Stress-Inducible Caspase Substrate TRB3 Promotes Nuclear Translocation of Procaspase-3
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{"title"=>"Stress-inducible caspase substrate TRB3 promotes nuclear translocation of procaspase-3", "type"=>"journal", "authors"=>[{"first_name"=>"Kouhei", "last_name"=>"Shimizu", "scopus_author_id"=>"36172145100"}, {"first_name"=>"Shoukichi", "last_name"=>"Takahama", "scopus_author_id"=>"39362353300"}, {"first_name"=>"Yaeta", "last_name"=>"Endo", "scopus_author_id"=>"7401811182"}, {"first_name"=>"Tatsuya", "last_name"=>"Sawasaki", "scopus_author_id"=>"7004404369"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pmid"=>"22912727", "pui"=>"365442042", "scopus"=>"2-s2.0-84864999290", "doi"=>"10.1371/journal.pone.0042721", "sgr"=>"84864999290"}, "id"=>"6cb64f1c-2e72-3508-9760-313f0b66dc64", "abstract"=>"Pseudokinase TRB3 is a stress-inducible nuclear protein, which has recently been shown to be involved in ER stress-induced apoptosis. However, it remains unclear how TRB3 contributes to the process. We recently demonstrated that TRB3 was cleaved by caspase-3 (CASP3) in vitro and also in apoptosis-induced cells. Thus, we investigate the role of TRB3 cleavage in the apoptotic process to address the above question. Overexpression studies revealed that the cleavage of TRB3 promoted CASP3/7 activation and apoptosis. In contrast, the anti-apoptotic effects were found under TRB3 non-cleavable conditions, such as ER stress, and also when the CASP3/7 activation was enhanced by knockdown of endogenous TRB3 expression. Interestingly, nuclear translocation of procaspase-3 (proCASP3) was observed in cells either overexpressing TRB3 or under tunicamycin-induced ER stress. Although forced cytoplasmic expression of proCASP3 enhanced apoptosis significantly, its nuclear expression did not produce any pro-apoptotic effect, suggesting that nuclear distribution of proCASP3 is not critical for the execution of apoptosis. Thus, TRB3 might prevent cytoplasmic activation of CASP3 by promoting proCASP3 entry into the nucleus, and thereby inhibit apoptosis. Taken together, our results suggest that TRB3, through its own cleavage, functions as a molecular switch between the cell survival and apoptotic pathways under stressful conditions.", "link"=>"http://www.mendeley.com/research/stressinducible-caspase-substrate-trb3-promotes-nuclear-translocation-procaspase3", "reader_count"=>22, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>1, "Researcher"=>7, "Student > Ph. D. Student"=>5, "Student > Master"=>4, "Other"=>3, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>1, "Researcher"=>7, "Student > Ph. D. Student"=>5, "Student > Master"=>4, "Other"=>3, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>14, "Medicine and Dentistry"=>2, "Chemistry"=>1, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Lebanon"=>1, "Japan"=>2, "Germany"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/313425", "https://ndownloader.figshare.com/files/313444", "https://ndownloader.figshare.com/files/313462", "https://ndownloader.figshare.com/files/313477", "https://ndownloader.figshare.com/files/313489", "https://ndownloader.figshare.com/files/313506", "https://ndownloader.figshare.com/files/313521", "https://ndownloader.figshare.com/files/313531", "https://ndownloader.figshare.com/files/313542", "https://ndownloader.figshare.com/files/313553", "https://ndownloader.figshare.com/files/313570", "https://ndownloader.figshare.com/files/313582", "https://ndownloader.figshare.com/files/313593"], "description"=>"<div><p>Pseudokinase TRB3 is a stress-inducible nuclear protein, which has recently been shown to be involved in ER stress-induced apoptosis. However, it remains unclear how TRB3 contributes to the process. We recently demonstrated that TRB3 was cleaved by caspase-3 (CASP3) <em>in vitro</em> and also in apoptosis-induced cells. Thus, we investigate the role of TRB3 cleavage in the apoptotic process to address the above question. Overexpression studies revealed that the cleavage of TRB3 promoted CASP3/7 activation and apoptosis. In contrast, the anti-apoptotic effects were found under TRB3 non-cleavable conditions, such as ER stress, and also when the CASP3/7 activation was enhanced by knockdown of endogenous TRB3 expression. Interestingly, nuclear translocation of procaspase-3 (proCASP3) was observed in cells either overexpressing TRB3 or under tunicamycin-induced ER stress. Although forced cytoplasmic expression of proCASP3 enhanced apoptosis significantly, its nuclear expression did not produce any pro-apoptotic effect, suggesting that nuclear distribution of proCASP3 is not critical for the execution of apoptosis. Thus, TRB3 might prevent cytoplasmic activation of CASP3 by promoting proCASP3 entry into the nucleus, and thereby inhibit apoptosis. Taken together, our results suggest that TRB3, through its own cleavage, functions as a molecular switch between the cell survival and apoptotic pathways under stressful conditions.