Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Mechanistic insights from structure of Mycobacterium smegmatis topoisomerase I with ssDNA bound to both N- and C-terminal domains

Journal Article · · Nucleic Acids Research
DOI:https://doi.org/10.1093/nar/gkaa201· OSTI ID:1607798
 [1];  [2];  [3];  [1];  [1]
  1. Department of Chemistry and Biochemistry, Florida International University, Miami, FL 33199, USA, Biomolecular Sciences Institute, Florida International University, 11200 SW 8 St, Miami, FL 33199, USA
  2. Structural Biology Center, X-ray Science Division, Advanced Photon Source, Argonne National Laboratory, 9700 S. Cass Avenue, Lemont, IL 60439, USA
  3. X-ray Science Division, Advanced Photon Source, Argonne National Laboratory, 9700 S. Cass Avenue, Lemont, IL 60439, USA
Abstract

Type IA topoisomerases interact with G-strand and T-strand ssDNA to regulate DNA topology. However, simultaneous binding of two ssDNA segments to a type IA topoisomerase has not been observed previously. We report here the crystal structure of a type IA topoisomerase with ssDNA segments bound in opposite polarity to the N- and C-terminal domains. Titration of small ssDNA oligonucleotides to Mycobacterium smegmatis topoisomerase I with progressive C-terminal deletions showed that the C-terminal region has higher affinity for ssDNA than the N-terminal active site. This allows the C-terminal domains to capture one strand of underwound negatively supercoiled DNA substrate first and position the N-terminal domains to bind and cleave the opposite strand in the relaxation reaction. Efficiency of negative supercoiling relaxation increases with the number of domains that bind ssDNA primarily with conserved aromatic residues and possibly with assistance from polar/basic residues. A comparison of bacterial topoisomerase I structures showed that a conserved transesterification unit (N-terminal toroid structure) for cutting and rejoining of a ssDNA strand can be combined with two different types of C-terminal ssDNA binding domains to form diverse bacterial topoisomerase I enzymes that are highly efficient in their physiological role of preventing excess negative supercoiling in the genome.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
Bill and Melinda Gates Foundation; Federal Ministry of Education and Research (Germany); Global Alliance for TB Drug Development (TB Alliance); National Institutes of Health (NIH); USDOE; USDOE Office of Science (SC), Office of Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1607798
Alternate ID(s):
OSTI ID: 1756927
Journal Information:
Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 8 Vol. 48; ISSN 0305-1048
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (46)

