Mechanism of Transcription Termination by RNA Polymerase III Utilizes a Non-template Strand Sequence-Specific Signal Element

Molecular Cell

Volumn 58, Issue 6, 2015, Pages 1124-1132

  Arimbasseri, Aneeshkumar G ^a   Maraia, Richard J ^a,b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b U S PUBLIC HEALTH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAROSE; DNA DIRECTED RNA POLYMERASE III; HOLOENZYME; NUCLEOTIDE; FUNGAL DNA; FUNGAL RNA; PROTEIN BINDING; RNA PRECURSOR; RPC11 PROTEIN, S CEREVISIAE; RPC37 PROTEIN, S CEREVISIAE; RPC53 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ACCURACY; ALGORITHM; ARTICLE; DIMERIZATION; DNA RNA HYBRIDIZATION; DNA TEMPLATE; MUTANT; NUCLEOTIDE SEQUENCE; POSITION WEIGHT MATRIX; RELEASE ASSAY; RNA SEQUENCE; TRANSCRIPTION TERMINATION; BIOLOGICAL MODEL; GENETICS; METABOLISM; REGULATOR GENE; SIGNAL TRANSDUCTION;

EUKARYOTA;

BASE SEQUENCE; DNA, FUNGAL; MODELS, GENETIC; PROTEIN BINDING; RNA POLYMERASE III; RNA PRECURSORS; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TERMINATOR REGIONS, GENETIC; TRANSCRIPTION TERMINATION, GENETIC;

EID: 84937596472     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.04.002     Document Type: Article

References (40)

