Conserved Regulation of p53 Network Dosage by MicroRNA–125b Occurs through Evolving miRNA–Target Gene Pairs
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{"title"=>"Conserved regulation of p53 network dosage by microRNA-125b occurs through evolving miRNA-target gene pairs", "type"=>"journal", "authors"=>[{"first_name"=>"Minh T.N.", "last_name"=>"Le", "scopus_author_id"=>"8251310800"}, {"first_name"=>"Ng", "last_name"=>"Shyh-Chang", "scopus_author_id"=>"56003172200"}, {"first_name"=>"Swea Ling", "last_name"=>"Khaw", "scopus_author_id"=>"53866613900"}, {"first_name"=>"Lingzi", "last_name"=>"Chin", "scopus_author_id"=>"53866075100"}, {"first_name"=>"Cathleen", "last_name"=>"Teh", "scopus_author_id"=>"17736447400"}, {"first_name"=>"Junliang", "last_name"=>"Tay", "scopus_author_id"=>"53867095600"}, {"first_name"=>"Elizabeth", "last_name"=>"O'Day", "scopus_author_id"=>"14822462500"}, {"first_name"=>"Vladimir", "last_name"=>"Korzh", "scopus_author_id"=>"7006844905"}, {"first_name"=>"Henry", "last_name"=>"Yang", "scopus_author_id"=>"23468238300"}, {"first_name"=>"Ashish", "last_name"=>"Lal", "scopus_author_id"=>"7201847359"}, {"first_name"=>"Judy", "last_name"=>"Lieberman", "scopus_author_id"=>"7202237594"}, {"first_name"=>"Harvey F.", "last_name"=>"Lodish", "scopus_author_id"=>"36050903500"}, {"first_name"=>"Bing", "last_name"=>"Lim", "scopus_author_id"=>"7201984111"}], "year"=>2011, "source"=>"PLoS Genetics", "identifiers"=>{"pmid"=>"21935352", "doi"=>"10.1371/journal.pgen.1002242", "sgr"=>"80053437994", "isbn"=>"1553-7404 (Electronic)\\n1553-7390 (Linking)", "scopus"=>"2-s2.0-80053437994", "issn"=>"15537390", "pui"=>"362681108"}, "id"=>"55c7789f-bbde-39ee-8e84-9ce022625028", "abstract"=>"MicroRNAs regulate networks of genes to orchestrate cellular functions. MiR-125b, the vertebrate homologue of the Caenorhabditis elegans microRNA lin-4, has been implicated in the regulation of neural and hematopoietic stem cell homeostasis, analogous to how lin-4 regulates stem cells in C. elegans. Depending on the cell context, miR-125b has been proposed to regulate both apoptosis and proliferation. Because the p53 network is a central regulator of both apoptosis and proliferation, the dual roles of miR-125b raise the question of what genes in the p53 network might be regulated by miR-125b. By using a gain- and loss-of-function screen for miR-125b targets in humans, mice, and zebrafish and by validating these targets with the luciferase assay and a novel miRNA pull-down assay, we demonstrate that miR-125b directly represses 20 novel targets in the p53 network. These targets include both apoptosis regulators like Bak1, Igfbp3, Itch, Puma, Prkra, Tp53inp1, Tp53, Zac1, and also cell-cycle regulators like cyclin C, Cdc25c, Cdkn2c, Edn1, Ppp1ca, Sel1l, in the p53 network. We found that, although each miRNA-target pair was seldom conserved, miR-125b regulation of the p53 pathway is conserved at the network level. Our results lead us to propose that miR-125b buffers and fine-tunes p53 network activity by regulating the dose of both proliferative and apoptotic regulators, with implications for tissue stem cell homeostasis and oncogenesis.", "link"=>"http://www.mendeley.com/research/conserved-regulation-p53-network-dosage-microrna125b-occurs-through-evolving-mirnatarget-gene-pairs", "reader_count"=>112, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>8, "Student > Doctoral Student"=>7, "Researcher"=>36, "Student > Ph. D. Student"=>33, "Other"=>3, "Student > Master"=>9, "Student > Bachelor"=>9, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>8, "Student > Doctoral Student"=>7, "Researcher"=>36, "Student > Ph. D. Student"=>33, "Other"=>3, "Student > Master"=>9, "Student > Bachelor"=>9, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>15, "Agricultural and Biological Sciences"=>72, "Medicine and Dentistry"=>8, "Neuroscience"=>3, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>2, "Immunology and Microbiology"=>1, "Engineering"=>4}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>4}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>8}, "Neuroscience"=>{"Neuroscience"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>72}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>15}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Belgium"=>1, "United States"=>2, "China"=>1, "Denmark"=>1, "Mexico"=>2, "Australia"=>1, "Germany"=>1, "Russia"=>1, "Spain"=>1}, "group_count"=>3}

