Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancer

High-risk non-muscle-invasive bladder cancer (NMIBC) presents high recurrence and progression rates. Despite the use of Bacillus Calmette-Guérin gold-standard immunotherapy and the recent irruption of anti-PD-1/PD-L1 drugs, we are missing a comprehensive understanding of the tumor microenvironment (...

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Main Authors: Carmen G. Cañizo, Félix Guerrero-Ramos, Mercedes Perez Escavy, Iris Lodewijk, Cristian Suárez-Cabrera, Lucía Morales, Sandra P. Nunes, Ester Munera-Maravilla, Carolina Rubio, Rebeca Sánchez, Marta Rodriguez-Izquierdo, Jaime Martínez de Villarreal, Francisco X. Real, Daniel Castellano, Cristina Martín-Arriscado, David Lora Pablos, Alfredo Rodríguez Antolín, Marta Dueñas, Jesús M. Paramio, Victor G. Martínez
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:OncoImmunology
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Online Access:https://www.tandfonline.com/doi/10.1080/2162402X.2024.2438291
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author Carmen G. Cañizo
Félix Guerrero-Ramos
Mercedes Perez Escavy
Iris Lodewijk
Cristian Suárez-Cabrera
Lucía Morales
Sandra P. Nunes
Ester Munera-Maravilla
Carolina Rubio
Rebeca Sánchez
Marta Rodriguez-Izquierdo
Jaime Martínez de Villarreal
Francisco X. Real
Daniel Castellano
Cristina Martín-Arriscado
David Lora Pablos
Alfredo Rodríguez Antolín
Marta Dueñas
Jesús M. Paramio
Victor G. Martínez
author_facet Carmen G. Cañizo
Félix Guerrero-Ramos
Mercedes Perez Escavy
Iris Lodewijk
Cristian Suárez-Cabrera
Lucía Morales
Sandra P. Nunes
Ester Munera-Maravilla
Carolina Rubio
Rebeca Sánchez
Marta Rodriguez-Izquierdo
Jaime Martínez de Villarreal
Francisco X. Real
Daniel Castellano
Cristina Martín-Arriscado
David Lora Pablos
Alfredo Rodríguez Antolín
Marta Dueñas
Jesús M. Paramio
Victor G. Martínez
author_sort Carmen G. Cañizo
collection DOAJ
description High-risk non-muscle-invasive bladder cancer (NMIBC) presents high recurrence and progression rates. Despite the use of Bacillus Calmette-Guérin gold-standard immunotherapy and the recent irruption of anti-PD-1/PD-L1 drugs, we are missing a comprehensive understanding of the tumor microenvironment (TME) that may help us find biomarkers associated to treatment outcome. Here, we prospectively analyzed TME composition and PD-L1 expression of tumor and non-tumoral tissue biopsies from 73 NMIBC patients and used scRNA-seq, transcriptomic cohorts and tissue micro-array to validate the prognostic value of cell types of interest. Compared to non-tumoral tissue, NMIBC presented microvascular alterations, increased cancer-associated fibroblast (CAF) and myofibroblast (myoCAF) presence, and varied immune cell distribution, such as increased macrophage infiltration. Heterogeneous PD-L1 expression was observed across subsets, with macrophages showing the highest expression levels, but cancer cells as the primary potential anti-PD-L1 binding targets. Unbiased analysis revealed that myoCAF and M2-like macrophages are specifically enriched in high-grade NMIBC tumors. The topological distribution of these two cell types changed as NMIBC progresses, as shown by immunofluorescence. Only myoCAFs were associated with higher rates of progression and recurrence in three independent cohorts (888 total patients), reaching prediction values comparable to transcriptomic classes, which we further validated using tissue micro-array. Our study provides a roadmap to establish the landscape of the NMIBC TME, highlighting myoCAFs as potential prognostic markers.
