RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription
Abstract
All organisms—bacteria, archaea, and eukaryotes—have a transcription initiation factor that contains a structural module that binds within the RNA polymerase (RNAP) active-center cleft and interacts with template-strand single-stranded DNA (ssDNA) in the immediate vicinity of the RNAP active center. This transcription initiation-factor structural module preorganizes template-strand ssDNA to engage the RNAP active center, thereby facilitating binding of initiating nucleotides and enabling transcription initiation from initiating mononucleotides. However, this transcription initiation-factor structural module occupies the path of nascent RNA and thus presumably must be displaced before or during initial transcription. In this paper, we report four sets of crystal structures of bacterial initially transcribing complexes that demonstrate and define details of stepwise, RNA-extension-driven displacement of the “σ-finger” of the bacterial transcription initiation factor σ. The structures reveal that—for both the primary σ-factor and extracytoplasmic (ECF) σ-factors, and for both 5'-triphosphate RNA and 5'-hydroxy RNA—the “σ-finger” is displaced in stepwise fashion, progressively folding back upon itself, driven by collision with the RNA 5'-end, upon extension of nascent RNA from ~5 nt to ~10 nt.
- Authors:
-
- Chinese Academy of Sciences (CAS), Shanghai (China); Univ. of Chinese Academy of Sciences, Beijing (China)
- Rutgers Univ., Piscataway, NJ (United States)
- Chinese Academy of Sciences (CAS), Shanghai (China); Rutgers Univ., Piscataway, NJ (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- Chinese Academy of Sciences (CAS); National Natural Science Foundation of China (NSFC); National Institutes of Health (NIH)
- OSTI Identifier:
- 1608866
- Grant/Contract Number:
- 31670067; 31822001; QYZDB-SSWSMC005; GM041376
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 117; Journal Issue: 11; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; transcription initiation; initial transcription; promoter escape; sigma factor; initiation factor
Citation Formats
Li, Lingting, Molodtsov, Vadim, Lin, Wei, Ebright, Richard H., and Zhang, Yu. RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription. United States: N. p., 2020.
Web. doi:10.1073/pnas.1920747117.
Li, Lingting, Molodtsov, Vadim, Lin, Wei, Ebright, Richard H., & Zhang, Yu. RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription. United States. https://doi.org/10.1073/pnas.1920747117
Li, Lingting, Molodtsov, Vadim, Lin, Wei, Ebright, Richard H., and Zhang, Yu. Tue .
"RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription". United States. https://doi.org/10.1073/pnas.1920747117. https://www.osti.gov/servlets/purl/1608866.
@article{osti_1608866,
title = {RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription},
author = {Li, Lingting and Molodtsov, Vadim and Lin, Wei and Ebright, Richard H. and Zhang, Yu},
abstractNote = {All organisms—bacteria, archaea, and eukaryotes—have a transcription initiation factor that contains a structural module that binds within the RNA polymerase (RNAP) active-center cleft and interacts with template-strand single-stranded DNA (ssDNA) in the immediate vicinity of the RNAP active center. This transcription initiation-factor structural module preorganizes template-strand ssDNA to engage the RNAP active center, thereby facilitating binding of initiating nucleotides and enabling transcription initiation from initiating mononucleotides. However, this transcription initiation-factor structural module occupies the path of nascent RNA and thus presumably must be displaced before or during initial transcription. In this paper, we report four sets of crystal structures of bacterial initially transcribing complexes that demonstrate and define details of stepwise, RNA-extension-driven displacement of the “σ-finger” of the bacterial transcription initiation factor σ. The structures reveal that—for both the primary σ-factor and extracytoplasmic (ECF) σ-factors, and for both 5'-triphosphate RNA and 5'-hydroxy RNA—the “σ-finger” is displaced in stepwise fashion, progressively folding back upon itself, driven by collision with the RNA 5'-end, upon extension of nascent RNA from ~5 nt to ~10 nt.},
doi = {10.1073/pnas.1920747117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 11,
volume = 117,
place = {United States},
year = {2020},
month = {3}
}
Web of Science
Works referenced in this record:
NanoRNAs Prime Transcription Initiation In Vivo
journal, June 2011
- Goldman, Seth R.; Sharp, Josh S.; Vvedenskaya, Irina O.
