Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease Progression

Introduction: Cellular senescence is characterized by generally irreversible cell cycle arrest and changes in secretory activity, with senescent renal epithelia proposed as drivers of kidney fibrosis. The lack of noninvasive biomarkers represents an obstacle to the design of human trials of senescen...

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Main Authors: David P. Baird, Maximilian Reck, Ross Campbell, Marie-Helena Docherty, Piotr P. Janas, Tilly Mason, Zenuida Mortuza, Matthieu Vermeren, Andy Nam, Wei Yang, Nathan Schurman, Claire Williams, Jamie P. Traynor, Patrick B. Mark, Katie J. Mylonas, Jeremy Hughes, Laura Denby, Bryan R. Conway, David A. Ferenbach
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Kidney International Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2468024925002608
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author David P. Baird
Maximilian Reck
Ross Campbell
Marie-Helena Docherty
Piotr P. Janas
Tilly Mason
Zenuida Mortuza
Matthieu Vermeren
Andy Nam
Wei Yang
Nathan Schurman
Claire Williams
Jamie P. Traynor
Patrick B. Mark
Katie J. Mylonas
Jeremy Hughes
Laura Denby
Bryan R. Conway
David A. Ferenbach
author_facet David P. Baird
Maximilian Reck
Ross Campbell
Marie-Helena Docherty
Piotr P. Janas
Tilly Mason
Zenuida Mortuza
Matthieu Vermeren
Andy Nam
Wei Yang
Nathan Schurman
Claire Williams
Jamie P. Traynor
Patrick B. Mark
Katie J. Mylonas
Jeremy Hughes
Laura Denby
Bryan R. Conway
David A. Ferenbach
author_sort David P. Baird
collection DOAJ
description Introduction: Cellular senescence is characterized by generally irreversible cell cycle arrest and changes in secretory activity, with senescent renal epithelia proposed as drivers of kidney fibrosis. The lack of noninvasive biomarkers represents an obstacle to the design of human trials of senescent cell–depleting medications. Methods: Proteomic analysis was performed on urine from patients with chronic kidney disease (CKD) alongside immunofluorescence staining of paired kidney biopsies (n = 51). Enzyme-linked immunosorbent assays (ELISAs) and immunofluorescence staining were performed in a second cohort of matched urine and kidney biopsies (n = 53). Spatial transcriptomic analysis was performed on kidney tissue from benign and fibrotic kidney disease (n = 13). Clusterin and senescence markers were analyzed in vitro by quantitative polymerase chain reaction (PCR) in irradiated human renal epithelia. Urinary biomarker concentrations were quantified by ELISA (n = 322) to assess their ability to predict patient outcomes (end-stage kidney disease or > 40% renal functional loss). Results: P21+Ki67- epithelial senescence correlated with age and inversely with renal function. Urinary clusterin-to-creatinine ratio (uCCR) correlated tightly with P21+Ki67- epithelial senescence in both matched urine and kidney biopsy cohorts (rho > 0.5, P < 0.001) and predicted levels of senescence after adjusting for other variables. Clusterin was upregulated transcriptomically in CDKN1A (p21) expressing epithelia in vitro and in vivo. An elevated uCCR predicted adverse renal end points in a cohort of patients with CKD after adjusting for baseline estimated glomerular filtration rate (eGFR), urinary albumin-to-creatinine ratio (uACR), age, systolic blood pressure, and sex. Conclusion: uCCR represents a surrogate for histologic quantification of p21+Ki67- senescent renal epithelia and predicts outcomes in human kidney disease independent of existing clinical risk factors.
