Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axis

Inflammatory bowel disease (IBD), comprising mainly Crohn’s disease (CD) and ulcerative colitis (UC), is a chronic inflammatory disease of the gastrointestinal tract. In recent years, a wealth of data has been accumulated demonstrating the complex interplay of many different factors in the pathogene...

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Main Authors: Saida Mukanova, Anton Borissenko, Alexey Kim, Aigerim Bolatbek, Ainur Abdrakhmanova, Luca Vangelista, Eva Sonnenberg-Riethmacher, Dieter Riethmacher
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.956691/full
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author Saida Mukanova
Anton Borissenko
Alexey Kim
Aigerim Bolatbek
Ainur Abdrakhmanova
Luca Vangelista
Eva Sonnenberg-Riethmacher
Eva Sonnenberg-Riethmacher
Dieter Riethmacher
Dieter Riethmacher
author_facet Saida Mukanova
Anton Borissenko
Alexey Kim
Aigerim Bolatbek
Ainur Abdrakhmanova
Luca Vangelista
Eva Sonnenberg-Riethmacher
Eva Sonnenberg-Riethmacher
Dieter Riethmacher
Dieter Riethmacher
author_sort Saida Mukanova
collection DOAJ
description Inflammatory bowel disease (IBD), comprising mainly Crohn’s disease (CD) and ulcerative colitis (UC), is a chronic inflammatory disease of the gastrointestinal tract. In recent years, a wealth of data has been accumulated demonstrating the complex interplay of many different factors in the pathogenesis of IBD. Among these are factors impacting the epithelial barrier function, including vessel and extracellular matrix (ECM) formation, the gut microbiome (e.g., bacterial antigens), and, most importantly, the production of cytokines (pro- and anti-inflammatory) directly shaping the immune response. Patients failing to resolve the acute intestinal inflammation develop chronic inflammation. It has been shown that the expression of the matricellular protein periostin is enhanced during IBD and is one of the drivers of this disease. The C-C chemokine receptor 5 (CCR5) is engaged by the chemotactic mediators CCL3/MIP-1α, CCL4/MIP-1β, and CCL5/RANTES. CCR5 blockade has been reported to ameliorate inflammation in a murine IBD model. Thus, both periostin and CCR5 are involved in the development of IBD. In this study, we investigated the potential crosstalk between the two signaling systems and tested a highly potent CCL5 derivative acting as a CCR5 antagonist in a murine model of IBD. We observed that the absence of periostin influences the CCR5-expressing cell population of the gut. Our data further support the notion that targeted modulation of the periostin and CCR5 signaling systems bears therapeutic potential for IBD.
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spelling doaj.art-fdb0dcd3ea714a6c9860721173239b532022-12-22T04:36:56ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-10-011310.3389/fimmu.2022.956691956691Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axisSaida Mukanova0Anton Borissenko1Alexey Kim2Aigerim Bolatbek3Ainur Abdrakhmanova4Luca Vangelista5Eva Sonnenberg-Riethmacher6Eva Sonnenberg-Riethmacher7Dieter Riethmacher8Dieter Riethmacher9Department of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana, KazakhstanDepartment of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana, KazakhstanSchool of Medicine, Nazarbayev University, Astana, KazakhstanDepartment of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana, KazakhstanSchool of Medicine, Nazarbayev University, Astana, KazakhstanDepartment of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana, KazakhstanDepartment of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana, KazakhstanDepartment of Human Development and Health, School of Medicine, University of Southampton, Southampton, United KingdomDepartment of Biomedical Sciences, School of Medicine, Nazarbayev University, Astana, KazakhstanDepartment of Human Development and Health, School of Medicine, University of Southampton, Southampton, United KingdomInflammatory bowel disease (IBD), comprising mainly Crohn’s disease (CD) and ulcerative colitis (UC), is a chronic inflammatory disease of the gastrointestinal tract. In recent years, a wealth of data has been accumulated demonstrating the complex interplay of many different factors in the pathogenesis of IBD. Among these are factors impacting the epithelial barrier function, including vessel and extracellular matrix (ECM) formation, the gut microbiome (e.g., bacterial antigens), and, most importantly, the production of cytokines (pro- and anti-inflammatory) directly shaping the immune response. Patients failing to resolve the acute intestinal inflammation develop chronic inflammation. It has been shown that the expression of the matricellular protein periostin is enhanced during IBD and is one of the drivers of this disease. The C-C chemokine receptor 5 (CCR5) is engaged by the chemotactic mediators CCL3/MIP-1α, CCL4/MIP-1β, and CCL5/RANTES. CCR5 blockade has been reported to ameliorate inflammation in a murine IBD model. Thus, both periostin and CCR5 are involved in the development of IBD. In this study, we investigated the potential crosstalk between the two signaling systems and tested a highly potent CCL5 derivative acting as a CCR5 antagonist in a murine model of IBD. We observed that the absence of periostin influences the CCR5-expressing cell population of the gut. Our data further support the notion that targeted modulation of the periostin and CCR5 signaling systems bears therapeutic potential for IBD.https://www.frontiersin.org/articles/10.3389/fimmu.2022.956691/fullperiostin (POSTN)CCL5-CCR5-signaling systemIBD – inflammatory bowel diseaseinflammationtreatment optionchemically induced colitis
spellingShingle Saida Mukanova
Anton Borissenko
Alexey Kim
Aigerim Bolatbek
Ainur Abdrakhmanova
Luca Vangelista
Eva Sonnenberg-Riethmacher
Eva Sonnenberg-Riethmacher
Dieter Riethmacher
Dieter Riethmacher
Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axis
Frontiers in Immunology
periostin (POSTN)
CCL5-CCR5-signaling system
IBD – inflammatory bowel disease
inflammation
treatment option
chemically induced colitis
title Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axis
title_full Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axis
title_fullStr Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axis
title_full_unstemmed Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axis
title_short Role of periostin in inflammatory bowel disease development and synergistic effects mediated by the CCL5–CCR5 axis
title_sort role of periostin in inflammatory bowel disease development and synergistic effects mediated by the ccl5 ccr5 axis
topic periostin (POSTN)
CCL5-CCR5-signaling system
IBD – inflammatory bowel disease
inflammation
treatment option
chemically induced colitis
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.956691/full
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