Upregulation of the Cell-Cycle Regulator RGC-32 in Epstein-Barr Virus-Immortalized Cells
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{"title"=>"Upregulation of the cell-cycle regulator RGC-32 in epstein-barr virus-immortalized cells", "type"=>"journal", "authors"=>[{"first_name"=>"Sandra N.", "last_name"=>"Schlick", "scopus_author_id"=>"54418042400"}, {"first_name"=>"C. David", "last_name"=>"Wood", "scopus_author_id"=>"57199015112"}, {"first_name"=>"Andrea", "last_name"=>"Gunnell", "scopus_author_id"=>"24544431900"}, {"first_name"=>"Helen M.", "last_name"=>"Webb", "scopus_author_id"=>"56212124300"}, {"first_name"=>"Sarika", "last_name"=>"Khasnis", "scopus_author_id"=>"54417276600"}, {"first_name"=>"Aloys", "last_name"=>"Schepers", "scopus_author_id"=>"6701359341"}, {"first_name"=>"Michelle J.", "last_name"=>"West", "scopus_author_id"=>"7402068676"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-82755192438", "sgr"=>"82755192438", "pui"=>"363035568", "pmid"=>"22163048", "doi"=>"10.1371/journal.pone.0028638"}, "id"=>"4872dd6a-049b-30d9-a345-229071009aca", "abstract"=>"Epstein-Barr virus (EBV) is implicated in the pathogenesis of multiple human tumours of lymphoid and epithelial origin. The virus infects and immortalizes B cells establishing a persistent latent infection characterized by varying patterns of EBV latent gene expression (latency 0, I, II and III). The CDK1 activator, Response Gene to Complement-32 (RGC-32, C13ORF15), is overexpressed in colon, breast and ovarian cancer tissues and we have detected selective high-level RGC-32 protein expression in EBV-immortalized latency III cells. Significantly, we show that overexpression of RGC-32 in B cells is sufficient to disrupt G2 cell-cycle arrest consistent with activation of CDK1, implicating RGC-32 in the EBV transformation process. Surprisingly, RGC-32 mRNA is expressed at high levels in latency I Burkitt's lymphoma (BL) cells and in some EBV-negative BL cell-lines, although RGC-32 protein expression is not detectable. We show that RGC-32 mRNA expression is elevated in latency I cells due to transcriptional activation by high levels of the differentially expressed RUNX1c transcription factor. We found that proteosomal degradation or blocked cytoplasmic export of the RGC-32 message were not responsible for the lack of RGC-32 protein expression in latency I cells. Significantly, analysis of the ribosomal association of the RGC-32 mRNA in latency I and latency III cells revealed that RGC-32 transcripts were associated with multiple ribosomes in both cell-types implicating post-initiation translational repression mechanisms in the block to RGC-32 protein production in latency I cells. In summary, our results are the first to demonstrate RGC-32 protein upregulation in cells transformed by a human tumour virus and to identify post-initiation translational mechanisms as an expression control point for this key cell-cycle regulator.", "link"=>"http://www.mendeley.com/research/upregulation-cellcycle-regulator-rgc32-epsteinbarr-virusimmortalized-cells", "reader_count"=>14, "reader_count_by_academic_status"=>{"Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Master"=>4, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>2, "Student > Master"=>4, "Other"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>8, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>8}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}}, "reader_count_by_country"=>{"United Kingdom"=>1, "Germany"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/358120", "https://ndownloader.figshare.com/files/358213"], "description"=>"<div><p>Epstein-Barr virus (EBV) is implicated in the pathogenesis of multiple human tumours of lymphoid and epithelial origin. The virus infects and immortalizes B cells establishing a persistent latent infection characterized by varying patterns of EBV latent gene expression (latency 0, I, II and III). The CDK1 activator, Response Gene to Complement-32 (RGC-32, C13ORF15), is overexpressed in colon, breast and ovarian cancer tissues and we have detected selective high-level RGC-32 protein expression in