Structures of E. coli σS-transcription initiation complexes provide new insights into polymerase mechanism

Liu, Bin; Zuo, Yuhong; Steitz, Thomas A.

doi:10.1073/pnas.1520555113

Title: Structures of E. coli σ^S-transcription initiation complexes provide new insights into polymerase mechanism

Abstract

In bacteria, multiple σ factors compete to associate with the RNA polymerase (RNAP) core enzyme to form a holoenzyme that is required for promoter recognition. During transcription initiation RNAP remains associated with the upstream promoter DNA via sequence-specific interactions between the σ factor and the promoter DNA while moving downstream for RNA synthesis. As RNA polymerase repetitively adds nucleotides to the 3'-end of the RNA, a pyrophosphate ion is generated after each nucleotide incorporation. It is currently unknown how the release of pyrophosphate affects transcription. Here we report the crystal structures of E. coli transcription initiation complexes (TICs) containing the stress-responsive σS factor, a de novo synthesized RNA oligonucleotide, and a complete transcription bubble (σ^S-TIC) at about 3.9-Å resolution. The structures show the 3D topology of the σ^S factor and how it recognizes the promoter DNA, including likely specific interactions with the template-strand residues of the –10 element. In addition, σ^S-TIC structures display a highly stressed pretranslocated initiation complex that traps a pyrophosphate at the active site that remains closed. The position of the pyrophosphate and the unusual phosphodiester linkage between the two terminal RNA residues suggest an unfinished nucleotide-addition reaction that is likely at equilibrium between nucleotide addition andmore »« less

Authors:

Liu, Bin ^[1]; Zuo, Yuhong ^[1]; Steitz, Thomas A. ^[1]

Yale Univ., New Haven, CT (United States)

Publication Date:: Mon Mar 28 00:00:00 EDT 2016

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Org.:: National Institutes of Health (NIH)

OSTI Identifier:: 1248383

Grant/Contract Number:: GM22778

Resource Type:: Accepted Manuscript

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Volume: 113; Journal Issue: 15; Journal ID: ISSN 0027-8424

Publisher:: National Academy of Sciences

Country of Publication:: United States

Language:: ENGLISH

Subject:: 59 BASIC BIOLOGICAL SCIENCES; transcription initiation; RNA polymerase; σS factor; promoter recognition; pyrophosphate release

Citation Formats


                    Liu, Bin, Zuo, Yuhong, and Steitz, Thomas A. Structures of E. coli σS-transcription initiation complexes provide new insights into polymerase mechanism.  United States: N. p., 2016. 
Web.  doi:10.1073/pnas.1520555113.

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                    Liu, Bin, Zuo, Yuhong, & Steitz, Thomas A. Structures of E. coli σS-transcription initiation complexes provide new insights into polymerase mechanism.  United States.  https://doi.org/10.1073/pnas.1520555113

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                    Liu, Bin, Zuo, Yuhong, and Steitz, Thomas A. Mon .  
"Structures of E. coli σS-transcription initiation complexes provide new insights into polymerase mechanism".  United States.  https://doi.org/10.1073/pnas.1520555113.  https://www.osti.gov/servlets/purl/1248383.

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@article{osti_1248383,

  title        = {Structures of E. coli σS-transcription initiation complexes provide new insights into polymerase mechanism},

  author       = {Liu, Bin and Zuo, Yuhong and Steitz, Thomas A.},

  abstractNote = {In bacteria, multiple σ factors compete to associate with the RNA polymerase (RNAP) core enzyme to form a holoenzyme that is required for promoter recognition. During transcription initiation RNAP remains associated with the upstream promoter DNA via sequence-specific interactions between the σ factor and the promoter DNA while moving downstream for RNA synthesis. As RNA polymerase repetitively adds nucleotides to the 3'-end of the RNA, a pyrophosphate ion is generated after each nucleotide incorporation. It is currently unknown how the release of pyrophosphate affects transcription. Here we report the crystal structures of E. coli transcription initiation complexes (TICs) containing the stress-responsive σS factor, a de novo synthesized RNA oligonucleotide, and a complete transcription bubble (σS-TIC) at about 3.9-Å resolution. The structures show the 3D topology of the σS factor and how it recognizes the promoter DNA, including likely specific interactions with the template-strand residues of the –10 element. In addition, σS-TIC structures display a highly stressed pretranslocated initiation complex that traps a pyrophosphate at the active site that remains closed. The position of the pyrophosphate and the unusual phosphodiester linkage between the two terminal RNA residues suggest an unfinished nucleotide-addition reaction that is likely at equilibrium between nucleotide addition and pyrophosphorolysis. Although these σS-TIC crystals are enzymatically active, they are slow in nucleotide addition, as suggested by an NTP soaking experiment. As a result, pyrophosphate release completes the nucleotide addition reaction and is associated with extensive conformational changes around the secondary channel but causes neither active site opening nor transcript translocation.},

