SIRT6 Suppresses Cancer Stem-like Capacity in Tumors with PI3K Activation Independently of Its Deacetylase Activity
Cancer stem cells (CSCs) have high tumorigenic capacity. Here, we show that stem-like traits of specific human cancer cells are reduced by overexpression of the histone deacetylase sirtuin 6 (SIRT6). SIRT6-sensitive cancer cells bear mutations that activate phosphatidylinositol-3-kinase (PI3K) signa...
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| Vydáno v: | Cell reports (Cambridge) Ročník 18; číslo 8; s. 1858 - 1868 |
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| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
Elsevier Inc
21.02.2017
Cell Press Elsevier |
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| ISSN: | 2211-1247, 2211-1247 |
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| Abstract | Cancer stem cells (CSCs) have high tumorigenic capacity. Here, we show that stem-like traits of specific human cancer cells are reduced by overexpression of the histone deacetylase sirtuin 6 (SIRT6). SIRT6-sensitive cancer cells bear mutations that activate phosphatidylinositol-3-kinase (PI3K) signaling, and overexpression of SIRT6 reduces growth, progression, and grade of breast cancer in a mouse model with PI3K activation. Tumor metabolomic and transcriptomic analyses reveal that SIRT6 overexpression dampens PI3K signaling and stem-like characteristics and causes metabolic rearrangements in this cancer model. Ablation of a PI3K activating mutation in otherwise isogenic cancer cells is sufficient to convert SIRT6-sensitive into SIRT6-insensitive cells. SIRT6 overexpression suppresses PI3K signaling at the transcriptional level and antagonizes tumor sphere formation independent of its histone deacetylase activity. Our data identify SIRT6 as a putative molecular target that hinders stemness of tumors with PI3K activation.
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•Enhanced SIRT6 hinders stemness of human cancer cells with PI3K activation•Enhanced SIRT6 rearranges metabolism of cancer cells with PI3K activation•Enhanced SIRT6 reduces grade and progression of murine tumors with PI3K activation•Anti-cancer-stemness action is independent of SIRT6 histone deacetylase activity
Ioris et al. provide in vitro and in vivo evidence that enhanced SIRT6 suppresses cancer progression and stemness in the context of constitutively active PI3K signaling. This effect is, at least in part, through suppression of the PI3K pathway at the transcriptional level and independent of SIRT6’s histone deacetylase activity. |
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| AbstractList | Cancer stem cells (CSCs) have high tumorigenic capacity. Here, we show that stem-like traits of specific human cancer cells are reduced by overexpression of the histone deacetylase sirtuin 6 (SIRT6). SIRT6-sensitive cancer cells bear mutations that activate phosphatidylinositol-3-kinase (PI3K) signaling, and overexpression of SIRT6 reduces growth, progression, and grade of breast cancer in a mouse model with PI3K activation. Tumor metabolomic and transcriptomic analyses reveal that SIRT6 overexpression dampens PI3K signaling and stem-like characteristics and causes metabolic rearrangements in this cancer model. Ablation of a PI3K activating mutation in otherwise isogenic cancer cells is sufficient to convert SIRT6-sensitive into SIRT6-insensitive cells. SIRT6 overexpression suppresses PI3K signaling at the transcriptional level and antagonizes tumor sphere formation independent of its histone deacetylase activity. Our data identify SIRT6 as a putative molecular target that hinders stemness of tumors with PI3K activation.
