Coordinated Activation of Candidate Proto-Oncogenes and Cancer Testes Antigens via Promoter Demethylation in Head and Neck Cancer and Lung Cancer
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{"title"=>"Coordinated activation of candidate proto-oncogenes and cancer testes antigens via promoter demethylation in head and neck cancer and lung cancer", "type"=>"journal", "authors"=>[{"first_name"=>"Ian M.", "last_name"=>"Smith", "scopus_author_id"=>"55987636200"}, {"first_name"=>"Chad A.", "last_name"=>"Glazer", "scopus_author_id"=>"11541146100"}, {"first_name"=>"Suhail K.", "last_name"=>"Mithani", "scopus_author_id"=>"12775884100"}, {"first_name"=>"Michael F.", "last_name"=>"Ochs", "scopus_author_id"=>"7006272363"}, {"first_name"=>"Wenyue", "last_name"=>"Sun", "scopus_author_id"=>"16550764200"}, {"first_name"=>"Sheetal", "last_name"=>"Bhan", "scopus_author_id"=>"26424553500"}, {"first_name"=>"Alexander", "last_name"=>"Vostrov", "scopus_author_id"=>"6603030515"}, {"first_name"=>"Ziedulla", "last_name"=>"Abdullaev", "scopus_author_id"=>"6701441857"}, {"first_name"=>"Victor", "last_name"=>"Lobanenkov", "scopus_author_id"=>"56920550900"}, {"first_name"=>"Andrew", "last_name"=>"Gray", "scopus_author_id"=>"55628575311"}, {"first_name"=>"Chunyan", "last_name"=>"Liu", "scopus_author_id"=>"57191676729"}, {"first_name"=>"Steven S.", "last_name"=>"Chang", "scopus_author_id"=>"23967943100"}, {"first_name"=>"Kimberly L.", "last_name"=>"Ostrow", "scopus_author_id"=>"6601961146"}, {"first_name"=>"William H.", "last_name"=>"Westra", "scopus_author_id"=>"7006754834"}, {"first_name"=>"Shahnaz", "last_name"=>"Begum", "scopus_author_id"=>"7101852533"}, {"first_name"=>"Mousumi", "last_name"=>"Dhara", "scopus_author_id"=>"55784487600"}, {"first_name"=>"Joseph", "last_name"=>"Califano", "scopus_author_id"=>"35426134100"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"63349100797", "isbn"=>"1932-6203 (Electronic)", "doi"=>"10.1371/journal.pone.0004961", "pmid"=>"19305507", "scopus"=>"2-s2.0-63349100797", "issn"=>"19326203", "pui"=>"354396058"}, "id"=>"fa3c55de-0556-36f1-ad56-d3228d62e3a5", "abstract"=>"BACKGROUND Epigenetic alterations have been implicated in the pathogenesis of solid tumors, however, proto-oncogenes activated by promoter demethylation have been sporadically reported. We used an integrative method to analyze expression in primary head and neck squamous cell carcinoma (HNSCC) and pharmacologically demethylated cell lines to identify aberrantly demethylated and expressed candidate proto-oncogenes and cancer testes antigens in HNSCC. METHODOLOGY/PRINCIPAL FINDINGS We noted coordinated promoter demethylation and simultaneous transcriptional upregulation of proto-oncogene candidates with promoter homology, and phylogenetic footprinting of these promoters demonstrated potential recognition sites for the transcription factor BORIS. Aberrant BORIS expression correlated with upregulation of candidate proto-oncogenes in multiple human malignancies including primary non-small cell lung cancers and HNSCC, induced coordinated proto-oncogene specific promoter demethylation and expression in non-tumorigenic cells, and transformed NIH3T3 cells. CONCLUSIONS/SIGNIFICANCE Coordinated, epigenetic unmasking of multiple genes with growth promoting activity occurs in aerodigestive cancers, and BORIS is implicated in the coordinated promoter demethylation and reactivation of epigenetically silenced genes in human cancers.", "link"=>"http://www.mendeley.com/research/coordinated-activation-candidate-protooncogenes-cancer-testes-antigens-via-promoter-demethylation-he", "reader_count"=>43, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>4, "Other"=>2, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>4, "Other"=>2, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>7, "Medicine and Dentistry"=>6, "Agricultural and Biological Sciences"=>20, "Veterinary Science and Veterinary Medicine"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Germany"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/447417", "https://ndownloader.figshare.com/files/447438", "https://ndownloader.figshare.com/files/447461", "https://ndownloader.figshare.com/files/447473", "https://ndownloader.figshare.com/files/447489"], "description"=>"<div><h3>Background</h3><p>Epigenetic alterations have been implicated in the pathogenesis of solid tumors, however, proto-oncogenes activated by promoter demethylation have been sporadically reported. We used an integrative method to analyze expression in primary head and neck squamous cell carcinoma (HNSCC) and pharmacologically demethylated cell lines to identify aberrantly demethylated and expressed candidate proto-oncogenes and cancer testes antigens in HNSCC.