Cited by 1,705Cancer Immunotherapy and BiomarkersImmune cells in cancerTGF-β signaling in diseases

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Fibroblast Heterogeneity and Immunosuppressive Environment in Human Breast Cancer

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Costa, Ana, Kieffer, Yann, Scholer-Dahirel, Alix, Pelon, Floriane, Bourachot, Brigitte, Cardon, Melissa, Sirven, Philemon, Magagna, Ilaria, Fuhrmann, Laetitia, Bernard, Charles, Bonneau, Claire, Kondratova, Maria, Kuperstein, Inna, Zinovyev, Andrei, Givel, Anne-Marie, Parrini, Maria-Carla, Soumelis, Vassili, Vincent-Salomon, Anne, Mechta-Grigoriou, Fatima·2018·Cancer Cell

DOI 10.1016/j.ccell.2018.01.011

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Abstract

Carcinoma-associated fibroblasts (CAF) are key players in the tumor microenvironment. Here, we characterize four CAF subsets in breast cancer with distinct properties and levels of activation. Two myofibroblastic subsets (CAF-S1, CAF-S4) accumulate differentially in triple-negative breast cancers (TNBC). CAF-S1 fibroblasts promote an immunosuppressive environment through a multi-step mechanism. By secreting CXCL12, CAF-S1 attracts CD4+CD25+ T lymphocytes and retains them by OX40L, PD-L2, and JAM2. Moreover, CAF-S1 increases T lymphocyte survival and promotes their differentiation into CD25 High FOXP3 High, through B7H3, CD73, and DPP4. Finally, in contrast to CAF-S4, CAF-S1 enhances the regulatory T cell capacity to inhibit T effector proliferation. These data are consistent with FOXP3+ T lymphocyte accumulation in CAF-S1-enriched TNBC and show how a CAF subset contributes to immunosuppression.

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Background
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Background
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Background
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BackgroundMethodResultInfluential
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Heterogeneity in Cancer
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Background
Lobular Breast Cancer: Histomorphology and Different Concepts of a Special Spectrum of Tumors
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Distinct fibroblast functional states drive clinical outcomes in ovarian cancer and are regulated by TCF21
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“…have suggested that in ﬂ ammatory cancer-associated ﬁ broblasts (iCAFs) have relatively high expression of pyruvate carboxylase genes 13 and can regulate the TME by secreting cytokines such as CXCL12, 16,17 which was shown to be an important chemokine in recruiting Tregs in our previous results.”
Artemisinin derivatives inactivate cancer-associated fibroblasts through suppressing TGF-β signaling in breast cancer
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“Prominently, different subtypes of CAFs that exhibit distinct characteristics and activity levels have been identified in breast cancer (88) and PDAC (89).”
Background
Heterogeneity of human prostate carcinoma-associated fibroblasts implicates a role for subpopulations in myeloid cell recruitment
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FAP‐Targeted Photodynamic Therapy Mediated by Ferritin Nanoparticles Elicits an Immune Response against Cancer Cells and Cancer Associated Fibroblasts
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“However, in other solid tumors such as those of the head and neck, breast, and pancreas, recent studies show that CAFs contained in one tumor were heterogeneous, presenting different gene expression patterns and a variety of functions [21, 70, 71].”
Background
Identifying key questions in the ecology and evolution of cancer
Dujon, A. M., Aktipis, A., Alix‐Panabières, C., Amend, S. R., Boddy, A. M., Brown, J. S., Capp, J., DeGregori, J. V., Ewald, P. W., Gatenby, R. A., et al. (2020) · Evolutionary Applications · doi:10.1111/eva.13190 · Cited by 93
The Multifaceted Nature of Tumor Microenvironment in Breast Carcinomas
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Landscape of cancer-associated fibroblasts identifies the secreted biglycan as a protumor and immunosuppressive factor in triple-negative breast cancer
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BackgroundInfluential
Gut complement induced by the microbiota combats pathogens and spares commensals
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COL11A1 activates cancer-associated fibroblasts by modulating TGF-β3 through the NF-κB/IGFBP2 axis in ovarian cancer cells
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Background
STING and IRF3 in stromal fibroblasts enable sensing of genomic stress in cancer cells to undermine oncolytic viral therapy
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Single‐Cell Transcriptomic Analysis of Primary and Metastatic Tumor Ecosystems in Esophageal Squamous Cell Carcinoma
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Role of Hypoxic Stress in Regulating Tumor Immunogenicity, Resistance and Plasticity
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Key Players of the Immunosuppressive Tumor Microenvironment and Emerging Therapeutic Strategies
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Signaling pathways in the regulation of cancer stem cells and associated targeted therapy
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Spatial dissection of tumour microenvironments in gastric cancers reveals the immunosuppressive crosstalk between CCL2+ fibroblasts and STAT3 -activated macrophages
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“As previously proposed, 27 28 the depletion of both CD4+ and CD8+ T cells in fibrotic GCs could be mediated by interactions between fibroblasts and other types of immune or TME cells.”
Metabolism in the Tumor Microenvironment
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Macrophages orchestrate the expansion of a proangiogenic perivascular niche during cancer progression
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“, promoting an immunosuppressive microenvironment) and localization inside the tumor [63], illustrating CAF heterogeneity and offering an explanation to their conflicting role.”
Background
CCL18 signaling from tumor-associated macrophages activates fibroblasts to adopt a chemoresistance-inducing phenotype
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“DISCUSSION CAFs are one of the most abundant stromal cells in the tumor microenvironment and have prominent roles in cancer progression, including remodeling the ECM for tumor invasion [34], providing a niche to support chemoresistance [3], secreting cytokines to promote angiogenesis [1] and inducing immunosuppression…”
Background
Systematic dissection of tumor-normal single-cell ecosystems across a thousand tumors of 30 cancer types
Kang, J., Lee, J. H., Cha, H., An, J., Kwon, J., Lee, S., Kim, S., Baykan, M. Y., Kim, S. Y., An, D., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-48310-4 · Cited by 90
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BackgroundInfluential
Tumor-derived osteopontin drives the resident fibroblast to myofibroblast differentiation through Twist1 to promote breast cancer progression
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Tertiary Lymphoid Structure-B Cells Narrow Regulatory T Cells Impact in Lung Cancer Patients
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Deep Learning-Based Classification for Melanoma Detection Using XceptionNet
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Background
Transcriptomic and immunophenotypic profiling reveals molecular and immunological hallmarks of colorectal cancer tumourigenesis
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“CAFs have been proved to be closely associated with the immunosuppressive functional state of Tregs 42 .”
The Complex Interaction between the Tumor Micro-Environment and Immune Checkpoints in Breast Cancer
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“TNBC exhibit CAF subsets, ↑CAF-S1→ ↑T Lymphocyte survival→ ↑Treg→ Ø T effector proliferation→ Immunosuppression Female BC patient cohort (Luminal, HER2 and TN subtype tissues) FC [171]”
Background
Relationship between podoplanin-expressing cancer-associated fibroblasts and the immune microenvironment of early lung squamous cell carcinoma
Suzuki, J., Aokage, K., Neri, S., Sakai, T., Hashimoto, H., Su, Y., Yamazaki, S., Nakamura, H., Tane, K., Miyoshi, T., et al. (2020) · Lung Cancer · doi:10.1016/j.lungcan.2020.12.020 · Cited by 83