- Molecular Cell, Vol. 42, Issue 6
Displacement of the transcription factor B reader domain during transcription initiation
journal, August 2018
- Dexl, Stefan; Reichelt, Robert; Kraatz, Katharina
- Nucleic Acids Research, Vol. 46, Issue 19
Near-atomic resolution visualization of human transcription promoter opening
journal, May 2016
- He, Yuan; Yan, Chunli; Fang, Jie
- Nature, Vol. 533, Issue 7603
The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) σ factor protein family: ECF σ factor classification
journal, September 2009
- Staroń, Anna; Sofia, Heidi J.; Dietrich, Sascha
- Molecular Microbiology, Vol. 74, Issue 3
Abortive Initiation and Productive Initiation by RNA Polymerase Involve DNA Scrunching
journal, November 2006
- Revyakin, A.; Liu, C.; Ebright, R. H.
- Science, Vol. 314, Issue 5802
Initial Transcription by RNA Polymerase Proceeds Through a DNA-Scrunching Mechanism
journal, November 2006
- Kapanidis, A. N.; Margeat, E.; Ho, S. O.
- Science, Vol. 314, Issue 5802
Molecular mechanism of promoter opening by RNA polymerase III
journal, January 2018
- Vorländer, Matthias K.; Khatter, Heena; Wetzel, Rene
- Nature, Vol. 553, Issue 7688
Themes and variations in gene regulation by extracytoplasmic function (ECF) sigma factors
journal, April 2017
- Sineva, Elena; Savkina, Maria; Ades, Sarah E.
- Current Opinion in Microbiology, Vol. 36
RNA polymerase II–TFIIB structure and mechanism of transcription initiation
journal, October 2009
- Kostrewa, Dirk; Zeller, Mirijam E.; Armache, Karim-Jean
- Nature, Vol. 462, Issue 7271
Changes in Conserved Region 3 of Escherichia coli ς 70 Reduce Abortive Transcription and Enhance Promoter Escape
journal, December 2002
- Cashel, Michael; Hsu, Lilian M.; Hernandez, V. James
- Journal of Biological Chemistry, Vol. 278, Issue 8
Structural basis of RNA polymerase III transcription initiation
journal, January 2018
- Abascal-Palacios, Guillermo; Ramsay, Ewan Phillip; Beuron, Fabienne
- Nature, Vol. 553, Issue 7688
TFIIB Is Only ∼9 Å Away from the 5'-End of a Trimeric RNA Primer in a Functional RNA Polymerase II Preinitiation Complex
journal, March 2015
- Bick, Matthew J.; Malik, Sohail; Mustaev, Arkady
- PLOS ONE, Vol. 10, Issue 3
Structure and function of the initially transcribing RNA polymerase II–TFIIB complex
journal, November 2012
- Sainsbury, Sarah; Niesser, Jürgen; Cramer, Patrick
- Nature, Vol. 493, Issue 7432
Structural basis of transcription activation
journal, June 2016
- Feng, Y.; Zhang, Y.; Ebright, R. H.
