Modeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups

Abstract Idiopathic Nephrotic Syndrome (INS) is a common childhood glomerular disease requiring intense immunosuppressive drug treatments. Prediction of treatment response and the occurrence of relapses remains challenging. Biofluid-derived extracellular vesicles (EVs) may serve as novel liquid biop...

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Main Authors: Giulia Cricri, Andrea Gobbini, Stefania Bruno, Linda Bellucci, Sarah Tassinari, Federico Caicci, Chiara Tamburello, Teresa Nittoli, Irene Paraboschi, Alfredo Berrettini, Renata Grifantini, Benedetta Bussolati, William Morello, Giovanni Montini, Federica Collino
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Language:English
Published: Nature Portfolio 2024-10-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-76727-w
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author Giulia Cricri
Andrea Gobbini
Stefania Bruno
Linda Bellucci
Sarah Tassinari
Federico Caicci
Chiara Tamburello
Teresa Nittoli
Irene Paraboschi
Alfredo Berrettini
Renata Grifantini
Benedetta Bussolati
William Morello
Giovanni Montini
Federica Collino
author_facet Giulia Cricri
Andrea Gobbini
Stefania Bruno
Linda Bellucci
Sarah Tassinari
Federico Caicci
Chiara Tamburello
Teresa Nittoli
Irene Paraboschi
Alfredo Berrettini
Renata Grifantini
Benedetta Bussolati
William Morello
Giovanni Montini
Federica Collino
author_sort Giulia Cricri
collection DOAJ
description Abstract Idiopathic Nephrotic Syndrome (INS) is a common childhood glomerular disease requiring intense immunosuppressive drug treatments. Prediction of treatment response and the occurrence of relapses remains challenging. Biofluid-derived extracellular vesicles (EVs) may serve as novel liquid biopsies for INS classification and monitoring. Our cohort was composed of 105 INS children at different clinical time points (onset, relapse, and persistent proteinuria, remission, respectively), and 19 healthy controls. The expression of 37 surface EV surface markers was evaluated by flow cytometry in serum (n = 83) and urine (n = 74) from INS children (mean age = 10.1, 58% males) at different time points. Urine EVs (n = 7) and serum EVs (n = 11) from age-matched healthy children (mean age = 7.8, 94% males) were also analyzed. Tetraspanin expression in urine EVs was enhanced during active disease phase in respect to the remission group and positively correlates with proteinuria levels. Unsupervised clustering analysis identified an INS signature of 8 markers related to immunity and angiogenesis/adhesion processes. The CD41b, CD29, and CD105 showed the best diagnostic scores separating the INS active phase from the healthy condition. Interestingly, combining urinary and serum EV markers from the same patient improved the precision of clinical staging separation. Three urinary biomarkers (CD19, CD44, and CD8) were able to classify INS based on steroid sensitivity. Biofluid EVs offer a non-invasive tool for INS clinical subclassification and “personalized” interventions.
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spelling doaj-art-dc611bf76e4c463db0a0a87791899b922024-12-08T12:25:23ZengNature PortfolioScientific Reports2045-23222024-10-0114111510.1038/s41598-024-76727-wModeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroupsGiulia Cricri0Andrea Gobbini1Stefania Bruno2Linda Bellucci3Sarah Tassinari4Federico Caicci5Chiara Tamburello6Teresa Nittoli7Irene Paraboschi8Alfredo Berrettini9Renata Grifantini10Benedetta Bussolati11William Morello12Giovanni Montini13Federica Collino14Laboratory of Translational Research in Paediatric Nephro-Urology, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoIstituto Nazionale Genetica Molecolare (INGM), Istituto Nazionale Genetica Molecolare Romeo ed Enrica InvernizziDepartment of Medical Sciences, University of TurinLaboratory of Translational Research in Paediatric Nephro-Urology, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoDepartment of Molecular Biotechnology and Health Sciences, University of TurinDepartment of Biology, University of PadovaPaediatric Nephrology, Dialysis and Transplant Unit, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoPaediatric Nephrology, Dialysis and Transplant Unit, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoPediatric Urology Unit, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoPediatric Urology Unit, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoIstituto Nazionale Genetica Molecolare (INGM), Istituto Nazionale Genetica Molecolare Romeo ed Enrica InvernizziDepartment of Medical Sciences, University of TurinPaediatric Nephrology, Dialysis and Transplant Unit, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoLaboratory of Translational Research in Paediatric Nephro-Urology, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoLaboratory of Translational Research in Paediatric Nephro-Urology, Fondazione IRCCS Ca’ Granda-Ospedale Maggiore PoliclinicoAbstract Idiopathic Nephrotic Syndrome (INS) is a common childhood glomerular disease requiring intense immunosuppressive drug treatments. Prediction of treatment response and the occurrence of relapses remains challenging. Biofluid-derived extracellular vesicles (EVs) may serve as novel liquid biopsies for INS classification and monitoring. Our cohort was composed of 105 INS children at different clinical time points (onset, relapse, and persistent proteinuria, remission, respectively), and 19 healthy controls. The expression of 37 surface EV surface markers was evaluated by flow cytometry in serum (n = 83) and urine (n = 74) from INS children (mean age = 10.1, 58% males) at different time points. Urine EVs (n = 7) and serum EVs (n = 11) from age-matched healthy children (mean age = 7.8, 94% males) were also analyzed. Tetraspanin expression in urine EVs was enhanced during active disease phase in respect to the remission group and positively correlates with proteinuria levels. Unsupervised clustering analysis identified an INS signature of 8 markers related to immunity and angiogenesis/adhesion processes. The CD41b, CD29, and CD105 showed the best diagnostic scores separating the INS active phase from the healthy condition. Interestingly, combining urinary and serum EV markers from the same patient improved the precision of clinical staging separation. Three urinary biomarkers (CD19, CD44, and CD8) were able to classify INS based on steroid sensitivity. Biofluid EVs offer a non-invasive tool for INS clinical subclassification and “personalized” interventions.https://doi.org/10.1038/s41598-024-76727-wIdiopathic nephrotic syndromeExtracellular vesiclesProtein biomarkersSteroid resistance
spellingShingle Giulia Cricri
Andrea Gobbini
Stefania Bruno
Linda Bellucci
Sarah Tassinari
Federico Caicci
Chiara Tamburello
Teresa Nittoli
Irene Paraboschi
Alfredo Berrettini
Renata Grifantini
Benedetta Bussolati
William Morello
Giovanni Montini
Federica Collino
Modeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups
Scientific Reports
Idiopathic nephrotic syndrome
Extracellular vesicles
Protein biomarkers
Steroid resistance
title Modeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups
title_full Modeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups
title_fullStr Modeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups
title_full_unstemmed Modeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups
title_short Modeling a biofluid-derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups
title_sort modeling a biofluid derived extracellular vesicle surface signature to differentiate pediatric idiopathic nephrotic syndrome clinical subgroups
topic Idiopathic nephrotic syndrome
Extracellular vesicles
Protein biomarkers
Steroid resistance
url https://doi.org/10.1038/s41598-024-76727-w
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