Mod5 protein binds to tRNA gene complexes and affects local transcriptional silencing

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 33, 2013, Pages

  Pratt Hyatt, Matthew ^a,b,e   Pai, Dave A ^a   Haeusler, Rebecca A ^a,f   Wozniak, Lenn G ^a   Good, Paul D ^a   Miller, Erin L ^a   McLeod, Ian X ^c,g   Yates III, John R ^c   Hopper, Anita K ^d   Engelke, David R ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^f Duke University ^*  (United States)

^g DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Maf1; RNA silencing

Indexed keywords

MOD5 PROTEIN; RNA POLYMERASE II; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; RNA STRUCTURE;

MAF1; RNA SILENCING;

ALKYL AND ARYL TRANSFERASES; ARABIDOPSIS; BLOTTING, NORTHERN; CELL NUCLEOLUS; CHROMATIN IMMUNOPRECIPITATION; CLONING, MOLECULAR; DNA PRIMERS; GENE SILENCING; HEPTANOIC ACIDS; HUMANS; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; OLIGONUCLEOTIDES; PROMOTER REGIONS, GENETIC; PYRROLES; RNA POLYMERASE II; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84882313983     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1219946110     Document Type: Article

References (54)

1. Goffeau A, et al. (1996) Life with 6000 genes. Science 274(5287):546-567.
2. Hull MW, Erickson J, Johnston M, Engelke DR (1994) tRNA genes as transcriptional repressor elements. Mol Cell Biol 14(2):1266-1277.
3. Wang L, et al. (2005) Silencing near tRNA genes requires nucleolar localization. J Biol Chem 280(10):8637-8639.
4. Noma K, Cam HP, Maraia RJ, Grewal SI (2006) A role for TFIIIC transcription factor complex in genome organization. Cell 125(5):859-872.
5. Simms TA, et al. (2008) TFIIIC binding sites function as both heterochromatin barriers and chromatin insulators in Saccharomyces cerevisiae. Eukaryot Cell 7(12):2078-2086.
6. Valenzuela L, Dhillon N, Kamakaka RT (2009) Transcription independent insulation at TFIIIC-dependent insulators. Genetics 183(1):131-148.
7. Thompson M, Haeusler RA, Good PD, Engelke DR (2003) Nucleolar clustering of dispersed tRNA genes. Science 302(5649):1399-1401.
8. Desai N, et al. (2005) Two steps in Maf1-dependent repression of transcription by RNA polymerase III. J Biol Chem 280(8):6455-6462.
9. Moir RD, et al. (2006) Protein kinase A regulates RNA polymerase III transcription through the nuclear localization of Maf1. Proc Natl Acad Sci USA 103(41):15044- 15049.
10. Pluta K, et al. (2001) Maf1p, a negative effector of RNA polymerase III in Saccharomyces cerevisiae. Mol Cell Biol 21(15):5031-5040.
11. Roberts DN, Stewart AJ, Huff JT, Cairns BR (2003) The RNA polymerase III transcriptome revealed by genome-wide localization and activity-occupancy relationships. Proc Natl Acad Sci USA 100(25):14695-14700.
12. Boguta M, Czerska K, Zoładek T (1997) Mutation in a new gene MAF1 affects tRNA suppressor efficiency in Saccharomyces cerevisiae. Gene 185(2):291-296.
13. Murawski M, et al. (1994) maf1 mutation alters the subcellular localization of the Mod5 protein in yeast. Acta Biochim Pol 41(4):441-448.
14. Dihanich ME, et al. (1987) Isolation and characterization of MOD5, a gene required for isopentenylation of cytoplasmic and mitochondrial tRNAs of Saccharomyces cerevisiae. Mol Cell Biol 7(1):177-184.
15. Gefter ML, Bikoff E (1971) Studies on synthesis and modification of transfer RNA. Cancer Res 31(5):667-670.
16. Gillman EC, Slusher LB, Martin NC, Hopper AK (1991) MOD5 translation initiation sites determine N6-isopentenyladenosine modification of mitochondrial and cytoplasmic tRNA. Mol Cell Biol 11(5):2382-2390.
17. Laten H, Gorman J, Bock RM (1978) Isopentenyladenosine deficient tRNA from an antisuppressor mutant of Saccharomyces cerevisiae. Nucleic Acids Res 5(11):4329-4342.
18. Kendall A, et al. (2000) A CBF5 mutation that disrupts nucleolar localization of early tRNA biosynthesis in yeast also suppresses tRNA gene-mediated transcriptional silencing. Proc Natl Acad Sci USA 97(24):13108-13113.
19. Kaminska J, et al. (2002) The isoprenoid biosynthetic pathway in Saccharomyces cerevisiae is affected in a maf1-1 mutant with altered tRNA synthesis. FEMS Yeast Res 2(1):31-37.
20. Haeusler RA, Pratt-Hyatt M, Good PD, Gipson TA, Engelke DR (2008) Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev 22(16):2204-2214.
21. Oficjalska-Pham D, et al. (2006) General repression of RNA polymerase III transcription is triggered by protein phosphatase type 2A-mediated dephosphorylation of Maf1. Mol Cell 22(5):623-632.
22. Upadhya R, Lee J, Willis IM (2002) Maf1 is an essential mediator of diverse signals that repress RNA polymerase III transcription. Mol Cell 10(6):1489-1494.
23. Benko AL, Vaduva G, Martin NC, Hopper AK (2000) Competition between a sterol biosynthetic enzyme and tRNA modification in addition to changes in the protein synthesis machinery causes altered nonsense suppression. Proc Natl Acad Sci USA 97(1):61-66.
