Acetylation of the Proto-Oncogene EVI1 Abrogates Bcl-xL Promoter Binding and Induces Apoptosis
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{"title"=>"Acetylation of the Proto-Oncogene EVI1 abrogates BcL-xL promoter binding and induces apoptosis", "type"=>"journal", "authors"=>[{"first_name"=>"Anjan Kumar", "last_name"=>"Pradhan", "scopus_author_id"=>"49461610100"}, {"first_name"=>"Aloks Das", "last_name"=>"Mohapatra", "scopus_author_id"=>"35120664000"}, {"first_name"=>"Kasturi Bala", "last_name"=>"Nayak", "scopus_author_id"=>"53868303900"}, {"first_name"=>"Soumen", "last_name"=>"Chakraborty", "scopus_author_id"=>"35551948600"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"362648512", "sgr"=>"80053252121", "issn"=>"19326203", "pmid"=>"21980434", "scopus"=>"2-s2.0-80053252121", "doi"=>"10.1371/journal.pone.0025370", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"966890df-ee3e-3b11-b4a7-e6e7d513b9a3", "abstract"=>"EVI1 (Ecotropic Viral Integration site I), which was originally identified as a myeloid transforming gene by means of retroviral insertional mutagenesis in mouse leukemia, encodes a nuclear DNA binding zinc finger protein. The presence of zinc fingers that are able to bind to specific sequences of DNA suggests that EVI1 is a transcriptional regulator; however, except a few, target genes of EVI1 are poorly functionally identified thus far. In this study we provide evidence that EVI1 directly induces the expression of Bcl-xL through the first set of zinc finger and thereby inhibits apoptosis. ChIP analysis showed that EVI1 binds to the Bcl-xL promoter in HT-29 cells, a colon carcinoma cell line, which expresses EVI1. The observation is also supported by the fact that EVI1 siRNA treated HT-29 cells, shows a down regulation of Bcl-xL expression and that over expression of EVI1 results in the induction of the Bcl-xL reporter construct. A set of EVI1 positive chronic myeloid leukemia (CML) samples also showed higher Bcl-xL expression with respect to EVI1 negative samples. Interestingly, co-expression of EVI1 with wild type, but not with dominant-negative form of PCAF, abolishes the effect of EVI1 on Bcl-xL, indicating that acetylation of EVI1 abrogates its ability not only to bind Bcl-xL promoter but also alleviate Bcl-xL activity. Finally we have shown that EVI1 expression regulates apoptosis in HT-29 cells, which is abrogated when HT-29 cells are transfected with EVI1 siRNA or PCAF. The result for the first time shows a direct pathway by which EVI1 can protect cells from apoptosis and also demonstrates that the pathway can be reversed when EVI1 is acetylated.", "link"=>"http://www.mendeley.com/research/acetylation-protooncogene-evi1-abrogates-bclxl-promoter-binding-induces-apoptosis", "reader_count"=>18, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>3, "Lecturer"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>3, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>3, "Lecturer"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>10, "Medicine and Dentistry"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>10}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}}, "reader_count_by_country"=>{"Greece"=>1, "United Kingdom"=>1, "France"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/731071"], "description"=>"<p>A. HT-29 cells were transfected and treated as above (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025370#pone-0025370-g004\" target=\"_blank\">Figure 4</a>). After thirty six hours of transfection, cells were stained with TUNEL reagent (BD biosciences, USA) as per the instruction of the manufacturer. The approximate percentages of cells that are positive for TUNEL are 41, 55, 58 and 28 for HT-29 cells, EVI1 specific siRNA transfected HT-29 cells, PCAF-wt or PCAF-DN transfected HT-29 cells respectively (p value = 0.0036). B. A part of the same transfected cells that were used for apoptosis assay was checked for the BCL-XL mRNA level through real time PCR. As shown Bcl-xL mRNA level was higher in HT-29 cells however it was reduced when EVI1 