Transcription termination by the eukaryotic RNA polymerase III.

RNA polymerase (pol) III transcribes a multitude of tRNA and 5S rRNA genes as well as other small RNA genes distributed through the genome. By being sequence-specific, precise and efficient, transcription termination by pol III not only defines the 3' end of the nascent RNA which directs subsequent association with the stabilizing La protein, it also prevents transcription into downstream DNA and promotes efficient recycling. Each of the RNA polymerases appears to have evolved unique mechanisms to initiate the process of termination in response to different types of termination signals. However, in eukaryotes much less is known about the final stage of termination, destabilization of the elongation complex with release of the RNA and DNA from the polymerase active center. By comparison to pols I and II, pol III exhibits the most direct coupling of the initial and final stages of termination, both of which occur at a short oligo(dT) tract on the non-template strand (dA on the template) of the DNA. While pol III termination is autonomous involving the core subunits C2 and probably C1, it also involves subunits C11, C37 and C53, which act on the pol III catalytic center and exhibit homology to the pol II elongation factor TFIIS and TFIIFα/β respectively. Here we compile knowledge of pol III termination and associate mutations that affect this process with structural elements of the polymerase that illustrate the importance of C53/37 both at its docking site on the pol III lobe and in the active center. The models suggest that some of these features may apply to the other eukaryotic pols. This article is part of a Special Issue entitled: Transcription by Odd Pols.

[1]  D. Haussecker,et al.  Human tRNA-derived small RNAs in the global regulation of RNA silencing. , 2010, RNA.

[2]  M. Chamberlin,et al.  RNA chain elongation by Escherichia coli RNA polymerase. Factors affecting the stability of elongating ternary complexes. , 1990, Journal of molecular biology.

[3]  S. Tenenbaum,et al.  Differential phosphorylation and subcellular localization of La RNPs associated with precursor tRNAs and translation-related mRNAs. , 2003, Molecular cell.

[4]  C. Moore,et al.  Unravelling the means to an end: RNA polymerase II transcription termination , 2011, Nature Reviews Molecular Cell Biology.

[5]  C. Carles,et al.  Insights into transcription initiation and termination from the electron microscopy structure of yeast RNA polymerase III. , 2007, Molecular cell.

[6]  G. Kassavetis,et al.  The C53/C37 Subcomplex of RNA Polymerase III Lies Near the Active Site and Participates in Promoter Opening* , 2009, The Journal of Biological Chemistry.

[7]  R. Roeder,et al.  Nuclear factor 1 (NF1) affects accurate termination and multiple‐round transcription by human RNA polymerase III , 2000, The EMBO journal.

[8]  William J. Rice,et al.  Structure and Function of the Transcription Elongation Factor GreB Bound to Bacterial RNA Polymerase , 2003, Cell.

[9]  M. Mathews,et al.  Termination sequence requirements vary among genes transcribed by RNA polymerase III. , 1999, Journal of molecular biology.

[10]  J. Qin,et al.  Phosphorylation of the Human La Antigen on Serine 366 Can Regulate Recycling of RNA Polymerase III Transcription Complexes , 1997, Cell.

[11]  E. Geiduschek,et al.  Two components of Saccharomyces cerevisiae transcription factor IIIB (TFIIIB) are stereospecifically located upstream of a tRNA gene and interact with the second-largest subunit of TFIIIC , 1991, Molecular and cellular biology.

[12]  B. Hall,et al.  The RET1 gene of yeast encodes the second-largest subunit of RNA polymerase III. Structural analysis of the wild-type and ret1-1 mutant alleles. , 1991, The Journal of biological chemistry.

[13]  D. Scherly,et al.  Structure and transcription termination of a lysine tRNA gene from Xenopus laevis. , 1987, Journal of molecular biology.

[14]  Dahlia R. Weiss,et al.  RNA polymerase II trigger loop residues stabilize and position the incoming nucleotide triphosphate in transcription , 2010, Proceedings of the National Academy of Sciences.

[15]  I. Albert,et al.  Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome , 2007, Nature.