EBV-immortalized latency III cells. Significantly, we show that overexpression of RGC-32 in B cells is sufficient to disrupt G2 cell-cycle arrest consistent with activation of CDK1, implicating RGC-32 in the EBV transformation process. Surprisingly, RGC-32 mRNA is expressed at high levels in latency I Burkitt's lymphoma (BL) cells and in some EBV-negative BL cell-lines, although RGC-32 protein expression is not detectable. We show that RGC-32 mRNA expression is elevated in latency I cells due to transcriptional activation by high levels of the differentially expressed RUNX1c transcription factor. We found that proteosomal degradation or blocked cytoplasmic export of the RGC-32 message were not responsible for the lack of RGC-32 protein expression in latency I cells. Significantly, analysis of the ribosomal association of the RGC-32 mRNA in latency I and latency III cells revealed that RGC-32 transcripts were associated with multiple ribosomes in both cell-types implicating post-initiation translational repression mechanisms in the block to RGC-32 protein production in latency I cells. In summary, our results are the first to demonstrate RGC-32 protein upregulation in cells transformed by a human tumour virus and to identify post-initiation translational mechanisms as an expression control point for this key cell-cycle regulator.</p> </div>", "links"=>[], "tags"=>["upregulation", "cell-cycle", "rgc-32", "epstein-barr", "virus-immortalized", "cells"], "article_id"=>130782, "categories"=>["Molecular Biology", "Cancer", "Genetics"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.s001", "https://dx.doi.org/10.1371/journal.pone.0028638.s002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Upregulation_of_the_Cell_Cycle_Regulator_RGC_32_in_Epstein_Barr_Virus_Immortalized_Cells/130782", "title"=>"Upregulation of the Cell-Cycle Regulator RGC-32 in Epstein-Barr Virus-Immortalized Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-12-06 00:13:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/705460"], "description"=>"<p>(A) Western blot analysis of RGC-32 protein expression in a panel of EBV negative and positive B-cell-lines. Blots were stripped and re-probed with anti-actin antibodies as a loading control (B) Western blot analysis of RGC-32 protein expression in two EBV negative BL cell-lines (BL2 and BL31) infected with recombinant wild-type EBV bacmids <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028638#pone.0028638-Anderton1\" target=\"_blank\">[15]</a>. (C) Western blot analysis of RGC-32 protein expression in Mutu III cell-cycle fractions obtained by centrifugal elutriation. Blots were probed for CDK1 and cyclin B1 as controls for cell-cycle phases. Cell-cycle phases were confirmed by Flow cytometry (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028638#pone.0028638.s001\" target=\"_blank\">Figure S1</a>).</p>", "links"=>[], "tags"=>["selectively", "ebv", "infected", "latency", "iii"], "article_id"=>375818, "categories"=>["Virology", "Molecular Biology", "Cancer", "Genetics", "Infectious Diseases"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RGC_32_protein_is_selectively_expressed_in_EBV_infected_latency_III_cells_/375818", "title"=>"RGC-32 protein is selectively expressed in EBV infected latency III cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:36:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/705528"], "description"=>"<p>(A) Histone H1 kinase assay carried out using recombinant CDK1/Cyclin B1 in the absence or presence of purified recombinant His-RGC-32. (B) Quantification of [<sup>32</sup>P]-Histone H1 signals. Results show mean fold increases in CDK1 activity in the presence of RGC-32 +/- standard deviation from 3 independent experiments. (C) Representative cell cycle profile analysis of DG75 FRT control cells and DG75 FRT/FLAG-RGC-32 cells treated for 24 hours with etoposide. Control cells (0) were harvested prior to etoposide treatment. (D) Representative cell cycle profile analysis of BJAB FRT control cells and BJAB FRT/FLAG-RGC-32 cells treated for 48 hours with etoposide. (E) Graph showing the percentage change in the G0/G1 population in BJAB FRT/FLAG-RGC-32 cells compared to control BJAB FRT cells, prior to (0), or following etoposide treatment for 48 hours. Results represent the mean +/− standard deviation of 3 independent experiments.