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spelling doaj-art-d2a26e159f814b64b95e56888c0ec4552025-08-20T02:35:19ZengElsevierKidney International Reports2468-02492025-07-011072344235610.1016/j.ekir.2025.04.035Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease ProgressionDavid P. Baird0Maximilian Reck1Ross Campbell2Marie-Helena Docherty3Piotr P. Janas4Tilly Mason5Zenuida Mortuza6Matthieu Vermeren7Andy Nam8Wei Yang9Nathan Schurman10Claire Williams11Jamie P. Traynor12Patrick B. Mark13Katie J. Mylonas14Jeremy Hughes15Laura Denby16Bryan R. Conway17David A. Ferenbach18Centre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UK; Correspondence: David P. Baird, Centre for Inflammation Research, Institute for Regeneration and Repair, 4-5 Little France Crescent, Edinburgh EH16 4UU, UK.Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKBruker Spatial Biology, Seattle, Washington, USABruker Spatial Biology, Seattle, Washington, USABruker Spatial Biology, Seattle, Washington, USABruker Spatial Biology, Seattle, Washington, USASchool of Medicine, Dentistry and Nursing, University of Glasgow, Glasgow, UKSchool of Cardiovascular and Metabolic Health, University of Glasgow, Glasgow, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKCentre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh, UKCentre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh, UKCentre for Inflammation Research, Institute for Regeneration and Repair, University of Edinburgh, UKIntroduction: Cellular senescence is characterized by generally irreversible cell cycle arrest and changes in secretory activity, with senescent renal epithelia proposed as drivers of kidney fibrosis. The lack of noninvasive biomarkers represents an obstacle to the design of human trials of senescent cell–depleting medications. Methods: Proteomic analysis was performed on urine from patients with chronic kidney disease (CKD) alongside immunofluorescence staining of paired kidney biopsies (n = 51). Enzyme-linked immunosorbent assays (ELISAs) and immunofluorescence staining were performed in a second cohort of matched urine and kidney biopsies (n = 53). Spatial transcriptomic analysis was performed on kidney tissue from benign and fibrotic kidney disease (n = 13). Clusterin and senescence markers were analyzed in vitro by quantitative polymerase chain reaction (PCR) in irradiated human renal epithelia. Urinary biomarker concentrations were quantified by ELISA (n = 322) to assess their ability to predict patient outcomes (end-stage kidney disease or > 40% renal functional loss). Results: P21+Ki67- epithelial senescence correlated with age and inversely with renal function. Urinary clusterin-to-creatinine ratio (uCCR) correlated tightly with P21+Ki67- epithelial senescence in both matched urine and kidney biopsy cohorts (rho > 0.5, P < 0.001) and predicted levels of senescence after adjusting for other variables. Clusterin was upregulated transcriptomically in CDKN1A (p21) expressing epithelia in vitro and in vivo. An elevated uCCR predicted adverse renal end points in a cohort of patients with CKD after adjusting for baseline estimated glomerular filtration rate (eGFR), urinary albumin-to-creatinine ratio (uACR), age, systolic blood pressure, and sex. Conclusion: uCCR represents a surrogate for histologic quantification of p21+Ki67- senescent renal epithelia and predicts outcomes in human kidney disease independent of existing clinical risk factors.http://www.sciencedirect.com/science/article/pii/S2468024925002608agingbiomarkerscellular senescencechronic kidney diseaseclusterinfibrosis
spellingShingle David P. Baird
Maximilian Reck
Ross Campbell
Marie-Helena Docherty
Piotr P. Janas
Tilly Mason
Zenuida Mortuza
Matthieu Vermeren
Andy Nam
Wei Yang
Nathan Schurman
Claire Williams
Jamie P. Traynor
Patrick B. Mark
Katie J. Mylonas
Jeremy Hughes
Laura Denby
Bryan R. Conway
David A. Ferenbach
Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease Progression
Kidney International Reports
aging
biomarkers
cellular senescence
chronic kidney disease
clusterin
fibrosis
title Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease Progression
title_full Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease Progression
title_fullStr Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease Progression
title_full_unstemmed Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease Progression
title_short Urinary Clusterin is a Biomarker of Renal Epithelial Senescence and Predicts Human Kidney Disease Progression
title_sort urinary clusterin is a biomarker of renal epithelial senescence and predicts human kidney disease progression
topic aging
biomarkers
cellular senescence
chronic kidney disease
clusterin
fibrosis
url http://www.sciencedirect.com/science/article/pii/S2468024925002608
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