Roles of Topoisomerases in Maintaining Steady-state DNA Supercoiling in Escherichia coli

Zechiedrich, Lynn; Khodursky, Arkady B.; Bachellier, Sophie; Schneider, Robert; Chen, Dongrong; Lilley, David M.J.; Cozzarelli, Nicholas R.

doi:10.1074/jbc.275.11.8103

Cited by 301 publications

(319 citation statements)

References 72 publications

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“…It is also prudent to keep in mind that E. coli and related bacteria also possess DNA topoisomerase IV, an enzyme with a structure that is closely related to that of gyrase but which lacks the ability to negatively supercoil DNA (Kato et al 1990). Topo IV is also ATP dependent and is the principal decatenase of the cell, responsible for the topological separation of daughter chromosomes at the end of genome replication; Topo IV also has the ability to relax negatively supercoiled DNA (Bates and Maxwell 2007;Zawadzki et al 2015;Zechiedrich et al 2000). Like DNA gyrase, Topo IV is sensitive to adenylylation by FicT toxins that interfere with ATP binding activity (Harms et al 2015).…”

Section: Introductionmentioning

confidence: 99%

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

Dorman

2016

Biophys Rev

107

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Although it has become routine to consider DNA in terms of its role as a carrier of genetic information, it is also an important contributor to the control of gene expression. This regulatory principle arises from its structural properties. DNA is maintained in an underwound state in most bacterial cells and this has important implications both for DNA storage in the nucleoid and for the expression of genetic information. Underwinding of the DNA through reduction in its linking number potentially imparts energy to the duplex that is available to drive DNA transactions, such as transcription, replication and recombination. The topological state of DNA also influences its affinity for some DNA binding proteins, especially in DNA sequences that have a high A + T base content. The underwinding of DNA by the ATP-dependent topoisomerase DNA gyrase creates a continuum between metabolic flux, DNA topology and gene expression that underpins the global response of the genome to changes in the intracellular and external environments. These connections describe a fundamental and generalised mechanism affecting global gene expression that underlies the specific control of transcription operating through conventional transcription factors. This mechanism also provides a basal level of control for genes acquired by horizontal DNA transfer, assisting microbial evolution, including the evolution of pathogenic bacteria.

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Section: Introductionmentioning

confidence: 99%

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

Dorman

2016

Biophys Rev

107

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“…DNA gyrase is unique among the type II DNA topoisomerases in being able to negatively supercoil DNA. This activity is largely responsible for maintaining bacterial DNA within a physiological range of negative superhelical density in vivo (Zechiedrich et al, 2000). DNA gyrase is also involved in removing positive supercoils generated by DNA replication and transcription and in separating the decatenated daughter chromosomes during cell division (Wang, 1996;Champoux, 2001).…”

Section: Introductionmentioning

confidence: 99%

DNA Gyrase Is Involved in Chloroplast Nucleoid Partitioning

et al. 2004

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DNA gyrase, which catalyzes topological transformation of DNA, plays an essential role in replication and transcription in prokaryotes. Virus-induced gene silencing of NbGyrA or NbGyrB, which putatively encode DNA gyrase subunits A and B, respectively, resulted in leaf yellowing phenotypes in Nicotiana benthamiana. NbGyrA and NbGyrB complemented the gyrA and gyrB temperature-sensitive mutations of Escherichia coli, respectively, which indicates that the plant and bacterial subunits are functionally similar. NbGyrA and NbGyrB were targeted to both chloroplasts and mitochondria, and depletion of these subunits affected both organelles by reducing chloroplast numbers and inducing morphological and physiological abnormalities in both organelles. Flow cytometry analysis revealed that the average DNA content in the affected chloroplasts and mitochondria was significantly higher than in the control organelles. Furthermore, 49,6-diamidino-2-phenylindole staining revealed that the abnormal chloroplasts contained one or a few large nucleoids instead of multiple small nucleoids dispersed throughout the stroma. Pulse-field gel electrophoresis analyses of chloroplasts demonstrated that the sizes and/ or structure of the DNA molecules in the abnormal chloroplast nucleoids are highly aberrant. Based on these results, we propose that DNA gyrase plays a critical role in chloroplast nucleoid partitioning by regulating DNA topology.

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“…Consequently, decatenation is an essential step for chromosome segregation. Although these replication-induced topological entanglements are harmful for the cell, a proper level of (Ϫ) supercoiling is considered to set the topological homeostasis, which governs certain cellular processes (2), such as transcription and replication initiation, that require DNA unwinding (3). In bacteria, the resolution of DNA entanglements and maintenance of topological homeostasis are largely handled by two essential type IIA topoisomerases (Topos), 1 DNA gyrase and Topo IV (4).…”

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confidence: 99%

Structure of the Topoisomerase IV C-terminal Domain

Hsieh

Farh

Huang

et al. 2004

Journal of Biological Chemistry

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Bacteria possess two closely related yet functionally distinct essential type IIA topoisomerases (Topos). DNA gyrase supports replication and transcription with its unique supercoiling activity, whereas Topo IV preferentially relaxes (؉) supercoils and is a decatenating enzyme required for chromosome segregation. Here we report the crystal structure of the C-terminal domain of Topo IV ParC subunit (ParC-CTD) from Bacillus stearothermophilus and provide a structure-based explanation for how Topo IV and DNA gyrase execute distinct activities. Although the topological connectivity of ParC-CTD is similar to the recently determined CTD structure of DNA gyrase GyrA subunit (GyrA-CTD), ParC-CTD surprisingly folds as a previously unseen broken form of a six-bladed ␤-propeller. Propeller breakage is due to the absence of a DNA gyrase-specific GyrA box motif, resulting in the reduction of curvature of the proposed DNA binding region, which explains why ParC-CTD is less efficient than GyrA-CTD in mediating DNA bending, a difference that leads to divergent activities of the two homologous enzymes. Moreover, we found that the topology of the propeller blades observed in ParC-CTD and GyrA-CTD can be achieved from a concerted ␤-hairpin invasion-induced fold change event of a canonical six-bladed ␤-propeller; hence, we proposed to name this new fold as "hairpininvaded ␤-propeller" to highlight the high degree of similarity and a potential evolutionary linkage between them. The possible role of ParC-CTD as a geometry facilitator during various catalytic events and the evolutionary relationships between prokaryotic type IIA Topos have also been discussed according to these new structural insights.

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Roles of Topoisomerases in Maintaining Steady-state DNA Supercoiling in Escherichia coli

Cited by 301 publications

References 72 publications

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

DNA Gyrase Is Involved in Chloroplast Nucleoid Partitioning

Structure of the Topoisomerase IV C-terminal Domain

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