Silencing near tRNA genes is nucleosome-mediated and distinct from boundary element function

Gene

Volumn 526, Issue 1, 2013, Pages 7-15

  Good, Paul D ^a   Kendall, Ann ^a   Ignatz Hoover, James ^a,b   Miller, Erin L ^a   Pai, Dave A ^a   Rivera, Sara R ^a   Carrick, Brian ^a   Engelke, David R ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Deacetylase; Histone; Phosphatase; Remodeling; RNA polymerase III; Tgm silencing

Indexed keywords

HISTONE DEACETYLASE; TRANSFER RNA;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CHROMATIN; CHROMATIN STRUCTURE; DEACETYLATION; GENE LOCATION; GENE LOCUS; GENE SILENCING; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE PHOSPHORYLATION; NUCLEOSOME; PRIORITY JOURNAL; RNA GENE; SUMOYLATION;

AC; ACETYLATION; ATPASE; C TERMINUS; CARBOXY TERMINUS; CASEIN KINASE 2; CHROMATIN REMODELING COMPLEX; CK2; DEACETYLASE; ENZYME HYDROLYZING ADENOSINE TRIPHOSPHATE; FLUOROOROTIC ACID; FOA; H2A; H2A.Z; H2B; H3; H4; HISTONE; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; HISTONE VARIANT H2A.Z; ME; METHYLATION; OPEN READING FRAME; ORF; P; PHOSPHATASE; PHOSPHORYLATION; POL II; POL III; PROTEIN COMPLEX CONTAINING RPD3 PROTEIN; REMODELING; RNA POLYMERASE II; RNA POLYMERASE III; RNA POLYMERASE III TRANSCRIPTION FACTOR IIIB; RNA POLYMERASE III TRANSCRIPTION FACTOR IIIC; RPD3L; RPD3S; RSC; SCANNING HISTONE MUTAGENESIS WITH ALANINE; SD; SGR; SHIMA; SHORT INTERSPERSED ELEMENT; SINE; SYNTHETIC YEAST MEDIA WITH DEXTROSE; SYNTHETIC YEAST MEDIA WITH GALACTOSE AND RAFFINOSE; TARGET OF RAPAMYCIN; TFIIIB; TFIIIC; TGM; TGM SILENCING; TOR; TRANSFER RNA; TRNA; TRNA GENE-MEDIATED; URA; URACIL;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE SILENCING; GENES, FUNGAL; HISTONES; INSULATOR ELEMENTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOSOMES; PROTEIN CONFORMATION; RNA POLYMERASE III; RNA, FUNGAL; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84880325195     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2013.05.016     Document Type: Article

References (59)

