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{"title"=>"Neural epidermal growth factor-like like protein 2 (NELL2) promotes aggregation of embryonic carcinoma P19 cells by inducing N-cadherin expression", "type"=>"journal", "authors"=>[{"first_name"=>"Dong Hee", "last_name"=>"Kim", "scopus_author_id"=>"57194467431"}, {"first_name"=>"Han Rae", "last_name"=>"Kim", "scopus_author_id"=>"25227334300"}, {"first_name"=>"Eun Jung", "last_name"=>"Choi", "scopus_author_id"=>"27170908400"}, {"first_name"=>"Dong Yeol", "last_name"=>"Kim", "scopus_author_id"=>"36572051400"}, {"first_name"=>"Kwang Kon", "last_name"=>"Kim", "scopus_author_id"=>"56393403300"}, {"first_name"=>"Byung Sam", "last_name"=>"Kim", "scopus_author_id"=>"55553736170"}, {"first_name"=>"Jeong Woo", "last_name"=>"Park", "scopus_author_id"=>"57190284550"}, {"first_name"=>"Byung Ju", "last_name"=>"Lee", "scopus_author_id"=>"25929939400"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84908179524", "sgr"=>"84908179524", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0085898", "pmid"=>"24465772", "pui"=>"372852764"}, "id"=>"f4b5a9ba-8bad-3d98-8dd3-4a54bd12a505", "abstract"=>"NELL2 was first identified as a mammalian homolog of chick NEL (Neural EGF-like) protein. It is almost exclusively expressed in neurons of the rat brain and has been suggested to play a role in neural differentiation. However, there is still no clear evidence for the detailed function of NELL2 in the differentiation of neurons. In this study, we identified NELL2 function during neural differentiation of mouse embryonic carcinoma P19 cells. Endogenous expression of NELL2 in the P19 cells increased in parallel with the neuronal differentiation induced by retinoic acid (RA). We found that the mouse NELL2 promoter contains RA response elements (RAREs) and that treatment with RA increased NELL2 promoter activity. Transfection of P19 cells with NELL2 expression vectors induced a dramatic increase in cell aggregation, resulting in the facilitation of neural differentiation. Moreover, NELL2 significantly increased N-cadherin expression in the P19 cell. These data suggest that NELL2 plays an important role in the regulation of neuronal differentiation via control of N-cadherin expression and cell aggregation.", "link"=>"http://www.mendeley.com/research/neural-epidermal-growth-factorlike-like-protein-2-nell2-promotes-aggregation-embryonic-carcinoma-p19", "reader_count"=>11, "reader_count_by_academic_status"=>{"Researcher"=>2, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>2, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_user_role"=>{"Researcher"=>2, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Student > Master"=>1, "Other"=>1, "Student > Bachelor"=>2, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>7, "Medicine and Dentistry"=>1, "Neuroscience"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

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• http://doi.org/10.14348/molcells.2015.2216
• http://doi.org/10.1038/ncomms11473
• http://doi.org/10.1002/ajmg.a.37079
• http://doi.org/10.1111/ahg.12279

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/1353455"], "description"=>"<p>(A) General scheme for the neuronal differentiation process in this study. P19 cells were aggregated for 4 days with 1 µM RA treatment, and the aggregates were harvested and replated as the single-cell suspension and cultured without RA for 4 days. (B) Representative photos showing morphological changes in P19 cells during the neuronal differentiation process. Cells show aggregated morphologies as embryonic bodies at 2 and 4 days of aggregation, and reveal bipolar shapes with processes at 2 and 4 days after replating. Control (CTL) represents 2 days of aggregation without any treatment. (C, E, F) Real-time PCR analysis of <i>NELL2</i> (C), <i>Tuj-1</i> (E) and <i>Nestin</i> (F) mRNA expression in the P19 cells during the process of aggregation and replating. Agg, aggregation; Rep, replating; AU, arbitrary units. All experiments were repeated at least four times and data are presented as mean ± SEM. *, p<0.05; **, p<0.01; ***, p<0.001 versus control (CTL). (D) Western blot analysis of NELL2 and Tuj-1 protein expression during the neuronal differentiation process of the P19 cells.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "nell2", "ra-induced", "neuronal", "differentiation", "p19"], "article_id"=>905922, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Change_in_NELL2_expression_during_the_RA_induced_neuronal_differentiation_of_P19_cells_/905922", "title"=>"Change in NELL2 expression during the RA-induced neuronal differentiation of P19 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353460"], "description"=>"<p>(A) Overexpression of NELL2 in P19 cells permanently transfected with NELL2 expression vectors confirmed by RT-PCR using RNA extracted from the cells. CTL, control cells; pcDNA, cells transfected with control pcDNA vectors; NELL2, cells transfected with NELL2 expression vectors. (B). Western blot analysis for overexpression of NELL2 protein in the P19 cells permanently transfected with NELL2 expression vectors. (C) Representative photograms showing the morphological changes of P19 cells by overexpression of the NELL2 expression vectors with or without the treatment of RA (1 µM). (D–F) Real-time PCR analysis of <i>Ngn-1</i> (D), <i>Nestin</i> (E) and <i>Tuj-1</i> (F) mRNA expression in the P19 cells overexpressing NELL2 during the aggregation and replating process of the neuronal differentiation. RNA samples were collected from P19 cells with the indicated treatment at 2 and 4 days after aggregation and replating. (G) Western blot analysis of NeuN protein expression in P19 cells during aggregation and replating processes. All experiments were repeated at least four times and data are presented as mean ± SEM. *, p<0.05; **, p<0.01; ***, p<0.001 versus control pcDNA group.