TDP-43-Mediated Neuron Loss In Vivo Requires RNA-Binding Activity
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{"title"=>"TDP-43-mediated neuron loss In Vivo requires RNA-binding activity", "type"=>"journal", "authors"=>[{"first_name"=>"Aaron", "last_name"=>"Voigt", "scopus_author_id"=>"7102088269"}, {"first_name"=>"David", "last_name"=>"Herholz", "scopus_author_id"=>"36552532400"}, {"first_name"=>"Fabienne C.", "last_name"=>"Fiesel", "scopus_author_id"=>"24179392800"}, {"first_name"=>"Kavita", "last_name"=>"Kaur", "scopus_author_id"=>"36552353200"}, {"first_name"=>"Daniel", "last_name"=>"Müller", "scopus_author_id"=>"57199771930"}, {"first_name"=>"Peter", "last_name"=>"Karsten", "scopus_author_id"=>"6602400574"}, {"first_name"=>"Stephanie S.", "last_name"=>"Weber", "scopus_author_id"=>"26667281600"}, {"first_name"=>"Philipp J.", "last_name"=>"Kahle", "scopus_author_id"=>"7003861568"}, {"first_name"=>"Till", "last_name"=>"Marquardt", "scopus_author_id"=>"7004604110"}, {"first_name"=>"Jörg B.", "last_name"=>"Schulz", "scopus_author_id"=>"7201479829"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-77957918535", "sgr"=>"77957918535", "pui"=>"359761525", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pmid"=>"20806063", "doi"=>"10.1371/journal.pone.0012247"}, "id"=>"0ac44601-3d84-3f65-adb9-9f85219ae599", "abstract"=>"Alteration and/or mutations of the ribonucleoprotein TDP-43 have been firmly linked to human neurodegenerative diseases, including amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). The relative impacts of TDP-43 alteration, mutation, or inherent protein function on neural integrity, however, remain less clear--a situation confounded by conflicting reports based on transient and/or random-insertion transgenic expression. We therefore performed a stringent comparative investigation of impacts of these TDP-43 modifications on neural integrity in vivo. To achieve this, we systematically screened ALS/FTLD-associated and synthetic TDP-43 isoforms via same-site gene insertion and neural expression in Drosophila; followed by transposon-based motor neuron-specific transgenesis in a chick vertebrate system. Using this bi-systemic approach we uncovered a requirement of inherent TDP-43 RNA-binding function--but not ALS/FTLD-linked mutation, mislocalization, or truncation--for TDP-43-mediated neurotoxicity in vivo.", "link"=>"http://www.mendeley.com/research/tdp43mediated-neuron-loss-vivo-requires-rnabinding-activity", "reader_count"=>97, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>3, "Researcher"=>27, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>5, "Student > Master"=>9, "Other"=>3, "Student > Bachelor"=>7, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>3, "Researcher"=>27, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>32, "Student > Postgraduate"=>5, "Student > Master"=>9, "Other"=>3, "Student > Bachelor"=>7, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>10, "Agricultural and Biological Sciences"=>65, "Medicine and Dentistry"=>15, "Neuroscience"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>15}, "Neuroscience"=>{"Neuroscience"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>65}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>1, "United Kingdom"=>4, "Spain"=>2}, "group_count"=>1}

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  • {"files"=>["https://ndownloader.figshare.com/files/835427"], "description"=>"<p>(A) TDP-43 expression reduces longevity in <i>Drosophila</i>. Flies with pan-neural (<i>elav</i>::<i>Gal4</i>) expression of indicated TDP-43 variants were assayed for longevity. (B) Median survival of respective survival curves. (C) Cross-comparison of survival curves with regard to statistical significance after Bonferroni correction. (D) Age-dependent locomotion defects after TDP-43 expression in motor neurons. Flies expressing indicated TDP-43 variants specifically in motor neurons (<i>D42::Gal4</i>) were assayed for negative geotaxis at 1, 10 and 20 days post eclosion. (E) Detailed summary of statistical analysis (2-Way ANOVA followed by Bonferroni post-hoc tests) of age-dependent locomotion effects. Genotypes of flies analyzed: <i>elav<sup>C155</sup>::Gal4/Y;UAS::TDP-43/+</i> in longevity analysis and <i>w/Y;UAS::TDP-43/+;D42::Gal4/+</i> in case of locomotion assay. <i>elav<sup>C155</sup>::Gal4/Y</i> (longevity) and <i>w/Y;;D42::Gal4</i> (climbing) served as controls. *p<0.05; **p<0.01; ***p<0.001; ns not significant.