Mitochondrial Calcium Uniporter Activity Is Dispensable for MDA-MB-231 Breast Carcinoma Cell Survival
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{"title"=>"Mitochondrial calcium uniporter activity is dispensable for MDA-MB-231 breast carcinoma cell survival", "type"=>"journal", "authors"=>[{"first_name"=>"Duane D.", "last_name"=>"Hall", "scopus_author_id"=>"7404435084"}, {"first_name"=>"Yuejin", "last_name"=>"Wu", "scopus_author_id"=>"7406894765"}, {"first_name"=>"Frederick E.", "last_name"=>"Domann", "scopus_author_id"=>"7003649146"}, {"first_name"=>"Douglas R.", "last_name"=>"Spitz", "scopus_author_id"=>"7006046019"}, {"first_name"=>"Mark E.", "last_name"=>"Anderson", "scopus_author_id"=>"7404765536"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84900451895", "pmid"=>"24802861", "pui"=>"373074606", "isbn"=>"10.1371/journal.pone.0096866", "scopus"=>"2-s2.0-84900451895", "doi"=>"10.1371/journal.pone.0096866", "issn"=>"19326203"}, "id"=>"02005c2b-0819-3797-8f49-b0b1bc765d60", "abstract"=>"Calcium uptake through the mitochondrial Ca2+ uniporter (MCU) is thought to be essential in regulating cellular signaling events, energy status, and survival. Functional dissection of the uniporter is now possible through the recent identification of the genes encoding for MCU protein complex subunits. Cancer cells exhibit many aspects of mitochondrial dysfunction associated with altered mitochondrial Ca2+ levels including resistance to apoptosis, increased reactive oxygen species production and decreased oxidative metabolism. We used a publically available database to determine that breast cancer patient outcomes negatively correlated with increased MCU Ca2+ conducting pore subunit expression and decreased MICU1 regulatory subunit expression. We hypothesized breast cancer cells may therefore be sensitive to MCU channel manipulation. We used the widely studied MDA-MB-231 breast cancer cell line to investigate whether disruption or increased activation of mitochondrial Ca2+ uptake with specific siRNAs and adenoviral overexpression constructs would sensitize these cells to therapy-related stress. MDA-MB-231 cells were found to contain functional MCU channels that readily respond to cellular stimulation and elicit robust AMPK phosphorylation responses to nutrient withdrawal. Surprisingly, knockdown of MCU or MICU1 did not affect reactive oxygen species production or cause significant effects on clonogenic cell survival of MDA-MB-231 cells exposed to irradiation, chemotherapeutic agents, or nutrient deprivation. Overexpression of wild type or a dominant negative mutant MCU did not affect basal cloning efficiency or ceramide-induced cell killing. In contrast, non-cancerous breast epithelial HMEC cells showed reduced survival after MCU or MICU1 knockdown. These results support the conclusion that MDA-MB-231 breast cancer cells do not rely on MCU or MICU1 activity for survival in contrast to previous findings in cells derived from cervical, colon, and prostate cancers and suggest that not all carcinomas will be sensitive to therapies targeting mitochondrial Ca2+ uptake mechanisms.", "link"=>"http://www.mendeley.com/research/mitochondrial-calcium-uniporter-activity-dispensable-mdamb231-breast-carcinoma-cell-survival-5", "reader_count"=>32, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>12, "Materials Science"=>1, "Agricultural and Biological Sciences"=>11, "Medicine and Dentistry"=>2, "Chemistry"=>1, "Psychology"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>12}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Italy"=>2, "France"=>1}, "group_count"=>6}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1486394", "https://ndownloader.figshare.com/files/1486395"], "description"=>"<div><p>Calcium uptake through the mitochondrial Ca<sup>2+</sup> uniporter (MCU) is thought to be essential in regulating cellular signaling events, energy status, and survival. Functional dissection of the uniporter is now possible through the recent identification of the genes encoding for MCU protein complex subunits. Cancer cells exhibit many aspects of mitochondrial dysfunction associated with altered mitochondrial Ca<sup>2+</sup> levels including resistance to apoptosis, increased reactive oxygen species production and decreased oxidative metabolism. We used a publically available database to determine that breast cancer patient outcomes negatively correlated with increased MCU Ca<sup>2+</sup> conducting pore subunit expression and decreased MICU1 regulatory subunit expression. We hypothesized breast cancer cells may therefore be sensitive