Structures of the Catalytic Domain of Bacterial Primase DnaG in Complexes with DNA Provide Insight into Key Priming Events

Hou, Caixia; Biswas, Tapan; Tsodikov, Oleg V.

doi:10.1021/acs.biochem.8b00036

Title: Structures of the Catalytic Domain of Bacterial Primase DnaG in Complexes with DNA Provide Insight into Key Priming Events

Abstract

Bacterial primase DnaG is an essential nucleic acid polymerase that generates primers for replication of chromosomal DNA. The mechanism of DnaG remains unclear due to the paucity of structural information on DnaG in complexes with other replisome components. Furthermore we report the first crystal structures of noncovalent DnaG–DNA complexes, obtained with the RNA polymerase domain of Mycobacterium tuberculosis DnaG and various DNA ligands. One structure, obtained with ds DNA, reveals interactions with DnaG as it slides on ds DNA and suggests how DnaG binds template for primer synthesis. In another structure, DNA in the active site of DnaG mimics the primer, providing insight into mechanisms for the nucleotide transfer and DNA translocation. In conjunction with the recent cryo-EM structure of the bacteriophage T7 replisome, this study yields a model for primer elongation and hand-off to DNA polymerase.

Authors:

Hou, Caixia ^[1]; Biswas, Tapan ^[2];

^[1]

Univ. of Kentucky, Lexington, KY (United States)
Univ. of California, San Diego, La Jolla, CA (United States)

Publication Date:: Tue Mar 20 00:00:00 EDT 2018

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

Sponsoring Org.:: SER-CAT

OSTI Identifier:: 1438848

Resource Type:: Accepted Manuscript

Journal Name:: Biochemistry

Additional Journal Information:: Journal Volume: 57; Journal Issue: 14; Journal ID: ISSN 0006-2960

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: ENGLISH

Subject:: 59 BASIC BIOLOGICAL SCIENCES; anions; peptides and proteins; genetics; crystal structure; ions; DNA replication; replisome; DNA binding; tuberculosis

Citation Formats


                    Hou, Caixia, Biswas, Tapan, and Tsodikov, Oleg V. Structures of the Catalytic Domain of Bacterial Primase DnaG in Complexes with DNA Provide Insight into Key Priming Events.  United States: N. p., 2018. 
Web.  doi:10.1021/acs.biochem.8b00036.

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                    Hou, Caixia, Biswas, Tapan, & Tsodikov, Oleg V. Structures of the Catalytic Domain of Bacterial Primase DnaG in Complexes with DNA Provide Insight into Key Priming Events.  United States.  https://doi.org/10.1021/acs.biochem.8b00036

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                    Hou, Caixia, Biswas, Tapan, and Tsodikov, Oleg V. Tue .  
"Structures of the Catalytic Domain of Bacterial Primase DnaG in Complexes with DNA Provide Insight into Key Priming Events".  United States.  https://doi.org/10.1021/acs.biochem.8b00036.  https://www.osti.gov/servlets/purl/1438848.

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@article{osti_1438848,

  title        = {Structures of the Catalytic Domain of Bacterial Primase DnaG in Complexes with DNA Provide Insight into Key Priming Events},

  author       = {Hou, Caixia and Biswas, Tapan and Tsodikov, Oleg V.},

  abstractNote = {Bacterial primase DnaG is an essential nucleic acid polymerase that generates primers for replication of chromosomal DNA. The mechanism of DnaG remains unclear due to the paucity of structural information on DnaG in complexes with other replisome components. Furthermore we report the first crystal structures of noncovalent DnaG–DNA complexes, obtained with the RNA polymerase domain of Mycobacterium tuberculosis DnaG and various DNA ligands. One structure, obtained with ds DNA, reveals interactions with DnaG as it slides on ds DNA and suggests how DnaG binds template for primer synthesis. In another structure, DNA in the active site of DnaG mimics the primer, providing insight into mechanisms for the nucleotide transfer and DNA translocation. In conjunction with the recent cryo-EM structure of the bacteriophage T7 replisome, this study yields a model for primer elongation and hand-off to DNA polymerase.},

  doi          = {10.1021/acs.biochem.8b00036},

  journal      = {Biochemistry},

  number       = 14,

  volume       = 57,

  place        = {United States},

  year         = {Tue Mar 20 00:00:00 EDT 2018},

  month        = {Tue Mar 20 00:00:00 EDT 2018}

}

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https://doi.org/10.1021/acs.biochem.8b00036

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Works referencing / citing this record:

A structural view of bacterial DNA replication
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Protein Science, Vol. 28, Issue 6
DOI: 10.1002/pro.3615

DnaG Primase—A Target for the Development of Novel Antibacterial Agents
journal, August 2018

Ilic, Stefan; Cohen, Shira; Singh, Meenakshi
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Title: Structures of the Catalytic Domain of Bacterial Primase DnaG in Complexes with DNA Provide Insight into Key Priming Events

Abstract

Citation Formats

Structure of the zinc-binding domain of Bacillus stearothermophilus DNA primase journal, March 2000

Crosstalk between Primase Subunits Can Act to Regulate Primer Synthesis in trans journal, November 2005

Structure of the RNA Polymerase Domain of E. coli Primase journal, March 2000

A TOPRIM domain in the crystal structure of the catalytic core of Escherichia coli primase confirms a structural link to DNA topoisomerases 1 1Edited by P. E. Wright journal, July 2000

Binding Mechanism of Metal⋅NTP Substrates and Stringent-Response Alarmones to Bacterial DnaG-Type Primases journal, September 2012

Bacterial DNA replication enzymes as targets for antibacterial drug discovery journal, February 2012

Small molecule inhibitors of E. coli primase, a novel bacterial target journal, May 2007

