Nuclear Mitochondrial DNA Activates Replication in Saccharomyces cerevisiae
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{"title"=>"Nuclear mitochondrial DNA activates replication in Saccharomyces cerevisiae", "type"=>"journal", "authors"=>[{"first_name"=>"Laurent", "last_name"=>"Chatre", "scopus_author_id"=>"12772290600"}, {"first_name"=>"Miria", "last_name"=>"Ricchetti", "scopus_author_id"=>"6603811009"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"361404868", "sgr"=>"79952422045", "issn"=>"19326203", "pmid"=>"21408151", "scopus"=>"2-s2.0-79952422045", "doi"=>"10.1371/journal.pone.0017235", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"fc7f49e1-57fd-343e-8a9a-3f5149657d1d", "abstract"=>"The nuclear genome of eukaryotes is colonized by DNA fragments of mitochondrial origin, called NUMTs. These insertions have been associated with a variety of germ-line diseases in humans. The significance of this uptake of potentially dangerous sequences into the nuclear genome is unclear. Here we provide functional evidence that sequences of mitochondrial origin promote nuclear DNA replication in Saccharomyces cerevisiae. We show that NUMTs are rich in key autonomously replicating sequence (ARS) consensus motifs, whose mutation results in the reduction or loss of DNA replication activity. Furthermore, 2D-gel analysis of the mrc1 mutant exposed to hydroxyurea shows that several NUMTs function as late chromosomal origins. We also show that NUMTs located close to or within ARS provide key sequence elements for replication. Thus NUMTs can act as independent origins, when inserted in an appropriate genomic context or affect the efficiency of pre-existing origins. These findings show that migratory mitochondrial DNAs can impact on the replication of the nuclear region they are inserted in.", "link"=>"http://www.mendeley.com/research/nuclear-mitochondrial-dna-activates-replication-saccharomyces-cerevisiae", "reader_count"=>32, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>11, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>9, "Student > Master"=>2, "Other"=>2, "Student > Bachelor"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>11, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>9, "Student > Master"=>2, "Other"=>2, "Student > Bachelor"=>1, "Lecturer > Senior Lecturer"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>21, "Medicine and Dentistry"=>1, "Business, Management and Accounting"=>1, "Social Sciences"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>21}, "Computer Science"=>{"Computer Science"=>1}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}}, "reader_count_by_country"=>{"Sweden"=>1, "Turkey"=>1, "United States"=>1, "France"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/793257"], "description"=>"<p>Transformation efficiency (upper panels) and plasmid loss rate (middle panels) of sequences containing different combinations of an ARS and a NUMT, full sequences or various portions of them (schematized in the lower panels). NUMT13 (69 bp) overlaps by 39 bp the 5′ portion of ARS1215 (229 bp). NUMT30 (23 bp) is located in the middle of ARS1635 (231). NUMT14 (43 bp) is distant 387 bp from proARS408 (1349 bp); the definition of proARS is according to OriDB, since its activity has not been experimentally confirmed. For each of the three NUMT/ARS combinations, the full sequence and various portions of it (schematized in the lower panels) were analysed. For each construction, vectors pIRT2Δ (white bars) and pRS405 (grey bars) were used. The 17 bp ACS motif of NUMTs and ARS is indicated in red; no confirmed or predicted ACS element is reported for proARS408. A star indicates that the ACS motif has been replaced with a G+C rich region. The chromosomal coordinates of NUMTs and ARS are indicated; when portions of the full sequence are analysed, their coordinates are also indicated.</p>", "links"=>[], "tags"=>["numt", "ars", "containing"], "article_id"=>463628, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Laurent Chatre", "Miria Ricchetti"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017235.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Replication_efficiency_of_NUMT_in_ARS_containing_regions_/463628", "title"=>"Replication efficiency of NUMT in ARS containing regions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-08 01:00:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/793347"], "description"=>"<p>The table indicates the number of NUMTs, and the relative percentages, for each group of distances (bp), according to values shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone-0017235-t001\" target=\"_blank\">Table 1</a>.</p>", "links"=>[], "tags"=>["genetics and genomics", "microbiology", "molecular biology", "cell biology", "Evolutionary biology"], "article_id"=>463720, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Laurent Chatre", "Miria Ricchetti"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017235.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NUMT_ARS_distance_/463720", "title"=>"NUMT-ARS distance.