[16]  B. Peterlin,et al.  7SK snRNA: a noncoding RNA that plays a major role in regulating eukaryotic transcription , 2012, Wiley interdisciplinary reviews. RNA.

[17]  E. Nudler,et al.  The RNA–DNA Hybrid Maintains the Register of Transcription by Preventing Backtracking of RNA Polymerase , 1997, Cell.

[18]  Si Wu,et al.  A minimal RNA polymerase III transcription system from human cells reveals positive and negative regulatory roles for CK2. , 2003, Molecular cell.

[19]  S. Mahapatra,et al.  Yeast H2A.Z, FACT complex and RSC regulate transcription of tRNA gene through differential dynamics of flanking nucleosomes , 2011, Nucleic acids research.

[20]  P. Cramer,et al.  Structural Basis of Transcription: RNA Polymerase II at 2.8 Ångstrom Resolution , 2001, Science.

[21]  N. Jarrous,et al.  Human RNase P: a tRNA-processing enzyme and transcription factor , 2007, Nucleic acids research.

[22]  G. Barton,et al.  Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. , 2009, RNA.

[23]  Patrick Cramer,et al.  Structural basis of transcription: α-Amanitin–RNA polymerase II cocrystal at 2.8 Å resolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  A. Sentenac,et al.  Facilitated Recycling Pathway for RNA Polymerase III , 1996, Cell.

[25]  R. Maraia,et al.  tRNAomics: tRNA gene copy number variation and codon use provide bioinformatic evidence of a new anticodon:codon wobble pair in a eukaryote. , 2012, RNA.

[26]  A. Németh,et al.  The Reb1‐homologue Ydr026c/Nsi1 is required for efficient RNA polymerase I termination in yeast , 2012, The EMBO journal.

[27]  B. Hall,et al.  In vitro analysis of elongation and termination by mutant RNA polymerases with altered termination behavior , 1996, Molecular and cellular biology.

[28]  Z. Zehner,et al.  A human tRNA(iMet) gene produces multiple transcripts , 1987, Molecular and cellular biology.

[29]  J. Gurdon,et al.  The transcription of 5 S DNA injected into Xenopus oocytes. , 1978, Developmental biology.

[30]  C. Pikaard,et al.  Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing , 2011, Nature Reviews Molecular Cell Biology.

[31]  A. Vannini A structural perspective on RNA polymerase I and RNA polymerase III transcription machineries. , 2013, Biochimica et biophysica acta.

[32]  Jeffrey W. Roberts,et al.  Mechanism of intrinsic transcription termination and antitermination. , 1999, Science.

[33]  B. Cairns,et al.  RSC regulates nucleosome positioning at Pol II genes and density at Pol III genes , 2008, The EMBO journal.

[34]  J. Keene,et al.  Eukaryotic transcription termination factor La mediates transcript release and facilitates reinitiation by RNA polymerase III , 1994, Molecular and cellular biology.

[35]  S. Clarkson,et al.  Efficient synthesis, termination and release of RNA polymerase III transcripts in Xenopus extracts depleted of La protein , 1998, The EMBO journal.

[36]  P. Cramer,et al.  Architecture of the RNA Polymerase II-TFIIS Complex and Implications for mRNA Cleavage , 2003, Cell.

[37]  E. Nudler,et al.  An allosteric path to transcription termination. , 2007, Molecular cell.

[38]  M. Kashlev,et al.  RNA Polymerase Switches between Inactivated and Activated States By Translocating Back and Forth along the DNA and the RNA* , 1997, The Journal of Biological Chemistry.

[39]  J. D. Gralla,et al.  Specific termination of in vitro transcription by calf thymus RNA polymerase III , 1984, Nucleic Acids Res..

[40]  Patrick Cramer,et al.  CTD Tyrosine Phosphorylation Impairs Termination Factor Recruitment to RNA Polymerase II , 2012, Science.

[41]  M. Wegnez,et al.  [Biochemical research on oogenesis. 7. Synthesis and maturation of 5S RNA in the small oocytes of Xenopus laevis]. , 1973, Biochimie.

