Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus
Objectives: To gain insights into the pathogenesis of neuropsychiatric systemic lupus erythematosus (NPSLE) and identify potential drug targets through investigation of whole-blood human transcriptome. Methods: We analysed differentially expressed genes in peripheral blood from active central nervou...
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2025-12-01
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| Series: | Journal of Translational Autoimmunity |
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| author | Julius Lindblom Guillermo Barturen Lorenzo Beretta Daniel Toro-Domínguez Elena Carnero-Montoro Maria Orietta Borghi Jessica Castillo Ellen Iacobaeus Yvonne Enman Chandra Mohan Marta E. Alarcón-Riquelme Dionysis Nikolopoulos Ioannis Parodis Jacques-Olivier Pers Alain Saraux Valérie Devauchelle-Pensec Sandrine Jousse-Joulin Bernard Lauwerys Julie Ducreux Anne-Lise Maudoux Ana Tavares Isabel Almeida Miguel Angel Gonzalez-Gay Mantecón Ricardo Blanco Alonso Alfonso Corrales Martínez Ignasi Rodríguez-Pintó Gerard Espinosa Rik Lories Nicolas Hunzelmann Doreen Belz Niklas Baerlecken Michael Zauner Michaela Lehner Eduardo Collantes Ma Angeles Aguirre-Zamorano Alejandro Escudero-Contreras Ma Carmen Castro-Villegas Norberto Ortego María Concepción Fernández Roldán Enrique Raya Inmaculada Jiménez Moleón Enrique de Ramon Isabel Díaz Quintero Pier Luigi Meroni Tommaso Schioppo Carolina Artusi Carlo Chizzolini Aleksandra Zuber Donatienne Wynar Attila Balog Magdolna Deák Márta Bocskai Sonja Dulic Gabriella Kádár Falk Hiepe Silvia Thiel Manuel Rodriguez Maresca Antonio López-Berrio Rocío Aguilar-Quesada Héctor Navarro-Linares |
| author_facet | Julius Lindblom Guillermo Barturen Lorenzo Beretta Daniel Toro-Domínguez Elena Carnero-Montoro Maria Orietta Borghi Jessica Castillo Ellen Iacobaeus Yvonne Enman Chandra Mohan Marta E. Alarcón-Riquelme Dionysis Nikolopoulos Ioannis Parodis Jacques-Olivier Pers Alain Saraux Valérie Devauchelle-Pensec Sandrine Jousse-Joulin Bernard Lauwerys Julie Ducreux Anne-Lise Maudoux Ana Tavares Isabel Almeida Miguel Angel Gonzalez-Gay Mantecón Ricardo Blanco Alonso Alfonso Corrales Martínez Ignasi Rodríguez-Pintó Gerard Espinosa Rik Lories Nicolas Hunzelmann Doreen Belz Niklas Baerlecken Michael Zauner Michaela Lehner Eduardo Collantes Ma Angeles Aguirre-Zamorano Alejandro Escudero-Contreras Ma Carmen Castro-Villegas Norberto Ortego María Concepción Fernández Roldán Enrique Raya Inmaculada Jiménez Moleón Enrique de Ramon Isabel Díaz Quintero Pier Luigi Meroni Tommaso Schioppo Carolina Artusi Carlo Chizzolini Aleksandra Zuber Donatienne Wynar Attila Balog Magdolna Deák Márta Bocskai Sonja Dulic Gabriella Kádár Falk Hiepe Silvia Thiel Manuel Rodriguez Maresca Antonio López-Berrio Rocío Aguilar-Quesada Héctor Navarro-Linares |
| author_sort | Julius Lindblom |
| collection | DOAJ |
| description | Objectives: To gain insights into the pathogenesis of neuropsychiatric systemic lupus erythematosus (NPSLE) and identify potential drug targets through investigation of whole-blood human transcriptome. Methods: We analysed differentially expressed genes in peripheral blood from active central nervous system (CNS) lupus (n = 26) and active non-neuropsychiatric SLE (n = 38) patients versus healthy controls (n = 497) from the European PRECISESADS project (NTC02890121). We further explored dysregulated gene modules in active CNS lupus and their correlation with serological markers. Lastly, we performed regulatory network and druggability analysis. Results: Unsupervised weighted gene co-expression network analysis (WGCNA) revealed 23 dysregulated gene modules and two subgroups of active CNS lupus. The interferon gene module was prominently upregulated in subgroup 1, while the B cell, T cell, and cytotoxic/natural killer (NK) cell modules were downregulated. Subgroup 2 showed less marked dysregulation patterns. Subgroup 1 had lower estimated proportions of lymphoid cell subsets and proportionally more patients positive for anti-dsDNA antibodies compared to subgroup 2, pointing to molecularly distinct subgroups