•
Enhanced SIRT6 hinders stemness of human cancer cells with PI3K activation
•
Enhanced SIRT6 rearranges metabolism of cancer cells with PI3K activation
•
Enhanced SIRT6 reduces grade and progression of murine tumors with PI3K activation
•
Anti-cancer-stemness action is independent of SIRT6 histone deacetylase activity
Ioris et al. provide in vitro and in vivo evidence that enhanced SIRT6 suppresses cancer progression and stemness in the context of constitutively active PI3K signaling. This effect is, at least in part, through suppression of the PI3K pathway at the transcriptional level and independent of SIRT6’s histone deacetylase activity. Cancer stem cells (CSCs) have high tumorigenic capacity. Here, we show that stem-like traits of specific human cancer cells are reduced by overexpression of the histone deacetylase sirtuin 6 (SIRT6). SIRT6-sensitive cancer cells bear mutations that activate phosphatidylinositol-3-kinase (PI3K) signaling, and overexpression of SIRT6 reduces growth, progression, and grade of breast cancer in a mouse model with PI3K activation. Tumor metabolomic and transcriptomic analyses reveal that SIRT6 overexpression dampens PI3K signaling and stem-like characteristics and causes metabolic rearrangements in this cancer model. Ablation of a PI3K activating mutation in otherwise isogenic cancer cells is sufficient to convert SIRT6-sensitive into SIRT6-insensitive cells. SIRT6 overexpression suppresses PI3K signaling at the transcriptional level and antagonizes tumor sphere formation independent of its histone deacetylase activity. Our data identify SIRT6 as a putative molecular target that hinders stemness of tumors with PI3K activation. Cancer stem cells (CSCs) have high tumorigenic capacity. Here, we show that stem-like traits of specific human cancer cells are reduced by overexpression of the histone deacetylase sirtuin 6 (SIRT6). SIRT6-sensitive cancer cells bear mutations that activate phosphatidylinositol-3-kinase (PI3K) signaling, and overexpression of SIRT6 reduces growth, progression, and grade of breast cancer in a mouse model with PI3K activation. Tumor metabolomic and transcriptomic analyses reveal that SIRT6 overexpression dampens PI3K signaling and stem-like characteristics and causes metabolic rearrangements in this cancer model. Ablation of a PI3K activating mutation in otherwise isogenic cancer cells is sufficient to convert SIRT6-sensitive into SIRT6-insensitive cells. SIRT6 overexpression suppresses PI3K signaling at the transcriptional level and antagonizes tumor sphere formation independent of its histone deacetylase activity. Our data identify SIRT6 as a putative molecular target that hinders stemness of tumors with PI3K activation.Cancer stem cells (CSCs) have high tumorigenic capacity. Here, we show that stem-like traits of specific human cancer cells are reduced by overexpression of the histone deacetylase sirtuin 6 (SIRT6). SIRT6-sensitive cancer cells bear mutations that activate phosphatidylinositol-3-kinase (PI3K) signaling, and overexpression of SIRT6 reduces growth, progression, and grade of breast cancer in a mouse model with PI3K activation. Tumor metabolomic and transcriptomic analyses reveal that SIRT6 overexpression dampens PI3K signaling and stem-like characteristics and causes metabolic rearrangements in this cancer model. Ablation of a PI3K activating mutation in otherwise isogenic cancer cells is sufficient to convert SIRT6-sensitive into SIRT6-insensitive cells. SIRT6 overexpression suppresses PI3K signaling at the transcriptional level and antagonizes tumor sphere formation independent of its histone deacetylase activity. Our data identify SIRT6 as a putative molecular target that hinders stemness of tumors with PI3K activation. Cancer stem cells (CSCs) have high tumorigenic capacity. Here, we show that stem-like traits of specific human cancer cells are reduced by overexpression of the histone deacetylase sirtuin 6 (SIRT6). SIRT6-sensitive cancer cells bear mutations that activate phosphatidylinositol-3-kinase (PI3K) signaling, and overexpression of SIRT6 reduces growth, progression, and grade of breast cancer in a mouse model with PI3K activation. Tumor metabolomic and transcriptomic analyses reveal that SIRT6 overexpression dampens PI3K signaling and stem-like characteristics and causes metabolic rearrangements in this cancer model. Ablation of a PI3K activating mutation in otherwise isogenic cancer cells is sufficient to convert SIRT6-sensitive into SIRT6-insensitive cells. SIRT6 overexpression suppresses PI3K signaling at the transcriptional level and antagonizes tumor sphere formation independent of its histone deacetylase activity. Our data identify SIRT6 as a putative molecular target that hinders stemness of tumors with PI3K activation. [Display omitted] •Enhanced SIRT6 hinders stemness of human cancer cells with PI3K activation•Enhanced SIRT6 rearranges metabolism of cancer cells with PI3K activation•Enhanced SIRT6 reduces grade and progression of murine tumors with PI3K activation•Anti-cancer-stemness action is independent of SIRT6 histone deacetylase activity Ioris et al. provide in vitro and in vivo evidence that enhanced SIRT6 suppresses cancer progression and stemness in the context of constitutively active PI3K signaling. This effect is, at least in part, through suppression of the PI3K pathway at the transcriptional level and independent of SIRT6’s histone deacetylase activity. |
