Nuclear Receptor Unfulfilled Regulates Axonal Guidance and Cell Identity of Drosophila Mushroom Body Neurons
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{"title"=>"Nuclear receptor unfulfilled regulates axonal guidance and cell identity of Drosophila mushroom body neurons", "type"=>"journal", "authors"=>[{"first_name"=>"Suewei", "last_name"=>"Lin", "scopus_author_id"=>"13103731500"}, {"first_name"=>"Yaling", "last_name"=>"Huang", "scopus_author_id"=>"16679192500"}, {"first_name"=>"Tzumin", "last_name"=>"Lee", "scopus_author_id"=>"7501439031"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"20027309", "doi"=>"10.1371/journal.pone.0008392", "sgr"=>"77649157766", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-77649157766", "issn"=>"19326203", "pui"=>"359087796"}, "id"=>"2996d351-ffb1-3fbe-9315-2d6589090fac", "abstract"=>"Nuclear receptors (NRs) comprise a family of ligand-regulated transcription factors that control diverse critical biological processes including various aspects of brain development. Eighteen NR genes exist in the Drosophila genome. To explore their roles in brain development, we knocked down individual NRs through the development of the mushroom bodies (MBs) by targeted RNAi. Besides recapitulating the known MB phenotypes for three NRs, we found that unfulfilled (unf), an ortholog of human photoreceptor specific nuclear receptor (PNR), regulates axonal morphogenesis and neuronal subtype identity. The adult MBs develop through remodeling of gamma neurons plus de-novo elaboration of both alpha'/beta' and alpha/beta neurons. Notably, unf is largely dispensable for the initial elaboration of gamma neurons, but plays an essential role in their re-extension of axons after pruning during early metamorphosis. The subsequently derived MB neuron types also require unf for extension of axons beyond the terminus of the pruned bundle. Tracing single axons revealed misrouting rather than simple truncation. Further, silencing unf in single-cell clones elicited misguidance of axons in otherwise unperturbed MBs. Such axon guidance defects may occur as MB neurons partially lose their subtype identity, as evidenced by suppression of various MB subtype markers in unf knockdown MBs. In sum, unf governs axonal morphogenesis of multiple MB neuron types, possibly through regulating neuronal subtype identity.", "link"=>"http://www.mendeley.com/research/nuclear-receptor-unfulfilled-regulates-axonal-guidance-cell-identity-drosophila-mushroom-body-neuron", "reader_count"=>35, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>2, "Student > Master"=>4}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Librarian"=>1, "Researcher"=>8, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>2, "Student > Master"=>4}, "reader_count_by_subject_area"=>{"Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>27, "Neuroscience"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"South Korea"=>1, "United States"=>1, "France"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/871159"], "description"=>"<p>Newly generated neurons of wild-type (A,C,E) and <i>unf</i> knockdown (B,D,F) MB labeled by <i>asense-GAL4</i> (green) at the indicated developmental stages. <i>unf</i> was knocked down by <i>asense-GAL4</i> dependent induction of <i>unf</i> miRNA-a. The arrowheads in [A]–[C] and [E] indicate the normal axonal bundles of the larval MB. The arrows in [D] and [F] indicate the axonal bundles that failed to extend beyond the MB peduncle. Scale bar: 20 µm.