Akt and 14-3-3 Control a PACS-2 Homeostatic Switch that Integrates Membrane Traffic with TRAIL-Induced Apoptosis
TRAIL selectively kills diseased cells in vivo, spurring interest in this death ligand as a potential therapeutic. However, many cancer cells are resistant to TRAIL, suggesting the mechanism mediating TRAIL-induced apoptosis is complex. Here we identify PACS-2 as an essential TRAIL effector, require...
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| Published in: | Molecular cell Vol. 34; no. 4; pp. 497 - 509 |
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| Main Authors: | , , , , , , , , , , , , , , , , |
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| Abstract | TRAIL selectively kills diseased cells in vivo, spurring interest in this death ligand as a potential therapeutic. However, many cancer cells are resistant to TRAIL, suggesting the mechanism mediating TRAIL-induced apoptosis is complex. Here we identify PACS-2 as an essential TRAIL effector, required for killing tumor cells in vitro and virally infected hepatocytes in vivo. PACS-2 is phosphorylated at Ser437 in vivo, and pharmacologic and genetic studies demonstrate Akt is an in vivo Ser437 kinase. Akt cooperates with 14-3-3 to regulate the homeostatic and apoptotic properties of PACS-2 that mediate TRAIL action. Phosphorylated Ser437 binds 14-3-3 with high affinity, which represses PACS-2 apoptotic activity and is required for PACS-2 to mediate trafficking of membrane cargo. TRAIL triggers dephosphorylation of Ser437, reprogramming PACS-2 to promote apoptosis. Together, these studies identify the phosphorylation state of PACS-2 Ser437 as a molecular switch that integrates cellular homeostasis with TRAIL-induced apoptosis. |
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| AbstractList | TRAIL selectively kills diseased cells in vivo, spurring interest in this death ligand as a potential therapeutic. However, many cancer cells are resistant to TRAIL suggesting the mechanism mediating TRAIL-induced apoptosis is complex. Here we identify PACS-2 as an essential TRAIL effector, required for killing tumor cells in vitro and virally infected hepatocytes in vivo. PACS-2 is phosphorylated at Ser
437
in vivo and pharmacologic and genetic studies demonstrate Akt is an in vivo Ser
437
kinase. Akt cooperates with 14-3-3 to regulate the homeostatic and apoptotic properties of PACS-2 that mediate TRAIL action. Phosphorylated Ser
437
binds 14-3-3 with high affinity, which represses PACS-2 apoptotic activity and is required for PACS-2 to mediate trafficking of membrane cargo. TRAIL triggers dephosphorylation of Ser
437
, reprogramming PACS-2 to promote apoptosis. Together, these studies identify the phosphorylation state of PACS-2 Ser
437
as a molecular switch that integrates cellular homeostasis with TRAIL-induced apoptosis. TRAIL selectively kills diseased cells in vivo, spurring interest in this death ligand as a potential therapeutic. However, many cancer cells are resistant to TRAIL, suggesting the mechanism mediating TRAIL-induced apoptosis is complex. Here we identify PACS-2 as an essential TRAIL effector, required for killing tumor cells in vitro and virally infected hepatocytes in vivo. PACS-2 is phosphorylated at Ser437 in vivo, and pharmacologic and genetic studies demonstrate Akt is an in vivo Ser437 kinase. Akt cooperates with 14-3-3 to regulate the homeostatic and apoptotic properties of PACS-2 that mediate TRAIL action. Phosphorylated Ser437 binds 14-3-3 with high affinity, which represses PACS-2 apoptotic activity and is required for PACS-2 to mediate trafficking of membrane cargo. TRAIL triggers dephosphorylation of Ser437, reprogramming PACS-2 to promote apoptosis. Together, these studies identify the phosphorylation state of PACS-2 Ser437 as a molecular switch that integrates cellular homeostasis with TRAIL-induced apoptosis. TRAIL selectively kills diseased cells in vivo, spurring interest in this death ligand as a potential therapeutic. However, many cancer cells are resistant to TRAIL, suggesting the mechanism mediating TRAIL-induced apoptosis is complex. Here we identify PACS-2 as an essential TRAIL effector, required for killing tumor cells in vitro and virally infected hepatocytes in vivo. PACS-2 is phosphorylated at Ser437 in vivo, and pharmacologic and genetic studies demonstrate Akt is an in vivo Ser437 kinase. Akt cooperates with 14-3-3 to regulate the homeostatic and apoptotic properties of PACS-2 that mediate TRAIL action. Phosphorylated Ser437 binds 14-3-3 with high affinity, which represses PACS-2 apoptotic activity and is required for PACS-2 to mediate trafficking of membrane cargo. TRAIL triggers dephosphorylation of Ser437, reprogramming PACS-2 to promote apoptosis. Together, these studies identify the phosphorylation state of PACS-2 Ser437 as a molecular switch that integrates cellular homeostasis with TRAIL-induced apoptosis. |
| Author | Williamson, Danielle M. Thomas, Laurel Du, Yuhong Fu, Haian You, Huihong Shu, Hongjun Sprott, Kam Brush, Matthew H. Greis, Kenneth D. Aslan, Joseph E. Endig, Jessica Youker, Robert T. Milewski, Robert L. Runckel, Douglas N. Vogel, Arndt Possemato, Anthony Thomas, Gary |