</p><h3>Methodology/Principal Findings</h3><p>We noted coordinated promoter demethylation and simultaneous transcriptional upregulation of proto-oncogene candidates with promoter homology, and phylogenetic footprinting of these promoters demonstrated potential recognition sites for the transcription factor BORIS. Aberrant BORIS expression correlated with upregulation of candidate proto-oncogenes in multiple human malignancies including primary non-small cell lung cancers and HNSCC, induced coordinated proto-oncogene specific promoter demethylation and expression in non-tumorigenic cells, and transformed NIH3T3 cells.</p><h3>Conclusions/Significance</h3><p>Coordinated, epigenetic unmasking of multiple genes with growth promoting activity occurs in aerodigestive cancers, and BORIS is implicated in the coordinated promoter demethylation and reactivation of epigenetically silenced genes in human cancers.</p></div>", "links"=>[], "tags"=>["coordinated", "activation", "proto-oncogenes", "cancer", "testes", "antigens", "promoter", "demethylation"], "article_id"=>148173, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.s001", "https://dx.doi.org/10.1371/journal.pone.0004961.s002", "https://dx.doi.org/10.1371/journal.pone.0004961.s003", "https://dx.doi.org/10.1371/journal.pone.0004961.s004", "https://dx.doi.org/10.1371/journal.pone.0004961.s005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Coordinated_Activation_of_Candidate_Proto_Oncogenes_and_Cancer_Testes_Antigens_via_Promoter_Demethylation_in_Head_and_Neck_Cancer_and_Lung_Cancer/148173", "title"=>"Coordinated Activation of Candidate Proto-Oncogenes and Cancer Testes Antigens via Promoter Demethylation in Head and Neck Cancer and Lung Cancer", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-03-23 02:16:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/903112"], "description"=>"<p>(a) Initially, minimally-transformed cell lines were treated with 5-aza-deoxycytidine and TSA to unmask epigenetically silenced genes. In order to correlate epigenetic unmasking with meaningful upregulated cancer-specific genes, we performed a comparative epigenetic approach with Cancer Outlier Profiling Analysis (COPA) using 49 tumors and 19 normal tissues that had been characterized on the Affymetrix U133A mRNA expression microarray platform. Genes (by probeset) were ranked first by degree of upfold regulation with 5-aza/TSA treatment and second by COPA upregulation at the 90<sup>th</sup> percentile. The product of these ranks was used to rank all targets and a significance threshold (α = 0.005) was chosen resulting in 106 genes of which the top 26 genes were evaluated. In order to not exclude genes outside the U133A platform, we also considered all other genes in the U133 Plus 2.0 platform on the sole basis of 5-aza/TSA upfold regulation. Genes were subsequently screened by presence of CpG islands using MethPrimer and all genes were validated by bisulfite sequencing of tumor and normal tissues, and QRT-PCR of cell lines and primary tumors. Of the integrative targets 7/26 passed our validation, while 2/46 of the non-integrative targets passed. Functional experiments were then conducted on these genes. (b) Representative COPA graph of <i>MAGEA3</i> demonstrating the statistical approach to finding candidate overexpressed oncogenes. Difference in tumor (n = 49) versus normal (n = 19) expression was significant, p value<0.001 measured by Mann-Whitney U test. (c) Promoter demethylation causes transcriptional upregulation. Upregulation after treatment with 5-aza/TSA is shown in cell lines as measured by QRT-PCR. The ratio of 5-aza/TSA treated expression to baseline is shown for <i>C19ORF28</i>, <i>H19</i>, <i>TKLT1</i>, <i>GPR17</i>, <i>GRIN1</i>, <i>MAGEA2</i>, <i>MAGEA3/6</i>, <i>MAGEA4</i>, <i>MAGEA11</i>. Each gene demonstrated significant upregulation by 5-aza/TSA treatment in at least one cell-line. Error bars show SE.