</p> </div>", "links"=>[], "tags"=>["stress-inducible", "caspase", "substrate", "trb3", "promotes", "translocation", "procaspase-3"], "article_id"=>121824, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Biological Sciences"], "users"=>["Kouhei Shimizu", "Shoukichi Takahama", "Yaeta Endo", "Tatsuya Sawasaki"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0042721.s001", "https://dx.doi.org/10.1371/journal.pone.0042721.s002", "https://dx.doi.org/10.1371/journal.pone.0042721.s003", "https://dx.doi.org/10.1371/journal.pone.0042721.s004", "https://dx.doi.org/10.1371/journal.pone.0042721.s005", "https://dx.doi.org/10.1371/journal.pone.0042721.s006", "https://dx.doi.org/10.1371/journal.pone.0042721.s007", "https://dx.doi.org/10.1371/journal.pone.0042721.s008", "https://dx.doi.org/10.1371/journal.pone.0042721.s009", "https://dx.doi.org/10.1371/journal.pone.0042721.s010", "https://dx.doi.org/10.1371/journal.pone.0042721.s011", "https://dx.doi.org/10.1371/journal.pone.0042721.s012", "https://dx.doi.org/10.1371/journal.pone.0042721.s013"], "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Stress_Inducible_Caspase_Substrate_TRB3_Promotes_Nuclear_Translocation_of_Procaspase_3/121824", "title"=>"Stress-Inducible Caspase Substrate TRB3 Promotes Nuclear Translocation of Procaspase-3", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-08-09 00:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/594232"], "description"=>"<p>(A–D) HeLa cells were separately transfected with the plasmid expressing EmGFP-tagged wild type proCASP3 (proCASP3-EmGFP), nuclear localization signal (NLS) containing proCASP3-EmGFP (proCASP3-NLS-EmGFP), or DsRed-NLS fusion protein (DsRed-NLS). After 24 hr, transfected cells were trypsinized and plated together in one glass bottom dish. After a further 24 hr, apoptosis was induced by the addition of anti-Fas antibody. Cells expressing the indicated fusion protein are shown (A). Behavior of the EmGFP-fusion protein positive and DsRed positive cells (same field at different times) was recorded by live imaging (B). Representative frames showing images of cells expressing the indicated fusion protein in a given field, as recorded in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042721#pone-0042721-g005\" target=\"_blank\">Figure 5B</a>, are displayed (C). Scale bars = 20 µm (A and C), 50 µm (B). The number of apoptotic cells (based on cell morphology) was counted at 450 min after apoptosis induction by anti-Fas antibody (D). A minimum number of 30 cells were counted in a field for each type of fusion protein expressing cells. Four fields were randomly chosen for counting the number of apoptotic cells. Error bar: mean ±SD. *<i>P</i><0.001.</p>", "links"=>[], "tags"=>["procasp3", "did"], "article_id"=>264722, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Biological Sciences"], "users"=>["Kouhei Shimizu", "Shoukichi Takahama", "Yaeta Endo", "Tatsuya Sawasaki"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0042721.g005", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nuclear_proCASP3_did_not_promote_apoptosis_/264722", "title"=>"Nuclear proCASP3 did not promote apoptosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-09 01:18:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/593816"], "description"=>"<p>(A and B) Twenty-four hours after transfection of HeLa (A) and Jurkat (B) cells with the indicated V5-TRB3 expression plasmid or control (ctrl) vector, the cells were treated with TNFα/CHX for 4 hr (HeLa cells) or anti-Fas antibody for 6 hr (Jurkat cells). The resulting dead cells were counted by trypan blue staining. Error bars indicate mean ±SD of three independent experiments. *<i>P</i><0.05, **<i>P</i><0.005, ***<i>P</i><0.001, statistically significant difference. (C and D) Twenty-four hours after transfection with the indicated V5-TRB3 expression plasmid or control vector, HeLa (C) and Jurkat (D) cells were reseeded in 96-well plates (1.0×10<sup>4</sup> cells/well), and then treated with TNFα/CHX and anti-Fas antibody, respectively, for the indicated times and CASP3/7 activity was then measured using the luminometric Caspase-Glo® 3/7 Assay Kit. Each data point represents mean ±SD of three independent experiments.