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{"title"=>"Molecular mechanisms of regulation and action of microRNA-199a in testicular germ cell tumor and glioblastomas", "type"=>"journal", "authors"=>[{"first_name"=>"Shen", "last_name"=>"Gu", "scopus_author_id"=>"55322167700"}, {"first_name"=>"Hoi Hung", "last_name"=>"Cheung", "scopus_author_id"=>"25932065800"}, {"first_name"=>"Tin Lap", "last_name"=>"Lee", "scopus_author_id"=>"35292432600"}, {"first_name"=>"Gang", "last_name"=>"Lu", "scopus_author_id"=>"56906468600"}, {"first_name"=>"Wai Sang", "last_name"=>"Poon", "scopus_author_id"=>"7103025507"}, {"first_name"=>"Wai Yee", "last_name"=>"Chan", "scopus_author_id"=>"7403918043"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"24391856", "doi"=>"10.1371/journal.pone.0083980", "sgr"=>"84896699945", "isbn"=>"1932-6203; 1932-6203", "scopus"=>"2-s2.0-84896699945", "issn"=>"19326203", "pui"=>"372407346"}, "id"=>"661318c1-4d72-3f4c-874a-6ff831733eca", "abstract"=>"MicroRNA-199a (miRNA-199a) has been shown to have comprehensive functions and behave differently in different systems and diseases. It is encoded by two loci in the human genome, miR-199a-1 in chromosome 19 and miR-199a-2 in chromosome 1. Both loci give rise to the same miRNAs (miR-199a-5p and miR-199a-3p). The cause of the diverse action of the miRNA in different systems is not clear. However, it is likely due to different regulation of the two genomic loci and variable targets of the miRNA in different cells and tissues. Here we studied promoter methylation of miR-199a in testicular germ cell tumors (TGCTs) and glioblastomas (gliomas) and discovered that hypermethylation in TGCTs of both miR-199a-1 and -2 resulted in its reduced expression, while hypomethylation of miR-199a-2 but not -1 in gliomas may be related to its elevated expression. We also identified a common regulator, REST, which preferentially bound to the methylated promoters of both miR-199a-1 and miR-199a-2. The action of miR-199a is dependent on its downstream targets. We identified MAFB as a putative target of miRNA-199a-5p in TGCTs and confirmed that the tumor suppression activity of the microRNA is mediated by its target MAFB. By studying the mechanisms that control the expressions of miR-199a and its various downstream targets, we hope to use miR-199a as a model to understand the complexity of miRNA biology.", "link"=>"http://www.mendeley.com/research/molecular-mechanisms-regulation-action-microrna199a-testicular-germ-cell-tumor-glioblastomas-2", "reader_count"=>20, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>3, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>3, "Other"=>1, "Student > Master"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>3, "Neuroscience"=>1, "Psychology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>1}

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• http://doi.org/10.7314/APJCP.2014.15.15.6243
• http://doi.org/10.2478/raon-2018-0043
• http://doi.org/10.3892/ol.2016.4996
• http://doi.org/10.3892/ijo.2017.4200
• http://doi.org/10.1016/j.ucl.2015.08.013
• http://doi.org/10.1530/REP-14-0239
• http://doi.org/10.3390/ijms18122648
• http://doi.org/10.1016/j.gene.2018.03.072
• http://doi.org/10.3390/cancers12030749
• http://doi.org/10.1007/s13277-015-3409-z
• http://doi.org/10.1007/s00018-019-03022-7
• http://doi.org/10.3389/fped.2014.00042
• http://doi.org/10.1016/j.omtn.2019.09.005
• http://doi.org/10.1038/srep06413
• http://doi.org/10.2217/epi-2016-0081
• http://doi.org/10.3389/fcell.2020.594528

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/1333162"], "description"=>"<p>A). All these genes were potential direct targets of miR-199a-5p according to prediction programs, e.g. Targetscan and MiRanda. *, p<0.05 compared miR-199a-5p transfected group with the control. B) Ingenuity Pathway Analysis showed the relationship among the potential targets. “Master regulator” MAFB were selected for further studies (indicated by an arrow).</p>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "arrays", "qpcr"], "article_id"=>889888, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083980.g005", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_the_expression_arrays_data_by_qPCR_of_selected_genes_/889888", "title"=>"Validation of the expression arrays data by qPCR of selected genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 02:54:19"}
