Bid Regulates the Pathogenesis of Neurotropic Reovirus
Publication Date
July 01, 2010
Journal
PLOS Pathogens
Authors
Pranav Danthi, Andrea J. Pruijssers, Angela K. Berger, Geoffrey H. Holm, et al
Volume
6
Issue
7
Pages
e1000980
DOI
https://dx.plos.org/10.1371/journal.ppat.1000980
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1000980
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/20617182
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2895667
Europe PMC
http://europepmc.org/abstract/MED/20617182
Web of Science
000280527000014
Scopus
77957677378
Mendeley
http://www.mendeley.com/research/bid-regulates-pathogenesis-neurotropic-reovirus
Events
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Mendeley | Further Information

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/419275"], "description"=>"<div><p>Reovirus infection leads to apoptosis in both cultured cells and the murine central nervous system (CNS). NF-κB-driven transcription of proapoptotic cellular genes is required for the effector phase of the apoptotic response. Although both extrinsic death-receptor signaling pathways and intrinsic pathways involving mitochondrial injury are implicated in reovirus-induced apoptosis, mechanisms by which either of these pathways are activated and their relationship to NF-κB signaling following reovirus infection are unknown. The proapoptotic Bcl-2 family member, Bid, is activated by proteolytic cleavage following reovirus infection. To understand how reovirus integrates host signaling circuits to induce apoptosis, we examined proapoptotic signaling following infection of Bid-deficient cells. Although reovirus growth was not affected by the absence of Bid, cells lacking Bid failed to undergo apoptosis. Furthermore, we found that NF-κB activation is required for Bid cleavage and subsequent proapoptotic signaling. To examine the functional significance of Bid-dependent apoptosis in reovirus disease, we monitored fatal encephalitis caused by reovirus in the presence and absence of Bid. Survival of Bid-deficient mice was significantly enhanced in comparison to wild-type mice following either peroral or intracranial inoculation of reovirus. Decreased reovirus virulence in Bid-null mice was accompanied by a reduction in viral yield. These findings define a role for NF-κB-dependent cleavage of Bid in the cell death program initiated by viral infection and link Bid to viral virulence.</p></div>", "links"=>[], "tags"=>["regulates", "pathogenesis", "neurotropic", "reovirus"], "article_id"=>142805, "categories"=>["Cell Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980", "stats"=>{"downloads"=>0, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Bid_Regulates_the_Pathogenesis_of_Neurotropic_Reovirus/142805", "title"=>"Bid Regulates the Pathogenesis of Neurotropic Reovirus", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-07-01 00:46:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/842138"], "description"=>"<p>Two-day-old wild-type and Bid-deficient mice were inoculated intracranially with 5 PFU of T3SA+. At 10 d post-inoculation, brains from infected mice were resected, fixed, and embedded in paraffin. (A) Low magnification image of H&E-stained hippocampal region of wild-type and Bid-deficient mouse brains. Scale bars, 500 µm. (B) Higher magnification images of the boxed region of the hippocampus shown in (A) stained in consecutive sections with H&E, polyclonal reovirus-specific antiserum, or activated caspase-3-specific antiserum. Scale bars, 100 µm. Intense brown staining indicates caspase-3- or reovirus-positive cells.</p>", "links"=>[], "tags"=>["histopathologic", "diminished", "cns", "bid-deficient"], "article_id"=>512597, "categories"=>["Plant Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980.g007", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reovirus_induced_histopathologic_injury_is_diminished_in_the_CNS_of_Bid_deficient_mice_/512597", "title"=>"Reovirus-induced histopathologic injury is diminished in the CNS of Bid-deficient mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-01 00:43:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/841648"], "description"=>"<p>(A) Wild-type MEFs or MEFs deficient in Bid were transfected with pNF-κB-luc, which expresses firefly luciferase under control of NF-κB, and a control plasmid, which constitutively expresses Renilla luciferase. At 18 h after transfection, cells were mock-infected or infected with T3D at an MOI of 100 PFU/cell. Cells treated with 10 ng/ml of TNFα were used as controls. Luciferase activity in cell lysates was quantified at 24 h following infection or 8 h following TNFα treatment. Results are expressed as the ratio of relative luciferase activity of experimental samples to relative luciferase activity of mock-infected cells. Error bars indicate SD. (B) Wild-type and p65/RelA-deficient MEFs were mock-infected, infected with T3D at an MOI of 100 PFU/cell, or treated with 10 ng/ml of TNFα and 10 µg/ml of cycloheximide (CHX). Whole cell lysates were prepared at the indicated times after infection or 12 h following TNFα/CHX treatment and resolved in 18% polyacrylamide gels and transferred to nitrocellulose membranes. The membranes were probed with polyclonal antisera specific for Bid or actin and appropriate HRP-conjugated secondary antibodies and visualized using chemiluminescence.