Type I topoisomerase activity is required for proper chromosomal segregation in
            <i>Escherichia coli</i>

Zhu, Qing; Pongpech, Pintip; DiGate, Russell J.

doi:10.1073/pnas.171579898

Cited by 78 publications

(86 citation statements)

References 34 publications

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“…Topoisomerase I is efficient at relaxing negatively supercoiled DNA, whereas topoisomerase III is an efficient decatenating enzyme (DiGate and Marians, 1988;Champoux, 2001;Nurse et al ., 2003). E. coli cells that lack both type IA topoisomerase activities filament extensively and do not segregate chromosomal DNA properly (Zhu et al ., 2001). Deletion of the recA gene suppresses this phenotype.…”

Section: Introductionmentioning

confidence: 99%

“…These results have led to the suggestion that the type IA enzymes are involved in RecA-mediated recombination and that they may specifically remove recombination intermediates before chromosome segregation (Zhu et al ., 2001;Wang, 2002). Furthermore, yeast Sgs1 and human BLM helicases, members of the RecQ family, have been shown to interact with Topo III (Gangloff et al ., 1994;1999;Haber, 1999;Bennett et al ., 2000;Shimamoto et al ., 2000;Wu et al ., 2000;Fricke et al ., 2001).…”

Section: Introductionmentioning

confidence: 99%

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Oligonucleotide cleavage and rejoining by topoisomerase III from the hyperthermophilic archaeon Sulfolobus solfataricus: temperature dependence and strand annealing‐promoted DNA religation

Chen

Huang²

2006

Molecular Microbiology

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SummaryTopoisomerase III from the hyperthermophilic archaeon Sulfolobus solfataricus ( Sso topo III) is optimally active in DNA relaxation at 75 ∞ C. We report here that Sso topo III-catalysed DNA cleavage and religation differed significantly in temperature dependence: the enzyme was most active in cleaving ssDNA containing a cleavage site at 25-50 ∞ C, but was efficient in rejoining the cleaved DNA strand only at higher temperatures (e.g. ≥ 45 ∞ C). The failure of Sso topo III to rejoin the cleaved DNA strand efficiently appeared to be responsible for the inability of the enzyme to relax negatively supercoiled DNA at low temperature (e.g. 25 ∞ C). Intriguingly, Sso topo III facilitated DNA annealing although it showed higher affinity for ssDNA than for dsDNA. Religation of the DNA strand cleaved by Sso topo III was drastically enhanced when the DNA was allowed to anneal to a complementary noncleaved oligonucleotide, presumably as a result of destabilization of the interaction between the enzyme and the cleaved strand through the formation of duplex DNA. A region in the non-cleaved strand corresponding to a sequence containing six bases on the 5 ¢ side and two bases on the 3 ¢ side of the cleavage site in the cleaved strand was crucial to the annealingpromoted religation. However, the annealing-promoted religation was relatively insensitive to mismatches in this region and the region conserved for oligonucleotide cleavage, except for that at the 5 ¢ end of the broken strand. These results suggest that Sso topo III is well suited for a role in DNA rewinding, whether it leads to homoduplex or heteroduplex formation.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Oligonucleotide cleavage and rejoining by topoisomerase III from the hyperthermophilic archaeon Sulfolobus solfataricus: temperature dependence and strand annealing‐promoted DNA religation

Chen

Huang²

2006

Molecular Microbiology

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“…This omnipresence of the type IA enzymes suggests that they play an essential role in processing intracellular DNA, and genetic studies of microorganisms have provided strong support of this idea. Escherichia coli lacking both of the type IA DNA topoisomerases, for example, is not viable (4). Similarly, yeast top3 mutants lacking DNA topoisomerase III (Top3), the only type IA enzyme in yeasts, exhibit a complex phenotype including slow growth, hypersensitivity to DNA-damaging agents, genome instability, and low viability (5-7).…”

mentioning

confidence: 99%

“…Whereas sporulation of Saccharomyces cerevisiae top3 diploids yields no viable spores, this lethality can be prevented by blocking meiotic recombination (7). Concordantly, inactivation of the E. coli recA gene, which is essential for homologous recombination, restores viability of a topA topB double mutant lacking both DNA topoisomerases I and III (4). Earlier studies also showed that the defects of mitotic yeast top3 cells could largely be suppressed by mutations in a helicase of the RecQ family, the Sgs1 protein in S. cerevisiae and the Rqh1 protein in Schizosaccharomyces pombe (6,8,9).…”

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confidence: 99%

Infertility and aneuploidy in mice lacking a type IA DNA topoisomerase IIIβ

Kwan

Møens

Wang

2003

Proc. Natl. Acad. Sci. U.S.A.

