Dre-miR-2188 Targets Nrp2a and Mediates Proper Intersegmental Vessel Development in Zebrafish Embryos
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{"title"=>"Dre-miR-2188 targets Nrp2a and mediates proper intersegmental vessel development in zebrafish embryos", "type"=>"journal", "authors"=>[{"first_name"=>"Ana R.", "last_name"=>"Soares", "scopus_author_id"=>"26633318000"}, {"first_name"=>"Marisa", "last_name"=>"Reverendo", "scopus_author_id"=>"55195649100"}, {"first_name"=>"Patrícia M.", "last_name"=>"Pereira", "scopus_author_id"=>"55947748400"}, {"first_name"=>"Olivier", "last_name"=>"Nivelles", "scopus_author_id"=>"23985568300"}, {"first_name"=>"Hélène", "last_name"=>"Pendeville", "scopus_author_id"=>"6506150604"}, {"first_name"=>"Ana Rita", "last_name"=>"Bezerra", "scopus_author_id"=>"54398243600"}, {"first_name"=>"Gabriela R.", "last_name"=>"Moura", "scopus_author_id"=>"6603700986"}, {"first_name"=>"Ingrid", "last_name"=>"Struman", "scopus_author_id"=>"6602619248"}, {"first_name"=>"Manuel A S", "last_name"=>"Santos", "scopus_author_id"=>"15825809000"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84862690378", "doi"=>"10.1371/journal.pone.0039417", "sgr"=>"84862690378", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"22761789", "issn"=>"19326203", "pui"=>"365066292"}, "id"=>"16a49198-ccf4-3270-8dc0-4f7973ab14f4", "abstract"=>"BACKGROUND: MicroRNAs (miRNAs) are a class of small RNAs that are implicated in the control of eukaryotic gene expression by binding to the 3'UTR of target mRNAs. Several algorithms have been developed for miRNA target prediction however, experimental validation is still essential for the correct identification of miRNA targets. We have recently predicted that Neuropilin2a (Nrp2a), a vascular endothelial growth factor receptor which is essential for normal developmental angiogenesis in zebrafish, is a dre-miR-2188 target.\\n\\nMETHODOLOGY: Here we show that dre-miR-2188 targets the 3'-untranslated region (3'UTR) of Nrp2a mRNA and is implicated in proper intersegmental vessel development in vivo. Over expression of miR-2188 in zebrafish embryos down regulates Nrp2a expression and results in intersegmental vessel disruption, while its silencing increases Nrp2a expression and intersegmental vessel sprouting. An in vivo GFP sensor assay based on a fusion between the GFP coding region and the Nrp2a 3'UTR confirms that miR-2188 binds to the 3'UTR of Nrp2a and inhibits protein translation.\\n\\nCONCLUSIONS: We demonstrate that miR-2188 targets Nrp2a and affects intersegmental vessel development in zebrafish embryos.", "link"=>"http://www.mendeley.com/research/dremir2188-targets-nrp2a-mediates-proper-intersegmental-vessel-development-zebrafish-embryos", "reader_count"=>20, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>7, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>7, "Other"=>1, "Student > Master"=>3, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>13, "Medicine and Dentistry"=>2, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Belgium"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/619276"], "description"=>"<p>A) Single cell embryos were injected with the GFP reporter (50 ng/µL) in the presence or absence of MO<sub>miR-2188</sub>, miR-2188 and scrambled duplexes or a mixture of both MO<sub>miR-2188</sub> and miR-2188 duplex. Fluorescence levels were observed at 24 hpf and representative embryos of each condition were photographed. Fluorescence was recovered in MO<sub>miR-2188</sub>+ miR-2188 injected embryos, when compared to miR-2188 duplex injected embryos. B) Embryo lysates were prepared from 24 hpf embryos injected with the GFP reporter in the presence or absence of MO<sub>miR-2188</sub>, miR-2188 and scrambled duplexes or a mixture of MO<sub>miR-2188</sub> and miR-2188. Protein levels were determined by western blot analysis and β-tubulin was used as an internal control. <b>C)</b> Quantification of the reporter proteins (%). Asterisks indicate conditions where GFP expression was significantly down regulated by miR-2188 relative to control conditions. miR-2188 injected embryos showed a statistically significant down regulation of GFP levels, indicating that <i>Nrp2a</i> 3′UTR is a true miR-2188 target. Co-injection of the MO<sub>miR-2188</sub> with the miR-2188 duplex resulted in the rescue of GFP fluorescence, further confirming that <i>Nrp2a</i> is a bona fide target of miR-2188. Data are mean +/−stdev, p<0,005 (t test, unpaired), n>3. All lanes were normalized to the β-tubulin signal.