Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adults

IntroductionCoronavirus disease 2019 (COVID-19) affects the population unequally, with a greater impact on older and immunosuppressed people.MethodsHence, we performed a prospective experimental cohort study to characterise the effect of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) v...

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Main Authors: Juan H-Vázquez, Paloma Cal-Sabater, Elisa Arribas-Rodríguez, Aida Fiz-López, Candido Perez-Segurado, Álvaro Martín-Muñoz, Ángel De Prado, Marina Perez Mazzali, Carolina G. de Castro, Alejandro G. del Hierro, Ignacio de la Fuente Graciani, Sonia Pérez González, Sara Gutiérrez, Pablo Tellería, Cristina Novoa, Silvia Rojo Rello, Antonio Garcia-Blesa, Rosa Sedano, Ana María Martínez García, Sonsoles Garcinuño Pérez, Marta Domínguez-Gil, Cristina Hernán García, Ma Mercedes Guerra, Eduardo Muñoz-Sánchez, Cristina Barragan-Pérez, Soraya Diez Morales, Oriana Casazza Donnarumma, Daniel Ramos Pollo, Natalia Santamarta Solla, Paula Ma Álvarez Manzanares, Sara Bravo, Cristina García Alonso, Luis Alberto Avendaño Fernández, Jenifer Gay Alonso, José A. Garrote, Eduardo Arranz, José María Eiros, Fernando Rescalvo Santiago, Carolina Quevedo Villegas, Eduardo Tamayo, Antonio Orduña, Carlos Dueñas, María Jesús Peñarrubia, Sara Cuesta-Sancho, María Montoya, David Bernardo
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Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2024.1405217/full
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author Juan H-Vázquez
Paloma Cal-Sabater
Elisa Arribas-Rodríguez
Aida Fiz-López
Candido Perez-Segurado
Álvaro Martín-Muñoz
Ángel De Prado
Marina Perez Mazzali
Carolina G. de Castro
Alejandro G. del Hierro
Ignacio de la Fuente Graciani
Sonia Pérez González
Sara Gutiérrez
Pablo Tellería
Cristina Novoa
Silvia Rojo Rello
Antonio Garcia-Blesa
Rosa Sedano
Ana María Martínez García
Sonsoles Garcinuño Pérez
Marta Domínguez-Gil
Cristina Hernán García
Ma Mercedes Guerra
Eduardo Muñoz-Sánchez
Cristina Barragan-Pérez
Soraya Diez Morales
Oriana Casazza Donnarumma
Daniel Ramos Pollo
Natalia Santamarta Solla
Paula Ma Álvarez Manzanares
Sara Bravo
Cristina García Alonso
Luis Alberto Avendaño Fernández
Jenifer Gay Alonso
José A. Garrote
Eduardo Arranz
José María Eiros
Fernando Rescalvo Santiago
Carolina Quevedo Villegas
Eduardo Tamayo
Eduardo Tamayo
Antonio Orduña
Carlos Dueñas
María Jesús Peñarrubia
Sara Cuesta-Sancho
María Montoya
David Bernardo
David Bernardo
author_facet Juan H-Vázquez
Paloma Cal-Sabater
Elisa Arribas-Rodríguez
Aida Fiz-López
Candido Perez-Segurado
Álvaro Martín-Muñoz
Ángel De Prado
Marina Perez Mazzali
Carolina G. de Castro
Alejandro G. del Hierro
Ignacio de la Fuente Graciani
Sonia Pérez González
Sara Gutiérrez
Pablo Tellería
Cristina Novoa
Silvia Rojo Rello
Antonio Garcia-Blesa
Rosa Sedano
Ana María Martínez García
Sonsoles Garcinuño Pérez
Marta Domínguez-Gil
Cristina Hernán García
Ma Mercedes Guerra
Eduardo Muñoz-Sánchez
Cristina Barragan-Pérez
Soraya Diez Morales
Oriana Casazza Donnarumma
Daniel Ramos Pollo
Natalia Santamarta Solla
Paula Ma Álvarez Manzanares
Sara Bravo
Cristina García Alonso
Luis Alberto Avendaño Fernández
Jenifer Gay Alonso
José A. Garrote
Eduardo Arranz
José María Eiros
Fernando Rescalvo Santiago
Carolina Quevedo Villegas
Eduardo Tamayo
Eduardo Tamayo
Antonio Orduña
Carlos Dueñas
María Jesús Peñarrubia
Sara Cuesta-Sancho
María Montoya
David Bernardo
David Bernardo
author_sort Juan H-Vázquez
collection DOAJ
description IntroductionCoronavirus disease 2019 (COVID-19) affects the population unequally, with a greater impact on older and immunosuppressed people.MethodsHence, we performed a prospective experimental cohort study to characterise the effect of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in immune-compromised patients (older adults and oncohaematologic patients), compared with healthy counterparts, based on deep characterisation of the circulating immune cell subsets.Results and discussionWhile acquired humoral and cellular memory did not predict subsequent infection 18 months after full vaccination, spectral and computational cytometry revealed several subsets within the CD8+ T-cells, B-cells, natural killer (NK) cells, monocytes and TEMRA Tγδ cells that were differentially expressed in individuals who were subsequently infected and not infected not just following immunisation, but also prior to vaccination. Of note, we found up to seven clusters within the TEMRA Tγδ cell population, with some of them being expanded and others decreased in subsequently infected individuals. Moreover, some of these cellular clusters were also related to COVID-19-induced hospitalisation in oncohaematologic patients. Therefore, we have identified a cellular signature that even before vaccination is related to COVID-19 vulnerability as opposed to the acquisition of cellular and/or humoral memory following vaccination with SARS-CoV-2 messenger RNA (mRNA) vaccines.
