Degradation of the Disease-Associated Prion Protein by a Serine Protease from Lichens
Publication Date
May 11, 2011
Journal
PLOS ONE
Authors
Christopher J. Johnson, James P. Bennett, Steven M. Biro, Juan Camilo Duque Velasquez, et al
Volume
6
Issue
5
Pages
e19836
DOI
https://dx.plos.org/10.1371/journal.pone.0019836
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0019836
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21589935
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3092769
Europe PMC
http://europepmc.org/abstract/MED/21589935
Web of Science
000290483600032
Scopus
79955885574
Mendeley
http://www.mendeley.com/research/degradation-diseaseassociated-prion-protein-serine-protease-lichens
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Mendeley | Further Information

{"title"=>"Degradation of the disease-associated prion protein by a serine protease from lichens", "type"=>"journal", "authors"=>[{"first_name"=>"Christopher J.", "last_name"=>"Johnson", "scopus_author_id"=>"55636318963"}, {"first_name"=>"James P.", "last_name"=>"Bennett", "scopus_author_id"=>"13005193600"}, {"first_name"=>"Steven M.", "last_name"=>"Biro", "scopus_author_id"=>"39261023400"}, {"first_name"=>"Juan Camilo", "last_name"=>"Duque-Velasquez", "scopus_author_id"=>"36501302000"}, {"first_name"=>"Cynthia M.", "last_name"=>"Rodriguez", "scopus_author_id"=>"56257138200"}, {"first_name"=>"Richard A.", "last_name"=>"Bessen", "scopus_author_id"=>"6603963438"}, {"first_name"=>"Tonie E.", "last_name"=>"Rocke", "scopus_author_id"=>"7004530075"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"361753556", "sgr"=>"79955885574", "issn"=>"19326203", "pmid"=>"21589935", "scopus"=>"2-s2.0-79955885574", "doi"=>"10.1371/journal.pone.0019836", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"375bfa32-fba3-34a7-9116-2c784802b7f4", "abstract"=>"The disease-associated prion protein (PrP(TSE)), the probable etiological agent of the transmissible spongiform encephalopathies (TSEs), is resistant to degradation and can persist in the environment. Lichens, mutualistic symbioses containing fungi, algae, bacteria and occasionally cyanobacteria, are ubiquitous in the environment and have evolved unique biological activities allowing their survival in challenging ecological niches. We investigated PrP(TSE) inactivation by lichens and found acetone extracts of three lichen species (Parmelia sulcata, Cladonia rangiferina and Lobaria pulmonaria) have the ability to degrade prion protein (PrP) from TSE-infected hamsters, mice and deer. Immunoblots measuring PrP levels and protein misfolding cyclic amplification indicated at least two logs of reductions in PrP(TSE). Degradative activity was not found in closely related lichen species or in algae or a cyanobacterium that inhabit lichens. Degradation was blocked by Pefabloc SC, a serine protease inhibitor, but not inhibitors of other proteases or enzymes. Additionally, we found that PrP levels in PrP(TSE)-enriched preps or infected brain homogenates are also reduced following exposure to freshly-collected P. sulcata or an aqueous extract of the lichen. Our findings indicate that these lichen extracts efficiently degrade PrP(TSE) and suggest that some lichens could have potential to inactivate TSE infectivity on the landscape or be a source for agents to degrade prions. Further work to clone and characterize the protease, assess its effect on TSE infectivity and determine which organism or organisms present in lichens produce or influence the protease activity is warranted.", "link"=>"http://www.mendeley.com/research/degradation-diseaseassociated-prion-protein-serine-protease-lichens", "reader_count"=>60, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>16, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>6, "Student > Bachelor"=>12, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>16, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>3, "Other"=>2, "Student > Master"=>6, "Student > Bachelor"=>12, "Professor"=>5}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>8, "Materials Science"=>1, "Agricultural and Biological Sciences"=>34, "Medicine and Dentistry"=>3, "Neuroscience"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Physics