSOMES, FUNGAL; DNA, FUNGAL; DNA, RIBOSOMAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HISTONE DEACETYLASES; PEPTIDES; RECOMBINATION, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, FUNGAL; RNA, RIBOSOMAL, 18S; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION; SILENT INFORMATION REGULATOR PROTEINS, SACCHAROMYCES CEREVISIAE; SIRTUINS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 0030831573     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.21.6495     Document Type: Article

References (94)

1. Aguilera,A. and Klein,H.L. (1990) HPR1, a novel yeast gene that prevents intrachromosomal excision recombination, shows carboxyterminal homology to the Saccharomyces cerevisiae TOP1 gene. Mol. Cell. Biol, 10, 1439-1451.
2. Alani,E., Cao,L. and Kleckner,N. (1987) A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics. 116, 541-545.
3. Aparicio,O.M. and Gottschling,D.E. (1994) Overcoming telomeric silencing: a trans-activator competes to establish gene expression in a cell cycle-dependent way. Genes Dev., 8, 1133-1146.
4. Aparicio,O.M., Billington,B.L. and Gottschling,D.E. (1991) Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell, 66, 1279-1287.
5. rk, A.J. and Sharp,P.A. (1977) Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell, 12, 721-732.
6. Bonven,B.J., Gocke,K. and Westergaard,O. (1985) A high affinity Topoisomerase I binding sequence is clustered at DNase I hypersensitive sites in Tetrahymena R chromatin. Cell, 41, 541-551.
7. Brachmann,C.B., Sherman,J.M., Devine,S.E., Cameron,E.E., Pillus,L. and Boeke,J.D. (1995) The SIR2 gene family, conserved from bacteria to humans, functions in silencing cell cycle progression, and chromosome stability. Genes Dev., 9, 2888-2902.
8. Brand,A.H., Breeden,L., Abraham,J., Sternglanz,R. and Nasmyth,K. (1985) Characterization of a 'silencer' in yeast: a DNA sequence with properties opposite to those of a transcriptional enhancer. Cell, 41, 41-48.
9. Brand,A.H., Micklem,G. and Nasmyth,K.A. (1987) A yeast silencer contains sequences that can promote autonomous plasmid replication and transcriptional activation. Cell, 51, 709-719.
10. Braunstein,M., Rose,A.B., Holmes,S.G., Allis,C.D. and Broach,J.R. (1993) Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev., 7, 592-604.
11. Brewer,B.J. and Fangman,W.L. (1988) A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell, 55, 637-643.
12. Bryk,M., Banerjee,M., Mutphy,M., Knudsen,K.E., Garfinkel,D.J. and Curcio,M.J. (1997) Transcriptional silencing of Ty1 elements in the RDN1 locus of yeast. Genes Dev., 11, 255-269.
13. Buchman,A.R., Kimmerly,WJ., Rine,J. and Kornberg,R.D. (1988) Two DNA-hinding factors recognize specific sequences at silencers. upstream activating sequences, autonomously replicating sequences. and telomeres in Saccharomyces cerevisiae. Mol. Cell. Biol., 8, 210-225.
14. Chien,C.T., Buck,S., Sternglanz,R. and Shore,D. (1993) Targeting of SIR1 protein establishes transcriptional silencing at HM loci and telomeres in yeast. Cell, 75, 531-541.
15. Christianson,T.W., Sikorski,R.S., Dante,M., Shero,J.H. and Hieter,P. (1992) Multifunctional yeast higli-copy-number shuttle vectors. Gene. 110, 119-122.
16. Chrtstman,M.K. Dietrich,F.S. and Fink,G.R. (1988) Mitotic recombination in the rDNA of S. cerevisiae is suppressed by the combined action of DNA topoisomerases I and II. Cell. 55, 413-425.
17. Dammann,R., Luechini,R., Koller,T. and Sogo,J.M. (1993) Chromatin structures and transcription of rDNA in yeast. Saccharomyces cerevisiae. Nucleic Acids Res., 21, 2331-2338.
18. Derbyshire,M.K., Weinstock,K.G. and Strathern,J.N. (1996) HST1. a neu member of the SIR2 family of genes. Yeast, 12, 631-640.
19. Diffley,J.K and Stillman,B. (1988) Purification of a yeast protein that binds to origins of DNA replication and a transcriptional silencer. Proc. Natl Acad. Sci. USA, 85, 2120-2124.
