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Cancer Immunology Research

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Research Articles

Collapse of the Plasmacytoid Dendritic Cell Compartment in Advanced Cutaneous Melanomas by Components of the Tumor Cell Secretome

Raffaella Vescovi, Matilde Monti, Daniele Moratto, Lucia Paolini, Francesca Consoli, Luisa Benerini, Laura Melocchi, Stefano Calza, Mariella Chiudinelli, Giulio Rossi, Mattia Bugatti, Michele Maio, Ester Fonsatti, Camillo Farisoglio, Michele Simbolo, Camillo Almici, Rosanna Verardi, Aldo Scarpa, Paolo Bergese, Ausilia Manganoni, Fabio Facchetti and William Vermi
Raffaella Vescovi
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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Matilde Monti
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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Daniele Moratto
Laboratory of Genetic Disorders of Childhood, "Angelo Nocivelli" Institute for Molecular Medicine, Spedali Civili, Brescia, Italy.
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Lucia Paolini
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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  • ORCID record for Lucia Paolini
Francesca Consoli
Oncology Unit, ASST Spedali Civili di Brescia, Italy.
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Luisa Benerini
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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Laura Melocchi
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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Stefano Calza
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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Mariella Chiudinelli
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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Giulio Rossi
Pathology Unit, Azienda Romagna, Hospital Santa Maria delle Croci, Ravenna, Italy.
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Mattia Bugatti
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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Michele Maio
Medical Oncology and Immunotherapy, University Hospital of Siena, Istituto Toscano Tumori, Siena, Italy.
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Ester Fonsatti
Medical Oncology and Immunotherapy, University Hospital of Siena, Istituto Toscano Tumori, Siena, Italy.
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Camillo Farisoglio
Dermathology Unit, ASST Spedali Civili di Brescia, Italy.
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Michele Simbolo
ARC-Net Research Centre and Department of Diagnostics and Public Health, Section of Pathology, Università degli Studi di Verona, Verona, Italy.
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  • ORCID record for Michele Simbolo
Camillo Almici
Department of Transfusion Medicine, Laboratory for Stem Cells Manipulation and Cryopreservation, ASST Spedali Civili, Brescia, Italy.
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Rosanna Verardi
Department of Transfusion Medicine, Laboratory for Stem Cells Manipulation and Cryopreservation, ASST Spedali Civili, Brescia, Italy.
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Aldo Scarpa
ARC-Net Research Centre and Department of Diagnostics and Public Health, Section of Pathology, Università degli Studi di Verona, Verona, Italy.
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Paolo Bergese
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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  • ORCID record for Paolo Bergese
Ausilia Manganoni
Dermathology Unit, ASST Spedali Civili di Brescia, Italy.
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Fabio Facchetti
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.
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William Vermi
Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, Missouri.
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  • For correspondence: william.vermi@unibs.it
DOI: 10.1158/2326-6066.CIR-18-0141 Published January 2019
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This article has a correction. Please see:

  • Correction: Collapse of the Plasmacytoid Dendritic Cell Compartment in Advanced Cutaneous Melanomas by Components of the Tumor Cell Secretome - April 1, 2019

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Abstract

Melanoma is an immunogenic neoplasm infiltrated by T cells, although these adaptive T cells usually fail to eradicate the tumor. Plasmacytoid dendritic cells (PDCs) are potent regulators of the adaptive immune response and can eliminate melanoma cells via TLR-mediated effector functions. The PDC compartment is maintained by progressively restricted bone marrow progenitors. Terminally differentiated PDCs exit the bone marrow into the circulation, then home to lymph nodes and inflamed peripheral tissues. Infiltration by PDCs is documented in various cancers. However, their role within the melanoma immune contexture is not completely known. We found that in locoregional primary cutaneous melanoma (PCM), PDC infiltration was heterogeneous, occurred early, and was recurrently localized at the invasive margin, the site where PDCs interact with CD8+ T cells. A reduced PDC density was coupled with an increased Breslow thickness and somatic mutations at the NRAS p.Q61 codon. Compared with what was seen in PCM, high numbers of PDCs were found in regional lymph nodes, as also identified by in silico analysis. In contrast, in metastatic melanoma patients, PDCs were mostly absent in the tumor tissues and were significantly reduced in the circulation, particularly in the advanced M1c group. Exposure of circulating PDCs to melanoma cell supernatant (SN-mel) depleted of extracellular vesicles resulted in significant PDC death. SN-mel exposure also resulted in a defect of PDC differentiation from CD34+ progenitors. These findings indicate that soluble components released by melanoma cells support the collapse of the PDC compartment, with clinical implications for refining TLR agonist–based trials.

Footnotes

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

  • Received March 7, 2018.
  • Revision received August 16, 2018.
  • Accepted November 1, 2018.
  • Published first November 6, 2018.
  • Corrected online February 28, 2019.
  • ©2018 American Association for Cancer Research.
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Cancer Immunology Research: 7 (1)
January 2019
Volume 7, Issue 1
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Collapse of the Plasmacytoid Dendritic Cell Compartment in Advanced Cutaneous Melanomas by Components of the Tumor Cell Secretome
Raffaella Vescovi, Matilde Monti, Daniele Moratto, Lucia Paolini, Francesca Consoli, Luisa Benerini, Laura Melocchi, Stefano Calza, Mariella Chiudinelli, Giulio Rossi, Mattia Bugatti, Michele Maio, Ester Fonsatti, Camillo Farisoglio, Michele Simbolo, Camillo Almici, Rosanna Verardi, Aldo Scarpa, Paolo Bergese, Ausilia Manganoni, Fabio Facchetti and William Vermi
Cancer Immunol Res January 1 2019 (7) (1) 12-28; DOI: 10.1158/2326-6066.CIR-18-0141

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Collapse of the Plasmacytoid Dendritic Cell Compartment in Advanced Cutaneous Melanomas by Components of the Tumor Cell Secretome
Raffaella Vescovi, Matilde Monti, Daniele Moratto, Lucia Paolini, Francesca Consoli, Luisa Benerini, Laura Melocchi, Stefano Calza, Mariella Chiudinelli, Giulio Rossi, Mattia Bugatti, Michele Maio, Ester Fonsatti, Camillo Farisoglio, Michele Simbolo, Camillo Almici, Rosanna Verardi, Aldo Scarpa, Paolo Bergese, Ausilia Manganoni, Fabio Facchetti and William Vermi
Cancer Immunol Res January 1 2019 (7) (1) 12-28; DOI: 10.1158/2326-6066.CIR-18-0141
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