MMP9 Processing of HSPB1 Regulates Tumor Progression
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{"title"=>"MMP9 processing of HSPB1 regulates tumor progression", "type"=>"journal", "authors"=>[{"first_name"=>"Seo Hyun", "last_name"=>"Choi", "scopus_author_id"=>"24464183700"}, {"first_name"=>"Hae June", "last_name"=>"Lee", "scopus_author_id"=>"57195000661"}, {"first_name"=>"Yeung Bae", "last_name"=>"Jin", "scopus_author_id"=>"35344928700"}, {"first_name"=>"Junho", "last_name"=>"Jang", "scopus_author_id"=>"56645447500"}, {"first_name"=>"Ga Young", "last_name"=>"Kang", "scopus_author_id"=>"24481333200"}, {"first_name"=>"Minyoung", "last_name"=>"Lee", "scopus_author_id"=>"7409115789"}, {"first_name"=>"Chun Ho", "last_name"=>"Kim", "scopus_author_id"=>"16304279500"}, {"first_name"=>"Joon", "last_name"=>"Kim", "scopus_author_id"=>"7601371861"}, {"first_name"=>"Sam S.", "last_name"=>"Yoon", "scopus_author_id"=>"7404036067"}, {"first_name"=>"Yun Sil", "last_name"=>"Lee", "scopus_author_id"=>"17137192000"}, {"first_name"=>"Yoon Jin", "last_name"=>"Lee", "scopus_author_id"=>"55716141500"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"372852946", "doi"=>"10.1371/journal.pone.0085509", "sgr"=>"84908308383", "scopus"=>"2-s2.0-84908308383", "pmid"=>"24465581"}, "id"=>"6e8d0c63-1662-33ca-9427-7a7664356912", "abstract"=>"Matrix metalloproteinases regulate pathophysiological events by processing matrix proteins and secreted proteins. Previously, we demonstrated that soluble heat shock protein B1 (HSPB1) is released primarily from endothelial cells (ECs) and regulates angiogenesis via direct interaction with vascular endothelial growth factor (VEGF). Here we report that MMP9 can cleave HSPB1 and release anti-angiogenic fragments, which play a key role in tumorprogression. We mapped the cleavage sites and explored their physiological relevance during these processing events. HSPB1 cleavage by MMP9 inhibited VEGF-induced ECs activation and the C-terminal HSPB1 fragment exhibited more interaction with VEGF than did full-length HSPB1. HSPB1 cleavage occurs during B16F10 lung progression in wild-type mice. Also, intact HSPB1 was more detected on tumor endothelium of MMP9 null mice than wild type mice. Finally, we confirmed that secretion of C-terminal HSPB1 fragment was significantly inhibited lung and liver tumor progression of B16F10 melanoma cells and lung tumor progression of CT26 colon carcinoma cells, compared to full-length HSPB1. These data suggest that in vivo MMP9-mediated processing of HSPB1 acts to regulate VEGF-induced ECs activation for tumor progression, releasing anti-angiogenic HSPB1 fragments. Moreover, these findings potentially explain an anti-target effect for the failure of MMP inhibitors in clinical trials, suggesting that MMP inhibitors may have pro-tumorigenic effects by reducing HSPB1 fragmentation.", "link"=>"http://www.mendeley.com/research/mmp9-processing-hspb1-regulates-tumor-progression", "reader_count"=>23, "reader_count_by_academic_status"=>{"Librarian"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>9, "Student > Master"=>3, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Librarian"=>1, "Researcher"=>2, "Student > Ph. D. Student"=>9, "Student > Master"=>3, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Mathematics"=>1, "Agricultural and Biological Sciences"=>12, "Medicine and Dentistry"=>2, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1350960"], "description"=>"<p><b>A</b> Co-localization of HSBP1 and CD31 on tumor vessels in soft tissue sarcomas and lung adenocarcinomas derived from Kras<i><sup>LSL-G12D/WT</sup></i>; p53<i><sup>Flox/Flox</sup></i> mice was detected by immunofluorescence. <b>B</b> Tumor cells and tumor endothelial cells (ECs) were isolated from sarcomas and lung adenocarcinomas of Kras<i><sup>LSL-G12D/WT</sup></i>; p53<i><sup>Flox/Flox</sup></i> mice and cell lysates were analyzed by western blot. Secreted HSPB1 was detected in conditioned media (C.M.) from these cells. arrows, full length HSPB1; open arrows, cleaved HSPB1 <b>C</b> Serum HSPB1 levels in Kras<i><sup>LSL-G12D/WT</sup></i>; p53<i><sup>Flox/Flox</sup></i> mice with or without tumors were measured by ELISA assays for detecting intact HSPB1 as described in Methods; blue bars, anti-HSPB1 (10-21)+anti-HSPB1 (158-205) antibody. Red and green bars obtained from general ELISA assays using antibodies to the N- (10-21) or C-termini (158-201) of HSPB1 (*<i>P</i><0.05 and **<i>P</i><0.01 vs intact HSPB1).