The carboxyl terminal domain ofEscherichia coli DNA topoisomerase I confers higher affinity to DNA journal January 1989
R-loop-dependent hypernegative supercoiling in Escherichia coli topA mutants preferentially occurs at low temperatures and correlates with growth inhibition journal November 1999
C-terminal domains of Escherichia coli topoisomerase I belong to the zinc-ribbon superfamily journal June 2000
Type IA DNA Topoisomerases: A Universal Core and Multiple Activities book November 2017
Enzymatic Assembly of Overlapping DNA Fragments book May 2011
Determination of Domain Structure of Proteins from X-Ray Solution Scattering journal June 2001
Restoring Low Resolution Structure of Biological Macromolecules from Solution Scattering Using Simulated Annealing journal June 1999
Escherichia coli DNA topoisomerase I is a zinc metalloprotein with three repetitive zinc-binding domains. journal November 1988
Covalent bonds between protein and DNA. Formation of phosphotyrosine linkage between certain DNA topoisomerases and DNA. journal June 1980
Topoisomerase I of Helicobacter pylori: juxtaposition with a flagellin gene (flaB) and functional requirement of a fourth zinc finger motif journal March 1998
Type IA topoisomerases: A simple puzzle? journal April 2007
DNA topoisomerase I and DNA gyrase as targets for TB therapy journal March 2017
Crystal Structure of Full Length Topoisomerase I from Thermotoga maritima journal May 2006
Insights from the Structure of Mycobacterium tuberculosis Topoisomerase I with a Novel Protein Fold journal January 2016
Genetic and chemical validation identifies Mycobacterium tuberculosis topoisomerase I as an attractive anti-tubercular target journal September 2015
Solution structure of the C-terminal single-stranded DNA-binding domain of Escherichia coli topoisomerase I journal June 1995
Structural diversity of supercoiled DNA journal October 2015
All tangled up: how cells direct, manage and exploit topoisomerase function journal November 2011
Cellular roles of DNA topoisomerases: a molecular perspective journal June 2002
Topoisomerase 3β interacts with RNAi machinery to promote heterochromatin formation and transcriptional silencing in Drosophila journal November 2018
Crystal structure of a covalent intermediate in DNA cleavage and rejoining by Escherichia coli DNA topoisomerase I journal April 2011
DNA Topoisomerase I from Mycobacterium smegmatis: AN ENZYME WITH DISTINCT FEATURES journal May 1998
On the Molecular Basis of the Thermal Sensitivity of an Escherichia coli topA Mutant journal November 2001
The Strictly Conserved Arg-321 Residue in the Active Site of Escherichia coli Topoisomerase I Plays a Critical Role in DNA Rejoining journal April 2011
Type IA topoisomerases can be “magicians” for both DNA and RNA in all domains of life journal May 2017
Phylogenomics of DNA topoisomerases: their origin and putative roles in the emergence of modern organisms journal February 2009
Residues of E. coli topoisomerase I conserved for interaction with a specific cytosine base to facilitate DNA cleavage journal July 2012
Carboxyl terminal domain basic amino acids of mycobacterial topoisomerase I bind DNA to promote strand passage journal June 2013
Structural basis for suppression of hypernegative DNA supercoiling by E. coli topoisomerase I journal October 2015
RNA topoisomerase is prevalent in all domains of life and associates with polyribosomes in animals journal June 2016
C-terminal lysine repeats in Streptomyces topoisomerase I stabilize the enzyme–DNA complex and confer high enzyme processivity journal September 2017
Investigating mycobacterial topoisomerase I mechanism from the analysis of metal and DNA substrate interactions at the active site journal June 2018
Phase Imaging and Nanoscale Currents in Phase Objects Imaged with Fast Electrons journal July 2003
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering journal January 2009
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes journal July 2006
Molecular replacement with MOLREP journal December 2009
Features and development of Coot journal March 2010
Towards automated crystallographic structure refinement with phenix.refine journal March 2012
The Structural Biology Center 19ID undulator beamline: facility specifications and protein crystallographic results journal December 2005
SOS Induction by Stabilized Topoisomerase IA Cleavage Complex Occurs via the RecBCD Pathway journal February 2008
Structure and mechanism of action of type IA DNA topoisomerases journal December 2009
New Mechanistic and Functional Insights into DNA Topoisomerases journal June 2013
DNA Topoisomerases journal June 1996
Analysis of DNA relaxation and cleavage activities of recombinant Mycobacterium tuberculosis DNA topoisomerase I from a new expression and purification protocol journal January 2009
The DNA relaxation activity and covalent complex accumulation of Mycobacterium tuberculosis topoisomerase I can be assayed in Escherichia coli: application for identification of potential FRET-dye labeling sites journal January 2010
Segmentally Variable Genes:A New Perspective on Adaptation journal April 2004

Similar Records

Structural basis for suppression of hypernegative DNA supercoiling by E. coli topoisomerase I
Journal Article · Mon Oct 19 20:00:00 EDT 2015 · Nucleic Acids Research · OSTI ID:1261152

Microbial Type IA Topoisomerase C-Terminal Domain Sequence Motifs, Distribution and Combination
Journal Article · Thu Aug 04 20:00:00 EDT 2022 · International Journal of Molecular Sciences (Online) · OSTI ID:1880977

Related Subjects