• {"files"=>["https://ndownloader.figshare.com/files/1333164"], "description"=>"<p>A) Western blot showing expression decreased at protein level of MAFB after miR-199a-5p transfection; B) Luciferase receptor assay demonstrated direct binding between MAFB and miR-199a-5p. 3′-UTR of MAFB containing miR-199a-5p targeting site (MAFB) was cloned to the 3′-end of firefly luciferase (pGL vector). The plasmids were co-transfected with miR-199a-5p mimics (5p) or scrambled miRNA control. Lower panel showed the seed binding region between miR-199a-5p and 3′-UTR of MAFB (adapted from MiRanda database).</p>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "mafb", "mir-199a-5p", "nt2"], "article_id"=>889890, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083980.g006", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_MAFB_to_be_a_direct_target_of_miR_199a_5p_in_NT2_cells_/889890", "title"=>"Validation of MAFB to be a direct target of miR-199a-5p in NT2 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 02:54:19"}
• {"files"=>["https://ndownloader.figshare.com/files/1333167"], "description"=>"<p>A). Representative images of immunohistochemistry of MAFB in non-cancerous and malignant testicular tumor sections. B). Testis patient samples were divided into four groups(negative, weak, moderate or strong) based on the MAFB level and the proportion of different grades of tumors showing that MAFB protein is highly expressed in malignant testicular tumor. C) Depletion of MAFB by RNAi suppressed cell proliferation <i>in vitro</i> as revealed by CCK8 assay. *, p<0.05 siMAFB transfected NT2 cells compared with scrambled control transfected cells. D) Scatter plots of miR-199a-5p and miR-199a-3p expression against MAFB level. Expression of miR-199a-5p, but not -3p, correlates negatively with MAFB level (Negative: n = 12; Weak: n = 31; Moderate: n = 24; Strong: n = 26; miR-199a-5p: Spearman correlation = −0.276, <i>p</i> = 0.005; miR-199a-3p: Spearman correlation = −0.027, <i>p</i> = 0.791).</p>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "studies", "mafb"], "article_id"=>889893, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083980.g007", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_studies_of_MAFB_in_TGCTs_/889893", "title"=>"Functional studies of MAFB in TGCTs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 02:54:19"}
• {"files"=>["https://ndownloader.figshare.com/files/1333168", "https://ndownloader.figshare.com/files/1333169", "https://ndownloader.figshare.com/files/1333170", "https://ndownloader.figshare.com/files/1333171", "https://ndownloader.figshare.com/files/1333172", "https://ndownloader.figshare.com/files/1333173", "https://ndownloader.figshare.com/files/1333174", "https://ndownloader.figshare.com/files/1333175"], "description"=>"<div><p>MicroRNA-199a (miRNA-199a) has been shown to have comprehensive functions and behave differently in different systems and diseases. It is encoded by two loci in the human genome, miR-199a-1 in chromosome 19 and miR-199a-2 in chromosome 1. Both loci give rise to the same miRNAs (miR-199a-5p and miR-199a-3p). The cause of the diverse action of the miRNA in different systems is not clear. However, it is likely due to different regulation of the two genomic loci and variable targets of the miRNA in different cells and tissues. Here we studied promoter methylation of miR-199a in testicular germ cell tumors (TGCTs) and glioblastomas (gliomas) and discovered that hypermethylation in TGCTs of both miR-199a-1 and -2 resulted in its reduced expression, while hypomethylation of miR-199a-2 but not -1 in gliomas may be related to its elevated expression. We also identified a common regulator, REST, which preferentially bound to the methylated promoters of both miR-199a-1 and miR-199a-2. The action of miR-199a is dependent on its downstream targets. We identified MAFB as a putative target of miRNA-199a-5p in TGCTs and confirmed that the tumor suppression activity of the microRNA is mediated by its target MAFB. By studying the mechanisms that control the expressions of miR-199a and its various downstream targets, we hope to use miR-199a as a model to understand the complexity of miRNA biology.