</p>", "links"=>[], "tags"=>["epigenetic", "validation"], "article_id"=>573542, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Integrative_epigenetic_screening_strategy_and_strategy_for_validation_of_targets_/573542", "title"=>"Integrative epigenetic screening strategy and strategy for validation of targets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-23 00:59:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/903268"], "description"=>"<p>(a) Shown are the bisulfite sequencing results in 10 tumors and 10 normals for: <i>TKTL1</i> (4/10, p<0.05), <i>H19</i> (6/10, p<0.05), <i>MAGEA2</i> (5/10, p<0.05), <i>MAGEA3/6</i> (5/10, p<0.05), <i>MAGEA4</i> (5/10, p<0.05), <i>MAGEA11</i> (5/10, p<0.05), <i>GPR17</i> (3/10, p<0.10), <i>GRIN1</i> (6/10, p<0.05), <i>C19ORF28</i> (5/10, p<0.05). (b–j) QRT-PCR expression with the bisulfite sequencing of the respective promoter below (white is unmethylated, grey is methylated). Significance was measured by comparison of expression of methylated to unmethylated by Mann-Whitney U test. Significance was found in MAGEA2 (p = 0.007), MAGEA3/6 (p = 0.007), MAGEA11 (p = 0.05). Strong associations between expression and promoter methylation status were also found for TKTL1 (p = 0.06), MAGEA4 (p = 0.09), C19ORF28 (p = 0.09), GRIN1 (p = 0.06). H19 (p = 0.7) and GPR17 (p = 0.38) did not show associations between bisulfite sequencing and expression in this cohort. Error bars depict standard error.</p>", "links"=>[], "tags"=>["methylation"], "article_id"=>573704, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Promoter_methylation_status_in_primary_tissues_/573704", "title"=>"Promoter methylation status in primary tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-23 01:01:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/903368"], "description"=>"<p>(a) Transient transfection of an <i>H19</i> construct into OKF6-Tert-1R cells (at day 4, 41.4%±15% growth increase). (b) Transient transfection of an <i>MAGEA2</i> construct into OKF6-Tert-1R cells (at day 3, 72.7%±26% growth increase). (c) Transient transfection of an <i>TKTL1</i> construct into OKF6-Tert-1R cells(at day 4, 50.1%±38% growth increase). (d) Transient transfection of <i>MAGEA4</i> construct into OKF6-Tert-1R cells (at day 4, 203%±17% growth increase). For (e) we developed a quantitative assay for measuring unmethylated promoters, termed Quantitative Unmethylation-Specific PCR (QUMSP). QUMSP percentage of <i>C19ORF28</i>, <i>GRIN1</i>, <i>H19</i>, <i>MAGEA11</i>, <i>MAGEA2</i>, <i>MAGEA3/6</i>, <i>GPR17</i>, and <i>TKTL1</i> was conducted in a separate cohort of head and neck cancer patients using 25 tumors and 11 upper aerodigestive mucosal samples to assay promoter demethylation. Statistically significant differences were found in <i>GRIN1</i>, <i>MAGEA11</i>, <i>MAGEA2</i>. Next promoter demethylation was considered as a cause of mRNA expression increases seen in the expO dataset. (f) shows the QUMSP results for an independent cohort of 14 lung normals and 13 lung tumor patients. Significant differences in QUMSP were found in <i>H19</i>, <i>MAGEA11</i>, <i>MAGEA2</i>, and <i>MAGEA3/6</i>.</p>", "links"=>[], "tags"=>["transfection", "genes", "minimally", "transformed"], "article_id"=>573806, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transient_transfection_of_target_genes_in_minimally_transformed_oral_keratinocytes_/573806", "title"=>"Transient transfection of target genes in minimally transformed oral keratinocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-23 01:03:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/903555"], "description"=>"<p>(a) TKTL1 forced overexpression via transient transfection in background low expressing JHU-011 cells induces increased anchorage dependent colony formation and (b) TKTL1 shRNA in high-expressing FaDu cell line induces growth inhibition. (c) Anchorage independent growth of UM-22B cells is significantly inhibited by TKTL1 shRNA (d), with decrease in colony size. (* = p<0.01, ** = p<0.001, chi square).