Double NF1 Inactivation Affects Adrenocortical Function in NF1Prx1 Mice and a Human Patient
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{"title"=>"Double NF1 inactivation affects adrenocortical function in NF1Prx1 mice and a human patient", "type"=>"journal", "authors"=>[{"first_name"=>"Karolina", "last_name"=>"Kobus", "scopus_author_id"=>"56196934600"}, {"first_name"=>"Daniela", "last_name"=>"Hartl", "scopus_author_id"=>"36192809100"}, {"first_name"=>"Claus Eric", "last_name"=>"Ott", "scopus_author_id"=>"15835410400"}, {"first_name"=>"Monika", "last_name"=>"Osswald", "scopus_author_id"=>"57196609522"}, {"first_name"=>"Angela", "last_name"=>"Huebner", "scopus_author_id"=>"7007176577"}, {"first_name"=>"Maja", "last_name"=>"Von Der Hagen", "scopus_author_id"=>"10142042500"}, {"first_name"=>"Denise", "last_name"=>"Emmerich", "scopus_author_id"=>"56387165200"}, {"first_name"=>"Jirko", "last_name"=>"Kühnisch", "scopus_author_id"=>"16836725900"}, {"first_name"=>"Hans", "last_name"=>"Morreau", "scopus_author_id"=>"7004153007"}, {"first_name"=>"Frederik J.", "last_name"=>"Hes", "scopus_author_id"=>"6602903359"}, {"first_name"=>"Victor F.", "last_name"=>"Mautner", "scopus_author_id"=>"7005686458"}, {"first_name"=>"Anja", "last_name"=>"Harder", "scopus_author_id"=>"7006700529"}, {"first_name"=>"Sigrid", "last_name"=>"Tinschert", "scopus_author_id"=>"7004017497"}, {"first_name"=>"Stefan", "last_name"=>"Mundlos", "scopus_author_id"=>"7005248176"}, {"first_name"=>"Mateusz", "last_name"=>"Kolanczyk", "scopus_author_id"=>"11339613300"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"603024271", "doi"=>"10.1371/journal.pone.0119030", "sgr"=>"84925014350", "pmid"=>"25775093", "scopus"=>"2-s2.0-84925014350"}, "id"=>"5155be88-c2f7-36bf-a9cc-526a9fb8f258", "abstract"=>"BACKGROUND: Neurofibromatosis type I (NF1, MIM#162200) is a relatively frequent genetic condition, which predisposes to tumor formation. Apart from tumors, individuals with NF1 often exhibit endocrine abnormalities such as precocious puberty (2,5-5% of NF1 patients) and some cases of hypertension (16% of NF1 patients). Several cases of adrenal cortex adenomas have been described in NF1 individuals supporting the notion that neurofibromin might play a role in adrenal cortex homeostasis. However, no experimental data were available to prove this hypothesis.\\n\\nMATERIALS AND METHODS: We analysed Nf1Prx1 mice and one case of adrenal cortical hyperplasia in a NF1patient.\\n\\nRESULTS: In Nf1Prx1 mice Nf1 is inactivated in the developing limbs, head mesenchyme as well as in the adrenal gland cortex, but not the adrenal medulla or brain. We show that adrenal gland size is increased in NF1Prx1 mice. Nf1Prx1 female mice showed corticosterone and aldosterone overproduction. Molecular analysis of Nf1 deficient adrenals revealed deregulation of multiple proteins, including steroidogenic acute regulatory protein (StAR), a vital mitochondrial factor promoting transfer of cholesterol into steroid making mitochondria. This was associated with a marked upregulation of MAPK pathway and a female specific increase of cAMP concentration in murine adrenal lysates. Complementarily, we characterized a patient with neurofibromatosis type I with macronodular adrenal hyperplasia with ACTH-independent cortisol overproduction. Comparison of normal control tissue- and adrenal hyperplasia- derived genomic DNA revealed loss of heterozygosity (LOH) of the wild type NF1 allele, showing that biallelic NF1 gene inactivation occurred in the hyperplastic adrenal gland.