and Astronomy"=>2, "Chemistry"=>4, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>4}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>34}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>3}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Mexico"=>1, "Indonesia"=>2}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/776001"], "description"=>"<p>(A) Dose-response of the indicated lichen extracts (0–10 mg lichen\n equivalents) on degrading PTA-enriched PrP<sup>TSE</sup> (30 µg\n total protein). (B) The indicated concentrations of PK (0–10000\n µg·mL<sup>−1</sup>) were incubated with\n PTA-enriched PrP<sup>TSE</sup> (30 µg total protein) to assess\n degradation and for comparison with lichen extracts. Immunoblots used\n mAb 3F4.</p>", "links"=>[], "tags"=>["lichen", "extract", "prp"], "article_id"=>446366, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_lichen_extract_dose_on_PrP_degradation_/446366", "title"=>"Effect of lichen extract dose on PrP degradation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:30:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/776064"], "description"=>"<p>Reaction solutions were buffered at the indicated pHs (5–8) and the\n effect of each indicated lichen extract (10 mg lichen equivalents) on\n degradation of PTA-enriched PrP<sup>TSE</sup> (30 µg total\n protein) was observed by immunoblotting with mAb 3F4.</p>", "links"=>[], "tags"=>["ph", "prp", "degradation", "and"], "article_id"=>446426, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g005", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_pH_on_PrP_degradation_by_P_sulcata_and_____L_pulmonaria_extracts_/446426", "title"=>"Effect of pH on PrP degradation by <i>P. sulcata</i> and\n <i>L. pulmonaria</i> extracts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/775850"], "description"=>"<p>(A) Lichen extracts (10 mg lichen equivalents) were incubated with equal\n amounts (10 µL) of 10% brain homogenates from hamsters\n infected with Hyper (HY) TME, Drowsy (DY) TME or 263K scrapie strains of\n TSE agents and PrP degradation was assessed by immunoblotting. Treatment\n of each hamster brain homogenate with 50\n µg·mL<sup>−1</sup> of PK demonstrates the\n presence of abnormal PrP in the starting material. Using the same\n conditions as in (A), lichen extracts cause degradation of PrP in (B) a\n CWD-infected white-tailed deer, (C) PK-treated HY hamster and (D)\n uninfected hamster brain homogenates. (E) Protein C5 of the 20S subunit\n of the proteasome, an unrelated protein, was also degraded by lichen\n extracts. Immunoblots (IB) used mAbs 3F4 (A, C and D), 6H4 (B) or pAb\n anti-C5 (E).</p>", "links"=>[], "tags"=>["extracts", "degrade", "brain"], "article_id"=>446216, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g002", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lichen_extracts_degrade_PrP_TSE_in_brain____homogenate_/446216", "title"=>"Lichen extracts degrade PrP<sup>TSE</sup> in brain\n homogenate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:29:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/776172"], "description"=>"<p>Reactions of PTA-enriched PrP<sup>TSE</sup> (30 µg total protein)\n and the indicated lichen extracts (10 mg lichen equivalents) were\n prepared with enzyme inhibitors: (A) EDTA (1 or 10 mM) to inhibit\n metalloenzymes, (B) ascorbate (5 mM) as an antioxidant and chelator, (C)\n Cd<sup>2+</sup> (80 mM) to inhibit laccases or (D) a\n broad-spectrum protease inhibitor cocktail (10 µL per reaction).\n The effect of each inhibitor on <i>P. sulcata</i> or\n <i>L. pulmonaria</i> extract-mediated degradation of PrP\n was measured by immunoblotting with mAb 3F4.</p>", "links"=>[], "tags"=>["enzymatic", "prp"], "article_id"=>446545, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g007", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Assessing_enzymatic_activity_responsible_for_PrP_degradation_/446545", "title"=>"Assessing enzymatic activity responsible for PrP degradation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:31:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/776250"], "description"=>"<p>Incubation of PTA-enriched PrP<sup>TSE</sup> (30 µg total protein)\n with lichen extracts (10 mg lichen equivalents) were performed in the\n presence and absence of Pefabloc SC (14 mM). Reactions with the\n inhibitor had increased PrP immunoreactivity with mAb 3F4 (reduced PrP\n degradation).