20. Dower,W.J., Miller,J.F. and Ragsdale,C.W. (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res., 16, 6127-6145.
21. Ferguson,B.M. and Fangman,W.L. (1992) A position effect on the time of replication origin activation in yeast. Cell, 68, 333-339.
22. Fritze,C.H. (1994) Control of recombination and gene expression in the rDNA tandem repeated array of S. cerevisiae. PhD Thesis, The University of Chicago, Chicago, IL, USA.
23. Gangloff, S., McDonald,J.P. Bendixen,C., Arthur,L. and Rothstein,R. (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrasc. Mol. Cell. Biol., 14, 8391-8398.
24. Gangloff,S., Zou,H. and Rothstein,R. (1996) Gene conversion plays the major role in controlling the stability of large tandem repeats in yeast. EMBO J., 15, 1715-1725.
25. Gotta,M., Strahl-Bolsinger,S., Renauld,H., Laroche,T., Kennedy,B.K., Grunstein,M. and Gasser, S.M. (1997) Localization of Sir2p: the nucleolus as a compartment for silent information regulators. EMBO J., 16, 3243-3255.
26. Gottlieb,S. (1989) Genetic control of recombination between repeated genes in the yeast Saccharomyces cerevisiae. PhD Thesis, University of Chicago, IL, USA.
27. Gotllieb,S. and Esposito,R.E. (1989) A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell. 56, 771-776.
28. Gottlieb,S., Wagstaff,J. and Eastern Esposito,R. (1989) Evidence for two pathways of meiotic intrachromosomal recombination in yeast. Proc. Natl Acad. Sci. USA, 86, 7072-7076.
29. Gottschling,D.E. (1992) Telomere-proximal DNA in Saccharomyces revisiae is refractory to methyltransferase activity HI vivo. Proc. Natl Acad. Sci. USA, 89, 4062-4065.
30. Gottschling,D.E., Aparicio,O.M., Billington,B.L. and Zakian,V.A. (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell, 63, 751-762.
31. Grenson,M., Mousset,M., Wiame,J.M. and Bechet,J. (1966) Multiplicity of amino acid permeases in Saccharomyces cerevisiae IV: evidence for a specific arginine transporting system. Biochim. Biophys. Acta, 127, 325-338.
32. Haber, J.E. and George,J.P. (1979) A mutation that permits expression of normally silent copies of mating-type information in Saccharomyces cerevisiae. Genetics, 93, 13-35.
33. Hecht,A., Laroche,T., Strahl,B.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.
34. Hecht,A., Strahl,B.S. and Grunstein,M. (1996) Spreading of transcriptional repressor SIR3 from telomeric heterochromatin. Nature, 383, 92-96.
35. Henikoff,S. and Eghtedarzadeh,M.K. (1987) Conserved arrangement of nested genes at the Drosophila Gart locus. Genetics, 117, 711-725.
36. Herskowitz,I. (1990) A regulator, hierarchy for cell specialization in yeast. Nature, 586, 854-857.
37. Hoffman,C.S. and Winston,F. (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene, 57, 267-272.
38. Hoffmann,W. (1985) Molecular characterization of the CAN1 locus in Saccharomyces cerevisiae. A transmembrane protein without N-terminal hydrophobic signal sequence. J. Biol. Chem, 260, 11831-11837.
39. Holm,C., Meeks-Wagner,D., Fangman,W. and Botstein,D. (1986) A rapid efficient method for isolating DNA from yeast. Gene, 42, 169-173.
40. Huang,G.S. and Keil,R.L. (1995) Requirements for activity of the yeast mitotic recombination hotspot HOT1: RNA polymerase I and multiple cis-acting sequences. Genetics, 141, 845-855.
41. Huigbregtse,J.M., Evans,C.F. and Engelke,D.R. (1987) Comparison of tRNA gene transcription complexes formed in vitro and in nuclei. Mol. Cell. Biol., 7, 3212-3220.
42. Ide,G. and Saunders,C. (1981) Isolation of nuclei from Saccharomyces cerevisiae. Curr. Genet., 4, 85-90.
43. Ivy,J.M., Klar,A.J. and Hicks,J.B. (1986) Cloning and characterization of four SIR genes of Saccharomyces cerevisiae. Mol. Cell. Biol., 6, 688-702.
44. Kayne,P.S., Kim,V.J., Han,M., Mullen,J.R., Yoshizaki,F. and Grunstein,M. (1988) Extremely conserved histone H4 N terminus is dispensable for growth but is essential for repressing the silent mating loci in yeast. Cell, 55, 27-39.
