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

Background & Aims 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 v...

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Autores: Cappuyns, Sarah, Piqué-Gili, Marta, Esteban-Fabró, Roger, Philips, Gino, Balaseviciute, Ugne, Pinyol, Roser, Gris-Oliver, Albert, Vandecaveye, Vincent, Abril-Fornaguera, Jordi, Montironi, Carla, Bassaganyas, Laia, Peix, Judit, Zeitlhoefle, Marcus, Mesropian, Agavni, Huguet-Pradell, Júlia, Haber, Philipp K., Figueiredo, Igor, Ioannou, Giorgio, Gonzalez-Kozlova, Edgar, D’Alessio, Antonio, Mohr, Raphae, Meyer, Tim, Lachenmayer, Anja, Marquardt, Jens U., Reeves, Helen L., Edeline, Julien, Finkelmeier, Fabian, Trojan, Jörg, Galle, Peter R., Foerster, Friedrich, Mínguez, Beatriz, Montal Roura, Robert, Gnjatic, Sacha, Pinato, David J., Heikenwalder, Mathias, Verslype, Chris, Van Cutsem, Eric, Lambrechts, Diether, Villanueva, Augusto, Dekervel, Jeroen, Llovet, Josep M.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10459.1/468218
Acceso en línea:https://doi.org/10.1016/j.jhep.2024.12.016
https://hdl.handle.net/10459.1/468218
Access Level:acceso abierto
Palabra clave:Advanced Hepatocellular Carcinoma
Atezolizumab and bevacizumab
Biomarkers of Response
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spelling Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinomaCappuyns, SarahPiqué-Gili, MartaEsteban-Fabró, RogerPhilips, GinoBalaseviciute, UgnePinyol, RoserGris-Oliver, AlbertVandecaveye, VincentAbril-Fornaguera, JordiMontironi, CarlaBassaganyas, LaiaPeix, JuditZeitlhoefle, MarcusMesropian, AgavniHuguet-Pradell, JúliaHaber, Philipp K.Figueiredo, IgorIoannou, GiorgioGonzalez-Kozlova, EdgarD’Alessio, AntonioMohr, RaphaeMeyer, TimLachenmayer, AnjaMarquardt, Jens U.Reeves, Helen L.Edeline, JulienFinkelmeier, FabianTrojan, JörgGalle, Peter R.Foerster, FriedrichMínguez, BeatrizMontal Roura, RobertGnjatic, SachaPinato, David J.Heikenwalder, MathiasVerslype, ChrisVan Cutsem, EricLambrechts, DietherVillanueva, AugustoDekervel, JeroenLlovet, Josep M.Advanced Hepatocellular CarcinomaAtezolizumab and bevacizumabBiomarkers of ResponseBackground & Aims 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. Methods 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. Results 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. Conclusion 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.Elsevier2025info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttps://doi.org/10.1016/j.jhep.2024.12.016https://hdl.handle.net/10459.1/468218reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésReproducció del document publicat a https://doi.org/10.1016/j.jhep.2024.12.016Journal of Hepatology, 2025, vol. 82, núm. 6, p. 1036-1049cc-by-nc-nd (c) Sarah Cappuyns et al., 2025Attribution-NonCommercial-NoDerivatives 4.0 Internationalinfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-nd/4.0/oai:recercat.cat:10459.1/4682182026-05-29T05:05:01Z
dc.title.none.fl_str_mv Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
title Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
spellingShingle Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
Cappuyns, Sarah
Advanced Hepatocellular Carcinoma
Atezolizumab and bevacizumab
Biomarkers of Response
title_short Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
title_full Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
title_fullStr Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
title_full_unstemmed Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
title_sort Single-cell RNA sequencing-derived signatures define response patterns to atezolizumab + bevacizumab in advanced hepatocellular carcinoma
dc.creator.none.fl_str_mv Cappuyns, Sarah
Piqué-Gili, Marta
Esteban-Fabró, Roger
Philips, Gino
Balaseviciute, Ugne
Pinyol, Roser
Gris-Oliver, Albert
Vandecaveye, Vincent
Abril-Fornaguera, Jordi
Montironi, Carla
Bassaganyas, Laia
Peix, Judit
Zeitlhoefle, Marcus
Mesropian, Agavni
Huguet-Pradell, Júlia
Haber, Philipp K.