to MCU channel manipulation. We used the widely studied MDA-MB-231 breast cancer cell line to investigate whether disruption or increased activation of mitochondrial Ca<sup>2+</sup> uptake with specific siRNAs and adenoviral overexpression constructs would sensitize these cells to therapy-related stress. MDA-MB-231 cells were found to contain functional MCU channels that readily respond to cellular stimulation and elicit robust AMPK phosphorylation responses to nutrient withdrawal. Surprisingly, knockdown of MCU or MICU1 did not affect reactive oxygen species production or cause significant effects on clonogenic cell survival of MDA-MB-231 cells exposed to irradiation, chemotherapeutic agents, or nutrient deprivation. Overexpression of wild type or a dominant negative mutant MCU did not affect basal cloning efficiency or ceramide-induced cell killing. In contrast, non-cancerous breast epithelial HMEC cells showed reduced survival after MCU or MICU1 knockdown. These results support the conclusion that MDA-MB-231 breast cancer cells do not rely on MCU or MICU1 activity for survival in contrast to previous findings in cells derived from cervical, colon, and prostate cancers and suggest that not all carcinomas will be sensitive to therapies targeting mitochondrial Ca<sup>2+</sup> uptake mechanisms.</p></div>", "links"=>[], "tags"=>["Biochemistry", "cell biology", "Signal transduction", "cell signaling", "Calcium signaling", "Molecular cell biology", "genetics", "epigenetics", "RNA interference", "gene expression", "Human genetics", "organisms", "viruses", "DNA viruses", "Clinical genetics", "Mitochondrial diseases", "oncology", "Cancer risk factors", "Genetic causes of cancer", "Cancers and neoplasms", "Breast tumors", "breast cancer", "Basic cancer research", "Cancer treatment", "calcium", "uniporter", "dispensable", "mda-mb-231", "carcinoma"], "article_id"=>1017566, "categories"=>["Biological Sciences"], "users"=>["Duane D. Hall", "Yuejin Wu", "Frederick E. Domann", "Douglas R. Spitz", "Mark E. Anderson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0096866.s001", "https://dx.doi.org/10.1371/journal.pone.0096866.s002"], "stats"=>{"downloads"=>8, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mitochondrial_Calcium_Uniporter_Activity_Is_Dispensable_for_MDA_MB_231_Breast_Carcinoma_Cell_Survival_/1017566", "title"=>"Mitochondrial Calcium Uniporter Activity Is Dispensable for MDA-MB-231 Breast Carcinoma Cell Survival", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-05-06 02:53:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1486391"], "description"=>"<p><b>A.</b> Immunoblots of lysates from cells treated for 1(HBS, Starve). <b>B.</b> Quantification of starvation response as measured by the ratio of phospho-T<sub>172</sub> AMPKα (P-AMPK) to total AMPKα from immunoblots (n = 12–14, t-test). <b>C, D.</b> Similar to <b>A</b> and <b>B</b> but for siRNA transfected cells after 2–4 hrs HBS treatment. Significantly different relationships are indicated (n = 3–9, ANOVA). <b>E.</b> Clonogenic survival assay for siRNA transfected cells harvested and seeded after incubation in HBS as indicated. No significant difference between siRNA groups was found for individual starvation durations (n = 6–9, ANOVA).</p>", "links"=>[], "tags"=>["Biochemistry", "cell biology", "Signal transduction", "cell signaling", "Calcium signaling", "Molecular cell biology", "genetics", "epigenetics", "RNA interference", "gene expression", "Human genetics", "organisms", "viruses", "DNA viruses", "Clinical genetics", "Mitochondrial diseases", "oncology", "Cancer risk factors", "Genetic causes of cancer", "Cancers and neoplasms", "Breast tumors", "breast cancer", "Basic cancer research", "Cancer treatment", "determines", "ampk", "activation", "altering", "starvation-induced", "clonogenic"], "article_id"=>1017563, "categories"=>["Biological Sciences"], "users"=>["Duane D. Hall", "Yuejin Wu", "Frederick E. Domann", "Douglas R. Spitz", "Mark E. Anderson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096866.g004", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MCU_activity_determines_AMPK_activation_without_altering_starvation_induced_clonogenic_cell_killing_/1017563", "title"=>"MCU activity determines AMPK activation without altering starvation-induced clonogenic cell killing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-06 02:53:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1486393"], "description"=>"<p><b>A, B.</b> Adenoviruses engineered to overexpress MCU express full length, mitochondrial localized MCU. <b>A.