</p>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "hspb1", "secreted", "endothelial"], "article_id"=>903789, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509.g001", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Soluble_HSPB1_is_secreted_by_tumor_endothelial_cells_/903789", "title"=>"Soluble HSPB1 is secreted by tumor endothelial cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-20 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1350983"], "description"=>"<p><b>A</b> B16F10 melanoma cell lines were injected into the tail vein of wild-type and MMP9-null mice. 14 days later, lung tumor tissues were harvested. HSPB1 levels in the lung tissue samples were analyzed by western blotting using the HSPB1 (158–205) antibody. <b>B</b> Immunofluorescence staining of the N-terminal and C-terminal HSPB1 fragments in normal and B6F10 lung tissues using the HSPB1 (10–21) and (158–205) antibodies, respectively. <b>C</b> Lung tumor tissues were obtained via intravenous injection of B6F10 cells secreting wild-type HSPB1 into wild-type or MMP9-null mice. Immunoprecipitates with control IgG, anti-Flag, and anti-Myc in lysates of lung tumor tissues were subjected to western blot analysis using the indicated antibodies. <b>D</b> Immunofluorescence staining of the N-terminal and C-terminal HSPB1 fragments in B6F10 lung tumor tissues, using the Flag and Myc antibodies, respectively.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "cleavage", "mmp9", "occurs"], "article_id"=>903806, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509.g006", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HSPB1_cleavage_by_MMP9_occurs_during_tumor_progression_/903806", "title"=>"HSPB1 cleavage by MMP9 occurs during tumor progression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-20 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1350992"], "description"=>"<div><p>Matrix metalloproteinases regulate pathophysiological events by processing matrix proteins and secreted proteins. Previously, we demonstrated that soluble heat shock protein B1 (HSPB1) is released primarily from endothelial cells (ECs) and regulates angiogenesis via direct interaction with vascular endothelial growth factor (VEGF). Here we report that MMP9 can cleave HSPB1 and release anti-angiogenic fragments, which play a key role in tumorprogression. We mapped the cleavage sites and explored their physiological relevance during these processing events. HSPB1 cleavage by MMP9 inhibited VEGF-induced ECs activation and the C-terminal HSPB1 fragment exhibited more interaction with VEGF than did full-length HSPB1. HSPB1 cleavage occurs during B16F10 lung progression in wild-type mice. Also, intact HSPB1 was more detected on tumor endothelium of MMP9 null mice than wild type mice. Finally, we confirmed that secretion of C-terminal HSPB1 fragment was significantly inhibited lung and liver tumor progression of B16F10 melanoma cells and lung tumor progression of CT26 colon carcinoma cells, compared to full-length HSPB1. These data suggest that <i>in vivo</i> MMP9-mediated processing of HSPB1 acts to regulate VEGF-induced ECs activation for tumor progression, releasing anti-angiogenic HSPB1 fragments. Moreover, these findings potentially explain an anti-target effect for the failure of MMP inhibitors in clinical trials, suggesting that MMP inhibitors may have pro-tumorigenic effects by reducing HSPB1 fragmentation.