\\n\\nCONCLUSIONS: Our data suggest that biallelic loss of Nf1 induces autonomous adrenal hyper-activity. We conclude that Nf1 is involved in the regulation of adrenal cortex function in mice and humans.", "link"=>"http://www.mendeley.com/research/double-nf1-inactivation-affects-adrenocortical-function-nf1prx1-mice-human-patient", "reader_count"=>9, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>4, "Student > Ph. D. Student"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Mathematics"=>1, "Agricultural and Biological Sciences"=>2, "Medicine and Dentistry"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>2}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Belgium"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1950155"], "description"=>"<p>(A) Expression of Akr1b7 labelling zona fasciculata and zona reticularis in the Nf1Prx1 adrenals. Paraffin sections of Nf1Prx1 and control adrenal glands immunostained for Akr1b7 (green) and counterstained with DAPI (blue). Note changes in the cell morphology of the zona fasciculata in mutant (graphically represented in the inset panels on the left) and abnormal expression pattern of Akr1b7 in the mutant cortex as compared to control specimens (white interrupted line and orange arrows). C.) qPCR measurement of the Akr1b7 gene expression in adrenal glands of Nf1Prx1. Expression was measured in six adrenal glands of female and male mice of both genotypes. T-test with Welch’s correction: 3 asterisks: p<0,001.</p>", "links"=>[], "tags"=>["mim", "type NF 1 allele", "NF 1 patients", "biallelic NF 1 gene inactivation", "NF 1patient Nf 1Prx mice Nf 1", "Human Patient BackgroundNeurofibromatosis type", "Double NF 1 Inactivation Affects Adrenocortical Function", "NF 1Prx Mice", "NF 1 individuals", "NF 1", "dna", "mapk", "loh", "cortex"], "article_id"=>1336877, "categories"=>["Biological Sciences"], "users"=>["Karolina Kobus", "Daniela Hartl", "Claus Eric Ott", "Monika Osswald", "Angela Huebner", "Maja von der Hagen", "Denise Emmerich", "Jirko Kühnisch", "Hans Morreau", "Frederik J. Hes", "Victor F. Mautner", "Anja Harder", "Sigrid Tinschert", "Stefan Mundlos", "Mateusz Kolanczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0119030.g003", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_adrenal_cortex_morphology_in_Nf1Prx1_mice_/1336877", "title"=>"Changes in adrenal cortex morphology in Nf1Prx1 mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-16 04:09:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1950154"], "description"=>"<p>(A) Macroscopic appearance of the representative female control and mutant adrenal glands. (B) Increased adrenal gland weight in female Nf1Prx1 mice. (C) Representative H&E staining of adrenal glands from 2-month-old female wt and Nf1Prx1 mice. Higher magnification illustrating, thicker and structurally irregular and disorganized adrenal cortex in comparison with control mice (lower panel). (D) Azan stained sections. Increased thickness of the (ZR) zona reticularis and (ZF) zona fasciculata in the adrenals of mutant Nf1Prx1 mice. (E, F, G) ELISA based quantitative analysis of the serum corticosterone and Aldosterone levels. Note a female specific increase of the corticosterone and Aldosterone level (measured 9–11 a.m.) Statistical evaluation was done with T-test with Welch’s correction.</p>", "links"=>[], "tags"=>["mim", "type NF 1 allele", "NF 1 patients", "biallelic NF 1 gene inactivation", "NF 1patient Nf 1Prx mice Nf 1", "Human Patient BackgroundNeurofibromatosis type", "Double NF 1 Inactivation Affects Adrenocortical Function", "NF 1Prx Mice", "NF 1 individuals", "NF 1", "dna", "mapk", "loh", "cortex"], "article_id"=>1336876, "categories"=>["Biological Sciences"], "users"=>["Karolina Kobus", "Daniela Hartl", "Claus Eric Ott", "Monika Osswald", "Angela Huebner", "Maja von der Hagen", "Denise Emmerich", "Jirko Kühnisch", "Hans Morreau", "Frederik J. Hes", "Victor F. Mautner", "Anja Harder", "Sigrid Tinschert", "Stefan Mundlos", "Mateusz Kolanczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0119030.g002", "stats"=>{"downloads"=>1, "page_views"=>144, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_weight_of_adrenal_glands_and_defects_of_adrenal_cortex_zonation_in_the_female_Nf1Prx1_mice_/1336876", "title"=>"Increased weight of adrenal glands and defects of adrenal cortex zonation in the female Nf1Prx1 mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-16 04:09:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1950159", "https://ndownloader.figshare.com/files/1950160"], "description"=>"<div><p>Background</p><p>Neurofibromatosis type I (NF1, MIM#162200) is a relatively frequent genetic condition, which predisposes to tumor formation. Apart from tumors, individuals with NF1 often exhibit endocrine abnormalities such as precocious puberty (2,5–5% of NF1 patients) and some cases of hypertension (16% of NF1 patients). Several cases of adrenal cortex adenomas have been described in NF1 individuals supporting the notion that neurofibromin might play a role in adrenal cortex homeostasis. However, no experimental data were available to prove this hypothesis.