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-03-08 01:02:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/793170"], "description"=>"<p>2D-gel electrophoresis visualizes replication events at NUMTs in wild-type (wt), <i>mrc1</i> and <i>rad53-11</i> strains. Cells were arrested in G1 with alpha-factor and then released into YPD medium for 25 min, 35 min or 50 min alone (upper part of the figure), or in the presence of 0.2 M HU for 60 min (lower part of the figure). A scheme of the migration pattern in 2D-gel electrophoresis is shown. The extremely efficient ARS305 was used as control. Star indicates bubble molecules (origin firing). Probes specific for the examined fragments were created by PCR amplification of the region of interest. Fragments examined: ARS305, <i>EcoR</i>I 5.8 Kbp; NUMT2, <i>Hind</i>III 4.5 Kbp; NUMT14, <i>Eco</i>RI 7.4 Kbp; NUMT28, PstI 7.7 Kbp; FY1679, <i>Hind</i>III 5.4 Kbp; 34pBE28, <i>Hind</i>III 3.3 Kbp; 34pAS7, <i>Hind</i>III 3.35 Kbp; 34pAS15, <i>Hind</i>III 3.54 Kbp. A colour scheme (right, below) indicates the position of the NUMT according to the <i>S. cerevisiae</i> replication profiles reported in reference <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone.0017235-Raghuraman1\" target=\"_blank\">[42]</a>. Yellow curve, replication time; peaks, origins of replication (early origins are higher); NUMTs, green circles; ARS, pink circles. ARS, named and indicated with a white arrow; NUMTs names, white rectangle. The distance between two ARS or between an ARS and a NUMT is indicated in kbp. CEN (a purple circle) corresponds to centromere; the Y-axe indicates “early” (top) and “late” (bottom) replication activity; trep, replication time in min. See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone.0017235.s006\" target=\"_blank\">Fig. S6</a> for the distribution of all NUMTs on replication profiles of the <i>S. cerevisiae</i> genome.</p>", "links"=>[], "tags"=>["gels", "replication", "intermediates", "chromosomes", "localization", "numts"], "article_id"=>463541, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Laurent Chatre", "Miria Ricchetti"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017235.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_2D_gels_analysis_of_replication_intermediates_in_chromosomes_and_localization_of_NUMTs_at_nuclear_replication_profiles_/463541", "title"=>"2D gels analysis of replication intermediates in chromosomes and localization of NUMTs at nuclear replication profiles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-08 00:59:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/396897", "https://ndownloader.figshare.com/files/396932", "https://ndownloader.figshare.com/files/396962", "https://ndownloader.figshare.com/files/396985", "https://ndownloader.figshare.com/files/397008", "https://ndownloader.figshare.com/files/397038", "https://ndownloader.figshare.com/files/397070", "https://ndownloader.figshare.com/files/397082", "https://ndownloader.figshare.com/files/397097", "https://ndownloader.figshare.com/files/397122", "https://ndownloader.figshare.com/files/397151", "https://ndownloader.figshare.com/files/397195", "https://ndownloader.figshare.com/files/397228", "https://ndownloader.figshare.com/files/397264", "https://ndownloader.figshare.com/files/397284"], "description"=>"<div><p>The nuclear genome of eukaryotes is colonized by DNA fragments of mitochondrial origin, called NUMTs. These insertions have been associated with a variety of germ-line diseases in humans. The significance of this uptake of potentially dangerous sequences into the nuclear genome is unclear. Here we provide functional evidence that sequences of mitochondrial origin promote nuclear DNA replication in <em>Saccharomyces cerevisiae</em>. We show that NUMTs are rich in key autonomously replicating sequence (ARS) consensus motifs, whose mutation results in the reduction or loss of DNA replication activity. Furthermore, 2D-gel analysis of the <em>mrc1</em> mutant exposed to hydroxyurea shows that several NUMTs function as late chromosomal origins. We also show that NUMTs located close to or within ARS provide key sequence elements for replication. Thus NUMTs can act as independent origins, when inserted in an appropriate genomic context or affect the efficiency of pre-existing origins. These findings show that migratory mitochondrial DNAs can impact on the replication of the nuclear region they are inserted in.</p> </div>", "links"=>[], "tags"=>["mitochondrial", "dna", "activates", "replication"], "article_id"=>138406, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Laurent Chatre", "Miria Ricchetti"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0017235.s001", "https://dx.doi.org/10.1371/journal.pone.0017235.s002", "https://dx.doi.org/10.1371/journal.pone.0017235.s003", "https://dx.doi.org/10.1371/journal.pone.0017235.s004", "https://dx.doi.org/10.1371/journal.pone.0017235.s005", "https://dx.doi.org/10.1371/journal.pone.0017235.s006", "https://dx.doi.org/10.1371/journal.pone.0017235.s007", "https://dx.doi.org/10.1371/journal.pone.0017235.s008", "https://dx.doi.org/10.1371/journal.pone.0017235.s009", "https://dx.doi.org/10.1371/journal.pone.0017235.s010", "https://dx.doi.org/10.1371/journal.pone.0017235.s011", "https://dx.doi.org/10.1371/journal.pone.0017235.s012", "https://dx.doi.org/10.1371/journal.pone.0017235.s013", "https://dx.doi.org/10.1371/journal.pone.0017235.s014", "https://dx.doi.org/10.1371/journal.pone.0017235.s015"], "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Nuclear_Mitochondrial_DNA_Activates_Replication_in_Saccharomyces_cerevisiae_/138406", "title"=>"Nuclear