Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory Mechanisms

ABSTRACT Regulatory T cell (Treg)‐derived extracellular vesicles (EVs) represent a contact‐independent mechanism by which Tregs suppress dysregulated immune responses. These EVs carry diverse immunomodulatory molecules, including CD73, an ectoenzyme that hydrolyses AMP into adenosine. Adenosine subs...

Full description

Saved in:
Bibliographic Details
Main Authors: Carolina Rojas, Michelle García, Luis González‐Osuna, Mauricio Campos‐Mora, Enrique Ponce deLeón, Alfredo Sierra‐Cristancho, Claudia Terraza, Cristian Cortez, Luis Daniel Sansores‐España, Paola Carvajal, Jordan Bazoer, Qi Peng, Charlotte Lawson, Lesley A. Smyth, Karina Pino‐Lagos, Rolando Vernal
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Journal of Extracellular Vesicles
Subjects:
Online Access:https://doi.org/10.1002/jev2.70118
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849730441934798848
author Carolina Rojas
Michelle García
Luis González‐Osuna
Mauricio Campos‐Mora
Enrique Ponce deLeón
Alfredo Sierra‐Cristancho
Claudia Terraza
Cristian Cortez
Luis Daniel Sansores‐España
Paola Carvajal
Jordan Bazoer
Qi Peng
Charlotte Lawson
Lesley A. Smyth
Karina Pino‐Lagos
Rolando Vernal
author_facet Carolina Rojas
Michelle García
Luis González‐Osuna
Mauricio Campos‐Mora
Enrique Ponce deLeón
Alfredo Sierra‐Cristancho
Claudia Terraza
Cristian Cortez
Luis Daniel Sansores‐España
Paola Carvajal
Jordan Bazoer
Qi Peng
Charlotte Lawson
Lesley A. Smyth
Karina Pino‐Lagos
Rolando Vernal
author_sort Carolina Rojas
collection DOAJ
description ABSTRACT Regulatory T cell (Treg)‐derived extracellular vesicles (EVs) represent a contact‐independent mechanism by which Tregs suppress dysregulated immune responses. These EVs carry diverse immunomodulatory molecules, including CD73, an ectoenzyme that hydrolyses AMP into adenosine. Adenosine subsequently acts as a potent immunosuppressive mediator that inhibits effector CD4⁺ T cell activation and controls pathological inflammation. Periodontitis is a highly prevalent inflammatory disease characterised by the accumulation of IL‐17A‐expressing CD4⁺ T cells in response to dysbiotic oral bacterial biofilms, ultimately leading to RANKL‐mediated alveolar bone resorption and tooth loss. We tested the hypothesis that CD73⁺ Treg‐derived EVs, isolated from Tregs induced with polarising cytokines in the presence of retinoic acid, could limit inflammation and prevent alveolar bone loss in periodontitis. Our findings demonstrate that Tregs induced with polarising cytokines in the presence of retinoic acid express high levels of CD73 and secrete adenosine‐producing suppressive CD73+ EVs. Furthermore, local administration of these CD73⁺ Treg‐derived EVs in a murine periodontitis model reduced activated CD4⁺ T cell infiltration, decreased IL‐17A and RANKL expression, and attenuated osteoclast‐mediated alveolar bone loss. In conclusion, retinoic acid‐induced Treg‐derived EVs suppress CD4⁺ T cell‐driven inflammation and ameliorate periodontitis, at least in part through CD73/adenosine‐dependent immunomodulatory mechanisms.
format Article
id doaj-art-6c909ce885fa4849b6f87f7b0b75dbbd
institution DOAJ
issn 2001-3078
language English
publishDate 2025-07-01
publisher Wiley
record_format Article
series Journal of Extracellular Vesicles
spelling doaj-art-6c909ce885fa4849b6f87f7b0b75dbbd2025-08-20T03:08:52ZengWileyJournal of Extracellular Vesicles2001-30782025-07-01147n/an/a10.1002/jev2.70118Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory MechanismsCarolina Rojas0Michelle García1Luis González‐Osuna2Mauricio Campos‐Mora3Enrique Ponce deLeón4Alfredo Sierra‐Cristancho5Claudia Terraza6Cristian Cortez7Luis Daniel Sansores‐España8Paola Carvajal9Jordan Bazoer10Qi Peng11Charlotte Lawson12Lesley A. Smyth13Karina Pino‐Lagos14Rolando Vernal15Laboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileLaboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileLaboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileCentro de Investigación e Innovación Biomédica, Faculty of Medicine Universidad de Los Andes Santiago ChileDepartamento de Rehabilitación Oral, Faculty of Dentistry Universidad de Chile Santiago ChileLaboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileLaboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileEscuela de Tecnología Médica, Faculty of Sciences Pontificia Universidad Católica de Valparaíso Valparaíso ChileLaboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileLaboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileSchool of Medicine and Biomedical Sciences University of West London London UKCentre for Nephrology, Urology and Transplantation, School of Immunology and