</p><p>Materials and Methods</p><p>We analysed Nf1Prx1 mice and one case of adrenal cortical hyperplasia in a NF1patient.</p><p>Results</p><p>In Nf1Prx1 mice <i>Nf1</i> is inactivated in the developing limbs, head mesenchyme as well as in the adrenal gland cortex, but not the adrenal medulla or brain. We show that adrenal gland size is increased in NF1Prx1 mice. Nf1Prx1 female mice showed corticosterone and aldosterone overproduction. Molecular analysis of Nf1 deficient adrenals revealed deregulation of multiple proteins, including steroidogenic acute regulatory protein (StAR), a vital mitochondrial factor promoting transfer of cholesterol into steroid making mitochondria. This was associated with a marked upregulation of MAPK pathway and a female specific increase of cAMP concentration in murine adrenal lysates. Complementarily, we characterized a patient with neurofibromatosis type I with macronodular adrenal hyperplasia with ACTH-independent cortisol overproduction. Comparison of normal control tissue- and adrenal hyperplasia- derived genomic DNA revealed loss of heterozygosity (LOH) of the wild type <i>NF1</i> allele, showing that biallelic <i>NF1</i> gene inactivation occurred in the hyperplastic adrenal gland.</p><p>Conclusions</p><p>Our data suggest that biallelic loss of <i>Nf1</i> induces autonomous adrenal hyper-activity. We conclude that <i>Nf1</i> is involved in the regulation of adrenal cortex function in mice and humans.</p></div>", "links"=>[], "tags"=>["mim", "type NF 1 allele", "NF 1 patients", "biallelic NF 1 gene inactivation", "NF 1patient Nf 1Prx mice Nf 1", "Human Patient BackgroundNeurofibromatosis type", "Double NF 1 Inactivation Affects Adrenocortical Function", "NF 1Prx Mice", "NF 1 individuals", "NF 1", "dna", "mapk", "loh", "cortex"], "article_id"=>1336881, "categories"=>["Biological Sciences"], "users"=>["Karolina Kobus", "Daniela Hartl", "Claus Eric Ott", "Monika Osswald", "Angela Huebner", "Maja von der Hagen", "Denise Emmerich", "Jirko Kühnisch", "Hans Morreau", "Frederik J. Hes", "Victor F. Mautner", "Anja Harder", "Sigrid Tinschert", "Stefan Mundlos", "Mateusz Kolanczyk"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0119030.s001", "https://dx.doi.org/10.1371/journal.pone.0119030.s002"], "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Double_NF1_Inactivation_Affects_Adrenocortical_Function_in_NF1Prx1_Mice_and_a_Human_Patient_/1336881", "title"=>"Double NF1 Inactivation Affects Adrenocortical Function in NF1Prx1 Mice and a Human Patient", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-03-16 04:09:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1950157"], "description"=>"<p>A.) Densitometry based quantification of the western blots showing relative expression intensity of pMEK1 vs. MEK1 and pERK1/2 vs. ERK1/2. The upper inserts show representative bands of the female adrenal gland analysis. B.) Quantitative 2D-gel based analysis of the StAR expression level. 2D gels were performed with whole organ lysates of six control and six mutant murine adrenal glands. Relative spot intensity was determined with densitometry. The spots were identified with help of mass spectrometry as described in methods C.) Quantitative Western blot analysis of pStAR vs. StAR expression level in the adrenal glands from three months old Nf1Prx1 and control mice. The number of adrenal gland lysates used per genotype is given in the graph for each experiment. Band intensities were measured densitometrically and band intensity ratios were calculated. D.) 2D gel Western blot analysis of pStAR and StAR expression in female adrenal glands. Note increased phosphorylation of multiple StAR isoforms in the lysates of Nf1Prx1 adrenal glands. E.) ELISA determined concentrations of cAMP per mg of protein in the whole organ lysates from adrenal glands of three months old mice. T-test with Welch’s correction: 1 asterisks: p<0.1; 2 asterisks: p<0.01; 3 asterisks: p<0.001.