[42]  R. Burgess,et al.  Termination efficiency at rho-dependent terminators depends on kinetic coupling between RNA polymerase and rho. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[43]  R. Maraia,et al.  A carboxy-terminal basic region controls RNA polymerase III transcription factor activity of human La protein , 1997, Molecular and cellular biology.

[44]  J. Steitz,et al.  Function of the mammalian La protein: evidence for its action in transcription termination by RNA polymerase III. , 1989, The EMBO journal.

[45]  R. Landick,et al.  Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  J. Acker,et al.  Distinct roles of transcription factors TFIIIB and TFIIIC in RNA polymerase III transcription reinitiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[47]  M. Mathews,et al.  Structure of genes for virus-associated RNAI and RNAII of adenovirus type 2. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. Green,et al.  Gene encoding human Ro-associated autoantigen Y5 RNA. , 1996, Nucleic acids research.

[49]  R. Maraia,et al.  3′ processing of eukaryotic precursor tRNAs , 2011, Wiley interdisciplinary reviews. RNA.

[50]  P. Cramer,et al.  Structural biology of RNA polymerase III: subcomplex C17/25 X-ray structure and 11 subunit enzyme model. , 2006, Molecular cell.

[51]  F. Werner,et al.  Evolution of multisubunit RNA polymerases in the three domains of life , 2011, Nature Reviews Microbiology.

[52]  B. Hall,et al.  Termination-altering mutations in the second-largest subunit of yeast RNA polymerase III , 1995, Molecular and cellular biology.

[53]  M. Teichmann,et al.  RNA polymerase III transcription control elements: themes and variations. , 2012, Gene.

[54]  J. Steitz,et al.  Precursor molecules of both human 5S ribosomal RNA and transfer RNAs are bound by a cellular protein reactive with anti-La Lupus antibodies , 1982, Cell.

[55]  J. Epstein,et al.  Imprecise transcription termination within Escherichia coli greA leader gives rise to an array of short transcripts, GraL , 2009, Nucleic acids research.

[56]  B. Coulombe,et al.  Interaction of RNA Polymerase II Fork Loop 2 with Downstream Non-template DNA Regulates Transcription Elongation* , 2011, The Journal of Biological Chemistry.

[57]  R. Reeder,et al.  Transcription termination of RNA polymerase I due to a T-rich element interacting with Reb1p. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[58]  E. Nudler,et al.  Control of Intrinsic Transcription Termination by N and NusA The Basic Mechanisms , 2001, Cell.

[59]  R. Corradini,et al.  Functional Dissection of RNA Polymerase III Termination Using a Peptide Nucleic Acid as a Transcriptional Roadblock* , 2004, Journal of Biological Chemistry.

[60]  J. Reeve,et al.  Archaeal RNA polymerase is sensitive to intrinsic termination directed by transcribed and remote sequences. , 2006, Journal of molecular biology.

[61]  R. Morse,et al.  A transcriptionally active tRNA gene interferes with nucleosome positioning in vivo , 1992, Molecular and cellular biology.

[62]  M. Wegnez,et al.  Biochemical research on oogenesis , 1975 .

[63]  Robert Landick,et al.  Bacterial transcription terminators: the RNA 3'-end chronicles. , 2011, Journal of molecular biology.

[64]  S. Wolin,et al.  Multiple functional interactions between components of the Lsm2-Lsm8 complex, U6 snRNA, and the yeast La protein. , 2001, Genetics.

[65]  Z. Wang,et al.  TFIIIC1 acts through a downstream region to stabilize TFIIIC2 binding to RNA polymerase III promoters , 1996, Molecular and cellular biology.

[66]  L. Tora,et al.  RNA Polymerase II Pausing Downstream of Core Histone Genes Is Different from Genes Producing Polyadenylated Transcripts , 2012, PloS one.

[67]  D. Setzer,et al.  Transcription termination by RNA polymerase III: uncoupling of polymerase release from termination signal recognition , 1992, Molecular and cellular biology.