</p>", "links"=>[], "tags"=>["cleavage", "reovirus"], "article_id"=>512106, "categories"=>["Plant Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NF_954_B_is_required_for_Bid_cleavage_following_reovirus_infection_/512106", "title"=>"NF-κB is required for Bid cleavage following reovirus infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-01 00:35:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/841931"], "description"=>"<p>(A and C) Two-day-old wild-type and Bid-deficient mice were inoculated intracranially with 100 PFU (A) or 5 PFU (C) of T3SA+. Mice (<i>n</i> = 13–23) were monitored for survival for 21 days. *, <i>P</i><0.05 as determined by log-rank test in comparison to wild-type mice. (B and D) Two-day-old wild-type and Bid-deficient mice were inoculated intracranially with 100 PFU (B) or 5 PFU (D) of T3SA+ and euthanized at the times shown. Brains were resected and homogenized by freeze-thaw and sonication. Viral titers in brain homogenates were determined by plaque assay. Results are expressed as viral titer in organs of single infected animals as indicated by closed (wild-type) or open (Bid-deficient) circles. Horizontal black lines indicate mean viral titers. *, <i>P</i><0.05 as determined by Mann Whitney test in comparison to wild-type mice at the same time post-inoculation. **, <i>P</i><0.01 as determined by Mann Whitney test in comparison to wild-type mice at the same time post-inoculation.</p>", "links"=>[], "tags"=>["modulates", "reovirus", "replication", "pathogenesis", "ic"], "article_id"=>512388, "categories"=>["Plant Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980.g006", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bid_modulates_reovirus_replication_and_pathogenesis_following_IC_inoculation_/512388", "title"=>"Bid modulates reovirus replication and pathogenesis following IC inoculation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-01 00:39:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/841457"], "description"=>"<p>(A) L929 cells were adsorbed with PBS (mock) or reovirus T3D at an MOI of 100 PFU/cell. Following incubation at 37°C for the indicated intervals, whole cell extracts were prepared, resolved by SDS-PAGE, and immunoblotted using antisera specific for Bid, actin, or procasapse-9. (B) L929 cells were adsorbed with reovirus T3D at an MOI of 100 PFU/cell. Following incubation at 37°C for the indicated intervals in the presence of 0 or 10 µM of Z-IETD-FMK, whole cell extracts were prepared, resolved by SDS-PAGE, and immunoblotted using antisera specific for Bid, actin, or procasapse-9. Protein bands are indicated on the right. A non-specific band is indicated by an asterisk (*).</p>", "links"=>[], "tags"=>["cleaved", "reovirus", "murine"], "article_id"=>511909, "categories"=>["Plant Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bid_is_cleaved_following_reovirus_infection_of_murine_fibroblasts_/511909", "title"=>"Bid is cleaved following reovirus infection of murine fibroblasts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-01 00:31:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/841728"], "description"=>"<p>(A) Wild-type or TRAIL-R-deficient MEFs were adsorbed with T3D at the MOIs shown. After incubation at 37°C for 24 h, caspase-3/7 activity in cell lysates was determined. Results are expressed as the mean ratio of caspase-3/7 activity from infected cell lysates to that from mock-infected cell lysates for triplicate samples. Error bars indicate SD. *, <i>P</i><0.05 as determined by Student's <i>t</i>-test relative to wild-type MEFs infected at an equivalent MOI. (B) Wild-type or TRAIL-R-deficient MEFs were adsorbed with T3D at the MOIs shown. After incubation at 37°C for 48 h, cells were stained with AO. Results are expressed as the mean percentage of cells undergoing apoptosis for three independent experiments. Error bars indicate SD. *, <i>P</i><0.05 as determined by Student's <i>t</i>-test relative to wild-type MEFs infected at an equivalent MOI. (C) Wild-type and TRAIL-R-deficient MEFs were adsorbed with T3D at an MOI of 2 PFU/cell. The inoculum was removed, and cells were incubated at 37°C for 0, 12, 24 and 48 h. Viral titers were determined after two cycles of freeze-thaw by plaque assay using L929 cells. Results are presented as mean titers from three independent experiments. Error bars indicate SD. (D) Wild-type and TRAIL-R-deficient MEFs were mock-infected or infected with T3D at an MOI of 100 PFU/cell. Whole cell lysates were prepared at 48 h after infection and resolved in 18% polyacrylamide gels and transferred to nitrocellulose membranes. The membranes were probed with polyclonal antisera specific for Bid or actin and appropriate HRP-conjugated secondary antibodies and visualized using chemiluminescence.</p>", "links"=>[], "tags"=>["signaling", "trail-r", "contributes", "cleavage", "apoptosis", "induction", "reovirus"], "article_id"=>512179, "categories"=>["Plant Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Death_signaling_via_TRAIL_R_contributes_to_Bid_cleavage_and_apoptosis_induction_following_reovirus_infection_/512179", "title"=>"Death signaling via TRAIL-R contributes to Bid cleavage and apoptosis induction following reovirus infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-01 00:36:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/841514"], "description"=>"<p>(A) Wild-type or Bid-deficient MEFs were adsorbed with T3D at the MOIs shown. After incubation at 37°C for 24 h, caspase-3/7 activity in cell lysates was determined. Results are expressed as the mean ratio of caspase-3/7 activity from infected cell lysates to that from mock-infected cells for triplicate samples. Error bars indicate SD. *, <i>P</i><0.05 as determined by Student's <i>t</i>-test relative to wild-type MEFs infected at an equivalent MOI. Cells were treated with 10 µM staurosporine (Sts) for 24 h as a control. (B) Wild-type or Bid-deficient MEFs were adsorbed with T3D at the MOIs shown. After