Relevance of Simultaneous Mono-Ubiquitinations of Multiple Units of PCNA Homo-Trimers in DNA Damage Tolerance
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{"title"=>"Relevance of simultaneous mono-ubiquitinations of multiple units of PCNA homo-trimers in DNA damage tolerance", "type"=>"journal", "authors"=>[{"first_name"=>"Rie", "last_name"=>"Kanao", "scopus_author_id"=>"14832598100"}, {"first_name"=>"Yuji", "last_name"=>"Masuda", "scopus_author_id"=>"35248563400"}, {"first_name"=>"Saori", "last_name"=>"Deguchi", "scopus_author_id"=>"56524979300"}, {"first_name"=>"Mayumi", "last_name"=>"Yumoto-Sugimoto", "scopus_author_id"=>"56525243400"}, {"first_name"=>"Fumio", "last_name"=>"Hanaoka", "scopus_author_id"=>"35400560900"}, {"first_name"=>"Chikahide", "last_name"=>"Masutani", "scopus_author_id"=>"35403228400"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84923313708", "doi"=>"10.1371/journal.pone.0118775", "pui"=>"602339356", "pmid"=>"25692884", "scopus"=>"2-s2.0-84923313708", "issn"=>"19326203"}, "id"=>"0518f663-8b15-351d-a477-6fb82a412058", "abstract"=>"DNA damage tolerance (DDT) pathways, including translesion synthesis (TLS) and additional unknown mechanisms, enable recovery from replication arrest at DNA lesions. DDT pathways are regulated by post-translational modifications of proliferating cell nuclear antigen (PCNA) at its K164 residue. In particular, mono-ubiquitination by the ubiquitin ligase RAD18 is crucial for Polη-mediated TLS. Although the importance of modifications of PCNA to DDT pathways is well known, the relevance of its homo-trimer form, in which three K164 residues are present in a single ring, remains to be elucidated. Here, we show that multiple units of a PCNA homo-trimer are simultaneously mono-ubiquitinated in vitro and in vivo. RAD18 catalyzed sequential mono-ubiquitinations of multiple units of a PCNA homo-trimer in a reconstituted system. Exogenous PCNA formed hetero-trimers with endogenous PCNA in WI38VA13 cell transformants. When K164R-mutated PCNA was expressed in these cells at levels that depleted endogenous PCNA homo-trimers, multiple modifications of PCNA complexes were reduced and the cells showed defects in DDT after UV irradiation. Notably, ectopic expression of mutant PCNA increased the UV sensitivities of Polη-proficient, Polη-deficient, and REV1-depleted cells, suggesting the disruption of a DDT pathway distinct from the Polη- and REV1-mediated pathways. These results suggest that simultaneous modifications of multiple units of a PCNA homo-trimer are required for a certain DDT pathway in human cells.", "link"=>"http://www.mendeley.com/research/relevance-simultaneous-monoubiquitinations-multiple-units-pcna-homotrimers-dna-damage-tolerance", "reader_count"=>17, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Master"=>3, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Master"=>3, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>9, "Materials Science"=>1, "Agricultural and Biological Sciences"=>5}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Japan"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1910332", "https://ndownloader.figshare.com/files/1910333", "https://ndownloader.figshare.com/files/1910334", "https://ndownloader.figshare.com/files/1910335"], "description"=>"<div><p>DNA damage tolerance (DDT) pathways, including translesion synthesis (TLS) and additional unknown mechanisms, enable recovery from replication arrest at DNA lesions. DDT pathways are regulated by post-translational modifications of proliferating cell nuclear antigen (PCNA) at its K164 residue. In particular, mono-ubiquitination by the ubiquitin ligase RAD18 is crucial for Polη-mediated TLS. Although the importance of modifications of PCNA to DDT pathways is well known, the relevance of its homo-trimer form, in which three K164 residues are present in a single ring, remains to be elucidated. Here, we show that multiple units of a PCNA homo-trimer are simultaneously mono-ubiquitinated <i>in vitro</i> and <i>in vivo</i>. RAD18 catalyzed sequential mono-ubiquitinations of multiple units of a PCNA homo-trimer in a reconstituted system. Exogenous PCNA formed hetero-trimers with endogenous PCNA in WI38VA13 cell transformants. When K164R-mutated PCNA was expressed in these cells at levels that depleted endogenous PCNA homo-trimers, multiple modifications of PCNA complexes were reduced and the cells showed defects in DDT after UV irradiation. Notably, ectopic expression of mutant PCNA increased the UV sensitivities of Polη-proficient, Polη-deficient, and REV1-depleted cells, suggesting the disruption of a DDT pathway distinct from the Polη- and REV1-mediated pathways. These results suggest that simultaneous modifications of multiple units of a PCNA homo-trimer are required for a certain DDT pathway in human cells.