Intestinal inhibition of Atg7 prevents tumour initiation through a microbiome-influenced immune response and suppresses tumour growth

Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in intestinal epithelial cells inhibits the formation of pre-cancerous lesions in Apc +/− mice by enhancing anti-tumour responses. The antibody-m...

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Published in:	Nature cell biology Vol. 17; no. 8; pp. 1062 - 1073
Main Authors:	Lévy, Jonathan, Cacheux, Wulfran, Bara, Medhi Ait, L’Hermitte, Antoine, Lepage, Patricia, Fraudeau, Marie, Trentesaux, Coralie, Lemarchand, Julie, Durand, Aurélie, Crain, Anne-Marie, Marchiol, Carmen, Renault, Gilles, Dumont, Florent, Letourneur, Franck, Delacre, Myriam, Schmitt, Alain, Terris, Benoit, Perret, Christine, Chamaillard, Mathias, Couty, Jean-Pierre, Romagnolo, Béatrice
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 01-08-2015 Nature Publishing Group
Subjects:	13/1 13/105 13/2 13/21 13/31 13/51 14/28 38/23 38/32 38/39 38/61 631/67 631/80/39 64/60 Adenocarcinoma - genetics Adenocarcinoma - immunology Adenocarcinoma - microbiology Adenocarcinoma - pathology Adenocarcinoma - prevention & control Adenoma - genetics Adenoma - immunology Adenoma - microbiology Adenoma - pathology Adenoma - prevention & control AMP-Activated Protein Kinases - metabolism Animals Autophagy Autophagy (Cytology) Autophagy-Related Protein 7 Cancer Research CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism CD8-Positive T-Lymphocytes - microbiology Cell Biology Cell Cycle Checkpoints Cell Proliferation Cell Transformation, Neoplastic - genetics Cell Transformation, Neoplastic - immunology Cell Transformation, Neoplastic - metabolism Cell Transformation, Neoplastic - pathology Cellular proteins Colon - immunology Colon - metabolism Colon - microbiology Colon - pathology Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - genetics Colorectal Neoplasms - immunology Colorectal Neoplasms - microbiology Colorectal Neoplasms - pathology Colorectal Neoplasms - prevention & control Development and progression Developmental Biology Disease Models, Animal Dysbiosis Enzyme Activation Female Gene expression Genes, APC Genetic aspects Health aspects Host-Pathogen Interactions Humans Immune response Immunity, Mucosal Inactivation Life Sciences Male Mice, Inbred C57BL Mice, Knockout Microbiota - immunology Microtubule-Associated Proteins - deficiency Microtubule-Associated Proteins - genetics Properties Stem Cells Time Factors Tumor Burden Tumor Suppressor Protein p53 - metabolism Tumors Ubiquitin-Activating Enzymes - metabolism
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Abstract	Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in intestinal epithelial cells inhibits the formation of pre-cancerous lesions in Apc +/− mice by enhancing anti-tumour responses. The antibody-mediated depletion of CD8 + T cells showed that these cells are essential for the anti-tumoral responses mediated by the inhibition of autophagy. We show that Atg7 deficiency leads to intestinal dysbiosis and that the microbiota is required for anticancer responses. In addition, Atg7 deficiency resulted in a stress response accompanied by metabolic defects, AMPK activation and p53-mediated cell-cycle arrest in tumour cells but not in normal tissue. This study reveals that the inhibition of autophagy within the epithelium may prevent the development and progression of colorectal cancer in genetically predisposed patients. Romagnolo and colleagues report that Atg7 deficiency has a tumour-suppressive role in the intestinal epithelium, by inducing a microbiome-influenced immune response and inhibiting tumour growth through p53- and AMPK-related mechanisms.
AbstractList	Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in intestinal epithelial cells inhibits the formation of pre-cancerous lesions in Apc(+/-) mice by enhancing anti-tumour responses. The antibody-mediated depletion of CD8(+) T cells showed that these cells are essential for the anti-tumoral responses mediated by the inhibition of autophagy. We show that Atg7 deficiency leads to intestinal dysbiosis and that the microbiota is required for anticancer responses. In addition, Atg7 deficiency resulted in a stress response accompanied by metabolic defects, AMPK activation and p53-mediated cell-cycle arrest in tumour cells but not in normal tissue. This study reveals that the inhibition of autophagy within the epithelium may prevent the development and progression of colorectal cancer in genetically predisposed patients. Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in intestinal epithelial cells inhibits the formation of pre-cancerous lesions in Apc +/− mice by enhancing anti-tumour responses. The antibody-mediated depletion of CD8 + T cells showed that these cells are essential for the anti-tumoral responses mediated by the inhibition of autophagy. We show that Atg7 deficiency leads to intestinal dysbiosis and that the microbiota is required for anticancer responses. In addition, Atg7 deficiency resulted in a stress response accompanied by metabolic defects, AMPK activation and p53-mediated cell-cycle arrest in tumour cells but not in normal tissue. This study reveals that the inhibition of autophagy within the epithelium may prevent the development and progression of colorectal cancer in genetically predisposed patients. Romagnolo and colleagues report that Atg7 deficiency has a tumour-suppressive role in the intestinal epithelium, by inducing a microbiome-influenced immune response and inhibiting tumour growth through p53- and AMPK-related mechanisms. Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in intestinal epithelial cells inhibits the formation of pre-cancerous lesions in [Apc.sup.+/-] mice by enhancing anti-tumour responses. The antibody-mediated depletion of [CD8.sup.+] T cells showed that these cells are essential for the anti-tumoral responses mediated by the inhibition of autophagy. We show that Atg7 deficiency leads to intestinal dysbiosis and that the microbiota is required for anticancer responses. In addition, Atg7 deficiency resulted in a stress response accompanied by metabolic defects, AMPK activation and p53-mediated cell-cycle arrest in tumour cells but not in normal tissue. This study reveals that the inhibition of autophagy within the epithelium may prevent the development and progression of colorectal cancer in genetically predisposed patients. Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in intestinal epithelial cells inhibits the formation of pre-cancerous lesions in Apc super(+/-) mice by enhancing anti-tumour responses. The antibody-mediated depletion of CD8 super(+) T cells showed that these cells are essential for the anti-tumoral responses mediated by the inhibition of autophagy. We show that Atg7 deficiency leads to intestinal dysbiosis and that the microbiota is required for anticancer responses. In addition, Atg7 deficiency resulted in a stress response accompanied by metabolic defects, AMPK activation and p53-mediated cell-cycle arrest in tumour cells but not in normal tissue. This study reveals that the inhibition of autophagy within the epithelium may prevent the development and progression of colorectal cancer in genetically predisposed patients.
Audience	Academic
Author	Lévy, Jonathan Delacre, Myriam Perret, Christine Marchiol, Carmen Cacheux, Wulfran Chamaillard, Mathias Fraudeau, Marie Durand, Aurélie L’Hermitte, Antoine Dumont, Florent Schmitt, Alain Couty, Jean-Pierre Lepage, Patricia Lemarchand, Julie Romagnolo, Béatrice Trentesaux, Coralie Crain, Anne-Marie Terris, Benoit Letourneur, Franck Bara, Medhi Ait Renault, Gilles
Author_xml	– sequence: 1 givenname: Jonathan surname: Lévy fullname: Lévy, Jonathan organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 2 givenname: Wulfran surname: Cacheux fullname: Cacheux, Wulfran organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016, Department of Medical Oncology, Institut Curie, 26 rue d’Ulm, 75248 Paris Cedex 05, France, Department of Genetics, Pharmacogenomics Unit, Institut Curie, 26 rue d’Ulm, 75248 Paris Cedex 05, France – sequence: 3 givenname: Medhi Ait surname: Bara fullname: Bara, Medhi Ait organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 4 givenname: Antoine surname: L’Hermitte fullname: L’Hermitte, Antoine organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 5 givenname: Patricia surname: Lepage fullname: Lepage, Patricia organization: Institut National de la Recherche Agronomique, Micalis UMR1319, AgroParisTech, Micalis UMR1319 – sequence: 6 