A CRM1-Mediated Nuclear Export Signal Is Essential for Cytoplasmic Localization of Neurogenin 3 in Neurons
Publication Date
January 30, 2013
Journal
PLOS ONE
Authors
Julia Simon Areces, Estefania Acaz Fonseca, Isabel Ruiz Palmero, Luis Miguel Garcia Segura, et al
Volume
8
Issue
1
Pages
e55237
DOI
https://dx.plos.org/10.1371/journal.pone.0055237
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0055237
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23383123
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3559332
Europe PMC
http://europepmc.org/abstract/MED/23383123
Web of Science
000315563800134
Scopus
84873832349
Mendeley
http://www.mendeley.com/research/crm1mediated-nuclear-export-signal-essential-cytoplasmic-localization-neurogenin-3-neurons
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Mendeley | Further Information

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/498988"], "description"=>"<p>At 3 DIV, neurons were immunostained for Ngn3 (red) and stained for actin with phalloidin (green) (panels A,E) or immunostained for Ngn3 (red) and tubulin (green) (panels B-D and F). (<b>A</b> and <b>D</b>) Representative confocal images. (<b>E</b> and <b>F</b>) Detail of growth cones. Note the association of Ngn3 with microtubules. In contrast Ngn3 was clearly not associated with actin filaments.</p>", "links"=>[], "tags"=>["co-localizes", "microtubules", "actin"], "article_id"=>169507, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ngn3_co_localizes_with_microtubules_and_not_with_actin_filaments_/169507", "title"=>"Ngn3 co-localizes with microtubules and not with actin filaments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 16:17:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/499286"], "description"=>"<p>Double-stranded oligonucleotides used for the construction of wild-type EGFP-NES1 and EGFP-NES2 constructs.</p>", "links"=>[], "tags"=>["oligonucleotides", "wild-type", "egfp-nes1", "egfp-nes2"], "article_id"=>169800, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.t001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Double_stranded_oligonucleotides_used_for_the_construction_of_wild_type_EGFP_NES1_and_EGFP_NES2_constructs_/169800", "title"=>"Double-stranded oligonucleotides used for the construction of wild-type EGFP-NES1 and EGFP-NES2 constructs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 16:19:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/499253"], "description"=>"<p>Primer sequences used for construction of pCS2-myc-Ngn3-L135A.</p>", "links"=>[], "tags"=>["sequences"], "article_id"=>169770, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.t003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primer_sequences_used_for_construction_of_pCS2_myc_Ngn3_L135A_/169770", "title"=>"Primer sequences used for construction of pCS2-myc-Ngn3-L135A.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 16:19:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/498301"], "description"=>"<p>The putative NES2 sequence is well conserved in various species. In the consensus NES sequence, X indicates any amino acid and Ø indicates a hydrophobic residue, such as leucine, isoleucine, valine or methionine. Letters colored green correspond to amino acids that are not conserved in the species studied. Residues critical to NES activity are indicated by red letters.</p>", "links"=>[], "tags"=>["putative", "sequences", "ngn3", "nes", "motifs", "homologues"], "article_id"=>168811, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_putative_nuclear_export_sequences_NESs_in_Ngn3_protein_with_consensus_NES_motifs_and_Ngn3_homologues_of_various_species_/168811", "title"=>"Comparison of putative nuclear export sequences (NESs) in Ngn3 protein with consensus NES motifs and Ngn3 homologues of various species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 16:13:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/499159"], "description"=>"<p>(<b>A</b>) Cultured neurons were untreated or treated with paclitaxel (Taxol; 20 µM) for 40 minutes; then cells were lysated and centrifuged. Proteins present in the precipitate, that includes microtubules and associated proteins (P) and supernatant (S) were analyzed by Western blotting. Ngn3 is enriched in