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spelling doaj-art-5e00e40de8c641538e2fc8cc4ff5fa3f2024-11-14T06:21:14ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-11-011510.3389/fimmu.2024.14052171405217Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adultsJuan H-Vázquez0Paloma Cal-Sabater1Elisa Arribas-Rodríguez2Aida Fiz-López3Candido Perez-Segurado4Álvaro Martín-Muñoz5Ángel De Prado6Marina Perez Mazzali7Carolina G. de Castro8Alejandro G. del Hierro9Ignacio de la Fuente Graciani10Sonia Pérez González11Sara Gutiérrez12Pablo Tellería13Cristina Novoa14Silvia Rojo Rello15Antonio Garcia-Blesa16Rosa Sedano17Ana María Martínez García18Sonsoles Garcinuño Pérez19Marta Domínguez-Gil20Cristina Hernán García21Ma Mercedes Guerra22Eduardo Muñoz-Sánchez23Cristina Barragan-Pérez24Soraya Diez Morales25Oriana Casazza Donnarumma26Daniel Ramos Pollo27Natalia Santamarta Solla28Paula Ma Álvarez Manzanares29Sara Bravo30Cristina García Alonso31Luis Alberto Avendaño Fernández32Jenifer Gay Alonso33José A. Garrote34Eduardo Arranz35José María Eiros36Fernando Rescalvo Santiago37Carolina Quevedo Villegas38Eduardo Tamayo39Eduardo Tamayo40Antonio Orduña41Carlos Dueñas42María Jesús Peñarrubia43Sara Cuesta-Sancho44María Montoya45David Bernardo46David Bernardo47Mucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainFlow Cytometry Facility, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainDepartment of Hematology, Hospital Clínico Universitario de Valladolid, Valladolid, SpainDepartment of Hematology, Hospital Clínico Universitario de Valladolid, Valladolid, SpainInternal Medicine Department, Hospital Clínico Universitario de Valladolid, Valladolid, SpainInternal Medicine Department, Hospital Clínico Universitario de Valladolid, Valladolid, SpainInternal Medicine Department, Hospital Clínico Universitario de Valladolid, Valladolid, SpainMicrobiology and Inmunology Unit, Hospital Clínico Universitario de Valladolid, Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainInternal Medicine Department, Hospital Clínico Universitario de Valladolid, Valladolid, SpainMicrobiology and Inmunology Unit, Hospital Clínico Universitario de Valladolid, Valladolid, SpainMicrobiology and Inmunology Unit, Hospital Clínico Universitario de Valladolid, Valladolid, SpainMicrobiology Department, Hospital Universitario Río Hortega, Valladolid, SpainServicio de Medicina Preventiva, Hospital Clínico Universitario de Valladolid, Valladolid, SpainServicio de Medicina Preventiva, Hospital Clínico Universitario de Valladolid, Valladolid, SpainUnidad de Cuidados Paliativos del Hospital Universitario Río Hortega, Valladolid, SpainUnidad de Cuidados Paliativos del Hospital Universitario Río Hortega, Valladolid, SpainUnidad de Cuidados Paliativos del Hospital Universitario Río Hortega, Valladolid, SpainUnidad de Cuidados Paliativos del Hospital Universitario Río Hortega, Valladolid, SpainUnidad de Cuidados Paliativos del Hospital Universitario Río Hortega, Valladolid, SpainUnidad de Cuidados Paliativos del Hospital Universitario Río Hortega, Valladolid, SpainUnidad de Cuidados Paliativos del Hospital Universitario Río Hortega, Valladolid, SpainDepartment of Hematology, Hospital Clínico Universitario de Valladolid, Valladolid, SpainDepartment of Hematology, Hospital Clínico Universitario de Valladolid, Valladolid, SpainServicio de Prevención de Riesgos Laborales, Hospital Clínico Universitario de Valladolid, Valladolid, Spain0Residencia y Centro de Día ORPEA Valladolid, Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, SpainMicrobiology Department, Hospital Universitario Río Hortega, Valladolid, SpainServicio de Prevención de Riesgos Laborales, Hospital Clínico Universitario de Valladolid, Valladolid, SpainServicio de Prevención de Riesgos Laborales, Hospital Clínico Universitario de Valladolid, Valladolid, Spain1Unidad Investigación, Hospital Clínico Universitario de Valladolid, Valladolid, Spain2Centro de Investigaciones Biomédicas en Red de Enfermedades Infecciosas (CIBERINFEC), Madrid, SpainMicrobiology and Inmunology Unit, Hospital Clínico Universitario de Valladolid, Valladolid, SpainInternal