</p>", "links"=>[], "tags"=>["trb3", "apoptosis", "casp3"], "article_id"=>264313, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Biological Sciences"], "users"=>["Kouhei Shimizu", "Shoukichi Takahama", "Yaeta Endo", "Tatsuya Sawasaki"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0042721.g002", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cleavage_of_TRB3_promotes_apoptosis_along_with_CASP3_activation_/264313", "title"=>"Cleavage of TRB3 promotes apoptosis along with CASP3 activation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-09 01:11:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/593723"], "description"=>"<p>(A) Schematic representation of proteins expressed by the recombinant TRB3 constructs used in this study. WT, wild type TRB3; D338A, CASP3 cleavage-site mutant TRB3; and ΔC20, CASP3-cleaved form of TRB3. (B and C) Each recombinant TRB3 was synthesized and biotinylated using the wheat cell-free expression system as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042721#s4\" target=\"_blank\">Materials and Methods</a>. The translation mixture was incubated with or without the indicated active caspase for 2 hr at 30°C. For the detection of N-terminal biotinylated-TRB3, the blot was probed with Alexa 488-conjugated streptavidin. DA denotes D338A-TRB3. (D) Twenty-four hours after transfection of HeLa and Jurkat cells with the indicated V5-tagged TRB3 expression plasmid, cells were treated with TNFα (20 ng/mL)/CHX (100 µM) (HeLa cells) or anti-Fas antibody (125 ng/mL) (Jurkat cells) in the absence or presence of z-VAD-FMK (100 µM) for 4 hr. DMSO was used as a treatment control. The cell lysates were subjected to immunoblot analysis using anti-V5 antibody to detect the N-terminal V5-tagged TRB3. α-Tubulin was used as an internal control.</p>", "links"=>[], "tags"=>["cleaved", "caspases", "vitro", "apoptotic"], "article_id"=>264217, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Biological Sciences"], "users"=>["Kouhei Shimizu", "Shoukichi Takahama", "Yaeta Endo", "Tatsuya Sawasaki"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0042721.g001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRB3_is_cleaved_by_caspases_in_vitro_and_in_the_apoptotic_process_/264217", "title"=>"TRB3 is cleaved by caspases in vitro and in the apoptotic process.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-09 01:10:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/593956"], "description"=>"<p>(A) HeLa cells were treated with the indicated concentrations of tunicamycin for 8 hr. The effective concentration of tunicamycin needed for inducing TRB3 expression was determined by densitometric image analysis. (B) CASP3/7 activity in HeLa cells was measured as described in the legend of <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042721#pone-0042721-g002\" target=\"_blank\">Figure 2C</a>, except that here apoptosis was induced by incubation with 5 µM tunicamycin for the indicated times. Each data point represents mean ±SD of three independent experiments. (C) Twenty-four hours after transfection with the indicated V5-TRB3 expression plasmid or control vector, HeLa cells were treated with tunicamycin for 48 hr. The resulting dead cells were counted by trypan blue staining. Error bars indicate mean ±SD of four independent experiments. *<i>P</i><0.001. (D) Twenty-four hours after transfection with the given V5-TRB3 expression plasmid, HeLa cells were treated with TNFα/CHX or tunicamycin for the indicated times. The cell lysates were subjected to immunoblot analysis using the anti-V5 antibody. α-Tubulin was used as an internal control. (E) HeLa cells plated in 96-well plates (1.0×10<sup>4</sup> cells/well) were treated with TNFα/CHX or tunicamycin for the indicated times. CASP3/7 activity was measured using the luminometric Caspase-Glo® 3/7 Assay Kit. Each data point represents mean ±SD of three independent experiments. (F-H) HeLa cells were transfected with negative control siRNA (siNC) or TRB3 siRNA (siTRB3). Twenty-four hours after, the cells were treated with tunicamycin for the indicated time points (F). The cell lysates were subjected to immunoblot analysis using the anti-TRB3 antibody (G). Cell lysates were also used for the Caspase-Glo® 3/7 assay to measure the CASP3/7 activity (H). The relative CASP3/7 activity was then determined after normalizing each value with respect to the relative amount of expressed α-Tubulin as estimated by densitometric image analysis. Each data point represents mean ±SD of three independent experiments.