Autophagy in malignant transformation and cancer progression
Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is r...
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| Published in | The EMBO journal Vol. 34; no. 7; pp. 856 - 880 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Blackwell Publishing Ltd
01.04.2015
Nature Publishing Group UK Springer Nature B.V BlackWell Publishing Ltd |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0261-4189 1460-2075 1460-2075 |
| DOI | 10.15252/embj.201490784 |
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| Abstract | Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is required for optimal anticancer immunosurveillance. In neoplastic cells, however, autophagic responses constitute a means to cope with intracellular and environmental stress, thus favoring tumor progression. This implies that at least in some cases, oncogenesis proceeds along with a temporary inhibition of autophagy or a gain of molecular functions that antagonize its oncosuppressive activity. Here, we discuss the differential impact of autophagy on distinct phases of tumorigenesis and the implications of this concept for the use of autophagy modulators in cancer therapy.
Graphical Abstract
Autophagy has been described to have tumor‐suppressive as well as tumor‐promoting functions. This review discusses how stage and context alters the role for autophagy in cancer, and argues for further research prior to targeting autophagy in cancer therapy. |
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| AbstractList | Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is required for optimal anticancer immunosurveillance. In neoplastic cells, however, autophagic responses constitute a means to cope with intracellular and environmental stress, thus favoring tumor progression. This implies that at least in some cases, oncogenesis proceeds along with a temporary inhibition of autophagy or a gain of molecular functions that antagonize its oncosuppressive activity. Here, we discuss the differential impact of autophagy on distinct phases of tumorigenesis and the implications of this concept for the use of autophagy modulators in cancer therapy. Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is required for optimal anticancer immunosurveillance. In neoplastic cells, however, autophagic responses constitute a means to cope with intracellular and environmental stress, thus favoring tumor progression. This implies that at least in some cases, oncogenesis proceeds along with a temporary inhibition of autophagy or a gain of molecular functions that antagonize its oncosuppressive activity. Here, we discuss the differential impact of autophagy on distinct phases of tumorigenesis and the implications of this concept for the use of autophagy modulators in cancer therapy. Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is required for optimal anticancer immunosurveillance. In neoplastic cells, however, autophagic responses constitute a means to cope with intracellular and environmental stress, thus favoring tumor progression. This implies that at least in some cases, oncogenesis proceeds along with a temporary inhibition of autophagy or a gain of molecular functions that antagonize its oncosuppressive activity. Here, we discuss the differential impact of autophagy on distinct phases of tumorigenesis and the implications of this concept for the use of autophagy modulators in cancer therapy. Autophagy has been described to have tumor‐suppressive as well as tumor‐promoting functions. This review discusses how stage and context alters the role for autophagy in cancer, and argues for further research prior to targeting autophagy in cancer therapy. Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is required for optimal anticancer immunosurveillance. In neoplastic cells, however, autophagic responses constitute a means to cope with intracellular and environmental stress, thus favoring tumor progression. This implies that at least in some cases, oncogenesis proceeds along with a temporary inhibition of autophagy or a gain of molecular functions that antagonize its oncosuppressive activity. Here, we discuss the differential impact of autophagy on distinct phases of tumorigenesis and the implications of this concept for the use of autophagy modulators in cancer therapy.Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is required for optimal anticancer immunosurveillance. In neoplastic cells, however, autophagic responses constitute a means to cope with intracellular and environmental stress, thus favoring tumor progression. This implies that at least in some cases, oncogenesis proceeds along with a temporary inhibition of autophagy or a gain of molecular functions that antagonize its oncosuppressive activity. Here, we discuss the differential impact of autophagy on distinct phases of tumorigenesis and the implications of this concept for the use of autophagy modulators in cancer therapy. Autophagy plays a key role in the maintenance of cellular homeostasis. In healthy cells, such a homeostatic activity constitutes a robust barrier against malignant transformation. Accordingly, many oncoproteins inhibit, and several oncosuppressor proteins promote, autophagy. Moreover, autophagy is required for optimal anticancer immunosurveillance. In neoplastic cells, however, autophagic responses constitute a means to cope with intracellular and environmental stress, thus favoring tumor progression. This implies that at least in some cases, oncogenesis proceeds along with a temporary inhibition of autophagy or a gain of molecular functions that antagonize its oncosuppressive activity. Here, we discuss the differential impact of autophagy on distinct phases of tumorigenesis and the implications of this concept for the use of autophagy modulators in cancer therapy. Graphical Abstract Autophagy has been described to have tumor‐suppressive as well as tumor‐promoting functions. This review discusses how stage and context alters the role for autophagy in cancer, and argues for further research prior to targeting autophagy in cancer therapy. |
| Author | Karantza, Vassiliki Rubinsztein, David C Simonsen, Anne Codogno, Patrice Piacentini, Mauro Galluzzi, Lorenzo Penninger, Josef Gewirtz, David A Ryan, Kevin M Kimmelman, Alec Kumar, Sharad Thorburn, Andrew M Bravo‐San Pedro, José Manuel Baehrecke, Eric H Simon, Hans‐Uwe Velasco, Guillermo Pietrocola, Federico Debnath, Jayanta Maiuri, Maria Chiara Martin, Seamus J Amaravadi, Ravi K Kroemer, Guido Cecconi, Francesco Levine, Beth |
| Author_xml | – sequence: 1 givenname: Lorenzo surname: Galluzzi fullname: Galluzzi, Lorenzo email: deadoc@vodafone.it organization: Equipe 11 labellisée pas la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France – sequence: 2 givenname: Federico surname: Pietrocola fullname: Pietrocola, Federico organization: Equipe 11 labellisée pas la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France – sequence: 3 givenname: José Manuel surname: Bravo-San Pedro fullname: Bravo-San Pedro, José Manuel organization: Equipe 11 labellisée pas la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France – sequence: 4 givenname: Ravi K surname: Amaravadi fullname: Amaravadi, Ravi K organization: Abramson Cancer Center, University of Pennsylvania, PA, Philadelphia, USA – sequence: 5 givenname: Eric H surname: Baehrecke fullname: Baehrecke, Eric H organization: Department of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, MA, Worcester, USA – sequence: 6 givenname: Francesco surname: Cecconi fullname: Cecconi, Francesco organization: Cell Stress and Survival Unit, Danish Cancer Society Research Center, Copenhagen, Denmark – sequence: 7 givenname: Patrice surname: Codogno fullname: Codogno, Patrice organization: Université Paris Descartes, Sorbonne Paris Cité, Paris, France – sequence: 8 givenname: Jayanta surname: Debnath fullname: Debnath, Jayanta organization: Department of Pathology and Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, CA, San Francisco, USA – sequence: 9 givenname: David A surname: Gewirtz fullname: Gewirtz, David A organization: Department of Pharmacology, Toxicology and Medicine, Virginia Commonwealth University, VA, RichmondVirginia, USA – sequence: 10 givenname: Vassiliki surname: Karantza fullname: Karantza, Vassiliki organization: Merck Research Laboratories, NJ, Rahway, USA – sequence: 11 givenname: Alec surname: Kimmelman fullname: Kimmelman, Alec organization: Division of Genomic Stability and DNA Repair, Department of Radiation Oncology, Dana-Farber Cancer Institute, MA, Boston, USA – sequence: 12 givenname: Sharad surname: Kumar fullname: Kumar, Sharad organization: Centre for Cancer Biology, University of South Australia, SA, Adelaide, Australia – sequence: 13 givenname: Beth surname: Levine fullname: Levine, Beth organization: Center for Autophagy Research, Department of Internal Medicine, University of Texas Southwestern Medical Center, Dallas, TX, USA – sequence: 14 givenname: Maria Chiara surname: Maiuri fullname: Maiuri, Maria Chiara organization: Equipe 11 labellisée pas la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France – sequence: 15 givenname: Seamus J surname: Martin fullname: Martin, Seamus J organization: Department of Genetics, Trinity College, The Smurfit Institute, Dublin, Ireland – sequence: 16 givenname: Josef surname: Penninger fullname: Penninger, Josef organization: Institute of Molecular Biotechnology of the Austrian Academy of Sciences, Vienna, Austria – sequence: 17 givenname: Mauro surname: Piacentini fullname: Piacentini, Mauro organization: Department of Biology, University of Rome Tor Vergata, Rome, Italy – sequence: 18 givenname: David C surname: Rubinsztein fullname: Rubinsztein, David C organization: Department of Medical Genetics, Cambridge Institute for Medical Research, University of Cambridge, Cambridge, UK – sequence: 19 givenname: Hans-Uwe surname: Simon fullname: Simon, Hans-Uwe organization: Institute of Pharmacology, University of Bern, Bern, Switzerland – sequence: 20 givenname: Anne surname: Simonsen fullname: Simonsen, Anne organization: Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway – sequence: 21 givenname: Andrew M surname: Thorburn fullname: Thorburn, Andrew M organization: Department of Pharmacology, University of Colorado School of Medicine, CO, Aurora, USA – sequence: 22 givenname: Guillermo surname: Velasco fullname: Velasco, Guillermo organization: Department of Biochemistry and Molecular Biology I, School of Biology, Complutense University of Madrid, Madrid, Spain – sequence: 23 givenname: Kevin M surname: Ryan fullname: Ryan, Kevin M organization: Cancer Research UK Beatson Institute, Glasgow, UK – sequence: 24 givenname: Guido surname: Kroemer fullname: Kroemer, Guido organization: Equipe 11 labellisée pas la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25712477$$D View this record in MEDLINE/PubMed |
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| CODEN | EMJODG |
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| Issue | 7 |
| Keywords | mitophagy KRAS adaptive stress responses inflammation Beclin 1 |
| Language | English |
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| Notes | Institutional Research Grant - No. IRG-14-192-40 National Health and Medical Research Council of Australia Project Grant - No. 1041807 Fondation Bettencourt-Schueller Fondo Europeo de Desarrollo Regional (FEDER) - No. PI12/02248; No. FR2009-0052; No. IT2009-0053 European Commission (ArtForce) SIRIC Stratified Oncology Cell DNA Repair and Tumor Immune Elimination (SOCRATE) LabEx Immuno-Oncology European Commission (MEL-PLEX) American Cancer Society Fundación Mutua Madrileña - No. AP101042012 Ministry of Health of Italy ('Ricerca Corrente' and 'Ricerca Finalizzata') Spanish Ministry of Economy and Competitiveness (MINECO) istex:1DD0F6A1097CF6D38BD562148AEBD9804AA41BFD Paris Alliance of Cancer Research Institutes (PACRI) Institut National du Cancer (INCa) ark:/67375/WNG-46P3WC04-L Senior Principal Research Fellowship - No. 1002863 Association pour la recherche sur le cancer (ARC) SIRIC Cancer Research and Personalized Medicine (CARPEM) Cancéropôle Ile-de-France Swiss National Science Foundation Fundació La Marató de TV3 - No. 20134031 ArticleID:EMBJ201490784 Fondation pour la Recherche Médicale (FRM) Associazione Italiana per la Ricerca sul Cancro (AIRC) Fondation de France European Research Council (ERC) Agence National de la Recherche (ANR) Swiss Cancer League ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Review-3 content type line 23 These authors contributed equally to this work These authors share senior co-authorship |
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| SubjectTerms | adaptive stress responses Animals Autophagy Beclin 1 Cancer therapies Cell Transformation, Neoplastic - immunology Cell Transformation, Neoplastic - metabolism Cell Transformation, Neoplastic - pathology Cellular biology EMBO03 EMBO07 Environmental stress Humans inflammation KRAS mitophagy Neoplasms - immunology Neoplasms - metabolism Neoplasms - pathology Neoplasms - therapy Review Reviews Tumor Escape Tumor Suppressor Proteins - immunology Tumor Suppressor Proteins - metabolism |
| Title | Autophagy in malignant transformation and cancer progression |
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