</p>", "links"=>[], "tags"=>["activates", "cdk1", "disrupts", "checkpoint", "B-cell"], "article_id"=>375886, "categories"=>["Virology", "Molecular Biology", "Cancer", "Genetics", "Infectious Diseases"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RGC_32_activates_CDK1_and_disrupts_the_G2_M_checkpoint_in_B_cell_lines_/375886", "title"=>"RGC-32 activates CDK1 and disrupts the G2/M checkpoint in B-cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:38:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/705620"], "description"=>"<p>(A) Diagram showing RGC-32 transcript variants. Black boxes represent exons and dotted lines show the parts of exons 1 and 2 that are not included in the shorter RGC-32 transcript (AF036549) that encodes a protein of 117 amino acids <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028638#pone.0028638-Badea2\" target=\"_blank\">[28]</a>. The longer RGC-32 (C13ORF15) transcript (NM_014059) is predicted to encode a protein of 137 amino acids. (B) Q-PCR analysis using primers in exon 3. Transcript quantities were normalized to those of GAPDH and then expressed relative to the signal obtained in DG75 cells. Results show the mean of 3 independent experiments +/− standard deviation. (C) Non-quantitative PCR analysis of cDNA samples using primers that amplify across exon 2 to exon 4. pFLAG-RGC-32 was used as a positive control (con). Q-PCR analysis using primers that amplify across exons 2 and 3 (D) or exons 4 and 5 (E). Transcript quantities were normalized to GAPDH and results show the mean of 3 independent experiments +/− standard deviation. (F) Northern blot analysis of RGC-32 transcripts. Blots were probed with a [<sup>32</sup>P]-labelled probe generated from the entire RGC-32 cDNA and then stripped and re-probed for GAPDH.</p>", "links"=>[], "tags"=>["mrna", "differentially", "regulated", "types", "ebv"], "article_id"=>375973, "categories"=>["Virology", "Molecular Biology", "Cancer", "Genetics", "Infectious Diseases"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RGC_32_mRNA_expression_is_differentially_regulated_in_different_types_of_EBV_latency_/375973", "title"=>"RGC-32 mRNA expression is differentially regulated in different types of EBV latency.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:39:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/705703"], "description"=>"<p>(A) Q-PCR analysis of RUNX1c mRNA levels. Transcript quantities were normalized to those of GAPDH and then expressed relative to the signal obtained in DG75 cells. Results show the mean of 3 independent experiments +/− standard deviation. (B) Western blot analysis of RUNX1c protein expression in a panel of EBV negative and positive B-cell-lines. Actin levels serve as a loading control. (C) Transient reporter assays in DG75 cells transfected with 4 µg of the RGC-32 promoter-reporter construct (pRGC-32pluc), 2 µg pRL-CMV as a transfection control and increasing amounts (2.5, 5 and 10 µg) of a RUNX1c-expressing plasmid (pBK-CMV-RUNX1c). Firefly luciferase signals were normalized to Renilla luciferase signals. Results show the mean of 3 independent experiments +/− standard deviation. RGC-32 promoter activation is expressed relative to the RUNX1-negative control. ** P value <0.01 (0.004), * p value <0.05 (0.036). (D) IB4 cells were transfected with pCEP4 or pCEP4-RUNX1c plasmids and transfected cells selected in Hygromycin B. 6 days post-transfection samples were analysed for RUNX1c protein expression by western blotting using actin as a loading control and endogenous RGC-32 mRNA expression using Q-PCR. Results show the mean of 2 independent experiments −/+ standard deviation. * P value <0.05 (0.012).