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  • {"files"=>["https://ndownloader.figshare.com/files/735483"], "description"=>"<p>(A) Human p53 network. (B) Mouse p53 network. (C) Zebrafish p53 network. Models were constructed by Ingenuity Pathway Analysis. Red: predicted targets validated by 3 assays; Orange: predicted targets validated by 2 assays; Yellow: predicted targets validated by 1 assay; Pink: predicted targets not validated by any assay, but validated by 3 assays in another species. (D) Incoherent feedforward loop (FFL) motifs characterize miR-125b regulation of p53 network genes that mediate apoptosis or cell cycle arrest.</p>", "links"=>[], "tags"=>["mir-125b", "p53", "networks"], "article_id"=>405824, "categories"=>["Genetics"], "users"=>["Minh T. N. Le", "Ng Shyh-Chang", "Swea Ling Khaw", "Lingzi Chin", "Cathleen Teh", "Junliang Tay", "Elizabeth O'Day", "Vladimir Korzh", "Henry Yang", "Ashish Lal", "Judy Lieberman", "Harvey F. Lodish", "Bing Lim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002242.g006", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Models_of_miR_125b_regulation_of_p53_networks_in_humans_mice_and_zebrafish_/405824", "title"=>"Models of miR-125b regulation of p53 networks in humans, mice, and zebrafish.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:37:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/734888"], "description"=>"<p>(A) Loss-of-function (LOF) screens were performed in human primary lung fibroblasts (hLF) or mouse 3T3 fibroblasts by transfecting an antisense RNA against both miR-125a and miR-125b (miR-125a/b-AS), or by microinjecting morpholinos (MO) against pre-<i>mir-125b</i> hairpin precursors (all 3 isoforms) into zebrafish embryos. Gain-of-function (GOF) screens were performed in human SH-SY5Y and mouse N2A neuroblastoma by transfecting the miR-125b duplex into cells in culture, or by coinjecting the miR-125b duplex with the morpholinos against pre-<i>mir-125b</i> into zebrafish embryos. Fold changes in gene expression were measured by qRT-PCR twenty-four hours after transfection or injection, relative to the mock and negative control miRNA or morpholino, and shown as log<sub>2</sub>(fold change) using a heat-map. (B) Human: 13 genes were significantly derepressed by a loss of miR-125b, while 20 genes were significantly repressed by a gain of miR-125b, making a total of 22 genes that passed the screen (P<0.05, fold change > 1.3, relative to mock control). (C) Mouse: 11 genes were significantly derepressed by a loss of miR-125b, while 12 genes were significantly repressed by a loss of miR-125b, making a total of 13 genes that passed the screen (P<0.05, fold change > 1.3, relative to mock control). (D) Zebrafish: 13 genes were significantly derepressed by a loss of pre-<i>mir-125b</i> (P<0.05, fold change > 1.3, relative to control MO), while 12 genes were significantly repressed/rescued by a gain of miR-125b (P<0.05, fold change > 1.3, relative to pre-<i>mir-125b</i> MO), making a total of 14 genes that passed the screen. All experiments were performed with at least three biological replicates.</p>", "links"=>[], "tags"=>["p53", "genes", "regulated"], "article_id"=>405229, "categories"=>["Genetics"], "users"=>["Minh T. N. Le", "Ng Shyh-Chang", "Swea Ling Khaw", "Lingzi Chin", "Cathleen Teh", "Junliang Tay", "Elizabeth O'Day", "Vladimir Korzh", "Henry Yang", "Ashish Lal", "Judy Lieberman", "Harvey F. Lodish", "Bing Lim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002242.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GOF_LOF_screen_for_p53_network_genes_regulated_by_miR_125b_/405229", "title"=>"GOF/LOF screen for p53 network genes regulated by miR-125b.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:27:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/734787"], "description"=>"<p>Schematic of experimental design and workflow. (A) Bioinformatic analysis was performed on p53 network genes listed in the Ingenuity Pathways Analysis database and p53 Knowledgebase, and miR-125b binding sites predicted by the TargetScan and MicroCosm databases. (B) p53 network genes were screened for miR-125b targets by using gain- (GOF) and loss-of-function (LOF) of miR-125b in human cells, mouse cells and zebrafish embryos, as indicated by effects on gene expression using qRT-PCR. (C) p53 network genes that were positive in either the GOF or LOF screen were assayed for direct binding to miR-125b using a biotinylated microRNA pull-down method. (D) p53 network genes that were also positive in the miR-125b pull-down were finally validated as miR-125b targets by 3′ UTR luciferase reporter assays and Western blots for protein expression. (E) A model of how miR-125b regulates the p53 network across vertebrates was constructed using our combined datasets for human, mouse and zebrafish cells.