</p></div>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "hspb1", "regulates"], "article_id"=>903815, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MMP9_Processing_of_HSPB1_Regulates_Tumor_Progression_/903815", "title"=>"MMP9 Processing of HSPB1 Regulates Tumor Progression", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-20 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1350974"], "description"=>"<p><b>A</b> HUVECs infected with MMP9 shRNA lentiviral and control vectors were pretreated for 30(1ug/ml) or rHSPB1 fragments (59–203; 1 µg/ml) and then incubated with VEGF (30 ng/mL). After 10 min, cell lysates and conditioned media were subjected to western blotting using indicated antibodies. Bar graph shows ± SEM of band intensities of P-VEGFR2 signals normalized to P-VEGFR2 signals of control for 3 independent experiments. <b>B</b> After 48 hr, proliferation of HUVECs was analyzed by MTT assay. <b>C</b> Transendothelial migration of HOS cells in the presence of rHSPB1 WT (1ug/ml) or rHSPB1 fragments (59–203; 1 µg/ml). After HOS cells were marked with CytoTracker, they were allowed to attach and migrate to the HUVEC monolayer. Fluorescence graph of migratory cells labeled with CytoTracker shows ± SEM for three independent experiments (*<i>P</i> <0.05 and **<i>P</i> <0.01, upper graph). HUVECs infected with MMP9 shRNA lentiviral and control vectors were subjected to tumor transendothelial migration assay in the presence of rHSPB1 WT (1ug/ml) (bottom graph). <b>D</b> HUVECs infected with MMP9 shRNA lentiviral and control vectors were transfected with sHSPB1WT or sHSPB1 fragments (1–58, 59–203) and then activated with VEGF (30 ng/mL). After 10 min, cell lysates and conditioned media were subjected to western blotting. Bar graph shows ± SEM of band intensities of P-VEGFR2 signals normalized to P-VEGFR2 signals of control for 3 independent experiments. <b>E</b> After 48 hr, proliferation of HUVECs was analyzed by MTT assay.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "mmp9-induced", "hspb1", "cleavage", "vegf-mediated", "endothelial"], "article_id"=>903797, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509.g005", "stats"=>{"downloads"=>1, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_MMP9_induced_HSPB1_cleavage_on_VEGF_mediated_endothelial_cell_activation_/903797", "title"=>"Effect of MMP9-induced HSPB1 cleavage on VEGF-mediated endothelial cell activation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-20 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1350968"], "description"=>"<p><b>A</b> Recombinant proteins (1 µg/mL) were incubated for 6 hr at 4°C with recombinant human VEGF (50 ng/mL). Immunoprecipitates using the Flag antibody were subjected to binding assays with VEGF<sub>165</sub> and western blotting using the Flag and VEGF antibodies. <b>B</b> The amount of HSPB1 WT or HSPB1 (59–203) bound to VEGF<sub>165</sub> was measured by ELISA assay. Data are presented as mean ± SEM. **<i>P</i> <0.01. <b>C</b> K<sub>d</sub> value for binding of HSPB1 WT or HSPB1 (59–203) to VEGF<sub>165</sub> were calculated by Scatchard analysis. Slope of each line = − 1/K<sub>d</sub>.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "c-terminal", "bound"], "article_id"=>903793, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HSPB1_C_terminal_fragment_bound_more_specifically_to_VEGF_165_/903793", "title"=>"HSPB1 C-terminal fragment bound more specifically to VEGF<sub>165</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-20 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1350987"], "description"=>"<p><b>A</b> B16F10 melanoma cell lines were stably transfected with PPTLS, sHSPB1WT, sHSPB1 (59–203), and HSPB1WT. Cell lysates and conditioned media of two stable lines (1,2) were repectively subjected to western blotting (top). <b>B</b> Effects of conditioned media of B16F10 stable cell lines on VEGF<sub>165</sub>-induced VEGFR2 activation and proliferation activity in HUVECs. <b>C</b> Mean number of metastases at 14 days after intravenous injection of B6F10 stable cells into wild-type mice. The graph shows the mean ± SEM from three independent experiments of six mice per group f (*<i>P</i> <0.05 and **<i>P</i> <0.01 vs PPTLS). Right panel shows representative images. <b>D</b> Intratumoral microvessel density (MVD) per high-powered field (h.p.f.) was quantified by CD31 immunofluorescence. (*<i>P</i> <0.05 and **<i>P</i> <0.01 vs PPTLS). <b>E</b> Mean weight of liver with tumor at 14 days after intrasplenic injection of B6F10 stable cells into wild-type mice.