Mitochondrial DNA Activates Replication in <em>Saccharomyces cerevisiae</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-03-08 02:20:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/792909"], "description"=>"<p>(<b>A</b>) Density of ACS motifs within a given sequence. On the X-axis is indicated the type of sequence analysed, and on the Y-axis the percentage of the sequence (in bp) occupied by ACS motifs. Coloured dots indicate sequences that have been analysed in this study. In several cases the name of the sequence is indicated. Significantly different values for the group of <i>S. cerevisiae</i> NUMTs versus the group of genic and intergenic regions (p = 1.4×10<sup>−11</sup>) according to the t-Student test. (<b>B</b>) Sequence and position of the 17 bp ARS core-A motif (ACS) (rectangle) in several NUMTs. The sequence of confirmed ACS is shown below. A star indicates the ACS motif that has been mutated in this study. (<b>C</b>) Summary of the sequences, carrying either NUMT or non-NUMT sequences (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone.0017235.s009\" target=\"_blank\">Tables S1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone.0017235.s010\" target=\"_blank\">S2</a>), inserted in pIRT2Δ, pRS405 and pRS405-CEN. Nd = not identified; Sp = <i>S. pombe</i>. “v” indicates captured NUMTs <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone.0017235-Ricchetti1\" target=\"_blank\">[5]</a>. The nomenclature of yeast NUMTs is adapted from reference <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone.0017235-Ricchetti1\" target=\"_blank\">[5]</a>.</p>", "links"=>[], "tags"=>["origins", "replication"], "article_id"=>463280, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Laurent Chatre", "Miria Ricchetti"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017235.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Paradigm_to_investigate_origins_of_replication_in_Saccharomyces_cerevisiae_/463280", "title"=>"Paradigm to investigate origins of replication in <i>Saccharomyces cerevisiae</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-08 00:54:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/793047"], "description"=>"<p>Plasmid loss rate per generation measured in 6 independent transformants (circles) per construct (average ± standard deviation). When values are identical, only one circle is shown. (<b>A</b>) Analysis with vector pRS405. <i>ARS1</i> and <i>ARS121</i> are positive controls. The empty vector as well as the insertion of random control sequences are unable to promote plasmid replication, therefore they do not support colony growth (N.T., for no transformants). Insertion of an ARS or a NUMT sequence activates plasmid replication and colony growth, therefore plasmid loss rate was measurable in these samples. The size and the AT content of each sequence are indicated in the bottom (<b>B</b>) Analysis with vector pRS405-CEN, a pRS405 derivative that contains the centromeric region CEN4. (<b>C–D</b>) Replication activity with mutated ACS. Plasmid loss rate following ARS and NUMT mutagenesis (“m”) to replace the 17-bp ACS motif in vectors pRS405 and pRS405-CEN. A star shows a significant difference between the mutated sequence and the corresponding original sequence (n = 6; p<0.05, Mann-Whitney test) (<b>C</b>) Vector pRS405. Mutation of the motif in both ARS and in NUMT20 results in complete loss of replication activity (no transformants, N.T). Mutation of one or both ACS motifs in NUMT2 (shown in dark rectangles in the scheme below) results in a progressive increase in plasmid loss rate. (<b>D</b>) Vector pRS405-CEN. Mutation of the motif in both ARS and in NUMT20 results in complete loss of replication activity (no transformants, N.T). Mutation of one or both ACS motifs in NUMT2 results in a progressive increase in plasmid loss rate.</p>", "links"=>[], "tags"=>["carrying", "numts"], "article_id"=>463421, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Laurent Chatre", "Miria Ricchetti"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017235.g002", "stats"=>{"downloads"=>3, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Plasmids_carrying_NUMTs_display_low_loss_rate_in_yeast_/463421", "title"=>"Plasmids carrying NUMTs display low loss rate in yeast.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-08 00:57:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/793370"], "description"=>"<p>Summary of the presence of NUMT at replication origins. This table summarize data presented in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0017235#pone.0017235.s013\" target=\"_blank\">Table S5</a>. The first column indicates the NUMT, and the second column the presence of the NUMT at replication origin according to one or more tests (the type of test is indicated). The third column indicates the distence (in bp) between the NUMT and the closest ARS element. The last column indicates the type of ARS, according to OriDB:“ confirmed” are origins that have been detected by ARS assay or 2D-gels, “likely” ARS are probable origins identified by two or more microarray studies and “dubious” are sites proposed to be origin only by one microarray-based study. Lines in bold (22/34) indicate NUMTs located at replication origins. Since multiple insertions occurred at some <i>loci</i>, the number of loci with NUMT(s) is 28, while individual NUMTs are 34.