</p>", "links"=>[], "tags"=>["mir-125b", "targets", "p53"], "article_id"=>405132, "categories"=>["Genetics"], "users"=>["Minh T. N. Le", "Ng Shyh-Chang", "Swea Ling Khaw", "Lingzi Chin", "Cathleen Teh", "Junliang Tay", "Elizabeth O'Day", "Vladimir Korzh", "Henry Yang", "Ashish Lal", "Judy Lieberman", "Harvey F. Lodish", "Bing Lim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002242.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identifying_miR_125b_targets_in_the_p53_network_of_vertebrates_/405132", "title"=>"Identifying miR-125b targets in the p53 network of vertebrates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:25:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/735016"], "description"=>"<p>Biotinylated miR-125b was used as bait to pull-down mRNAs bound to miR-125b, using streptavidin-conjugated magnetic beads. The mRNAs were quantified by qRT-PCR, normalized to <i>Gapdh,</i> and then compared relative to the same mRNA species pulled down by a biotinylated <i>C. elegans</i> negative control microRNA. The enrichment of mRNAs bound to miR-125b is presented as mean log<sub>2</sub> fold change ± s.e.m. (n≥3 biological replicates). (A) Human: 13 out of 22 candidate targets were significantly enriched by miR-125b pull-down in human primary lung fibroblasts (hLF) 24 hours after transfection. (B) Mouse: 11 out of 13 candidate targets were significantly enriched by miR-125b pull-down in mouse 3T3 fibroblasts 24 hours after transfection. (C) Zebrafish: 8 of 14 candidate targets were significantly enriched by miR-125b pull-down in zebrafish embryos 24 hours after injection. Dashed line: cutoff for genes that were significantly enriched (Log<sub>2</sub> Fold change > 0.5, P<0.05).</p>", "links"=>[], "tags"=>["binding", "mir-125b", "p53"], "article_id"=>405360, "categories"=>["Genetics"], "users"=>["Minh T. N. Le", "Ng Shyh-Chang", "Swea Ling Khaw", "Lingzi Chin", "Cathleen Teh", "Junliang Tay", "Elizabeth O'Day", "Vladimir Korzh", "Henry Yang", "Ashish Lal", "Judy Lieberman", "Harvey F. Lodish", "Bing Lim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002242.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Direct_binding_of_miR_125b_to_p53_network_targets_/405360", "title"=>"Direct binding of miR-125b to p53 network targets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:29:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/735338"], "description"=>"<p>Only targets that passed ≥ 2 validation assays, in at least one species, are shown. Red: predicted targets validated by 3 assays; Orange: predicted targets validated by 2 assays; Yellow: predicted targets validated by 1 assay; Pink: predicted targets not validated by any assay, but validated by 3 assays in another species.</p>", "links"=>[], "tags"=>["genes", "p53", "targeted"], "article_id"=>405678, "categories"=>["Genetics"], "users"=>["Minh T. N. Le", "Ng Shyh-Chang", "Swea Ling Khaw", "Lingzi Chin", "Cathleen Teh", "Junliang Tay", "Elizabeth O'Day", "Vladimir Korzh", "Henry Yang", "Ashish Lal", "Judy Lieberman", "Harvey F. Lodish", "Bing Lim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002242.g005", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_genes_in_p53_network_that_are_directly_targeted_by_miR_125b_/405678", "title"=>"Summary of genes in p53 network that are directly targeted by miR-125b.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:34:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/370872", "https://ndownloader.figshare.com/files/370899"], "description"=>"<div><p>MicroRNAs regulate networks of genes to orchestrate cellular functions. <em>MiR-125b</em>, the vertebrate homologue of the <em>Caenorhabditis elegans</em> microRNA <em>lin-4</em>, has been implicated in the regulation of neural and hematopoietic stem cell homeostasis, analogous to how <em>lin-4</em> regulates stem cells in <em>C. elegans</em>. Depending on the cell context, <em>miR-125b</em> has been proposed to regulate both apoptosis and proliferation. Because the p53 network is a central regulator of both apoptosis and proliferation, the dual roles of <em>miR-125b</em> raise the question of what genes in the p53 network might be regulated by <em>miR-125b</em>. By using a gain- and loss-of-function screen for <em>miR-125b</em> targets in humans, mice, and zebrafish and by validating these targets with the luciferase assay and a novel miRNA pull-down assay, we demonstrate that <em>miR-125b</em> directly represses 20 novel targets in the p53 network. These targets include