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Cancer Immunology Research
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MicroRNAs in Tumor Exosomes Drive Immune Escape in Melanoma

Virginie Vignard, Maureen Labbé, Nadège Marec, Gwennan André-Grégoire, Nicolas Jouand, Jean-François Fonteneau, Nathalie Labarrière and Delphine Fradin
Virginie Vignard
1CRCINA, INSERM, Université d'Angers, Université de Nantes, Nantes, France.
2CHU Nantes, Nantes, France.
3LabEx IGO “Immunotherapy, Graft, Oncology,” Nantes, France.
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Maureen Labbé
1CRCINA, INSERM, Université d'Angers, Université de Nantes, Nantes, France.
3LabEx IGO “Immunotherapy, Graft, Oncology,” Nantes, France.
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  • ORCID record for Maureen Labbé
Nadège Marec
4Plateforme CytoCell, SFR François Bonamy, Nantes, France.
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Gwennan André-Grégoire
5CRCINA, INSERM, CNRS, Université d'Angers, Université de Nantes, Nantes, France.
6Institut de Cancérologie de l'Ouest, Saint Herblain, France.
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Nicolas Jouand
4Plateforme CytoCell, SFR François Bonamy, Nantes, France.
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  • ORCID record for Nicolas Jouand
Jean-François Fonteneau
1CRCINA, INSERM, Université d'Angers, Université de Nantes, Nantes, France.
3LabEx IGO “Immunotherapy, Graft, Oncology,” Nantes, France.
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Nathalie Labarrière
1CRCINA, INSERM, Université d'Angers, Université de Nantes, Nantes, France.
3LabEx IGO “Immunotherapy, Graft, Oncology,” Nantes, France.
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  • ORCID record for Nathalie Labarrière
Delphine Fradin
1CRCINA, INSERM, Université d'Angers, Université de Nantes, Nantes, France.
3LabEx IGO “Immunotherapy, Graft, Oncology,” Nantes, France.
7Cancéropole Grand-Ouest, Réseau Epigénétique (RepiCGO), Nantes, France.
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  • ORCID record for Delphine Fradin
  • For correspondence: delphine.fradin@inserm.fr
DOI: 10.1158/2326-6066.CIR-19-0522 Published February 2020
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Abstract

MicroRNAs (miRNA), small noncoding RNAs that regulate gene expression, exist not only in cells but also in a variety of body fluids. These circulating miRNAs could enable intercellular communication. miRNAs are packaged in membrane-encapsulated vesicles, such as exosomes, or protected by RNA-binding proteins. Here, we report that miRNAs included in human melanoma exosomes regulate the tumor immune response. Using microscopy and flow cytometry, we demonstrate that CD8+ T cells internalize exosomes from different tumor types even if these cells do not internalize vesicles as readily as other immune cells. We explored the function of melanoma-derived exosomes in CD8+ T cells and showed that these exosomes downregulate T-cell responses through decreased T-cell receptor (TCR) signaling and diminished cytokine and granzyme B secretions. The result reduces the cells' cytotoxic activity. Using mimics, we found that miRNAs enriched in exosomes—such as Homo sapiens (hsa)-miR-3187-3p, hsa-miR-498, hsa-miR-122, hsa-miR149, and hsa-miR-181a/b—regulate TCR signaling and TNFα secretion. Our observations suggest that miRNAs in melanoma-derived exosomes aid tumor immune evasion and could be a therapeutic target.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Immunology Research Online (http://cancerimmunolres.aacrjournals.org/).

  • Cancer Immunol Res 2020;8:255–67

  • Received July 9, 2019.
  • Revision received October 14, 2019.
  • Accepted December 10, 2019.
  • Published first December 19, 2019.
  • ©2019 American Association for Cancer Research.
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Cancer Immunology Research: 8 (2)
February 2020
Volume 8, Issue 2
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MicroRNAs in Tumor Exosomes Drive Immune Escape in Melanoma
Virginie Vignard, Maureen Labbé, Nadège Marec, Gwennan André-Grégoire, Nicolas Jouand, Jean-François Fonteneau, Nathalie Labarrière and Delphine Fradin
Cancer Immunol Res February 1 2020 (8) (2) 255-267; DOI: 10.1158/2326-6066.CIR-19-0522

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MicroRNAs in Tumor Exosomes Drive Immune Escape in Melanoma
Virginie Vignard, Maureen Labbé, Nadège Marec, Gwennan André-Grégoire, Nicolas Jouand, Jean-François Fonteneau, Nathalie Labarrière and Delphine Fradin
Cancer Immunol Res February 1 2020 (8) (2) 255-267; DOI: 10.1158/2326-6066.CIR-19-0522
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