</p>", "links"=>[], "tags"=>["axonal", "morphogenesis", "types", "mb"], "article_id"=>541619, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_unf_is_required_for_the_initial_axonal_morphogenesis_in_later_types_of_MB_neurons_/541619", "title"=>"<i>unf</i> is required for the initial axonal morphogenesis in later types of MB neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:26:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/871472"], "description"=>"<p>(A–F) <i>GAL4-OK107</i> labeled flip-out clones (green in [A] and [B]; black in [C]–[F]) induced in a wild-type (A) or a <i>unf</i> knockdown (B–F) MB. Brains in [A] and [B] were co-labeled with anti-FasII Ab (magenta). [C]–[F] are high magnification views of some axons in the MB lobe in [B]. The arrows in [C] and [E] mark the axons with an unusual back turn(C), or even form a loop (E). [D] and [F] are duplicate images of [C] and [E] with the abnormal axonal paths highlighted by black lines for better visualization. Scale bars: 20 µm. (G–H) Wild-type (G) and <i>unf</i> knockdown (H) MARCM clones labeled by <i>GAL4-OK107</i> (green). <i>unf</i> was knocked down by <i>GAL4-OK107</i> induced <i>unf</i> miRNA-a. Brains were counterstained with anti-FasII Ab (magenta) to mark MB γ and α/β lobes. The arrow in [H] indicates a misrouted axon. Scale bar: 20 µm. (I–J) The calyx region of a <i>unf</i> knockdown adult MB labeled by <i>GAL4-OK107</i> (green; I) and anti-FasII immunostaining (magenta; I–J). <i>unf</i> was knockdown by <i>GAL4-OK107</i> induced <i>unf</i> miRNA-a. The arrows indicate a misrouted FasII-positive axonal bundle. Scale bar: 20 µm. (K–L) A illustration of the axonal projections in wild-type (K) and <i>unf</i> knockdown (L) MB.</p>", "links"=>[], "tags"=>["regulates", "axon", "pathfinding", "mb"], "article_id"=>541931, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_unf_regulates_axon_pathfinding_of_MB_neurons_/541931", "title"=>"<i>unf</i> regulates axon pathfinding of MB neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:32:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/870692"], "description"=>"<p>(A–C) Anti-FasII antibody staining (magenta) revealed the γ and α/β lobe morphology of wild-type (A), <i>EcR-</i> (B) and <i>usp-</i> (C) knockdown adult MBs. The knockdown was induced by <i>GAL4-OK107</i> dependent induction of miRNAs. Note the <i>EcR-</i> and <i>usp-</i>knockdown MBs contained unpruned γ processes (arrows in [B] and [C]) and lacked a normal-looking γ lobe (e.g. arrowhead in [A]). Scale bar: 20 µm. (D–F) Adult wild-type (D), <i>tll</i>- (E) and <i>unf-</i> (F) knockdown MB, labeled by <i>GAL4-OK107</i> (green). The knockdown was induced by <i>GAL4-OK107</i> dependent induction of miRNAs. Note the <i>tll-</i>knockdown MB contained only few neurons (E), and the axon lobes of <i>unf-</i>knockdown MB failed to extend along the correct paths (F).</p>", "links"=>[], "tags"=>["axonogenesis"], "article_id"=>541149, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_unf_is_required_for_the_proper_axonogenesis_of_the_mushroom_body_neurons_/541149", "title"=>"<i>unf</i> is required for the proper axonogenesis of the mushroom body neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:19:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/431884"], "description"=>"<div><p>Nuclear receptors (NRs) comprise a family of ligand-regulated transcription factors that control diverse critical biological processes including various aspects of brain development. Eighteen NR genes exist in the <em>Drosophila</em> genome. To explore their roles in brain development, we knocked down individual NRs through the development of the mushroom bodies (MBs) by targeted RNAi. Besides recapitulating the known MB phenotypes for three NRs, we found that <em>unfulfilled</em> (<em>unf</em>), an ortholog of human <em>photoreceptor specific nuclear receptor</em> (<em>PNR</em>), regulates axonal morphogenesis and neuronal subtype identity. The adult MBs develop through remodeling of γ neurons plus de-novo elaboration of both α′/β′ and α/β neurons. Notably, <em>unf</em> is largely dispensable for the initial elaboration of γ neurons, but plays an essential role in their re-extension of axons after pruning during early metamorphosis. The subsequently derived MB neuron types also require <em>unf</em> for extension of axons beyond the terminus of the pruned bundle. Tracing single axons revealed misrouting rather than simple truncation. Further, silencing <em>unf</em> in single-cell clones elicited misguidance of axons in otherwise unperturbed MBs. Such axon guidance defects may occur as MB neurons partially lose their subtype identity, as evidenced by suppression of various MB subtype markers in <em>unf</em> knockdown MBs. In sum, <em>unf</em> governs axonal morphogenesis of multiple MB neuron types, possibly through regulating neuronal subtype identity.