Reverse gyrase, a hallmark of the hyperthermophilic archaebacteria

Tour, Claire Bouthier de la; Portemer, Christiane; Nadal, Marc; Stetter, Karl O.; Forterre, Patrick; Duguet, Michel

doi:10.1128/jb.172.12.6803-6808.1990

Cited by 106 publications

(58 citation statements)

References 38 publications

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“…This type I topoisomerase is the only enzyme unique to hyperthermophiles and the only known topoisomerase that can actively introduce positive superhelical twists into DNA (56,(65)(66)(67)(68).…”

Section: Resultsmentioning

confidence: 99%

Human Topoisomerase IIα Rapidly Relaxes Positively Supercoiled DNA

McClendon

Rodríguez

Osheroff

2005

Journal of Biological Chemistry

142

107

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Movement of the DNA replication machinery through the double helix induces acute positive supercoiling ahead of the fork and precatenanes behind it. Because topoisomerase I and II create transient single-and double-stranded DNA breaks, respectively, it has been assumed that type I enzymes relax the positive supercoils that precede the replication fork. Conversely, type II enzymes primarily resolve the precatenanes and untangle catenated daughter chromosomes. However, studies on yeast and bacteria suggest that type II topoisomerases may also function ahead of the replication machinery. If this is the case, then positive DNA supercoils should be the preferred relaxation substrate for topoisomerase II␣, the enzyme isoform involved in replicative processes in humans. Results indicate that human topoisomerase II␣ relaxes positively supercoiled plasmids >10-fold faster than negatively supercoiled molecules. In contrast, topoisomerase II␤, which is not required for DNA replication, displays no such preference. In addition to its high rates of relaxation, topoisomerase II␣ maintains lower levels of DNA cleavage complexes with positively supercoiled molecules. These properties suggest that human topoisomerase II␣ has the potential to alleviate torsional stress ahead of replication forks in an efficient and safe manner.

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Section: Resultsmentioning

confidence: 99%

Human Topoisomerase IIα Rapidly Relaxes Positively Supercoiled DNA

McClendon

Rodríguez

Osheroff

2005

Journal of Biological Chemistry

142

107

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“…It was suggested that overlinking could compensate for the effect of temperature on DNA structure (16). The enzyme is widely distributed in thermophilic archaea (6,8). The first reverse gyrase characterized was isolated from the hyperthermophilic archaeum Sulfolobus acidocaldarius (23,33).…”

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Reverse gyrase from hyperthermophiles: probable transfer of a thermoadaptation trait from Archaea to Bacteria

et al. 2000

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The hyperthermophilic bacterium Thermotoga maritima MSB8 possesses a reverse gyrase whose enzymatic properties are very similar to those of archaeal reverse gyrases. It catalyzes the positive supercoiling of the DNA in an Mg 2؉ -and ATP-dependent process. Its optimal temperature of activity is around 90°C, and it is highly thermostable. We have cloned and DNA sequenced the corresponding gene (T. maritima topR). This is the first report describing the analysis of a gene encoding a reverse gyrase in bacteria. The T. maritima topR gene codes for a protein of 1,104 amino acids with a deduced molecular weight of 128,259, a value in agreement with that estimated from the denaturing gel electrophoresis of the purified enzyme. Like its archaeal homologs, the T. maritima reverse gyrase exhibits helicase and topoisomerase domains, and its sequence matches very well the consensus sequence for six reverse gyrases now available. Phylogenetic analysis shows that all reverse gyrases, including the T. maritima enzyme, form a very homogeneous group, distinct from the type I 5 topoisomerases of the TopA subfamily, for which we have previously isolated a representative gene in T. What are the molecular mechanisms involved in the adaptation of life to elevated temperatures? In terms of DNA dynamics, part of the answer was provided by the discovery in thermophilic organisms of a particular topoisomerase, the reverse gyrase, that modifies the topological state of DNA by introducing positive supercoils in an ATP-dependent process (14). It was suggested that overlinking could compensate for the effect of temperature on DNA structure (16). The enzyme is widely distributed in thermophilic archaea (6,8). The first reverse gyrase characterized was isolated from the hyperthermophilic archaeum Sulfolobus acidocaldarius (23,33). Mechanistic studies showed that it is transiently linked to the DNA by a 5Ј phosphotyrosyl bond (22,24), classifying it in the type I 5Ј topoisomerase family as proposed by Roca (38). Sequence analysis further showed that it is a single polypeptide containing putative helicase and topoisomerase domains located in the amino-and carboxy-terminal, respectively, parts of the protein (9). The helicase domain exhibits motifs found in DNA and RNA helicases, and the topoisomerase domain exhibits a significant similarity with the 5Ј topoisomerase I (protein ) from Escherichia coli. From all of these data, a mechanism of reverse gyration involving the concerted action of two such domains was proposed (9, 14).To date, four other archaeal reverse gyrase genes have been sequenced: from Sulfolobus shibatae (21), Methanopyrus kandleri (26), Pyrococcus furiosus (3), and Methanococcus jannaschii (7). A comparative analysis of reverse gyrases from two members of the order Sulfolobales (S. acidocaldarius and S. shibatae) and M. kandleri with the other type I topoisomerases of the 5Ј family (21) showed that the reverse gyrases constitute a new group within this family distinct from the previously described TopA and TopB groups, represent...