Discovery of Inhibitors of Bacillus anthracis Primase DnaG journal, September 2013

A novel non-radioactive primase–pyrophosphatase activity assay and its application to the discovery of inhibitors of Mycobacterium tuberculosis primase DnaG journal, December 2012

Evaluation of DNA Primase DnaG as a Potential Target for Antibiotics journal, December 2013

Antimycobacterial activity of DNA intercalator inhibitors of Mycobacterium tuberculosis primase DnaG journal, September 2014

It Seems Like Only Yesterday journal, June 2015

Identification of DNA primase inhibitors via a combined fragment-based and virtual screening journal, November 2016

Development of potential broad spectrum antimicrobials using C2-symmetric 9-fluorenone alkyl amine journal, April 2016

Architecture and Conservation of the Bacterial DNA Replication Machinery, an Underexploited Drug Target journal, March 2012

Structure of Hexameric DnaB Helicase and Its Complex with a Domain of DnaG Primase journal, October 2007

Modular Architecture of the Bacteriophage T7 Primase Couples RNA Primer Synthesis to DNA Synthesis journal, May 2003

The Crystal Structure of the Bifunctional Primase-Helicase of Bacteriophage T7 journal, November 2003

Identification of a DNA primase template tracking site redefines the geometry of primer synthesis journal, January 2008

Cryo-EM structure of the replisome reveals multiple interactions coordinating DNA synthesis journal, February 2017

Hexameric ring structure of the N-terminal domain of Mycobacterium tuberculosis DnaB helicase: Mycobacterium tuberculosis DnaB helicase journal, May 2008

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

Phaser crystallographic software journal, July 2007

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Refinement of Macromolecular Structures by the Maximum-Likelihood Method journal, May 1997

Role of Conserved Amino Acids in the Catalytic Activity of Escherichia coli Primase journal, May 2006

Crystal structure and DNA binding functions of ERCC1, a subunit of the DNA structure-specific endonuclease XPF-ERCC1 journal, August 2005

Identification of the Magnesium Ion Binding Site in the Catalytic Center of Escherichia coli Primase by Iron Cleavage journal, December 1999

Acidic Residues in the Nucleotide-binding Site of the Bacteriophage T7 DNA Primase journal, July 2005

Zinc-binding Domain of the Bacteriophage T7 DNA Primase Modulates Binding to the DNA Template journal, November 2012

Molecular interactions in the priming complex of bacteriophage T7 journal, May 2012

Mechanism of sequence-specific template binding by the DNA primase of bacteriophage T7 journal, March 2010

Primer initiation and extension by T7 DNA primase journal, April 2006

Interaction of adjacent primase domains within the hexameric gene 4 helicase-primase of bacteriophage T7 journal, September 2002

A structural view of bacterial DNA replication journal, April 2019

DnaG Primase—A Target for the Development of Novel Antibacterial Agents journal, August 2018

Structure of the zinc-binding domain of Bacillus stearothermophilus DNA primase
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Crosstalk between Primase Subunits Can Act to Regulate Primer Synthesis in trans
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Structure of the RNA Polymerase Domain of E. coli Primase
journal, March 2000

A TOPRIM domain in the crystal structure of the catalytic core of Escherichia coli primase confirms a structural link to DNA topoisomerases 1 1Edited by P. E. Wright
journal, July 2000

Binding Mechanism of Metal⋅NTP Substrates and Stringent-Response Alarmones to Bacterial DnaG-Type Primases
journal, September 2012

Bacterial DNA replication enzymes as targets for antibacterial drug discovery
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Small molecule inhibitors of E. coli primase, a novel bacterial target
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Discovery of Inhibitors of Bacillus anthracis Primase DnaG
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A novel non-radioactive primase–pyrophosphatase activity assay and its application to the discovery of inhibitors of Mycobacterium tuberculosis primase DnaG
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It Seems Like Only Yesterday
journal, June 2015

Identification of DNA primase inhibitors via a combined fragment-based and virtual screening
journal, November 2016

Development of potential broad spectrum antimicrobials using C2-symmetric 9-fluorenone alkyl amine
journal, April 2016

Architecture and Conservation of the Bacterial DNA Replication Machinery, an Underexploited Drug Target
journal, March 2012

Structure of Hexameric DnaB Helicase and Its Complex with a Domain of DnaG Primase
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Modular Architecture of the Bacteriophage T7 Primase Couples RNA Primer Synthesis to DNA Synthesis
journal, May 2003

The Crystal Structure of the Bifunctional Primase-Helicase of Bacteriophage T7
journal, November 2003

Identification of a DNA primase template tracking site redefines the geometry of primer synthesis
journal, January 2008

Cryo-EM structure of the replisome reveals multiple interactions coordinating DNA synthesis
journal, February 2017

Hexameric ring structure of the N-terminal domain of Mycobacterium tuberculosis DnaB helicase: Mycobacterium tuberculosis DnaB helicase
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[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997

Phaser crystallographic software
journal, July 2007

Features and development of Coot
journal, March 2010

Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997

Role of Conserved Amino Acids in the Catalytic Activity of Escherichia coli Primase
journal, May 2006

Crystal structure and DNA binding functions of ERCC1, a subunit of the DNA structure-specific endonuclease XPF-ERCC1
journal, August 2005

Identification of the Magnesium Ion Binding Site in the Catalytic Center of Escherichia coli Primase by Iron Cleavage
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Acidic Residues in the Nucleotide-binding Site of the Bacteriophage T7 DNA Primase
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Zinc-binding Domain of the Bacteriophage T7 DNA Primase Modulates Binding to the DNA Template
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Mechanism of sequence-specific template binding by the DNA primase of bacteriophage T7
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Interaction of adjacent primase domains within the hexameric gene 4 helicase-primase of bacteriophage T7
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