Structural basis for suppression of hypernegative DNA supercoiling by E. coli topoisomerase I

Tan, Kemin; Zhou, Qingxuan; Cheng, Bokun; Zhang, Zhongtao; Joachimiak, Andrzej; Tse-Dinh, Yuk -Ching

doi:10.1093/nar/gkv1073

Structural basis for suppression of hypernegative DNA supercoiling by E. coli topoisomerase I

Journal Article · Tue Oct 20 00:00:00 EDT 2015 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkv1073· OSTI ID:1261152

Tan, Kemin ^[1]; Zhou, Qingxuan ^[2]; Cheng, Bokun ^[3]; Zhang, Zhongtao ^[3]; Joachimiak, Andrzej ^[1]; Tse-Dinh, Yuk -Ching ^[4]

Argonne National Lab. (ANL), Argonne, IL (United States)
Florida Intl Univ., Miami, FL (United States). Dept. of Chemistry and Biochemistry
New York Medical College, Valhalla, NY (United States)
Florida Intl Univ., Miami, FL (United States). Dept. of Chemistry and Biochemistry; Florida Intl Univ., Miami, FL (United States). Biomolecular Sciences Inst.

Escherichia coli topoisomerase I has an essential function in preventing hypernegative supercoiling of DNA. A full length structure of E. coli topoisomerase I reported here shows how the C-terminal domains bind single-stranded DNA (ssDNA) to recognize the accumulation of negative supercoils in duplex DNA. These C-terminal domains of E. coli topoisomerase I are known to interact with RNA polymerase, and two flexible linkers within the C-terminal domains may assist in the movement of the ssDNA for the rapid removal of transcription driven negative supercoils. The structure has also unveiled for the first time how the 4-Cys zinc ribbon domain and zinc ribbon-like domain bind ssDNA with primarily π -stacking interactions. Finally, this novel structure, in combination with new biochemical data, provides important insights into the mechanism of genome regulation by type IA topoisomerases that is essential for life, as well as the structures of homologous type IA TOP3α and TOP3β from higher eukaryotes that also have multiple 4-Cys zinc ribbon domains required for their physiological functions.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: National Institute of Health (NIH); USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1261152

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 22 Vol. 43; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (72)