  doi          = {10.1073/pnas.1520555113},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 15,

  volume       = 113,

  place        = {United States},

  year         = {Mon Mar 28 00:00:00 EDT 2016},

  month        = {Mon Mar 28 00:00:00 EDT 2016}

}

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DOI: 10.1073/pnas.1920747117

Resonance assignments of sigma factor S binding protein Crl from Escherichia coli
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Zhao, Siyu; Zhang, Kaining; Jiang, Songzi
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Active site closure stabilizes the backtracked state of RNA polymerase
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Turtola, Matti; Mäkinen, Janne J.; Belogurov, Georgiy A.
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Structural insights into NusG regulating transcription elongation
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Liu, Bin; Steitz, Thomas A.
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Qiu, Chenxi; Erinne, Olivia C.; Dave, Jui M.
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The bacterial σ factors confer promoter specificity to the RNA polymerase (RNAP). One alternative σ factor, σ^N, is unique in its structure and functional mechanism, forming transcriptionally inactive promoter complexes that require activation by specialized AAA⁺ATPases. We report a 3.4-Å resolution X-ray crystal structure of a σ^Nfragment in complex with its cognate promoter DNA, revealing the molecular details of promoter recognition by σ^N. The structure allowed us to build and refine an improved σ^N-holoenzyme model based on previously published 3.8-Å resolution X-ray data. The improved σ^N-holoenzyme model reveals a conserved interdomain interface within σ^Nthat, when disrupted by mutations, leads tomore »« less
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Title: Structures of E. coli σS-transcription initiation complexes provide new insights into polymerase mechanism

Abstract

Citation Formats

Structural basis of initial RNA polymerase II transcription: Initial RNA Pol II transcription journal, November 2011

Overview of the CCP 4 suite and current developments journal, March 2011

Complete Structural Model of Escherichia coli RNA Polymerase from a Hybrid Approach journal, September 2010

Key features of S required for specific recognition by Crl, a transcription factor promoting assembly of RNA polymerase holoenzyme journal, September 2013

Active site opening and closure control translocation of multisubunit RNA polymerase journal, May 2012

Bacterial RNA polymerases: the wholo story journal, February 2003

Processive pyrophosphorolysis of RNA by Escherichia coli RNA polymerase journal, January 1982

Structural Basis of Transcription: An RNA Polymerase II Elongation Complex at 3.3 A Resolution journal, April 2001

Competition among seven Escherichia coli sigma subunits: relative binding affinities to the core RNA polymerase journal, September 2000

Structure and function of the initially transcribing RNA polymerase II–TFIIB complex journal, November 2012

Trigger loop folding determines transcription rate of Escherichia coli’s RNA polymerase journal, December 2014

Crystal Structures of the E. coli Transcription Initiation Complexes with a Complete Bubble journal, May 2015

Structures of the RNA polymerase- 54 reveal new and conserved regulatory strategies journal, August 2015

Structural Basis of Transcription: Role of the Trigger Loop in Substrate Specificity and Catalysis journal, December 2006

Structural Basis of Transcription Initiation journal, October 2012

Complete RNA Polymerase II Elongation Complex Structure and Its Interactions with NTP and TFIIS journal, December 2004

Structural Basis for Promoter −10 Element Recognition by the Bacterial RNA Polymerase σ Subunit journal, December 2011

Rapid Pyrophosphate Release from Transcriptional Elongation Complexes Appears to be Coupled to a Nucleotide-Induced Conformational Change in E. coli Core Polymerase journal, October 2011

Proteolysis of σS (RpoS) and the general stress response in Escherichia coli journal, November 2009

Trigger-helix folding pathway and SI3 mediate catalysis and hairpin-stabilized pausing by Escherichia coli RNA polymerase journal, October 2014

What makes an Escherichia coli promoter σS dependent? Role of the −13/−14 nucleotide promoter positions and region 2.5 of σS: Region 2.5 of σS and promoter recognition journal, March 2001