Medicine Department, Hospital Clínico Universitario de Valladolid, Valladolid, SpainDepartment of Hematology, Hospital Clínico Universitario de Valladolid, Valladolid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, Spain3Viral Immunology, Therapies and Vaccines Lab, Centro de Investigaciones Biológicas Margarita Salas (CIB), Madrid, SpainMucosal Immunology Lab, Unit of Excellence Institute of Biomedicine and Molecular Genetics of Valladolid (IBGM, University of Valladolid-CSIC), Valladolid, Spain2Centro de Investigaciones Biomédicas en Red de Enfermedades Infecciosas (CIBERINFEC), Madrid, SpainIntroductionCoronavirus disease 2019 (COVID-19) affects the population unequally, with a greater impact on older and immunosuppressed people.MethodsHence, we performed a prospective experimental cohort study to characterise the effect of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) vaccination in immune-compromised patients (older adults and oncohaematologic patients), compared with healthy counterparts, based on deep characterisation of the circulating immune cell subsets.Results and discussionWhile acquired humoral and cellular memory did not predict subsequent infection 18 months after full vaccination, spectral and computational cytometry revealed several subsets within the CD8+ T-cells, B-cells, natural killer (NK) cells, monocytes and TEMRA Tγδ cells that were differentially expressed in individuals who were subsequently infected and not infected not just following immunisation, but also prior to vaccination. Of note, we found up to seven clusters within the TEMRA Tγδ cell population, with some of them being expanded and others decreased in subsequently infected individuals. Moreover, some of these cellular clusters were also related to COVID-19-induced hospitalisation in oncohaematologic patients. Therefore, we have identified a cellular signature that even before vaccination is related to COVID-19 vulnerability as opposed to the acquisition of cellular and/or humoral memory following vaccination with SARS-CoV-2 messenger RNA (mRNA) vaccines.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1405217/fullcomputational cytometryvaccine failureCOVID-19immunomeimmunocompromised adult
spellingShingle Juan H-Vázquez
Paloma Cal-Sabater
Elisa Arribas-Rodríguez
Aida Fiz-López
Candido Perez-Segurado
Álvaro Martín-Muñoz
Ángel De Prado
Marina Perez Mazzali
Carolina G. de Castro
Alejandro G. del Hierro
Ignacio de la Fuente Graciani
Sonia Pérez González
Sara Gutiérrez
Pablo Tellería
Cristina Novoa
Silvia Rojo Rello
Antonio Garcia-Blesa
Rosa Sedano
Ana María Martínez García
Sonsoles Garcinuño Pérez
Marta Domínguez-Gil
Cristina Hernán García
Ma Mercedes Guerra
Eduardo Muñoz-Sánchez
Cristina Barragan-Pérez
Soraya Diez Morales
Oriana Casazza Donnarumma
Daniel Ramos Pollo
Natalia Santamarta Solla
Paula Ma Álvarez Manzanares
Sara Bravo
Cristina García Alonso
Luis Alberto Avendaño Fernández
Jenifer Gay Alonso
José A. Garrote
Eduardo Arranz
José María Eiros
Fernando Rescalvo Santiago
Carolina Quevedo Villegas
Eduardo Tamayo
Eduardo Tamayo
Antonio Orduña
Carlos Dueñas
María Jesús Peñarrubia
Sara Cuesta-Sancho
María Montoya
David Bernardo
David Bernardo
Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adults
Frontiers in Immunology
computational cytometry
vaccine failure
COVID-19
immunome
immunocompromised adult
title Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adults
title_full Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adults
title_fullStr Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adults
title_full_unstemmed Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adults
title_short Unbiased immunome characterisation correlates with COVID-19 mRNA vaccine failure in immunocompromised adults
title_sort unbiased immunome characterisation correlates with covid 19 mrna vaccine failure in immunocompromised adults
topic computational cytometry
vaccine failure
COVID-19
immunome
immunocompromised adult
url https://www.frontiersin.org/articles/10.3389/fimmu.2024.1405217/full
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