| Author | Mostoslavsky, Raul Ioris, Rafael M. Aras, Ebru Martinvalet, Denis Brenachot, Xavier Anderson, Jason G. Sebastián, Carlos Baldi, Pierre Coppari, Roberto Charollais, Anne Ceglia, Nicholas Galié, Mirco Ramadori, Giorgio Konstantinidou, Georgia Goga, Algera |
| AuthorAffiliation | 8 The Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA 4 Department of Internal Medicine, Division of Hypothalamic Research, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA 7 Institute for Genomics and Bioinformatics, University of California Irvine, Irvine, CA 92697, USA 9 The MGH Center for Regenerative Medicine, Harvard Medical School, Boston, MA 02114, USA 10 The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA 3 Department of Neurosciences, Biomedicine and Movement, University of Verona, Verona 37134, Italy 1 Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland 2 Diabetes Center of the Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland 5 Institute of Pharmacology, University of Bern, 3010 Bern, Switzerland 6 Department of Computer Science University of California Irvine, Irvine, CA 92697, USA |
| AuthorAffiliation_xml | – name: 3 Department of Neurosciences, Biomedicine and Movement, University of Verona, Verona 37134, Italy – name: 6 Department of Computer Science University of California Irvine, Irvine, CA 92697, USA – name: 9 The MGH Center for Regenerative Medicine, Harvard Medical School, Boston, MA 02114, USA – name: 4 Department of Internal Medicine, Division of Hypothalamic Research, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA – name: 8 The Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA – name: 10 The Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA – name: 5 Institute of Pharmacology, University of Bern, 3010 Bern, Switzerland – name: 2 Diabetes Center of the Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – name: 1 Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – name: 7 Institute for Genomics and Bioinformatics, University of California Irvine, Irvine, CA 92697, USA |
| Author_xml | – sequence: 1 givenname: Rafael M. surname: Ioris fullname: Ioris, Rafael M. organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 2 givenname: Mirco surname: Galié fullname: Galié, Mirco organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 3 givenname: Giorgio surname: Ramadori fullname: Ramadori, Giorgio organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 4 givenname: Jason G. surname: Anderson fullname: Anderson, Jason G. organization: Department of Internal Medicine, Division of Hypothalamic Research, The University of Texas Southwestern Medical Center, Dallas, TX 75390, USA – sequence: 5 givenname: Anne surname: Charollais fullname: Charollais, Anne organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 6 givenname: Georgia surname: Konstantinidou fullname: Konstantinidou, Georgia organization: Institute of Pharmacology, University of Bern, 3010 Bern, Switzerland – sequence: 7 givenname: Xavier surname: Brenachot fullname: Brenachot, Xavier organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 8 givenname: Ebru surname: Aras fullname: Aras, Ebru organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 9 givenname: Algera surname: Goga fullname: Goga, Algera organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 10 givenname: Nicholas surname: Ceglia fullname: Ceglia, Nicholas organization: Department of Computer Science University of California Irvine, Irvine, CA 92697, USA – sequence: 11 givenname: Carlos surname: Sebastián fullname: Sebastián, Carlos organization: The Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA – sequence: 12 givenname: Denis surname: Martinvalet fullname: Martinvalet, Denis organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland – sequence: 13 givenname: Raul surname: Mostoslavsky fullname: Mostoslavsky, Raul organization: The Massachusetts General Hospital Cancer Center, Harvard Medical School, Boston, MA 02114, USA – sequence: 14 givenname: Pierre surname: Baldi fullname: Baldi, Pierre organization: Department of Computer Science University of California Irvine, Irvine, CA 92697, USA – sequence: 15 givenname: Roberto surname: Coppari fullname: Coppari, Roberto email: roberto.coppari@unige.ch organization: Department of Cell Physiology and Metabolism, Faculty of Medicine, University of Geneva, 1211 Geneva 4, Switzerland |
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| Keywords | PI3K SIRT6 cancer stemness |
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| SubjectTerms | Acetylation Animals cancer stemness Carcinogenesis - metabolism Cell Line, Tumor Cell Proliferation - physiology Humans Mice Mice, Inbred NOD Mice, SCID Mutation - physiology Neoplasms - metabolism Neoplastic Stem Cells - metabolism Phosphatidylinositol 3-Kinases - metabolism PI3K Signal Transduction - physiology SIRT6 Sirtuins - metabolism Transcription, Genetic - physiology |
| Title | SIRT6 Suppresses Cancer Stem-like Capacity in Tumors with PI3K Activation Independently of Its Deacetylase Activity |
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