siRNA or PCAF was transfected in the HT-29 cells. Expression of PCAF-DN again increased the Bcl-xL mRNA level (p value = 0.0016). C. Another part of the same transfected cells that were used for apoptosis assay was checked for the BCL-XL protein expression with Bcl-xL antibody (Imgenex India Pvt. Ltd.) and beta-actin antibody (Santa Cruz) through western blotting. As shown BCL-XL expression was higher in HT-29 cells however BCL-XL expression was reduced when EVI1 siRNA or PCAF was transfected in the HT-29 cells. Expression of PCAF-DN again increased the BCL-XL expression. D. The same western blotting data was quantified by Bio-rad gel doc volume analysis method. Figure shows a quantification of Bcl-xL with respect to the beta actin (p value = 0.0039).</p>", "links"=>[], "tags"=>["evi1", "induces", "apoptosis", "ht-29", "cells"], "article_id"=>401424, "categories"=>["Hematology", "Biochemistry", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anjan Kumar Pradhan", "Alok Das Mohapatra", "Kasturi Bala Nayak", "Soumen Chakraborty"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025370.g005", "stats"=>{"downloads"=>1, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Acetylation_of_EVI1_induces_apoptosis_in_HT_29_cells_TUNEL_assay_/401424", "title"=>"Acetylation of EVI1 induces apoptosis in HT-29 cells (TUNEL assay).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:22:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/730830"], "description"=>"<p>A. Nuclear extracts from EVI1-wt or EVI1-wt+PCAF-wt or EVI1-wt+PCAF-DN transfected cells were incubated with a radiolabelled, double-stranded oligo containing the wild type Bcl-xL EVI1 site and analyzed by EMSA. EVI1 binds to Bcl-xL <i>in vitro</i> (as shown earlier) (lane 1). However, acetylated EVI1 (EVI1+PCAF-wt) failed to bind the Bcl-xL probe (lane 2). The binding was observed again when EVI1 was transfected along with PCAF-DN (lane 3). B. The same nuclear extract was electrophoresed on a SDS-PAGE and transferred to a PVDF membrane which was subsequently probed with the anti acetylated lysine antibody (Cell Signaling Technology, USA). Acetylated band of EVI1 was observed only when EVI1 was transfected along with PCAF (upper panel, lane 3) whereas no acetylated band was observed when EVI1 was transfected alone (upper panel, lane 2) or with PCAF-DN (upper panel, lane 4). The same blot was stripped and reprobed with the anti-flag antibody (Sigma). Expression of EVI1, PCAF and PCAF-DN was observed as shown on the figure (lower panel). Lane 1 showed the only empty vector transfected nuclear extract. C. 293T cells were transfected with constructs as mentioned in the figure along with the promoter construct and renilla luciferase (as an internal control). Twenty four hours later the cells were lysed and luciferase activity was measured using the luminometer. Up regulation of Bcl-xL was blocked when cells were transfected with both EVI1 and PCAF-wt; however the block was released when cells were transfected with EVI1-wt and PCAF-DN. Only PCAF-wt and PCAF-DN showed no effect on the promoter activity. The respective fold change with respect to vector for EVI1-wt, Vector with PCAF siRNA, EVI1 with PCAF siRNA, EVI1-wt with PCAF-wt, EVI1-wt with PCAF-DN, PCAF-wt and PCAF-DN are 2.72, 1.18, 4.14, 1.052, 2.89, 1.20 and 1.046 (p value<0.0001). D. 293T cells were transfected with vector and EVI1 with increasing concentrations of PCAF (1 µg to 5 µg) with the promoter construct and renilla luciferase. Luciferase assay was done as described above. Up regulation of Bcl-xL was blocked by PCAF in a dose dependent manner (p value<0.0001).</p>", "links"=>[], "tags"=>["evi1", "deregulates", "bcl-xl", "binding"], "article_id"=>401188, "categories"=>["Hematology", "Biochemistry", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anjan Kumar Pradhan", "Alok Das Mohapatra", "Kasturi Bala Nayak", "Soumen Chakraborty"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025370.