NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma

Background: Activating and inhibitory receptors of natural killer (NK) cells such as NKp, NKG2, or CLEC are highly relevant to cold tumors including glioblastoma (GBM). Here, we aimed to characterize the expression of these receptors in GBM to gain insight into their potential role as modulators of...

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Autores: Dios Huerta, Olaya de, Ramírez-González, María A, Gómez-Soria, Irene, Segura-Collar, Berta, Manosalva, Juliana, Megías, Diego, de Andrea, Carlos E, Fernández-Rubio, Leticia, Hernández-Laín, Aurelio, Sepúlveda-Sánchez, Juan Manuel, Rodriguez-Ruiz, Maria E, Pérez-Núñez, Ángel, Wainwright, Derek A, Gargini, Ricardo, Sánchez-Gómez, Pilar
Tipo de recurso: artículo
Fecha de publicación:2024
País:España
Institución:Instituto de Salud Carlos III (ISCIII)
Repositorio:Repisalud
Idioma:inglés
OAI Identifier:oai:repisalud.isciii.es:20.500.12105/25097
Acceso en línea:https://hdl.handle.net/20.500.12105/25097
Access Level:acceso abierto
Palabra clave:Central Nervous System Cancer
Immune Checkpoint Inhibitor
Macrophage
NK Cell Lectin-Like Receptor Subfamily K
Tumor microenvironment - TME
Animals
Brain Neoplasms
Cell Line, Tumor
Female
Glioblastoma
Humans
Immunotherapy
Killer Cells, Natural
Mice
NK Cell Lectin-Like Receptor Subfamily C
Tumor Microenvironment
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dc.title.none.fl_str_mv NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
title NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
spellingShingle NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
Dios Huerta, Olaya de
Central Nervous System Cancer
Immune Checkpoint Inhibitor
Macrophage
NK Cell Lectin-Like Receptor Subfamily K
Tumor microenvironment - TME
Animals
Brain Neoplasms
Cell Line, Tumor
Female
Glioblastoma
Humans
Immunotherapy
Killer Cells, Natural
Mice
NK Cell Lectin-Like Receptor Subfamily C
Tumor Microenvironment
title_short NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
title_full NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
title_fullStr NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
title_full_unstemmed NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
title_sort NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastoma
dc.creator.none.fl_str_mv Dios Huerta, Olaya de
Ramírez-González, María A
Gómez-Soria, Irene
Segura-Collar, Berta
Manosalva, Juliana
Megías, Diego
de Andrea, Carlos E
Fernández-Rubio, Leticia
Hernández-Laín, Aurelio
Sepúlveda-Sánchez, Juan Manuel
Rodriguez-Ruiz, Maria E
Pérez-Núñez, Ángel
Wainwright, Derek A
Gargini, Ricardo
Sánchez-Gómez, Pilar
author Dios Huerta, Olaya de
author_facet Dios Huerta, Olaya de
Ramírez-González, María A
Gómez-Soria, Irene
Segura-Collar, Berta
Manosalva, Juliana
Megías, Diego
de Andrea, Carlos E
Fernández-Rubio, Leticia
Hernández-Laín, Aurelio
Sepúlveda-Sánchez, Juan Manuel
Rodriguez-Ruiz, Maria E
Pérez-Núñez, Ángel
Wainwright, Derek A
Gargini, Ricardo
Sánchez-Gómez, Pilar
author_role author
author2 Ramírez-González, María A
Gómez-Soria, Irene
Segura-Collar, Berta
Manosalva, Juliana
Megías, Diego
de Andrea, Carlos E
Fernández-Rubio, Leticia
Hernández-Laín, Aurelio
Sepúlveda-Sánchez, Juan Manuel
Rodriguez-Ruiz, Maria E
Pérez-Núñez, Ángel
Wainwright, Derek A
Gargini, Ricardo
Sánchez-Gómez, Pilar
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Unión Europea. Fondo Europeo de Desarrollo Regional (FEDER/ERDF)
Instituto de Salud Carlos III
National Institutes of Health (Estados Unidos)
Cancer Research UK (Reino Unido)
American Cancer Society
Asociación Española Contra el Cáncer
Brain Tumor Association (ABTA)

dc.subject.none.fl_str_mv Central Nervous System Cancer
Immune Checkpoint Inhibitor
Macrophage
NK Cell Lectin-Like Receptor Subfamily K
Tumor microenvironment - TME
Animals
Brain Neoplasms
Cell Line, Tumor
Female
Glioblastoma
Humans
Immunotherapy
Killer Cells, Natural
Mice
NK Cell Lectin-Like Receptor Subfamily C
Tumor Microenvironment
topic Central Nervous System Cancer
Immune Checkpoint Inhibitor
Macrophage
NK Cell Lectin-Like Receptor Subfamily K
Tumor microenvironment - TME
Animals
Brain Neoplasms
Cell Line, Tumor
Female
Glioblastoma
Humans
Immunotherapy
Killer Cells, Natural
Mice