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "neuronal", "differentiation", "p19"], "article_id"=>905929, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NELL2_promotes_neuronal_differentiation_of_P19_cells_/905929", "title"=>"NELL2 promotes neuronal differentiation of P19 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353463"], "description"=>"<p>P19 cells permanently transfected with NELL2 expression vectors were cultured in the presence or absence of 1 µM RA for 2 (A) or 4 (B) days. To knock down NELL2 synthesis, the indicated groups of P19 cells were transfected with siRNA against <i>NELL2</i> mRNA (siNELL2). Each upper panel reveals representative photos and the lower panel includes results showing difference in single cell numbers among treatment groups. All experiments were repeated at least four times and data are presented as mean ± SEM. *, p<0.05; **, p<0.01; ***, p<0.001 versus control pcDNA group or between lined groups.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "aggregation", "p19"], "article_id"=>905937, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NELL2_promotes_aggregation_of_P19_cells_/905937", "title"=>"NELL2 promotes aggregation of P19 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353464"], "description"=>"<p>(A, B) Real-time PCR analysis of <i>E-cadherin</i> (A) and <i>N-cadherin</i> (B) mRNA expression in the P19 cells expressing NELL2 with or without treatment of RA, as indicated. For real-time PCR analysis, RNA samples were harvested from the cells at 2 and 4 days after aggregation and replating. (C) Data showing changes in N-cadherin protein expression calculated from Western blot analysis of samples collected at the aggregation and replating processes of neuronal differentiation of P19 cells. All experiments were repeated at least four times and data are presented as mean ± SEM. *, p<0.05; **, p<0.01; ***, p<0.001 versus control pcDNA group.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "nell2", "n-cadherin", "p19"], "article_id"=>905938, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g006", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_NELL2_on_the_N_cadherin_expression_in_P19_cells_/905938", "title"=>"Effect of NELL2 on the N-cadherin expression in P19 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353466"], "description"=>"<p>P19 cells permanently transfected with NELL2 expression vectors were treated with 5 µM U0126 (a MEK inhibitor) in the presence or absence of 1 µM RA for 4 days. (A) Representative Western blots showing effect of U0126 on the ERK phosphorylation and N-cadherin and c-Fos expression. (B–D) Data showing the U0126-induced changes in phosphorylation of ERK (B) and expression of N-cadherin (C) and c-Fos (D), calculated from Western blot analyses. All experiments were repeated at least four times and data are presented as mean ± SEM. *, p<0.05; **, p<0.01; ***, p<0.001 versus control pcDNA group or between indicated groups.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "regulates", "n-cadherin", "erk"], "article_id"=>905940, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g007", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NELL2_regulates_N_cadherin_expression_through_the_ERK_signaling_/905940", "title"=>"NELL2 regulates N-cadherin expression through the ERK signaling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353467"], "description"=>"<p>RA diffuses across the plasma membrane and RA-receptor (RAR/RXR) complexes bind to the RA response elements (RAREs) of the <i>NELL2</i> promoter region. These complexes transcriptionally activate NELL2 expression, and, in turn, released NELL2 stimulates the ERK pathway via as yet unknown receptor signaling. The activated ERK increases synthesis of N-cadherin, which mediates cell-cell adhesion and neuronal differentiation.