or misclassification of subgroup 2. In silico prediction algorithms demonstrated a greater anticipated response to anifrolumab, C3 inhibitors, and calcineurin inhibitors for patients in CNS lupus subgroup 1 compared with subgroup 2. Conclusions: Gene dysregulation patterns related to innate and adaptive lymphoid immunity separated active CNS lupus patients into two distinct subgroups with differential anticipated response to type I interferon, C3, and calcineurin inhibition. Our study provides a conceptual framework for precision medicine in NPSLE and implications for overcoming the major clinical challenge of attributing neuropsychiatric features to SLE versus other causes. |
| format | Article |
| id | doaj-art-998fca04c7b64acfaa40135f146e8006 |
| institution | DOAJ |
| issn | 2589-9090 |
| language | English |
| publishDate | 2025-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Journal of Translational Autoimmunity |
| spelling | doaj-art-998fca04c7b64acfaa40135f146e80062025-08-20T03:15:54ZengElsevierJournal of Translational Autoimmunity2589-90902025-12-011110029610.1016/j.jtauto.2025.100296Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosusJulius Lindblom0Guillermo Barturen1Lorenzo Beretta2Daniel Toro-Domínguez3Elena Carnero-Montoro4Maria Orietta Borghi5Jessica Castillo6Ellen Iacobaeus7Yvonne Enman8Chandra Mohan9Marta E. Alarcón-Riquelme10Dionysis Nikolopoulos11Ioannis Parodis12Jacques-Olivier Pers13Alain Saraux14Valérie Devauchelle-Pensec15Sandrine Jousse-Joulin16Bernard Lauwerys17Julie Ducreux18Anne-Lise Maudoux19Ana Tavares20Isabel Almeida21Miguel Angel Gonzalez-Gay Mantecón22Ricardo Blanco Alonso23Alfonso Corrales Martínez24Ignasi Rodríguez-Pintó25Gerard Espinosa26Rik Lories27Nicolas Hunzelmann28Doreen Belz29Niklas Baerlecken30Michael Zauner31Michaela Lehner32Eduardo Collantes33Ma Angeles Aguirre-Zamorano34Alejandro Escudero-Contreras35Ma Carmen Castro-Villegas36Norberto Ortego37María Concepción Fernández Roldán38Enrique Raya39Inmaculada Jiménez Moleón40Enrique de Ramon41Isabel Díaz Quintero42Pier Luigi Meroni43Tommaso Schioppo44Carolina Artusi45Carlo Chizzolini46Aleksandra Zuber47Donatienne Wynar48Attila Balog49Magdolna Deák50Márta Bocskai51Sonja Dulic52Gabriella Kádár53Falk Hiepe54Silvia Thiel55Manuel Rodriguez Maresca56Antonio López-Berrio57Rocío Aguilar-Quesada58Héctor Navarro-Linares59Division of Rheumatology, Department of Medicine Solna, Karolinska Institutet, and Karolinska University Hospital, SE-17176, Stockholm, Sweden; Center for Molecular Medicine, Stockholm, Sweden; Corresponding author. Division of Rheumatology, Department of Medicine Solna, Karolinska Institutet, and Karolinska University Hospital, SE-17176, Stockholm, Sweden.GENYO, Centre for Genomics and Oncological Research: Pfizer, University of Granada / Andalusian Regional Government, Medical Genomics, Granada, Spain; Department of Genetics, Faculty of Sciences, University of Granada, Granada, SpainReferral Center for Systemic Autoimmune Diseases, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico di Milano, ItalyGENYO, Centre for Genomics and Oncological Research: Pfizer, University of Granada / Andalusian Regional Government, Medical Genomics, Granada, SpainGENYO, Centre for Genomics and Oncological Research: Pfizer, University of Granada / Andalusian Regional Government, Medical Genomics, Granada, SpainDepartment of Clinical Sciences and Community Health, Università Degli Studi di Milano, Milan, Italy; IRCCS, Istituto Auxologico Italiano, Milan, ItalyDepartment of Biomedical Engineering, University of Houston, Houston, TX, USANeuroimmunology Unit, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, SwedenDivision of Rheumatology, Department of Medicine Solna, Karolinska Institutet, and Karolinska University Hospital, SE-17176, Stockholm, Sweden; Center for Molecular Medicine, Stockholm, SwedenDepartment of Biomedical Engineering, University of Houston, Houston, TX, USAGENYO, Centre for Genomics and Oncological Research: Pfizer, University of Granada / Andalusian Regional Government, Medical Genomics, Granada, Spain; Institute of Environmental Medicine, Karolinska