Stenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalance

Abstract In this pilot study, we assessed the role of autophagy in Crohn’s Disease (CD), particularly in patients with a stenosing phenotype. Through the analysis of biopsied specimens from 36 patients, including 11 controls and 25 CD patients, categorized into inflammatory and stenosing groups, we...

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Main Authors: Leonardo Schirone, Maria Carla Di Paolo, Daniele Vecchio, Cristina Nocella, Alessandra D’Amico, Riccardo Urgesi, Lorella Pallotta, Gianfranco Fanello, Giuseppe Villotti, Maria Giovanna Graziani, Mariangela Peruzzi, Elena De Falco, Roberto Carnevale, Sebastiano Sciarretta, Giacomo Frati, Cristiano Pagnini
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-79308-z
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author Leonardo Schirone
Maria Carla Di Paolo
Daniele Vecchio
Cristina Nocella
Alessandra D’Amico
Riccardo Urgesi
Lorella Pallotta
Gianfranco Fanello
Giuseppe Villotti
Maria Giovanna Graziani
Mariangela Peruzzi
Elena De Falco
Roberto Carnevale
Sebastiano Sciarretta
Giacomo Frati
Cristiano Pagnini
author_facet Leonardo Schirone
Maria Carla Di Paolo
Daniele Vecchio
Cristina Nocella
Alessandra D’Amico
Riccardo Urgesi
Lorella Pallotta
Gianfranco Fanello
Giuseppe Villotti
Maria Giovanna Graziani
Mariangela Peruzzi
Elena De Falco
Roberto Carnevale
Sebastiano Sciarretta
Giacomo Frati
Cristiano Pagnini
author_sort Leonardo Schirone
collection DOAJ
description Abstract In this pilot study, we assessed the role of autophagy in Crohn’s Disease (CD), particularly in patients with a stenosing phenotype. Through the analysis of biopsied specimens from 36 patients, including 11 controls and 25 CD patients, categorized into inflammatory and stenosing groups, we identified a significant reduction in the autophagosomal marker Lc3b-II in patients with active inflammation and stenosis. This was paralleled by an increase in oxidative stress markers, including sNOX2-dp and H2O2, and a decrease in the antioxidant capacity measured by HBA, suggesting an imbalance in autophagy and oxidative stress mechanisms. Additionally, our findings show a correlation between autophagy markers and oxidative stress levels, indicating that autophagy dysfunction may play a pivotal role in CD and in the progression of a stenosing disease phenotype, by failing to eliminate detrimental molecules and pathogenic bacteria, thereby promoting fibrosis. This study is the first to demonstrate in vivo autophagy inhibition in stenosing CD patients and suggests that stimulating autophagic processes could offer a new avenue for the prevention and treatment of intestinal fibrosis in CD. Our results highlight the importance of exploring the interactions between autophagy, the fibrotic process, and the inflammatory cascade, opening avenues for potential therapeutic interventions in CD management.
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spelling doaj-art-3aeed55b3fd74bc9b75a7bbd123b9beb2024-11-10T12:24:00ZengNature PortfolioScientific Reports2045-23222024-11-011411710.1038/s41598-024-79308-zStenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalanceLeonardo Schirone0Maria Carla Di Paolo1Daniele Vecchio2Cristina Nocella3Alessandra D’Amico4Riccardo Urgesi5Lorella Pallotta6Gianfranco Fanello7Giuseppe Villotti8Maria Giovanna Graziani9Mariangela Peruzzi10Elena De Falco11Roberto Carnevale12Sebastiano Sciarretta13Giacomo Frati14Cristiano Pagnini15IRCCS NeuromedS. Giovanni Addolorata HospitalDepartment of Medical and Surgical Sciences and Biotechnologies, Sapienza University of RomeDepartment of Clinical Internal, Anesthesiology and Cardiovascular Sciences, Sapienza University of RomeDepartment of Medical and Surgical Sciences and Biotechnologies, Sapienza University of RomeS. Giovanni Addolorata HospitalS. Giovanni Addolorata HospitalS. Giovanni Addolorata HospitalS. Giovanni Addolorata HospitalS. Giovanni Addolorata HospitalDepartment of Clinical Internal, Anesthesiology and Cardiovascular Sciences, Sapienza University of RomeDepartment of Medical and Surgical Sciences and Biotechnologies, Sapienza University of RomeIRCCS NeuromedIRCCS NeuromedIRCCS NeuromedS. Giovanni Addolorata HospitalAbstract In this pilot study, we assessed the role of autophagy in Crohn’s Disease (CD), particularly in patients with a stenosing phenotype. Through the analysis of biopsied specimens from 36 patients, including 11 controls and 25 CD patients, categorized into inflammatory and stenosing groups, we identified a significant reduction in the autophagosomal marker Lc3b-II in patients with active inflammation and stenosis. This was paralleled by an increase in oxidative stress markers, including sNOX2-dp and H2O2, and a decrease in the antioxidant capacity measured by HBA, suggesting an imbalance in autophagy and oxidative stress mechanisms. Additionally, our findings show a correlation between autophagy markers and oxidative stress levels, indicating that autophagy dysfunction may play a pivotal role in CD and in the progression of a stenosing disease phenotype, by failing to eliminate detrimental molecules and pathogenic bacteria, thereby promoting fibrosis. This study is the first to demonstrate in vivo autophagy inhibition in stenosing CD patients and suggests that stimulating autophagic processes could offer a new avenue for the prevention and treatment of intestinal fibrosis in CD. Our results highlight the importance of exploring the interactions between autophagy, the fibrotic process, and the inflammatory cascade, opening avenues for potential therapeutic interventions in CD management.https://doi.org/10.1038/s41598-024-79308-zInflammatory Bowel Disease (IBD)Autophagic DysregulationReactive Oxygen Species (ROS)Fibrostenotic ComplicationsRedox Homeostasis
spellingShingle Leonardo Schirone
Maria Carla Di Paolo
Daniele Vecchio
Cristina Nocella
Alessandra D’Amico
Riccardo Urgesi
Lorella Pallotta
Gianfranco Fanello
Giuseppe Villotti
Maria Giovanna Graziani
Mariangela Peruzzi
Elena De Falco
Roberto Carnevale
Sebastiano Sciarretta
Giacomo Frati
Cristiano Pagnini
Stenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalance
Scientific Reports
Inflammatory Bowel Disease (IBD)
Autophagic Dysregulation
Reactive Oxygen Species (ROS)
Fibrostenotic Complications
Redox Homeostasis
title Stenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalance
title_full Stenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalance
title_fullStr Stenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalance
title_full_unstemmed Stenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalance
title_short Stenosing Crohn’s disease patients display gut autophagy/oxidative stress imbalance
title_sort stenosing crohn s disease patients display gut autophagy oxidative stress imbalance
topic Inflammatory Bowel Disease (IBD)
Autophagic Dysregulation
Reactive Oxygen Species (ROS)
Fibrostenotic Complications
Redox Homeostasis
url https://doi.org/10.1038/s41598-024-79308-z
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