Lineage Tracing of Lamellocytes Demonstrates Drosophila Macrophage Plasticity
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{"title"=>"Lineage tracing of lamellocytes demonstrates Drosophila macrophage plasticity", "type"=>"journal", "authors"=>[{"first_name"=>"Martin", "last_name"=>"Stofanko", "scopus_author_id"=>"25645003000"}, {"first_name"=>"So Yeon", "last_name"=>"Kwon", "scopus_author_id"=>"7402623038"}, {"first_name"=>"Paul", "last_name"=>"Badenhorst", "scopus_author_id"=>"7004340566"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-78649511614", "pui"=>"360051126", "doi"=>"10.1371/journal.pone.0014051", "isbn"=>"10.1371/journal.pone.0014051", "sgr"=>"78649511614", "pmid"=>"21124962"}, "id"=>"73213bd0-3da9-3164-9298-f012990af3bd", "abstract"=>"Leukocyte-like cells called hemocytes have key functions in Drosophila innate immunity. Three hemocyte types occur: plasmatocytes, crystal cells, and lamellocytes. In the absence of qimmune challenge, plasmatocytes are the predominant hemocyte type detected, while crystal cells and lamellocytes are rare. However, upon infestation by parasitic wasps, or in melanotic mutant strains, large numbers of lamellocytes differentiate and encapsulate material recognized as \"non-self\". Current models speculate that lamellocytes, plasmatocytes and crystal cells are distinct lineages that arise from a common prohemocyte progenitor. We show here that over-expression of the CoREST-interacting transcription factor Chn in plasmatocytes induces lamellocyte differentiation, both in circulation and in lymph glands. Lamellocyte increases are accompanied by the extinction of plasmatocyte markers suggesting that plasmatocytes are transformed into lamellocytes. Consistent with this, timed induction of Chn over-expression induces rapid lamellocyte differentiation within 18 hours. We detect double-positive intermediates between plasmatocytes and lamellocytes, and show that isolated plasmatocytes can be triggered to differentiate into lamellocytes in vitro, either in response to Chn over-expression, or following activation of the JAK/STAT pathway. Finally, we have marked plasmatocytes and show by lineage tracing that these differentiate into lamellocytes in response to the Drosophila parasite model Leptopilina boulardi. Taken together, our data suggest that lamellocytes arise from plasmatocytes and that plasmatocytes may be inherently plastic, possessing the ability to differentiate further into lamellocytes upon appropriate challenge.", "link"=>"http://www.mendeley.com/research/lineage-tracing-lamellocytes-demonstrates-drosophila-macrophage-plasticity", "reader_count"=>75, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>16, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>4, "Other"=>2, "Student > Master"=>13, "Student > Bachelor"=>8, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>16, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>4, "Other"=>2, "Student > Master"=>13, "Student > Bachelor"=>8, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>57, "Medicine and Dentistry"=>2, "Neuroscience"=>1, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>6}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>57}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Czech Republic"=>1, "Argentina"=>1, "United States"=>5, "United Kingdom"=>3}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/817545"], "description"=>"<p><i>Pxn-GAL4</i>, <i>UAS-GFP; Ubi-GAL80<sup>ts</sup> x UAS-chn</i> larvae were raised at 18°C (GAL4 repressed) and Chn was induced by up-shift to 29°C for 24 hours. <i>Pxn-GAL4</i>, <i>UAS-GFP; Ubi-GAL80<sup>ts</sup> x UAS-chn</i> larvae raised entirely at 18°C provided an uninduced control. mRNA was isolated from hemocytes from wandering stage third instar larvae and relative transcript abundance in Chn expressing relative to uninduced control hemocytes was determined by real-time PCR. <i>RpL32</i> provided an endogenous control to normalize expression. Relative transcript abundance after Chn over-expression of (<b>A</b>) lamellocyte markers and (<b>B</b>) plasmatocyte markers. Data are mean and standard deviation of three independent determinations.</p>", "links"=>[], "tags"=>["over-expression", "activates", "transcription", "lamellocyte", "markers", "represses", "plasmatocyte"], "article_id"=>487905, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g003", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chn_over_expression_activates_transcription_of_lamellocyte_markers_and_represses_transcription_of_plasmatocyte_markers_/487905", "title"=>"Chn over-expression activates transcription of lamellocyte markers and represses transcription of plasmatocyte markers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:11:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/817800"], "description"=>"<p>(<b>A–D</b>) MAb L1-staining (green) of hemocytes isolated from third instar larvae (<b>A</b>) 0 hr, (<b>B</b>) 24 hr, (<b>C</b>) 36 hr, and (<b>D</b>) 48 hr after 12 hr infestation with the parasitic wasp <i>L. boulardi.