Institutet, Stockholm, SwedenDivision of Rheumatology, Department of Medicine Solna, Karolinska Institutet, and Karolinska University Hospital, SE-17176, Stockholm, Sweden; Center for Molecular Medicine, Stockholm, SwedenDivision of Rheumatology, Department of Medicine Solna, Karolinska Institutet, and Karolinska University Hospital, SE-17176, Stockholm, Sweden; Center for Molecular Medicine, Stockholm, Sweden; Department of Rheumatology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden; Corresponding author. Division of Rheumatology, Department of Medicine Solna, Karolinska Institutet, and Karolinska University Hospital, SE-17176, Stockholm, Sweden.Centre Hospitalier Universitaire de Brest, Hospital de la Cavale Blanche, Brest, FranceCentre Hospitalier Universitaire de Brest, Hospital de la Cavale Blanche, Brest, FranceCentre Hospitalier Universitaire de Brest, Hospital de la Cavale Blanche, Brest, FranceCentre Hospitalier Universitaire de Brest, Hospital de la Cavale Blanche, Brest, FrancePôle de pathologies rhumatismales systémiques et inflammatoires, Institut de Recherche Expérimentale et Clinique, Université catholique de Louvain, Brussels, BelgiumPôle de pathologies rhumatismales systémiques et inflammatoires, Institut de Recherche Expérimentale et Clinique, Université catholique de Louvain, Brussels, BelgiumPôle de pathologies rhumatismales systémiques et inflammatoires, Institut de Recherche Expérimentale et Clinique, Université catholique de Louvain, Brussels, BelgiumCentro Hospitalar do Porto, PortugalCentro Hospitalar do Porto, PortugalServicio Cantabro de Salud, Hospital Universitario Marqués de Valdecilla, Santander, SpainServicio Cantabro de Salud, Hospital Universitario Marqués de Valdecilla, Santander, SpainServicio Cantabro de Salud, Hospital Universitario Marqués de Valdecilla, Santander, SpainDepartment of Autoimmune Diseases, Hospital Clínic, Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Catalonia, SpainDepartment of Autoimmune Diseases, Hospital Clínic, Institut d’Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Catalonia, SpainKatholieke Universiteit Leuven, BelgiumKlinikum der Universitaet zu Koeln, Cologne, GermanyKlinikum der Universitaet zu Koeln, Cologne, GermanyMedizinische Hochschule Hannover, GermanyMedical University Vienna, Vienna, AustriaMedical University Vienna, Vienna, AustriaServicio Andaluz de Salud, Hospital Universitario Reina Sofía Córdoba, SpainServicio Andaluz de Salud, Hospital Universitario Reina Sofía Córdoba, SpainServicio Andaluz de Salud, Hospital Universitario Reina Sofía Córdoba, SpainServicio Andaluz de Salud, Hospital Universitario Reina Sofía Córdoba, SpainServicio Andaluz de Salud, Complejo hospitalario Universitario de Granada (Hospital Universitario San Cecilio), SpainServicio Andaluz de Salud, Complejo hospitalario Universitario de Granada (Hospital Universitario San Cecilio), SpainServicio Andaluz de Salud, Complejo hospitalario Universitario de Granada (Hospital Virgen de las Nieves), SpainServicio Andaluz de Salud, Complejo hospitalario Universitario de Granada (Hospital Virgen de las Nieves), SpainServicio Andaluz de Salud, Hospital Regional Universitario de Málaga, SpainServicio Andaluz de Salud, Hospital Regional Universitario de Málaga, SpainUniversità degli studi di Milano, Milan, ItalyUniversità degli studi di Milano, Milan, ItalyUniversità degli studi di Milano, Milan, ItalyHospitaux Universitaires de Genève, SwitzerlandHospitaux Universitaires de Genève, SwitzerlandHospitaux Universitaires de Genève, SwitzerlandUniversity of Szeged, Szeged, HungaryUniversity of Szeged, Szeged, HungaryUniversity of Szeged, Szeged, HungaryUniversity of Szeged, Szeged, HungaryUniversity of Szeged, Szeged, HungaryCharite, Berlin, GermanyCharite, Berlin, GermanyAndalusian Public Health System Biobank, Granada, SpainAndalusian Public Health System Biobank, Granada, SpainAndalusian Public Health System Biobank, Granada, SpainAndalusian Public Health System Biobank, Granada, SpainObjectives: To gain insights into the pathogenesis of neuropsychiatric systemic lupus erythematosus (NPSLE) and identify potential drug targets through investigation