The critical role of AMPK in driving Akt activation under stress, tumorigenesis and drug resistance
PI3K/Akt signaling is activated in cancers and governs tumor initiation and progression, but how Akt is activated under diverse stresses is poorly understood. Here we identify AMPK as an essential regulator for Akt activation by various stresses. Surprisingly, AMPK is also activated by growth factor...
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Published in | Nature communications Vol. 9; no. 1; pp. 4728 - 16 |
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Main Authors | , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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London
Nature Publishing Group UK
09.11.2018
Nature Publishing Group Nature Portfolio |
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Abstract | PI3K/Akt signaling is activated in cancers and governs tumor initiation and progression, but how Akt is activated under diverse stresses is poorly understood. Here we identify AMPK as an essential regulator for Akt activation by various stresses. Surprisingly, AMPK is also activated by growth factor EGF through Ca2+/Calmodulin-dependent kinase and is essential for EGF-mediated Akt activation and biological functions. AMPK phosphorylates Skp2 at S256 and promotes the integrity and E3 ligase activity of Skp2 SCF complex leading to K63-linked ubiquitination and activation of Akt and subsequent oncogenic processes. Importantly, AMPK-mediated Skp2 S256 phosphorylation promotes breast cancer progression in mouse tumor models, correlates with Akt and AMPK activation in breast cancer patients, and predicts poor survival outcomes. Finally, targeting AMPK-mediated Skp2 S256 phosphorylation sensitizes cells to anti-EGF receptor targeted therapy. Our study sheds light on how stress and EGF induce Akt activation and new mechanisms for AMPK-mediated oncogenesis and drug resistance.
How Akt pathway is activated under stress is poorly understood. Here, the authors demonstrate the crucial role of AMPK for cellular stresses and growth factors- mediated Akt activation through a mechanism involving the E3 ubiquitin ligase Skp2 and Cullin-1. |
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AbstractList | PI3K/Akt signaling is activated in cancers and governs tumor initiation and progression, but how Akt is activated under diverse stresses is poorly understood. Here we identify AMPK as an essential regulator for Akt activation by various stresses. Surprisingly, AMPK is also activated by growth factor EGF through Ca2+/Calmodulin-dependent kinase and is essential for EGF-mediated Akt activation and biological functions. AMPK phosphorylates Skp2 at S256 and promotes the integrity and E3 ligase activity of Skp2 SCF complex leading to K63-linked ubiquitination and activation of Akt and subsequent oncogenic processes. Importantly, AMPK-mediated Skp2 S256 phosphorylation promotes breast cancer progression in mouse tumor models, correlates with Akt and AMPK activation in breast cancer patients, and predicts poor survival outcomes. Finally, targeting AMPK-mediated Skp2 S256 phosphorylation sensitizes cells to anti-EGF receptor targeted therapy. Our study sheds light on how stress and EGF induce Akt activation and new mechanisms for AMPK-mediated oncogenesis and drug resistance. How Akt pathway is activated under stress is poorly understood. Here, the authors demonstrate the crucial role of AMPK for cellular stresses and growth factors- mediated Akt activation through a mechanism involving the E3 ubiquitin ligase Skp2 and Cullin-1. PI3K/Akt signaling is activated in cancers and governs tumor initiation and progression, but how Akt is activated under diverse stresses is poorly understood. Here we identify AMPK as an essential regulator for Akt activation by various stresses. Surprisingly, AMPK is also activated by growth factor EGF through Ca2+/Calmodulin-dependent kinase and is essential for EGF-mediated Akt activation and biological functions. AMPK phosphorylates Skp2 at S256 and promotes the integrity and E3 ligase activity of Skp2 SCF complex leading to K63-linked ubiquitination and activation of Akt and subsequent oncogenic processes. Importantly, AMPK-mediated Skp2 S256 phosphorylation promotes breast cancer progression in mouse tumor models, correlates with Akt and AMPK activation in breast cancer patients, and predicts poor survival outcomes. Finally, targeting AMPK-mediated Skp2 S256 phosphorylation sensitizes cells to anti-EGF receptor targeted therapy. Our study sheds light on how stress and EGF induce Akt activation and new mechanisms for AMPK-mediated oncogenesis and drug resistance. How Akt pathway is activated under stress is poorly understood. Here, the authors demonstrate the crucial role of AMPK for cellular stresses and growth factors- mediated Akt activation through a mechanism involving the E3 ubiquitin ligase Skp2 and Cullin-1. Abstract PI3K/Akt signaling is activated in cancers and governs tumor initiation and progression, but how Akt is activated under diverse stresses is poorly understood. Here we identify AMPK as an essential regulator for Akt activation by various stresses. Surprisingly, AMPK is also activated by growth factor EGF through Ca2+/Calmodulin-dependent kinase and is essential for EGF-mediated Akt activation and biological functions. AMPK phosphorylates Skp2 at S256 and promotes the integrity and E3 ligase activity of Skp2 SCF complex leading to K63-linked ubiquitination and activation of Akt and subsequent oncogenic processes. Importantly, AMPK-mediated Skp2 S256 phosphorylation promotes breast cancer progression in mouse tumor models, correlates with Akt and AMPK activation in breast cancer patients, and predicts poor survival outcomes. Finally, targeting AMPK-mediated Skp2 S256 phosphorylation sensitizes cells to anti-EGF receptor targeted therapy. Our study sheds light on how stress and EGF induce Akt activation and new mechanisms for AMPK-mediated oncogenesis and drug resistance. |