NK Cell Lectin-Like Receptor Subfamily C
Tumor Microenvironment
description Background: Activating and inhibitory receptors of natural killer (NK) cells such as NKp, NKG2, or CLEC are highly relevant to cold tumors including glioblastoma (GBM). Here, we aimed to characterize the expression of these receptors in GBM to gain insight into their potential role as modulators of the intratumoral microenvironment. Methods: We performed a transcriptomic analysis of several NK receptors with a focus on the activating receptor encoded by KLRC2, NKG2C, among bulk and single-cell RNA sequencing GBM data sets. We also evaluated the effects of KLRC2-overexpressing GL261 cells in mice treated with or without programmed cell death protein-1 (PD-1) monoclonal antibody (mAb). Finally, we analyzed samples from two clinical trials evaluating PD-1 mAb effects in patients with GBM to determine the potential of NKG2C to serve as a biomarker of response. Results: We observed significant expression of several inhibitory NK receptors on GBM-infiltrating NK and T cells, which contrasts with the strong expression of KLRC2 on tumor cells, mainly at the infiltrative margin. Neoplastic KLRC2 expression was associated with a reduction in the number of myeloid-derived suppressor cells and with a higher level of tumor-resident lymphocytes. A stronger antitumor activity after PD-1 mAb treatment was observed in NKG2Chigh-expressing tumors both in mouse models and patients with GBM whereas the expression of inhibitory NK receptors showed an inverse association. Conclusions: This study explored the role of neoplastic NKG2C/KLRC2 expression in shaping the immune profile of GBM and suggests that it is a predictive biomarker for positive responses to immune checkpoint inhibitor treatment in patients with GBM. Future studies could further validate this finding in prospective trials.
publishDate 2024
dc.date.none.fl_str_mv 2024
2024-10-14
2024
2024-08-30
2024
2024-08-30
dc.type.none.fl_str_mv research article
http://purl.org/coar/resource_type/c_2df8fbb1
VoR
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dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/20.500.12105/25097
url https://hdl.handle.net/20.500.12105/25097
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv Instituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 (ISCIII) PI20%2F00434 INMUNOTERAPIA INTRATUMORAL BASADA EN AGONISTAS TLR3 COMO POTENCIADOR DE LOS EFECTOS LOCALES Y SISTEMICOS DE LA RADIOTERAPIA
ES RTC2019-006860-1 Not available
Instituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 (ISCIII) PI21%2F01406 NUEVAS ESTRATEGIAS CONTRA LAS RESISTENCIAS TERAPEUTICAS DE LOS GLIOMAS CENTRADAS EN EL MICROAMBIENTE TUMORAL Y SUS REGULADORES.
Instituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica, Técnica y de Innovación 2021-2023 PI22%2F01171 Reprogramación epigenómica del microambiente tumoral para eliminar los oncogenes que promueven al glioma
Instituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 (ISCIII) PI21%2F01168 CARACTERIZACION DEL AREA PERITUMORAL DE LOS GLIOBLASTOMAS: QUEMANDO LOS PUENTES HACIA LA PROGRESION
ES PI21CIII 00002
ES TED2021-132318B-I00 Not available
ES P2022 BMD-7344
ES CD21 00080
ES CD22CIII 00001
ES CP21 00116
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial 4.0 International
http://creativecommons.org/licenses/by-nc/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
Attribution-NonCommercial 4.0 International
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eu_rights_str_mv openAccess
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dc.publisher.none.fl_str_mv BMJ Publishing Group
publisher.none.fl_str_mv BMJ Publishing Group
dc.source.none.fl_str_mv reponame:Repisalud
instname:Instituto de Salud Carlos III (ISCIII)
instname_str Instituto de Salud Carlos III (ISCIII)