[68]  Z. Wang,et al.  DNA topoisomerase I and PC4 can interact with human TFIIIC to promote both accurate termination and transcription reinitiation by RNA polymerase III. , 1998, Molecular cell.

[69]  W. Rutter,et al.  Specific Inhibition of Nuclear RNA Polymerase II by α-Amanitin , 1970, Science.

[70]  N. Matsumoto,et al.  Mutations in POLR3A and POLR3B encoding RNA Polymerase III subunits cause an autosomal-recessive hypomyelinating leukoencephalopathy. , 2011, American journal of human genetics.

[71]  A. Vanderver,et al.  Mutations of POLR3A encoding a catalytic subunit of RNA polymerase Pol III cause a recessive hypomyelinating leukodystrophy. , 2011, American journal of human genetics.

[72]  Ying Huang,et al.  Isolation and Cloning of Four Subunits of a Fission Yeast TFIIIC Complex That Includes an Ortholog of the Human Regulatory Protein TFIIICβ* , 2000, The Journal of Biological Chemistry.

[73]  M. Nomura,et al.  Visual Analysis of the Yeast 5S rRNA Gene Transcriptome: Regulation and Role of La Protein , 2008, Molecular and Cellular Biology.

[74]  C. Guthrie,et al.  Transcription of a yeast U6 snRNA gene requires a polymerase III promoter element in a novel position. , 1990, Genes & development.

[75]  A. Berk,et al.  Purification and characterization of transcription factor IIIC2. , 1989, The Journal of biological chemistry.

[76]  B. Hall,et al.  Transcription in yeast: alpha-amanitin sensitivity and other properties which distinguish between RNA polymerases I and III. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Kelvin Hsu,et al.  The RNA polymerase III terminator used by a B1-Alu element can modulate 3' processing of the intermediate RNA product , 1992, Molecular and cellular biology.

[78]  G. Drouin,et al.  The increase in the number of subunits in eukaryotic RNA polymerase III relative to RNA polymerase II is due to the permanent recruitment of general transcription factors. , 2010, Molecular biology and evolution.

[79]  R. Maraia,et al.  Terminator-specific Recycling of a B1-AluTranscription Complex by RNA Polymerase III Is Mediated by the RNA Terminus-binding Protein La* , 1998, The Journal of Biological Chemistry.

[80]  V. Praz,et al.  Widespread occurrence of non-canonical transcription termination by human RNA polymerase III , 2011, Nucleic acids research.

[81]  M. Mohamed,et al.  Determinants of vaccinia virus early gene transcription termination. , 2008, Virology.

[82]  J. Acker,et al.  A subcomplex of RNA polymerase III subunits involved in transcription termination and reinitiation , 2006, The EMBO journal.

[83]  Robert J. White,et al.  Human La is found at RNA polymerase III-transcribed genes in vivo. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[84]  E. Geiduschek,et al.  Analysis of RNA chain elongation and termination by Saccharomyces cerevisiae RNA polymerase III. , 1994, Journal of molecular biology.

[85]  M. Gillespie,et al.  Schizosaccharomyces U6 genes have a sequence within their introns that matches the B box consensus of tRNA internal promoters. , 1990, Nucleic acids research.

[86]  J. Gurdon,et al.  Cloned single repeating units of 5S DNA direct accurate transcription of 5S RNA when injected into Xenopus oocytes. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Y. Ben-Asouli,et al.  A role for the catalytic ribonucleoprotein RNase P in RNA polymerase III transcription. , 2006, Genes & development.

[88]  J. Garrels,et al.  Characterization and purification of lupus antigen La, and RNA-binding protein , 1985, Molecular and cellular biology.

[89]  S. Shivaswamy,et al.  High-Level Activation of Transcription of the Yeast U6 snRNA Gene in Chromatin by the Basal RNA Polymerase III Transcription Factor TFIIIC , 2004, Molecular and Cellular Biology.

[90]  Patrick Cramer,et al.  Review Conservation between the Rna Polymerase I, Ii, and Iii Transcription Initiation Machineries , 2022 .

[91]  D. Bushnell,et al.  Structural basis of eukaryotic gene transcription , 2005, FEBS letters.

