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Oncolytic attenuated measles virus encoding NY-ESO-1 induces HLA I and II presentation of this tumor antigen by melanoma and dendritic cells

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Abstract

Antitumor virotherapy stimulates the antitumor immune response during tumor cell lysis induced by oncolytic viruses (OVs). OV can be modified to express additional transgenes that enhance their therapeutic potential. In this study, we armed the spontaneously oncolytic Schwarz strain of measles viruses (MVs) with the gene encoding the cancer/testis antigen NY-ESO-1 to obtain MVny. We compared MV and MVny oncolytic activity and ability to induce NY-ESO-1 expression in six human melanoma cell lines. After MVny infection, we measured the capacity of melanoma cells to present NY-ESO-1 peptides to CD4 + and CD8 + T cell clones specific for this antigen. We assessed the ability of MVny to induce NY-ESO-1 expression and presentation in monocyte-derived dendritic cells (DCs). Our results show that MVny and MV oncolytic activity are similar with a faster cell lysis induced by MVny. We also observed that melanoma cell lines and DC expressed the NY-ESO-1 protein after MVny infection. In addition, MVny-infected melanoma cells and DCs were able to stimulate NY-ESO-1-specific CD4 + and CD8 + T cells. Finally, MVny was able to induce DC maturation. Altogether, these results show that MVny could be an interesting candidate to stimulate NY-ESO-1-specific T cells in melanoma patients with NY-ESO-1-expressing tumor cells.

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Data availability statement

The data that support the findings of this study are available from the corresponding author (jean-francois.fonteneau@inserm.fr) upon reasonable request.

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Acknowledgements

We thank Philippe Hulin and the cellular and tissular core facility of Nantes University (MicroPiCell) for their expertise in video microscopy. We thank Nicolas Jouand and the core facility of flow cytometry from Nantes University (Cytocell).

Funding

This work was supported by “La Ligue Régionale Grand Ouest contre le Cancer” (CD16, CD22, CD44, CD49, CD72, CD79 and CD85), “l’association ARSMESO44”, “la Fondation ARC (PJA 20191209661)”, “l’Agence Nationale pour la Recherche (ANR-16-CE18-0016)”, and “LabEX IGO” program supported by the National Research Agency via the investment of the future program ANR-11-LABX-0016–01”.

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Author notes

  1. MG and MI equally contributed to this work.

Authors and Affiliations

  1. Nantes Université, Inserm UMR 1307, CNRS UMR 6075, Université d’Angers, CRCI2NA, F-44000, Nantes, France

    Marion Grard, Mohamed Idjellidaine, Camille Chatelain, Laurine Berland, Soizic Dutoit, Sophie Deshayes, Virginie Dehame, Delphine Fradin, Nicolas Boisgerault, Christophe Blanquart & Jean-François Fonteneau

  2. Labex IGO, Immunology Graft Oncology, Nantes, France

    Marion Grard, Mohamed Idjellidaine, Camille Chatelain, Laurine Berland, Soizic Dutoit, Sophie Deshayes, Virginie Dehame, Nathalie Labarrière, Delphine Fradin, Nicolas Boisgerault, Christophe Blanquart & Jean-François Fonteneau

  3. Vaccines Innovation Laboratory, Institut Pasteur, Université de Paris Cité, 75015, Paris, France

    Atousa Arbabian, Chantal Combredet & Frédéric Tangy

  4. Nantes Université, Université d’Angers, Inserm, Immunology and New Concepts in ImmunoTherapy, INCIT, UMR 1302, 44000, Nantes, France

    Nathalie Labarrière

  5. Oncovita, 75015, Paris, France

    Frédéric Tangy

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  1. Marion Grard
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Contributions

FT and JFF contributed to experiments conception. MG, MI, AA, CCh, LB, CCo, SD, VD, NB and JFF contributed to experiments. MG, NL, DF, NB, CB, FT and JFF performed data analysis and manuscript writing.

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Correspondence to Jean-François Fonteneau.

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Competing interests

FT and JFF are authors of patents on MV. FT owns equity in Oncovita, an oncolytic virotherapy company.

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Grard, M., Idjellidaine, M., Arbabian, A. et al. Oncolytic attenuated measles virus encoding NY-ESO-1 induces HLA I and II presentation of this tumor antigen by melanoma and dendritic cells. Cancer Immunol Immunother 72, 3309–3322 (2023). https://doi.org/10.1007/s00262-023-03486-4

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