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Acetylated_EVI1_deregulates_Bcl_xL_binding_and_transactivation_/401188", "title"=>"Acetylated EVI1 deregulates Bcl-xL binding and transactivation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:21:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/730956"], "description"=>"<p>A. HT-29 cells transfected with EVI1 specific siRNA or PCAF-wt or PCAF-DN were cultured for twenty four hours and then 1 µM of plumbagin (Sigma) was added for another twelve hours. After thirty six hours of transfection, surface exposure of phosphatidyl serine in the apoptotic cells was measured by Annexin-V-PE and 7-AAD, by using the Annexin-V-PE apoptosis detection kit (BD biosciences, USA) as per the instruction of the manufacturer. Apoptotic cells are Annexin-V positive and 7 AAD negative but dead cells are positive for both. The percentages of cells that are positive for Annexin-V are 15.2, 46.68, 34.72 and 22.28 for HT-29 cells, EVI1 specific siRNA transfected HT-29 cells, PCAF-wt or PCAF-DN transfected HT-29 cells respectively. B. A part of the same transfected cells that were used for apoptosis assay was checked for the BCL-XL protein expression with Bcl-xL antibody (Imgenex India Pvt. Ltd.) through fluorescence intensity by FACS. As shown BCL-XL expression was higher in HT-29 cells however BCL-XL expression was reduced when EVI1 siRNA or PCAF was transfected in the HT-29 cells. Expression of PCAF-DN again increased the BCL-XL expression (p value<0.0001).</p>", "links"=>[], "tags"=>["evi1", "induces", "apoptosis", "ht-29", "cells"], "article_id"=>401306, "categories"=>["Hematology", "Biochemistry", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anjan Kumar Pradhan", "Alok Das Mohapatra", "Kasturi Bala Nayak", "Soumen Chakraborty"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025370.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Acetylation_of_EVI1_induces_apoptosis_in_HT_29_cells_Annexin_V_binding_assay_/401306", "title"=>"Acetylation of EVI1 induces apoptosis in HT-29 cells (Annexin-V-binding assay).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:21:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/730749"], "description"=>"<p>A. HT-29 cell line was transfected with EVI1 siRNA and its negative control. After 24 h of transfection total RNA was isolated by TRIzol reagent (Invitrogen). Complementary DNA (cDNA) was prepared using oligodT (Fermentas, Germany) and subsequently RQ-PCR was performed with primers Bcl-xL-F-GCCACTTACCTGAATGACCAC, Bcl-xL-R-TGGATGGTCAGTGTCTGGT with SYBR green gold real time master mix (Eurogentec, Belgium). β-actin primers were used on the same sample for normalization. Bcl-xL level went down by 5.02 fold for siRNA transfected cells as compared to normal cells (p value = 0.0141). The left panel showed the expression of EVI1 protein level. siRNA negative control neither showed any change in Bcl-xL mRNA level nor in EVI1 protein level as compared to only HT-29 cells. B. Bcl-xL mRNA was up regulated in EVI1 transfected cells. 293T cells transfected with only empty vector or EVI1 were processed as described above. The EVI1-positive cells showed 5.07 fold more Bcl-xL expression in comparison to normalized vector control (p value = 0.047). C. Total protein was isolated from 293T cells transfected with only vector or with EVI1 and checked for BCL-XL protein level by standard Western blotting by using anti-Bcl-xL antibody (Imgenex India Pvt. Ltd). D. EVI1 positive (n = 13) and negative cases (n = 10) of CML patients were checked for Bcl-xL mRNA by RQ-PCR as described above. The EVI1 positive cases showed an up regulation of Bcl-xL compared to EVI1 negative cases. (P value = 0.0001). E. 293T cell line was transfected with either empty vector or EVI1 along with the pGL2-Bcl-xL promoter or pGL2 Bcl-xL (mut) and renilla luciferase (internal control). Twenty four hours later the cells were lysed and luciferase activity was measured using the luminometer (GLOMAX 20/20, Promega). EVI1 up regulated the Bcl-xL promoter activity by 5.81 fold and not the mutated promoter. Also EVI1-ΔD up regulated the wild type promoter by 5.68 fold and not EVI1-ΔA. The results were expressed as mean ± s.e. of triplicate experiments, which are representative of three different assays (p value<0.0001). F. NIH3T3 cell line was transfected with either empty vector or EVI1 along with the pGL2-Bcl-xL promoter and renilla luciferase (internal control). Luciferase activity was measured as described above. EVI1 up regulated the Bcl-xL promoter activity by 3.6 fold in NIH3T3 cells (p value = 0.0066).