</p>", "links"=>[], "tags"=>["serine", "protease", "inhibitor", "pefabloc", "sc", "prevents", "prp"], "article_id"=>446607, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g008", "stats"=>{"downloads"=>0, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_serine_protease_inhibitor_Pefabloc_SC_prevents_PrP____degradation_/446607", "title"=>"The serine protease inhibitor Pefabloc SC prevents PrP\n degradation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:31:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/776375"], "description"=>"<p>*Only Pefabloc SC inhibited degradation of PrP by lichen\n extracts.</p>", "links"=>[], "tags"=>["inhibitors", "tested", "prp", "degradation", "by", "lichen"], "article_id"=>446734, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.t001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Protease_inhibitors_tested_to_interfere_with_PrP_degradation_by____lichen_extracts_/446734", "title"=>"Protease inhibitors tested to interfere with PrP degradation by\n lichen extracts.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 18:32:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/776121"], "description"=>"<p>Samples of PTA-enriched PrP<sup>TSE</sup> (30 µg total protein)\n were incubated with the indicated concentrations of lecanoric acid (LA),\n usnic acid, atranorin or vehicle followed by immunoblot analysis with\n mAb 3F4. <i>P. sulcata</i> extract (10 mg lichen equivalent)\n served as a positive control for PrP degradation.</p>", "links"=>[], "tags"=>["lichen", "chemicals", "prp"], "article_id"=>446487, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Common_lichen_chemicals_do_not_affect_PrP_levels_/446487", "title"=>"Common lichen chemicals do not affect PrP levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:31:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/776312"], "description"=>"<p>(A) Freshly-collected <i>P. sulcata</i> or <i>P.\n squarrosa</i> (4 mg, each) were incubated with infected brain\n homogenate (100 µL of 10% v/w in distilled water) for 24 h.\n Following incubation, the lichen-treated brain homogenates (sup) and the\n lichen tissues (pel) were analyzed for PrP by immunoblotting with mAb\n 3F4. A reduction in PrP signal was associated with <i>P.\n sulcata</i>, but not with <i>P. squarrosa</i>. (B)\n PTA-enriched PrP<sup>TSE</sup> (30 µg total protein) exposed to\n chitin beads is bound by the beads, but is extractable using NuPAGE\n sample buffer. Little immunoreactivity in the supernatant (sup) shows\n the protein binds chitin and treatment of bound PrP with sample buffer\n yields immunoreactivity approximately equal to PrP starting material.\n (C) A water extract from <i>P. sulcata</i>, but not <i>P.\n squarrosa</i>, causes PrP degradation. Immunoblotting\n comparison of PTA-enriched PrP<sup>TSE</sup> (30 µg total protein)\n incubated in only water or exposed to a water extract of <i>P.\n sulcata</i> (100 mg lichen equivalent) with and without the\n serine protease inhibitor Pefabloc SC (10 mM). Water extract of\n <i>P. sulcata</i> induces a substantial reduction of\n immunoreactivity that is blocked by PefaBloc SC whereas a water extract\n of the related lichen <i>P. squarrosa</i> does not degrade PrP\n under the same conditions.</p>", "links"=>[], "tags"=>["extract", "the", "lichen", "degrades"], "article_id"=>446675, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g009", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intact_P_sulcata_tissue_or_a_water_extract_of_the____lichen_degrades_PrP_/446675", "title"=>"Intact <i>P. sulcata</i> tissue or a water extract of the\n lichen degrades PrP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:32:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/775922"], "description"=>"<p>(A) The extent of mouse RML PrP<sup>TSE</sup> degradation was measured by\n PMCA analysis of dilutions\n (10<sup>−2</sup>–10<sup>−6</sup>) of vehicle or\n <i>L. pulmonaria</i> extract-treated RML. (B) Control\n reactions lacking PrP<sup>TSE</sup> seed or sonication did not show\n amplification as measured by PK digestion. (C) RML samples were\n incubated with vehicle for 1 hr or with <i>L. pulmonaria</i>\n extract (reacted: 1 hr; spiked <10 sec) then diluted and subjected to\n PMCA. Adding <i>L. pulmonaria</i> extract in PMCA reactions\n without allowing time for reaction (spiked samples) does not appear to\n reduce PrP<sup>TSE</sup> levels or affect amplification compared to\n control (vehicle). All immunoblots used mAb SAF83.