Cited by 340Cancer Cells and MetastasisRedox biology and oxidative stressCancer, Hypoxia, and Metabolism

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Oxidative stress promotes myofibroblast differentiation and tumour spreading

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Toullec, Aurore, Gerald, Damien, Despouy, Gilles, Bourachot, Brigitte, Cardon, Melissa, Lefort, Sylvain, Richardson, Marion, Rigaill, Guillem, Parrini, Maria‐Carla, Lucchesi, Carlo, Bellanger, Dorine, Stern, Marc‐Henri, Dubois, Thierry, Sastre‐Garau, Xavier, Delattre, Olivier, Vincent‐Salomon, Anne, Mechta‐Grigoriou, Fatima·2010·EMBO Molecular Medicine

DOI 10.1002/emmm.201000073PMC PMC3377319

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Abstract

JunD regulates genes involved in antioxidant defence. We took advantage of the chronic oxidative stress resulting from junD deletion to examine the role of reactive oxygen species (ROS) in tumour development. In a model of mammary carcinogenesis, junD inactivation increased tumour incidence and revealed an associated reactive stroma. junD-inactivation in the stroma was sufficient to shorten tumour-free survival rate and enhance metastatic spread. ROS promoted conversion of fibroblasts into highly migrating myofibroblasts through accumulation of the hypoxia-inducible factor (HIF)-1alpha transcription factor and the CXCL12 chemokine. Accordingly, treatment with an antioxidant reduced the levels of HIF and CXCL12 and numerous myofibroblast features. CXCL12 accumulated in the stroma of HER2-human breast adenocarcinomas. Moreover, HER2 tumours exhibited a high proportion of myofibroblasts, which was significantly correlated to nodal metastases. Interestingly, this subset of tumours exhibited a significant nuclear exclusion of JunD and revealed an associated oxido-reduction signature, further demonstrating the relevance of our findings in human cancers. Collectively, our data uncover a new mechanism by which oxidative stress increases the migratory properties of stromal fibroblasts, which in turn potentiate tumour dissemination.

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Authors: Toullec, A., Gerald, D., Despouy, G., Bourachot, B., Cardon, M., Lefort, S., Richardson, M., Rigaill, G., Parrini, M., Lucchesi, C., Bellanger, D., Stern, M., Dubois, T., Sastre‐Garau, X., Delattre, O., Vincent‐Salomon, A., & Mechta‐Grigoriou, F.
Affiliations: Inserm (FR)
Institut Curie (FR)
Corresponding author: Mechta‐Grigoriou, Fatima
ORCID: Despouy, Gilles
Bourachot, Brigitte
Lefort, Sylvain
Richardson, Marion
Rigaill, Guillem
Lucchesi, Carlo
Bellanger, Dorine
Stern, Marc‐Henri
Dubois, Thierry
Sastre‐Garau, Xavier
Delattre, Olivier
Vincent‐Salomon, Anne
Mechta‐Grigoriou, Fatima
Venue: EMBO Molecular Medicine
Publisher: Springer Science and Business Media LLC
Published: 2010-06-01
Volume: 2
Issue: 6
Pages: 211-230
ISSN: 1757-4676 (ISSN-L)
1757-4684
DOI: 10.1002/emmm.201000073
PMC: PMC3377319
OpenAlex: W2107028932
Cited by: 339
References: 91
Citations by year: 2026: 16 · 2025: 15 · 2024: 27 · 2023: 38 · 2022: 33 · 2021: 30 · 2020: 23 · 2019: 12 · 2018: 11 · 2017: 17 · 2016: 14 · 2015: 13 · 2014: 19 · 2013: 22 · 2012: 22
FWCI: 11.24
Type: journal article
Language: en
Open access: gold
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: EMBO Molecular Medicine (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion, cc-by-nc)
Funders: Institut National de la Santé et de la Recherche Médicale
Institut Curie
Fondation de France
Agence Nationale de la Recherche
French National Institut of Cancer
Association pour la Recherche contre le Cancer
Topics: Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Keywords: oxidative stress, JunD, myofibroblast differentiation, tumour metastasis, reactive oxygen species, mammary carcinogenesis, stromal fibroblasts, HIF-1α, CXCL12, HER2-positive breast cancer, antioxidant therapy, tumor microenvironment, hypoxia
MeSH terms: Animals, Breast Neoplasms, Cell Differentiation, Cell Line, Female, Fibroblasts, Histocytochemistry, Humans, Immunohistochemistry, Locomotion, Microscopy, Microscopy, Fluorescence, Models, Biological, Neoplasm Metastasis, Proto-Oncogene Proteins, Mammary Neoplasms, Animal, Incidence, Survival Analysis, Proto-Oncogene Proteins c-jun, Reactive Oxygen Species, Mice, Knockout, Oxidative Stress, Mice, Hypoxia-Inducible Factor 1, alpha Subunit, Chemokine CXCL12

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Oxidative stress promotes myofibroblast differentiation and tumour spreading

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