Skip to main content
Top
Published in: Cancer Immunology, Immunotherapy 10/2023

19-07-2023 | Melanoma | Research

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

Authors: Marion Grard, Mohamed Idjellidaine, Atousa Arbabian, Camille Chatelain, Laurine Berland, Chantal Combredet, Soizic Dutoit, Sophie Deshayes, Virginie Dehame, Nathalie Labarrière, Delphine Fradin, Nicolas Boisgerault, Christophe Blanquart, Frédéric Tangy, Jean-François Fonteneau

Published in: Cancer Immunology, Immunotherapy | Issue 10/2023

Login to get access

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.
Appendix
Available only for authorised users
Literature
1.
go back to reference Macedo N, Miller DM, Haq R, Kaufman HL (2020) Clinical landscape of oncolytic virus research in 2020. J Immunother Cancer 8 Macedo N, Miller DM, Haq R, Kaufman HL (2020) Clinical landscape of oncolytic virus research in 2020. J Immunother Cancer 8
2.
3.
go back to reference Gauvrit A, Brandler S, Sapede-Peroz C et al (2008) Measles virus induces oncolysis of mesothelioma cells and allows dendritic cells to cross-prime tumor-specific CD8 response. Cancer Res 68:4882–4892CrossRefPubMed Gauvrit A, Brandler S, Sapede-Peroz C et al (2008) Measles virus induces oncolysis of mesothelioma cells and allows dendritic cells to cross-prime tumor-specific CD8 response. Cancer Res 68:4882–4892CrossRefPubMed
4.
go back to reference Guillerme JB, Boisgerault N, Roulois D et al (2013) Measles virus vaccine-infected tumor cells induce tumor antigen cross-presentation by human plasmacytoid dendritic cells. Clin Cancer Res 19:1147–1158CrossRefPubMed Guillerme JB, Boisgerault N, Roulois D et al (2013) Measles virus vaccine-infected tumor cells induce tumor antigen cross-presentation by human plasmacytoid dendritic cells. Clin Cancer Res 19:1147–1158CrossRefPubMed
5.
go back to reference Coulie PG, Van den Eynde BJ, van der Bruggen P, Boon T (2014) Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat Rev Cancer 14:135–146CrossRefPubMed Coulie PG, Van den Eynde BJ, van der Bruggen P, Boon T (2014) Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat Rev Cancer 14:135–146CrossRefPubMed
6.
go back to reference Meng X, Sun X, Liu Z, He Y (2021) A novel era of cancer/testis antigen in cancer immunotherapy. Int Immunopharmacol 98:107889CrossRefPubMed Meng X, Sun X, Liu Z, He Y (2021) A novel era of cancer/testis antigen in cancer immunotherapy. Int Immunopharmacol 98:107889CrossRefPubMed
7.
go back to reference Gnjatic S, Nishikawa H, Jungbluth AA et al (2006) NY-ESO-1: review of an immunogenic tumor antigen. Adv Cancer Res 95:1–30CrossRefPubMed Gnjatic S, Nishikawa H, Jungbluth AA et al (2006) NY-ESO-1: review of an immunogenic tumor antigen. Adv Cancer Res 95:1–30CrossRefPubMed
8.
go back to reference Jager E, Chen YT, Drijfhout JW et al (1998) Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J Exp Med 187:265–270CrossRefPubMedPubMedCentral Jager E, Chen YT, Drijfhout JW et al (1998) Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J Exp Med 187:265–270CrossRefPubMedPubMedCentral
9.
go back to reference Wang RF, Wang HY (2017) Immune targets and neoantigens for cancer immunotherapy and precision medicine. Cell Res 27:11–37CrossRefPubMed Wang RF, Wang HY (2017) Immune targets and neoantigens for cancer immunotherapy and precision medicine. Cell Res 27:11–37CrossRefPubMed
12.
go back to reference Boisgerault N, Guillerme JB, Pouliquen D et al (2013) Natural oncolytic activity of live-attenuated measles virus against human lung and colorectal adenocarcinomas. Biomed Res Int 2013:387362CrossRefPubMedPubMedCentral Boisgerault N, Guillerme JB, Pouliquen D et al (2013) Natural oncolytic activity of live-attenuated measles virus against human lung and colorectal adenocarcinomas. Biomed Res Int 2013:387362CrossRefPubMedPubMedCentral
15.