45. Keil,R.L. and Lin,Y.-H. (1991) Mutations affecting RNA polymerase I-stimulated exchange and rDNA recombination in yeast. Genetics, 127, 31-38.
46. Keil,R.L. and McWilliams,A.D. (1993) A gene with specific and global effects on recombination of sequences from tandemly repeated genes in Saccharomyces cerevisiae. Genetics, 135, 711-718.
47. Keil,R.L. and Roeder,G.S. (1984) Co-acting, recombination-stimulating activity in a fragment of the ribosomal DNA of S. cerevisiae. Cell, 39, 377-386.
48. Kempter,B., Luppa,P. and Neumeier,D. (1991) A short procedure for Southern blotting on neutral and anionic membranes. Trends Genet., 7, 109-110.
49. Kennedy,B.K., Gotta,M., Sinclair,D.A., Mills,K., McNabb,D.S., Murthy,M., Pak,S.M., Laroche,T., Gasser,S.M. and Guarente,I. (1997) Redistribution of silencing proteins from telomeres to the nucleolus is associated with extension of life span in S.cerevisiae. Cell, 89, 381-391.
50. Klar,A.J.S., Fogel,S. and MacLeod,K. (1979) MARI - a regulator of HMa and HMα loci in Saccharomyces cerevisiae. Genetics, 93, 37-50.
51. Laurenson,P. and Rme,J. (1992) Silencers, silencing, and heritable transcriptional states. (Review). Microbiol. Rev., 56, 543-560.
52. Lewin,B.E. (1990) Genes IV. Cell Press, Cambridge MA.
53. Lin,Y.H. and Keil,R.L. (1991) Mutations affecting RNA polymerase I-stitnulated exchange and rDNA recombination in yeast. Genetics, 127, 31-38.
54. Linskens,M.H. and Huberman,J.A. (1988) Organization of replication of ribosomal DNA in Saccharomyces cerevisiae. Mol. Cell. Biol., 8, 4927-4935.
55. Lucchini, R. and Sogo,J.M. (1994) Chromatin structure and transcriptional activity around the replication forks arrested at the 3′ end of the yeast rRNA genes. Mol. Cell. Biol., 14, 318-326.
56. Mahoney,D.J., Marquardt,R., Shei,G.J., Rose,A.B. and Broach,J.R. (1991) Mutations in the HML E silencer of Saccharomyces cerevisiae yield metastable inheritance of transcriptional repression. Genes Dev., 5, 605-615.
57. McNally,F.J. and Rine,J. (1991) A synthetic silencer mediates SIR-dependent functions in Saccharomyces cerevisiae. Mol. Cell. Biol., 11, 5648-5659.
58. Miller,A.M., Sternglanz,R. and Nasmyth,K.A. (1984) The role of DNA replication in the repression of the yeast mating-type silent loci. Cold Spring Harbor Symp. Quant. Biol., 49, 105-113.
59. Moretti,P., Freeman,K., Coodly,L. and Shore,D. (1994) Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding prolein RAP1. Genes Dev. 8, 2257-2269.
60. Nasmyth,K. (1982) The regulation of yeast mating type chromatin structure by SIR: an action at a distance affecting both transcription and transposition. Cell, 30, 567-578.
61. Ohta,K., Shibata,T. and Nicolas,A. (1994) Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMRO J., 13, 5754-5763.
62. Ozenberger,B.A. and Roeder,G.S. (1991) A unique pathway of double-strand break repair operates in tandemly repeated genes. Mol. Cell. Biol., 11, 1222-1231.
63. Petes,T.D. (1979) Yeast ribosomal DNA genes are located on chromosome XII. Proc. Natl Acad. Sci. USA, 76, 410-414.
64. Petes,T.D. and Botstein,D. (1977) Simple Mendelian inheritance of the reiterated ribosomal DNA of yeast. Proc. Natl Acad. Sci. USA, 74, 5091-5095.
65. Pillus,L. and Rine,J. (1989) Epigenetic inheritance of transcriptional states in S. cerevisiae. Cell, 59, 637-647.
66. Planta,R.J. and Raue,H.A. (1988) The control of ribosome biogenesis. Trends Genet. Sci., 4, 64-68.
67. Renauld,H., Aparicio,O.M., Zierath,P.D., Billington,B.L., Chhablani,S.K. and Gottschling,D.E. (1993) Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev. 7, 1133-1145.