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“…Reverse gyrase is the only topoisomerase known to overwind DNA. So far it has been found exclusively in hyperthermophiles, organisms that live above ϳ80°C (4,5). The role of the protein in vivo remains unclear (6); one suggestion is that it rewinds the DNA strands in regions of the chromosome that have opened up to allow transcription or replication (7).…”

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confidence: 99%

Studies of a Positive Supercoiling Machine

Rodríguez

2002

Journal of Biological Chemistry

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Reverse gyrase, the only topoisomerase known to positively supercoil DNA, has an N-terminal ATPase domain that drives the activity of a topoisomerase domain. This study shows that the N-terminal domain represses topoisomerase activity in the absence of nucleotide, and nucleotide binding is sufficient to relieve the repression. A "latch" region in the N-terminal part was observed to close over the topoisomerase domain in the reverse gyrase crystal structure. Mutants lacking all or part of the latch relax DNA in the absence of nucleotide, indicating that this region mediates topoisomerase repression. The mutants also show altered DNA-dependent ATPase activity, suggesting that the latch may be involved in coupling nucleotide hydrolysis to supercoiling. It is not required for this process, however, because the mutants can still positively supercoil DNA. Nucleotide hydrolysis is essential to the specificity of reverse gyrase for increasing the linking number of DNA. Although with ATP the enzyme performs strand passage always toward increasing linking number, it can increase or decrease the linking number in the presence of a nonhydrolyzable ATP analog. This suggests that the mechanism of reverse gyrase is best described by a combination of recently proposed models.Topoisomerases participate in practically every DNA transaction, including transcription, replication, recombination, and chromosomal segregation (1). They change the topological state of DNA by altering its linking number, i.e. the number of times that one strand of the double helix crosses the other. They use a three-step mechanism of cleavage, strand passage, and religation. In the first step, a nucleophilic tyrosine attacks the phosphodiester backbone, cleaving the DNA and leading to a covalent intermediate of protein-DNA termed the "cleavage complex." Type I topoisomerases cleave one strand of the duplex; type II enzymes cleave both strands. The enzyme, covalently attached to the cut DNA, separates the free ends of the cleaved strand(s) and allows the other strand of the duplex (type I), or another region of duplex (type II), to pass through this gap. The protein then reseals the backbone of the cleaved DNA and releases the product.Although all topoisomerases can relax supercoiled DNA, only prokaryotic gyrase is able to introduce negative supercoils in DNA. This type II topoisomerase uses the energy of ATP hydrolysis to reduce the linking number, leading to an underwound, or negatively supercoiled, product. Until recently, gyrase was the only topoisomerase known to supercoil DNA. Later, another supercoiling enzyme was discovered and named reverse gyrase, because it increases the linking number, leading to overwound, or positively supercoiled, product (2, 3). Reverse gyrase is the only topoisomerase known to overwind DNA. So far it has been found exclusively in hyperthermophiles, organisms that live above ϳ80°C (4, 5). The role of the protein in vivo remains unclear (6); one suggestion is that it rewinds the DNA strands in regions of the chromosome that...

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Reverse gyrase, a hallmark of the hyperthermophilic archaebacteria

Cited by 106 publications

References 38 publications

Human Topoisomerase IIα Rapidly Relaxes Positively Supercoiled DNA

Human Topoisomerase IIα Rapidly Relaxes Positively Supercoiled DNA

Reverse gyrase from hyperthermophiles: probable transfer of a thermoadaptation trait from Archaea to Bacteria

Studies of a Positive Supercoiling Machine

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