</p>", "links"=>[], "tags"=>["replication"], "article_id"=>463748, "categories"=>["Molecular Biology", "Cell Biology", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Laurent Chatre", "Miria Ricchetti"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0017235.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NUMTs_and_replication_origins_/463748", "title"=>"NUMTs and replication origins.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-03-08 01:02:28"}

PMC Usage Stats | Further Information

  • {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"6", "full-text"=>"28", "unique-ip"=>"36", "pdf"=>"22", "year"=>"2011", "figure"=>"11", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"11", "full-text"=>"43", "year"=>"2011", "pdf"=>"31", "unique-ip"=>"52", "figure"=>"13", "scanned-summary"=>"0", "supp-data"=>"7"}
  • {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"2", "full-text"=>"22", "unique-ip"=>"28", "pdf"=>"13", "year"=>"2011", "figure"=>"15", "scanned-summary"=>"0", "supp-data"=>"1"}
  • {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"9", "year"=>"2011", "pdf"=>"4", "unique-ip"=>"11", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"7", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"13", "unique-ip"=>"15", "pdf"=>"2", "year"=>"2011", "figure"=>"3", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"8", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"13", "year"=>"2011", "pdf"=>"6", "unique-ip"=>"14", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"9", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"17", "unique-ip"=>"13", "pdf"=>"3", "year"=>"2011", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"10", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"16", "year"=>"2011", "pdf"=>"6", "unique-ip"=>"17", "figure"=>"5", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"11", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"15", "unique-ip"=>"14", "pdf"=>"1", "year"=>"2011", "figure"=>"3", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"12", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"14", "year"=>"2011", "pdf"=>"5", "unique-ip"=>"13", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"1"}
  • {"scanned-page-browse"=>"0", "month"=>"1", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"3", "unique-ip"=>"7", "pdf"=>"1", "year"=>"2012", "figure"=>"6", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"2", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"44", "year"=>"2012", "pdf"=>"4", "unique-ip"=>"33", "figure"=>"25", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"3", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"24", "unique-ip"=>"23", "pdf"=>"8", "year"=>"2012", "figure"=>"9", "scanned-summary"=>"0", "supp-data"=>"2"}
  • {"month"=>"4", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"7", "year"=>"2012", "pdf"=>"3", "unique-ip"=>"7", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"5", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"8", "unique-ip"=>"9", "pdf"=>"4", "year"=>"2012", "figure"=>"1", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"6", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "year"=>"2012", "pdf"=>"4", "unique-ip"=>"6", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"2", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2012", "month"=>"7"}
  • {"unique-ip"=>"12", "full-text"=>"13", "pdf"=>"5", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"12", "cited-by"=>"0", "year"=>"2012", "month"=>"8"}
  • {"unique-ip"=>"35", "full-text"=>"28", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"27", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2012", "month"=>"9"}
  • {"unique-ip"=>"18", "full-text"=>"19", "pdf"=>"9", "abstract"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2012", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2012", "month"=>"12"}
  • {"unique-ip"=>"12", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"4"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2012", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"15", "cited-by"=>"0", "year"=>"2013", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"4", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"6"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"15", "cited-by"=>"0", "year"=>"2013", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"15", "cited-by"=>"0", "year"=>"2013", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"14", "cited-by"=>"0", "year"=>"2013", "month"=>"10"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2013", "month"=>"11"}
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