</i> DAPI-stained nuclei are shown in purple. Scalebar denotes 50 µm. (<b>E</b>) Schematic of the lineage tracing experiment. <i>Pxn-GAL4</i> drives expression of FLP in plasmatocytes. FLP excises an FRT flanked transcription stop cassette from the <i>act5C>stop>lacZ</i> transgene, turning on expression of lacZ in a plasmatocytes. <i>act5C-lacZ</i> expression is then independent of <i>Pxn-GAL4</i>, marking cells that were plasmatocytes during subsequent lamellocyte differentiation. (<b>F</b>) MAb L1 (green) and anti-lacZ (red) antibody staining reveals lacZ<sup>+</sup>/MAb L1<sup>+</sup> lamellocytes confirming the plasmatocyte origin of lamellocytes. Three classes of lamellocytes occur, lacZ<sup>−</sup> lamellocytes (open arrows), and lacZ<sup>+</sup> lamellocytes that are <40 µm (closed arrows) or >40 µm (closed arrowheads) lacZ<sup>+</sup>/MAb L1<sup>−</sup> hemocytes indicated by open arrowheads. (<b>G</b>) 31.3% of hemocytes are lacZ<sup>+</sup>, of which 26.4% are lacZ<sup>+</sup>/MAb L1<sup>+</sup>. Consistent with the origin of lamellocytes from small precursors, lacZ<sup>+</sup>/MAb L1<sup>+</sup> cells <40 µm in diameter and cells >40 µm in diameter are detected.</p>", "links"=>[], "tags"=>["tracing", "reveals", "wasp-induced", "lamellocytes"], "article_id"=>488170, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g006", "stats"=>{"downloads"=>3, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lineage_tracing_reveals_that_wasp_induced_lamellocytes_arise_from_plasmatocytes_/488170", "title"=>"Lineage tracing reveals that wasp-induced lamellocytes arise from plasmatocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:16:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/817224"], "description"=>"<p>Chn overexpression decreases (<b>A</b>,<b>E</b>) sessile (asterisk) and (<b>B</b>,<b>F</b>) circulating plasmatocyte numbers. (<b>C</b>, <b>G</b>) Anti-Hemese staining detects hemocytes after Chn expression although hemocyte size is increased (arrowheads) (<b>D</b>,<b>H</b>) MAb L1 staining confirms that Chn expression increases lamellocyte number. Circulating hemocytes were isolated from (<b>B–D</b>) <i>Pxn-GAL4</i>, <i>UAS-GFP x w<sup>1118</sup></i> and (<b>F–H</b>) <i>Pxn-GAL4</i>, <i>UAS-GFP x UAS-chn</i> third instar larvae. Antibody staining is shown in green, DAPI-stained nuclei in purple. Scalebars denote 50 µm. (<b>I</b>) Lamellocyte frequency after Chn expression driven by different GAL4 lines. Control driver cross with <i>w<sup>1118</sup></i> provides a reference. (<b>J</b>) Comparison of lamellocyte differentiation induced by expression of other transcription factors with <i>Pxn-GAL4</i>. Each data point in (<b>I</b>,<b>J</b>) is the mean +/− s.d. of at least 5 assays.</p>", "links"=>[], "tags"=>["over-expression", "increases", "lamellocyte"], "article_id"=>487596, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chn_over_expression_increases_lamellocyte_number_/487596", "title"=>"Chn over-expression increases lamellocyte number.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:06:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/817609"], "description"=>"<p>(<b>A</b>) <i>chn</i> transcript levels are elevated in hemocyte populations relative to whole larvae. Elevation of <i>chn</i> transcript levels parallels that observed for the hemocyte expressed <i>He</i> and <i>Hml</i> transcripts. In contrast <i>chn</i> transcripts are reduced in fat body relative to whole larvae. Data are mean and standard deviation of three independent determinations (<b>B</b>) RNAi knockdown of Chn reduces lamellocyte differentiation observed after wasp infestation. Lamellocyte frequencies were determined after MAb L1 staining. Data are mean and standard deviation of 5 confocal panels from each of 4 separate infested larvae hemocyte preparations.</p>", "links"=>[], "tags"=>["chn"], "article_id"=>487982, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Endogenous_Chn_expression_/487982", "title"=>"Endogenous Chn expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:13:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/817987"], "description"=>"<p>Current models for the origin of the three hemocyte types propose that plasmatocytes, crystal cells and lamellocytes represent distinct lineages that arise separately from a common stem cell or prohemocyte. We propose that prohemocytes generate either crystal cells or plasmatocytes. Plasmatocytes are a plastic population that can, in turn, generate other hemocyte types such as lamellocytes and podocytes.