24. Dimster-Denk D, et al. (1999) Comprehensive evaluation of isoprenoid biosynthesis regulation in Saccharomyces cerevisiae utilizing the Genome Reporter Matrix. J Lipid Res 40(5):850-860.
25. Warner GJ, et al. (2000) Inhibition of selenoprotein synthesis by selenocysteine tRNA [Ser]Sec lacking isopentenyladenosine. J Biol Chem 275(36):28110-28119.
26. Golovko A, Hjälm G, Sitbon F, Nicander B (2000) Cloning of a human tRNA isopentenyl transferase. Gene 258(1-2):85-93.
27. Golovko A, Sitbon F, Tillberg E, Nicander B (2002) Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana. Plant Mol Biol 49(2):161-169.
28. Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276(28):26405-26410.
29. Boguta M, et al. (1994) Subcellular locations of MOD5 proteins: Mapping of sequences sufficient for targeting to mitochondria and demonstration that mitochondrial and nuclear isoforms commingle in the cytosol. Mol Cell Biol 14(4): 2298-2306.
30. Tolerico LH, et al. (1999) Saccharomyces cerevisiae Mod5p-II contains sequences antagonistic for nuclear and cytosolic locations. Genetics 151(1):57-75.
31. Washburn MP (2004) Utilisation of proteomics datasets generated via multidimensional protein identification technology (MudPIT). Brief Funct Genomics Proteomics 3(3): 280-286.
32. Johnson TL, Chamberlin MJ (1994) Complexes of yeast RNA polymerase II and RNA are substrates for TFIIS-induced RNA cleavage. Cell 77(2):217-224.
33. Sawadogo M (1981) On the inhibition of yeast RNA polymerases A and B by tRNA and alpha-amanitin. Biochem Biophys Res Commun 98(1):261-267.
34. Espinoza CA, Allen TA, Hieb AR, Kugel JF, Goodrich JA (2004) B2 RNA binds directly to RNA polymerase II to repress transcript synthesis. Nat Struct Mol Biol 11(9):822-829.
35. Herbert CJ, Labouesse M, Dujardin G, Slonimski PP (1988) The NAM2 proteins from S. cerevisiae and S. douglasii are mitochondrial leucyl-tRNA synthetases, and are involved in mRNA splicing. EMBO J 7(2):473-483.
36. Labouesse M (1990) The yeast mitochondrial leucyl-tRNA synthetase is a splicing factor for the excision of several group I introns. Mol Gen Genet 224(2):209-221.
37. Zhao X, et al. (2004) Regulation of nuclear receptor activity by a pseudouridine synthase through posttranscriptional modification of steroid receptor RNA activator. Mol Cell 15(4):549-558.
38. Allen TA, Von Kaenel S, Goodrich JA, Kugel JF (2004) The SINE-encoded mouse B2 RNA represses mRNA transcription in response to heat shock. Nat Struct Mol Biol 11(9):816-821.
39. Mariner PD, et al. (2008) Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell 29(4):499-509.
40. Spinola M, et al. (2005) Identification and functional characterization of the candidate tumor suppressor gene TRIT1 in human lung cancer. Oncogene 24(35): 5502-5509.
41. Suzuki G, Shimazu N, Tanaka M (2012) A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336(6079):355-359.
42. Ghaemmaghami S, et al. (2003) Global analysis of protein expression in yeast. Nature 425(6959):737-741.
43. Longtine MS, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14(10):953-961.
44. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122(1):19-27.
45. Bertrand E, Houser-Scott F, Kendall A, Singer RH, Engelke DR (1998) Nucleolar localization of early tRNA processing. Genes Dev 12(16):2463-2468.
46. Long RM, Elliott DJ, Stutz F, Rosbash M, Singer RH (1995) Spatial consequences of defective processing of specific yeast mRNAs revealed by fluorescent in situ hybridization. RNA 1(10):1071-1078.
47. Li Y, Moir RD, Sethy-Coraci IK, Warner JR,Willis IM (2000) Repression of ribosome and tRNA synthesis in secretion-defective cells is signaled by a novel branch of the cell integrity pathway. Mol Cell Biol 20(11):3843-3851.
48. Gille C, Goede A, Preissner R, Rother K, Frömmel C (2000) Conservation of substructures in proteins: Interfaces of secondary structural elements in proteasomal subunits. J Mol Biol 299(4):1147-1154.
49. Ren B, et al. (2000) Genome-wide location and function of DNA binding proteins. Science 290(5500):2306-2309.
50. Puig O, et al. (2001) The tandem affinity purification (TAP) method: A general procedure of protein complex purification. Methods 24(3):218-229.
51. Alberts AW, et al. (1980) Mevinolin: A highly potent competitive inhibitor of hydroxymethylglutaryl-coenzyme A reductase and a cholesterol-lowering agent. Proc Natl Acad Sci USA 77(7):3957-3961.
52. Brachmann CB, et al. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14(2):115-132.
53. Winzeler EA, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285(5429):901-906.
54. Rothstein RJ (1983) One-step gene disruption in yeast. Methods Enzymol 101: 202-211.