</p>", "links"=>[], "tags"=>["mim", "type NF 1 allele", "NF 1 patients", "biallelic NF 1 gene inactivation", "NF 1patient Nf 1Prx mice Nf 1", "Human Patient BackgroundNeurofibromatosis type", "Double NF 1 Inactivation Affects Adrenocortical Function", "NF 1Prx Mice", "NF 1 individuals", "NF 1", "dna", "mapk", "loh", "cortex"], "article_id"=>1336879, "categories"=>["Biological Sciences"], "users"=>["Karolina Kobus", "Daniela Hartl", "Claus Eric Ott", "Monika Osswald", "Angela Huebner", "Maja von der Hagen", "Denise Emmerich", "Jirko Kühnisch", "Hans Morreau", "Frederik J. Hes", "Victor F. Mautner", "Anja Harder", "Sigrid Tinschert", "Stefan Mundlos", "Mateusz Kolanczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0119030.g005", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MAPK_activation_StAR_overexpression_and_StAR_hyperphosphorylation_in_the_Nf1Prx1_female_adrenal_glands_/1336879", "title"=>"MAPK activation StAR overexpression and StAR hyperphosphorylation in the Nf1Prx1 female adrenal glands.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-16 04:09:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1950158"], "description"=>"<p>A.) Surgically removed adrenal gland of the 30 years old NF1 patient with yellow coloured adrenal hyperplasia. B.) Azan stained section of the adrenal tissue showing border between hyperplastic and healthy adrenal cortex tissue. C.) Sanger sequencing showing mixed sequences of the wt allele and c.405delG mutation in the blood (same in normally part of the adrenal gland) and a loss of heterozygosity detected in the hyperplastic part of the adrenal gland. D.) Real time quantitative PCR measuring gene copy number throughout chromosme 17 and on the control chromosomes. The mean values were calculated for each amplicon relative to albumin (ALB) on 4q11 as autosomal two-copy control. Error bars indicate the 95% confidence interval as given by the ABI 7900 SDS-Software. Results were calibrated to the mean values of a healthy control tissue (white bars). Decreased signal intensities were obtained in two hyperplastic adrenal tissue samples (grey bars) for all amplicons on chromosome 17 including amplicons for NF1 type1 deletions (CPD, RHOT1), NF1 type 2 deletions (SUZ12P, SUZ12), an amplicon localized upon the NF1 mutation detected by sequencing (NF1-exon4), and an amplicon on the short arm of chromosome 17 (17p12). In contrast, control amplicons localized on chromosome 6 (6p21.1, 6q21) and the X chromosome (Xq28) revealed normal signal intensities. These results indicate that a complete loss of chromosome 17 lead to NF1 loss of heterozygosity (LOH) detected by sequencing analysis. Copy-number analyses were repeated twice with similar results and confirmed using additional qPCR amplicons (not shown).</p>", "links"=>[], "tags"=>["mim", "type NF 1 allele", "NF 1 patients", "biallelic NF 1 gene inactivation", "NF 1patient Nf 1Prx mice Nf 1", "Human Patient BackgroundNeurofibromatosis type", "Double NF 1 Inactivation Affects Adrenocortical Function", "NF 1Prx Mice", "NF 1 individuals", "NF 1", "dna", "mapk", "loh", "cortex"], "article_id"=>1336880, "categories"=>["Biological Sciences"], "users"=>["Karolina Kobus", "Daniela Hartl", "Claus Eric Ott", "Monika Osswald", "Angela Huebner", "Maja von der Hagen", "Denise Emmerich", "Jirko Kühnisch", "Hans Morreau", "Frederik J. Hes", "Victor F. Mautner", "Anja Harder", "Sigrid Tinschert", "Stefan Mundlos", "Mateusz Kolanczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0119030.g006", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Loss_of_heterozygosity_in_NF1_locus_associates_with_adrenal_macronodular_hyperplasia_and_cortisol_overproduction_in_NF1_female_patient_/1336880", "title"=>"Loss of heterozygosity in NF1 locus associates with adrenal macronodular hyperplasia and cortisol overproduction in NF1 female patient.