Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathway

Abstract During obesity, macrophages infiltrate the breast tissue leading to low‐grade chronic inflammation, a factor considered responsible for the higher risk of breast cancer associated with obesity. Here, we formally demonstrate that breast epithelial cells acquire malignant properties when expo...

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Main Authors: Ewa Wilcz‐Villega, Edward Carter, Alastair Ironside, Ruoyan Xu, Isabella Mataloni, Julie Holdsworth, William Jones, Rocío Moreno Béjar, Lukas Uhlik, Robert B Bentham, Susana A Godinho, Jesmond Dalli, Richard Grose, Gyorgy Szabadkai, Louise Jones, Kairbaan Hodivala‐Dilke, Katiuscia Bianchi
Format: Article
Language:English
Published: Springer Nature 2020-01-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201910491
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author Ewa Wilcz‐Villega
Edward Carter
Alastair Ironside
Ruoyan Xu
Isabella Mataloni
Julie Holdsworth
William Jones
Rocío Moreno Béjar
Lukas Uhlik
Robert B Bentham
Susana A Godinho
Jesmond Dalli
Richard Grose
Gyorgy Szabadkai
Louise Jones
Kairbaan Hodivala‐Dilke
Katiuscia Bianchi
author_facet Ewa Wilcz‐Villega
Edward Carter
Alastair Ironside
Ruoyan Xu
Isabella Mataloni
Julie Holdsworth
William Jones
Rocío Moreno Béjar
Lukas Uhlik
Robert B Bentham
Susana A Godinho
Jesmond Dalli
Richard Grose
Gyorgy Szabadkai
Louise Jones
Kairbaan Hodivala‐Dilke
Katiuscia Bianchi
author_sort Ewa Wilcz‐Villega
collection DOAJ
description Abstract During obesity, macrophages infiltrate the breast tissue leading to low‐grade chronic inflammation, a factor considered responsible for the higher risk of breast cancer associated with obesity. Here, we formally demonstrate that breast epithelial cells acquire malignant properties when exposed to medium conditioned by macrophages derived from human healthy donors. These effects were mediated by the breast cancer oncogene IKKε and its downstream target—the serine biosynthesis pathway as demonstrated by genetic or pharmacological tools. Furthermore, amlexanox, an FDA‐approved drug targeting IKKε and its homologue TBK1, delayed in vivo tumour formation in a combined genetic mouse model of breast cancer and high‐fat diet‐induced obesity/inflammation. Finally, in human breast cancer tissues, we validated the link between inflammation–IKKε and alteration of cellular metabolism. Altogether, we identified a pathway connecting obesity‐driven inflammation to breast cancer and a potential therapeutic strategy to reduce the risk of breast cancer associated with obesity.
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issn 1757-4676
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language English
publishDate 2020-01-01
publisher Springer Nature
record_format Article
series EMBO Molecular Medicine
spelling doaj-art-3d45047ea6d84002b19ab4d66c3f95362025-08-20T03:05:55ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842020-01-0112212010.15252/emmm.201910491Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathwayEwa Wilcz‐Villega0Edward Carter1Alastair Ironside2Ruoyan Xu3Isabella Mataloni4Julie Holdsworth5William Jones6Rocío Moreno Béjar7Lukas Uhlik8Robert B Bentham9Susana A Godinho10Jesmond Dalli11Richard Grose12Gyorgy Szabadkai13Louise Jones14Kairbaan Hodivala‐Dilke15Katiuscia Bianchi16Centre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Tumour Biology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Tumour Biology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Tumour Biology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonDepartment of Cell and Developmental Biology, Consortium for Mitochondrial Research, University College LondonCentre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonLipid Mediator Unit, Biochemical Pharmacology, William Harvey Research Institute, Barts and the London School of Medicine, Queen Mary University of LondonCentre for Tumour Biology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonDepartment of Cell and Developmental Biology, Consortium for Mitochondrial Research, University College LondonCentre for Tumour Biology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Tumour Biology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonCentre for Molecular Oncology, Barts Cancer Institute, John Vane Science Centre, Queen Mary University of LondonAbstract During obesity, macrophages infiltrate the breast tissue leading to low‐grade chronic inflammation, a factor considered responsible for the higher risk of breast cancer associated with obesity. Here, we formally demonstrate that breast epithelial cells acquire malignant properties when exposed to medium conditioned by macrophages derived from human healthy donors. These effects were mediated by the breast cancer oncogene IKKε and its downstream target—the serine biosynthesis pathway as demonstrated by genetic or pharmacological tools. Furthermore, amlexanox, an FDA‐approved drug targeting IKKε and its homologue TBK1, delayed in vivo tumour formation in a combined genetic mouse model of breast cancer and high‐fat diet‐induced obesity/inflammation. Finally, in human breast cancer tissues, we validated the link between inflammation–IKKε and alteration of cellular metabolism. Altogether, we identified a pathway connecting obesity‐driven inflammation to breast cancer and a potential therapeutic strategy to reduce the risk of breast cancer associated with obesity.https://doi.org/10.15252/emmm.201910491inflammationmacrophagesmalignant transformationobesitytumour metabolism
spellingShingle Ewa Wilcz‐Villega
Edward Carter
Alastair Ironside
Ruoyan Xu
Isabella Mataloni
Julie Holdsworth
William Jones
Rocío Moreno Béjar
Lukas Uhlik
Robert B Bentham
Susana A Godinho
Jesmond Dalli
Richard Grose
Gyorgy Szabadkai
Louise Jones
Kairbaan Hodivala‐Dilke
Katiuscia Bianchi
Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathway
EMBO Molecular Medicine
inflammation
macrophages
malignant transformation
obesity
tumour metabolism
title Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathway
title_full Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathway
title_fullStr Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathway
title_full_unstemmed Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathway
title_short Macrophages induce malignant traits in mammary epithelium via IKKε/TBK1 kinases and the serine biosynthesis pathway
title_sort macrophages induce malignant traits in mammary epithelium via ikkε tbk1 kinases and the serine biosynthesis pathway
topic inflammation
macrophages
malignant transformation
obesity
tumour metabolism
url https://doi.org/10.15252/emmm.201910491
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