</b> Immunoblot (IB) of MDA-MB-231 cell lysates infected with MCU-expressing adenoviruses at indicated MOI for total MCU (top) and C-terminal Myc-tag (bottom). Endogenous MCU expression can be seen as a slightly faster migrating band than tagged MCU as detected by the total anti-MCU antibody and present in control infected samples. <b>B.</b> Representative confocal immunofluorescent micorgraphs of cells with and without co-infection of MCU and mt-Pericam viruses. Mitochondrial were labeled with MitoTracker (red), fixed, and immunostained with anti-myc (blue) for overexpressed MCU-myc and anti-GFP (green) for mt-Pericam fluorescence. Colocalization of mitochondria, mt-Pericam, and overexpressed MCU is evidenced by white pixels in the merged panels. Scale bar, 10 µm. <b>C.</b> Representative mt-Pericam signal (485 nm/415 nm excitation ratio) after stimulation with 100 µM ATP as indicated with and without co-infections of MCU expressing viruses. <b>D.</b> Summary data for the integrated area of mt-Pericam responses (n = 30–86). <b>E.</b> Plating efficiency of MDA-MB-231 cells after infection with indicated adenoviruses by clonogenic assay (n = 3–9). <b>F.</b> Results of clonogenic survival assays of adenovirally transduced cells after 24 hour treatment with C2-ceramide (n = 3–9).</p>", "links"=>[], "tags"=>["Biochemistry", "cell biology", "Signal transduction", "cell signaling", "Calcium signaling", "Molecular cell biology", "genetics", "epigenetics", "RNA interference", "gene expression", "Human genetics", "organisms", "viruses", "DNA viruses", "Clinical genetics", "Mitochondrial diseases", "oncology", "Cancer risk factors", "Genetic causes of cancer", "Cancers and neoplasms", "Breast tumors", "breast cancer", "Basic cancer research", "Cancer treatment", "wt", "dn", "mcu", "mda-mb-231"], "article_id"=>1017565, "categories"=>["Biological Sciences"], "users"=>["Duane D. Hall", "Yuejin Wu", "Frederick E. Domann", "Douglas R. Spitz", "Mark E. Anderson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096866.g005", "stats"=>{"downloads"=>3, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_WT_or_DN_MCU_does_not_alter_MDA_MB_231_cell_survival_/1017565", "title"=>"Overexpression of WT or DN MCU does not alter MDA-MB-231 cell survival.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-06 02:53:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1486387"], "description"=>"<p><b>A.</b> MDA-MB-231 mitochondria are capable of taking up Ca<sup>2+</sup> in response extracellular stimulation. An example mt-Pericam recording from an adenovirally transduced cell during cellular stimulation with 100 µM ATP for the indicated duration. Mitochondrial Ca<sup>2+</sup> levels were monitored from the ratio of its dual excitation absorbances (485 nm/415 nm) on emission (535 nm). <b>B, C.</b> Efficient down-regulation of MCU and MICU1 mRNA as determined by qPCR (<b>B</b>) and protein (<b>C</b>) after transient siRNA transfection. NC-si, negative control siRNA. For immunoblots (C), cells were fractionated into cytosolic and mitochondrial fractions prior to SDS-PAGE, as indicated. <b>D.</b> Fraction of mt-Pericam positive cells responding to 100 µM extracellular ATP application is significantly reduced after MCU knockdown (n = 44, p<0.0001. Fisher's exact test) and increased after MICU1 knockdown (n = 63, p<0.01) compared to NC-si (n = 129). <b>E.</b> Average mt-Pericam signals in response to 100 µM ATP as indicated in siRNA transfected cells. Averages are shown as bold lines with SEM as fine lines. <b>F, G.</b> Summary data of mt-Pericam responses calculated for peak amplitude above baseline (F) and area under of the curve (G). Data are mean +/− SEM, t-test.</p>", "links"=>[], "tags"=>["Biochemistry", "cell biology", "Signal transduction", "cell signaling", "Calcium signaling", "Molecular cell biology", "genetics", "epigenetics", "RNA interference", "gene expression", "Human genetics", "organisms", "viruses", "DNA viruses", "Clinical genetics", "Mitochondrial diseases", "oncology", "Cancer risk factors", "Genetic causes of cancer", "Cancers and neoplasms", "Breast tumors", "breast cancer", "Basic cancer research", "Cancer treatment", "mitochondrial", "influx", "abrogated", "enhanced", "mcu", "micu1"], "article_id"=>1017559, "categories"=>["Biological Sciences"], "users"=>["Duane D. Hall", "Yuejin Wu", "Frederick E. Domann", "Douglas R. Spitz", "Mark E. Anderson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096866.