ATP-Independent Cooperative Binding of Yeast Isw1a to Bare and Nucleosomal DNA
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{"title"=>"ATP-independent cooperative binding of yeast Isw1a to bare and nucleosomal DNA", "type"=>"journal", "authors"=>[{"first_name"=>"Anne", "last_name"=>"de Cian", "scopus_author_id"=>"8769330500"}, {"first_name"=>"Elise", "last_name"=>"Praly", "scopus_author_id"=>"12041750600"}, {"first_name"=>"Fangyuan", "last_name"=>"Ding", "scopus_author_id"=>"35195551700"}, {"first_name"=>"Vijender", "last_name"=>"Singh", "scopus_author_id"=>"55195443200"}, {"first_name"=>"Christophe", "last_name"=>"Lavelle", "scopus_author_id"=>"12794558400"}, {"first_name"=>"Eric", "last_name"=>"Cam", "scopus_author_id"=>"7004170524"}, {"first_name"=>"Vincent", "last_name"=>"Croquette", "scopus_author_id"=>"7003635823"}, {"first_name"=>"Olivier", "last_name"=>"Piétrement", "scopus_author_id"=>"6602491422"}, {"first_name"=>"David", "last_name"=>"Bensimon", "scopus_author_id"=>"7004247047"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"22359636", "doi"=>"10.1371/journal.pone.0031845", "sgr"=>"84857126330", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-84857126330", "issn"=>"19326203", "pui"=>"364271837"}, "id"=>"d1061590-40f3-369a-988e-e1428ca796ce", "abstract"=>"Among chromatin remodeling factors, the ISWI family displays a nucleosome-enhanced ATPase activity coupled to DNA translocation. While these enzymes are known to bind to DNA, their activity has not been fully characterized. Here we use TEM imaging and single molecule manipulation to investigate the interaction between DNA and yeast Isw1a. We show that Isw1a displays a highly cooperative ATP-independent binding to and bridging between DNA segments. Under appropriate tension, rare single nucleation events can sometimes be observed and loop DNA with a regular step. These nucleation events are often followed by binding of successive complexes bridging between nearby DNA segments in a zipper-like fashion, as confirmed by TEM observations. On nucleosomal substrates, we show that the specific ATP-dependent remodeling activity occurs in the context of cooperative Isw1a complexes bridging extranucleosomal DNA. Our results are interpreted in the context of the recently published partial structure of Isw1a and support its acting as a \"protein ruler\" (with possibly more than one tick).", "link"=>"http://www.mendeley.com/research/atpindependent-cooperative-binding-yeast-isw1a-bare-nucleosomal-dna", "reader_count"=>27, "reader_count_by_academic_status"=>{"Researcher"=>15, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>8, "Other"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Researcher"=>15, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>8, "Other"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>18, "Physics and Astronomy"=>2, "Chemistry"=>2, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}}, "reader_count_by_country"=>{"France"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/681617"], "description"=>"<p>(A) Scheme of a torsion experiment when the DNA molecule is not nicked (no ATP). (B) Simultaneous recordings of the extension of two DNA molecules (one nicked and one not) in the presence of Isw1a (F = 1.1 pN) as a function of the number of rotations <i>n</i> of the pulling magnets (upper continuous trace). While the extension of the nicked DNA molecule (upper trace) remains constant as the magnets are rotated, the extension of the unnicked one (lower trace) decreases rapidly once it buckles to form supercoiled (i.e. when <i>n</i> = +10 turns). (C) (i) Extension-versus-rotation curve at 0.4 pN for an unnicked DNA molecule. (ii) Recording of the extension of the same molecule in the presence of Isw1a while imposing either +6 or −6 turns. The extension of the molecule (ℓ<sub>F</sub> (±6) is reduced by a similar amount whether the molecule is rotated by +6 or −6 turns. (iii) Histogram of the mean difference in extension between successive ±6 turns (ℓ<sub>F</sub> (+6)−ℓ<sub>F</sub> (−6)) in the presence of Isw1a. The histogram is gaussianly distributed with a mean value of −39±31 nm.</p>", "links"=>[], "tags"=>["isw1a", "binding", "dna"], "article_id"=>352094, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031845.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_Isw1a_binding_on_DNA_twist_/352094", "title"=>"Effect of Isw1a binding on DNA twist.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-16 00:34:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/681418"], "description"=>"<p>(A) Schematic drawing of the experiment monitoring individual Isw1a binding events. (B) Recordings (averaged over 0.5 s) of the extension of three nicked DNA molecules of extension ℓ<sub>F</sub>∼1.2 µm, in the presence of Isw1a and without ATP. Successive increases (or shortenings) of the extension are observed as the force is increased (decreased) above (below) ∼1 pN, each of them being a multiple of δℓ = δℓ<sub>F</sub>/λ<sub>W LC</sub>∼30 nm. These variations in length are attributed to the binding or the unbinding of one or more Isw1a complexes. (C) Size distribution of δℓ for 215 events, for forces comprised between 0.33 and 3.8 pN.</p>", "links"=>[], "tags"=>["variations", "induced", "isw1a", "binding"], "article_id"=>351899, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031845.