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "hypothetical", "nell2", "neuronal", "differentiation", "p19"], "article_id"=>905941, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g008", "stats"=>{"downloads"=>4, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_hypothetical_model_for_NELL2_action_in_the_neuronal_differentiation_of_P19_cells_/905941", "title"=>"A hypothetical model for NELL2 action in the neuronal differentiation of P19 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353469", "https://ndownloader.figshare.com/files/1353470", "https://ndownloader.figshare.com/files/1353471"], "description"=>"<div><p>NELL2 was first identified as a mammalian homolog of chick NEL (Neural EGF-like) protein. It is almost exclusively expressed in neurons of the rat brain and has been suggested to play a role in neural differentiation. However, there is still no clear evidence for the detailed function of NELL2 in the differentiation of neurons. In this study, we identified NELL2 function during neural differentiation of mouse embryonic carcinoma P19 cells. Endogenous expression of NELL2 in the P19 cells increased in parallel with the neuronal differentiation induced by retinoic acid (RA). We found that the mouse <i>NELL2</i> promoter contains RA response elements (RAREs) and that treatment with RA increased <i>NELL2</i> promoter activity. Transfection of P19 cells with <i>NELL2</i> expression vectors induced a dramatic increase in cell aggregation, resulting in the facilitation of neural differentiation. Moreover, NELL2 significantly increased N-cadherin expression in the P19 cell. These data suggest that NELL2 plays an important role in the regulation of neuronal differentiation via control of N-cadherin expression and cell aggregation.</p></div>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "neural", "epidermal", "factor-like", "aggregation", "embryonic", "carcinoma", "p19", "cells", "inducing", "n-cadherin"], "article_id"=>905943, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0085898.s001", "https://dx.doi.org/10.1371/journal.pone.0085898.s002", "https://dx.doi.org/10.1371/journal.pone.0085898.s003"], "stats"=>{"downloads"=>9, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Neural_Epidermal_Growth_Factor_Like_Like_Protein_2_NELL2_Promotes_Aggregation_of_Embryonic_Carcinoma_P19_Cells_by_Inducing_N_Cadherin_Expression/905943", "title"=>"Neural Epidermal Growth Factor-Like Like Protein 2 (<i>NELL2</i>) Promotes Aggregation of Embryonic Carcinoma P19 Cells by Inducing N-Cadherin Expression", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353451"], "description"=>"<p>(A) To determine the effects of RA on m<i>NELL2</i> promoter activity, a 1.3 kb m<i>NELL2</i> promoter-luciferase (luc) reporter construct was transfected into the P19 cells, and the luciferase activity was determined 24 h after the RA treatment. (B) Real-time PCR analysis showing the change in endogenous <i>NELL2</i> mRNA expression by RA treatment. (C) Western blot analysis to determine changes in RA-induced NELL2 expression. High concentration (1 µM) of RA increased intracellular NELL2 or secreted NELL2 (sNELL2). All experiments were repeated at least four times and data are presented as mean ± SEM. *, p<0.05; ***, p<0.001 versus control (DMSO for A, 0 µM for B).</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology", "activates", "promoter", "endogenous", "mrna", "p19"], "article_id"=>905918, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Retinoic_acid_RA_activates_m_NELL2_promoter_activity_and_expression_of_endogenous_NELL2_mRNA_and_protein_in_P19_cells_/905918", "title"=>"Retinoic acid (RA) activates m<i>NELL2</i> promoter activity and expression of endogenous <i>NELL2</i> mRNA and protein in P19 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}
• {"files"=>["https://ndownloader.figshare.com/files/1353452"], "description"=>"<p>EMSAs were performed using double-stranded oligomer probes containing the putative half-RAREs found in the m<i>NELL2</i> promoter sequence. (A) Autoradiogram showing binding activity of half-RAREs derived from the m<i>NELL2</i> promoter to the nuclear extracts from P19 cells treated with RA (1 µM). Numbers on the gel images indicate the sites in the m<i>NELL2</i> promoter sequence where the oligomer probes were designed; M following the numbers means that the indicted probes bear a mutation in the half-RARE sites. B, protein-bound DNA; F, free DNA; PC, a positive control palindromic RARE; NC, a negative control of mutant RARE. (B) ChIP assays using DNA precipitated by using RAR antibodies. The immunoprecipitated DNA from P19 cells treated with RA or DMSO was PCR-amplified using primer sets designed to detect m<i>NELL2</i> promoter fragments including the two half-RARE sequences (at −223 and −1047). Input represents the used DNA extracted from the P19 cells before immunoprecipitation. Normal rabbit IgG was included for immunoprecipitation in the assay as a negative control.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Protein interactions", "developmental biology", "Cell differentiation", "Cell fate determination", "Molecular cell biology", "Cellular types", "neurons", "Signal transduction", "neuroscience", "Cellular neuroscience", "Neuronal morphology"], "article_id"=>905919, "categories"=>["Biological Sciences"], "users"=>["Dong Hee Kim", "Han Rae Kim", "Eun Jung Choi", "Dong Yeol Kim", "Kwang Kon Kim", "Byung Sam Kim", "Jeong Woo Park", "Byung Ju Lee"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085898.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_EMSA_and_ChIP_assays_/905919", "title"=>"EMSA and ChIP assays.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:43:01"}

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Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[285]}, {"subject_area"=>"/Biology and life sciences/Molecular biology", "average_usage"=>[292, 461]}]}

F1000Prime