Home LiteratureArticle Details
PMID: 11387215 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The RNA polymerase III transcription initiation factor TFIIIB participates in two steps of promoter opening.

The EMBO journal ·Vol. 20 ·No. 11 ·2001-06-01 ·Pages 2823-34

Kassavetis GA, Letts GA, Geiduschek EP

Abstract

Evidence for post-recruitment functions of yeast transcription factor (TF)IIIB in initiation of transcription was first provided by the properties of TFIIIB-RNA polymerase III-promoter complexes assembled with deletion mutants of its Brf and B" subunits that are transcriptionally inactive because they fail to open the promoter. The experiments presented here show that these defects can be repaired by unpairing short (3 or 5 bp) DNA segments spanning the transcription bubble of the open promoter complex. Analysis of this suppression phenomenon indicates that TFIIIB participates in two steps of promoter opening by RNA polymerase III that are comparable to the successive steps of promoter opening by bacterial RNA polymerase holoenzyme. B" deletions between amino acids 355 and 421 interfere with the initiating step of DNA strand separation at the upstream end of the transcription bubble. Removing an N-terminal domain of Brf interferes with downstream propagation of the transcription bubble to and beyond the transcriptional start site.

MeSH Terms
Base Sequence Candida albicans/genetics DNA, Fungal/chemistry,genetics Kluyveromyces/genetics Molecular Sequence Data Nucleic Acid Conformation Nucleic Acid Heteroduplexes/chemistry,genetics Promoter Regions, Genetic Protein Subunits RNA Polymerase III/chemistry,genetics,metabolism Recombinant Proteins/chemistry,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins Sequence Deletion TATA Box Templates, Genetic Transcription Factor TFIIIB Transcription Factors/chemistry,genetics,metabolism Transcription, Genetic
Chemicals
BRF1 protein, S cerevisiae DNA, Fungal Nucleic Acid Heteroduplexes Protein Subunits Recombinant Proteins Saccharomyces cerevisiae Proteins Transcription Factor TFIIIB Transcription Factors RNA Polymerase III
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kassavetis G A
Department of Biology and Center for Molecular Genetics, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0634, USA. [email protected]
Letts G A
Geiduschek E P
References (55)
55 references, click to expand
  1. The TFIIIC90 subunit of TFIIIC interacts with multiple components of the RNA polymerase III machinery and contains a histone-specific acetyltransferase activity.
    Mol Cell Biol. 1999 Nov;19(11):7697-704 PMID: 10523658
  2. A protein-protein interaction map of yeast RNA polymerase III.
    Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):7815-20 PMID: 10393904
  3. Interaction between yeast RNA polymerase III and transcription factor TFIIIC via ABC10alpha and tau131 subunits.
    J Biol Chem. 1999 Nov 19;274(47):33462-8 PMID: 10559229
  4. A novel subunit of yeast RNA polymerase III interacts with the TFIIB-related domain of TFIIIB70.
    Mol Cell Biol. 2000 Jan;20(2):488-95 PMID: 10611227
  5. Escherichia coli promoter opening and -10 recognition: mutational analysis of sigma70.
    EMBO J. 2000 Mar 1;19(5):1130-7 PMID: 10698953
  6. Peeling by binding or twisting by cranking: models for promoter opening and transcription initiation by RNA polymerase II.
    Bioessays. 2000 Apr;22(4):316-26 PMID: 10723029
  7. The zinc ribbon domains of the general transcription factors TFIIB and Brf: conserved functional surfaces but different roles in transcription initiation.
    Genes Dev. 2000 Mar 15;14(6):719-30 PMID: 10733531
  8. The role of transcription factor B in transcription initiation and promoter clearance in the archaeon Sulfolobus acidocaldarius.
    J Biol Chem. 2000 Apr 28;275(17):12934-40 PMID: 10777593
  9. DNA melting and promoter clearance by eukaryotic RNA polymerase I.
    J Mol Biol. 2000 May 26;299(1):75-89 PMID: 10860723
  10. Aromatic amino acids in region 2.3 of Escherichia coli sigma 70 participate collectively in the formation of an RNA polymerase-promoter open complex.
