Maf1-mediated repression of RNA polymerase III transcription inhibits tRNA degradation via RTD pathway

RNA

Volumn 18, Issue 10, 2012, Pages 1823-1832

  Turowski, Tomasz W ^a   Karkusiewicz, Iwona ^b   Kowal, Justyna ^b   Boguta, Magdalena ^a,b  

^a WARSAW UNIVERSITY OF TECHNOLOGY   (Poland)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

Author keywords

Maf1; Rapid tRNA decay; RNA polymerase III; Translation elongation factor; tRNA; tRNA transcription

Indexed keywords

DNA DIRECTED RNA POLYMERASE III; MAF1 PROTEIN; TRANSFER RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; DEPHOSPHORYLATION; GENE OVEREXPRESSION; GENE REPRESSION; MOLECULAR CLONING; MUTANT; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; RNA DEGRADATION; TRANSCRIPTION REGULATION; YEAST;

DOWN-REGULATION; GENE EXPRESSION REGULATION, FUNGAL; GENE LIBRARY; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; MUTANT PROTEINS; ORGANISMS, GENETICALLY MODIFIED; PLASMIDS; RNA POLYMERASE III; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 84866634409     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.033597.112     Document Type: Article

References (36)

1. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, Grayhack EJ, Phizicky EM. 2006. Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21: 87-96.
2. Anderson JS, Parker RP. 1998. The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J 17: 1497-1506.
3. Boguta M, Graczyk D. 2011. RNA polymerase III under control: Repression and de-repression. Trends Biochem Sci 36: 451-456.
4. Boguta M, Czerska K, Zoladek T. 1997. Mutation in a new gene MAF1 affects tRNA suppressor efficiency in Saccharomyces cerevisiae. Gene 185: 291-296.
5. Chernyakov I, Baker MA, Grayhack EJ, Phizicky EM. 2008a. Chapter 11. Identification and analysis of tRNAs that are degraded in Saccharomyces cerevisiae due to lack of modifications. Methods Enzymol 449: 221-237.
6. Chernyakov I, Whipple JM, Kotelawala L, Grayhack EJ, Phizicky EM. 2008b. Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5′-3′exonucleases Rat1 and Xrn1. Genes Dev 22: 1369-1380.
7. Ciesla M, Towpik J, Graczyk D, Oficjalska-Pham D, Harismendy O, Suleau A, Balicki K, Conesa C, Lefebvre O, Boguta M. 2007. Maf1 is involved in coupling carbon metabolism to RNA polymerase III transcription. Mol Cell Biol 27: 7693-7702.
8. Desai N, Lee J, Upadhya R, Chu Y, Moir RD, Willis IM. 2005. Two steps in Maf1-dependent repression of transcription by RNA polymerase III. J Biol Chem 280: 6455-6462.
9. Ferri ML, Peyroche G, Siaut M, Lefebvre O, Carles C, Conesa C, Sentenac A. 2000. A novel subunit of yeast RNA polymerase III interacts with the TFIIB-related domain of TFIIIB70. Mol Cell Biol 20: 488-495.
10. Gajda A, Towpik J, Steuerwald U, Muller CW, Lefebvre O, Boguta M. 2010. Full repression of RNA polymerase III transcription requires interaction between two domains of its negative regulator Maf1. J Biol Chem 285: 35719-35727.
11. Graczyk D, Debski J, Muszynska G, Bretner M, Lefebvre O, Boguta M. 2011. Casein kinase II-mediated phosphorylation of general repressor Maf1 triggers RNA polymerase III activation. Proc Natl Acad Sci 108: 4926-4931.
12. Huber A, Bodenmiller B, Uotila A, Stahl M, Wanka S, Gerrits B, Aebersold R, Loewith R. 2009. Characterization of the rapamycin-sensitive phosphoproteome reveals that Sch9 is a central coordinator of protein synthesis. Genes Dev 23: 1929-1943.
13. Jha S, Dutta A. 2009. RVB1/RVB2: Running rings around molecular biology. Mol Cell 34: 521-533.