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-16 04:09:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1950156"], "description"=>"<p>(A) qPCR based determination of the expression of genes involved in corticosteroid synthesis. Note decreased expression of StAR, Cyp11b1 and Cyp21a1 genes, which are involved in corticosterone synthesis and increased expression of Hsd3b6, the gene involved in aldosterone synthesis in female Nf1Prx1 adrenal glands. T-test with Welch’s correction: 1 asterisks: p<0.1; 2 asterisks: p<0.01; 3 asterisks: p<0.001. (B) A diagram of the corticosterone synthesis pathway depicting synthesis steps and major genes involved in the catalysis. Gene deregulations detected by the qPCR in the adrenal glands of Nf1Prx1 mice are indicated with red arrows.</p>", "links"=>[], "tags"=>["mim", "type NF 1 allele", "NF 1 patients", "biallelic NF 1 gene inactivation", "NF 1patient Nf 1Prx mice Nf 1", "Human Patient BackgroundNeurofibromatosis type", "Double NF 1 Inactivation Affects Adrenocortical Function", "NF 1Prx Mice", "NF 1 individuals", "NF 1", "dna", "mapk", "loh", "cortex"], "article_id"=>1336878, "categories"=>["Biological Sciences"], "users"=>["Karolina Kobus", "Daniela Hartl", "Claus Eric Ott", "Monika Osswald", "Angela Huebner", "Maja von der Hagen", "Denise Emmerich", "Jirko Kühnisch", "Hans Morreau", "Frederik J. Hes", "Victor F. Mautner", "Anja Harder", "Sigrid Tinschert", "Stefan Mundlos", "Mateusz Kolanczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0119030.g004", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_corticosteroid_gene_expression_in_adrenal_glands_of_Nf1Prx1_mice_/1336878", "title"=>"Changes in corticosteroid gene expression in adrenal glands of Nf1Prx1 mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-16 04:09:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1950153"], "description"=>"<p>Whole mount LacZ staining showing a mosaic Cre-mediated recombination in adrenal cortex (dotted line) of 5-weeks-old Rosa26-lacZ reporter x Prx1-Cre mice. (B) Similar mosaic Cre recombination in the adrenal cortex visualized with mT/mG reporter mice. Note, no recombination was observed in the medulla. (C) PCR-based detection of recombined allele in the genomic DNA of 2-month-old Nf1Prx1 animals with varying degree of inactivation in the individual adrenal glands. Knock-out efficiency in the individual Nf1Prx1 adrenal glands assessed by quantitative RT-PCR. Note, out of 12 analysed mutant adrenal glands only one showed less than 30% efficiency of NF1 inactivation. c—cortex, m—medulla, f- fat, L- liver.</p>", "links"=>[], "tags"=>["mim", "type NF 1 allele", "NF 1 patients", "biallelic NF 1 gene inactivation", "NF 1patient Nf 1Prx mice Nf 1", "Human Patient BackgroundNeurofibromatosis type", "Double NF 1 Inactivation Affects Adrenocortical Function", "NF 1Prx Mice", "NF 1 individuals", "NF 1", "dna", "mapk", "loh", "cortex"], "article_id"=>1336875, "categories"=>["Biological Sciences"], "users"=>["Karolina Kobus", "Daniela Hartl", "Claus Eric Ott", "Monika Osswald", "Angela Huebner", "Maja von der Hagen", "Denise Emmerich", "Jirko Kühnisch", "Hans Morreau", "Frederik J. Hes", "Victor F. Mautner", "Anja Harder", "Sigrid Tinschert", "Stefan Mundlos", "Mateusz Kolanczyk"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0119030.g001", "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NF1_inactivation_in_the_adrenal_gland_cortex_/1336875", "title"=>"NF1 inactivation in the adrenal gland cortex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-03-16 04:09:16"}

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  • {"unique-ip"=>"26", "full-text"=>"26", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"13", "full-text"=>"14", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"23", "full-text"=>"22", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"18", "full-text"=>"21", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"11", "full-text"=>"13", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"27", "full-text"=>"32", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"1", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}

Relative Metric

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