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CD4 T cells and neutrophils contribute to epithelial-mesenchymal transition in breast cancer

Amélien Sanlaville, Aurélien Voissière, Dominique Poujol, View ORCID ProfileMargaux Hubert, Suzanne André, Clémence Perret, View ORCID ProfileJean-Philippe Foy, Nadège Goutagny, Marine Malfroy, Isabelle Durand, Marie Châlons-Cottavoz, View ORCID ProfileJenny Valladeau-Guilemond, View ORCID ProfilePierre Saintigny, Alain Puisieux, View ORCID ProfileChristophe Caux, View ORCID ProfileMarie-Cécile Michallet, View ORCID ProfileIsabelle Puisieux, View ORCID ProfileNathalie Bendriss-Vermare
doi: https://doi.org/10.1101/2023.02.15.528594
Amélien Sanlaville
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Aurélien Voissière
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Dominique Poujol
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Margaux Hubert
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
3Lyon Immunotherapy of Cancer Laboratory (LICL), Lyon, France
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  • ORCID record for Margaux Hubert
Suzanne André
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Clémence Perret
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Jean-Philippe Foy
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
4Department of Translational Research and Innovation, Centre Léon Bérard, Lyon, France
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Nadège Goutagny
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Marine Malfroy
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Isabelle Durand
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
5Cytometry platform, Cancer Research Center of Lyon, Lyon, France
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Marie Châlons-Cottavoz
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
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Jenny Valladeau-Guilemond
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Pierre Saintigny
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
4Department of Translational Research and Innovation, Centre Léon Bérard, Lyon, France
6Department of Medical Oncology, Centre Léon Bérard, Lyon, France
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Alain Puisieux
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
7Institut Curie, PSL Research University, Paris, France
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Christophe Caux
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
3Lyon Immunotherapy of Cancer Laboratory (LICL), Lyon, France
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Marie-Cécile Michallet
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Isabelle Puisieux
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
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Nathalie Bendriss-Vermare
1Université de Lyon, Université Claude Bernard Lyon 1, INSERM 1052, CNRS 5286, Centre Léon Bérard, Cancer Research Center of Lyon, Institut Convergence Plascan, Lyon, 69008, France
2LabEx DEVweCAN, Université de Lyon, F-69000 Lyon, France
3Lyon Immunotherapy of Cancer Laboratory (LICL), Lyon, France
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  • For correspondence: nathalie.bendriss-vermare@lyon.unicancer.fr
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ABSTRACT

Epithelial-mesenchymal transition (EMT) is a central oncogenic mechanism, contributing both to transformation and metastatic dissemination. Inflammation and innate immune cells are known to favor EMT induction, but the role of adaptive immunity still remains unclear. Using an original murine mammary tumor model in immune cell subpopulation depletion experiments, we demonstrated that tumor cells maintain their epithelial phenotype in mice deficient for adaptive immune response, but undergo EMT in the presence of T-cells. This phenotypic conversion involves the major contribution of CD4 T cells, but not CD8 T cells nor B cells, undoubtedly demonstrating the pro-EMT role of CD4 T cells specifically among adaptive immune cells. Moreover, combined intra-tumor immune infiltrate and transcriptomic analyses of murine mammary tumors with various EMT phenotype revealed an inverse correlation between mesenchymal tumor cell and intratumoral neutrophil proportions, due to the reduced ability of mesenchymal cells to recruit neutrophils. Last, selective in vivo depletion of neutrophils and transcriptomic analysis of human breast tumor cohorts demonstrated the pro-EMT role of neutrophils and suggest a cooperation with CD4 T cells in EMT promotion. Collectively, our data highlight a novel mechanism of EMT regulation by both innate and adaptive immune compartments.

Competing Interest Statement

The authors have declared no competing interest.

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Posted February 15, 2023.
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CD4 T cells and neutrophils contribute to epithelial-mesenchymal transition in breast cancer
Amélien Sanlaville, Aurélien Voissière, Dominique Poujol, Margaux Hubert, Suzanne André, Clémence Perret, Jean-Philippe Foy, Nadège Goutagny, Marine Malfroy, Isabelle Durand, Marie Châlons-Cottavoz, Jenny Valladeau-Guilemond, Pierre Saintigny, Alain Puisieux, Christophe Caux, Marie-Cécile Michallet, Isabelle Puisieux, Nathalie Bendriss-Vermare
bioRxiv 2023.02.15.528594; doi: https://doi.org/10.1101/2023.02.15.528594
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CD4 T cells and neutrophils contribute to epithelial-mesenchymal transition in breast cancer
Amélien Sanlaville, Aurélien Voissière, Dominique Poujol, Margaux Hubert, Suzanne André, Clémence Perret, Jean-Philippe Foy, Nadège Goutagny, Marine Malfroy, Isabelle Durand, Marie Châlons-Cottavoz, Jenny Valladeau-Guilemond, Pierre Saintigny, Alain Puisieux, Christophe Caux, Marie-Cécile Michallet, Isabelle Puisieux, Nathalie Bendriss-Vermare
bioRxiv 2023.02.15.528594; doi: https://doi.org/10.1101/2023.02.15.528594

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