PTEN self-regulates through USP11 via the PI3K-FOXO pathway to stabilize tumor suppression

PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an un...

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Published inNature communications Vol. 10; no. 1; pp. 636 - 17
Main Authors Park, Mi Kyung, Yao, Yixin, Xia, Weiya, Setijono, Stephanie Rebecca, Kim, Jae Hwan, Vila, Isabelle K., Chiu, Hui-Hsuan, Wu, Yun, Billalabeitia, Enrique González, Lee, Min Gyu, Kalb, Robert G., Hung, Mien-Chie, Pandolfi, Pier Paolo, Song, Su Jung, Song, Min Sup
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 07.02.2019
Nature Publishing Group
Nature Portfolio
Subjects
1-Phosphatidylinositol 3-kinase
631/67/1244
631/80/474/2289
64/60
96/95
AKT protein
Animals
Cancer
Cells, Cultured
Forkhead protein
Forkhead Transcription Factors - genetics
Forkhead Transcription Factors - metabolism
Gene Expression Regulation, Neoplastic - genetics
Gene Expression Regulation, Neoplastic - physiology
Humanities and Social Sciences
Life Sciences
Lipids
Localization
Magnetic Resonance Imaging
Male
Metastases
Mice
Mice, Knockout
Mice, Nude
multidisciplinary
Phosphatase
Phosphatidylinositol 3-Kinases - genetics
Phosphatidylinositol 3-Kinases - metabolism
PTEN Phosphohydrolase - genetics
PTEN Phosphohydrolase - metabolism
PTEN protein
Science
Science (multidisciplinary)
Signal Transduction - genetics
Signal Transduction - physiology
Stability
Thiolester Hydrolases - genetics
Thiolester Hydrolases - metabolism
Transcription
Tumor suppressor genes
Tumors
Online AccessGet full text

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Abstract PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN. PTEN is a lipid phosphatase that functions as a dose-dependent tumor suppressor through the PI3K/AKT pathway. Here the authors describe a signaling feedback mechanism where PTEN stability is regulated through transcriptional upregulation of X-linked ubiquitin-specific protease 11 (USP11) via the PI3K/FOXO pathway.
AbstractList PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN. PTEN is a lipid phosphatase that functions as a dose-dependent tumor suppressor through the PI3K/AKT pathway. Here the authors describe a signaling feedback mechanism where PTEN stability is regulated through transcriptional upregulation of X-linked ubiquitin-specific protease 11 (USP11) via the PI3K/FOXO pathway.
PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN.PTEN is a lipid phosphatase that functions as a dose-dependent tumor suppressor through the PI3K/AKT pathway. Here the authors describe a signaling feedback mechanism where PTEN stability is regulated through transcriptional upregulation of X-linked ubiquitin-specific protease 11 (USP11) via the PI3K/FOXO pathway.
PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN.PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN.
PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN.
PTEN is a lipid phosphatase that functions as a dose-dependent tumor suppressor through the PI3K/AKT pathway. Here the authors describe a signaling feedback mechanism where PTEN stability is regulated through transcriptional upregulation of X-linked ubiquitin-specific protease 11 (USP11) via the PI3K/FOXO pathway.
PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN.
Abstract PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that control PTEN levels therefore offer potential routes to therapy, but these are as yet poorly defined. Here we demonstrate that PTEN plays an unexpected role in regulating its own stability through the transcriptional upregulation of the deubiquitinase USP11 by the PI3K/FOXO pathway, and further show that this feedforward mechanism is implicated in its tumor-suppressive role, as mice lacking Usp11 display increased susceptibility to PTEN-dependent tumor initiation, growth and metastasis. Notably, USP11 is downregulated in cancer patients, and correlates with PTEN expression and FOXO nuclear localization. Our findings therefore demonstrate that PTEN-PI3K-FOXO-USP11 constitute the regulatory feedforward loop that improves the stability and tumor suppressive activity of PTEN.
ArticleNumber 636
Author Wu, Yun
Hung, Mien-Chie
Pandolfi, Pier Paolo
Park, Mi Kyung
Setijono, Stephanie Rebecca
Kim, Jae Hwan
Yao, Yixin
Lee, Min Gyu
Song, Min Sup
Vila, Isabelle K.
Xia, Weiya
Billalabeitia, Enrique González
Song, Su Jung
Kalb, Robert G.
Chiu, Hui-Hsuan
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  givenname: Yun
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  fullname: Wu, Yun
  organization: Department of Pathology, The University of Texas MD Anderson Cancer Center
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  givenname: Enrique González
  surname: Billalabeitia
  fullname: Billalabeitia, Enrique González
  organization: Department of Clinical Oncology, Hospital Universitario Morales Meseguer-IMIB, Universidad Católica San Antonio de Murcia-UCAM
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  surname: Lee
  fullname: Lee, Min Gyu
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  givenname: Robert G.
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  givenname: Mien-Chie
  surname: Hung
  fullname: Hung, Mien-Chie
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Cancer Biology Program, The University of Texas Graduate School of Biomedical Sciences, The University of Texas MD Anderson Cancer Center, Center for Molecular Medicine and Graduate Institute of Cancer Biology, China Medical University
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  orcidid: 0000-0002-5352-5295
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  email: ssong1@sch.ac.kr
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  givenname: Min Sup
  surname: Song
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  email: msong1@mdanderson.org
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Cancer Biology Program, The University of Texas Graduate School of Biomedical Sciences, The University of Texas MD Anderson Cancer Center
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Issue 1
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SSID ssj0000391844
Score 2.5071855
Snippet PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular mechanisms that...
Abstract PTEN is a lipid phosphatase that antagonizes the PI3K/AKT pathway and is recognized as a major dose-dependent tumor suppressor. The cellular...
PTEN is a lipid phosphatase that functions as a dose-dependent tumor suppressor through the PI3K/AKT pathway. Here the authors describe a signaling feedback...
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proquest
pubmed
crossref
springer
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Open Access Repository
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Enrichment Source
Publisher
StartPage 636
SubjectTerms 1-Phosphatidylinositol 3-kinase
631/67/1244
631/80/474/2289
64/60
96/95
AKT protein
Animals
Cancer
Cells, Cultured
Forkhead protein
Forkhead Transcription Factors - genetics
Forkhead Transcription Factors - metabolism
Gene Expression Regulation, Neoplastic - genetics
Gene Expression Regulation, Neoplastic - physiology
Humanities and Social Sciences
Life Sciences
Lipids
Localization
Magnetic Resonance Imaging
Male
Metastases
Mice
Mice, Knockout
Mice, Nude
multidisciplinary
Phosphatase
Phosphatidylinositol 3-Kinases - genetics
Phosphatidylinositol 3-Kinases - metabolism
PTEN Phosphohydrolase - genetics
PTEN Phosphohydrolase - metabolism
PTEN protein
Science
Science (multidisciplinary)
Signal Transduction - genetics
Signal Transduction - physiology
Stability
Thiolester Hydrolases - genetics
Thiolester Hydrolases - metabolism
Transcription
Tumor suppressor genes
Tumors
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Title PTEN self-regulates through USP11 via the PI3K-FOXO pathway to stabilize tumor suppression
URI https://link.springer.com/article/10.1038/s41467-019-08481-x
https://www.ncbi.nlm.nih.gov/pubmed/30733438
https://www.proquest.com/docview/2176707572
https://www.proquest.com/docview/2194593080
https://hal.science/hal-04765231
https://pubmed.ncbi.nlm.nih.gov/PMC6367354
https://doaj.org/article/b1a406900145437995bad2a50a3a9b15
Volume 10
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