</p>", "links"=>[], "tags"=>["rna-binding", "tdp-43-mediated", "neural", "defects"], "article_id"=>505790, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012247.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Requirement_for_RNA_binding_activity_for_TDP_43_mediated_neural_defects_in_Drosophila_/505790", "title"=>"Requirement for RNA-binding activity for TDP-43-mediated neural defects in <i>Drosophila</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-18 01:36:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/834957"], "description"=>"<p>(A) Schematic overview of TDP-43 variants tested <i>in vivo</i>. Positions and nature of amino acid substitutions and size of two C-terminal fragments (CTFs) analyzed are indicated. Synthetic mutations (SM) were introduced to interfere with TDP-43 localization or function. Mutations in the nuclear localization signal (ΔNLS) were introduced to target TDP-43 to the cytoplasm and mutations F147L/F149L (FFLL) in the first RNA recognition motive (RRM1) were introduced to impair TDP-43 inherent RNA-binding capacity. (B) Loss of RNA-binding by TDP-43<sup>FFLL</sup>. Biotinylated oligonucleotides were incubated with lysates from either untransfected HEK293 cells or HEK293 cells transfected with FLAG-tagged TDP-43<sup>WT</sup> or TDP-43<sup>FFLL</sup> (left, input) followed by UV crosslinking and streptavidin-pulldown of Biotin-RNA (right, pulldown). Precipitates were separated, blotted and membranes probed with FLAG- (upper panel) and TDP-43-specific (lower panel) antibodies to assay co-precipitation of TDP-43. Note: Co-precipitation of endogenous TDP-43 with (UG)<sub>12</sub>-repeats in all lysates. Ectopic FLAG-TDP-43<sup>WT</sup>, but not FLAG-TDP-43<sup>FFLL</sup> co-precipitated with cognate UG repeats. GAPDH served as loading control for protein input. (C) Equalized pan-neural expression of <i>φ-C31</i>-inserted TDP-43 variants in adult <i>Drosophilae</i>. TDP-43 expression was visualized using an anti-human TDP-43 antibody. Syntaxin served as loading control. (D) Assessment of relative TBPH and TDP-43 expression levels. Left graph: Relative abundance of endogenous TBPH transcripts in relation to <i>actin5C</i> of wild type strain OregonR (OreR), the Gal4-driver line (<i>elav<sup>C155</sup>::Gal4</i>) and flies with pan-neural TDP-43 expression (<i>elav<sup>C155</sup>::Gal4/Y;UAS::TDP-43<sup>WT</sup>/+</i>). TBPH levels were not significantly different in analyzed genotypes. Right graph: mRNA abundance of TDP-43 in flies with pan-neural expression of the different TDP-43 variants normalized to <i>actin5C</i> and <i>TBPH</i> mRNA levels. Significant differences are indicated. *p<0.05; ***p<0.001. Head lysates of flies with pan-neural expression of TDP-43 were used for Western blot and qPCR analysis. <i>elav::Gal4</i> flies without a TDP-43 transgene (elav) were used as negative control.</p>", "links"=>[], "tags"=>["tdp-43", "variants", "ectopic"], "article_id"=>505321, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012247.