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We report that disruption of the mouse TOP3␤ gene encoding DNA topoisomerase III␤, one of the two mammalian type IA DNA topoisomerases, leads to a progressive reduction in fecundity. The litter size in crosses of top3␤ ؊/؊ mice decreases over time and through successive generations, and this decrease seems to reflect embryonic death rather than impaired fertilization. These observations are suggestive of a gradual accumulation of chromosomal defects in germ cells lacking DNA topoisomerase III␤, and this interpretation is supported by the observation of a high incidence of aneuploidy in the spermatocytes of infertile top3␤ ؊/؊ males. Cytogenetic examination of spermatocytes of wild-type mice also indicates that DNA topoisomerase III␤ becomes prominently associated with the asynaptic regions of the XY bivalents during pachytene, and that there is a time lag between the appearance of chromosome-bound DNA topoisomerase III␤ and Rad51, a protein known to be involved in an early step of homologous recombination. We interpret these findings, together with the known mechanistic characteristics of different subfamilies of DNA topoisomerases, in terms of a specific role of a type IA DNA topoisomerase in the resolution of meiotic double-Holliday junctions without crossing over. This interpretation is most likely applicable to mitotic cells as well and can explain the universal presence of at least one type IA DNA topoisomerase in all organisms.

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“…The complexity of DNA topoisomerase II, with two dissimilar polypeptides each with multiple domains having different enzymic activities, seems too great to have preceded topoisomerase I. The fact that DNA topoisomerase I is essential for bacterial DNA seqregation (Zhu et al, 2001) is consistent with an early origin.…”

Section: Origin Of the Basic Machinery For General Recombinationmentioning

confidence: 99%

Origins of the machinery of recombination and sex

2002

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Mutation plays the primary role in evolution that Weismann mistakenly attributed to sex. Homologous recombination, as in sex, is important for population genetics -shuffling of minor variants, but relatively insignificant for large-scale evolution. Major evolutionary innovations depend much more on illegitimate recombination, which makes novel genes by gene duplication and by gene chimaerisationessentially mutational forces. The machinery of recombination and sex evolved in two distinct bouts of quantum evolution separated by nearly 3 Gy of stasis; I discuss their nature and causes. The dominant selective force in the evolution of recombination and sex has been selection for replicational fidelity and viability; without the recombination machinery, accurate reproduction, stasis, resistance to radical deleterious evolutionary change and preservation of evolutionary innovations would be impossible. Recombination proteins betray in their phylogeny and domain structure a key role for gene duplication and chimaerisation in their own origin. They arose about 3.8 Gy ago to enable faithful replication and segregation of the first circular DNA genomes in precellular ancestors of Gram-negative eubacteria. Then they were recruited and modified by selfish genetic parasites (viruses; transposons) to help them spread from host to host. Bacteria differ fundamentally from eukaryotes in that gene transfer between cells, whether incidental to their absorptive feeding on DNA and virus infection or directly by plasmids, involves only genomic fragments. This was radically changed by the neomuran revolution about 850 million years ago when a posibacterium evolved

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Type I topoisomerase activity is required for proper chromosomal segregation in Escherichia coli

Cited by 78 publications

References 34 publications

Oligonucleotide cleavage and rejoining by topoisomerase III from the hyperthermophilic archaeon Sulfolobus solfataricus: temperature dependence and strand annealing‐promoted DNA religation

Oligonucleotide cleavage and rejoining by topoisomerase III from the hyperthermophilic archaeon Sulfolobus solfataricus: temperature dependence and strand annealing‐promoted DNA religation

Infertility and aneuploidy in mice lacking a type IA DNA topoisomerase IIIβ

Origins of the machinery of recombination and sex

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