</p></div>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311872, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0118775.s001", "https://dx.doi.org/10.1371/journal.pone.0118775.s002", "https://dx.doi.org/10.1371/journal.pone.0118775.s003", "https://dx.doi.org/10.1371/journal.pone.0118775.s004"], "stats"=>{"downloads"=>5, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relevance_of_Simultaneous_Mono_Ubiquitinations_of_Multiple_Units_of_PCNA_Homo_Trimers_in_DNA_Damage_Tolerance_/1311872", "title"=>"Relevance of Simultaneous Mono-Ubiquitinations of Multiple Units of PCNA Homo-Trimers in DNA Damage Tolerance", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910313"], "description"=>"<p>(A, B) The results of an <i>in vitro</i> mono-ubiquitination assay of triple-tagged PCNA hetero-trimers performed using purified RAD6-RAD18. The yellow and green shapes indicate wild-type (WT) and K164R (KR) PCNA molecules, respectively. (A) Immunoblot analysis using an anti-FLAG antibody of PCNA complexes containing a WT monomer that was or was not ubiquitinated. (B) The ratios of ubiquitinated to total FLAG-PCNA at the indicated time points. Data are represented as the mean ± standard deviation (SD) of n = 3 independent experiments. (C, D) The results of an <i>in vitro</i> mono-ubiquitination assay of a PCNA hetero-trimer consisting of one modifiable (WT) unit and two unmodifiable (K164R) units, and a 1:2 ratio of WT and K164R PCNA homo-trimers. (C) Immunoblot analysis using an anti-PCNA antibody. (D) The ratios of ubiquitinated to total PCNA at the indicated time points.</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311853, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g001", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PCNA_homo_trimers_undergo_multiple_mono_ubiquitinations_in_vitro_/1311853", "title"=>"PCNA homo-trimers undergo multiple-mono-ubiquitinations <i>in vitro</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910321"], "description"=>"<p>PCNA-wild-type (WT) and PCNA[KR] cells were transfected with empty vector (v) or FLAG-Polη (η) or FLAG-RAD18 (18) expression constructs. (A) Cells were mock-irradiated (UV-) or irradiated with 15 J/m<sup>2</sup> UVC (UV+), incubated for 3 h, and then subjected to immunoblotting using an anti-PCNA, anti-Polη, anti-RAD18, and anti-Lamin B antibodies. (B) Cells were co-transfected with GFP and empty vector or the FLAG-Polη or FLAG-RAD18 expression construct, and then treated with 2.5 mM thymidine for 24 h to concentrate the G1/S-phase populations. The cells were then mock-irradiated (UV-) or irradiated with 8 J/m<sup>2</sup> UV and cultured for the indicated periods. The cell-cycle profiles of the GFP-positive populations were determined by FACS analysis. The percentages of cells in the S-phase populations at the 12 h time point are indicated. (C) Cells were co-transfected with His-Ub and empty vector (v) or the FLAG-Polη (η) expression construct, mock-irradiated (-) or irradiated with 15 J/m<sup>2</sup> UVC (+), and then incubated for 3 h. Ni-pull-down assays were performed using the chromatin fractions (10% input) and samples were analyzed by immunoblotting using an anti-PCNA or anti-Polη antibody.</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311861, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g007", "stats"=>{"downloads"=>14, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Forced_increase_of_mono_ubiquitinated_PCNA_does_not_restore_the_DDT_defects_of_PCNA_KR_cells_/1311861", "title"=>"Forced increase of mono-ubiquitinated PCNA does not restore the DDT defects of PCNA[KR] cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910320"], "description"=>"<p>(A) Immunoprecipitation assays showing the formation of hetero-trimers of exogenous PCNA[KR] and endogenous PCNA in WI38VA13 cell transformants. The chromatin fractions (20% input) prepared from vector-transfected cells (v) and cells expressing varying levels of HA-PCNA[KR] (clone #1 = #2 > #3) were immunoprecipitated using an anti-HA antibody and then analyzed by immunoblotting using an anti-PCNA, anti-HA, or anti-Lamin B (control) antibody. The whole cell lysates (WCLs) and 20% unbound samples were also analyzed. The ratios of the signal intensities of endogenous PCNA detected in the unbound fractions of clones #1, #2, and #3 to control cells (v) are indicated below the upper panel. (B) Cell-cycle progression analyses of vector-transfected WI38VA13 cells and the HA-PCNA[KR] clone #1, #2 and #3 cells. The cells were synchronized by the double thymidine block method, mock-irradiated (UV-) or irradiated with 8 J/m<sup>2</sup> UVC (UV+) at the released time point, and then incubated for the indicated periods. The cell-cycle profiles were obtained by FACS analysis. The percentages of cells in the S-phase at the 15 h time point are indicated.</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311860, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g006", "stats"=>{"downloads"=>2, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ectopic_K164R_mutated_PCNA_forms_hetero_trimers_with_endogenous_PCNA_depletes_endogenous_PCNA_homo_trimers_and_disturbs_DDT_/1311860", "title"=>"Ectopic K164R-mutated PCNA forms hetero-trimers with endogenous PCNA, depletes endogenous PCNA homo-trimers, and disturbs DDT.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910317"], "description"=>"<p>The sensitivities of WI38VA13-derived cells to UV irradiation (A) or cisplatin (Cis-Pt) (B) with and without siRNA-mediated knockdown of endogenous PCNA (siPCNA). Clonogenic survival rates were determined after UVC irradiation or cisplatin treatment (24 h) of the indicated cell strains. Data are represented as the mean ± standard deviation of n = 3 independent experiments.</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311857, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g004", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PCNA_KR_cells_are_sensitive_to_DNA_damaging_agents_/1311857", "title"=>"PCNA[KR] cells are sensitive to DNA-damaging agents.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910315"], "description"=>"<p>The results of a pull-down assay using stably-expressed His-Ub. WI38VA13 cells stably expressing His-Ub (His-Ub) or vector-transfected control (vec) were mock-irradiated (-) or irradiated with 15 J/m<sup>2</sup> UVC (+) and incubated for 3 h. Ni-pull-down assays were performed using the chromatin fractions (2% input) and samples were analyzed by immunoblotting using an anti-PCNA or anti-Ub antibody. WCL, whole cell lysate.</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311855, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g002", "stats"=>{"downloads"=>2, "page_views"=>47, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PCNA_homo_trimers_undergo_multiple_mono_ubiquitinations_in_vivo_/1311855", "title"=>"PCNA homo-trimers undergo multiple-mono-ubiquitinations <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910316"], "description"=>"<p>(A) Immunoblot analyses of endogenous and ectopically expressed PCNA in vector-transfected, PCNA-wild-type (WT)-expressing and PCNA[KR]-expressing WI38VA13 cells that were untreated (untreat) or transfected with a nontargeting control (NTC) or PCNA-specific (siPCNA) siRNA. Four days after transfection, the cells were mock-irradiated (UV-) or irradiated with UVC at 10 J/m<sup>2</sup> (UV+), and then incubated for a further 3 h. Lamin B was detected as a loading control. (B) Ni-pull-down assay of PCNA-WT and PCNA[KR] cells transiently transfected with empty vector (vec) or the His-Ub expression construct (His-Ub). The cells were incubated for 36 h, mock-irradiated (-) or irradiated with 15 J/m<sup>2</sup> UVC (+), and then incubated for a further 3 h. Ni-pull-down assays were performed using the chromatin fractions (5% input) and samples were analyzed by immunoblotting using an anti-PCNA or anti-Ub antibody. WCL, whole cell lysate.</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311856, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g003", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ectopic_expression_of_K164R_mutated_PCNA_disturbs_multiple_mono_ubiquitinations_of_PCNA_trimers_in_human_cells_/1311856", "title"=>"Ectopic expression of K164R-mutated PCNA disturbs multiple mono-ubiquitinations of PCNA trimers in human cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910322"], "description"=>"<p>(A) Immunoblot analyses of PCNA expression in Polη-deficient XP2SASV3 cells stably expressing empty vector (vec), HA-PCNA-wild-type (WT) or HA-PCNA[KR] (KR). The cells were mock-irradiated (UV-) or irradiated with