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_different_TDP_43_variants_used_for_ectopic_expression_/505321", "title"=>"Analysis of different TDP-43 variants used for ectopic expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-18 01:28:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/415952", "https://ndownloader.figshare.com/files/415990", "https://ndownloader.figshare.com/files/416028", "https://ndownloader.figshare.com/files/416050", "https://ndownloader.figshare.com/files/416073"], "description"=>"<div><p>Alteration and/or mutations of the ribonucleoprotein TDP-43 have been firmly linked to human neurodegenerative diseases, including amyotrophic lateral sclerosis (ALS) and frontotemporal lobar degeneration (FTLD). The relative impacts of TDP-43 alteration, mutation, or inherent protein function on neural integrity, however, remain less clear—a situation confounded by conflicting reports based on transient and/or random-insertion transgenic expression. We therefore performed a stringent comparative investigation of impacts of these TDP-43 modifications on neural integrity <em>in vivo</em>. To achieve this, we systematically screened ALS/FTLD-associated and synthetic TDP-43 isoforms via same-site gene insertion and neural expression in <em>Drosophila</em>; followed by transposon-based motor neuron-specific transgenesis in a chick vertebrate system. Using this bi-systemic approach we uncovered a requirement of inherent TDP-43 RNA-binding function—but not ALS/FTLD-linked mutation, mislocalization, or truncation—for TDP-43-mediated neurotoxicity <em>in vivo</em>.</p></div>", "links"=>[], "tags"=>["tdp-43-mediated", "neuron", "requires", "rna-binding"], "article_id"=>142119, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0012247.s001", "https://dx.doi.org/10.1371/journal.pone.0012247.s002", "https://dx.doi.org/10.1371/journal.pone.0012247.s003", "https://dx.doi.org/10.1371/journal.pone.0012247.s004", "https://dx.doi.org/10.1371/journal.pone.0012247.s005"], "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/TDP_43_Mediated_Neuron_Loss_In_Vivo_Requires_RNA_Binding_Activity/142119", "title"=>"TDP-43-Mediated Neuron Loss <em>In Vivo</em> Requires RNA-Binding Activity", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-08-18 00:35:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/835676"], "description"=>"<p>Expression of TDP-43:GFP variants using different Gal4-driver lines. Impact of TDP-43 expression on vitality was assayed.</p>", "links"=>[], "tags"=>["neurological disorders", "neurological disorders/cognitive neurology and dementia", "neurological disorders/neurogenetics", "neurological disorders/neuromuscular diseases"], "article_id"=>506030, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012247.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_TDP_43_GFP_variants_/506030", "title"=>"Expression of TDP-43:GFP variants.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-08-18 01:40:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/835062"], "description"=>"<p>HEK293E cells transfected with N-terminal Flag-tagged TDP-43 variants detected with Flag- (left, green) and TDP-43 (middle, red) specific antibodies. Overlay (right) with Hoechst stained DNA (blue). (A) Exogenous TDP-43 had to be visualized via fused Flag-tag, as HEK cells show robust endogenous expression of TDP-43. (B) Ectopic TDP-43<sup>WT</sup> mainly localized to the nucleus. (C) In contrast, TDP-43<sup>ΔNLS</sup> exclusively localized to cytosol without showing nuclear Flag-signal. Similar to TDP-43<sup>FFLL</sup> (D), also TDP-43<sup>MS</sup> (E–I) displayed a nuclear localization. However, TDP-43<sup>FFLL</sup> localized in a characteristic punctuate pattern throughout the nucleus (D). (J) TDP-43<sup>CTF</sup> displayed a predominantly cytoplasmic localization similar to TDP-43<sup>ΔNLS</sup> (compare C and J). Scale bar indicates 10 µm.</p>", "links"=>[], "tags"=>["tdp-43", "variants"], "article_id"=>505423, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012247.