| AuthorAffiliation | 3 Genome Research Institute, University of Cincinnati, Cincinnati, OH, USA 5 Kaiser Permanente, Portland, OR, USA 4 Department of Pharmacology and Emory Chemical Biology Discovery Center, Emory University School of Medicine, Atlanta 6 Cell Signaling Technology, Danvers MA, USA 2 Clinic for Gastroenterology, Hepatology and Endocrinology, Hannover Medical School, Hannover, Germany 1 Vollum Institute, Oregon Health & Science University, Portland, OR, USA |
| AuthorAffiliation_xml | – name: 4 Department of Pharmacology and Emory Chemical Biology Discovery Center, Emory University School of Medicine, Atlanta – name: 6 Cell Signaling Technology, Danvers MA, USA – name: 2 Clinic for Gastroenterology, Hepatology and Endocrinology, Hannover Medical School, Hannover, Germany – name: 5 Kaiser Permanente, Portland, OR, USA – name: 3 Genome Research Institute, University of Cincinnati, Cincinnati, OH, USA – name: 1 Vollum Institute, Oregon Health & Science University, Portland, OR, USA |
| Author_xml | – sequence: 1 givenname: Joseph E. surname: Aslan fullname: Aslan, Joseph E. organization: Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA – sequence: 2 givenname: Huihong surname: You fullname: You, Huihong organization: Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA – sequence: 3 givenname: Danielle M. surname: Williamson fullname: Williamson, Danielle M. organization: Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA – sequence: 4 givenname: Jessica surname: Endig fullname: Endig, Jessica organization: Clinic for Gastroenterology, Hepatology, and Endocrinology, Hannover Medical School, 30625 Hannover, Germany – sequence: 5 givenname: Robert T. surname: Youker fullname: Youker, Robert T. organization: Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA – sequence: 6 givenname: Laurel surname: Thomas fullname: Thomas, Laurel organization: Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA – sequence: 7 givenname: Hongjun surname: Shu fullname: Shu, Hongjun organization: Genome Research Institute, University of Cincinnati, Cincinnati, OH 45237, USA – sequence: 8 givenname: Yuhong surname: Du fullname: Du, Yuhong organization: Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322, USA – sequence: 9 givenname: Robert L. surname: Milewski fullname: Milewski, Robert L. organization: Kaiser Permanente, Portland, OR 97230, USA – sequence: 10 givenname: Matthew H. surname: Brush fullname: Brush, Matthew H. organization: Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA – sequence: 11 givenname: Anthony surname: Possemato fullname: Possemato, Anthony organization: Cell Signaling Technology, Danvers, MA 01923, USA – sequence: 12 givenname: Kam surname: Sprott fullname: Sprott, Kam organization: Cell Signaling Technology, Danvers, MA 01923, USA – sequence: 13 givenname: Haian surname: Fu fullname: Fu, Haian organization: Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322, USA – sequence: 14 givenname: Kenneth D. surname: Greis fullname: Greis, Kenneth D. organization: Genome Research Institute, University of Cincinnati, Cincinnati, OH 45237, USA – sequence: 15 givenname: Douglas N. surname: Runckel fullname: Runckel, Douglas N. organization: Kaiser Permanente, Portland, OR 97230, USA – sequence: 16 givenname: Arndt surname: Vogel fullname: Vogel, Arndt organization: Clinic for Gastroenterology, Hepatology, and Endocrinology, Hannover Medical School, 30625 Hannover, Germany – sequence: 17 givenname: Gary surname: Thomas fullname: Thomas, Gary email: thomasg@ohsu.edu organization: Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA |
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| Snippet | TRAIL selectively kills diseased cells in vivo, spurring interest in this death ligand as a potential therapeutic. However, many cancer cells are resistant to... TRAIL selectively kills diseased cells in vivo, spurring interest in this death ligand as a potential therapeutic. However, many cancer cells are resistant to... |
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| SubjectTerms | 14-3-3 Proteins - genetics 14-3-3 Proteins - metabolism Animals Apoptosis - physiology BH3 Interacting Domain Death Agonist Protein - genetics BH3 Interacting Domain Death Agonist Protein - metabolism Caspases - metabolism Cell Line, Tumor Cell Membrane - metabolism CELLBIO CELLCYCLE Cells, Cultured Fibroblasts - cytology Fibroblasts - metabolism Homeostasis Humans Mice Mice, Knockout Neoplasms - metabolism Neoplasms - pathology PROTEINS Proto-Oncogene Proteins c-akt - genetics Proto-Oncogene Proteins c-akt - metabolism Recombinant Fusion Proteins - genetics Recombinant Fusion Proteins - metabolism Serine - metabolism TNF-Related Apoptosis-Inducing Ligand - genetics TNF-Related Apoptosis-Inducing Ligand - metabolism Vesicular Transport Proteins - genetics Vesicular Transport Proteins - metabolism |
| Title | Akt and 14-3-3 Control a PACS-2 Homeostatic Switch that Integrates Membrane Traffic with TRAIL-Induced Apoptosis |
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