Figueiredo, Igor
Ioannou, Giorgio
Gonzalez-Kozlova, Edgar
D’Alessio, Antonio
Mohr, Raphae
Meyer, Tim
Lachenmayer, Anja
Marquardt, Jens U.
Reeves, Helen L.
Edeline, Julien
Finkelmeier, Fabian
Trojan, Jörg
Galle, Peter R.
Foerster, Friedrich
Mínguez, Beatriz
Montal Roura, Robert
Gnjatic, Sacha
Pinato, David J.
Heikenwalder, Mathias
Verslype, Chris
Van Cutsem, Eric
Lambrechts, Diether
Villanueva, Augusto
Dekervel, Jeroen
Llovet, Josep M.
author Cappuyns, Sarah
author_facet Cappuyns, Sarah
Piqué-Gili, Marta
Esteban-Fabró, Roger
Philips, Gino
Balaseviciute, Ugne
Pinyol, Roser
Gris-Oliver, Albert
Vandecaveye, Vincent
Abril-Fornaguera, Jordi
Montironi, Carla
Bassaganyas, Laia
Peix, Judit
Zeitlhoefle, Marcus
Mesropian, Agavni
Huguet-Pradell, Júlia
Haber, Philipp K.
Figueiredo, Igor
Ioannou, Giorgio
Gonzalez-Kozlova, Edgar
D’Alessio, Antonio
Mohr, Raphae
Meyer, Tim
Lachenmayer, Anja
Marquardt, Jens U.
Reeves, Helen L.
Edeline, Julien
Finkelmeier, Fabian
Trojan, Jörg
Galle, Peter R.
Foerster, Friedrich
Mínguez, Beatriz
Montal Roura, Robert
Gnjatic, Sacha
Pinato, David J.
Heikenwalder, Mathias
Verslype, Chris
Van Cutsem, Eric
Lambrechts, Diether
Villanueva, Augusto
Dekervel, Jeroen
Llovet, Josep M.
author_role author
author2 Piqué-Gili, Marta
Esteban-Fabró, Roger
Philips, Gino
Balaseviciute, Ugne
Pinyol, Roser
Gris-Oliver, Albert
Vandecaveye, Vincent
Abril-Fornaguera, Jordi
Montironi, Carla
Bassaganyas, Laia
Peix, Judit
Zeitlhoefle, Marcus
Mesropian, Agavni
Huguet-Pradell, Júlia
Haber, Philipp K.
Figueiredo, Igor
Ioannou, Giorgio
Gonzalez-Kozlova, Edgar
D’Alessio, Antonio
Mohr, Raphae
Meyer, Tim
Lachenmayer, Anja
Marquardt, Jens U.
Reeves, Helen L.
Edeline, Julien
Finkelmeier, Fabian
Trojan, Jörg
Galle, Peter R.
Foerster, Friedrich
Mínguez, Beatriz
Montal Roura, Robert
Gnjatic, Sacha
Pinato, David J.
Heikenwalder, Mathias
Verslype, Chris
Van Cutsem, Eric
Lambrechts, Diether
Villanueva, Augusto
Dekervel, Jeroen
Llovet, Josep M.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Advanced Hepatocellular Carcinoma
Atezolizumab and bevacizumab
Biomarkers of Response
topic Advanced Hepatocellular Carcinoma
Atezolizumab and bevacizumab
Biomarkers of Response
description Background & Aims 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. Methods 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. Results 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. Conclusion 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.
publishDate 2025
dc.date.none.fl_str_mv 2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://doi.org/10.1016/j.jhep.2024.12.016
https://hdl.handle.net/10459.1/468218
url https://doi.org/10.1016/j.jhep.2024.12.016
https://hdl.handle.net/10459.1/468218
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a https://doi.org/10.1016/j.jhep.2024.12.016
Journal of Hepatology, 2025, vol. 82, núm. 6, p. 1036-1049
dc.rights.none.fl_str_mv cc-by-nc-nd (c) Sarah Cappuyns et al., 2025
Attribution-NonCommercial-NoDerivatives 4.0 International
info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by-nc-nd/4.0/
rights_invalid_str_mv cc-by-nc-nd (c) Sarah Cappuyns et al., 2025
Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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