68. Rine,J. and Herskowitz, (1987) Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics, 116, 9-22.
69. Roman,H. (1956) Studies of gene mutation in Saccharomyces. Cold Spring Harbor Symp. Quant. Biol., 21, 175-185.
70. Saffer,L.D. and Miller,O.J. (1986) Electron microscopic study of Saccharomyces cerevisiae rDNA chromatin replication. Mol. Cell. Biol., 6, 1148-1157.
71. Schiestl,R.H. and Gietz,R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet., 16, 339-346.
72. Sherman,F., Fink,G.R. and Lawrence,C.W. (1974) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY.
73. Shore,D., Stillman,D., Brand,A. and Nasmyth,K. (1987) Identification of silencer binding proteins from yeast: possible roles in SIR control and DNA replication. EMRO J., 6, 461-467.
74. 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.
75. Singh,J. and Klar,A.J. (1992) Active genes in budding yeast display enhanced in vivo accessibility to foreign DNA methylases: a novel in vivo probe for chromatin structure of yeast. Genes Dev., 6, 186-196.
76. Skryabin,K.G. et al. (1984) Structure and function of the non transcribed spacer regions of yeast rDNA. Nucleic Acids Res., 12, 2955-2968.
77. Smith,J.S. and Boeke,J.D. (1997) An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev., 11, 241-254.
78. Southern,E.M. (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol., 98, 503-517.
79. Stewart,S.E. and Roeder,G.S. (1989) Transcription by RNA polymerase I stimulates mitotic recombination in Saccharomyces cerevisiae. Mol. Cell. Biol., 9, 3464-3472.
80. Stone,E.M., Swanson,M.J., Romeo,A.M., Hicks,J.B. and Sternglanz,R. (1991) The SIR1 gene of Saccharomyces cerevisiae and its role as an extragenic suppressor of several mating-defective mutants. Mol. Cell. Biol., 11, 2253-2262.
81. Strahl,B.S., Hecht,A., Luo,K. and Grunstein,M. (1997) SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast. Genes Dev., 11, 83-93.
82. rosky,R.T. and Esposito,R.E. (1992) Early meiotic transcripts are highly unstable in Saccharomyces cerevisiae. Mol. Cell. Biol., 12, 3948-3958.
83. Sussel,L. and Shore,D. (1991) Separation of transcriptional activation and silencing functions of the RAP1-encoded repressor/activator protein 1: isolation of viable mutants affecting both silencing and telomere length. Proc. Natl Acad. Sci. USA, 88, 7749-7753.
84. Sussel,L., Vannier,D. and Shore,D. (1993) Epigenetic switching of transcriptional states: cis- and trans-acting factors affecting establishment of silencing at the HMR locus in Saccharomyces cerevisiae. Mol. Cell. Biol., 13, 3919-3928.
85. Thompson,J.S., Johnson,L.M. and Grunstein,M. (1994a) Specific repression of the yeast silent mating locus HMR by an adjacent telomere. Mol. Cell. Biol. 14, 446-455.
86. Thompson,J.S., Ling,X. and Grunstein,M. (1994b) Histone H3 amino terminus is required for telomeric and silent mating locus repression in yeast. Nature, 369, 245-247.
87. Voelkel-Meiman,K., Keil,R.L. and Roeder,S.G. (1987) Recombination stimulating sequences in yeast rihosomal DNA correspond to sequences regulating transcription by RNA polymerase I. Cell, 48. 1071-1079.
88. Wallis,J.W., Ghrebet,G., Brodsky,G., Rolfe,M. and Rothstein,R. (1989) A hyper-recombination mutation in S. cerevisiae identities a novel eukaryotic topoisomerase. Cell, 58, 409-419.
89. Walmsley,R.M., Johnston,L.H., Williamson,D.H. and Oliver,S.G. (1984) Replicon size of yeast ribosomal DNA. Mol. Gen. Genet., 195, 260-266.
90. Woodcock,D.M., Crowther,P.J., Doheny,J., Jefferson,S., DeCruz,E., Noyer,W.M., Smith,S.S., Michael,M.Z. and Graham,M.W. (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res., 17, 3469-3478.
91. Wu,C. (1980) The 5′ ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature, 286, 854-860.
92. Wu,T.C. and Lichten,M. (1994) Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science, 263, 515-518.
93. Yanisch,P.C., Vieira,J. and Messing,J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene, 33, 103-119.
94. Zamb,T.J. and Petes,T.D. (1982) Analysis of the junction between ribosomal RNA genes and single copy chromosomal sequences in the yeast Saccharomyces cerevisiae. Cell, 28, 355-364.