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MDA_MB_231_mitochondrial_Ca_2_influx_is_abrogated_and_enhanced_by_MCU_and_MICU1_knockdown_respectively_/1017559", "title"=>"MDA-MB-231 mitochondrial Ca<sup>2+</sup> influx is abrogated and enhanced by MCU and MICU1 knockdown, respectively.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-06 02:53:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1486388"], "description"=>"<p><b>A.</b> Relative basal plating efficiency of MDA-MB-231 cells after siRNA-mediated knockdown normalized to control NC-si. (n = 25–55). <b>B.</b> Mitochondrial superoxide levels determined by FACS analysis after incubating MDA-MB-231 cells with 2 µM MitoSOX. Maximal ROS production was induced by 10 µM antimycin-A. (n = 6–7). <b>C–D.</b> Clonogenic survival assays of knockdown cells normalized to mock irradiated conditions (<b>C</b>) or DMSO vehicle (<b>D</b>). Prior to seeding, cells were irradiated with 2–6 Gy ionizing radiation (C, n = 3) or treatment for 24 hr with paclitaxel (D, n = 3–9). <b>E.</b> Knockdown efficiency of MCU and MICU1 by siRNAs in HeLa and primary HMEC cultures determined by qPCR. <b>F.</b> Clonogenic survival assays of siRNA transfected HeLa, HMEC, and MDA-MB-231 (MB-231) cells after 24 hr C2-ceramide treatment. The three bars grouped for each siRNA represent 0, 20, and 50 µM ceramide incubation, respectively (n = 3–9). The surviving fraction was determined by normalizing the number of colonies to NC-si control conditions. <b>G.</b> Proliferation rate of HeLa and MDA-MB-231 (MB-231) cells after siRNA knockdown. Data are given as means +/− SEM and significance determined by one-way (A, E, G) or two-way (B–D, F) ANOVA.</p>", "links"=>[], "tags"=>["Biochemistry", "cell biology", "Signal transduction", "cell signaling", "Calcium signaling", "Molecular cell biology", "genetics", "epigenetics", "RNA interference", "gene expression", "Human genetics", "organisms", "viruses", "DNA viruses", "Clinical genetics", "Mitochondrial diseases", "oncology", "Cancer risk factors", "Genetic causes of cancer", "Cancers and neoplasms", "Breast tumors", "breast cancer", "Basic cancer research", "Cancer treatment", "ros", "therapy-related", "treatments", "mediated", "mcu"], "article_id"=>1017560, "categories"=>["Biological Sciences"], "users"=>["Duane D. Hall", "Yuejin Wu", "Frederick E. Domann", "Douglas R. Spitz", "Mark E. Anderson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096866.g003", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MDA_MB_231_ROS_levels_and_sensitivity_to_therapy_related_treatments_are_not_mediated_by_MCU_activity_/1017560", "title"=>"MDA-MB-231 ROS levels and sensitivity to therapy-related treatments are not mediated by MCU activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-06 02:53:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/1486386"], "description"=>"<p>Hazard ratios of queried gene expression combinations from the BreastMark mRNA survival analysis online algorithm. Patient survival was correlated to sample gene expression after genes were queried alone or in combination for overexpression (<b><i>bold</i></b>) and inverse underexpression (<i>not bold<sub>i</sub></i>) and represented as hazard ratios. See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0096866#pone.0096866.s001\" target=\"_blank\">Table S1</a> for more details including sample number, p-values, and queries for expression relationships for other uniporter subunit genes.</p>", "links"=>[], "tags"=>["Biochemistry", "cell biology", "Signal transduction", "cell signaling", "Calcium signaling", "Molecular cell biology", "genetics", "epigenetics", "RNA interference", "gene expression", "Human genetics", "organisms", "viruses", "DNA viruses", "Clinical genetics", "Mitochondrial diseases", "oncology", "Cancer risk factors", "Genetic causes of cancer", "Cancers and neoplasms", "Breast tumors", "breast cancer", "Basic cancer research", "Cancer treatment", "mitochondrial", "uniporter", "subunits", "cancer"], "article_id"=>1017558, "categories"=>["Biological Sciences"], "users"=>["Duane D. Hall", "Yuejin Wu", "Frederick E. Domann", "Douglas R. Spitz", "Mark E. Anderson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096866.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_mitochondrial_Ca_2_uniporter_subunits_is_associated_with_breast_cancer_patient_survival_/1017558", "title"=>"Expression of mitochondrial Ca<sup>2+</sup> uniporter subunits is associated with breast cancer patient survival.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-06 02:53:32"}

PMC Usage Stats | Further Information

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Relative Metric

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