Crystallization of a 67 kDa Fragment of Escherichia coli DNA Topoisomerase I Lima, Christopher D.; Wang, James C.; Mondragón, Alfonso Journal of Molecular Biology, Vol. 232, Issue 4 https://doi.org/10.1006/jmbi.1993.1474	journal	August 1993
C-terminal domains of Escherichia coli topoisomerase I belong to the zinc-ribbon superfamily Grishin, Nick V. Journal of Molecular Biology, Vol. 299, Issue 5 https://doi.org/10.1006/jmbi.2000.3841	journal	June 2000
Iron and zinc binding activity of Escherichia coli topoisomerase I homolog YrdD Cheng, Zishuo; Tan, Guoqiang; Wang, Wu BioMetals, Vol. 27, Issue 2 https://doi.org/10.1007/s10534-013-9698-z	journal	January 2014
Bacterial DNA topoisomerase I can relax positively supercoiled DNA containing a single-stranded loop Kirkegaard, Karla; Wang, James C. Journal of Molecular Biology, Vol. 185, Issue 3 https://doi.org/10.1016/0022-2836(85)90075-0	journal	October 1985
The contribution of co-transcriptional RNA:DNA hybrid structures to DNA damage and genome instability Hamperl, Stephan; Cimprich, Karlene A. DNA Repair, Vol. 19 https://doi.org/10.1016/j.dnarep.2014.03.023	journal	July 2014
Crystal Structure of Full Length Topoisomerase I from Thermotoga maritima Hansen, Guido; Harrenga, Axel; Wieland, Bernd Journal of Molecular Biology, Vol. 358, Issue 5 https://doi.org/10.1016/j.jmb.2006.03.012	journal	May 2006
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Breaking bad: R-loops and genome integrity Sollier, Julie; Cimprich, Karlene A. Trends in Cell Biology, Vol. 25, Issue 9 https://doi.org/10.1016/j.tcb.2015.05.003	journal	September 2015
RNase H overproduction allows the expression of stress-induced genes in the absence of topoisomerase I Cheng, Bokun; Rui, Shan; Ji, Chengling FEMS Microbiology Letters, Vol. 221, Issue 2 https://doi.org/10.1016/s0378-1097(03)00209-x	journal	April 2003
The structure of Escherichia coli DNA topoisomerase III Mondragón, Alfonso; DiGate, Russell Structure, Vol. 7, Issue 11 https://doi.org/10.1016/s0969-2126(00)80027-1	journal	November 1999
Solution structure of the C-terminal single-stranded DNA-binding domain of Escherichia coli topoisomerase I Yu, Liping; Zhu, Chang-Xi; Tse-Dinh, Yuk-Ching Biochemistry, Vol. 34, Issue 23 https://doi.org/10.1021/bi00023a008	journal	June 1995
All tangled up: how cells direct, manage and exploit topoisomerase function Vos, Seychelle M.; Tretter, Elsa M.; Schmidt, Bryan H. Nature Reviews Molecular Cell Biology, Vol. 12, Issue 12 https://doi.org/10.1038/nrm3228	journal	November 2011
Crystal structure of a covalent intermediate in DNA cleavage and rejoining by Escherichia coli DNA topoisomerase I Zhang, Z.; Cheng, B.; Tse-Dinh, Y. -C. Proceedings of the National Academy of Sciences, Vol. 108, Issue 17 https://doi.org/10.1073/pnas.1100300108	journal	April 2011
Preferential cleavage of plasmid-based R-loops and D-loops by Drosophila topoisomerase III Wilson-Sali, T.; Hsieh, T. -s. Proceedings of the National Academy of Sciences, Vol. 99, Issue 12 https://doi.org/10.1073/pnas.122007999	journal	June 2002
Supercoiling of the DNA template during transcription. Liu, L. F.; Wang, J. C. Proceedings of the National Academy of Sciences, Vol. 84, Issue 20 https://doi.org/10.1073/pnas.84.20.7024	journal	October 1987
Human TOP3: a single-copy gene encoding DNA topoisomerase III. Hanai, R.; Caron, P. R.; Wang, J. C. Proceedings of the National Academy of Sciences, Vol. 93, Issue 8 https://doi.org/10.1073/pnas.93.8.3653	journal	April 1996
The Role of the Carboxyl-terminal Amino Acid Residues in Escherichia coli DNA Topoisomerase III-mediated Catalysis Zhang, Hong Liang; Malpure, Swati; Li, Zhiyu Journal of Biological Chemistry, Vol. 271, Issue 15 https://doi.org/10.1074/jbc.271.15.9039	journal	April 1996
