HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice

Background Renal dysfunction and disruption of renal endothelial glycocalyx are two important events during septic acute kidney injury (AKI). Here, the role and mechanism of hyaluronidase 1 (HYAL1) in regulating renal injury and renal endothelial glycocalyx breakdown in septic AKI were explored for...

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Main Authors: Hongxia Xing, Shensen Li, Yongchao Fu, Xin Wan, Annan Zhou, Feifei Cao, Qing Sun, Nana Hu, Mengqing Ma, Wenwen Li, Changchun Cao
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:Renal Failure
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Online Access:https://www.tandfonline.com/doi/10.1080/0886022X.2023.2188966
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author Hongxia Xing
Shensen Li
Yongchao Fu
Xin Wan
Annan Zhou
Feifei Cao
Qing Sun
Nana Hu
Mengqing Ma
Wenwen Li
Changchun Cao
author_facet Hongxia Xing
Shensen Li
Yongchao Fu
Xin Wan
Annan Zhou
Feifei Cao
Qing Sun
Nana Hu
Mengqing Ma
Wenwen Li
Changchun Cao
author_sort Hongxia Xing
collection DOAJ
description Background Renal dysfunction and disruption of renal endothelial glycocalyx are two important events during septic acute kidney injury (AKI). Here, the role and mechanism of hyaluronidase 1 (HYAL1) in regulating renal injury and renal endothelial glycocalyx breakdown in septic AKI were explored for the first time.Methods BALB/c mice were injected with lipopolysaccharide (LPS, 10 mg/kg) to induce AKI. HYAL1 was blocked in vivo using lentivirus-mediated short hairpin RNA targeting HYAL1 (LV-sh-HYAL1). Biochemical assays were performed to measure the levels and concentrations of biochemical parameters associated with AKI as well as levels of inflammatory cytokines. Renal pathological lesions were determined by hematoxylin-eosin (HE) staining. Cell apoptosis in the kidney was detected using terminal-deoxynucleoitidyl transferase-mediated nick end labeling (TUNEL) assay. Immunofluorescence and immunohistochemical (IHC) staining assays were used to examine the levels of hyaluronic acid in the kidney. The protein levels of adenosine monophosphate-activated protein kinase (AMPK)/mammalian target of rapamycin (mTOR) signaling, endothelial glycocalyx, and autophagy-associated indicators were assessed by western blotting.Results The knockdown of HYAL1 in LPS-subjected mice by LV-sh-HYAL1 significantly reduced renal inflammation, oxidative stress, apoptosis and kidney dysfunction in AKI, as well as alleviated renal endothelial glycocalyx disruption by preventing the release of hyaluronic acid to the bloodstream. Additionally, autophagy-related protein analysis indicated that knockdown of HYAL1 significantly enhanced autophagy in LPS mice. Furthermore, the beneficial actions of HYAL1 blockade were closely associated with the AMPK/mTOR signaling.Conclusion HYAL1 deficiency attenuates LPS-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice.
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publishDate 2023-12-01
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series Renal Failure
spelling doaj-art-507667333bce461aa149d2a460a7a6042025-08-20T02:56:09ZengTaylor & Francis GroupRenal Failure0886-022X1525-60492023-12-0145110.1080/0886022X.2023.2188966HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in miceHongxia Xing0Shensen Li1Yongchao Fu2Xin Wan3Annan Zhou4Feifei Cao5Qing Sun6Nana Hu7Mengqing Ma8Wenwen Li9Changchun Cao10Department of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Nanjing First Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingDepartment of Nephrology, Sir Run Hospital, Nanjing Medical University, Jiangsu, China NanjingBackground Renal dysfunction and disruption of renal endothelial glycocalyx are two important events during septic acute kidney injury (AKI). Here, the role and mechanism of hyaluronidase 1 (HYAL1) in regulating renal injury and renal endothelial glycocalyx breakdown in septic AKI were explored for the first time.Methods BALB/c mice were injected with lipopolysaccharide (LPS, 10 mg/kg) to induce AKI. HYAL1 was blocked in vivo using lentivirus-mediated short hairpin RNA targeting HYAL1 (LV-sh-HYAL1). Biochemical assays were performed to measure the levels and concentrations of biochemical parameters associated with AKI as well as levels of inflammatory cytokines. Renal pathological lesions were determined by hematoxylin-eosin (HE) staining. Cell apoptosis in the kidney was detected using terminal-deoxynucleoitidyl transferase-mediated nick end labeling (TUNEL) assay. Immunofluorescence and immunohistochemical (IHC) staining assays were used to examine the levels of hyaluronic acid in the kidney. The protein levels of adenosine monophosphate-activated protein kinase (AMPK)/mammalian target of rapamycin (mTOR) signaling, endothelial glycocalyx, and autophagy-associated indicators were assessed by western blotting.Results The knockdown of HYAL1 in LPS-subjected mice by LV-sh-HYAL1 significantly reduced renal inflammation, oxidative stress, apoptosis and kidney dysfunction in AKI, as well as alleviated renal endothelial glycocalyx disruption by preventing the release of hyaluronic acid to the bloodstream. Additionally, autophagy-related protein analysis indicated that knockdown of HYAL1 significantly enhanced autophagy in LPS mice. Furthermore, the beneficial actions of HYAL1 blockade were closely associated with the AMPK/mTOR signaling.Conclusion HYAL1 deficiency attenuates LPS-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice.https://www.tandfonline.com/doi/10.1080/0886022X.2023.2188966HYAL1AMPK/mTOR signalingacute kidney injuryendothelial glycocalyxautophagy
spellingShingle Hongxia Xing
Shensen Li
Yongchao Fu
Xin Wan
Annan Zhou
Feifei Cao
Qing Sun
Nana Hu
Mengqing Ma
Wenwen Li
Changchun Cao
HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice
Renal Failure
HYAL1
AMPK/mTOR signaling
acute kidney injury
endothelial glycocalyx
autophagy
title HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice
title_full HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice
title_fullStr HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice
title_full_unstemmed HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice
title_short HYAL1 deficiency attenuates lipopolysaccharide-triggered renal injury and endothelial glycocalyx breakdown in septic AKI in mice
title_sort hyal1 deficiency attenuates lipopolysaccharide triggered renal injury and endothelial glycocalyx breakdown in septic aki in mice
topic HYAL1
AMPK/mTOR signaling
acute kidney injury
endothelial glycocalyx
autophagy
url https://www.tandfonline.com/doi/10.1080/0886022X.2023.2188966
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