</p>", "links"=>[], "tags"=>["hemocyte"], "article_id"=>488362, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g008", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_model_of_hemocyte_lineage_/488362", "title"=>"Proposed model of hemocyte lineage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:19:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/817427"], "description"=>"<p><i>Pxn-GAL4</i>, <i>UAS-GFP; Ubi-GAL80<sup>ts</sup> x UAS-chn</i> wandering stage third instar larvae were raised at 18°C (GAL4 repressed) and Chn was induced by up-shift to 29°C. (<b>A–D</b>) Lamellocytes are absent from circulation (<b>A</b>) 0 hr and (<b>B</b>) 12 hr after induction of Chn expression, but appear at (<b>C</b>) 18 hr, peaking at (<b>D</b>) 24 hr. (<b>E</b>) Proportion of lamellocytes <40 µm (red line) or >40 µm (blue line) relative to total hemocyte number (marked by DAPI staining) Time-points are the mean +/− s.d. of 10 determinations. (<b>F</b>) Proliferation index after Chn overexpression determined from number of anti-H3S10p antibody staining hemocytes relative to total hemocyte number (marked by DAPI staining) (<b>G</b>) Hemocytes freshly isolated from larvae grown at 18°C do not stain with MAb L1, but (<b>H</b>) after in vitro culture at 29°C for 24 hr to induce Chn expression many lamellocytes were detected, including mature (closed arrowheads) and intermediate (<40 µm) (open arrowheads) forms. (<b>I</b>) Lamellocyte frequencies before (0 hr) and 24 hr after culture at 29°C. Data are the mean +/− s.d. of 5 independent determinations. (<b>J–L</b>) Chn over-expression increases lamellocyte number in primary lymph glands (closed arrowheads), but (<b>M–O</b>) does not increase proliferation. Lamellocytes were not detected in the secondary lobes (open arrowheads) In (<b>J–O</b>) antibody staining is shown in green, DAPI-stained nuclei in purple. Scalebar in (<b>A–H</b>) denotes 50 µm, in (<b>J–O</b>) 200 µm.</p>", "links"=>[], "tags"=>["chn", "overexpression", "induces", "lamellocyte"], "article_id"=>487792, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pulsed_Chn_overexpression_induces_lamellocyte_differentiation_/487792", "title"=>"Pulsed Chn overexpression induces lamellocyte differentiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:09:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/407498", "https://ndownloader.figshare.com/files/407507", "https://ndownloader.figshare.com/files/407512", "https://ndownloader.figshare.com/files/407523"], "description"=>"<div><p>Leukocyte-like cells called hemocytes have key functions in <em>Drosophila</em> innate immunity. Three hemocyte types occur: plasmatocytes, crystal cells, and lamellocytes. In the absence of qimmune challenge, plasmatocytes are the predominant hemocyte type detected, while crystal cells and lamellocytes are rare. However, upon infestation by parasitic wasps, or in melanotic mutant strains, large numbers of lamellocytes differentiate and encapsulate material recognized as “non-self”. Current models speculate that lamellocytes, plasmatocytes and crystal cells are distinct lineages that arise from a common prohemocyte progenitor. We show here that over-expression of the CoREST-interacting transcription factor Chn in plasmatocytes induces lamellocyte differentiation, both in circulation and in lymph glands. Lamellocyte increases are accompanied by the extinction of plasmatocyte markers suggesting that plasmatocytes are transformed into lamellocytes. Consistent with this, timed induction of Chn over-expression induces rapid lamellocyte differentiation within 18 hours. We detect double-positive intermediates between plasmatocytes and lamellocytes, and show that isolated plasmatocytes can be triggered to differentiate into lamellocytes in vitro, either in response to Chn over-expression, or following activation of the JAK/STAT pathway. Finally, we have marked plasmatocytes and show by lineage tracing that these differentiate into lamellocytes in response to the <em>Drosophila</em> parasite model <em>Leptopilina boulardi</em>. Taken together, our data suggest that lamellocytes arise from plasmatocytes and that plasmatocytes may be inherently plastic, possessing the ability to differentiate further into lamellocytes upon appropriate challenge.