Cloning of cDNA Encoding a Novel Mouse DNA Topoisomerase III (Topo IIIβ) Possessing Negatively Supercoiled DNA Relaxing Activity, Whose Message Is Highly Expressed in the Testis Seki, Takahiko; Seki, Masayuki; Onodera, Ryoko Journal of Biological Chemistry, Vol. 273, Issue 44 https://doi.org/10.1074/jbc.273.44.28553	journal	October 1998
Relaxation of Transcription-induced Negative Supercoiling Is an Essential Function of Escherichia coli DNA Topoisomerase I Massé, Eric; Drolet, Marc Journal of Biological Chemistry, Vol. 274, Issue 23 https://doi.org/10.1074/jbc.274.23.16654	journal	June 1999
Essential Functions of C Terminus of Drosophila Topoisomerase IIIα in Double Holliday Junction Dissolution Chen, Stefanie Hartman; Wu, Chung-Hsuan; Plank, Jody L. Journal of Biological Chemistry, Vol. 287, Issue 23 https://doi.org/10.1074/jbc.m112.363044	journal	April 2012
Biochemical Characterization of an Invariant Histidine Involved in Escherichia coli DNA Topoisomerase I Catalysis Perry, Kay; Mondragón, Alfonso Journal of Biological Chemistry, Vol. 277, Issue 15 https://doi.org/10.1074/jbc.m112019200	journal	January 2002
Direct Interaction between Escherichia coli RNA Polymerase and the Zinc Ribbon Domains of DNA Topoisomerase I Cheng, Bokun; Zhu, Chang-Xi; Ji, Chengling Journal of Biological Chemistry, Vol. 278, Issue 33 https://doi.org/10.1074/jbc.m303403200	journal	June 2003
Flexibility at Gly-194 Is Required for DNA Cleavage and Relaxation Activity of Escherichia coli DNA Topoisomerase I Cheng, Bokun; Feng, Jingyang; Gadgil, Sharvari Journal of Biological Chemistry, Vol. 279, Issue 10 https://doi.org/10.1074/jbc.m312095200	journal	January 2004
Bacterial Cell Killing Mediated by Topoisomerase I DNA Cleavage Activity Cheng, Bokun; Shukla, Shikha; Vasunilashorn, Sarinnapha Journal of Biological Chemistry, Vol. 280, Issue 46 https://doi.org/10.1074/jbc.m509722200	journal	September 2005
Structural studies of type I topoisomerases Baker, N. M.; Rajan, R.; Mondragon, A. Nucleic Acids Research, Vol. 37, Issue 3 https://doi.org/10.1093/nar/gkn1009	journal	December 2008
Residues of E. coli topoisomerase I conserved for interaction with a specific cytosine base to facilitate DNA cleavage Narula, Gagandeep; Tse-Dinh, Yuk-Ching Nucleic Acids Research, Vol. 40, Issue 18 https://doi.org/10.1093/nar/gks688	journal	July 2012
Bacterial topoisomerase I and topoisomerase III relax supercoiled DNA via distinct pathways Terekhova, Ksenia; Gunn, Kathryn H.; Marko, John F. Nucleic Acids Research, Vol. 40, Issue 20 https://doi.org/10.1093/nar/gks780	journal	August 2012
The zinc ribbon domains of the general transcription factors TFIIB and Brf: conserved functional surfaces but different roles in transcription initiation Hahn, Steven; Roberts, Sadia Genes & Development, Vol. 14, Issue 6 https://doi.org/10.1101/gad.14.6.719	journal	March 2000
The Cleavage of DNA by Type-I DNA Topoisomerases Kirkegaard, K.; Pflugfelder, G.; Wang, J. C. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 49, Issue 0 https://doi.org/10.1101/sqb.1984.049.01.047	journal	January 1984
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/s0907444904026460	journal	November 2004
Molecular replacement with MOLREP Vagin, Alexei; Teplyakov, Alexei Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/s0907444909042589	journal	December 2009
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
The Structural Biology Center 19ID undulator beamline: facility specifications and protein crystallographic results Rosenbaum, Gerd; Alkire, Randy W.; Evans, Gwyndaf Journal of Synchrotron Radiation, Vol. 13, Issue 1 https://doi.org/10.1107/s0909049505036721	journal	December 2005
Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology Drolet, Marc Molecular Microbiology, Vol. 59, Issue 3 https://doi.org/10.1111/j.1365-2958.2005.05006.x	journal	February 2006
New Mechanistic and Functional Insights into DNA Topoisomerases Chen, Stefanie Hartman; Chan, Nei-Li; Hsieh, Tao-shih Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-061809-100002	journal	June 2013