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spelling NKG2C/ KLRC2 tumor cell expression enhances immunotherapeutic efficacy against glioblastomaDios Huerta, Olaya deRamírez-González, María AGómez-Soria, IreneSegura-Collar, BertaManosalva, JulianaMegías, Diegode Andrea, Carlos EFernández-Rubio, LeticiaHernández-Laín, AurelioSepúlveda-Sánchez, Juan ManuelRodriguez-Ruiz, Maria EPérez-Núñez, ÁngelWainwright, Derek AGargini, RicardoSánchez-Gómez, PilarCentral Nervous System CancerImmune Checkpoint InhibitorMacrophageNK Cell Lectin-Like Receptor Subfamily KTumor microenvironment - TMEAnimalsBrain NeoplasmsCell Line, TumorFemaleGlioblastomaHumansImmunotherapyKiller Cells, NaturalMiceNK Cell Lectin-Like Receptor Subfamily CTumor MicroenvironmentBackground: Activating and inhibitory receptors of natural killer (NK) cells such as NKp, NKG2, or CLEC are highly relevant to cold tumors including glioblastoma (GBM). Here, we aimed to characterize the expression of these receptors in GBM to gain insight into their potential role as modulators of the intratumoral microenvironment. Methods: We performed a transcriptomic analysis of several NK receptors with a focus on the activating receptor encoded by KLRC2, NKG2C, among bulk and single-cell RNA sequencing GBM data sets. We also evaluated the effects of KLRC2-overexpressing GL261 cells in mice treated with or without programmed cell death protein-1 (PD-1) monoclonal antibody (mAb). Finally, we analyzed samples from two clinical trials evaluating PD-1 mAb effects in patients with GBM to determine the potential of NKG2C to serve as a biomarker of response. Results: We observed significant expression of several inhibitory NK receptors on GBM-infiltrating NK and T cells, which contrasts with the strong expression of KLRC2 on tumor cells, mainly at the infiltrative margin. Neoplastic KLRC2 expression was associated with a reduction in the number of myeloid-derived suppressor cells and with a higher level of tumor-resident lymphocytes. A stronger antitumor activity after PD-1 mAb treatment was observed in NKG2Chigh-expressing tumors both in mouse models and patients with GBM whereas the expression of inhibitory NK receptors showed an inverse association. Conclusions: This study explored the role of neoplastic NKG2C/KLRC2 expression in shaping the immune profile of GBM and suggests that it is a predictive biomarker for positive responses to immune checkpoint inhibitor treatment in patients with GBM. Future studies could further validate this finding in prospective trials.BMJ Publishing GroupMinisterio de Ciencia, Innovación y Universidades (España)Unión Europea. Fondo Europeo de Desarrollo Regional (FEDER/ERDF)Instituto de Salud Carlos IIINational Institutes of Health (Estados Unidos)Cancer Research UK (Reino Unido)American Cancer SocietyAsociación Española Contra el CáncerBrain Tumor Association (ABTA)20242024-10-1420242024-08-3020242024-08-30research articlehttp://purl.org/coar/resource_type/c_2df8fbb1VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfapplication/vnd.openxmlformats-officedocument.spreadsheetml.sheetapplication/vnd.openxmlformats-officedocument.spreadsheetml.sheetapplication/pdfapplication/vnd.openxmlformats-officedocument.spreadsheetml.sheetapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttps://hdl.handle.net/20.500.12105/25097reponame:Repisaludinstname:Instituto de Salud Carlos III (ISCIII)InglésengInstituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 (ISCIII) PI20%2F00434 INMUNOTERAPIA INTRATUMORAL BASADA EN AGONISTAS TLR3 COMO POTENCIADOR DE LOS EFECTOS LOCALES Y SISTEMICOS DE LA RADIOTERAPIAES RTC2019-006860-1 Not availableInstituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 (ISCIII) PI21%2F01406 NUEVAS ESTRATEGIAS CONTRA LAS RESISTENCIAS TERAPEUTICAS DE LOS GLIOMAS CENTRADAS EN EL MICROAMBIENTE TUMORAL Y SUS REGULADORES.Instituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica, Técnica y de Innovación 2021-2023 PI22%2F01171 Reprogramación epigenómica del microambiente tumoral para eliminar los oncogenes que promueven al gliomaInstituto de Salud Carlos III http://dx.doi.org/10.13039/501100004587 Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 (ISCIII) PI21%2F01168 CARACTERIZACION DEL AREA PERITUMORAL DE LOS GLIOBLASTOMAS: QUEMANDO LOS PUENTES HACIA LA PROGRESIONES PI21CIII 00002ES TED2021-132318B-I00 Not availableES P2022 BMD-7344ES CD21 00080ES CD22CIII 00001ES CP21 00116open accesshttp://purl.org/coar/access_right/c_abf2Attribution-NonCommercial 4.0 Internationalhttp://creativecommons.org/licenses/by-nc/4.0/info:eu-repo/semantics/openAccessoai:repisalud.isciii.es:20.500.12105/250972026-06-12T12:43:37Z
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