Coot model-building tools for molecular graphics journal, November 2004

The RpoS-Mediated General Stress Response in Escherichia coli journal, October 2011

Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein journal, December 2010

Structure of a bacterial RNA polymerase holoenzyme open promoter complex journal, September 2015

CarD uses a minor groove wedge mechanism to stabilize the RNA polymerase open promoter complex journal, September 2015

Structural basis for transcription elongation by bacterial RNA polymerase journal, June 2007

Structural basis for substrate loading in bacterial RNA polymerase journal, June 2007

Promoter recognition and discrimination by EsigmaS RNA polymerase journal, November 2001

Torpedo Nuclease Rat1 Is Insufficient to Terminate RNA Polymerase II in Vitro journal, June 2009

Structural Basis of Transcription: Separation of RNA from DNA by RNA Polymerase II journal, February 2004

CPD damage recognition by transcribing RNA polymerase II journal, August 2007

[20] Processing of X-ray diffraction data collected in oscillation mode book, January 1997

Multiple Sigma Subunits and the Partitioning of Bacterial Transcription Space journal, October 2003

Crl stimulates RpoS activity during stationary phase journal, September 1998

Crystal Structure of a σ70 Subunit Fragment from E. coli RNA Polymerase journal, October 1996

Structural Basis of Transcription: Mismatch-Specific Fidelity Mechanisms and Paused RNA Polymerase II with Frayed RNA journal, June 2009

Structural Basis of Transcription: Backtracked RNA Polymerase II at 3.4 Angstrom Resolution journal, May 2009

CPD Damage Recognition by Transcribing RNA Polymerase II journal, February 2007

Mechanism of transcriptional stalling at cisplatin-damaged DNA journal, November 2007

Structure and Function of Lineage-specific Sequence Insertions in the Bacterial RNA Polymerase β′ Subunit journal, October 2005

Structural Basis of Transcription journal, December 2004

Factor Stimulating Transcription by RNA Polymerase journal, January 1969

Multisubunit RNA polymerases journal, February 2002

Abortive Initiation and Productive Initiation by RNA Polymerase Involve DNA Scrunching journal, November 2006

Initial Transcription by RNA Polymerase Proceeds Through a DNA-Scrunching Mechanism journal, November 2006

Structures of RNA polymerase II complexes with Bye1, a chromatin-binding PHF3/DIDO homologue text, January 2013

Structural Basis of Transcription Initiation by Bacterial RNA Polymerase Holoenzyme journal, June 2014

Structural basis for transcription reactivation by RapA journal, February 2015

Molecular basis of RNA-dependent RNA polymerase II activity journal, November 2007

Mechanism of Translesion Transcription by RNA Polymerase II and Its Role in Cellular Resistance to DNA Damage journal, April 2012

GE23077 binds to the RNA polymerase ‘i’ and ‘i+1’ sites and prevents the binding of initiating nucleotides journal, April 2014

A stressed intermediate in the formation of stably initiated RNA chains at the Escherichia coli lac UV5 promoter journal, January 1987

Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution journal, May 2002

Structures of RNA polymerase II complexes with Bye1, a chromatin-binding PHF3/DIDO homologue journal, September 2013

Direct Detection of Abortive RNA Transcripts in Vivo journal, May 2009

Initiation Complex Structure and Promoter Proofreading journal, July 2011

Crystal Structure of a Transcribing RNA Polymerase II Complex Reveals a Complete Transcription Bubble journal, July 2015

Structural basis of transcription inhibition by α-amanitin and implications for RNA polymerase II translocation journal, June 2008

REFMAC 5 for the refinement of macromolecular crystal structures journal, March 2011

Sequences in the -35 region of Escherichia coli rpoS-dependent genes promote transcription by E sigma S. journal, January 1996

Mechanism of Bacterial Transcription Initiation: RNA Polymerase - Promoter Binding, Isomerization to Initiation-Competent Open Complexes, and Initiation of RNA Synthesis journal, October 2011

Overview of the CCP4 suite and current developments. text, January 2011

Structural Basis of Transcriptional Pausing in Bacteria journal, January 2013

Structural Basis of Transcription journal, November 2004

X-ray structure and mechanism of RNA polymerase II stalled at an antineoplastic monofunctional platinum-DNA adduct journal, May 2010

Crl Facilitates RNA Polymerase Holoenzyme Formation journal, September 2006

A Central Role of the RNA Polymerase Trigger Loop in Active-Site Rearrangement during Transcriptional Pausing journal, August 2007