Authors: Costa, A., Kieffer, Y., Scholer-Dahirel, A., Pelon, F., Bourachot, B., Cardon, M., Sirven, P., Magagna, I., Fuhrmann, L., Bernard, C., Bonneau, C., Kondratova, M., Kuperstein, I., Zinovyev, A., Givel, A.-M., Parrini, M.-C., Soumelis, V., Vincent-Salomon, A., & Mechta-Grigoriou, F.
Affiliations: Inserm (FR)
Institut Curie (FR)
ORCID: Costa, Ana
Kieffer, Yann
Pelon, Floriane
Bourachot, Brigitte
Magagna, Ilaria
Fuhrmann, Laetitia
Bernard, Charles
Bonneau, Claire
Kuperstein, Inna
Zinovyev, Andrei
Soumelis, Vassili
Mechta-Grigoriou, Fatima
Venue: Cancer Cell
Publisher: Elsevier BV
Published: 2018-03
Volume: 33
Issue: 3
Pages: 463-479.e10
ISSN: 1535-6108 (ISSN-L)
DOI: 10.1016/j.ccell.2018.01.011
OpenAlex: W2786031287
Cited by: 1,705
References: 74
Citations by year: 2026: 165 · 2025: 202 · 2024: 264 · 2023: 255 · 2022: 236 · 2021: 262 · 2020: 173 · 2019: 99 · 2018: 47
FWCI: 54.69
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 376 d)
Locations: Cancer Cell (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Funders: Fondation de France
Fondation Pierre-Gilles de Gennes
Institut National Du Cancer (INCa-DGOS-9963)
Fondation pour la Recherche Médicale
SiRIC-Curie program (INCa-DGOS-4654)
Institut National de la Santé et de la Recherche Médicale
Institut Curie
Ligue Nationale Contre le Cancer
ICGex (ANR-10-EQPX-03)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
Keywords: cancer-associated fibroblasts, breast cancer, triple-negative breast cancer, tumor microenvironment, immunosuppression, regulatory T cells, CXCL12, OX40L, PD-L2, JAM2, B7-H3, CD73, dipeptidyl peptidase IV, Foxp3, CD4+ T cells, T cell survival, fibroblast heterogeneity
MeSH terms: Breast Neoplasms, Cell Differentiation, Fibroblasts, Humans, Immune Tolerance, Lymphocyte Activation, Lymphocytes, Tumor-Infiltrating, Cell Proliferation, T-Lymphocytes, Regulatory, Forkhead Transcription Factors, Tumor Microenvironment

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Fibroblast Heterogeneity and Immunosuppressive Environment in Human Breast Cancer

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