UVC at 10 J/m<sup>2</sup> (UV+) and then incubated for 3 h. Whole cell lysates were analyzed by immunoblotting using an anti-PCNA or anti-Lamin B (control) antibody. (B) The UVC sensitivities of Polη-deficient XP2SASV3-derived cells (XP-V) expressing empty vector, HA-PCNA-WT or HA-PCNA[KR] after treatment with an siRNA to knockdown endogenous PCNA (siPCNA) or a nontargeting control siRNA (NTC). Data are represented as the mean ± standard deviation (SD) of n = 3 independent experiments. (C) GFP-Polη was transiently expressed in WI38VA13/PCNA-WT or WI38VA13/PCNA[KR] cells treated with an siPCNA or a NTC. The cells were irradiated with 15 J/m<sup>2</sup> UVC and then incubated for 3 h. After extraction of Triton-soluble materials and fixation, PCNA was detected using an anti-PCNA antibody and nuclei were visualized by Hoechst 33342 staining. A typical nucleus of each cell type is shown. (D) Immunoblot analyses of REV1 and Lamin B (control) expression in WI38VA13 cells expressing empty vector (vec), PCNA-WT (WT) or PCNA[KR] (KR), and transfected with or without a REV1-specific siRNA. Four days after transfection, whole cell lysates were analyzed by immunoblotting using an anti-REV1 or anti-Lamin B antibody. (E) The effects of knockdown of REV1 on the UV sensitivities of the cells described in (D). The ratios of surviving cells exposed to 8 J/m<sup>2</sup> of UVC irradiation to those that were mock-irradiated were determined. The survival rates of the cells that were not treated with the REV1-specific siRNA (untreat) were taken from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0118775#pone.0118775.g004\" target=\"_blank\">Fig. 4A</a>. Data are represented as the mean ± SD of n = 3 independent experiments. (F) Schematic illustration of PCNA mono-ubiquitination-mediated DDT pathways in human cells.</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311862, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g008", "stats"=>{"downloads"=>3, "page_views"=>98, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_DDT_pathway_disturbed_by_expression_of_PCNA_KR_is_distinct_from_Pol_951_and_Rev1_mediated_TLS_/1311862", "title"=>"The DDT pathway disturbed by expression of PCNA[KR] is distinct from Polη- and Rev1-mediated TLS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/1910319"], "description"=>"<p>(A, B) S-phase progression analysis. Vector-transfected, PCNA-wild-type (WT) or PCNA[KR] WI38VA13 cells were synchronized using the double thymidine block method, mock-irradiated (UV-) or irradiated with UVC at the released time point, and then incubated for the indicated periods prior to FACS analysis of the cell-cycle profile. (C) Immunoblot analysis of CHK1 phosphorylation. Cells were irradiated with 10 J/m<sup>2</sup> UVC and incubated for the indicated periods. Immunoblotting was performed using anti-phospho-CHK1 (Ser345), anti-CHK1 and anti-actin antibodies. (D) Analysis of γH2AX-positive populations. The indicated cells were irradiated with 5 J/m<sup>2</sup> UVC and incubated for the indicated periods. The cells were then fixed and stained with an anti-γH2AX antibody (shown in red). Nuclei were visualized by Hoechst 33342 staining (shown in blue).</p>", "links"=>[], "tags"=>["WI 38VA cell transformants", "DDT pathway", "DNA Damage Tolerance DNA damage tolerance", "K 164 residues", "uv", "K 164R PCNA", "DDT pathways", "rev", "tls", "K 164 residue", "ubiquitin ligase RAD 18"], "article_id"=>1311859, "categories"=>["Biological Sciences"], "users"=>["Rie Kanao", "Yuji Masuda", "Saori Deguchi", "Mayumi Yumoto-Sugimoto", "Fumio Hanaoka", "Chikahide Masutani"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0118775.g005", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PCNA_KR_cells_show_DNA_replication_problems_after_UV_irradiation_/1311859", "title"=>"PCNA[KR] cells show DNA replication problems after UV irradiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-02-18 02:50:57"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"6", "cited-by"=>"0", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
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  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
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  • {"unique-ip"=>"8", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"7", "full-text"=>"17", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"13", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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