Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma

The combination of atezolizumab and bevacizumab (atezo+bev) is the current standard of care for advanced hepatocellular carcinoma (HCC), providing a median overall survival (OS) of 19.2 months. Here, we aim to uncover the underlying cellular processes driving clinical benefit vs. resistance to atezo...

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Autores: Cappuyns, Sarah, Piqué-Gili, Marta, Esteban-Fabró, Roger, Philips, Gino, Balaseviciute, Ugne, Pinyol, Roser|||0000-0002-0288-6314, Gris-Oliver, Albert|||0000-0003-1802-9541, Vandecaveye, Vincent, Abril-Fornaguera, Jordi|||0000-0002-5871-4052, Montironi, Carla|||0000-0002-1453-2193, Bassaganyas, Laia|||0000-0002-4575-0214, Peix, Judit, Zeitlhoefler, Marcus, Mesropian, Agavni, Huguet Pradell, Júlia, Haber, Philipp K, Figueiredo, Igor, Ioannou, Giorgio, Gonzalez Kozlova, Edgar, D'Alessio, Antonio, Mohr, Raphael, Meyer, Tim, Lachenmayer, Anja|||0000-0002-5879-5737, Marquardt, Jens U, Reeves, Helen L.|||0000-0003-0359-9795, Edeline, Julien, Finkelmeier, Fabian, Trojan, Jorg, Galle, Peter R, Foerster, Friedrich, Mínguez Rosique, Beatriz|||0000-0002-7276-9666, Montal, Robert, Gnjatic, Sacha, Pinato, David James|||0000-0002-3529-0103, Heikenwälder, Mathias, Verslype, Chris, Van Cutsem, Eric|||0000-0002-6372-1230, Lambrechts, Diether, Villanueva, Augusto|||0000-0003-3585-3727, Dekervel, Jeroen, Llovet, Josep M.|||0000-0003-0547-2667
Tipo de recurso: artículo
Fecha de publicación:2025
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:dnet:uabarcelona_::748b7601601a72c6320f6623ecfb4d84
Acceso en línea:https://ddd.uab.cat/record/328431
https://dx.doi.org/urn:doi:10.1016/j.jhep.2024.12.016
Access Level:acceso abierto
Palabra clave:Advanced Hepatocellular Carcinoma
Atezolizumab and bevacizumab
Biomarkers of Response
Single-Cell RNA-Sequencing
Primary Resistance
Descripción
Sumario:The combination of atezolizumab and bevacizumab (atezo+bev) is the current standard of care for advanced hepatocellular carcinoma (HCC), providing a median overall survival (OS) of 19.2 months. Here, we aim to uncover the underlying cellular processes driving clinical benefit vs. resistance to atezo+bev. We harnessed the power of single-cell RNA sequencing in advanced HCC to derive gene expression signatures recapitulating 21 cell phenotypes. These signatures were applied to 422 RNA-sequencing samples of patients with advanced HCC treated with atezo+bev (n = 317) vs. atezolizumab (n = 47) or sorafenib (n = 58) as comparators. We unveiled two distinct patterns of response to atezo+bev. First, an immune-mediated response characterised by the combined presence of CD8+ T effector cells and pro-inflammatory CXCL10+ macrophages, representing an immune-rich microenvironment. Second, a non-immune, angiogenesis-related response distinguishable by a reduced expression of the VEGF co-receptor neuropilin-1 (NRP1), a biomarker that specifically predicts improved OS upon atezo+bev vs. sorafenib (p = 0.039). Primary resistance was associated with an enrichment of immunosuppressive myeloid populations, namely CD14+ monocytes and TREM2+ macrophages, and Notch pathway activation. Based on these mechanistic insights we define " Immune-competent " and " Angiogenesis-driven " molecular subgroups, each associated with a significantly longer OS with atezo+bev vs. sorafenib (p of interaction = 0.027), and a " Resistant" subset. Our study unveils two distinct molecular subsets of clinical benefit to atezolizumab plus bevacizumab in advanced HCC (" Immune-competent" and " Angiogenesis-driven") as well as the main traits of primary resistance to this therapy, thus providing a molecular framework to stratify patients based on clinical outcome and guiding potential strategies to overcome resistance. Atezolizumab + bevacizumab (atezo+bev) is standard of care in advanced hepatocellular carcinoma (HCC), yet molecular determinants of clinical benefit to the combination remain unclear. This study harnesses the power of single-cell RNA sequencing, deriving gene expression signatures representing 21 cell subtypes in the advanced HCC microenvironment. By applying these signatures to RNA-sequencing samples, we reveal two distinct response patterns to atezo+bev and define molecular subgroups of patients (" Immune-competent" and " Angiogenesis-driven" vs. "Resistant") with differential clinical outcomes upon treatment with atezo+bev, pointing towards the role of immunosuppressive myeloid cell types and Notch pathway activation in primary resistance to atezo+bev. These results may help refine treatment strategies and improve outcomes for patients with advanced HCC, while also guiding future research aimed at overcoming resistance mechanisms.