</p></div>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "mechanisms", "microrna-199a", "testicular", "germ"], "article_id"=>889894, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0083980.s001", "https://dx.doi.org/10.1371/journal.pone.0083980.s002", "https://dx.doi.org/10.1371/journal.pone.0083980.s003", "https://dx.doi.org/10.1371/journal.pone.0083980.s004", "https://dx.doi.org/10.1371/journal.pone.0083980.s005", "https://dx.doi.org/10.1371/journal.pone.0083980.s006", "https://dx.doi.org/10.1371/journal.pone.0083980.s007", "https://dx.doi.org/10.1371/journal.pone.0083980.s008"], "stats"=>{"downloads"=>20, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Molecular_Mechanisms_of_Regulation_and_Action_of_microRNA_199a_in_Testicular_Germ_Cell_Tumor_and_Glioblastomas_/889894", "title"=>"Molecular Mechanisms of Regulation and Action of microRNA-199a in Testicular Germ Cell Tumor and Glioblastomas", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-12-31 02:54:19"}
• {"files"=>["https://ndownloader.figshare.com/files/1333154"], "description"=>"<p>A). Genomic representation of differential methylation region from chr19:10,928,097-10,928,800 (hg19). Promoter of miR-199a-1 (+5:−628) embedded in intron-15 of DNM2 is indicated with relative locations of all CpG sites (lolipops). B). Hypermethylation (95%) of miR-199a-1 promoter was found in testicular germ cell tumor cells (NT2 cells) comparing to unmethylation in normal testis fibroblasts (HT cells). C). Hypermethylation of miR-199a-1 promoter was found in both normal brain DNA, Normal Brain 340 and glioma patient samples (GBM 27, 30, 69 and 70).</p>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "mir-199a-1", "promoter", "chr19"], "article_id"=>889880, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083980.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Methylation_status_of_miR_199a_1_promoter_in_Chr19_in_tumors_/889880", "title"=>"Methylation status of miR-199a-1 promoter in Chr19 in tumors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 02:54:19"}
• {"files"=>["https://ndownloader.figshare.com/files/1333156"], "description"=>"<p>A). Genomic representation of differential methylation region from chr1:172,113,550-172,114,255 (hg19). miR-199a-2 and its upstream promoter (+234:−471) embedded in intron-14 of <i>DNM3</i> is indicated with relative locations of all CpG sites (lolipops). B). qPCR showing increased expression of both miR-199a-3p and -5p in three out of five glioma patients compared with normal brain. *, p<0.05 miR-199a-3p expression of GBM samples comparing to normal brain; **, p<0.05 miR-199a-5p expression of GBM samples comparing to normal brain. C). Hypomethylation of miR-199a-2 was found in glioma patients (GBM 27, 30. 69 and 70) comparing to normal brain.</p>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "mir-199a", "hypomethylation", "mir-199a-2", "promoter", "chr1"], "article_id"=>889882, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083980.g002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Elevated_expression_of_miR_199a_versus_hypomethylation_of_miR_199a_2_promoter_in_Chr1_in_glioma_/889882", "title"=>"Elevated expression of miR-199a versus hypomethylation of miR-199a-2 promoter in Chr1 in glioma.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 02:54:19"}