- Science, Vol. 352, Issue 6291
A Single-Molecule View of Archaeal Transcription
journal, September 2019
- Kramm, Kevin; Endesfelder, Ulrike; Grohmann, Dina
- Journal of Molecular Biology, Vol. 431, Issue 20
Structural Basis of RNA Polymerase I Transcription Initiation
journal, March 2017
- Engel, Christoph; Gubbey, Tobias; Neyer, Simon
- Cell, Vol. 169, Issue 1
Structural Basis of Transcription Initiation by Bacterial RNA Polymerase Holoenzyme
journal, June 2014
- Basu, Ritwika S.; Warner, Brittany A.; Molodtsov, Vadim
- Journal of Biological Chemistry, Vol. 289, Issue 35
Structures of RNA Polymerase Closed and Intermediate Complexes Reveal Mechanisms of DNA Opening and Transcription Initiation
journal, July 2017
- Glyde, Robert; Ye, Fuzhou; Darbari, Vidya Chandran
- Molecular Cell, Vol. 67, Issue 1
Structural insights into transcription initiation by yeast RNA polymerase I
journal, July 2017
- Sadian, Yashar; Tafur, Lucas; Kosinski, Jan
- The EMBO Journal, Vol. 36, Issue 18
Structural Basis for NusA Stabilized Transcriptional Pausing
journal, March 2018
- Guo, Xieyang; Myasnikov, Alexander G.; Chen, James
- Molecular Cell, Vol. 69, Issue 5
RNA Polymerase Pausing during Initial Transcription
journal, September 2016
- Duchi, Diego; Bauer, David L. V.; Fernandez, Laurent
- Molecular Cell, Vol. 63, Issue 6
Crystal Structures of the E. coli Transcription Initiation Complexes with a Complete Bubble
journal, May 2015
- Zuo, Yuhong; Steitz, Thomas A.
- Molecular Cell, Vol. 58, Issue 3
Structural basis for −10 promoter element melting by environmentally induced sigma factors
journal, February 2014
- Campagne, Sébastien; Marsh, May E.; Capitani, Guido
- Nature Structural & Molecular Biology, Vol. 21, Issue 3
Structures of the RNA polymerase- 54 reveal new and conserved regulatory strategies
journal, August 2015
- Yang, Y.; Darbari, V. C.; Zhang, N.
- Science, Vol. 349, Issue 6250
GE23077 binds to the RNA polymerase ‘i’ and ‘i+1’ sites and prevents the binding of initiating nucleotides
journal, April 2014
- Zhang, Yu; Degen, David; Ho, Mary X.
- eLife, Vol. 3
Structural mechanism of ATP-independent transcription initiation by RNA polymerase I
journal, June 2017
- Han, Yan; Yan, Chunli; Nguyen, Thi Hoang Duong
- eLife, Vol. 6
Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution
journal, May 2002
- Vassylyev, Dmitry G.; Sekine, Shun-ichi; Laptenko, Oleg
- Nature, Vol. 417, Issue 6890
Structural Basis of Transcription Initiation
journal, October 2012
- Zhang, Y.; Feng, Y.; Chatterjee, S.
- Science, Vol. 338, Issue 6110
Extra Cytoplasmic Function sigma factors, recent structural insights into promoter recognition and regulation
journal, February 2015
- Campagne, Sébastien; Allain, Frédéric H-T; Vorholt, Julia A.
- Current Opinion in Structural Biology, Vol. 30
The Structural Basis for Promoter −35 Element Recognition by the Group IV σ Factors
journal, August 2006
- Lane, William J.; Darst, Seth A.
- PLoS Biology, Vol. 4, Issue 9
Structure of an RNA Polymerase II–TFIIB Complex and the Transcription Initiation Mechanism
journal, November 2009
- Liu, Xin; Bushnell, David A.; Wang, Dong
- Science, Vol. 327, Issue 5962
Bacterial Sigma Factors: A Historical, Structural, and Genomic Perspective
journal, September 2014
- Feklístov, Andrey; Sharon, Brian D.; Darst, Seth A.
- Annual Review of Microbiology, Vol. 68, Issue 1
Transcription initiation complex structures elucidate DNA opening
journal, May 2016
- Plaschka, C.; Hantsche, M.; Dienemann, C.
- Nature, Vol. 533, Issue 7603
Structural Basis of Transcription Initiation: RNA Polymerase Holoenzyme at 4 Å Resolution
journal, May 2002
- Murakami, Katsuhiko S.; Masuda, Shoko; Darst, Seth A.
- Science, Vol. 296, Issue 5571, p. 1280-1284
Growth phase-dependent control of transcription start site selection and gene expression by nanoRNAs
journal, July 2012
- Vvedenskaya, I. O.; Sharp, J. S.; Goldman, S. R.