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_variations_in_length_induced_by_Isw1a_binding_and_unbinding_/351899", "title"=>"DNA variations in length induced by Isw1a binding and unbinding.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-16 00:31:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/681530"], "description"=>"<p>(A) Cooperative binding and bridging of Isw1a along DNA molecules on linear DNA at 140000× magnification. Control DNA (i), reacted with Isw1a 50 nM (ii) and Isw1a 250 nM followed by gel filtration purification (iii) are presented here. (B) Binding and bridging of Isw1a along DNA molecules (−) scDNA at 140000× magnifications. Control DNAs (i), reacted with Isw1a 50 nM (ii) and Isw1a 250 nM followed by gel filtration purification (iii) are presented here. (C) Panels (i) and (ii) corresponds to the 50-fold dilution in pure H<sub>2</sub>O of 0 or 50 nM Isw1a binding on (−) scDNA presented in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031845#pone-0031845-g003\" target=\"_blank\">Figures 3B (a) and 3B (b</a>), respectively. White arrows show Isw1a binding at apexes. For all images, scale bars represent 100 nm.</p>", "links"=>[], "tags"=>["isw1a", "linear", "negatively", "supercoiled"], "article_id"=>352008, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031845.g003", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Binding_of_Isw1a_on_linear_and_negatively_supercoiled_DNA_/352008", "title"=>"Binding of Isw1a on linear and negatively supercoiled DNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-16 00:33:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/681723"], "description"=>"<p>(A) Scheme of the experiments testing the binding in absence of ATP of Isw1a to two braided DNA molecules. (B) Recordings of the extension (dots) of two molecules braided by (i) −1 or (ii) +1 turn, in the presence of Isw1a at F = 0.9 pN. The continuous black line shows the amount of braiding (number of magnets rotations). The red curve corresponds to an average of the raw data over 0.25 s. Notice that in both cases following a return to zero rotation of the magnets (unbraiding of the DNA), the extension of the molecules increases back to its initial position albeit with a stochastic delay due to the transient bridging of the braid crossing by a single Isw1a molecule.</p>", "links"=>[], "tags"=>["bridging"], "article_id"=>352209, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031845.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_bridging_between_two_molecules_/352209", "title"=>"DNA bridging between two molecules.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-16 00:36:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/681925"], "description"=>"<p>(A) Schematic structure of Isw1a according to ref <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031845#pone.0031845-Yamada1\" target=\"_blank\">[46]</a>. The protein chain connecting HAND and ATPase domain is flexible, which may contributes to chromatin remodelling. (B) The formation of the Isw1a fiber on stretched DNA could proceed in successive steps: (i) binding/unbinding of a single nucleating complex which grows by binding of additional complexes ending in a zipped-up DNA molecule (ii–iii). A typical time trace taken at 0.7 pN of the extension of a DNA molecule in presence of Isw1a (without ATP) is shown. The dashed lines correspond to the change in extension upon addition of a single complex deduced from the measurements shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0031845#pone-0031845-g002\" target=\"_blank\">Figure 2</a>. (C) On nucleosomal substrate, the nucleation of Isw1a (i) may proceed from the vicinity of the nucleosome where the two DNA flanking regions provide an adequate substrate for the nucleation of a Isw1a fiber that proceeds by bridging the two arms of the nucleosomal substrate. (ii–iv) In presence of ATP, the Isw1a protein close to the nucleosome generates a DNA deformation, which may weaken the Ioc3 and Isw1 interaction with DNA. Then, the other Isw1a units along the DNA zipper act as “wheels” that in presence of ATP translocate the DNA molecule as a chain in a conveyor belt. As the nucleosome is remodelled, one DNA arm length is decreasing and some of the Isw1a bridges are weakened resulting in fewer bridged molecules after remodelling. Dark blue and black sites represent strong DNA binding of Ioc3 and Isw1, respectively. Light blue and gray sites represent weak binding sites of Ioc3 and Isw1, respectively, allowing the propagation of the DNA deformation. White sites show previously linked sites and released by the different sub-domains of Isw1a.</p>", "links"=>[], "tags"=>["isw1a", "nucleosomal", "dna", "tweezers", "tem"], "article_id"=>352400, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031845.g007", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Possible_model_for_the_formation_of_an_Isw1a_fiber_along_bare_and_nucleosomal_DNA_in_magnetic_tweezers_and_TEM_experiments_/352400", "title"=>"Possible model for the formation of an Isw1a fiber along bare and nucleosomal DNA in magnetic tweezers and TEM experiments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-16 00:40:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/347592", "https://ndownloader.figshare.com/files/347639", "https://ndownloader.figshare.com/files/347696", "https://ndownloader.figshare.com/files/347745", "https://ndownloader.figshare.com/files/347829", "https://ndownloader.figshare.com/files/347881", "https://ndownloader.figshare.com/files/348015", "https://ndownloader.figshare.com/files/348087", "https://ndownloader.figshare.com/files/348164"], "description"=>"<div><p>Among