Mucosal Biology King's College London London UKComparative Biomedical Sciences Royal Veterinary College London UKSchool of Medicine and Biomedical Sciences University of West London London UKCentro de Investigación e Innovación Biomédica, Faculty of Medicine Universidad de Los Andes Santiago ChileLaboratorio de Biología Periodontal, Faculty of Dentistry Universidad de Chile Santiago ChileABSTRACT Regulatory T cell (Treg)‐derived extracellular vesicles (EVs) represent a contact‐independent mechanism by which Tregs suppress dysregulated immune responses. These EVs carry diverse immunomodulatory molecules, including CD73, an ectoenzyme that hydrolyses AMP into adenosine. Adenosine subsequently acts as a potent immunosuppressive mediator that inhibits effector CD4⁺ T cell activation and controls pathological inflammation. Periodontitis is a highly prevalent inflammatory disease characterised by the accumulation of IL‐17A‐expressing CD4⁺ T cells in response to dysbiotic oral bacterial biofilms, ultimately leading to RANKL‐mediated alveolar bone resorption and tooth loss. We tested the hypothesis that CD73⁺ Treg‐derived EVs, isolated from Tregs induced with polarising cytokines in the presence of retinoic acid, could limit inflammation and prevent alveolar bone loss in periodontitis. Our findings demonstrate that Tregs induced with polarising cytokines in the presence of retinoic acid express high levels of CD73 and secrete adenosine‐producing suppressive CD73+ EVs. Furthermore, local administration of these CD73⁺ Treg‐derived EVs in a murine periodontitis model reduced activated CD4⁺ T cell infiltration, decreased IL‐17A and RANKL expression, and attenuated osteoclast‐mediated alveolar bone loss. In conclusion, retinoic acid‐induced Treg‐derived EVs suppress CD4⁺ T cell‐driven inflammation and ameliorate periodontitis, at least in part through CD73/adenosine‐dependent immunomodulatory mechanisms.https://doi.org/10.1002/jev2.701185’‐nucleotidaseadenosineextracellular vesiclesperiodontitisregulatory T cellretinoic acid
spellingShingle Carolina Rojas
Michelle García
Luis González‐Osuna
Mauricio Campos‐Mora
Enrique Ponce deLeón
Alfredo Sierra‐Cristancho
Claudia Terraza
Cristian Cortez
Luis Daniel Sansores‐España
Paola Carvajal
Jordan Bazoer
Qi Peng
Charlotte Lawson
Lesley A. Smyth
Karina Pino‐Lagos
Rolando Vernal
Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory Mechanisms
Journal of Extracellular Vesicles
5’‐nucleotidase
adenosine
extracellular vesicles
periodontitis
regulatory T cell
retinoic acid
title Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory Mechanisms
title_full Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory Mechanisms
title_fullStr Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory Mechanisms
title_full_unstemmed Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory Mechanisms
title_short Induced Treg‐Derived Extracellular Vesicles Suppress CD4+ T‐Cell‐Mediated Inflammation and Ameliorate Bone Loss During Periodontitis Partly Through CD73/Adenosine‐Dependent Immunomodulatory Mechanisms
title_sort induced treg derived extracellular vesicles suppress cd4 t cell mediated inflammation and ameliorate bone loss during periodontitis partly through cd73 adenosine dependent immunomodulatory mechanisms
topic 5’‐nucleotidase
adenosine
extracellular vesicles
periodontitis
regulatory T cell
retinoic acid
url https://doi.org/10.1002/jev2.70118
work_keys_str_mv AT carolinarojas inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT michellegarcia inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT luisgonzalezosuna inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT mauriciocamposmora inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT enriqueponcedeleon inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT alfredosierracristancho inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT claudiaterraza inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT cristiancortez inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT luisdanielsansoresespana inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT paolacarvajal inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT jordanbazoer inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT qipeng inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT charlottelawson inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT lesleyasmyth inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT karinapinolagos inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms
AT rolandovernal inducedtregderivedextracellularvesiclessuppresscd4tcellmediatedinflammationandamelioratebonelossduringperiodontitispartlythroughcd73adenosinedependentimmunomodulatorymechanisms