Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanoma

Myeloid cells within tumor microenvironments exhibit significant heterogeneity and play a critical role in influencing clinical outcomes. In this study, we investigated the infiltration of various myeloid cell subtypes in a cohort of cutaneous melanomas, revealing no significant correlation between...

Full description

Saved in:
Bibliographic Details
Main Authors: Celia Barrio-Alonso, Alicia Nieto-Valle, Lucía Barandalla-Revilla, José Antonio Avilés-Izquierdo, Verónica Parra-Blanco, Paloma Sánchez-Mateos, Rafael Samaniego
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1587545/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850193061543411712
author Celia Barrio-Alonso
Celia Barrio-Alonso
Alicia Nieto-Valle
Alicia Nieto-Valle
Alicia Nieto-Valle
Lucía Barandalla-Revilla
Lucía Barandalla-Revilla
José Antonio Avilés-Izquierdo
Verónica Parra-Blanco
Paloma Sánchez-Mateos
Paloma Sánchez-Mateos
Rafael Samaniego
author_facet Celia Barrio-Alonso
Celia Barrio-Alonso
Alicia Nieto-Valle
Alicia Nieto-Valle
Alicia Nieto-Valle
Lucía Barandalla-Revilla
Lucía Barandalla-Revilla
José Antonio Avilés-Izquierdo
Verónica Parra-Blanco
Paloma Sánchez-Mateos
Paloma Sánchez-Mateos
Rafael Samaniego
author_sort Celia Barrio-Alonso
collection DOAJ
description Myeloid cells within tumor microenvironments exhibit significant heterogeneity and play a critical role in influencing clinical outcomes. In this study, we investigated the infiltration of various myeloid cell subtypes in a cohort of cutaneous melanomas, revealing no significant correlation between myeloid cell densities and the occurrence of distant metastasis. We further examined the phenotypic characteristics of primary melanoma tumor-associated macrophages (TAMs) utilizing the seven-phenotype classification recently proposed by Ma et al., derived from extensive pan-cancer single-cell RNA-sequencing studies. First, we analyzed the transcriptomic profile of TAMs isolated from stage IV metastasizing primary melanomas, alongside melanoma-conditioned monocytes cultured in vitro, both supporting the inflammatory cytokine-producing macrophage phenotype. Next, we employed multicolor fluorescence confocal microscopy, to assess the expression of TAM phenotype markers at the protein level in a cohort of primary melanoma samples. Notably, markers indicative of the inflammatory TAM phenotype, quantified at single-cell level, were significantly enriched in metastasizing tumors, demonstrating an independent correlation with shorter disease-free and overall survival (log-rank test, p< 0.0002). Additionally, our screening of phenotype markers expression revealed that PD-L1 positivity in tumor cells, rather than in TAMs, was associated with poor prognosis, highlighting a novel aspect of the immune landscape in cutaneous melanoma.
format Article
id doaj-art-b68c7c527389488eb92b4bb10325dd59
institution OA Journals
issn 1664-3224
language English
publishDate 2025-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj-art-b68c7c527389488eb92b4bb10325dd592025-08-20T02:14:22ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-05-011610.3389/fimmu.2025.15875451587545Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanomaCelia Barrio-Alonso0Celia Barrio-Alonso1Alicia Nieto-Valle2Alicia Nieto-Valle3Alicia Nieto-Valle4Lucía Barandalla-Revilla5Lucía Barandalla-Revilla6José Antonio Avilés-Izquierdo7Verónica Parra-Blanco8Paloma Sánchez-Mateos9Paloma Sánchez-Mateos10Rafael Samaniego11Unidad de Microscopía Confocal, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainLaboratorio de Inmuno-oncología, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainUnidad de Microscopía Confocal, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainLaboratorio de Inmuno-oncología, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainDepartamento de Inmunología, Universidad Complutense de Madrid, Madrid, SpainUnidad de Microscopía Confocal, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainLaboratorio de Inmuno-oncología, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainServicio de Dermatología, Hospital General Universitario Gregorio Marañón, Madrid, SpainServicio de Anatomía Patológica, Hospital General Universitario Gregorio Marañón, Madrid, SpainLaboratorio de Inmuno-oncología, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainDepartamento de Inmunología, Universidad Complutense de Madrid, Madrid, SpainUnidad de Microscopía Confocal, Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, SpainMyeloid cells within tumor microenvironments exhibit significant heterogeneity and play a critical role in influencing clinical outcomes. In this study, we investigated the infiltration of various myeloid cell subtypes in a cohort of cutaneous melanomas, revealing no significant correlation between myeloid cell densities and the occurrence of distant metastasis. We further examined the phenotypic characteristics of primary melanoma tumor-associated macrophages (TAMs) utilizing the seven-phenotype classification recently proposed by Ma et al., derived from extensive pan-cancer single-cell RNA-sequencing studies. First, we analyzed the transcriptomic profile of TAMs isolated from stage IV metastasizing primary melanomas, alongside melanoma-conditioned monocytes cultured in vitro, both supporting the inflammatory cytokine-producing macrophage phenotype. Next, we employed multicolor fluorescence confocal microscopy, to assess the expression of TAM phenotype markers at the protein level in a cohort of primary melanoma samples. Notably, markers indicative of the inflammatory TAM phenotype, quantified at single-cell level, were significantly enriched in metastasizing tumors, demonstrating an independent correlation with shorter disease-free and overall survival (log-rank test, p< 0.0002). Additionally, our screening of phenotype markers expression revealed that PD-L1 positivity in tumor cells, rather than in TAMs, was associated with poor prognosis, highlighting a novel aspect of the immune landscape in cutaneous melanoma.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1587545/fulltumor-associated macrophagesinflammatory cytokine-producing TAMsprognostic factorPD-L1myeloid cellscutaneous melanoma
spellingShingle Celia Barrio-Alonso
Celia Barrio-Alonso
Alicia Nieto-Valle
Alicia Nieto-Valle
Alicia Nieto-Valle
Lucía Barandalla-Revilla
Lucía Barandalla-Revilla
José Antonio Avilés-Izquierdo
Verónica Parra-Blanco
Paloma Sánchez-Mateos
Paloma Sánchez-Mateos
Rafael Samaniego
Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanoma
Frontiers in Immunology
tumor-associated macrophages
inflammatory cytokine-producing TAMs
prognostic factor
PD-L1
myeloid cells
cutaneous melanoma
title Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanoma
title_full Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanoma
title_fullStr Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanoma
title_full_unstemmed Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanoma
title_short Translating genetics into tissue: inflammatory cytokine-producing TAMs and PD-L1 tumor expression as poor prognosis factors in cutaneous melanoma
title_sort translating genetics into tissue inflammatory cytokine producing tams and pd l1 tumor expression as poor prognosis factors in cutaneous melanoma
topic tumor-associated macrophages
inflammatory cytokine-producing TAMs
prognostic factor
PD-L1
myeloid cells
cutaneous melanoma
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1587545/full
work_keys_str_mv AT celiabarrioalonso translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT celiabarrioalonso translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT alicianietovalle translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT alicianietovalle translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT alicianietovalle translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT luciabarandallarevilla translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT luciabarandallarevilla translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT joseantonioavilesizquierdo translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT veronicaparrablanco translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT palomasanchezmateos translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT palomasanchezmateos translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma
AT rafaelsamaniego translatinggeneticsintotissueinflammatorycytokineproducingtamsandpdl1tumorexpressionaspoorprognosisfactorsincutaneousmelanoma