go back to reference Msaouel P, Opyrchal M, Dispenzieri A et al (2018) Clinical trials with oncolytic measles virus: current status and future prospects. Curr Cancer Drug Targets 18:177–187CrossRefPubMedPubMedCentral Msaouel P, Opyrchal M, Dispenzieri A et al (2018) Clinical trials with oncolytic measles virus: current status and future prospects. Curr Cancer Drug Targets 18:177–187CrossRefPubMedPubMedCentral
16.
go back to reference Backhaus PS, Veinalde R, Hartmann L, et al (2019) Immunological effects and viral gene expression determine the efficacy of oncolytic measles vaccines encoding IL-12 or IL-15 Agonists. Viruses 11 Backhaus PS, Veinalde R, Hartmann L, et al (2019) Immunological effects and viral gene expression determine the efficacy of oncolytic measles vaccines encoding IL-12 or IL-15 Agonists. Viruses 11
17.
go back to reference Speck T, Heidbuechel JPW, Veinalde R et al (2018) Targeted BiTE expression by an oncolytic vector augments therapeutic efficacy against solid tumors. Clin Cancer Res 24:2128–2137CrossRefPubMed Speck T, Heidbuechel JPW, Veinalde R et al (2018) Targeted BiTE expression by an oncolytic vector augments therapeutic efficacy against solid tumors. Clin Cancer Res 24:2128–2137CrossRefPubMed
18.
go back to reference Dispenzieri A, Tong C, LaPlant B et al (2017) Phase I trial of systemic administration of Edmonston strain of measles virus genetically engineered to express the sodium iodide symporter in patients with recurrent or refractory multiple myeloma. Leukemia 31:2791–2798CrossRefPubMedPubMedCentral Dispenzieri A, Tong C, LaPlant B et al (2017) Phase I trial of systemic administration of Edmonston strain of measles virus genetically engineered to express the sodium iodide symporter in patients with recurrent or refractory multiple myeloma. Leukemia 31:2791–2798CrossRefPubMedPubMedCentral
19.
go back to reference Frantz PN, Barinov A, Ruffie C et al (2021) A live measles-vectored COVID-19 vaccine induces strong immunity and protection from SARS-CoV-2 challenge in mice and hamsters. Nat Commun 12:6277CrossRefPubMedPubMedCentral Frantz PN, Barinov A, Ruffie C et al (2021) A live measles-vectored COVID-19 vaccine induces strong immunity and protection from SARS-CoV-2 challenge in mice and hamsters. Nat Commun 12:6277CrossRefPubMedPubMedCentral
20.
go back to reference Ramsauer K, Schwameis M, Firbas C et al (2015) Immunogenicity, safety, and tolerability of a recombinant measles-virus-based chikungunya vaccine: a randomised, double-blind, placebo-controlled, active-comparator, first-in-man trial. Lancet Infect Dis 15:519–527CrossRefPubMed Ramsauer K, Schwameis M, Firbas C et al (2015) Immunogenicity, safety, and tolerability of a recombinant measles-virus-based chikungunya vaccine: a randomised, double-blind, placebo-controlled, active-comparator, first-in-man trial. Lancet Infect Dis 15:519–527CrossRefPubMed
23.
go back to reference Fonteneau JF, Larsson M, Somersan S et al (2001) Generation of high quantities of viral and tumor-specific human CD4+ and CD8+ T-cell clones using peptide pulsed mature dendritic cells. J Immunol Methods 258:111–126CrossRefPubMed Fonteneau JF, Larsson M, Somersan S et al (2001) Generation of high quantities of viral and tumor-specific human CD4+ and CD8+ T-cell clones using peptide pulsed mature dendritic cells. J Immunol Methods 258:111–126CrossRefPubMed
24.
go back to reference Roulois D, Vignard V, Gueugnon F et al (2011) Recognition of pleural mesothelioma by mucin-1(950–958)/human leukocyte antigen A*0201-specific CD8+ T-cells. Eur Respir J 38:1117–1126CrossRefPubMed Roulois D, Vignard V, Gueugnon F et al (2011) Recognition of pleural mesothelioma by mucin-1(950–958)/human leukocyte antigen A*0201-specific CD8+ T-cells. Eur Respir J 38:1117–1126CrossRefPubMed
26.
go back to reference Coulais D, Panterne C, Fonteneau JF, Gregoire M (2012) Purification of circulating plasmacytoid dendritic cells using counterflow centrifugal elutriation and immunomagnetic beads. Cytotherapy 14:887–896CrossRefPubMed Coulais D, Panterne C, Fonteneau JF, Gregoire M (2012) Purification of circulating plasmacytoid dendritic cells using counterflow centrifugal elutriation and immunomagnetic beads. Cytotherapy 14:887–896CrossRefPubMed