[92]  J. E. Stefano Purified lupus antigen la recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts , 1984, Cell.

[93]  P. Cramer,et al.  Structural basis of transcription: mismatch-specific fidelity mechanisms and paused RNA polymerase II with frayed RNA. , 2009, Molecular cell.

[94]  P. Cramer,et al.  Structural basis of transcription inhibition by α-amanitin and implications for RNA polymerase II translocation , 2008, Nature Structural &Molecular Biology.

[95]  P. Cramer,et al.  Structural Basis of Transcription: An RNA Polymerase II Elongation Complex at 3.3 Å Resolution , 2001, Science.

[96]  Patricia Richard,et al.  Transcription termination by nuclear RNA polymerases. , 2009, Genes & development.

[97]  P. Cramer,et al.  Molecular basis of RNA polymerase III transcription repression by Maf1 & Structure of human mitochondrial RNA polymerase. , 2011 .

[98]  I. Tinoco,et al.  DNA-RNA hybrid duplexes containing oligo(dA:rU) sequences are exceptionally unstable and may facilitate termination of transcription. , 1980, Nucleic acids research.

[99]  L. J. Korn,et al.  Nucleotide sequence of xenopus borealis oocyte 5S DNA: Comparison of sequences that flank several related eucaryotic genes , 1978, Cell.

[100]  Craig D. Kaplan,et al.  Structural Basis of Transcription: Role of the Trigger Loop in Substrate Specificity and Catalysis , 2006, Cell.

[101]  R. Maraia,et al.  Transcription Termination by RNA Polymerase III in Fission Yeast , 2000, The Journal of Biological Chemistry.

[102]  N. Cozzarelli,et al.  Purified RNA polymerase III accurately and efficiently terminates transcription of 5s RNA genes , 1983, Cell.

[103]  Yu-Chun Lin,et al.  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 , 2011, Molecular and Cellular Biology.

[104]  Ying Huang,et al.  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 , 2005, Molecular and Cellular Biology.

[105]  E. Nudler,et al.  Coupling between transcription termination and RNA polymerase inchworming , 1995, Cell.

[106]  D. Brow,et al.  RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts , 2001, Nature.

[107]  A. Sentenac,et al.  Mutations in the alpha‐amanitin conserved domain of the largest subunit of yeast RNA polymerase III affect pausing, RNA cleavage and transcriptional transitions. , 1996, The EMBO journal.

[108]  E. Geiduschek,et al.  The subunit structure of Saccharomyces cerevisiae transcription factor IIIC probed with a novel photocrosslinking reagent. , 1990, The EMBO journal.

[109]  E. Nudler RNA polymerase active center: the molecular engine of transcription. , 2009, Annual review of biochemistry.

[110]  D. Bogenhagen,et al.  Nucleotide sequences in Xenopus 5S DNA required for transcription termination , 1981, Cell.

[111]  Jianhua Fu,et al.  Structure of the 12-Subunit RNA Polymerase II Refined with the Aid of Anomalous Diffraction Data* , 2009, Journal of Biological Chemistry.

[112]  D. Tollervey,et al.  Efficient termination of transcription by RNA polymerase I requires the 5' exonuclease Rat1 in yeast. , 2008, Genes & development.

[113]  K.,et al.  Hydrolytic cleavage of nascent RNA in RNA polymerase III ternary transcription complexes. , 1994, The Journal of biological chemistry.

[114]  N. Hernandez,et al.  Recruitment of RNA polymerase III to its target promoters. , 2002, Genes & development.

[115]  B. Hall,et al.  Mutational Analysis of the Hydrolytic Activity of Yeast RNA Polymerase III* , 1999, The Journal of Biological Chemistry.

[116]  A. Vanderver,et al.  Recessive mutations in POLR3B, encoding the second largest subunit of Pol III, cause a rare hypomyelinating leukodystrophy. , 2011, American journal of human genetics.

[117]  R. Maraia,et al.  Point mutations in the Rpb9-homologous domain of Rpc11 that impair transcription termination by RNA polymerase III , 2011, Nucleic acids research.

[118]  R. Ferrari,et al.  The transcription reinitiation properties of RNA polymerase III in the absence of transcription factors , 2007, Cellular & Molecular Biology Letters.

[119]  C. Carles,et al.  The RNA cleavage activity of RNA polymerase III is mediated by an essential TFIIS-like subunit and is important for transcription termination. , 1998, Genes & development.

[120]  K. Agarwal,et al.  The transcription factor TFIIS zinc ribbon dipeptide Asp-Glu is critical for stimulation of elongation and RNA cleavage by RNA polymerase II. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[121]  A. Hopper,et al.  Maf1 Protein, Repressor of RNA Polymerase III, Indirectly Affects tRNA Processing* , 2011, The Journal of Biological Chemistry.

[122]  S. Wolin,et al.  A role for the yeast La protein in U6 snRNP assembly: evidence that the La protein is a molecular chaperone for RNA polymerase III transcripts , 1998, The EMBO journal.

[123]  M. Kashlev,et al.  The 8-Nucleotide-long RNA:DNA Hybrid Is a Primary Stability Determinant of the RNA Polymerase II Elongation Complex* , 2000, The Journal of Biological Chemistry.

[124]  F. Dietrich,et al.  Identification and characterization of upstream open reading frames (uORF) in the 5′ untranslated regions (UTR) of genes in Saccharomyces cerevisiae , 2005, Current Genetics.

[125]  Evgeny Nudler,et al.  RNA Polymerase Backtracking in Gene Regulation and Genome Instability , 2012, Cell.

[126]  E. Nudler,et al.  The mechanism of intrinsic transcription termination. , 1999, Molecular cell.

[127]  Riccardo Percudani,et al.  Sequence Context Effects on Oligo(dT) Termination Signal Recognition by Saccharomyces cerevisiae RNA Polymerase III* , 2005, Journal of Biological Chemistry.

[128]  S. Wolin,et al.  The Yeast La Protein Is Required for the 3′ Endonucleolytic Cleavage That Matures tRNA Precursors , 1997, Cell.

[129]  R. Reddy,et al.  The 3' end formation in small RNAs. , 2002, Gene expression.

[130]  S. Shivaswamy,et al.  Positioned Nucleosomes Due to Sequential Remodeling of the Yeast U6 Small Nuclear RNA Chromatin Are Essential for Its Transcriptional Activation* , 2006, Journal of Biological Chemistry.

[131]  Robert J. White,et al.  Transcription by RNA polymerase III: more complex than we thought , 2011, Nature Reviews Genetics.

[132]  N. Proudfoot,et al.  Budding yeast RNA polymerases I and II employ parallel mechanisms of transcriptional termination. , 2008, Genes & development.

[133]  Robert J White RNA polymerase III transcription and cancer , 2004, Oncogene.

[134]  I. Tinoco,et al.  End-to-end transcription of an Alu family repeat. A new type of polymerase-III-dependent terminator and its evolutionary implication. , 1985, Journal of molecular biology.

[135]  Lynne Marshall,et al.  Diminished Activity of RNA Polymerase III Selectively Disrupts Tissues with the Most Actively Dividing Cells , 2007, PLoS biology.

[136]  D. D. Brown,et al.  The nucleotide sequence adjoining the 3' end of the genes coding for oocyte-type 5 S ribosomal RNA in Xenopus. , 1976, Journal of molecular biology.

[137]  Q. Ju,et al.  A model for transcription termination by RNA polymerase I , 1994, Cell.

[138]  C. Schmid,et al.  Palindromic sequences preceding the terminator increase polymerase III template activity. , 1997, Nucleic acids research.

[139]  B. Hall,et al.  ret1-1, a yeast mutant affecting transcription termination by RNA polymerase III. , 1990, Genetics.

[140]  P. Thuriaux,et al.  A protein-protein interaction map of yeast RNA polymerase III. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[141]  R. Landick,et al.  Amino acid changes in conserved regions of the beta-subunit of Escherichia coli RNA polymerase alter transcription pausing and termination. , 1990, Genes & development.

[142]  Jeffrey W. Roberts,et al.  Forward translocation is the natural pathway of RNA release at an intrinsic terminator. , 2004, Molecular cell.

[143]  A. Malhotra,et al.  A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). , 2009, Genes & development.

[144]  R. Maraia,et al.  RNA polymerase III mutants in TFIIFα-like C37 that cause terminator readthrough with no decrease in transcription output , 2012, Nucleic acids research.

[145]  J. Steitz,et al.  The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. , 1989, The EMBO journal.

[146]  B. Coulombe,et al.  Structural Perspective on Mutations Affecting the Function of Multisubunit RNA Polymerases , 2006, Microbiology and Molecular Biology Reviews.

[147]  Ying Huang,et al.  Separate RNA-binding surfaces on the multifunctional La protein mediate distinguishable activities in tRNA maturation , 2006, Nature Structural &Molecular Biology.

[148]  M. Teichmann,et al.  The expanding RNA polymerase III transcriptome. , 2007, Trends in genetics : TIG.

[149]  M. Kashlev,et al.  Shortening of RNA:DNA hybrid in the elongation complex of RNA polymerase is a prerequisite for transcription termination. , 2002, Molecular cell.

[150]  G. Hutvagner,et al.  Transfer RNA‐derived fragments: origins, processing, and functions , 2011, Wiley interdisciplinary reviews. RNA.

[151]  C. Gross,et al.  Determination of intrinsic transcription termination efficiency by RNA polymerase elongation rate. , 1994, Science.

[152]  I. Artsimovitch,et al.  Termination and antitermination: RNA polymerase runs a stop sign , 2011, Nature Reviews Microbiology.

[153]  J. Steitz,et al.  Association of the lupus antigen La with a subset of U6 snRNA molecules. , 1985, Nucleic acids research.

[154]  B. Hall,et al.  Substrate Specificity of the RNase Activity of Yeast RNA Polymerase III* , 1997, The Journal of Biological Chemistry.

[155]  P. Bhargava,et al.  Chromatin Structure and Expression of a Gene Transcribed by RNA Polymerase III Are Independent of H2A.Z Deposition , 2008, Molecular and Cellular Biology.

[156]  Jeffrey W. Roberts,et al.  Role of the non-template strand of the elongation bubble in intrinsic transcription termination. , 2003, Journal of molecular biology.

[157]  M. Kashlev,et al.  Crucial role of the RNA:DNA hybrid in the processivity of transcription. , 1998, Molecular cell.

[158]  M. Pack,et al.  Mutation of RNA Pol III Subunit rpc2/polr3b Leads to Deficiency of Subunit Rpc11 and Disrupts Zebrafish Digestive Development , 2007, PLoS biology.

[159]  R. Schiffmann,et al.  4H syndrome with late-onset growth hormone deficiency caused by POLR3A mutations. , 2012, Archives of neurology.

[160]  P. Cramer,et al.  Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. , 2004, Molecular cell.

[161]  O. Harismendy,et al.  Nucleosome Depletion Activates Poised RNA Polymerase III at Unconventional Transcription Sites in Saccharomyces cerevisiae* , 2006, Journal of Biological Chemistry.

[162]  O. Laptenko,et al.  Transcript cleavage factors GreA and GreB act as transient catalytic components of RNA polymerase , 2003, The EMBO journal.

[163]  C. Müller,et al.  Conformational flexibility of RNA polymerase III during transcriptional elongation , 2010, The EMBO journal.

[164]  R. Roeder,et al.  Isolation and genomic arrangement of active and inactive forms of mammalian 5 S RNA genes. , 1984, The Journal of biological chemistry.

[165]  B. Hall,et al.  Effects of alterations in the 3′ flanking sequence on in vivo and in vitro expression of the yeast SUP4‐o tRNATyr gene. , 1985, The EMBO journal.

[166]  M. Mathews,et al.  La antigen recognizes and binds to the 3'-oligouridylate tail of a small RNA , 1984, Molecular and cellular biology.