Structural basis of RNA polymerase II backtracking, arrest and reactivation journal, February 2011

Phaser crystallographic software journal, July 2007

The Structural Mechanism of Translocation and Helicase Activity in T7 RNA Polymerase journal, February 2004

A noncycling activity assay for the omega subunit of Escherichia coli RNA polymerase. journal, August 1979

The Role of Deoxyribonucleic Acid in Ribonucleic Acid Synthesis journal, November 1967

High-resolution phenotypic landscape of the RNA Polymerase II trigger loop journal, August 2016

Structural basis for transcription activation by Crl through tethering of σ S and RNA polymerase journal, August 2019

Structural basis for transcription activation by Crl through tethering of σ S and RNA polymerase journal, September 2019

Pausing controls branching between productive and non-productive pathways during initial transcription in bacteria journal, April 2018

Title: Structures of E. coli σ^S-transcription initiation complexes provide new insights into polymerase mechanism

Structural basis of initial RNA polymerase II transcription: Initial RNA Pol II transcription
journal, November 2011

Overview of the CCP 4 suite and current developments
journal, March 2011

Complete Structural Model of Escherichia coli RNA Polymerase from a Hybrid Approach
journal, September 2010

Key features of S required for specific recognition by Crl, a transcription factor promoting assembly of RNA polymerase holoenzyme
journal, September 2013

Active site opening and closure control translocation of multisubunit RNA polymerase
journal, May 2012

Bacterial RNA polymerases: the wholo story
journal, February 2003

Processive pyrophosphorolysis of RNA by Escherichia coli RNA polymerase
journal, January 1982

Structural Basis of Transcription: An RNA Polymerase II Elongation Complex at 3.3 A Resolution
journal, April 2001

Competition among seven Escherichia coli sigma subunits: relative binding affinities to the core RNA polymerase
journal, September 2000

Structure and function of the initially transcribing RNA polymerase II–TFIIB complex
journal, November 2012

Trigger loop folding determines transcription rate of Escherichia coli’s RNA polymerase
journal, December 2014

Crystal Structures of the E. coli Transcription Initiation Complexes with a Complete Bubble
journal, May 2015

Structures of the RNA polymerase- 54 reveal new and conserved regulatory strategies
journal, August 2015

Structural Basis of Transcription: Role of the Trigger Loop in Substrate Specificity and Catalysis
journal, December 2006

Structural Basis of Transcription Initiation
journal, October 2012

Complete RNA Polymerase II Elongation Complex Structure and Its Interactions with NTP and TFIIS
journal, December 2004

Structural Basis for Promoter −10 Element Recognition by the Bacterial RNA Polymerase σ Subunit
journal, December 2011

Rapid Pyrophosphate Release from Transcriptional Elongation Complexes Appears to be Coupled to a Nucleotide-Induced Conformational Change in E. coli Core Polymerase
journal, October 2011

Proteolysis of σS (RpoS) and the general stress response in Escherichia coli
journal, November 2009

Trigger-helix folding pathway and SI3 mediate catalysis and hairpin-stabilized pausing by Escherichia coli RNA polymerase
journal, October 2014

What makes an Escherichia coli promoter σS dependent? Role of the −13/−14 nucleotide promoter positions and region 2.5 of σS: Region 2.5 of σS and promoter recognition
journal, March 2001

Coot model-building tools for molecular graphics
journal, November 2004

The RpoS-Mediated General Stress Response in Escherichia coli
journal, October 2011

Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein
journal, December 2010

Structure of a bacterial RNA polymerase holoenzyme open promoter complex
journal, September 2015

CarD uses a minor groove wedge mechanism to stabilize the RNA polymerase open promoter complex
journal, September 2015

Structural basis for transcription elongation by bacterial RNA polymerase
journal, June 2007

Structural basis for substrate loading in bacterial RNA polymerase
journal, June 2007

Promoter recognition and discrimination by EsigmaS RNA polymerase
journal, November 2001

Torpedo Nuclease Rat1 Is Insufficient to Terminate RNA Polymerase II in Vitro
journal, June 2009

Structural Basis of Transcription: Separation of RNA from DNA by RNA Polymerase II
journal, February 2004

CPD damage recognition by transcribing RNA polymerase II
journal, August 2007

[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997

Multiple Sigma Subunits and the Partitioning of Bacterial Transcription Space
journal, October 2003

