Resolution of Holliday junction analogs by T4 endonuclease VII can be directed by substrate structure.

Mueller, John; Newton, C. J.; Jensch, F.; Kemper, Börries; Cunningham, Richard P.; Kallenbach, Neville R.; Seeman, Nadrian C.

doi:10.1016/s0021-9258(18)77436-x

Cited by 31 publications

(3 citation statements)

References 34 publications

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“…We and others have shown that it cleaves the crossover strands of four-arm Holliday junction analogues (Mueller et al, 1988;Duckett et al, 1988), and not the helical strands. Recently, we have shown that the enzyme requires more than eight nucleotide pairs in junction arms that are cleaved, and we have modeled some of the features of the molecule (Mueller et al, 1990). The endonuclease VII cleavage pattern of the five-arm and six-arm junctions provides an analysis complementary to the hydroxyl radical experiments.…”

Section: Resultsmentioning

confidence: 99%

Assembly and characterization of five-arm and six-arm DNA branched junctions

et al. 1991

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DNA branched junctions have been constructed that contain either five arms or six arms surrounding a branch point. These junctions are not as stable as junctions containing three or four arms; unlike the smaller junctions, they cannot be shown to migrate as a single band on native gels when each of their arms contains eight nucleotide pairs. However, they can be stabilized if their arms contain 16 nucleotide pairs. Ferguson analysis of these junctions in combination with three-arm and four-arm junctions indicates a linear increase in friction constant as the number of arms increases, with the four-arm junction migrating anomalously. The five-arm junction does not appear to have any unusual stacking structure, and all strands show similar responses to hydroxyl radical autofootprinting analysis. By contrast, one strand of the six-arm junction shows virtually no protection from hydroxyl radicals, suggesting that it is the helical strand of a preferred stacking domain. Both junctions are susceptible to digestion by T4 endonuclease VII, which resolves Holliday junctions. However, the putative helical strand of the six-arm junction shows markedly reduced cleavage, supporting the notion that its structure is largely found in a helical conformation. Branched DNA molecules can be assembled into structures whose helix axes form multiply connected objects and networks. The ability to construct five-arm and six-arm junctions vastly increases the number of structures and networks that can be built from branched DNA components. Icosahedral deltahedra and 11 networks with 432 symmetry, constructed from Platonic and Archimedean solids, are among the structures whose construction is feasible, now that these junctions can be made.

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Section: Resultsmentioning

confidence: 99%

Assembly and characterization of five-arm and six-arm DNA branched junctions

et al. 1991

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“…The latter model might even allow for dissociation of the enzyme followed some time later by the binding of a new molecule that introduces the second cleavage. Using cloverleaf‐type junctions, Mueller et al . (1990) showed that two cleavages are introduced within the same junction molecule by T4 endonuclease VII, but Kemper and colleagues (Pottmeyer and Kemper, 1992) have introduced what they term a ‘nick and counter‐nick’ model, implying uncoordinated cleavage at the two sites.…”

Section: Introductionmentioning

confidence: 99%

Near-simultaneous DNA cleavage by the subunits of the junction-resolving enzyme T4 endonuclease VII

Giraud-Panis¹,

Lilley²

1997

The EMBO Journal

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junction (Duckett et al., 1988; Mueller et al., 1988), Biochemistry, The University, Dundee DD1 4HN, UK suggesting that each subunit makes a single cleavage. The 1 Corresponding author E.coli resolving enzyme RuvC also tends to introduce pairs of cleavages within the core of a junction that can In common with a number of other DNA junctionundergo a limited degree of branch migration (Bennett resolving enzymes, endonuclease VII of bacteriophage et al., 1993). The crystal structure of this protein has been T4 binds to a four-way DNA junction as a dimer, and solved (Ariyoshi et al., 1994). It is a dimer of subunits, cleaves two strands of the junction. We have used a wherein clusters of acidic residues shown to be important supercoil-stabilized cruciform substrate to probe the for catalytic activity (Saito et al., 1995) are separated by simultaneity of cleavage at the two sites. Active endo-~30 Å between the two subunits. This would indicate that nuclease VII converts the supercoiled circular DNA the two active sites are likely to act independently. One directly into linear product, indicating that the two could envisage this occurring in two extreme ways. First, cleavage reactions must occur within the lifetime of the enzyme might bind, and both strands become cleaved the protein-junction complex. By contrast, a heterowithin a very short interval, i.e. giving effectively simultandimer of active enzyme and an inactive mutant endoeous cleavage of the two sites. Alternatively, the first site nuclease VII leads to the formation of nicked circular might be cleaved, followed later by cleavage at the second product, showing that the subunits operate fully indesite. The latter model might even allow for dissociation pendently.of the enzyme followed some time later by the binding Keywords: cruciform/DNA-protein interaction/DNA of a new molecule that introduces the second cleavage. supercoiling/Holliday junction/recombination Using cloverleaf-type junctions, Mueller et al. (1990) showed that two cleavages are introduced within the same junction molecule by T4 endonuclease VII, but Kemper and colleagues (Pottmeyer and Kemper, 1992) have intro-

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“…The presence of two crossover isomers in synthetic systems in Vitro (Zhang & Seeman, 1994;Carlstro ¨m & Chazin, 1996) can be ascribed to the formation of different isomers when strands are heated and cooled during the annealing process. Likewise, the presence of both possible resolvase products in in Vitro reactions (Mueller et al, 1990) could be a complicated function of the sequence specificity of the enzyme. Crossover isomers are the consequence of stacking dominance (Wang et al, 1991), in which one pair of stacking isomers is preferred to another pair.…”

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Direct Evidence for Holliday Junction Crossover Isomerization

Wang

Seeman

1997

Biochemistry

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The Holliday junction is a key intermediate in genetic recombination. This is a four-stranded branched DNA structure, whose double-helical arms are stacked in two domains; two of the strands are roughly helical, and the other two cross over between domains. Switching the strands between these two roles is known as crossover isomerization; this postulated reversal is thought to be one of the key transformations that the Holliday junction can undergo, because it can lead to changing the products from patch to splice recombinants. We present direct evidence that this reaction can indeed occur in Holliday junctions in solution. We have constructed a double-crossover molecule containing a branched junction, constrained not to be in its favored conformation. This junction is released from the double-crossover molecule by digestion with restriction endonucleases. We demonstrate by means of hydroxyl radical autofootprinting that the junction changes its crossover isomer spontaneously when released from the double crossover. We control for the possibility that the experimental protocol causes the isomerization. We also exclude dissociation and interaction with other molecules in solution as contributing to the phenomenon. Thus, crossover isomerization is an authentic spontaneous transformation of Holliday junctions.

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Resolution of Holliday junction analogs by T4 endonuclease VII can be directed by substrate structure.

Cited by 31 publications

References 34 publications

Assembly and characterization of five-arm and six-arm DNA branched junctions

Assembly and characterization of five-arm and six-arm DNA branched junctions

Near-simultaneous DNA cleavage by the subunits of the junction-resolving enzyme T4 endonuclease VII

Direct Evidence for Holliday Junction Crossover Isomerization

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