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 Narula, Gagandeep; Becker, Jennifer; Cheng, Bokun BMC Biochemistry, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2091-11-41	journal	January 2010
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids B., Chen, Vincent; C., Richardson, David; S., Richardson, Jane The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/m2an-p252	text	January 2007
Deletion of TOP3β, a component of FMRP-containing mRNPs, contributes to neurodevelopmental disorders Matthew, Hurles,; Bastian, Linder,; Minna, Torniainen, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/ws6w-m474	text	January 2013
The problem of hypernegative supercoiling and r-loop formation in transcription Drolet, Marc Frontiers in Bioscience, Vol. 8, Issue 4 https://doi.org/10.2741/970	journal	January 2003
The carboxyl terminal domain ofEscherichia coli DNA topoisomerase I confers higher affinity to DNA Beran-Steed, Rita K.; Tse-Dinh, Yuk-Ching Proteins: Structure, Function, and Genetics, Vol. 6, Issue 3 https://doi.org/10.1002/prot.340060307	journal	January 1989
Mutation in Cys662 ofEscherichia coliDNA Topoisomerase I Confers Temperature Sensitivity and Change in DNA Cleavage Selectivity Zhu, Chang-Xi; Qi, Hai-yan; Tse-Dinh, Yuk-Ching Journal of Molecular Biology, Vol. 250, Issue 5 https://doi.org/10.1006/jmbi.1995.0402	journal	July 1995
Escherichia coli DNA topoisomerase I is a zinc metalloprotein with three repetitive zinc-binding domains. Tse-Dinh, Y. C.; Beran-Steed, R. K. Journal of Biological Chemistry, Vol. 263, Issue 31 https://doi.org/10.1016/S0021-9258(18)37526-4	journal	November 1988
Zinc (II) coordination in Escherichia coli DNA topoisomerase I is required for cleavable complex formation with DNA Tse-Dinh, Y. C. Journal of Biological Chemistry, Vol. 266, Issue 22 https://doi.org/10.1016/S0021-9258(18)98686-2	journal	August 1991
RNase H overproduction allows the expression of stress-induced genes in the absence of topoisomerase I Cheng, Bokun; Rui, Shan; Ji, Chengling FEMS Microbiology Letters, Vol. 221, Issue 2 https://doi.org/10.1016/S0378-1097(03)00209-X	journal	April 2003
The structure of Escherichia coli DNA topoisomerase III Mondragón, Alfonso; DiGate, Russell Structure, Vol. 7, Issue 11 https://doi.org/10.1016/S0969-2126(00)80027-1	journal	November 1999
Arginine Methylation Facilitates the Recruitment of TOP3B to Chromatin to Prevent R Loop Accumulation Yang, Yanzhong; McBride, Kevin M.; Hensley, Sean Molecular Cell, Vol. 53, Issue 3 https://doi.org/10.1016/j.molcel.2014.01.011	journal	February 2014
Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I Lima, Christopher D.; Wang, James C.; Mondragón, Alfonso Nature, Vol. 367, Issue 6459 https://doi.org/10.1038/367138a0	journal	January 1994
Top3β is an RNA topoisomerase that works with fragile X syndrome protein to promote synapse formation Xu, Dongyi; Shen, Weiping; Guo, Rong Nature Neuroscience, Vol. 16, Issue 9 https://doi.org/10.1038/nn.3479	journal	August 2013
Deletion of TOP3β, a component of FMRP-containing mRNPs, contributes to neurodevelopmental disorders Stoll, Georg; Pietiläinen, Olli P. H.; Linder, Bastian Nature Neuroscience, Vol. 16, Issue 9 https://doi.org/10.1038/nn.3484	journal	August 2013
Studies of bacterial topoisomerases I and III at the single-molecule level Terekhova, Ksenia; Marko, John F.; Mondragón, Alfonso Biochemical Society Transactions, Vol. 41, Issue 2 https://doi.org/10.1042/BST20120297	journal	March 2013
DNA Topoisomerases Regulate R-loop Formation during Transcription of the rrnB Operon in Escherichia coli Massé, Eric; Phoenix, Pauline; Drolet, Marc Journal of Biological Chemistry, Vol. 272, Issue 19 https://doi.org/10.1074/jbc.272.19.12816	journal	May 1997
DNA Topoisomerase I from Mycobacterium smegmatis: AN ENZYME WITH DISTINCT FEATURES Bhaduri, Tisha; Bagui, Tapan Kumar; Sikder, Devanjan Journal of Biological Chemistry, Vol. 273, Issue 22 https://doi.org/10.1074/jbc.273.22.13925	journal	May 1998