</p></div>", "links"=>[], "tags"=>["receptor", "unfulfilled", "regulates", "axonal", "neurons"], "article_id"=>145256, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392", "stats"=>{"downloads"=>5, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Nuclear_Receptor_Unfulfilled_Regulates_Axonal_Guidance_and_Cell_Identity_of_Drosophila_Mushroom_Body_Neurons/145256", "title"=>"Nuclear Receptor Unfulfilled Regulates Axonal Guidance and Cell Identity of <em>Drosophila</em> Mushroom Body Neurons", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-12-22 01:27:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/871828"], "description"=>"<p>The cell body region of wild-type (A, C, E, G, I and K) or <i>unf</i> knockdown (B, D, F, H, J and L) adult (A–H) or wandering larval (I–L) MBs labeled with various MB specific markers, including Trio (A, B, I and J; magenta), <i>GAL4-NP21</i> (C and D; green), <i>GAL4-c305a</i> (E and F; green), <i>GAL4-c739</i> (G and H; green) and EcR-B1 (K and L; magenta). Brains in [A], [B], [I] and [J] were co-labeled with <i>GAL4-OK107</i>. The <i>unf</i> miRNA knockdown in [A], [B] and [I]–[L] was induced by <i>GAL4-OK107</i>, and the <i>unf</i> knockdown in [C]–[H] was induced by <i>asense-GAL4</i> together with <i>GAL4-NP21</i> (C and D), <i>GAL4-c305a</i> (E and F), or <i>GAL4-c739</i> (G and H). Note the Trio expression was normal in <i>unf</i> knockdown larval MB cell bodies (J), but became undetectable in <i>unf</i> knockdown adult MB cell bodies (B). <i>Um8G</i>: <i>UAS-mCD8::GFP</i>. Scale bar: 20 µm.</p>", "links"=>[], "tags"=>["markers", "knockdown"], "article_id"=>542287, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g009", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Subtype_specific_markers_were_lost_in_unf_knockdown_adult_MBs_/542287", "title"=>"Subtype-specific markers were lost in <i>unf</i> knockdown adult MBs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:38:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/870823"], "description"=>"<p>(A) Illustration of the <i>unf</i> cDNA that contains a 5′ region encoding a putative DNA binding domain (DBD) and a 3′ region encoding a putative ligand binding domain (LBD). <b>*</b>The miRNA target sites for <i>unf</i> miRNA-a. #The miRNA target site for <i>unf</i> miRNA-b. (B–C) <i>unf</i> in MB was knocked down by the <i>GAL4-OK107</i> induced <i>unf</i> miRNA-b in a wild-type fly (B), or a fly heterozygous for a deficiency <i>Df(2R)ED2426</i> that covers <i>unf</i> gene (C). Note some MB axons can still project to their correct positions when the <i>unf</i> miRNA-b was induced in the wild-type background (indicated by arrowheads in [B]). Scale bar: 20 µm. (D) Statistic results of the percentage of MB lacking dorsal projection in flies heterozygous for <i>Df(2R)ED2426</i> (<i>Df</i>), or in flies with <i>OK107-</i>dependent induction of <i>unf</i> miRNA-a(<i>unfi-a</i>), <i>unf</i> miRNA-b (<i>unfi-b</i>), or <i>unf</i> miRNA-b plus one allele of <i>Df(2R)ED2426</i> (<i>unfi-b/Df</i>).</p>", "links"=>[], "tags"=>["mb", "lobe", "phenotype", "was", "caused", "knockdown"], "article_id"=>541277, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_MB_lobe_phenotype_was_caused_by_specific_knockdown_of_unf_by_miRNA_/541277", "title"=>"The MB lobe phenotype was caused by specific knockdown of <i>unf</i> by miRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:21:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/871631"], "description"=>"<p>Wild-type brains (A,B,E–P) at the indicated development stages and a 6 hr-old larval brain with <i>GAL4-OK107</i> dependent induction of <i>unf</i> miRNA-a (C–D) were labeled with <i>GAL4-OK107</i> (green; A, C, E, G, I, K, M and O) and UNF immunostaining (magenta; A–P). Scale bars: 20 µm.