27.
go back to reference Combredet C, Labrousse V, Mollet L et al (2003) A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J Virol 77:11546–11554CrossRefPubMedPubMedCentral Combredet C, Labrousse V, Mollet L et al (2003) A molecularly cloned Schwarz strain of measles virus vaccine induces strong immune responses in macaques and transgenic mice. J Virol 77:11546–11554CrossRefPubMedPubMedCentral
28.
go back to reference Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMed Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMed
31.
go back to reference Sanchez David RY, Combredet C, Sismeiro O et al (2016) Comparative analysis of viral RNA signatures on different RIG-I-like receptors. eLife 5: 11275 Sanchez David RY, Combredet C, Sismeiro O et al (2016) Comparative analysis of viral RNA signatures on different RIG-I-like receptors. eLife 5: 11275
33.
go back to reference Donnelly OG, Errington-Mais F, Steele L et al (2011) Measles virus causes immunogenic cell death in human melanoma. Gene Ther Donnelly OG, Errington-Mais F, Steele L et al (2011) Measles virus causes immunogenic cell death in human melanoma. Gene Ther
34.
go back to reference Fonteneau JF, Brilot F, Munz C, Gannage M (2016) The tumor antigen NY-ESO-1 mediates direct recognition of melanoma cells by CD4+ T cells after intercellular antigen transfer. J Immunol 196:64–71CrossRefPubMed Fonteneau JF, Brilot F, Munz C, Gannage M (2016) The tumor antigen NY-ESO-1 mediates direct recognition of melanoma cells by CD4+ T cells after intercellular antigen transfer. J Immunol 196:64–71CrossRefPubMed
36.
go back to reference Velazquez EF, Jungbluth AA, Yancovitz M et al (2007) Expression of the cancer/testis antigen NY-ESO-1 in primary and metastatic malignant melanoma (MM)–correlation with prognostic factors. Cancer Immun 7:11PubMedPubMedCentral Velazquez EF, Jungbluth AA, Yancovitz M et al (2007) Expression of the cancer/testis antigen NY-ESO-1 in primary and metastatic malignant melanoma (MM)–correlation with prognostic factors. Cancer Immun 7:11PubMedPubMedCentral
37.
go back to reference Barrow C, Browning J, MacGregor D et al (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12:764–771CrossRefPubMed Barrow C, Browning J, MacGregor D et al (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12:764–771CrossRefPubMed
38.
go back to reference Goydos JS, Patel M, Shih W (2001) NY-ESO-1 and CTp11 expression may correlate with stage of progression in melanoma. J Surg Res 98:76–80CrossRefPubMed Goydos JS, Patel M, Shih W (2001) NY-ESO-1 and CTp11 expression may correlate with stage of progression in melanoma. J Surg Res 98:76–80CrossRefPubMed
39.
40.
go back to reference Robbins PF, Kassim SH, Tran TL et al (2015) A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res 21:1019–1027CrossRefPubMed Robbins PF, Kassim SH, Tran TL et al (2015) A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res 21:1019–1027CrossRefPubMed
Metadata
Title
Oncolytic attenuated measles virus encoding NY-ESO-1 induces HLA I and II presentation of this tumor antigen by melanoma and dendritic cells
Authors
Marion Grard
Mohamed Idjellidaine
Atousa Arbabian
Camille Chatelain
Laurine Berland
Chantal Combredet
Soizic Dutoit
Sophie Deshayes
Virginie Dehame
Nathalie Labarrière
Delphine Fradin
Nicolas Boisgerault
Christophe Blanquart
Frédéric Tangy
Jean-François Fonteneau
Publication date
19-07-2023
Publisher
Springer Berlin Heidelberg
Keywords
Melanoma
Melanoma
Published in
Cancer Immunology, Immunotherapy / Issue 10/2023
Print ISSN: 0340-7004
Electronic ISSN: 1432-0851
DOI
https://doi.org/10.1007/s00262-023-03486-4

Other articles of this Issue 10/2023

Cancer Immunology, Immunotherapy 10/2023 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine