STING protects breast cancer cells from intrinsic and genotoxic-induced DNA instability via a non-canonical, cell-autonomous pathway

STING (Stimulator of Interferon Genes) is an endoplasmic reticulum-anchored adaptor of the innate immunity best known to trigger pro-inflammatory cytokine expression in response to pathogen infection. In cancer, this canonical pathway can be activated by intrinsic or drug-induced genomic instability...

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Veröffentlicht in:Oncogene Jg. 40; H. 49; S. 6627 - 6640
Hauptverfasser: Cheradame, Laura, Guerrera, Ida Chiara, Gaston, Julie, Schmitt, Alain, Jung, Vincent, Goudin, Nicolas, Pouillard, Marion, Radosevic-Robin, Nina, Modesti, Mauro, Judde, Jean-Gabriel, Cairo, Stefano, Goffin, Vincent
Format: Journal Article
Sprache:Englisch
Veröffentlicht: London Nature Publishing Group UK 09.12.2021
Nature Publishing Group
Nature Publishing Group [1987-....]
Schlagworte:
13/51
13/89
14/1
14/28
631/337/1427
631/67/1347
631/80/2373
82/29
82/58
96/109
96/21
Animals
Antitumor activity
Apoptosis
Biomarkers, Tumor - genetics
Biomarkers, Tumor - metabolism
Breast cancer
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Breast Neoplasms - prevention & control
Cancer
Cancer cells
Cell Biology
Cell culture
Cell Proliferation
Cell survival
Chemotherapy
Deoxyribonucleic acid
Development and progression
DNA
DNA Damage
DNA-dependent protein kinase
Endoplasmic reticulum
Female
Gene Expression Regulation, Neoplastic
Genetic aspects
Genomic Instability
Genotoxicity
Health aspects
Human Genetics
Humans
Immune response
Immunosurveillance
Inflammation
Innate immunity
Interferon
Internal Medicine
Life Sciences
Medicine
Medicine & Public Health
Membrane proteins
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mice
Microsatellite instability
Neoplasm Recurrence, Local - genetics
Neoplasm Recurrence, Local - metabolism
Neoplasm Recurrence, Local - pathology
Neoplasm Recurrence, Local - prevention & control
Nucleotidyltransferases - genetics
Nucleotidyltransferases - metabolism
Oncology
Oncology, Experimental
Ovarian cancer
Prognosis
Survival Rate
Tumor cell lines
Tumor Cells, Cultured
Tumors
Xenograft Model Antitumor Assays
France
Cellular imaging
Breast cancer
DNA damage and repair
ISSN:0950-9232, 1476-5594, 1476-5594
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Abstract STING (Stimulator of Interferon Genes) is an endoplasmic reticulum-anchored adaptor of the innate immunity best known to trigger pro-inflammatory cytokine expression in response to pathogen infection. In cancer, this canonical pathway can be activated by intrinsic or drug-induced genomic instability, potentiating antitumor immune responses. Here we report that STING downregulation decreases cell survival and increases sensitivity to genotoxic treatment in a panel of breast cancer cell lines in a cell-autonomous manner. STING silencing impaired DNA Damage Response (53BP1) foci formation and increased DNA break accumulation. These newly identified properties were found to be independent of STING partner cGAS and of its canonical pro-inflammatory pathway. STING was shown to partially localize at the inner nuclear membrane in a variety of breast cancer cell models and clinical tumor samples. Interactomics analysis of nuclear STING identified several proteins of the DNA Damage Response, including the three proteins of the DNA-PK complex, further supporting a role of STING in the regulation of genomic stability. In breast and ovarian cancer patients that received adjuvant chemotherapy, high STING expression is associated with increased risk of relapse. In summary, this study highlights an alternative, non-canonical tumor-promoting role of STING that opposes its well-documented function in tumor immunosurveillance.
AbstractList STING (Stimulator of Interferon Genes) is an endoplasmic reticulum-anchored adaptor of the innate immunity best known to trigger pro-inflammatory cytokine expression in response to pathogen infection. In cancer, this canonical pathway can be activated by intrinsic or drug-induced genomic instability, potentiating antitumor immune responses. Here we report that STING downregulation decreases cell survival and increases sensitivity to genotoxic treatment in a panel of breast cancer cell lines in a cell-autonomous manner. STING silencing impaired DNA Damage Response (53BP1) foci formation and increased DNA break accumulation. These newly identified properties were found to be independent of STING partner cGAS and of its canonical pro-inflammatory pathway. STING was shown to partially localize at the inner nuclear membrane in a variety of breast cancer cell models and clinical tumor samples. Interactomics analysis of nuclear STING identified several proteins of the DNA Damage Response, including the three proteins of the DNA-PK complex, further supporting a role of STING in the regulation of genomic stability. In breast and ovarian cancer patients that received adjuvant chemotherapy, high STING expression is associated with increased risk of relapse. In summary, this study highlights an alternative, non-canonical tumor-promoting role of STING that opposes its well-documented function in tumor immunosurveillance.
STING (Stimulator of Interferon Genes) is an endoplasmic reticulum-anchored adaptor of the innate immunity best known to trigger pro-inflammatory cytokine expression in response to pathogen infection. In cancer, this canonical pathway can be activated by intrinsic or drug-induced genomic instability, potentiating antitumor immune responses. Here we report that STING downregulation decreases cell survival and increases sensitivity to genotoxic treatment in a panel of breast cancer cell lines in a cell-autonomous manner. STING silencing impaired DNA Damage Response (53BP1) foci formation and increased DNA break accumulation. These newly identified properties were found to be independent of STING partner cGAS and of its canonical pro-inflammatory pathway. STING was shown to partially localize at the inner nuclear membrane in a variety of breast cancer cell models and clinical tumor samples. Interactomics analysis of nuclear STING identified several proteins of the DNA Damage Response, including the three proteins of the DNA-PK complex, further supporting a role of STING in the regulation of genomic stability. In breast and ovarian cancer patients that received adjuvant chemotherapy, high STING expression is associated with increased risk of relapse. In summary, this study highlights an alternative, non-canonical tumor-promoting role of STING that opposes its well-documented function in tumor immunosurveillance.STING (Stimulator of Interferon Genes) is an endoplasmic reticulum-anchored adaptor of the innate immunity best known to trigger pro-inflammatory cytokine expression in response to pathogen infection. In cancer, this canonical pathway can be activated by intrinsic or drug-induced genomic instability, potentiating antitumor immune responses. Here we report that STING downregulation decreases cell survival and increases sensitivity to genotoxic treatment in a panel of breast cancer cell lines in a cell-autonomous manner. STING silencing impaired DNA Damage Response (53BP1) foci formation and increased DNA break accumulation. These newly identified properties were found to be independent of STING partner cGAS and of its canonical pro-inflammatory pathway. STING was shown to partially localize at the inner nuclear membrane in a variety of breast cancer cell models and clinical tumor samples. Interactomics analysis of nuclear STING identified several proteins of the DNA Damage Response, including the three proteins of the DNA-PK complex, further supporting a role of STING in the regulation of genomic stability. In breast and ovarian cancer patients that received adjuvant chemotherapy, high STING expression is associated with increased risk of relapse. In summary, this study highlights an alternative, non-canonical tumor-promoting role of STING that opposes its well-documented function in tumor immunosurveillance.
Audience Academic
Author Cheradame, Laura
Guerrera, Ida Chiara
Jung, Vincent
Gaston, Julie
Goffin, Vincent
Cairo, Stefano
Goudin, Nicolas
Modesti, Mauro
Judde, Jean-Gabriel
Schmitt, Alain
Pouillard, Marion
Radosevic-Robin, Nina
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  givenname: Laura
  orcidid: 0000-0002-8369-9923
  surname: Cheradame
  fullname: Cheradame, Laura
  organization: INSERM U1151, CNRS UMR8253, Institut Necker Enfants Malades (INEM), Université de Paris, XenTech
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  givenname: Ida Chiara
  orcidid: 0000-0002-4832-6793
  surname: Guerrera
  fullname: Guerrera, Ida Chiara
  organization: Proteomics platform Necker, Université de Paris - Structure Fédérative de Recherche Necker, INSERM US24/CNRS UMS3633
– sequence: 3
  givenname: Julie
  orcidid: 0000-0002-2660-1651
  surname: Gaston
  fullname: Gaston, Julie
  organization: INSERM U1151, CNRS UMR8253, Institut Necker Enfants Malades (INEM), Université de Paris, XenTech, Yubsis, 4 rue Pierre Fontaine
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  givenname: Alain
  surname: Schmitt
  fullname: Schmitt, Alain
  organization: Université de Paris, Institut Cochin, INSERM, CNRS
– sequence: 5
  givenname: Vincent
  orcidid: 0000-0003-0530-1737
  surname: Jung
  fullname: Jung, Vincent
  organization: Proteomics platform Necker, Université de Paris - Structure Fédérative de Recherche Necker, INSERM US24/CNRS UMS3633
– sequence: 6
  givenname: Nicolas
  orcidid: 0000-0002-3967-4016
  surname: Goudin
  fullname: Goudin, Nicolas
  organization: Inserm US24 – CNRS UMS 3633, Necker Bio-Image Analysis
– sequence: 7
  givenname: Marion
  surname: Pouillard
  fullname: Pouillard, Marion
  organization: INSERM U1151, CNRS UMR8253, Institut Necker Enfants Malades (INEM), Université de Paris
– sequence: 8
  givenname: Nina
  orcidid: 0000-0002-1633-8730
  surname: Radosevic-Robin
  fullname: Radosevic-Robin, Nina
  organization: U1240 INSERM/University Clermont Auvergne, Centre Jean Perrin, Department of Pathology
– sequence: 9
  givenname: Mauro
  orcidid: 0000-0002-4964-331X
  surname: Modesti
  fullname: Modesti, Mauro
  organization: Cancer Research Center of Marseille, CNRS UMR7258, Inserm U1068, Institut Paoli-Calmettes, Aix-Marseille Université
– sequence: 10
  givenname: Jean-Gabriel
  surname: Judde
  fullname: Judde, Jean-Gabriel
  organization: XenTech
– sequence: 11
  givenname: Stefano
  orcidid: 0000-0002-4725-5970
  surname: Cairo
  fullname: Cairo, Stefano
  organization: XenTech
– sequence: 12
  givenname: Vincent
  orcidid: 0000-0002-8021-3086
  surname: Goffin
  fullname: Goffin, Vincent
  email: vincent.goffin@inserm.fr
  organization: INSERM U1151, CNRS UMR8253, Institut Necker Enfants Malades (INEM), Université de Paris
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34625708$$D View this record in MEDLINE/PubMed
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The Author(s), under exclusive licence to Springer Nature Limited 2021.
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Copyright_xml – notice: The Author(s), under exclusive licence to Springer Nature Limited 2021
– notice: 2021. The Author(s), under exclusive licence to Springer Nature Limited.
– notice: COPYRIGHT 2021 Nature Publishing Group
– notice: The Author(s), under exclusive licence to Springer Nature Limited 2021.
– notice: Distributed under a Creative Commons Attribution 4.0 International License
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ISSN 0950-9232
1476-5594
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IsPeerReviewed true
IsScholarly true
Issue 49
Keywords Cellular imaging
Breast cancer
DNA damage and repair
Language English
License 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
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Snippet STING (Stimulator of Interferon Genes) is an endoplasmic reticulum-anchored adaptor of the innate immunity best known to trigger pro-inflammatory cytokine...
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StartPage 6627
SubjectTerms 13/51
13/89
14/1
14/28
631/337/1427
631/67/1347
631/80/2373
82/29
82/58
96/109
96/21
Animals
Antitumor activity
Apoptosis
Biomarkers, Tumor - genetics
Biomarkers, Tumor - metabolism
Breast cancer
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Breast Neoplasms - prevention & control
Cancer
Cancer cells
Cell Biology
Cell culture
Cell Proliferation
Cell survival
Chemotherapy
Deoxyribonucleic acid
Development and progression
DNA
DNA Damage
DNA-dependent protein kinase
Endoplasmic reticulum
Female
Gene Expression Regulation, Neoplastic
Genetic aspects
Genomic Instability
Genotoxicity
Health aspects
Human Genetics
Humans
Immune response
Immunosurveillance
Inflammation
Innate immunity
Interferon
Internal Medicine
Life Sciences
Medicine
Medicine & Public Health
Membrane proteins
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mice
Microsatellite instability
Neoplasm Recurrence, Local - genetics
Neoplasm Recurrence, Local - metabolism
Neoplasm Recurrence, Local - pathology
Neoplasm Recurrence, Local - prevention & control
Nucleotidyltransferases - genetics
Nucleotidyltransferases - metabolism
Oncology
Oncology, Experimental
Ovarian cancer
Prognosis
Survival Rate
Tumor cell lines
Tumor Cells, Cultured
Tumors
Xenograft Model Antitumor Assays
Title STING protects breast cancer cells from intrinsic and genotoxic-induced DNA instability via a non-canonical, cell-autonomous pathway
URI https://link.springer.com/article/10.1038/s41388-021-02037-4
https://www.ncbi.nlm.nih.gov/pubmed/34625708
https://www.proquest.com/docview/2608261136
https://www.proquest.com/docview/2580701168
https://amu.hal.science/hal-03438625
Volume 40
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