the insoluble fractions and its concentration increases as polymerized tubulin does. (<b>B</b>) Embryonic mouse brains were homogenized and a high-speed precipitate was resuspended and divided in two. Aliquots were left untreated or treated with 20 µM paclitaxel plus 1 mM GTP for 40 minutes at room temperature. Microtubular fraction sedimented by centrifugation (P) and supernatant (S) were analyzed by Western blotting. (<b>C</b>) The supernatants (S) of control (C) and paclitaxel (T) treated aliquots were immunoprecipitated (IP) with anti-βIII-tubulin antibody (or IgG control) to determine the interaction of Ngn3 with soluble tubulin. Precipitates were analyzed by Western blotting with anti-Ngn3 antibody. Graphs show the quantification of densitometry. Error bars show the mean+s.e.m. of three experiments. Significance levels were determined for the data sets connected by horizontal lines using the Student’s t-test. * p<0.05, **p<0.01.</p>", "links"=>[], "tags"=>["perturbation", "cytoskeleton", "suggests", "ngn3", "tubulin"], "article_id"=>169677, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pharmacological_perturbation_of_the_cytoskeleton_suggests_association_of_Ngn3_to_tubulin_and_microtubules_/169677", "title"=>"Pharmacological perturbation of the cytoskeleton suggests association of Ngn3 to tubulin and microtubules.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 16:18:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/498648"], "description"=>"<p>(<b>A–F</b>) Cultured neurons were co-transfected with constructs encoding EGFP and full-length myc-tagged wild-type Ngn3 (myc-Ngn3), Ngn3 with leucine 135 mutated to alanine (myc-Ngn3-L135A) or empty vector expressing myc-tag. After 16 h, double immunostaining was performed using an anti-myc antibody to determine subcellular localization of wild-type and mutated myc-Ngn3 (A-C) and an anti-GFP antibody to visualize neurons at full (D-F). (<b>G</b>) Quantification of the relative fluorescence in the cell nucleus versus the cytoplasm of neurons. Graphs show the results (mean+s.e.m.) of at least three experiments. Significance levels were determined using a Student’s t-test; *** p<0.001 versus values of neurons transfected with plasmid expressing myc-tag.</p>", "links"=>[], "tags"=>["mutation", "nes2", "induces", "accumulation", "full-length"], "article_id"=>169166, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Point_mutation_in_NES2_induces_nuclear_accumulation_of_full_length_Ngn3_/169166", "title"=>"Point mutation in NES2 induces nuclear accumulation of full-length Ngn3.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 16:15:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/498420"], "description"=>"<p>(<b>A–D</b>) Representative single optical sections acquired by confocal microscopy of neurons expressing NES1 or NES2 fused to green fluorescent protein (EGFP). Cultured neurons were transfected at 2 DIV with expression plasmids for EGFP (A), EGFP-NES1 (B), or EGFP-NES2 (C and D) and after 16 h were treated with or without 20 nM LMB for 3 h. EGFP fluorescence was analyzed by confocal microscopy. The relative fluorescence intensity in the nucleus versus the cytoplasm was evaluated. In the absence of LMB (C) NES2 was enriched in the cytoplasm. Nuclear NES2 localization was increased in the presence of LMB (D), indicating that the signal of active nuclear exports in the Ngn3 is the NES2. (<b>E</b>) Quantification of the subcellular localization of Ngn3 in the cell nucleus versus the cytoplasm. Randomly selected fields containing cells counterstained with DAPI were digitalized and the Mean Gray Value for Ngn3 immunostaining was measured in the nuclei and cytoplasm areas using ImageJ 1.37 v software. The graphs show the mean+s.e.m. of the relative fluorescence intensity in nucleus versus cytoplasm. At least 70 cells from three experiments were counted for each experimental condition. Significance levels were determined using a Student t-test; *** p<0.001 versus EGFP expressing neurons values; ### p<0.001 of EGFP-NES2 transfection treated with LMB versus the same transfection not treated with LMB.