</p>", "links"=>[], "tags"=>["pmca", "rml"], "article_id"=>446289, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Semi_quantitative_PMCA_to_assess_RML_PrP_TSE____degradation_/446289", "title"=>"Semi-quantitative PMCA to assess RML PrP<sup>TSE</sup>\n degradation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:30:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/775768"], "description"=>"<p>Equivalent amounts of PTA-enriched PrP<sup>TSE</sup> (30 µg total\n protein) were incubated with the indicated lichen extracts (labels, 10\n mg lichen equivalents) or with vehicle and were subjected to NuPAGE and\n immunoblotting. Extracts of lichens in panel (A) reduced PrP\n immunoreactivity compared to control, whereas extracts of lichens in\n panel (B) do not reduce PrP immunoreactivity. (C) Treatment of\n PrP<sup>TSE</sup> using the method employed in panels (A) and (B)\n with extracts of isolated algae or cyanobacterium cultures (10 mg\n equivalents) do not degrade PrP. (D) Dilutions of control reactions\n containing PrP<sup>TSE</sup> and no lichen extract indicate that PrP\n immunoreactivity was no longer detectable when dilution factors were\n greater than 100. (E) Adding <i>P. sulcata</i> extract to\n PrP<sup>TSE</sup>, but not allowing it time to react (spiked) did\n not reduce PrP immunoreactivity compared to control (vehicle).\n Equivalent samples in which <i>P. sulcata</i> extract was\n allowed time to incubate (reacted) did not have detectable PrP\n immunoreactivity. (F–H) Methods to remove lichen compounds and\n DMSO from samples post-reaction, such as (F) washing remaining protein\n with PBS using a centricon filter column (10–12 kDa MWCO) or (G\n & H) precipitating protein using methanol (MeOH) or trichloroacetic\n acid (TCA) do not restore PrP immunoreactivity. All immunoblots (IB)\n used anti-PrP mAb 3F4, except for panel (A) which used both 3F4 and\n SAF84.</p>", "links"=>[], "tags"=>["lichens", "degrade"], "article_id"=>446130, "categories"=>["Microbiology", "Biochemistry", "Infectious Diseases", "Plant Biology", "Biotechnology", "Chemistry"], "users"=>["Christopher J. Johnson", "James P. Bennett", "Steven M. Biro", "Juan Camilo Duque-Velasquez", "Cynthia M. Rodriguez", "Richard A. Bessen", "Tonie E. Rocke"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0019836.g001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Extracts_of_the_lichens_P_sulcata_C_____rangiferina_and_L_pulmonaria_degrade____PrP_/446130", "title"=>"Extracts of the lichens <i>P. sulcata</i>, <i>C.\n rangiferina</i> and <i>L. pulmonaria</i> degrade\n PrP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 18:29:17"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"28", "full-text"=>"29", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
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  • {"unique-ip"=>"40", "full-text"=>"44", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"30", "full-text"=>"35", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"28", "full-text"=>"36", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"36", "full-text"=>"39", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2019", "month"=>"10"}
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  • {"unique-ip"=>"31", "full-text"=>"42", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2020", "month"=>"2"}
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  • {"unique-ip"=>"32", "full-text"=>"38", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"27", "full-text"=>"28", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
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Relative Metric

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