incubation at 37°C for 48 h, cells were stained with AO. Results are expressed as the mean percentage of cells undergoing apoptosis for three independent experiments. Error bars indicate SD. *, <i>P</i><0.05 as determined by Student's <i>t</i>-test relative to wild-type MEFs infected at an equivalent MOI. (C) Wild-type and Bid-deficient MEFs were adsorbed with 10<sup>4</sup> particles/cell of T3D. After incubation at 37°C for 18 h, cells were visualized by immunostaining with polyclonal reovirus-specific antiserum, followed by incubation with Alexa546-labeled anti-rabbit IgG. Reovirus-infected cells were quantified by counting fluorescent cells. Results are expressed as mean fluorescent focus units (FFU) per field for triplicate samples. Error bars indicate SD. (D) Wild-type and Bid-deficient MEFs were adsorbed with T3D at an MOI of 2 PFU/cell. The inoculum was removed, and cells were incubated at 37°C for the times shown. Viral titers were determined after two cycles of freeze-thaw by plaque assay using L929 cells. Results are presented as mean titers from three independent experiments. Error bars indicate SD.</p>", "links"=>[], "tags"=>["apoptosis", "induction", "reovirus"], "article_id"=>511972, "categories"=>["Plant Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bid_is_required_for_apoptosis_induction_following_reovirus_infection_/511972", "title"=>"Bid is required for apoptosis induction following reovirus infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-01 00:32:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/841849"], "description"=>"<p>(A) Two-day-old wild-type and Bid-deficient mice were inoculated perorally with 10<sup>4</sup> PFU of T3SA+. Mice (<i>n</i> = 23 to 27) were monitored for survival for 21 days. ***, <i>P</i><0.005 as determined by log-rank test in comparison to wild-type mice. (B–E) Two-day-old wild-type and Bid-deficient mice were inoculated perorally with 10<sup>4</sup> PFU of T3SA+ and euthanized at the times shown. Intestines (B), liver (C), heart (D), and brain (E) were resected and homogenized by freeze-thaw and sonication. Viral titers in organ homogenates were determined by plaque assay. Results are expressed as viral titer in organs of single infected animals as indicated by closed (wild-type) or open (Bid-deficient) circles. Horizontal black lines indicate mean viral titers. *, <i>P</i><0.05 as determined by Mann Whitney test in comparison to wild-type mice at the same time post-inoculation. **, <i>P</i><0.01 as determined by Mann Whitney test in comparison to wild-type mice at the same time post-inoculation.</p>", "links"=>[], "tags"=>["modulates", "reovirus", "replication", "pathogenesis", "po"], "article_id"=>512306, "categories"=>["Plant Biology"], "users"=>["Pranav Danthi", "Andrea J. Pruijssers", "Angela K. Berger", "Geoffrey H. Holm", "Sandra S. Zinkel", "Terence S. Dermody"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000980.g005", "stats"=>{"downloads"=>4, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bid_modulates_reovirus_replication_and_pathogenesis_following_PO_inoculation_/512306", "title"=>"Bid modulates reovirus replication and pathogenesis following PO inoculation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-01 00:38:26"}

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  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2014", "month"=>"12"}
  • {"unique-ip"=>"6", "full-text"=>"1", "pdf"=>"4", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"1"}
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  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"6"}
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  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"9"}
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  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
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  • {"unique-ip"=>"5", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"3"}
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  • {"unique-ip"=>"2", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"5"}
  • {"unique-ip"=>"2", "full-text"=>"0", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"6"}
  • {"unique-ip"=>"8", "full-text"=>"1", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"0", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2016", "month"=>"8"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
  • {"unique-ip"=>"1", "full-text"=>"0", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2017", "month"=>"1"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"4"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"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"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"2", "full-text"=>"3", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"5", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2019", "month"=>"1"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"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"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "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"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"6", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"4", "full-text"=>"1", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"0", "cited-by"=>"3", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"4", "full-text"=>"11", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"9"}
  • {"unique-ip"=>"9", "full-text"=>"4", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"11"}
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Relative Metric

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