</p>", "links"=>[], "tags"=>["putative", "sequences", "leptomycin"], "article_id"=>168939, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Activity_of_the_putative_nuclear_export_sequences_NESs_1_and_2_with_or_without_leptomycin_B_LMB_treatment_/168939", "title"=>"Activity of the putative nuclear export sequences (NESs) 1 and 2, with or without leptomycin B (LMB) treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 16:14:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/499233"], "description"=>"<p>Primer sequences used for construction of EGFP-NES2 mutants.</p>", "links"=>[], "tags"=>["sequences", "egfp-nes2"], "article_id"=>169746, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.t002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primer_sequences_used_for_construction_of_EGFP_NES2_mutants_/169746", "title"=>"Primer sequences used for construction of EGFP-NES2 mutants.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-19 16:18:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/498532"], "description"=>"<p>Cultured neurons were transfected at 2 DIV with expression plasmids for EGFP, EGFP-NES2, or EGFP-mutated NES2. (<b>A</b> and <b>B</b>) Representative single optical sections acquired by confocal microscopy of neurons expressing EGFP-NES2 or EGFP-NES2L135A. (<b>C</b>) Quantification of the subcellular localization of Ngn3 in the cell nucleus versus the cytoplasm. The only one mutation that was able to modify the subcellular distribution of EGFP-NES2 was L135A. In the rest of the mutations tested the location of the fusion protein continued to be mainly cytoplasmic and LMB sensitive (except for L139A that resulted LMB insensitive). The graphs show the mean+s.e.m. of the relative fluorescence intensity in nucleus versus cytoplasm. At least 70 cells from three experiments were counted for each experimental condition. Significance levels were determined using a Student’s t-test; *** p<0.001 versus EGFP expressing neurons values; ## p<0.01, ### p<0.001 versus the same transfection not treated with LMB; ns, not significant.</p>", "links"=>[], "tags"=>["neuroscience", "developmental biology", "Biochemistry"], "article_id"=>169046, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutational_analysis_of_NES2_/169046", "title"=>"Mutational analysis of NES2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 16:15:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/498824"], "description"=>"<p>(<b>A–C</b>) Hippocampal neuronal cultures were co-transfected with constructs encoding EGFP and full-length myc-tagged wild-type Ngn3 (myc-Ngn3), Ngn3 with leucine 135 mutated to alanine (myc-Ngn3-L135A) or empty vector expressing myc-tag as control. After 16 h, double immunostaining was performed using an anti-GFP antibody to visualize transfected neurons and an anti-synaptophysin I antibody to determine the morphology and the total number of synapses of the transfected neurons. (<b>D–F</b>) Lower panels show the boxed regions at higher magnification (<b>G</b>) Number of primary dendrites of the transfected neurons. (<b>H</b>) Counts of synaptophysin I immunoreactive terminals in contact with a neuron within a circular region of interest (ROI) with a diameter of 100 µm and centered in the neuronal soma. Data are mean+s.e.m. and significance levels were determined using ANOVA followed by the Bonferroni post hoc test; *** p<0.001 versus control neuron values and ### p<0.001 versus myc-Ngn3 expressing neuron values.</p>", "links"=>[], "tags"=>["nes2", "counteracts", "ngn3", "overexpression", "neuronal", "morphology", "synaptic"], "article_id"=>169336, "categories"=>["Biochemistry", "Neuroscience", "Developmental Biology"], "users"=>["Julia Simon-Areces", "Estefania Acaz-Fonseca", "Isabel Ruiz-Palmero", "Luis-Miguel Garcia-Segura", "Maria-Angeles Arevalo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0055237.g005", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutation_of_the_NES2_L135A_counteracts_the_effects_of_Ngn3_overexpression_on_neuronal_morphology_and_synaptic_inputs_/169336", "title"=>"Mutation of the NES2 (L135A) counteracts the effects of Ngn3 overexpression on neuronal morphology and synaptic inputs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 16:16:32"}

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Relative Metric

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