</p>", "links"=>[], "tags"=>["genetics and genomics", "physiology", "developmental biology", "Biochemistry"], "article_id"=>289760, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.g005", "stats"=>{"downloads"=>0, "page_views"=>49, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GFP_rescue_sensor_assay_/289760", "title"=>"GFP rescue sensor assay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-22 02:42:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/619187"], "description"=>"<p>A) The GFP gene was fused with the 3′UTR of <i>Nrp2a</i> that contained the putative binding sites of miR-2188. This construct was transcribed <i>in vitro</i> into capped mRNA prior to injection. B) Single cell embryos were injected with the GFP reporter (50 ng/µL) in the presence or absence of miR-2188 and scrambled duplexes. Fluorescence levels were observed at 24 hpf and representative embryos of each condition were photographed. Decreased fluorescence was observed in miR-2188 duplex injected embryos. C) Embryo lysates were prepared from 24 hpf embryos injected with the wild type GFP reporter or the mutated reporters in the presence or absence of miR-2188 and scrambled duplexes. Protein levels were determined by western blot analysis and β-tubulin was used as an internal control. <b>D)</b> Quantification of the reporter proteins (%) in the conditions tested using 3 biological replicates. Asterisks indicate conditions where GFP expression was significantly down regulated by miR-2188 relative to control conditions. miR-2188 injected embryos showed a statistically significant down regulation of GFP levels, indicating that <i>Nrp2a</i> 3′UTR is a true miR-2188 target. Co-injection of the M1 reporter with the miR-2188 duplex produced normal GFP levels, indicating that the BS-1 mutation abolished miR-2188 binding. On the other hand, a significant decrease in GFP expression was observed after co-injection of the M2 reporter with miR-2188, relative to the controls, indicating that BS-2 was not critical for miR-2188 binding. Data are mean +/−stdev, p<0,005 (t test, unpaired), n>3. All lanes were normalized to the β-tubulin signal.</p>", "links"=>[], "tags"=>["genetics and genomics", "physiology", "developmental biology", "Biochemistry"], "article_id"=>289670, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GFP_sensor_assay_/289670", "title"=>"GFP sensor assay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-22 02:41:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/322168", "https://ndownloader.figshare.com/files/322199"], "description"=>"<div><h3>Background</h3><p>MicroRNAs (miRNAs) are a class of small RNAs that are implicated in the control of eukaryotic gene expression by binding to the 3′UTR of target mRNAs. Several algorithms have been developed for miRNA target prediction however, experimental validation is still essential for the correct identification of miRNA targets. We have recently predicted that Neuropilin2a (<em>Nrp2a</em>), a vascular endothelial growth factor receptor which is essential for normal developmental angiogenesis in zebrafish, is a dre-miR-2188 target.</p> <h3>Methodology</h3><p>Here we show that dre-miR-2188 targets the 3′-untranslated region (3′UTR) of <em>Nrp2a</em> mRNA and is implicated in proper intersegmental vessel development <em>in vivo</em>. Over expression of miR-2188 in zebrafish embryos down regulates <em>Nrp2a</em> expression and results in intersegmental vessel disruption, while its silencing increases <em>Nrp2a</em> expression and intersegmental vessel sprouting. An <em>in vivo</em> GFP sensor assay based on a fusion between the GFP coding region and the <em>Nrp2a</em> 3′UTR confirms that miR-2188 binds to the 3′UTR of <em>Nrp2a</em> and inhibits protein translation.</p> <h3>Conclusions</h3><p>We demonstrate that miR-2188 targets <em>Nrp2a</em> and affects intersegmental vessel development in zebrafish embryos.</p> </div>", "links"=>[], "tags"=>["dre-mir-2188", "targets", "mediates", "intersegmental", "zebrafish", "embryos"], "article_id"=>123590, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0039417.s001", "https://dx.doi.org/10.1371/journal.pone.0039417.s002"], "stats"=>{"downloads"=>2, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Dre_miR_2188_Targets_Nrp2a_and_Mediates_Proper_Intersegmental_Vessel_Development_in_Zebrafish_Embryos/123590", "title"=>"Dre-miR-2188 Targets <em>Nrp2a</em> and Mediates Proper Intersegmental Vessel Development in Zebrafish Embryos", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-06-22 00:59:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/618929"], "description"=>"<p>A) A miRNA duplex and a MO<sub>miR-2188</sub> were designed to over express and knockdown miR-2188 in zebrafish embryos, respectively. Duplex microinjections were performed in one cell stage embryos with rhodamine to visualize the injection process. Approximately 1000 pL of each duplex were injected. 2 µM of each duplex were chosen as the working concentration for the injections, as this duplex concentration did not induce high mortality rates or unspecific side effects. B) qPCR quantification of miR-2188 showed that miR-2188 duplex injection increased miR-2188 expression by 40 fold and MO<sub>miR-2188</sub> injection decreased miR-2188 expression by 12 fold. C) qPCR quantification of <i>Nrp2a</i> levels in 48 hpf embryos after over expression and knockdown of miR-2188 showed that this target was down regulated 1.6 fold after miR-2188 over expression and was up regulated 2 fold after miR-2188 knockdown.</p>", "links"=>[], "tags"=>["duplex", "morpholino"], "article_id"=>289416, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.g002", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_miR_2188_duplex_and_morpholino_injections_/289416", "title"=>"miR-2188 duplex and morpholino injections.