1. Andrews P.D., Stark M.J.R. Type 1 protein phosphatase is required for maintenance of cell wall integrity, morphogenesis and cell cycle progression in Saccharomyces cerevisiae. J. Cell Sci. 2000, 113:507-520.
2. Becker D.M., Lundblad V. Introduction of DNA into yeast cells. Curr. Protoc. Mol. Biol. 1993, 13.7.1-13.7.2.
3. Ben-Aroya S., Coombes C., Kwok T., O'Donnell K.A., Boeke J.D., Hieter P. Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol. Cell 2008, 30:248-258.
4. Bolton E.C., Boeke J.D. Transcriptional interactions between yeast tRNA genes, flanking genes and Ty elements: a genomic point of view. Genome Res. 2003, 13:254-263.
5. Brachmann C.B., et al. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998, 14:115-132.
6. Campos E.I., Reinberg D. Histones: annotating chromatin. Annu. Rev. Genet. 2009, 43:559-599.
7. Chaban Y., et al. Nat. Struct. Mol. Biol. 2008, 15:1272-1277.
8. Chang C.S., Pillus L. Collaboration between the essential Esa1 acetyltransferase and the Rpd3 deacetylase is mediated by H4K12 histone acetylation in Saccharomyces cerevisiae. Genetics 2009, 183:149-160.
9. Chatterjee N., Sinha D., Lemma-Dechassa M., Tan S., Shogren-Knaak M.A., Bartholomew B. Histone H3 tail acetylation modulates ATP-dependent remodeling though multiple mechanisms. Nucleic Acids Res. 2011, 39:8378-8391.
10. Chen X.-F., et al. The Rpd3 core complex is a chromatin stabilization module. Curr. Biol. 2012, 22:56-63.
11. D'Ambrosio C., et al. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev. 2008, 22:2215-2227.
12. Damelin M., et al. The genome-wide localization or Rsc9, a component of the RSC chromatin-remodeling complex, changes in response to stress. Mol. Cell 2002, 9:563-573.
13. Desai N., Lee J.-H., Upadhya R., Chu Y., Moir R.D., Willis I.M. Two steps in Maf1-dependent repression of transcription by RNA polymerase III. J. Biol. Chem. 2005, 280:6455-6462.
14. Dhillon N., et al. DNA polymerase epsilon, acetylases and remodellers cooperate to form a specialized chromatin structure at a tRNA insulator. EMBO J. 2009, 28:2583-2600.
15. Donze D., Kamakaka R.T. RNA polymerase III and RNA polymerase II promoter complexes are heterochromatin barriers in Saccharomyces cerevisiae. EMBO J. 2001, 20:520-531.
16. Du J., Nasir I., Benton B.K., Kladde M.P., Laurent B.C. Sth1p, a Saccharomyces cerevisiae Wnf2p/Swi2p homolog, is an essential ATPase in RSC and differs from Snf/Swi in its interactions with histones and chromatin-associated proteins. Genetics 1998, 150:987-1005.
17. Dubarry M., Loiodice I., Chen C.L., Thermes C., Taddei A. Tight protein-DNA interactions favor gene silencing. Gene Dev. 2011, 25:1365-1370.
18. Dubey R.N., Gartenberg M.R. A tDNA establishes cohesion of a neighboring silent chromatin domain. Genes Dev. 2007, 21:2150-2160.
19. Duffy S.K., et al. Exploring the yeast acetylome using functional genomics. Cell 2012, 149:936-948.
20. Goldstein A.L., McCusker J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 1999, 15:1541-1553.
21. Grigat M., Jaschke Y., Kliewe F., Pfeifer M., Walz S., Schuller H.J. Multiple histone deacetylases are recruited by corepressor Sin3 and contribute to gene repression mediated by Opi1 regulator of phospholipid biosynthesis in the yeast Saccharomyces cerevisiae. Mol. Genet. Genomics 2012, 287:461-472.
22. Haeusler R.A., Pratt-Hyatt M., Good P.D., Gipson T.A., Engelke D.R. Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev. 2008, 22:2204-2214.
23. Haldar D., Kamakaka R.T. tRNA genes as chromatin barriers. Nat. Struct. Mol. Biol. 2006, 13:192-193.
24. Hsu J.Y., et al. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 2000, 102:279-291.
25. Hull M.W., Erickson J., Johnston M., Engelke D.R. tRNA genes as transcriptional repressor elements. Mol. Cell. Biol. 1994, 14:1266-1277.
26. Johnson E.S., Blobel G. Ubc9 is the conjugating enzyme for the ubiquitin-like protein Smt3p. J. Biol. Chem. 1997, 272:26799-26802.
27. Kaiser C., Michaelis S., Mitchell A. Methods in Yeast Genetics 1994, Cold Spring Harbor Laboratory Press, Plainview, NY, (234 pp.).
28. Kendall A., Hull M.W., Bertrand E., Good P.D., Singer R.H., Engelke D.R. A CBF5 mutation that disrupts nucleolar localization of early tRNA biosynthesis in yeast also suppresses tRNA gene-mediated transcriptional silencing. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13108-13113.
29. Kirkland J.G., Kamakaka R.T. tRNA insulator function: insight into inheritance of transcription states?. Epigenetics 2010, 5:96-99.
