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
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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
Single-Cell RNA-Sequencing
Primary Resistance
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|||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
author Cappuyns, Sarah
author_facet 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
author_role author
author2 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
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author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
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dc.subject.none.fl_str_mv Advanced Hepatocellular Carcinoma
Atezolizumab and bevacizumab
Biomarkers of Response
Single-Cell RNA-Sequencing
Primary Resistance
topic Advanced Hepatocellular Carcinoma
Atezolizumab and bevacizumab
Biomarkers of Response
Single-Cell RNA-Sequencing
Primary Resistance
description 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.
publishDate 2025
dc.date.none.fl_str_mv 2
2025-01-01
2025
2025-01-01
dc.type.none.fl_str_mv Article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://ddd.uab.cat/record/328431
https://dx.doi.org/urn:doi:10.1016/j.jhep.2024.12.016
url https://ddd.uab.cat/record/328431
https://dx.doi.org/urn:doi:10.1016/j.jhep.2024.12.016
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 BES-2017-081286
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139365OB-I00
Generalitat de Catalunya https://doi.org/10.13039/501100002809 2021/SGR-00338
European Commission https://doi.org/10.13039/501100000780 101136622
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139365OB-I00
"la Caixa" Foundation https://doi.org/10.13039/100010434 LCF/PR/SP23/5295000
Generalitat de Catalunya https://doi.org/10.13039/501100002809 2021/SGR-01347
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dipòsit Digital de Documents de la UAB
instname:Universitat Autònoma de Barcelona
instname_str Universitat Autònoma de Barcelona
reponame_str Dipòsit Digital de Documents de la UAB
collection Dipòsit Digital de Documents de la UAB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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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, Roser|||0000-0002-0288-6314Gris-Oliver, Albert|||0000-0003-1802-9541Vandecaveye, VincentAbril-Fornaguera, Jordi|||0000-0002-5871-4052Montironi, Carla|||0000-0002-1453-2193Bassaganyas, Laia|||0000-0002-4575-0214Peix, JuditZeitlhoefler, MarcusMesropian, AgavniHuguet Pradell, JúliaHaber, Philipp KFigueiredo, IgorIoannou, GiorgioGonzalez Kozlova, EdgarD'Alessio, AntonioMohr, RaphaelMeyer, TimLachenmayer, Anja|||0000-0002-5879-5737Marquardt, Jens UReeves, Helen L.|||0000-0003-0359-9795Edeline, JulienFinkelmeier, FabianTrojan, JorgGalle, Peter RFoerster, FriedrichMínguez Rosique, Beatriz|||0000-0002-7276-9666Montal, RobertGnjatic, SachaPinato, David James|||0000-0002-3529-0103Heikenwälder, MathiasVerslype, ChrisVan Cutsem, Eric|||0000-0002-6372-1230Lambrechts, DietherVillanueva, Augusto|||0000-0003-3585-3727Dekervel, JeroenLlovet, Josep M.|||0000-0003-0547-2667Advanced Hepatocellular CarcinomaAtezolizumab and bevacizumabBiomarkers of ResponseSingle-Cell RNA-SequencingPrimary ResistanceThe 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. 22025-01-0120252025-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/328431https://dx.doi.org/urn:doi:10.1016/j.jhep.2024.12.016reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengAgencia Estatal de Investigación https://doi.org/10.13039/501100011033 BES-2017-081286Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139365OB-I00Generalitat de Catalunya https://doi.org/10.13039/501100002809 2021/SGR-00338European Commission https://doi.org/10.13039/501100000780 101136622Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 PID2022-139365OB-I00"la Caixa" Foundation https://doi.org/10.13039/100010434 LCF/PR/SP23/5295000Generalitat de Catalunya https://doi.org/10.13039/501100002809 2021/SGR-01347open accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, i la comunicació pública de l'obra, sempre que no sigui amb finalitats comercials, i sempre que es reconegui l'autoria de l'obra original. No es permet la creació d'obres derivades.https://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:dnet:uabarcelona_::748b7601601a72c6320f6623ecfb4d842026-06-06T12:50:31Z
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