Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway

Abstract Intestinal ischaemia–reperfusion (I/R) is a common clinical pathology with high incidence and mortality rates. However, the mechanisms underlying intestinal I/R injury remain unclear. In this study, we investigated the role and mechanism of chitinase 3‐like 1 (CHI3L1) during intestinal I/R...

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Main Authors: Lei Mi, Jie Jin, Yingying Zhang, Ming Chen, JianLi Cui, Rui Chen, Xiao Zheng, Changqing Jing
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Experimental Physiology
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Online Access:https://doi.org/10.1113/EP091768
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author Lei Mi
Jie Jin
Yingying Zhang
Ming Chen
JianLi Cui
Rui Chen
Xiao Zheng
Changqing Jing
author_facet Lei Mi
Jie Jin
Yingying Zhang
Ming Chen
JianLi Cui
Rui Chen
Xiao Zheng
Changqing Jing
author_sort Lei Mi
collection DOAJ
description Abstract Intestinal ischaemia–reperfusion (I/R) is a common clinical pathology with high incidence and mortality rates. However, the mechanisms underlying intestinal I/R injury remain unclear. In this study, we investigated the role and mechanism of chitinase 3‐like 1 (CHI3L1) during intestinal I/R injury. Therefore, we analysed the expression levels of CHI3L1 in the intestinal tissue of an intestinal I/R rat model and explored its effects and mechanism in a hypoxia–reoxygenation (H/R) IEC‐6 cell model. We found that intestinal I/R injury elevated CHI3L1 levels in the serum, ileum and duodenum, whereas H/R enhanced CHI3L1 expression in IEC‐6 cells. The H/R‐induced inhibition of proliferation and apoptosis was alleviated by CHI3L1 knockdown and aggravated by CHI3L1 overexpression. In addition, CHI3L1 knockdown alleviated, and CHI3L1 overexpression aggravated, the H/R‐induced inflammatory response and oxidative stress. Mechanistically, CHI3L1 overexpression weakened the activation of the phosphoinositide 3‐kinase (PI3K)/AKT pathway, suppressed the nuclear translocation of Nrf2, and promoted the nuclear translocation of nuclear factor κB (NF‐κB). Moreover, CHI3L1 knockdown had the opposite effect on the PI3K/AKT pathway, Nrf2, and NF‐κB. Moreover, the PI3K inhibitor LY294002 blocked the effect of CHI3L1 knockdown on the H/R‐induced inhibition of proliferation, apoptosis, inflammatory response and oxidative stress. In conclusion, CHI3L1 expression was induced during intestinal I/R and H/R injury in IEC‐6 cells, and CHI3L1 overexpression aggravated H/R injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway. Therefore, CHI3L1 may be an effective target for controlling intestinal I/R injury.
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spelling doaj-art-a67fd2466fe74b259c3c951f3d3946182024-11-30T11:02:31ZengWileyExperimental Physiology0958-06701469-445X2024-12-01109122073208710.1113/EP091768Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathwayLei Mi0Jie Jin1Yingying Zhang2Ming Chen3JianLi Cui4Rui Chen5Xiao Zheng6Changqing Jing7Department of Gastrointestinal Surgery The Affiliated Taian City Central Hospital of Qingdao University Tai'an ChinaDepartment of Traditional Chinese Medicine The Affiliated Taian City Central Hospital of Qingdao University Tai'an ChinaDepartment of Gastrointestinal Surgery The Affiliated Taian City Central Hospital of Qingdao University Tai'an ChinaDepartment of Gastrointestinal Surgery The Affiliated Taian City Central Hospital of Qingdao University Tai'an ChinaDepartment of Gastrointestinal Surgery The Affiliated Taian City Central Hospital of Qingdao University Tai'an ChinaDepartment of Gastrointestinal Surgery The Affiliated Taian City Central Hospital of Qingdao University Tai'an ChinaDepartment of Gastrointestinal Surgery The Affiliated Taian City Central Hospital of Qingdao University Tai'an ChinaDepartment of Gastrointestinal Surgery Shandong Provincial Hospital Affiliated to Shandong First Medical University Jinan ChinaAbstract Intestinal ischaemia–reperfusion (I/R) is a common clinical pathology with high incidence and mortality rates. However, the mechanisms underlying intestinal I/R injury remain unclear. In this study, we investigated the role and mechanism of chitinase 3‐like 1 (CHI3L1) during intestinal I/R injury. Therefore, we analysed the expression levels of CHI3L1 in the intestinal tissue of an intestinal I/R rat model and explored its effects and mechanism in a hypoxia–reoxygenation (H/R) IEC‐6 cell model. We found that intestinal I/R injury elevated CHI3L1 levels in the serum, ileum and duodenum, whereas H/R enhanced CHI3L1 expression in IEC‐6 cells. The H/R‐induced inhibition of proliferation and apoptosis was alleviated by CHI3L1 knockdown and aggravated by CHI3L1 overexpression. In addition, CHI3L1 knockdown alleviated, and CHI3L1 overexpression aggravated, the H/R‐induced inflammatory response and oxidative stress. Mechanistically, CHI3L1 overexpression weakened the activation of the phosphoinositide 3‐kinase (PI3K)/AKT pathway, suppressed the nuclear translocation of Nrf2, and promoted the nuclear translocation of nuclear factor κB (NF‐κB). Moreover, CHI3L1 knockdown had the opposite effect on the PI3K/AKT pathway, Nrf2, and NF‐κB. Moreover, the PI3K inhibitor LY294002 blocked the effect of CHI3L1 knockdown on the H/R‐induced inhibition of proliferation, apoptosis, inflammatory response and oxidative stress. In conclusion, CHI3L1 expression was induced during intestinal I/R and H/R injury in IEC‐6 cells, and CHI3L1 overexpression aggravated H/R injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway. Therefore, CHI3L1 may be an effective target for controlling intestinal I/R injury.https://doi.org/10.1113/EP091768CHI3L1intestinal ischaemia–reperfusionNF‐κBNrf2nuclear translocationPI3K/AKT
spellingShingle Lei Mi
Jie Jin
Yingying Zhang
Ming Chen
JianLi Cui
Rui Chen
Xiao Zheng
Changqing Jing
Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway
Experimental Physiology
CHI3L1
intestinal ischaemia–reperfusion
NF‐κB
Nrf2
nuclear translocation
PI3K/AKT
title Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway
title_full Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway
title_fullStr Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway
title_full_unstemmed Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway
title_short Chitinase 3‐like 1 overexpression aggravates hypoxia–reoxygenation injury in IEC‐6 cells by inhibiting the PI3K/AKT signalling pathway
title_sort chitinase 3 like 1 overexpression aggravates hypoxia reoxygenation injury in iec 6 cells by inhibiting the pi3k akt signalling pathway
topic CHI3L1
intestinal ischaemia–reperfusion
NF‐κB
Nrf2
nuclear translocation
PI3K/AKT
url https://doi.org/10.1113/EP091768
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