30. Kruger W., et al. Amino acid substitutions in the structured domains of histones H3 and H4 partially relieve the requirement of the yeast SWI/SNF complex for transcription. Genes Dev. 1995, 9:2770-2779.
31. Lambermon M.H.L., Fu Y., Kirk D.A.W., Dupasquier M., Filipowicz W., Lorkovic Z.J. Uba1 and Uba2, two proteins that interact with Ubp1, a multifunctional effector of pre-mRNA maturation in plants. Mol. Cell. Biol. 2002, 22:4346-4357.
32. Lunyak V.V., et al. Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 2007, 317:248-251.
33. Mahapatra S., Dewari P.S., Bhardwaj A., Bhargava P. Yeast H2A.Z, FACT complex and RSC regulate transcription of tRNA gene through differential dynamics of flanking nucleosomes. Nucleic Acids Res. 2011, 39:4023-4034.
34. Millar C.B., Grunstein M. Genome-wide patterns of histone modifications in yeast. Nat. Rev. Mol. Cell Biol. 2006, 7:657-666.
35. Moir R.D., Lee J.H., Haeusler R.A., Desai N., Engelke D.R., Willis I.M. Protein kinase A regulates RNA polymerase III transcription through the nuclear localization of Maf 1. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:15044-15049.
36. Morse R.H., Roth S., Simpson R.T. A transcriptionally active tRNA gene interferes with nucleosome positioning in vivo. Mol. Cell. Biol. 1992, 12:4015-4025.
37. Nakanishi S., Sanderson B.W., Delventhal K.M., Bradford W.D., Staehling-Hampton K., Shilatifard A. A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nat. Struct. Mol. Biol. 2008, 15:881-888.
38. Ng H.H., Robert F., Young R.A., Struhl K. Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev. 2002, 16:806-819.
39. Noma K., Kamakaka R.T. The human pol III transcriptome and information flow. Nat. Struct. Mol. Biol. 2010, 17:539-541.
40. Noma K., Cam H.P., Maraia R.J., Grewal S.I. A role for TFIIIC transcription factor complex in genome organization. Cell 2006, 125:859-872.
41. Oki M., Valenzuela L., Chiba T., Ito T., Kamakaka R.T. Barrier proteins remodel and modify chromatin to restrict silenced domains. Mol. Cell. Biol. 2004, 24:1956-1967.
42. Oler A.J., et al. Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat. Struct. Mol. Biol. 2010, 17:620-628.
43. Park J.H., Cosgrove M., Youngman E., Wolberger C., Boeke J.D. A core nucleosome surface crucial for transcriptional silencing. Nat. Genet. 2002, 32:273-279.
44. Parnell T.J., Huff J.T., Cairns B.R. RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes. EMBO J. 2008, 27:100-110.
45. Raab J.R., et al. Human tRNA genes function as chromatin insulators. EMBO J. 2011, 31:330-350.
46. Roberts D.N., Wilson B., Huff J.T., Stewart A.J., Cairns B.R. Dephosphorylation and genome-wide association of Maf with Pol III-transcribed genes during repression. Mol. Cell 2006, 22:633-644.
47. Robyr D., et al. Microarray deacetylation maps determine genome-wide functions for histone deacetylases. Cell 2002, 109:437-446.
48. Rodley* C.D.M., Pai* D.A., Mills T.A., Engelke D.R., O'Sullivan J.M. tRNA gene identity affects nuclear positioning. PLoS One 2011, 6:e29267. (*=equal contribution).
49. Russell I.D., Tollervey D. Nop3 is an essential yeast protein that is required for rRNA processing. J. Cell Biol. 1992, 119:737-747.
50. Santangelo G.M. Glucose signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2006, 70:253-282.
51. Simms T.A., et al. TFIIIC binding sites function as both heterochromatin barriers and chromatin insulators in Saccharomyces cerevisiae. Eukaryot. Cell 2008, 7:2078-2086.
52. Soutourina J., et al. Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Mol. Cell. Biol. 2006, 26:4920-4933.
53. Thompson M., Haeusler R.A., Good P.D., Engelke D.R. Nucleolar clustering of dispersed tRNA genes. Science 2003, 302:139-141.
54. Titus L.C., Dawson T.R., Rexer D.J., Ryan K.J., Wente S.R. Members of the RSC chromatin-remodeling complex are required for maintaining proper nuclear envelope structure and pore complex localization. Mol. Biol. Cell 2010, 21:1072-1087.
55. Valenzuela L., Dhillon N., Kamakaka R.T. Transcription independent insulation at TFIIIC-dependent insulators. Genetics 2009, 183:131-148.
56. Vannini A., Ringel R., Kusser A.G., Berninghausen O., Kassavetis G.A., Cramer P. Molecular basis of RNA polymerase III transcription repression by Maf1. Cell 2010, 143:59-70.
57. Venters B.J., et al. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol. Cell 2011, 41:480-492.
58. Wang L., Haeusler R.A., Good P.D., Thompson M., Nagar S., Engelke D.R. Silencing near tRNA genes requires nucleolar localization. J. Biol. Chem. 2005, 280:8637-8639.
59. White C.L., Sutto R.K., Luger K. Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. EMBO J. 2001, 20:5207-5218.