givenname: Marie surname: Fraudeau fullname: Fraudeau, Marie organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 7 givenname: Coralie surname: Trentesaux fullname: Trentesaux, Coralie organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 8 givenname: Julie surname: Lemarchand fullname: Lemarchand, Julie organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 9 givenname: Aurélie surname: Durand fullname: Durand, Aurélie organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 10 givenname: Anne-Marie surname: Crain fullname: Crain, Anne-Marie organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016, Université Paris Diderot, UFR Sciences du Vivant, Sorbonne Paris Cité – sequence: 11 givenname: Carmen surname: Marchiol fullname: Marchiol, 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Médicale (INSERM), U1016 – sequence: 15 givenname: Myriam surname: Delacre fullname: Delacre, Myriam organization: Université Lille Nord de France, Institut Pasteur de Lille, Center for Infection and Immunity of Lille, Centre National de la Recherche Scientifique, Unité Mixte de Recherche, Institut National de la Santé et de la Recherche Médicale – sequence: 16 givenname: Alain surname: Schmitt fullname: Schmitt, Alain organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 17 givenname: Benoit surname: Terris fullname: Terris, Benoit organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016, Service d’Anatomie et Cytologie Pathologiques, AP-HP, Hôpital Cochin, Université Paris Descartes – sequence: 18 givenname: Christine surname: Perret fullname: Perret, Christine organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016 – sequence: 19 givenname: Mathias surname: Chamaillard fullname: Chamaillard, Mathias organization: Université Lille Nord de France, Institut Pasteur de Lille, Center for Infection and Immunity of Lille, Centre National de la Recherche Scientifique, Unité Mixte de Recherche, Institut National de la Santé et de la Recherche Médicale – sequence: 20 givenname: Jean-Pierre surname: Couty fullname: Couty, Jean-Pierre organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016, Université Paris Diderot, UFR Sciences du Vivant, Sorbonne Paris Cité – sequence: 21 givenname: Béatrice surname: Romagnolo fullname: Romagnolo, Béatrice email: beatrice.romagnolo@inserm.fr organization: Institut Cochin, Université Paris Descartes, Centre National de la Recherche Scientifique (CNRS), UMR8104, Institut National de la Sante et de la Recherche Médicale (INSERM), U1016
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26214133$$D View this record in MEDLINE/PubMed https://hal.inrae.fr/hal-02637789$$DView record in HAL
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Snippet	Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in... Here, we show that autophagy is activated in the intestinal epithelium in murine and human colorectal cancer and that the conditional inactivation of Atg7 in...
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SubjectTerms	13/1 13/105 13/2 13/21 13/31 13/51 14/28 38/23 38/32 38/39 38/61 631/67 631/80/39 64/60 Adenocarcinoma - genetics Adenocarcinoma - immunology Adenocarcinoma - microbiology Adenocarcinoma - pathology Adenocarcinoma - prevention & control Adenoma - genetics Adenoma - immunology Adenoma - microbiology Adenoma - pathology Adenoma - prevention & control AMP-Activated Protein Kinases - metabolism Animals Autophagy Autophagy (Cytology) Autophagy-Related Protein 7 Cancer Research CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism CD8-Positive T-Lymphocytes - microbiology Cell Biology Cell Cycle Checkpoints Cell Proliferation Cell Transformation, Neoplastic - genetics Cell Transformation, Neoplastic - immunology Cell Transformation, Neoplastic - metabolism Cell Transformation, Neoplastic - pathology Cellular proteins Colon - immunology Colon - metabolism Colon - microbiology Colon - pathology Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - genetics Colorectal Neoplasms - immunology Colorectal Neoplasms - microbiology Colorectal Neoplasms - pathology Colorectal Neoplasms - prevention & control Development and progression Developmental Biology Disease Models, Animal Dysbiosis Enzyme Activation Female Gene expression Genes, APC Genetic aspects Health aspects Host-Pathogen Interactions Humans Immune response Immunity, Mucosal Inactivation Life Sciences Male Mice, Inbred C57BL Mice, Knockout Microbiota - immunology Microtubule-Associated Proteins - deficiency Microtubule-Associated Proteins - genetics Properties Stem Cells Time Factors Tumor Burden Tumor Suppressor Protein p53 - metabolism Tumors Ubiquitin-Activating Enzymes - metabolism
Title	Intestinal inhibition of Atg7 prevents tumour initiation through a microbiome-influenced immune response and suppresses tumour growth
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