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Localization_of_TDP_43_variants_in_human_cells_/505423", "title"=>"Localization of TDP-43 variants in human cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-18 01:30:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/835249"], "description"=>"<p>Confocal sections of eye imaginal discs from <i>Drosophila</i> larvae (left panel) and motor neurons from <i>Gallus</i> (right panel) expressing indicated TDP-43 variants. To be able to discriminate between the two <i>in vivo</i> systems, ectopic TDP-43 in <i>Drosophila</i> is shown in green, whereas TDP-43 in <i>Gallus</i> is shown in red. Subcellular localization of the different TDP-43 variants was found to be identical between fly and chick. TDP-43<sup>WT</sup> (A) localized mainly to the nucleus, while TDP-43<sup>ΔNLS</sup> (B) was found predominantly in the cytoplasm. TDP-43<sup>FFLL</sup> (C) and TDP-43<sup>A315T</sup> (D) displayed a nuclear distribution. Only cells with very high expression levels of usually nuclear TDP-43 displayed a detectable cytoplasmic staining (example in case of TDP-43<sup>FFLL</sup> marked by asterisk). DNA was stained with Sytox® Orange (fly, red) or DAPI (chick, white). Scale bar indicates 50 µm. Neuronal expression was mediated by <i>elav::Gal4</i> (flies) or <i>Hb9::Cre</i> (chick).</p>", "links"=>[], "tags"=>["tdp-43"], "article_id"=>505614, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012247.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Localization_of_TDP_43_in_Drosophila_melanogaster_and_Gallus_gallus_/505614", "title"=>"Localization of TDP-43 in <i>Drosophila melanogaster</i> and <i>Gallus gallus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-18 01:33:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/835557"], "description"=>"<p>(A) Stable unilateral expression of human TDP-43 variants in chick (<i>Gallus gallus</i>) spinal cord. [i] Schematic of expression system mediating motor neuron-restricted expression upon unilateral transfection. [ii] Unilateral expression of human TDP-43<sup>FFLL</sup> (red) in embryonic day 9 (E9) chick spinal cord (nuclei labeled with DAPI: blue): transversal section at lumbar levels. “−” and “+” respectively indicate control and transfected hemicords. Isl1/2 labels motor neuron nuclei (green). (B) [i] Examples of thoracic motor columns (Isl1/2<sup>+</sup> motor neurons: green) upon TDP-43 variant expression (red). [ii] Quantification of motor neuron loss upon TDP-43 variant expression over all obtained sections (in “-” versus “+” hemicord). Differences relative to control (t-student's test) are indicated. (C) [i] Activated Caspase-3 (green) detected in E5 motor neurons upon TDP-43<sup>WT</sup> expression (indicated by <i>IRES-cherry</i> bi-cistronic reporter: red). Compared to E5 motor neurons expressing TDP-43<sup>WT</sup>, little activation of Caspase-3 was detected upon TDP-43<sup>CTF</sup> expression. [ii] Quantification of Caspase-3 activation in motor neurons of transfected hemicords versus vector control. Significant differences are indicated (t-student's test - relative to control). *p<0.05; **p<0.01; ***p<0.001; ns not significant.</p>", "links"=>[], "tags"=>["tdp-43-mediated", "neuron"], "article_id"=>505916, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012247.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RNA_binding_activity_is_required_for_TDP_43_mediated_motor_neuron_loss_in_chick_/505916", "title"=>"RNA-binding activity is required for TDP-43-mediated motor neuron loss in chick.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-08-18 01:38:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/835710"], "description"=>"<p>Expression of TDP-43 variants using different Gal4-driver lines. Impact of TDP-43 expression on vitality was assayed.</p>", "links"=>[], "tags"=>["tdp-43"], "article_id"=>506073, "categories"=>["Neuroscience"], "users"=>["Aaron Voigt", "David Herholz", "Fabienne C. Fiesel", "Kavita Kaur", "Daniel Müller", "Peter Karsten", "Stephanie S. Weber", "Philipp J. Kahle", "Till Marquardt", "Jörg B. Schulz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0012247.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_TDP_43_variants_/506073", "title"=>"Expression of TDP-43 variants.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-08-18 01:41:13"}

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Relative Metric

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