</p>", "links"=>[], "tags"=>["continuously", "mb", "neurons"], "article_id"=>542091, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_unf_is_continuously_expressed_in_the_MB_neurons_throughout_development_/542091", "title"=>"<i>unf</i> is continuously expressed in the MB neurons throughout development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:34:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/871043"], "description"=>"<p>Wild-type (A,C,E,G) and <i>unf</i> knockdown (B,D,F,H) MB at the indicated developmental stages, labeled by <i>GAL4-201Y</i> (A–F) or <i>GAL4-MB247</i> (G,H). Brains in [A], [B], [G] and [H] were counterstained with anti-FasII antibody (magenta). <i>unf</i> was silenced by <i>GAL4-201Y</i> (B,D,F) or <i>GAL4-MB247</i> (H) induced <i>unf</i> miRNA-a. The arrows indicate the position of normal (A) and truncated γ lobes (B,H). Scale bars: 20 µm.</p>", "links"=>[], "tags"=>["acts", "mature", "neurons", "axon"], "article_id"=>541500, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_unf_acts_in_mature_neurons_to_govern_axon_re_extension_/541500", "title"=>"<i>unf</i> acts in mature γ neurons to govern axon re-extension.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:25:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/870922"], "description"=>"<p>Wild-type (A, C–F) and <i>unf</i> knockdown (B, G–J) MB at the indicated developmental stages were labeled by <i>GAL4-OK107</i> (A–J). The insect in [B] is an example of a small portion (12%; n = 75) of the <i>unf</i> -knockdown larval MB that displayed a thinner dorsal lobe phenotype. Brains in [E], [F], [I] and [J] were counterstained with anti-FasII antibody (magenta). <i>unf</i> was knocked down by <i>GAL4-OK107</i> induced <i>unf</i> miRNA-a. Scale bars: 20 µm.</p>", "links"=>[], "tags"=>["adult-specific", "mb"], "article_id"=>541386, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_unf_is_mainly_required_for_the_formation_of_adult_specific_MB_lobes_/541386", "title"=>"<i>unf</i> is mainly required for the formation of adult-specific MB lobes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:23:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/871318"], "description"=>"<p>GAL80[ts] was used to control the timing of <i>GAL4-OK107</i> dependent induction of <i>unf</i> miRNA-a to knock down <i>unf</i> in MB after mid-3rd instar (A–B), after adult eclosion (C–D) or after puparium formation (E–F). MBs were labeled by <i>GAL4-OK107</i> (green; A,C,E), anti-FasII (magenta; A–F) and anti-Dac (magenta; A,B,E,F) immunostaining. Scale bar: 20 µm.</p>", "links"=>[], "tags"=>["mb", "morphogenetic"], "article_id"=>541779, "categories"=>["Developmental Biology", "Neuroscience"], "users"=>["Suewei Lin", "Yaling Huang", "Tzumin Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0008392.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Direct_involvement_of_unf_in_later_MB_morphogenetic_processes_/541779", "title"=>"Direct involvement of <i>unf</i> in later MB morphogenetic processes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-12-22 00:29:39"}

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  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
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  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
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  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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  • {"unique-ip"=>"8", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"1", "full-text"=>"1", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
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Relative Metric

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