1. Arimbasseri A.G., Maraia R.J. Distinguishing core and holoenzyme mechanisms of transcription termination by RNA polymerase III. Mol. Cell. Biol. 2013, 33:1571-1581.
2. Arimbasseri A.G., Maraia R.J. Biochemical analysis of transcription termination by RNA polymerase III from yeast Saccharomyces cerevisiae. Methods Mol. Biol. 2015, 1276:185-198.
3. Arimbasseri A.G., Rijal K., Maraia R.J. Comparative overview of RNA polymerase II and III transcription cycles, with focus on RNA polymerase III termination and reinitiation. Transcription 2013, 5:e27369.
4. Arimbasseri A.G., Rijal K., Maraia R.J. Transcription termination by the eukaryotic RNA polymerase III. Biochim. Biophys. Acta 2013, 1829:318-330.
5. Arimbasseri A.G., Kassavetis G.A., Maraia R.J. Transcription. Comment on "Mechanism of eukaryotic RNA polymerase III transcription termination". Science 2014, 345:524.
6. Bartholomew B., Durkovich D., Kassavetis G.A., Geiduschek E.P. Orientation and topography of RNA polymerase III in transcription complexes. Mol. Cell. Biol. 1993, 13:942-952.
7. Bartholomew B., Braun B.R., Kassavetis G.A., Geiduschek E.P. Probing close DNA contacts of RNA polymerase III transcription complexes with the photoactive nucleoside 4-thiodeoxythymidine. J. Biol. Chem. 1994, 269:18090-18095.
8. Bogenhagen D.F., Brown D.D. Nucleotide sequences in Xenopus 5S DNA required for transcription termination. Cell 1981, 24:261-270.
9. Braglia P., Percudani R., Dieci G. Sequence context effects on oligo(dT) termination signal recognition by Saccharomyces cerevisiae RNA polymerase III. J. Biol. Chem. 2005, 280:19551-19562.
10. Braun B.R., Kassavetis G.A., Geiduschek E.P. Bending of the Saccharomyces cerevisiae 5S rRNA gene in transcription factor complexes. J. Biol. Chem. 1992, 267:22562-22569.
11. Chédin S., Riva M., Schultz P., Sentenac A., Carles C. The RNA cleavage activity of RNA polymerase III is mediated by an essential TFIIS-like subunit and is important for transcription termination. Genes Dev. 1998, 12:3857-3871.
12. Cozzarelli N.R., Gerrard S.P., Schlissel M., Brown D.D., Bogenhagen D.F. Purified RNA polymerase III accurately and efficiently terminates transcription of 5S RNA genes. Cell 1983, 34:829-835.
13. Dvir A., Conaway J.W., Conaway R.C. Mechanism of transcription initiation and promoter escape by RNA polymerase II. Curr. Opin. Genet. Dev. 2001, 11:209-214.
14. Gilmour D.S., Fan R. Derailing the locomotive: transcription termination. J. Biol. Chem. 2008, 283:661-664.
15. Hamada M., Sakulich A.L., Koduru S.B., Maraia R.J. Transcription termination by RNA polymerase III in fission yeast. A genetic and biochemically tractable model system. J. Biol. Chem. 2000, 275:29076-29081.
16. Huang Y., Intine R.V., Mozlin A., Hasson S., Maraia R.J. Mutations in the RNA polymerase III subunit Rpc11p that decrease RNA 3' cleavage activity increase 3'-terminal oligo(U) length and La-dependent tRNA processing. Mol. Cell. Biol. 2005, 25:621-636.
17. Iben J.R., Maraia R.J. Yeast tRNAomics: tRNA gene copy number variation and codon use provide bioinformatics evidence of a new wobble pair in a eukaryote. RNA 2012, 18:1358-1372.
18. Iben J.R., Mazeika J.K., Hasson S., Rijal K., Arimbasseri A.G., Russo A.N., Maraia R.J. Point mutations in the Rpb9-homologous domain of Rpc11 that impair transcription termination by RNA polymerase III. Nucleic Acids Res. 2011, 39:6100-6113.
19. Izban M.G., Samkurashvili I., Luse D.S. RNA polymerase II ternary complexes may become arrested after transcribing to within 10 bases of the end of linear templates. J. Biol. Chem. 1995, 270:2290-2297.
20. Kassavetis G.A., Prakash P., Shim E. The C53/C37 subcomplex of RNA polymerase III lies near the active site and participates in promoter opening. J. Biol. Chem. 2010, 285:2695-2706.
21. Keene R.G., Luse D.S. Initially transcribed sequences strongly affect the extent of abortive initiation by RNA polymerase II. J. Biol. Chem. 1999, 274:11526-11534.
22. Kireeva M.L., Komissarova N., Waugh D.S., Kashlev M. The 8-nucleotide-long RNA:DNA hybrid is a primary stability determinant of the RNA polymerase II elongation complex. J. Biol. Chem. 2000, 275:6530-6536.
23. Komissarova N., Kireeva M.L., Becker J., Sidorenkov I., Kashlev M. Engineering of elongation complexes of bacterial and yeast RNA polymerases. Methods Enzymol. 2003, 371:233-251.
24. Kubicek C.E., Chisholm R.D., Takayama S., Hawley D.K. RNA polymerase II mutations conferring defects in poly(A) site cleavage and termination in Saccharomyces cerevisiae. G3 (Bethesda) 2013, 3:167-180.
25. Landrieux E., Alic N., Ducrot C., Acker J., Riva M., Carles C. A subcomplex of RNA polymerase III subunits involved in transcription termination and reinitiation. EMBO J. 2006, 25:118-128.
26. Maraia R.J., Chang D.Y., Wolffe A.P., Vorce R.L., Hsu K. The RNA polymerase III terminator used by a B1-Alu element can modulate 3' processing of the intermediate RNA product. Mol. Cell. Biol. 1992, 12:1500-1506.
27. Martin F.H., Tinoco I. DNA-RNA hybrid duplexes containing oligo(dA:rU) sequences are exceptionally unstable and may facilitate termination of transcription. Nucleic Acids Res. 1980, 8:2295-2299.
28. Martinez-Rucobo F.W., Sainsbury S., Cheung A.C.M., Cramer P. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J. 2011, 30:1302-1310.
29. Matsuzaki H., Kassavetis G.A., Geiduschek E.P. Analysis of RNA chain elongation and termination by Saccharomyces cerevisiae RNA polymerase III. J. Mol. Biol. 1994, 235:1173-1192.
30. Molodtsov V., Anikin M., McAllister W.T. The presence of an RNA:DNA hybrid that is prone to slippage promotes termination by T7 RNA polymerase. J. Mol. Biol. 2014, 426:3095-3107.
31. NandyMazumdar M., Artsimovitch I. Ubiquitous transcription factors display structural plasticity and diverse functions: NusG proteins-shifting shapes and paradigms. Bioessays 2015, 37:324-334.
32. Richard P., Manley J.L. Transcription termination by nuclear RNA polymerases. Genes Dev. 2009, 23:1247-1269.
33. Rijal K., Maraia R.J. RNA polymerase III mutants in TFIIFα-like C37 that cause terminator readthrough with no decrease in transcription output. Nucleic Acids Res. 2013, 41:139-155.
34. Schneider T.D., Stephens R.M. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 1990, 18:6097-6100.
35. Shaaban S.A., Krupp B.M., Hall B.D. Termination-altering mutations in the second-largest subunit of yeast RNA polymerase III. Mol. Cell. Biol. 1995, 15:1467-1478.
36. Sidorenkov I., Komissarova N., Kashlev M. Crucial role of the RNA:DNA hybrid in the processivity of transcription. Mol. Cell 1998, 2:55-64.
37. Strathern J., Malagon F., Irvin J., Gotte D., Shafer B., Kireeva M., Lubkowska L., Jin D.J., Kashlev M. The fidelity of transcription: RPB1 (RPO21) mutations that increase transcriptional slippage in S. cerevisiae. J. Biol. Chem. 2013, 288:2689-2699.
38. Tomar S.K., Artsimovitch I. NusG-Spt5 proteins-universal tools for transcription modification and communication. Chem. Rev. 2013, 113:8604-8619.
39. Uptain S.M., Kane C.M., Chamberlin M.J. Basic mechanisms of transcript elongation and its regulation. Annu. Rev. Biochem. 1997, 66:117-172.
40. Wu C.C., Lin Y.C., Chen H.T. The TFIIF-like Rpc37/53 dimer lies at the center of a protein network to connect TFIIIC, Bdp1, and the RNA polymerase III active center. Mol. Cell. Biol. 2011, 31:2715-2728.