The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injury

Background: Growing evidence indicates that disruptions in mitochondrial quality management contribute to the development of acute kidney injury (AKI), incomplete or maladaptive kidney repair, and chronic kidney disease. However, the temporal dynamics of mitochondrial quality control alterations in...

Full description

Saved in:
Bibliographic Details
Main Authors: Priyanka N. Prem, Harish Swaminathan, Gino A. Kurian
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405844025000131
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1841533320181055488
author Priyanka N. Prem
Harish Swaminathan
Gino A. Kurian
author_facet Priyanka N. Prem
Harish Swaminathan
Gino A. Kurian
author_sort Priyanka N. Prem
collection DOAJ
description Background: Growing evidence indicates that disruptions in mitochondrial quality management contribute to the development of acute kidney injury (AKI), incomplete or maladaptive kidney repair, and chronic kidney disease. However, the temporal dynamics of mitochondrial quality control alterations in relation to renal injury and its recovery remain poorly understood and are addressed in this manuscript. Method: ology: Male Wistar rats (n = 60) were subjected to varying durations of ischemia and reperfusion. Ischemia was instigated by clamping both renal arteries and for reperfusion, the clamps were removed to restore the blood flow. Renal injury, physiological function, mitochondrial assessment, and cellular mediators were analyzed. Results: Prolonging ischemia duration reduces bioenergetic function while disrupting the balance of mitochondrial fusion, fission, and mitophagy at the gene expression level while maintaining intact mitochondrial copy number. However, reperfusing a kidney after 45 min of ischemia with varying reperfusion times exacerbates mitochondrial dysfunction and significantly decreases mitochondrial copy number. These declines are particularly evident at 24 h of reperfusion, with some parameters improving by 7 days of reperfusion. Despite these improvements, 7 days of reperfusion did not correlate with renal injury indicators (CrCl- 0.46 ± 0.01, BUN-86.29 ± 4.9, Cr-1.75 ± 0.16) following 45 min of ischemia. Conversely, 15 min of ischemia followed by 7 days of reperfusion restored mitochondrial quality and renal function (CrCl- 7.33 ± 0.59, BUN-43.6 ± 3.16, Cr-0.93 ± 0.14). Conclusion: The above findings emphasize that mitochondrial quality control alters with the extent of ischemia and subsequent reperfusion time, impacting not only mitochondrial copy number but also the resilience of mitochondria during tissue repair.
format Article
id doaj-art-944496bd2df040e6be30c87f5dbeffe1
institution Kabale University
issn 2405-8440
language English
publishDate 2025-01-01
publisher Elsevier
record_format Article
series Heliyon
spelling doaj-art-944496bd2df040e6be30c87f5dbeffe12025-01-17T04:51:48ZengElsevierHeliyon2405-84402025-01-01111e41634The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injuryPriyanka N. Prem0Harish Swaminathan1Gino A. Kurian2School of Chemical and Biotechnology, SASTRA Deemed University, Tirumalaisamudram, Thanjavur, Tamil Nadu, India; Vascular Biology Lab, Anusandhan Kendra-1, SASTRA Deemed University, Tirumalaisamudram, Thanjavur, Tamil Nadu, IndiaSchool of Chemical and Biotechnology, SASTRA Deemed University, Tirumalaisamudram, Thanjavur, Tamil Nadu, India; Vascular Biology Lab, Anusandhan Kendra-1, SASTRA Deemed University, Tirumalaisamudram, Thanjavur, Tamil Nadu, IndiaSchool of Chemical and Biotechnology, SASTRA Deemed University, Tirumalaisamudram, Thanjavur, Tamil Nadu, India; Vascular Biology Lab, Anusandhan Kendra-1, SASTRA Deemed University, Tirumalaisamudram, Thanjavur, Tamil Nadu, India; Corresponding author. Vascular Biology lab, School of Chemical and Biotechnology, SASTRA Deemed University, Thanjavur, India.Background: Growing evidence indicates that disruptions in mitochondrial quality management contribute to the development of acute kidney injury (AKI), incomplete or maladaptive kidney repair, and chronic kidney disease. However, the temporal dynamics of mitochondrial quality control alterations in relation to renal injury and its recovery remain poorly understood and are addressed in this manuscript. Method: ology: Male Wistar rats (n = 60) were subjected to varying durations of ischemia and reperfusion. Ischemia was instigated by clamping both renal arteries and for reperfusion, the clamps were removed to restore the blood flow. Renal injury, physiological function, mitochondrial assessment, and cellular mediators were analyzed. Results: Prolonging ischemia duration reduces bioenergetic function while disrupting the balance of mitochondrial fusion, fission, and mitophagy at the gene expression level while maintaining intact mitochondrial copy number. However, reperfusing a kidney after 45 min of ischemia with varying reperfusion times exacerbates mitochondrial dysfunction and significantly decreases mitochondrial copy number. These declines are particularly evident at 24 h of reperfusion, with some parameters improving by 7 days of reperfusion. Despite these improvements, 7 days of reperfusion did not correlate with renal injury indicators (CrCl- 0.46 ± 0.01, BUN-86.29 ± 4.9, Cr-1.75 ± 0.16) following 45 min of ischemia. Conversely, 15 min of ischemia followed by 7 days of reperfusion restored mitochondrial quality and renal function (CrCl- 7.33 ± 0.59, BUN-43.6 ± 3.16, Cr-0.93 ± 0.14). Conclusion: The above findings emphasize that mitochondrial quality control alters with the extent of ischemia and subsequent reperfusion time, impacting not only mitochondrial copy number but also the resilience of mitochondria during tissue repair.http://www.sciencedirect.com/science/article/pii/S2405844025000131Renal ischemia-reperfusion injuryMitochondrial biogenesisMitochondrial bioenergeticsMitochondrial dynamicsMitophagy
spellingShingle Priyanka N. Prem
Harish Swaminathan
Gino A. Kurian
The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injury
Heliyon
Renal ischemia-reperfusion injury
Mitochondrial biogenesis
Mitochondrial bioenergetics
Mitochondrial dynamics
Mitophagy
title The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injury
title_full The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injury
title_fullStr The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injury
title_full_unstemmed The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injury
title_short The temporal relationship between mitochondrial quality and renal tissue recovery following ischemia-reperfusion injury
title_sort temporal relationship between mitochondrial quality and renal tissue recovery following ischemia reperfusion injury
topic Renal ischemia-reperfusion injury
Mitochondrial biogenesis
Mitochondrial bioenergetics
Mitochondrial dynamics
Mitophagy
url http://www.sciencedirect.com/science/article/pii/S2405844025000131
work_keys_str_mv AT priyankanprem thetemporalrelationshipbetweenmitochondrialqualityandrenaltissuerecoveryfollowingischemiareperfusioninjury
AT harishswaminathan thetemporalrelationshipbetweenmitochondrialqualityandrenaltissuerecoveryfollowingischemiareperfusioninjury
AT ginoakurian thetemporalrelationshipbetweenmitochondrialqualityandrenaltissuerecoveryfollowingischemiareperfusioninjury
AT priyankanprem temporalrelationshipbetweenmitochondrialqualityandrenaltissuerecoveryfollowingischemiareperfusioninjury
AT harishswaminathan temporalrelationshipbetweenmitochondrialqualityandrenaltissuerecoveryfollowingischemiareperfusioninjury
AT ginoakurian temporalrelationshipbetweenmitochondrialqualityandrenaltissuerecoveryfollowingischemiareperfusioninjury