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spelling doaj-art-3e9ed1121f8b4b04a35bdf2fcc03c8e22025-08-20T02:52:23ZengTaylor & Francis GroupOncoImmunology2162-402X2025-12-0114110.1080/2162402X.2024.2438291Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancerCarmen G. Cañizo0Félix Guerrero-Ramos1Mercedes Perez Escavy2Iris Lodewijk3Cristian Suárez-Cabrera4Lucía Morales5Sandra P. Nunes6Ester Munera-Maravilla7Carolina Rubio8Rebeca Sánchez9Marta Rodriguez-Izquierdo10Jaime Martínez de Villarreal11Francisco X. Real12Daniel Castellano13Cristina Martín-Arriscado14David Lora Pablos15Alfredo Rodríguez Antolín16Marta Dueñas17Jesús M. Paramio18Victor G. Martínez19Urology Department, University Hospital ‘12 de Octubre’, Madrid, SpainUrology Department, University Hospital ‘12 de Octubre’, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainCell Technology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainUrology Department, University Hospital ‘12 de Octubre’, Madrid, SpainCentro de Investigación Biomédica en Red Cáncer (CIBERONC), Madrid, SpainCentro de Investigación Biomédica en Red Cáncer (CIBERONC), Madrid, SpainOncology Department, University Hospital ‘12 de Octubre’, Madrid, SpainScientific Support Unit, Research Institute I+12, University Hospital 12 de Octubre, Madrid, SpainScientific Support Unit, Research Institute I+12, University Hospital 12 de Octubre, Madrid, SpainUrology Department, University Hospital ‘12 de Octubre’, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainMolecular and Translational Oncology Division, Biomedical Innovation Unit, CIEMAT, Madrid, SpainHigh-risk non-muscle-invasive bladder cancer (NMIBC) presents high recurrence and progression rates. Despite the use of Bacillus Calmette-Guérin gold-standard immunotherapy and the recent irruption of anti-PD-1/PD-L1 drugs, we are missing a comprehensive understanding of the tumor microenvironment (TME) that may help us find biomarkers associated to treatment outcome. Here, we prospectively analyzed TME composition and PD-L1 expression of tumor and non-tumoral tissue biopsies from 73 NMIBC patients and used scRNA-seq, transcriptomic cohorts and tissue micro-array to validate the prognostic value of cell types of interest. Compared to non-tumoral tissue, NMIBC presented microvascular alterations, increased cancer-associated fibroblast (CAF) and myofibroblast (myoCAF) presence, and varied immune cell distribution, such as increased macrophage infiltration. Heterogeneous PD-L1 expression was observed across subsets, with macrophages showing the highest expression levels, but cancer cells as the primary potential anti-PD-L1 binding targets. Unbiased analysis revealed that myoCAF and M2-like macrophages are specifically enriched in high-grade NMIBC tumors. The topological distribution of these two cell types changed as NMIBC progresses, as shown by immunofluorescence. Only myoCAFs were associated with higher rates of progression and recurrence in three independent cohorts (888 total patients), reaching prediction values comparable to transcriptomic classes, which we further validated using tissue micro-array. Our study provides a roadmap to establish the landscape of the NMIBC TME, highlighting myoCAFs as potential prognostic markers.https://www.tandfonline.com/doi/10.1080/2162402X.2024.2438291Bladder cancercancer-associated fibroblastsMyofibroblastsPD-L1tumor microenvironment
spellingShingle Carmen G. Cañizo
Félix Guerrero-Ramos
Mercedes Perez Escavy
Iris Lodewijk
Cristian Suárez-Cabrera
Lucía Morales
Sandra P. Nunes
Ester Munera-Maravilla
Carolina Rubio
Rebeca Sánchez
Marta Rodriguez-Izquierdo
Jaime Martínez de Villarreal
Francisco X. Real
Daniel Castellano
Cristina Martín-Arriscado
David Lora Pablos
Alfredo Rodríguez Antolín
Marta Dueñas
Jesús M. Paramio
Victor G. Martínez
Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancer
OncoImmunology
Bladder cancer
cancer-associated fibroblasts
Myofibroblasts
PD-L1
tumor microenvironment
title Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancer
title_full Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancer
title_fullStr Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancer
title_full_unstemmed Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancer
title_short Characterisation of the tumour microenvironment and PD-L1 granularity reveals the prognostic value of cancer-associated myofibroblasts in non-invasive bladder cancer
title_sort characterisation of the tumour microenvironment and pd l1 granularity reveals the prognostic value of cancer associated myofibroblasts in non invasive bladder cancer
topic Bladder cancer
cancer-associated fibroblasts
Myofibroblasts
PD-L1
tumor microenvironment
url https://www.tandfonline.com/doi/10.1080/2162402X.2024.2438291
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