    J Mol Biol. 2000 Jun 23;299(5):1217-30 PMID: 10873447
  11. Isomerization of a binary sigma-promoter DNA complex by transcription activators.
    Nat Struct Biol. 2000 Jul;7(7):594-601 PMID: 10876247
  12. Structural organization of the RNA polymerase-promoter open complex.
    Cell. 2000 Jun 9;101(6):601-11 PMID: 10892647
  13. A structural model of transcription elongation.
    Science. 2000 Jul 28;289(5479):619-25 PMID: 10915625
  14. Promoter opening by sigma(54) and sigma(70) RNA polymerases: sigma factor-directed alterations in the mechanism and tightness of control.
    Genes Dev. 2000 Sep 1;14(17):2242-55 PMID: 10970887
  15. The Brf and TATA-binding protein subunits of the RNA polymerase III transcription factor IIIB mediate position-specific integration of the gypsy-like element, Ty3.
    J Biol Chem. 2000 Sep 22;275(38):29800-7 PMID: 10882723
  16. Sequence determinants for the recognition of the fork junction DNA containing the -10 region of promoter DNA by E. coli RNA polymerase.
    Biochemistry. 2000 Oct 10;39(40):12274-83 PMID: 11015206
  17. Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes.
    Cell. 1980 Mar;19(3):717-28 PMID: 6153931
  18. KMnO4 as a probe for lac promoter DNA melting and mechanism in vivo.
    J Biol Chem. 1989 May 15;264(14):8074-81 PMID: 2722774
  19. Transcription factor IIIB generates extended DNA interactions in RNA polymerase III transcription complexes on tRNA genes.
    Mol Cell Biol. 1989 Jun;9(6):2551-66 PMID: 2668737
  20. S. cerevisiae TFIIIB is the transcription initiation factor proper of RNA polymerase III, while TFIIIA and TFIIIC are assembly factors.
    Cell. 1990 Jan 26;60(2):235-45 PMID: 2404611
  21. Transcription termination by RNA polymerase III: uncoupling of polymerase release from termination signal recognition.
    Mol Cell Biol. 1992 May;12(5):2260-72 PMID: 1314952
  22. Formation of open and elongating transcription complexes by RNA polymerase III.
    J Mol Biol. 1992 Jul 5;226(1):47-58 PMID: 1619662
  23. Topography of transcription factor complexes on the Saccharomyces cerevisiae 5 S RNA gene.
    J Mol Biol. 1992 Dec 20;228(4):1063-77 PMID: 1474578
  24. Evidence that transcription factor IIB is required for a post-assembly step in transcription initiation.
    J Biol Chem. 1999 Sep 3;274(36):25807-13 PMID: 10464320
  25. A minimal RNA polymerase III transcription system.
    EMBO J. 1999 Sep 15;18(18):5042-51 PMID: 10487756
  26. Orientation and topography of RNA polymerase III in transcription complexes.
    Mol Cell Biol. 1993 Feb;13(2):942-52 PMID: 8423814
  27. TFIIIC relieves repression of U6 snRNA transcription by chromatin.
    Nature. 1993 Apr 1;362(6419):475-7 PMID: 8464480
  28. Interaction between a complex of RNA polymerase III subunits and the 70-kDa component of transcription factor IIIB.
    J Biol Chem. 1993 Oct 5;268(28):20721-4 PMID: 8407894
  29. A mutation in the second largest subunit of TFIIIC increases a rate-limiting step in transcription by RNA polymerase III.
    Mol Cell Biol. 1994 Jan;14(1):822-30 PMID: 8264649
  30. Identical components of yeast transcription factor IIIB are required and sufficient for transcription of TATA box-containing and TATA-less genes.
    Mol Cell Biol. 1994 Apr;14(4):2798-808 PMID: 8139577
  31. Probing close DNA contacts of RNA polymerase III transcription complexes with the photoactive nucleoside 4-thiodeoxythymidine.
    J Biol Chem. 1994 Jul 8;269(27):18090-5 PMID: 8027070
  32. Characterization of sua7 mutations defines a domain of TFIIB involved in transcription start site selection in yeast.
    J Biol Chem. 1994 Dec 2;269(48):30569-73 PMID: 7982976
  33. Conserved functional domains of the RNA polymerase III general transcription factor BRF.
    Genes Dev. 1994 Dec 1;8(23):2879-90 PMID: 7995525
  34. A mutation in the C31 subunit of Saccharomyces cerevisiae RNA polymerase III affects transcription initiation.
    EMBO J. 1995 Jan 16;14(2):351-9 PMID: 7835345
  35. Reciprocal interferences between nucleosomal organization and transcriptional activity of the yeast SNR6 gene.
    Genes Dev. 1995 Feb 15;9(4):410-22 PMID: 7883166
  36. Cloning, expression, and function of TFC5, the gene encoding the B" component of the Saccharomyces cerevisiae RNA polymerase III transcription factor TFIIIB.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9786-90 PMID: 7568218
  37. The symmetry of the yeast U6 RNA gene's TATA box and the orientation of the TATA-binding protein in yeast TFIIIB.
    Genes Dev. 1995 Dec 1;9(23):2974-85 PMID: 7498793
  38. Facilitated recycling pathway for RNA polymerase III.
    Cell. 1996 Jan 26;84(2):245-52 PMID: 8565070
  39. A suppressor of mutations in the class III transcription system encodes a component of yeast TFIIIB.
    EMBO J. 1996 Apr 15;15(8):1941-9 PMID: 8617241
  40. Cloning and functional characterization of the gene encoding the TFIIIB90 subunit of RNA polymerase III transcription factor TFIIIB.
    J Biol Chem. 1996 Jun 21;271(25):14903-9 PMID: 8662956
  41. A minimal set of RNA polymerase II transcription protein interactions.
    J Biol Chem. 1996 Aug 16;271(33):20170-4 PMID: 8702741
  42. Functional dissection of the B" component of RNA polymerase III transcription factor IIIB: a scaffolding protein with multiple roles in assembly and initiation of transcription.
    Mol Cell Biol. 1997 Apr;17(4):1868-80 PMID: 9121435
  43. DNA-melting at the Bacillus subtilis flagellin promoter nucleates near -10 and expands unidirectionally.
    J Mol Biol. 1997 Mar 21;267(1):47-59 PMID: 9096206
  44. Domains of the Brf component of RNA polymerase III transcription factor IIIB (TFIIIB): functions in assembly of TFIIIB-DNA complexes and recruitment of RNA polymerase to the promoter.
    Mol Cell Biol. 1997 Sep;17(9):5299-306 PMID: 9271407
  45. A differential response of wild type and mutant promoters to TFIIIB70 overexpression in vivo and in vitro.
    Nucleic Acids Res. 1998 May 15;26(10):2344-52 PMID: 9580684
  46. The N-terminal region of yeast TFIIB contains two adjacent functional domains involved in stable RNA polymerase II binding and transcription start site selection.
    J Biol Chem. 1998 Jul 10;273(28):17859-64 PMID: 9651390
  47. A post-recruitment function for the RNA polymerase III transcription-initiation factor IIIB.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9196-201 PMID: 9689057
  48. Functional and structural organization of Brf, the TFIIB-related component of the RNA polymerase III transcription initiation complex.
    Mol Cell Biol. 1998 Sep;18(9):5587-99 PMID: 9710642
  49. Intermediates in formation and activity of the RNA polymerase II preinitiation complex: holoenzyme recruitment and a postrecruitment role for the TATA box and TFIIB.
    Genes Dev. 1999 Jan 1;13(1):49-63 PMID: 9887099
  50. Human TFIIIC relieves chromatin-mediated repression of RNA polymerase III transcription and contains an intrinsic histone acetyltransferase activity.
    Mol Cell Biol. 1999 Feb;19(2):1605-15 PMID: 9891093
  51. The role of human TFIIB in transcription start site selection in vitro and in vivo.
    J Biol Chem. 1999 May 14;274(20):14337-43 PMID: 10318856
  52. Protein-nucleic acid interactions during open complex formation investigated by systematic alteration of the protein and DNA binding partners.
    Biochemistry. 1999 May 11;38(19):5959-67 PMID: 10320321
  53. Mutagenesis of yeast TFIIIB70 reveals C-terminal residues critical for interaction with TBP and C34.
    J Mol Biol. 1999 May 14;288(4):511-20 PMID: 10329159
  54. The yeast RNA polymerase III transcription machinery: a paradigm for eukaryotic gene activation.
    Cold Spring Harb Symp Quant Biol. 1998;63:381-9 PMID: 10384303
  55. The selective degradation of pyrimidines in nucleic acids by permanganate oxidation.
    Biochem Biophys Res Commun. 1967 Nov 30;29(4):556-61 PMID: 16496535
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2001-06-01
Pages
2823-34
Language
English
Region
England
NLM ID
8208664
PMCID
PMC125488
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]