• {"files"=>["https://ndownloader.figshare.com/files/1333157"], "description"=>"<p>A). Chromatin immunoprecipitation (ChIP) confirmed the direct binding of transcription factor REST on both promoters of miR-199a in Chr1 and Chr19 in NT2 and HT cells. qPCR following ChIP showed that there were higher binding in NT2 cells compared to HT cells. S1, S2 and S3 are three consecutive segments of miR-199a promoters in Chr1 and Chr19 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0083980#pone.0083980.s001\" target=\"_blank\">Figure S1</a>). There was binding of REST on Chr19-S2 in NT2 cells but not in HT cells. B). ChIP confirmed the direct binding of REST on one non-glioma brain tissue and two glioma tissues. C). <i>In vitro</i> methylation assay showed that REST preferentially bound to methylated miR-199a vectors than unmethylated vectors. Promoters of miR-199a-1 in Chr19 and miR-199a-2 in Chr1 were methylated <i>in vitro</i> and ligated into pGL3 luciferase vector (199A1-methylated and 199A2-methylated). Mock methylated (un-methylated) inserts were also ligated into pGL3 vector (199A1-mock and 199A2-mock). Ligated products were co-transfected with REST expressing vector into HEK-293T cells. Luciferase receptor assay was performed 48 hours after transfection. pGL4.73 vector was also transfected as normalization of the luciferase activity. *, p<0.05 luciferase activity compared methylated inserts with control. D). Reduced expression of REST resulted in increased expression of both miR-199a-3p and -5p in NT2 cells (Amount of siRNA of REST transfected: 30 nM). *, p<0.05 miR-199a-3p expression in NT2 cells with siREST transfection compared with control; **, p<0.05 miR-199a-5p expression in NT2 cells with siREST transfection compared with control.</p>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "dna", "methylation", "mir-199a"], "article_id"=>889883, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083980.g003", "stats"=>{"downloads"=>4, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Function_of_REST_on_DNA_methylation_of_miR_199a_promoters_/889883", "title"=>"Function of REST on DNA methylation of miR-199a promoters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 02:54:19"}
• {"files"=>["https://ndownloader.figshare.com/files/1333159"], "description"=>"<p>A). qPCR showing more than four thousand fold changes of miR-199a-5p expression levels after transiently transfection of mimic of miR-199a-5p into NT2 cells comparing to NT2 cells transfected with scrambled control RNA. (Amount of miR-199a-5p mimics or scrambled control transfected: 25 nM). *, p<0.05 miR-199a-5p expression compared miR-199a-5p mimics transfection in NT2 cells with control. B). Western Blot showing reduced expression of PODXL, a confirmed direct target of miR-199a-5p in TGCTs after miR-199a-5p overexpression. C). Heatmap showing hierarchical clustering of differently expressed genes after miR-199a-5p transfection (Fold change>1.2, FDR<0.6).</p>", "links"=>[], "tags"=>["developmental biology", "genetics", "epigenetics", "DNA modification", "RNA interference", "Molecular genetics", "Gene regulation", "Gene function", "Molecular cell biology", "gene expression", "dysregulated", "genes", "knock-in", "mir-199a-5p", "nt2"], "article_id"=>889885, "categories"=>["Biological Sciences"], "users"=>["Shen Gu", "Hoi Hung Cheung", "Tin Lap Lee", "Gang Lu", "Wai Sang Poon", "Wai Yee Chan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0083980.g004", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_dysregulated_genes_after_knock_in_of_miR_199a_5p_in_NT2_cells_/889885", "title"=>"Identification of dysregulated genes after knock-in of miR-199a-5p in NT2 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 02:54:19"}

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[266, 468, 593, 703, 804, 903, 993, 1084, 1171, 1256, 1339, 1422, 1492]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[272, 472, 600, 713, 815, 911, 1004, 1094, 1185, 1273, 1358, 1441]}, {"subject_area"=>"/Medicine and health sciences/Neurology", "average_usage"=>[271, 485, 617, 733, 835, 933, 1026, 1115, 1207, 1294, 1386, 1475, 1543]}]}

F1000Prime