- Genes & Development, Vol. 26, Issue 13
Region 3.2 of the σ Subunit Contributes to the Binding of the 3′-Initiating Nucleotide in the RNA Polymerase Active Center and Facilitates Promoter Clearance during Initiation
journal, May 2006
- Kulbachinskiy, Andrey; Mustaev, Arkady
- Journal of Biological Chemistry, Vol. 281, Issue 27
RNA Polymerase Accommodates a Pause RNA Hairpin by Global Conformational Rearrangements that Prolong Pausing
journal, March 2018
- Kang, Jin Young; Mishanina, Tatiana V.; Bellecourt, Michael J.
- Molecular Cell, Vol. 69, Issue 5
Structures of E . coli σ S -transcription initiation complexes provide new insights into polymerase mechanism
journal, March 2016
- Liu, Bin; Zuo, Yuhong; Steitz, Thomas A.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 15
Structure of a bacterial RNA polymerase holoenzyme open promoter complex
journal, September 2015
- Bae, Brian; Feklistov, Andrey; Lass-Napiorkowska, Agnieszka
- eLife, Vol. 4
Conserved Region 3 of Escherichia coli σ 70 Is Implicated in the Process of Abortive Transcription
journal, August 1996
- Hernandez, V. James; Hsu, Lilian M.; Cashel, Michael
- Journal of Biological Chemistry, Vol. 271, Issue 31
X-ray Crystal Structure of Escherichia coli RNA Polymerase σ 70 Holoenzyme
journal, February 2013
- Murakami, Katsuhiko S.
- Journal of Biological Chemistry, Vol. 288, Issue 13
Backtracked and paused transcription initiation intermediate of Escherichia coli RNA polymerase
journal, October 2016
- Lerner, Eitan; Chung, SangYoon; Allen, Benjamin L.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 43
Structures and mechanism of transcription initiation by bacterial ECF factors
journal, May 2019
- Fang, Chengli; Li, Lingting; Shen, Liqiang
- Nucleic Acids Research, Vol. 47, Issue 13
Structural basis of ECF-σ-factor-dependent transcription initiation
journal, February 2019
- Lin, Wei; Mandal, Sukhendu; Degen, David
- Nature Communications, Vol. 10, Issue 1
Structural basis for transcription initiation by bacterial ECF σ factors
journal, March 2019
- Li, Lingting; Fang, Chengli; Zhuang, Ningning
- Nature Communications, Vol. 10, Issue 1
Pausing controls branching between productive and non-productive pathways during initial transcription in bacteria
journal, April 2018
- Dulin, David; Bauer, David L. V.; Malinen, Anssi M.
- Nature Communications, Vol. 9, Issue 1
Structural Insights into the Eukaryotic Transcription Initiation Machinery
journal, May 2017
- Nogales, Eva; Louder, Robert K.; He, Yuan
- Annual Review of Biophysics, Vol. 46, Issue 1
Distinct functions of the RNA polymerase σ subunit region 3.2 in RNA priming and promoter escape
journal, January 2014
- Pupov, Danil; Kuzin, Ivan; Bass, Irina
- Nucleic Acids Research, Vol. 42, Issue 7
Transcription Factor B Contacts Promoter DNA Near the Transcription Start Site of the Archaeal Transcription Initiation Complex
journal, November 2003
- Renfrow, Matthew B.; Naryshkin, Nikolai; Lewis, L. Michelle
- Journal of Biological Chemistry, Vol. 279, Issue 4
Near-atomic resolution visualization of human transcription promoter opening
journal, May 2017
- He, Yuan; Yan, Chunli; Fang, Jie
- Acta Crystallographica Section A Foundations and Advances, Vol. 73, Issue a1
Bacterial Sigma Factors: A Historical, Structural, and Genomic Perspective
journal, September 2014
- Feklístov, Andrey; Sharon, Brian D.; Darst, Seth A.
- Annual Review of Microbiology, Vol. 68, Issue 1