ArticleNumber | 4728 |
Author | Han, Fei Morrow, John Lin, Hui-Kuan Xu, Dazhi Zhang, Shuxing Zhang, Wei-Na Zhang, Xian Li, Chien-Feng Xu, Chuan Wang, Guihua Wang, Chi-Yun Cai, Zhen Jin, Guoxiang |
Author_xml | – sequence: 1 givenname: Fei surname: Han fullname: Han, Fei organization: Department of Cancer Biology, Wake Forest School of Medicine, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center – sequence: 2 givenname: Chien-Feng surname: Li fullname: Li, Chien-Feng organization: Department of Pathology, Chi-Mei Foundational Medical Center, National Institute of Cancer Research, National Health Research Institutes – sequence: 3 givenname: Zhen surname: Cai fullname: Cai, Zhen organization: Department of Cancer Biology, Wake Forest School of Medicine, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center – sequence: 4 givenname: Xian orcidid: 0000-0001-9674-7886 surname: Zhang fullname: Zhang, Xian organization: Department of Cancer Biology, Wake Forest School of Medicine, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center – sequence: 5 givenname: Guoxiang surname: Jin fullname: Jin, Guoxiang organization: Department of Cancer Biology, Wake Forest School of Medicine, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center – sequence: 6 givenname: Wei-Na surname: Zhang fullname: Zhang, Wei-Na organization: Department of Cancer Biology, Wake Forest School of Medicine – sequence: 7 givenname: Chuan surname: Xu fullname: Xu, Chuan organization: Department of Cancer Biology, Wake Forest School of Medicine – sequence: 8 givenname: Chi-Yun surname: Wang fullname: Wang, Chi-Yun organization: Department of Cancer Biology, Wake Forest School of Medicine, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center – sequence: 9 givenname: John surname: Morrow fullname: Morrow, John organization: Department of Experimental Therapeutics, The University of Texas MD Anderson Cancer Center – sequence: 10 givenname: Shuxing surname: Zhang fullname: Zhang, Shuxing organization: Department of Experimental Therapeutics, The University of Texas MD Anderson Cancer Center – sequence: 11 givenname: Dazhi surname: Xu fullname: Xu, Dazhi email: xudzh@sysucc.org.cn organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Department of Gastric and Pancreatic Surgery, Sun Yat-Sen University Cancer Center – sequence: 12 givenname: Guihua surname: Wang fullname: Wang, Guihua email: ghwang18@163.com organization: Department of Cancer Biology, Wake Forest School of Medicine – sequence: 13 givenname: Hui-Kuan surname: Lin fullname: Lin, Hui-Kuan email: hulin@wakehealth.edu organization: Department of Cancer Biology, Wake Forest School of Medicine, Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Graduate Institute of Basic Medical Science, China Medical University, Department of Biotechnology, Asia University |
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Snippet | PI3K/Akt signaling is activated in cancers and governs tumor initiation and progression, but how Akt is activated under diverse stresses is poorly understood.... Abstract PI3K/Akt signaling is activated in cancers and governs tumor initiation and progression, but how Akt is activated under diverse stresses is poorly... How Akt pathway is activated under stress is poorly understood. Here, the authors demonstrate the crucial role of AMPK for cellular stresses and growth... |
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SubjectTerms | 1-Phosphatidylinositol 3-kinase 13 631/337/458/1733 631/67/395 96 Activation Adenylate Kinase - metabolism AKT protein Animal models Animals Breast cancer Calcium - metabolism Calcium ions Calcium-binding protein Calcium-Calmodulin-Dependent Protein Kinase Kinase - metabolism Calmodulin Cancer Carcinogenesis - drug effects Carcinogenesis - metabolism Carcinogenesis - pathology Cell Line, Tumor Cell Movement - drug effects Cell Survival - drug effects Disease Progression Drug resistance Drug Resistance, Neoplasm - drug effects Enzyme Activation - drug effects Epidermal Growth Factor - pharmacology ErbB Receptors - metabolism Fibroblasts - drug effects Fibroblasts - metabolism Glucose Glycolysis - drug effects Growth factors Human Umbilical Vein Endothelial Cells - metabolism Humanities and Social Sciences Humans Mice multidisciplinary Neovascularization, Pathologic - pathology Phosphorylation Phosphorylation - drug effects Phosphoserine - metabolism Proto-Oncogene Proteins c-akt - metabolism S-Phase Kinase-Associated Proteins - metabolism Science Science (multidisciplinary) Signal Transduction - drug effects Skp2 protein Stress, Physiological - drug effects Stresses Tumorigenesis Tumors Ubiquitin-protein ligase Ubiquitination Ubiquitination - drug effects |
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Title | The critical role of AMPK in driving Akt activation under stress, tumorigenesis and drug resistance |
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