</p>", "links"=>[], "tags"=>["transient", "transfection", "transcriptional", "repression"], "article_id"=>573990, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TKTL1_transient_transfection_and_transcriptional_repression_with_shRNA_/573990", "title"=>"TKTL1 transient transfection and transcriptional repression with shRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-23 01:06:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/903748"], "description"=>"<p>The expO dataset repository was mined for tumor tissue gene expression measured by the Affymetrix U133 Plus 2.0 mRNA expression platform. Initially data was median-normalized by expression array and each gene was median normalized for this figure. Only the subsets of non small cell lung cancer, lymphoma, melanoma, pancreas cancer, and urothelial cancer are displayed. (a) shows the expression of <i>H19</i> in these cancers. (b) <i>MAGEA2</i> expression, (c) <i>TKTL1</i> expression, and (d) <i>MAGEA4</i>. Statistical significance was measured in each tumor type by comparing gene expression in the tumor type to expression in all the remaining 1041 samples. Tumor types without p values did not approach statistical significance. Lung and urothelial showed significant expression overlap.</p>", "links"=>[], "tags"=>["demethylation"], "article_id"=>574190, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_and_demethylation_in_other_human_cancers_/574190", "title"=>"Overexpression and demethylation in other human cancers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-23 01:09:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/903901"], "description"=>"<p>(a) Shows the gene expression correlation p-value matrix for the coexpression for each gene pair across all tumors. This comparison shows the correlation of each gene pair in 49 head and neck tumors. (b) Gene pair expression p-value correlation matrix for 80 NSCLC. Of note C19ORF28 is not tiled on this array platform. (c) Analysis of promoter regions for the genes. Shown is a phylogram of our promoters of interest based on ClustalW analysis after multiple sequence alignment. The region of significant homology is shown after sequence alignment and E statistics from EMBL-EBI's PromoterWise comparison. (d) Promoter hypomethylation (QUMSP) correlation p-value matrix for HNSCC (25 tumors). (e) Promoter hypomethylation (QUMSP) correlation p-value matrix for NSCLC (13 tumors).</p>", "links"=>[], "tags"=>["demethylation"], "article_id"=>574346, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_expression_and_demethylation_correlation_/574346", "title"=>"Gene expression and demethylation correlation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-23 01:12:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/904025"], "description"=>"<p>(a) <i>BORIS</i> expression correlates with expression of target genes in HNSCC (QRT-PR) heat map (Pearson correlation) (b) Transient transfection of <i>BORIS</i> construct into NIH-3T3 and OKF6-Tert1R cell lines. <i>BORIS</i> overexpression resulted in increased cell growth in the 3T3 cell line (at day 3, 77%±34% growth increase) and in the OKF6-Tert1R cell line (at day 3, 161%±78% growth increase). Cell growth over baseline calculated by dividing values by day 1's Calcein signal. (c) Anchorage independent growth was assayed after transfection with empty vector (EV), CTCF, and BORIS at various concentrations of doxycycline, with representative colony (below). (d) QUMSP of nine targets of interest after transfection with empty vector (untreated) and BORIS construct (treated) in presence of 0.0625 µg/mL of doxycycline. (e) Fold increase Quantitiative RT-PCR of nine targets of interest after BORIS transfection normalized to values after transfection with empty vector.</p>", "links"=>[], "tags"=>["transfection"], "article_id"=>574461, "categories"=>["Genetics", "Cancer"], "users"=>["Ian M. Smith", "Chad A. Glazer", "Suhail K. Mithani", "Michael F. Ochs", "Wenyue Sun", "Sheetal Bhan", "Alexander Vostrov", "Ziedulla Abdullaev", "Victor Lobanenkov", "Andrew Gray", "Chunyan Liu", "Steven S. Chang", "Kimberly L. Ostrow", "William H. Westra", "Shahnaz Begum", "Mousumi Dhara", "Joseph Califano"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0004961.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BORIS_transfection_studies_/574461", "title"=>"BORIS transfection studies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-03-23 01:14:21"}

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Relative Metric

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