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-22 02:36:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/619503"], "description"=>"<p>Putative binding sites of miR-2188 in <i>Nrp2a</i> 3′UTR.</p>", "links"=>[], "tags"=>["binding", "sites", "mir-2188"], "article_id"=>289993, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Putative_binding_sites_of_miR_2188_in_Nrp2a_3_UTR_/289993", "title"=>"Putative binding sites of miR-2188 in <i>Nrp2a</i> 3′UTR.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-06-22 02:46:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/619030"], "description"=>"<p>A) After injection of miR-2188 duplex, <i>Nrp2a</i> detection decreased between the somite boundaries at 24 hpf. On the other hand, in miR-2188 morphants, <i>Nrp2a</i> detection was more prounounced throughout the trunk and tail region, between the somite boundaries, when compared with the control. B) At 48 hpf and after miR-2188 overexpression, <i>Nrp2a</i> was not detected in the blood vessels or in the PCV when compared with the control embryos. On the other hand, miR-2188 morphants express <i>Nrp2a</i> in the trunck and tail, especially between the somite boundaries, which is not detected in 48 hpf control embryos. All embryos are in lateral view, anterior to left. Arrows indicate hybridization signal. Microscopic pictures were taken with a 6,3x magnification.</p>", "links"=>[], "tags"=>["mir-2188"], "article_id"=>289522, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ISH_of_Nrp2a_after_miR_2188_deregulation_/289522", "title"=>"ISH of <i>Nrp2a</i> after miR-2188 deregulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-22 02:38:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/619552"], "description"=>"<p>Putative targets of dre-miR-2188.</p>", "links"=>[], "tags"=>["targets"], "article_id"=>290039, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.t002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Putative_targets_of_dre_miR_2188_/290039", "title"=>"Putative targets of dre-miR-2188.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-06-22 00:00:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/619394"], "description"=>"<p>A) Representation of the zebrafish circulatory system showing the major structures (DLAV - Dorsal Longitudinal Anastomotic Vessel; ISV – Intersegmental Vessel; DA – Dorsal Aorta; PCV – Posterior Cardinal Vein). B) Visualization of 24 hpf embryo blood vessels using fluorescence microscopy. After miR-2188 duplex microinjection under developed and absent ISVs were observed, non injected and scrambled duplex injected embryos did not show such defects. C) Visualization of 48 hpf embryo blood vessels using confocal microscopy (20x). ISVs of miR-2188 injected embryos were thinner than those of non injected and scrambled duplex injected embryos and displayed ISV’s patterning defects (arrows). MO<sub>miR-2188</sub> injected embryos revealed DLAV defects and branching of ISVs (arrows). Images shown in D) and E) are 60x amplification images of miR-2188 duplex and miR-2188-MO injected embryos, respectively.</p>", "links"=>[], "tags"=>["genetics and genomics", "physiology", "developmental biology", "Biochemistry"], "article_id"=>289880, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.g006", "stats"=>{"downloads"=>2, "page_views"=>71, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_blood_vessel_formation_in_Tg_flk1_GFP_s843_embryos_/289880", "title"=>"Analysis of blood vessel formation in Tg(flk1-GFP)s843 embryos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-22 02:44:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/618763"], "description"=>"<p>A) ISH of miR-2188 at 24 hpf showed low expression on the trunck and tail, however it increased at 48 hpf between the somite boundaries. Arrows indicate hybridization signal. B) <i>Nrp2a</i> ISH at 24 and 48 pf. At 24hpf <i>Nrp2a</i> was predominantly expressed in the head and somitic regions, while at 48 hpf its expression was restricted to the brain and romboencephalon. There was an indirect correlation between miR-2188 and <i>Nrp2a</i> expression. Increasing miR-2188 levels through development were accompanied by decreasing <i>Nrp2a</i> expression between the somite boundaries. All embryos are in lateral view, anterior to left. Microscopic pictures were taken with 6,3x magnification.</p>", "links"=>[], "tags"=>["mir-2188", "zebrafish"], "article_id"=>289246, "categories"=>["Physiology", "Biochemistry", "Genetics", "Developmental Biology"], "users"=>["Ana R. Soares", "Marisa Reverendo", "Patrícia M. Pereira", "Olivier Nivelles", "Hélène Pendeville", "Ana Rita Bezerra", "Gabriela R. Moura", "Ingrid Struman", "Manuel A. S. Santos"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0039417.g001", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_miR_2188_and_Nrp2a_in_zebrafish_embryos_/289246", "title"=>"Expression of miR-2188 and <i>Nrp2a</i> in zebrafish embryos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-22 02:34:06"}

PMC Usage Stats | Further Information

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Relative Metric

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