chromatin remodeling factors, the ISWI family displays a nucleosome-enhanced ATPase activity coupled to DNA translocation. While these enzymes are known to bind to DNA, their activity has not been fully characterized. Here we use TEM imaging and single molecule manipulation to investigate the interaction between DNA and yeast Isw1a. We show that Isw1a displays a highly cooperative ATP-independent binding to and bridging between DNA segments. Under appropriate tension, rare single nucleation events can sometimes be observed and loop DNA with a regular step. These nucleation events are often followed by binding of successive complexes bridging between nearby DNA segments in a zipper-like fashion, as confirmed by TEM observations. On nucleosomal substrates, we show that the specific ATP-dependent remodeling activity occurs in the context of cooperative Isw1a complexes bridging extranucleosomal DNA. Our results are interpreted in the context of the recently published partial structure of Isw1a and support its acting as a “protein ruler” (with possibly more than one tick).</p> </div>", "links"=>[], "tags"=>["atp-independent", "binding", "yeast", "isw1a", "nucleosomal", "dna"], "article_id"=>128728, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031845.s001", "https://dx.doi.org/10.1371/journal.pone.0031845.s002", "https://dx.doi.org/10.1371/journal.pone.0031845.s003", "https://dx.doi.org/10.1371/journal.pone.0031845.s004", "https://dx.doi.org/10.1371/journal.pone.0031845.s005", "https://dx.doi.org/10.1371/journal.pone.0031845.s006", "https://dx.doi.org/10.1371/journal.pone.0031845.s007", "https://dx.doi.org/10.1371/journal.pone.0031845.s008", "https://dx.doi.org/10.1371/journal.pone.0031845.s009"], "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/ATP_Independent_Cooperative_Binding_of_Yeast_Isw1a_to_Bare_and_Nucleosomal_DNA/128728", "title"=>"ATP-Independent Cooperative Binding of Yeast Isw1a to Bare and Nucleosomal DNA", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-02-16 02:25:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/681319"], "description"=>"<p>(A) (i) Illustration of the magnetic tweezers experiment: the extension (ℓ<sub>F</sub>∼1.2 µm) of two DNA molecules stretched between the surface of a glass slide and a magnetic bead (labelled respectively bead 1 and bead 2) is monitored, in the presence of Isw1a (but without ATP). (ii) Typical image of these two particular beads. (iii) While the force is controlled (upper continuous trace), the resulting extension of the molecules is recorded. At F = 1.7 pN (trace (1)) and F = 1.0 pN (trace (2)), the two beads show restricted Brownian fluctuations about a mean value that varies with the stretching force. At 0.7 pN (trace (3)), while the length of the DNA bound to bead 2 is unchanged (except for a quick transient decrease at ∼430 sec blown up in the inset), the DNA anchored to bead 1 exhibits a rapid decrease in extension. (B) Representative TEM observations of a 4 kb linear DNA in absence (i) or presence of Isw1a (ii) without ATP. The reaction was carried out in 20 mM Tris-HCl pH 8, 30 mM KCl, 17.5 mM NaCl, 1 mM Hepes pH 7.6, 0.75% glycerol with 750 nM of DNA (in bps, ie 0.19 nM in molecule) and 20 nM of Isw1a for 20 min at 30°C. DNA collapse is observed on some DNA molecules in presence of Isw1a, while naked DNA molecules are still present. Scarce punctual binding (top right molecule) can also be seen (red arrow). Scale bar represents 200 nm.</p>", "links"=>[], "tags"=>["binding", "isw1a"], "article_id"=>351798, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031845.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cooperative_binding_of_Isw1a_to_DNA_/351798", "title"=>"Cooperative binding of Isw1a to DNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-16 00:29:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/681837"], "description"=>"<p>(A) Image of 845 bps mononucleosomal DNA containing a histone positioning 601 sequence and schematic drawing representing the lengths measured in the analysis: in the non-oriented experiment ℓ<sub>−</sub> represents the shortest DNA arm, ℓ<sub>+</sub> the longest. Representative images of mononucleosomes on 845 bps DNA with 10 nM of Isw1a in absence (B) or presence (C) of 75 µM of ATP. Scale bars represent 100 nm. (D) Relative nucleosome position probabilities calculated as the ratio of (ℓ<sub>−</sub>)/( ℓ<sub>+</sub>+ℓ<sub>−</sub>) for five different experimental conditions.</p>", "links"=>[], "tags"=>["remodeling"], "article_id"=>352321, "categories"=>["Physics", "Biochemistry", "Biophysics", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anne De Cian", "Elise Praly", "Fangyuan Ding", "Vijender Singh", "Christophe Lavelle", "Eric Le Cam", "Vincent Croquette", "Olivier Piétrement", "David Bensimon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031845.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Isw1a_remodeling_activity_on_a_single_nucleosome_/352321", "title"=>"Isw1a remodeling activity on a single nucleosome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-16 00:38:41"}

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Relative Metric

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