</p></div>", "links"=>[], "tags"=>["lineage", "tracing", "lamellocytes", "demonstrates", "macrophage", "plasticity"], "article_id"=>140499, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0014051.s001", "https://dx.doi.org/10.1371/journal.pone.0014051.s002", "https://dx.doi.org/10.1371/journal.pone.0014051.s003", "https://dx.doi.org/10.1371/journal.pone.0014051.s004"], "stats"=>{"downloads"=>27, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Lineage_Tracing_of_Lamellocytes_Demonstrates_Drosophila_Macrophage_Plasticity/140499", "title"=>"Lineage Tracing of Lamellocytes Demonstrates <em>Drosophila</em> Macrophage Plasticity", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-11-19 00:08:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/817901"], "description"=>"<p><i>Pxn-GAL4</i>, <i>UAS-GFP; Ubi-GAL80<sup>ts</sup> x UAS-chn</i> larvae were raised at 18°C (GAL4 repressed) and injected with fluorescent polystyrene microspheres. Chn expression was induced by up-shift to 29°C for 24 hours to trigger lamellocyte differentiation. Isolated hemocytes were stained using MAb L1 antibodies to identify lamellocytes, and using rhodamine-phalloidin to distinguish cell boundaries. Engulfed microspheres were identified by intense yellow green fluorescence (which bleeds through into the red channel). A confocal Z stack was compiled through a MAb L1<sup>−</sup> plasmatocyte and a MAb L1<sup>+</sup> lamellocyte. Projections along the X- and Y-axis confirmed that both contained engulfed microspheres. In panels rhodamine-phalloidin staining is shown in red, fluorescent polystyrene microspheres as yellow spots (open arrowheads) and MAb L1 staining is pseudocolored green. MAb L1<sup>+</sup> lamellocyte is indicated by a closed arrow and MAb L1<sup>−</sup> plasmatocyte is indicated by an open arrow.</p>", "links"=>[], "tags"=>["phagocytes", "differentiate"], "article_id"=>488275, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g007", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Active_phagocytes_can_differentiate_into_lamellocytes_/488275", "title"=>"Active phagocytes can differentiate into lamellocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:17:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/817690"], "description"=>"<p>(<b>A–D</b>) <i>hop<sup>Tum-l</sup>/+; Pxn-GAL4-UAS-GFP/+</i> larvae raised at 20°C contain hemocytes intermediate between mature lamellocytes and plasmatocytes. (<b>A</b>) MAb L1 and (<b>C</b>) anti-GFP staining. (<b>B</b>) Merge showing overlap in MAb L1 (red) and anti-GFP (green) Small (<20 µm) GFP<sup>+</sup>/MAb L1<sup>−</sup> plasmatocytes (closed arrows), large (>40 µm) GFP<sup>−</sup>/MAb L1<sup>+</sup> lamellocytes (closed arrowheads) and intermediate sized (<40 µm) GFP<sup>+</sup>/MAb L1<sup>+</sup> hemocytes (open arrowheads) were detected. (<b>D</b>) 24.7% of hemocytes are the intermediate GFP<sup>+</sup>/MAb L1<sup>+</sup> population. No large (>40 µm) GFP<sup>+</sup>/MAb L1<sup>+</sup> lamellocytes were detected. Data are mean +/− s.d. of 8 determinations. (<b>E–I</b>) FACS purified GFP<sup>+</sup>/MAb L1<sup>−</sup> plasmatocytes from <i>hop<sup>Tum-l</sup>/+; </i><i>Pxn-GAL4-UAS-GFP/+</i> larvae can be induced to differentiate into lamellocytes in vitro at 29°C. (<b>E</b>) Hemocytes before sorting, stained with MAb L1 (red) and anti-GFP antibodies (green) Populations are labeled as in (<b>B</b>). (<b>F</b>) Hemocytes were FACS sorted to select GFP<sup>+</sup>/MAb L1<sup>−</sup> cells (lower right quadrant) (<b>G</b>) Confocal microscopy confirms sorted cells as GFP<sup>+</sup>/MAb L1<sup>−</sup> plasmatocytes. (<b>H</b>) These can differentiate into MAb L1<sup>+</sup> lamellocytes after in vitro culture at 29°C for 30 hr. Both large mature lamellocytes (closed arrowheads) and (<40 µm) intermediates (open arrowheads) were detected. (<b>I</b>) Increase in lamellocyte frequency after culture at 29°C (30 hr) Data are the mean +/− s.d. of three independent determinations. In (<b>E</b>,<b>G</b>,<b>H</b>) DAPI-stained nuclei are shown in purple. Scalebar in all panels denotes 50 µm.</p>", "links"=>[], "tags"=>["vitro", "differentiation", "lamellocytes"], "article_id"=>488061, "categories"=>["Genetics", "Developmental Biology"], "users"=>["Martin Stofanko", "So Yeon Kwon", "Paul Badenhorst"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0014051.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vitro_differentiation_of_lamellocytes_from_plasmatocytes_/488061", "title"=>"In vitro differentiation of lamellocytes from plasmatocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-11-19 02:14:21"}

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  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
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  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
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  • {"unique-ip"=>"11", "full-text"=>"9", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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  • {"unique-ip"=>"20", "full-text"=>"12", "pdf"=>"9", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"18", "full-text"=>"12", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
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Relative Metric

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