On the Molecular Basis of the Thermal Sensitivity of an Escherichia coli topA Mutant Wang, Yong; Lynch, A. Simon; Chen, Sue-Jane Journal of Biological Chemistry, Vol. 277, Issue 2 https://doi.org/10.1074/jbc.M109436200	journal	November 2001
Essential Functions of C Terminus of Drosophila Topoisomerase IIIα in Double Holliday Junction Dissolution Chen, Stefanie Hartman; Wu, Chung-Hsuan; Plank, Jody L. Journal of Biological Chemistry, Vol. 287, Issue 23 https://doi.org/10.1074/jbc.M112.363044	journal	April 2012
Biochemical Characterization of an Invariant Histidine Involved in Escherichia coli DNA Topoisomerase I Catalysis Perry, Kay; Mondragón, Alfonso Journal of Biological Chemistry, Vol. 277, Issue 15 https://doi.org/10.1074/jbc.M112019200	journal	January 2002
Direct Interaction between Escherichia coli RNA Polymerase and the Zinc Ribbon Domains of DNA Topoisomerase I Cheng, Bokun; Zhu, Chang-Xi; Ji, Chengling Journal of Biological Chemistry, Vol. 278, Issue 33 https://doi.org/10.1074/jbc.M303403200	journal	June 2003
Flexibility at Gly-194 Is Required for DNA Cleavage and Relaxation Activity of Escherichia coli DNA Topoisomerase I Cheng, Bokun; Feng, Jingyang; Gadgil, Sharvari Journal of Biological Chemistry, Vol. 279, Issue 10 https://doi.org/10.1074/jbc.M312095200	journal	January 2004
Bacterial Cell Killing Mediated by Topoisomerase I DNA Cleavage Activity Cheng, Bokun; Shukla, Shikha; Vasunilashorn, Sarinnapha Journal of Biological Chemistry, Vol. 280, Issue 46 https://doi.org/10.1074/jbc.M509722200	journal	September 2005
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Davis, I. W.; Leaver-Fay, A.; Chen, V. B. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm216	journal	May 2007
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
A highly processive topoisomerase I: studies at the single-molecule level Szafran, Marcin Jan; Strick, Terence; Strzałka, Agnieszka Nucleic Acids Research, Vol. 42, Issue 12 https://doi.org/10.1093/nar/gku494	journal	May 2014
The Cleavage of DNA by Type-I DNA Topoisomerases Kirkegaard, K.; Pflugfelder, G.; Wang, J. C. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 49, Issue 0 https://doi.org/10.1101/SQB.1984.049.01.047	journal	January 1984
A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression Skourti-Stathaki, K.; Proudfoot, N. J. Genes & Development, Vol. 28, Issue 13 https://doi.org/10.1101/gad.242990.114	journal	July 2014
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904026460	journal	November 2004
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
Molecular replacement with MOLREP Vagin, Alexei; Teplyakov, Alexei Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042589	journal	December 2009
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
The Structural Biology Center 19ID undulator beamline: facility specifications and protein crystallographic results Rosenbaum, Gerd; Alkire, Randy W.; Evans, Gwyndaf Journal of Synchrotron Radiation, Vol. 13, Issue 1 https://doi.org/10.1107/S0909049505036721	journal	December 2005
The role of the Zn(II) binding domain in the mechanism of E. coli DNA topoisomerase I Ahumada, Adriana; Tse-Dinh, Yuk-Ching BMC Biochemistry, Vol. 3, Issue 1, p. 13 https://doi.org/10.1186/1471-2091-3-13	journal	May 2002
On the viability of Escherichia coli cells lacking DNA topoisomerase I Stockum, Anna; Lloyd, Robert G.; Rudolph, Christian J. BMC Microbiology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2180-12-26	journal	January 2012
Solution Structure of the C-Terminal Single-Stranded DNA-Binding Domain of Escherichia Coli Topoisomerase I Yu, Liping; Zhu, Chang-Xi; Tse-Dinh, Yuk-Ching Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr4045	dataset	January 2001

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