14. Kadaba S, Krueger A, Trice T, Krecic AM, Hinnebusch AG, Anderson J. 2004. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev 18: 1227-1240.
15. Karkusiewicz I, Turowski TW, Graczyk D, Towpik J, Dhungel N, Hopper AK, Boguta M. 2011. Maf1 protein, repressor of RNA polymerase III, indirectly affects tRNA processing. J Biol Chem 286: 39478-39488.
16. Ser species. RNA 14: 158-169.
17. Kuai L, Fang F, Butler JS, Sherman F. 2004. Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc Natl Acad Sci 101: 8581-8586.
18. Met synthesis can drive cell proliferation and oncogenic transformation. Cell 133: 78-89.
19. Mateyak MK, Kinzy TG. 2010. eEF1A: Thinking outside the ribosome. J Biol Chem 285: 21209-21213.
20. Moir RD, Lee J, Haeusler RA, Desai N, Engelke DR, Willis IM. 2006. Protein kinase A regulates RNA polymerase III transcription through the nuclear localization of Maf1. Proc Natl Acad Sci 103: 15044-15049.
21. Oficjalska-Pham D, Harismendy O, Smagowicz WJ, Gonzalez de Peredo A, Boguta M, Sentenac A, Lefebvre O. 2006. General repression of RNA polymerase III transcription is triggered by protein phosphatase type 2A-mediated dephosphorylation of Maf1. Mol Cell 22: 623-632.
22. Phizicky EM, Hopper AK. 2010. tRNA biology charges to the front. Genes Dev 24: 1832-1860.
23. Pluta K, Lefebvre O, Martin NC, Smagowicz WJ, Stanford DR, Ellis SR, Hopper AK, Sentenac A, Boguta M. 2001. Maf1p, a negative effector of RNA polymerase III in Saccharomyces cerevisiae. Mol Cell Biol 21: 5031-5040.
24. Roberts DN, Wilson B, Huff JT, Stewart AJ, Cairns BR. 2006. Dephosphorylation and genome-wide association of Maf1 with Pol III-transcribed genes during repression. Mol Cell 22: 633-644.
25. Schrader JM, Chapman SJ, Uhlenbeck OC. 2011. Tuning the affinity of aminoacyl-tRNA to elongation factor Tu for optimal decoding. Proc Natl Acad Sci 108: 5215-5220.
26. Stark H, Rodnina MV, Wieden HJ, Zemlin F, Wintermeyer W, van Heel M. 2002. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat Struct Biol 9: 849-854.
27. Stettler S, Chiannilkulchai N, Hermann-Le Denmat S, Lalo D, Lacroute F, Sentenac A, Thuriaux P. 1993. A general suppressor of RNA polymerase I, II and III mutations in Saccharomyces cerevisiae. Mol Gen Genet 239: 169-176.
28. Tipper DJ. 1973. Inhibition of yeast ribonucleic acid polymerases by thiolutin. J Bacteriol 116: 245-256.
29. Towpik J, Graczyk D, Gajda A, Lefebvre O, Boguta M. 2008. Derepression of RNA polymerase III transcription by phosphorylation and nuclear export of its negative regulator, Maf1. J Biol Chem 283: 17168-17174.
30. Upadhya R, Lee J, Willis IM. 2002. Maf1 is an essential mediator of diverse signals that repress RNA polymerase III transcription. Mol Cell 10: 1489-1494.
31. Valle M, Sengupta J, Swami NK, Grassucci RA, Burkhardt N, Nierhaus KH, Agrawal RK, Frank J. 2002. Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J 21: 3557-3567.
32. Vannini A, Ringel R, Kusser AG, Berninghausen O, Kassavetis GA, Cramer P. 2010. Molecular basis of RNA polymerase III transcription repression by Maf1. Cell 143: 59-70.
33. Whipple JM, Lane EA, Chernyakov I, D'Silva S, Phizicky EM. 2011. The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes Dev 25: 1173-1184.
34. White RJ. 2004. RNA polymerase III transcription and cancer. Oncogene 23: 3208-3216.
35. Wilusz JE, Whipple JM, Phizicky EM, Sharp PA. 2011. tRNAs marked with CCACCA are targeted for degradation. Science 334: 817-821.
36. Wyers F, Rougemaille M, Badis G, Rousselle JC, Dufour ME, Boulay J, Regnault B, Devaux F, Namane A, Seraphin B, et al. 2005. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.