Crl stimulates RpoS activity during stationary phase
journal, September 1998

Crystal Structure of a σ70 Subunit Fragment from E. coli RNA Polymerase
journal, October 1996

Structural Basis of Transcription: Mismatch-Specific Fidelity Mechanisms and Paused RNA Polymerase II with Frayed RNA
journal, June 2009

Structural Basis of Transcription: Backtracked RNA Polymerase II at 3.4 Angstrom Resolution
journal, May 2009

CPD Damage Recognition by Transcribing RNA Polymerase II
journal, February 2007

Mechanism of transcriptional stalling at cisplatin-damaged DNA
journal, November 2007

Structure and Function of Lineage-specific Sequence Insertions in the Bacterial RNA Polymerase β′ Subunit
journal, October 2005

Structural Basis of Transcription
journal, December 2004

Factor Stimulating Transcription by RNA Polymerase
journal, January 1969

Multisubunit RNA polymerases
journal, February 2002

Abortive Initiation and Productive Initiation by RNA Polymerase Involve DNA Scrunching
journal, November 2006

Initial Transcription by RNA Polymerase Proceeds Through a DNA-Scrunching Mechanism
journal, November 2006

Structures of RNA polymerase II complexes with Bye1, a chromatin-binding PHF3/DIDO homologue
text, January 2013

Structural Basis of Transcription Initiation by Bacterial RNA Polymerase Holoenzyme
journal, June 2014

Structural basis for transcription reactivation by RapA
journal, February 2015

Molecular basis of RNA-dependent RNA polymerase II activity
journal, November 2007

Mechanism of Translesion Transcription by RNA Polymerase II and Its Role in Cellular Resistance to DNA Damage
journal, April 2012

GE23077 binds to the RNA polymerase ‘i’ and ‘i+1’ sites and prevents the binding of initiating nucleotides
journal, April 2014

A stressed intermediate in the formation of stably initiated RNA chains at the Escherichia coli lac UV5 promoter
journal, January 1987

Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution
journal, May 2002

Structures of RNA polymerase II complexes with Bye1, a chromatin-binding PHF3/DIDO homologue
journal, September 2013

Direct Detection of Abortive RNA Transcripts in Vivo
journal, May 2009

Initiation Complex Structure and Promoter Proofreading
journal, July 2011

Crystal Structure of a Transcribing RNA Polymerase II Complex Reveals a Complete Transcription Bubble
journal, July 2015

Structural basis of transcription inhibition by α-amanitin and implications for RNA polymerase II translocation
journal, June 2008

REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011

Sequences in the -35 region of Escherichia coli rpoS-dependent genes promote transcription by E sigma S.
journal, January 1996

Mechanism of Bacterial Transcription Initiation: RNA Polymerase - Promoter Binding, Isomerization to Initiation-Competent Open Complexes, and Initiation of RNA Synthesis
journal, October 2011

Overview of the CCP4 suite and current developments.
text, January 2011

Structural Basis of Transcriptional Pausing in Bacteria
journal, January 2013

Structural Basis of Transcription
journal, November 2004

X-ray structure and mechanism of RNA polymerase II stalled at an antineoplastic monofunctional platinum-DNA adduct
journal, May 2010

Crl Facilitates RNA Polymerase Holoenzyme Formation
journal, September 2006

A Central Role of the RNA Polymerase Trigger Loop in Active-Site Rearrangement during Transcriptional Pausing
journal, August 2007

Structural basis of RNA polymerase II backtracking, arrest and reactivation
journal, February 2011

Phaser crystallographic software
journal, July 2007

The Structural Mechanism of Translocation and Helicase Activity in T7 RNA Polymerase
journal, February 2004

A noncycling activity assay for the omega subunit of Escherichia coli RNA polymerase.
journal, August 1979

The Role of Deoxyribonucleic Acid in Ribonucleic Acid Synthesis
journal, November 1967

High-resolution phenotypic landscape of the RNA Polymerase II trigger loop
journal, August 2016

Structural basis for transcription activation by Crl through tethering of σ ^S and RNA polymerase
journal, August 2019

Structural basis for transcription activation by Crl through tethering of σ ^S and RNA polymerase
journal, September 2019

Pausing controls branching between productive and non-productive pathways during initial transcription in bacteria
journal, April 2018

The dormancy‐specific regulator, SutA, is intrinsically disordered and modulates transcription initiation in Pseudomonas aeruginosa
journal, July 2019

Structural basis of Q-dependent antitermination
journal, August 2019