</p>", "links"=>[], "tags"=>["induces", "bcl-xl", "promoter"], "article_id"=>401106, "categories"=>["Hematology", "Biochemistry", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anjan Kumar Pradhan", "Alok Das Mohapatra", "Kasturi Bala Nayak", "Soumen Chakraborty"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025370.g002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_EVI1_induces_Bcl_xL_promoter_trans_activity_/401106", "title"=>"EVI1 induces Bcl-xL promoter trans-activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:20:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/730632"], "description"=>"<p>A. A multiple sequence alignment of parts of Bcl-xL 2<sup>nd</sup> exon from different species are shown and the binding site is underlined. Genbank accession numbers of each of Bcl-xL sequence from different species that were used in the alignment analysis are as follows, <i>Canis familiaris</i>: NM_001003072.1, <i>Homo sapiens</i>: NM_138578.1, <i>Rattus rattus</i>: NM_001033670.1, <i>Gallus gallus</i>: NM_001025304.1, <i>Danio rerio</i>: NM_131807.1, <i>Felis catus</i>: NM_001009228.1, <i>Bos taurus</i>: NM_001077486.2 and <i>Mus musculus</i>: NM_009743.4. B. Nuclear extracts from EVI1 transfected 293T cells were incubated with a radiolabelled, double-stranded oligo designed from the EVI1 binding site in Bcl-xL promoter. EVI1 binds to Bcl-xL (lane 1) as shown by an arrow whereas a mutated probe failed to show any binding (lane 2). Lane 3 shows only the empty vector transfected cells and lane 6 shows the probe without any nuclear lysate. Increasing amount of specific cold competitor at 30× molar excess of radiolabelled probe (lane 4) failed to inhibit the binding of EVI1 to Bcl-xL promoter however a cold competitor at 50× molar excess of radiolabelled probe (lane 5) inhibited binding of EVI1 to Bcl-xL promoter. C. ChIP analysis shows the occupancy of EVI1 on the Bcl-xL promoter <i>in vivo</i>. After cross linking and chromatin fractionations DNA protein complexes were incubated with EVI1 antibody and the complex were processed as per the manufacturer's instructions (Imgenex India Pvt. Ltd.). Eluted DNA samples were then analyzed by PCR using specific primers flanking the EVI1 binding region. A band of 170 bp was observed only in HT-29 cells (lane 3) and no band was observed with IgG (lane 2) or with primers taken from the upstream region (lane 6). Marker (M) and the input controls for both regions are as shown (lane 1 and lane 4). D. ChIP was performed on 293T cells transfected with empty vector or EVI1 construct. For this assay flag-CMV-vector, flag-EVI1 wild type (Wt), flag- EVI1-ΔA (EVI1-Δ24 to 239) and flag-EVI1-ΔD (EVI1-Δ735 to 812) constructs were transfected separately in 293T cells. After processing as described above PCR showed an amplification of 170 bp when cells were transfected with EVI1 and EVI1-ΔD where as no amplification was observed in vector transfected cells or EVI1-ΔA transfected cells. Marker and the input control are as shown.</p>", "links"=>[], "tags"=>["binds", "bcl-xl", "promoter"], "article_id"=>400983, "categories"=>["Hematology", "Biochemistry", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Anjan Kumar Pradhan", "Alok Das Mohapatra", "Kasturi Bala Nayak", "Soumen Chakraborty"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025370.g001", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_EVI1_binds_to_Bcl_xL_promoter_element_/400983", "title"=>"EVI1 binds to Bcl-xL promoter element.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 14:20:10"}

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