both apoptosis regulators like <em>Bak1</em>, <em>Igfbp3, Itch, Puma</em>, <em>Prkra, Tp53inp1</em>, <em>Tp53</em>, <em>Zac1</em>, and also cell-cycle regulators like <em>cyclin C, Cdc25c</em>, <em>Cdkn2c, Edn1, Ppp1ca, Sel1l</em>, in the p53 network. We found that, although each miRNA–target pair was seldom conserved, miR-125b regulation of the p53 pathway is conserved at the network level. Our results lead us to propose that <em>miR-125b</em> buffers and fine-tunes p53 network activity by regulating the dose of both proliferative and apoptotic regulators, with implications for tissue stem cell homeostasis and oncogenesis. <em></em></p> </div>", "links"=>[], "tags"=>["conserved", "p53", "dosage", "occurs", "evolving", "pairs"], "article_id"=>133259, "categories"=>["Genetics"], "users"=>["Minh T. N. Le", "Ng Shyh-Chang", "Swea Ling Khaw", "Lingzi Chin", "Cathleen Teh", "Junliang Tay", "Elizabeth O'Day", "Vladimir Korzh", "Henry Yang", "Ashish Lal", "Judy Lieberman", "Harvey F. Lodish", "Bing Lim"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002242.s001", "https://dx.doi.org/10.1371/journal.pgen.1002242.s002"], "stats"=>{"downloads"=>13, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Conserved_Regulation_of_p53_Network_Dosage_by_MicroRNA_125b_Occurs_through_Evolving_miRNA_Target_Gene_Pairs/133259", "title"=>"Conserved Regulation of p53 Network Dosage by MicroRNA–125b Occurs through Evolving miRNA–Target Gene Pairs", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-15 00:54:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/735198"], "description"=>"<p>Candidate p53 network genes that were positive in both the GOF/LOF screen and miR-125b pull-down were validated for targeting by miR-125b using the 3′ UTR luciferase reporter assay and Western blots for protein expression. (A-C), Reporter genes containing the full-length 3′ UTRs of each selected target gene were co-transfected with miR-125b duplex into 293T cells. Luciferase readings were obtained 48 hours after transfection and presented here as the average percentage of luciferase activity ± s.e.m. (n≥3) relative to a scrambled duplex co-transfected control (100%). A reporter containing a 23-nucleotide-binding-site with perfect complementarity to miR-125b was used as the perfect match positive control, while the unmodified luciferase reporter was used as the empty negative control. (A) Human: 10 out of 13 candidate genes' 3′ UTRs showed significant repression by miR-125b relative to the control (p<0.01). (B) Mouse: 9 out of 11 candidate genes' 3′ UTRs showed significant repression by miR-125b relative to the control (p<0.01). (C) Zebrafish: 7 out of 8 candidate genes' 3′ UTRs showed significant repression by miR-125b relative to the control (p<0.01). (D) Alignment of predicted <i>miR-125b</i> binding sites in the 3′UTRs of Ppp1ca, Prkra and Tp53 across three species. Seed-binding sequences are underlined. Bases conserved in two (blue) or three (black) species are highlighted. (E) The 3′UTR seed-binding sequences of 7 target mRNAs were mutated and assayed for direct binding to <i>miR-125b</i> using the luciferase reporter assay, relative to wild-type 3′UTR sequences. (E) The seed-binding sequences in the 3′UTR of 7 predicted target mRNAs were mutated and compared to wild-type sequences for binding to <i>miR-125b</i> using luciferase reporter assay. (F-G) Western blot analysis of protein expression of selected target genes two days after a transfection of miR-125b duplex, miR-125b antisense (AS) or negative control duplex or negative control antisense. (F) Western blots showed that miR-125b repressed BAK1, PPP1CA, TP53, and PPP2CA levels in human SH-SY5Y neuroblastoma cells, while the antisense RNA miR-125b-AS derepressed expression of these proteins in human ReNcell VM neural progenitor cells. (G) Western blots showed that miR-125b repressed BAK1, PPP1CA, PUMA, and ITCH levels in mouse N2A neuroblastoma cells. Abbreviations: h, human; m, mouse; z, zebrafish.</p>", "links"=>[], "tags"=>["mir-125b"], "article_id"=>405547, "categories"=>["Genetics"], "users"=>["Minh T. N. Le", "Ng Shyh-Chang", "Swea Ling Khaw", "Lingzi Chin", "Cathleen Teh", "Junliang Tay", "Elizabeth O'Day", "Vladimir Korzh", "Henry Yang", "Ashish Lal", "Judy Lieberman", "Harvey F. Lodish", "Bing Lim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002242.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_miR_125b_targets_/405547", "title"=>"Validation of miR-125b targets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-15 01:32:27"}

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