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "hspb1", "cleavage"], "article_id"=>903810, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509.g007", "stats"=>{"downloads"=>3, "page_views"=>81, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_HSPB1_cleavage_on_tumor_progression_/903810", "title"=>"Effect of HSPB1 cleavage on tumor progression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-20 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1350962"], "description"=>"<p><b>A</b> HSPB1 cleavage sites and a schematic representation of the resulting fragments. The amino acid sequence of the HSPB1 fragment from a Coomassie blue stained gel was analyzed by MALDI-TOF and LC mass spectrometry. The N-terminus or C-terminus HSPB1 fragments were detected by western blot analysis using N-terminal or C-terminal HSPB1 antibodies, respectively. <b>B</b> A schematic representation of the soluble vector for HSPB1. HSPB1 was tagged with an N-terminal 3XFlag and a C-terminal Myc tag. For secretion of HSPB1, the preprotrypsin leader sequence (PPTLS) precedes the Flag sequence; these vectors contain an additional C-terminal His tag. COS-7 cell lines stably transfected with control vector; PPTLS, secretory wild-type HSPB1; sHSPB1WT, N-terminal-deleted secretory HSPB1 (59–203); sHSPB1 (59–203), or possible cleavage sequence-deleted secretory HSPB1 (Δ54–63); sHSPB1 (Δ54–63) were cultured in OPTI-MEM media (1% FBS). Secretion of N-terminal Flag or C-terminal Myc tagged protein was detected by western blot analysis of the lysates and culture supernatants (bottom). <b>C</b> Recombinant protein (wild-type or mutant HSPB1) was incubated for 30 min with MMP9 (2 µg/mL) and HSPB1 digestion was examined by western blotting using the Flag antibody. <b>D</b> Recombinant protein of sHSPB1 (Δ54–63) was incubated for 30 min with MMP2, 3 and 9 (2 µg/mL) and HSPB1 digestion was examined by western blotting using the Flag antibody.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "hspb1", "intramolecular"], "article_id"=>903791, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509.g003", "stats"=>{"downloads"=>3, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_HSPB1_intramolecular_cleavage_/903791", "title"=>"Characterization of HSPB1 intramolecular cleavage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-20 02:44:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1350961"], "description"=>"<p><b>A</b> HUVECs were treated for 24(2 µM). Cleaved HSPB1 levels in conditioned media (C.M.) were detected by western blot analysis using an HSPB1 antibody to amino acids 158-205. <b>B</b> Recombinant HSPB1 (2 µg/mL) was incubated with ADAMTS1, MMP3, or MMP9 (50 ng/mL) for the indicated times. HSP70 (2 µg/mL) was incubated with MMP9 as a negative control. HSPB1 cleavage was detected by immunoblot using the HSPB1 antibody to amino acids 158-205 as well as Coomassie staining. <b>C</b> Recombinant HSPB1 (2 µg/mL) was incubated with MMP9 (50 ng/mL) for the times indicated and analyzed by western blot using antibodies against the C- (158-205) and N-termini (10–21) of HSPB1.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymes", "proteins", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "oncology", "Basic cancer research", "metastasis", "Cancers and neoplasms", "cleaved"], "article_id"=>903790, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Seo-hyun Choi", "Hae-June Lee", "Yeung Bae Jin", "Junho Jang", "Ga-Young Kang", "Minyoung Lee", "Chun-Ho Kim", "Joon Kim", "Sam S. Yoon", "Yun-Sil Lee", "Yoon-Jin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085509.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HSPB1_is_cleaved_by_MMPs_/903790", "title"=>"HSPB1 is cleaved by MMPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-20 02:44:24"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"6", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"2"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2017", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
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Relative Metric

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