Knotting probability of DNA molecules confined in restricted volumes: DNA knotting in phage capsids

Arsuaga, Javier; Vázquez, Mariel; Trigueros, Sònia; Sumners, D. W.; Roca, Joaquím

doi:10.1073/pnas.032095099

Cited by 245 publications

(320 citation statements)

References 42 publications

(52 reference statements)

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“…DNA knotting probability is enhanced in P4 derivatives containing genome deletions (20) and in tailless mutants (21). We recently showed that most of these knots are formed by the cyclization of the DNA while it is confined inside the phage capsid (22). Here, we show that these knots capture information about the global arrangement of the packed DNA.…”

mentioning

confidence: 62%

“…Bacteriophage P4 vir1 del22 was prepared as described in ref. 22. Briefly, the phage was amplified in Escherichia coli strain C-1895, which is lysogenic for P2 (the helper prophage).…”

Section: Methodsmentioning

confidence: 99%

“…Algorithms that generate random distributions of equilateral polygons with zero volume and confined to spherical volumes, as well as algorithms that compute the Alexander polynomial (⌬(t)), have been reported previously (22). Each selected knotted polygon was further identified by evaluating its Alexander polynomial at t ϭ Ϫ2 and t ϭ Ϫ3.…”

Section: Methodsmentioning

confidence: 99%

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DNA knots reveal a chiral organization of DNA in phage capsids

Arsuaga

Vázquez

McGuirk

et al. 2005

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

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231

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Icosahedral bacteriophages pack their double-stranded DNA genomes to near-crystalline density and achieve one of the highest levels of DNA condensation found in nature. Despite numerous studies, some essential properties of the packaging geometry of the DNA inside the phage capsid are still unknown. We present a different approach to the problems of randomness and chirality of the packed DNA. We recently showed that most DNA molecules extracted from bacteriophage P4 are highly knotted because of the cyclization of the linear DNA molecule confined in the phage capsid. Here, we show that these knots provide information about the global arrangement of the DNA inside the capsid. First, we analyze the distribution of the viral DNA knots by high-resolution gel electrophoresis. Next, we perform Monte Carlo computer simulations of random knotting for freely jointed polygons confined to spherical volumes. Comparison of the knot distributions obtained by both techniques produces a topological proof of nonrandom packaging of the viral DNA. Moreover, our simulations show that the scarcity of the achiral knot 41 and the predominance of the torus knot 51 over the twist knot 52 observed in the viral distribution of DNA knots cannot be obtained by confinement alone but must include writhe bias in the conformation sampling. These results indicate that the packaging geometry of the DNA inside the viral capsid is writhe-directed.bacteriophage ͉ DNA condensation ͉ DNA electrophoresis ͉ Monte Carlo simulation ͉ DNA writhe A ll icosahedral bacteriophages with double-stranded DNA genomes are believed to pack their chromosomes in a similar manner (1). During phage morphogenesis, a procapsid is first assembled, and a linear DNA molecule is actively introduced inside it by the connector complex (2, 3). At the end of this process, the DNA and its associated water molecules fill the entire capsid volume, where DNA reaches concentrations of 800 mg͞ml (4). Some animal viruses (5) and lipo-DNA complexes used in gene therapy (6) are postulated to hold similar DNA arrangements as those found in bacteriophages.Although numerous studies have investigated the DNA packing geometry inside phage capsids, some of its properties remain unknown. Biochemical and structural analyses have revealed that DNA is kept in its B form (7-9) and that there are no specific DNA-protein interactions (10, 11) or correlation between DNA sequences and their spatial location inside the capsid, with the exception of the cos ends in some viruses (12). Many studies have found that regions of the packed DNA form domains of parallel fibers, which in some cases have different orientations, suggesting a certain degree of randomness (8,9,13,14). The above observations have led to the proposal of several long-range organization models for DNA inside phage capsids: the ball of string model (13), the coaxial spooling model (8,11,13,14), the spiral-fold model (15), and the folded toroidal model (16). Liquid crystalline models, which take into account properties of DNA at high concen...

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mentioning

confidence: 62%

“…Bacteriophage P4 vir1 del22 was prepared as described in ref. 22. Briefly, the phage was amplified in Escherichia coli strain C-1895, which is lysogenic for P2 (the helper prophage).…”

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

DNA knots reveal a chiral organization of DNA in phage capsids

Arsuaga

Vázquez

McGuirk

et al. 2005

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

Self Cite

231

282

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“…Sufficiently long polymers, such as DNA, are likely to be entangled [1,2]. On the other hand, there are very few knotted RNA molecules -in a recent assessment [3] only three cases have been identified, but the corresponding structures are resolved poorly.…”

Section: Introductionmentioning

confidence: 99%

Multiple folding pathways of proteins with shallow knots and co-translational folding

Chwastyk

Cieplak

2015

The Journal of Chemical Physics

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We study the folding process in the shallowly knotted protein MJ0366 within two variants of a structure-based model. We observe that the resulting topological pathways are much richer than identified in previous studies. In addition to the single knot-loop events, we find novel, and dominant, two-loop mechanisms. We demonstrate that folding takes place in a range of temperatures and the conditions of most successful folding are at temperatures which are higher than those required for the fastest folding. We also demonstrate that nascent conditions are more favorable to knotting than off-ribosome folding.

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“…Arsuaga et al showed that the tight geometric confinement the genome is subjected to is a significant contributor to the knot formation [7,17]. Such bacteriophages are the "viruses of bacteria", and they work by releasing their DNA into the cytosol of their host.…”

Section: Introductionmentioning

confidence: 99%

Sedimentation of knotted polymers

et al. 2013

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We investigate the sedimentation of knotted polymers by means of stochastic rotation dynamics, a molecular dynamics algorithm that takes hydrodynamics fully into account. We show that the sedimentation coefficient s, related to the terminal velocity of the knotted polymers, increases linearly with the average crossing number nc of the corresponding ideal knot. To the best of our knowledge, this provides the first direct computational confirmation of this relation, postulated on the basis of experiments in Ref.[1], for the case of sedimentation. Such a relation was previously shown to hold with simulations for knot electrophoresis. We also show that there is an accurate linear dependence of s on the inverse of the radius of gyration R −1 g , more specifically with the inverse of the Rg component that is perpendicular to the direction along which the polymer sediments. When the polymer sediments in a slab, the walls affect the results appreciably. However, R −1 g remains to a good precision linearly dependent on nc. Therefore, R −1 g is a good measure of a knot's complexity.

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Knotting probability of DNA molecules confined in restricted volumes: DNA knotting in phage capsids

Cited by 245 publications

References 42 publications

DNA knots reveal a chiral organization of DNA in phage capsids

DNA knots reveal a chiral organization of DNA in phage capsids

Multiple folding pathways of proteins with shallow knots and co-translational folding

Sedimentation of knotted polymers

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