</p>", "links"=>[], "tags"=>["transcriptionally", "regulated", "runx1c"], "article_id"=>376058, "categories"=>["Virology", "Molecular Biology", "Cancer", "Genetics", "Infectious Diseases"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RGC_32_is_transcriptionally_regulated_by_RUNX1c_in_B_cells_/376058", "title"=>"RGC-32 is transcriptionally regulated by RUNX1c in B-cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:40:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/705772"], "description"=>"<p>(A) Mutu I, Mutu III and IB4 cells were treated in parallel with 50 or 100 µM MG132 and harvested after 2 or 6 hrs for Western blot analysis. Blots were probed in sections for RGC-32 and actin. IB4 blots were also probed for p53 as a control for MG132-mediated protein stabilization through proteasomal inhibition. (B) Mutu I and III cells were fractionated into cytoplasmic (C) and nuclear (N) protein extracts and analysed by Western blotting for nuclear (Spt16) and cytoplasmic (actin) marker proteins to confirm purity of the fractions. RGC-32 (C) and GAPDH (D) transcript levels were quantified by Q- PCR in cytoplasmic (C) and nuclear (N) RNA extracts prepared in parallel to protein extracts.</p>", "links"=>[], "tags"=>["degradation", "blocked", "mrna", "rgc-32", "latency"], "article_id"=>376132, "categories"=>["Virology", "Molecular Biology", "Cancer", "Genetics", "Infectious Diseases"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proteasomal_degradation_or_blocked_mRNA_export_doesn_t_prevent_RGC_32_protein_expression_in_latency_I_cells_/376132", "title"=>"Proteasomal degradation or blocked mRNA export doesn't prevent RGC-32 protein expression in latency I cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:42:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/705839"], "description"=>"<p>Cell-lines were treated with Actinomycin D and samples analysed at the times indicated. RGC-32 mRNA levels were deteremined by Q-PCR and normalized to those of the stable control message GAPDH. Results are expressed relative to the level detected at time 0 and show the mean +/− standard deviation of 4 independent experiments for Akata (A) or two independent experiments for Mutu I (B) and Mutu III cells (C). The half-life values indicated were calculated using non-linear regression analysis.</p>", "links"=>[], "tags"=>["mrna", "stabilized", "latency"], "article_id"=>376197, "categories"=>["Virology", "Molecular Biology", "Cancer", "Genetics", "Infectious Diseases"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RGC_32_mRNA_is_not_stabilized_in_latency_I_cell_lines_/376197", "title"=>"RGC-32 mRNA is not stabilized in latency I cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:43:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/705916"], "description"=>"<p>Cytoplasmic extracts were sedimented on sucrose density gradients and 0.5 ml or 1 ml fractions collected with continuous monitoring of absorbance at 254 nm (upper panels in A and B). 80S monosome peaks are indicated by arrows. Transcript levels in each fraction were determined using Q-PCR and specific primers to RGC-32 (black bars), GAPDH (open bars) and actin (grey bars). Transcript levels are expressed as a percentage of the total transcript levels detected across the gradient (nt indicates fractions that were not tested). (A) Parallel analysis of Akata (latency I, no RGC-32 protein expression) and LCL#3 (latency III, RGC-32 protein expressed) polysomes. (B) Parallel analysis of Mutu I (latency I, no RGC-32 protein expression) and Mutu III (latency III, RGC-32 protein expressed) polysomes.</p>", "links"=>[], "tags"=>["mrna", "polysomes", "latency", "iii"], "article_id"=>376273, "categories"=>["Virology", "Molecular Biology", "Cancer", "Genetics", "Infectious Diseases"], "users"=>["Sandra N. Schlick", "C. David Wood", "Andrea Gunnell", "Helen M. Webb", "Sarika Khasnis", "Aloys Schepers", "Michelle J. West"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0028638.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RGC_32_mRNA_is_associated_with_polysomes_in_latency_I_and_latency_III_cells_/376273", "title"=>"RGC-32 mRNA is associated with polysomes in latency I and latency III cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-12-06 01:44:33"}

PMC Usage Stats | Further Information

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