</p>", "links"=>[], "tags"=>["inhibits", "casp3", "activation", "apoptosis", "er"], "article_id"=>264444, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Biological Sciences"], "users"=>["Kouhei Shimizu", "Shoukichi Takahama", "Yaeta Endo", "Tatsuya Sawasaki"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0042721.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRB3_inhibits_CASP3_activation_and_subsequent_apoptosis_under_ER_stress_condition_/264444", "title"=>"TRB3 inhibits CASP3 activation and subsequent apoptosis under ER stress condition.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-09 01:14:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/594093"], "description"=>"<p>(A) HeLa cells were cotransfected with the C163S-proCASP3-EmGFP and V5-WT-TRB3 expression plasmids. After 24 hr, the cells were stained with anti-V5 antibody (red) and counterstained with DAPI (blue). Arrow and arrowhead indicated V5-WT-TRB3 positive and negative cells respectively. Scale bars = 10 µm. (B) Twenty-four hours after transfection with the C163S-proCASP3-EmGFP expression plasmid, HeLa cells were incubated with or without tunicamycin for 8 hr. Arrowheads showed representative phenotypes of C163S-proCASP3-EmGFP localization in each condition. Scale bars = 20 µm. (C) Twenty-four hours after transfection with the C163S-proCASP3-EmGFP expression plasmid, HeLa cells were treated with tunicamycin, and localization of C163S-proCASP3-EmGFP was simultaneously monitored for 24 hr by live imaging. Representative frames displaying scenes of nuclear translocation (arrows) are shown. Scale bars = 10 µm. (D) Localization of C163S-proCASP3-EmGFP was quantified as cytoplasmic, mainly cytoplasmic or cytoplasmic equal to nuclear (C, C>N, C = N), or as nuclear or mainly nuclear (N, N>C) under conditions described above (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042721#pone-0042721-g004\" target=\"_blank\">Figure 4A, V</a>5-WT-TRB3; <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0042721#pone-0042721-g004\" target=\"_blank\">Figure 4B</a>, ctrl or Tunicamycin). This localization was also assessed in cells coexpressing V5-WT-TRB3 (right bar graph). Over 30 cells were assessed in three independent experiments. Error bar: mean ±SD. *<i>P</i><0.01, **<i>P</i><0.005. (E) HeLa cells were cotransfected with the C163S-proCASP3-HA and indicated artificial miRNA expression plasmids. After 24 hr, the cells were incubated with tunicamycin for 8 hr. The localization of C163S-proCASP3-HA was observed by immunofluorescence staining with an anti-HA antibody (red). The miRNA expressing cells of inner panel were visualized by cocistronic expression of EmGFP. Arrowheads showed the C163S-proCASP3-HA expressing cells. Scale bars = 20 µm. (F) The cells positive for nuclear C163S-proCASP3-HA (N, N>C, N = C) were quantified by immunofluorescence staining with an anti-HA antibody. Over 30 cells positive for EmGFP were assessed in six independent experiments. Error bar: mean ±SD. *<i>P</i><0.005, **<i>P</i><0.001. miR-NC denotes negative control miRNA.</p>", "links"=>[], "tags"=>["induces", "translocation"], "article_id"=>264589, "categories"=>["Molecular Biology", "Biochemistry", "Cell Biology", "Biological Sciences"], "users"=>["Kouhei Shimizu", "Shoukichi Takahama", "Yaeta Endo", "Tatsuya Sawasaki"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0042721.g004", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRB3_expression_induces_nuclear_translocation_of_proCASP3_/264589", "title"=>"TRB3 expression induces nuclear translocation of proCASP3.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-09 01:16:29"}

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Relative Metric

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