of whole-blood human transcriptome. Methods: We analysed differentially expressed genes in peripheral blood from active central nervous system (CNS) lupus (n = 26) and active non-neuropsychiatric SLE (n = 38) patients versus healthy controls (n = 497) from the European PRECISESADS project (NTC02890121). We further explored dysregulated gene modules in active CNS lupus and their correlation with serological markers. Lastly, we performed regulatory network and druggability analysis. Results: Unsupervised weighted gene co-expression network analysis (WGCNA) revealed 23 dysregulated gene modules and two subgroups of active CNS lupus. The interferon gene module was prominently upregulated in subgroup 1, while the B cell, T cell, and cytotoxic/natural killer (NK) cell modules were downregulated. Subgroup 2 showed less marked dysregulation patterns. Subgroup 1 had lower estimated proportions of lymphoid cell subsets and proportionally more patients positive for anti-dsDNA antibodies compared to subgroup 2, pointing to molecularly distinct subgroups or misclassification of subgroup 2. In silico prediction algorithms demonstrated a greater anticipated response to anifrolumab, C3 inhibitors, and calcineurin inhibitors for patients in CNS lupus subgroup 1 compared with subgroup 2. Conclusions: Gene dysregulation patterns related to innate and adaptive lymphoid immunity separated active CNS lupus patients into two distinct subgroups with differential anticipated response to type I interferon, C3, and calcineurin inhibition. Our study provides a conceptual framework for precision medicine in NPSLE and implications for overcoming the major clinical challenge of attributing neuropsychiatric features to SLE versus other causes.http://www.sciencedirect.com/science/article/pii/S2589909025000310Systemic lupus erythematosusNeuropsychiatric systemic lupus erythematosusPrecision medicineDruggabilityBiologicsTranscriptome |
| spellingShingle | Julius Lindblom Guillermo Barturen Lorenzo Beretta Daniel Toro-Domínguez Elena Carnero-Montoro Maria Orietta Borghi Jessica Castillo Ellen Iacobaeus Yvonne Enman Chandra Mohan Marta E. Alarcón-Riquelme Dionysis Nikolopoulos Ioannis Parodis Jacques-Olivier Pers Alain Saraux Valérie Devauchelle-Pensec Sandrine Jousse-Joulin Bernard Lauwerys Julie Ducreux Anne-Lise Maudoux Ana Tavares Isabel Almeida Miguel Angel Gonzalez-Gay Mantecón Ricardo Blanco Alonso Alfonso Corrales Martínez Ignasi Rodríguez-Pintó Gerard Espinosa Rik Lories Nicolas Hunzelmann Doreen Belz Niklas Baerlecken Michael Zauner Michaela Lehner Eduardo Collantes Ma Angeles Aguirre-Zamorano Alejandro Escudero-Contreras Ma Carmen Castro-Villegas Norberto Ortego María Concepción Fernández Roldán Enrique Raya Inmaculada Jiménez Moleón Enrique de Ramon Isabel Díaz Quintero Pier Luigi Meroni Tommaso Schioppo Carolina Artusi Carlo Chizzolini Aleksandra Zuber Donatienne Wynar Attila Balog Magdolna Deák Márta Bocskai Sonja Dulic Gabriella Kádár Falk Hiepe Silvia Thiel Manuel Rodriguez Maresca Antonio López-Berrio Rocío Aguilar-Quesada Héctor Navarro-Linares Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus Journal of Translational Autoimmunity Systemic lupus erythematosus Neuropsychiatric systemic lupus erythematosus Precision medicine Druggability Biologics Transcriptome |
| title | Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus |
| title_full | Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus |
| title_fullStr | Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus |
| title_full_unstemmed | Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus |
| title_short | Dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus |
| title_sort | dysregulation of innate and adaptive lymphoid immunity may have implications for symptom attribution and predict responses to targeted therapies in neuropsychiatric systemic lupus erythematosus |
| topic | Systemic lupus erythematosus Neuropsychiatric systemic lupus erythematosus Precision medicine Druggability Biologics Transcriptome |
| url | http://www.sciencedirect.com/science/article/pii/S2589909025000310 |
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