Excessive dietary lipid intake provokes an acquired form of lysosomal lipid storage disease in the kidney

Obesity and dyslipidaemia are features of the metabolic syndrome and risk factors for chronic kidney disease. The cellular mechanisms connecting metabolic syndrome with chronic kidney disease onset and progression remain largely unclear. We show that proximal tubular epithelium is a target site for...

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Published in:The Journal of pathology Vol. 246; no. 4; pp. 470 - 484
Main Authors: Rampanelli, Elena, Ochodnicky, Peter, Vissers, Johannes PC, Butter, Loes M, Claessen, Nike, Calcagni, Alessia, Kors, Lotte, Gethings, Lee A, Bakker, Stephan JL, de Borst, Martin H, Navis, Gerjan J, Liebisch, Gerhard, Speijer, Dave, van den Bergh Weerman, Marius A, Jung, Bettina, Aten, Jan, Steenbergen, Eric, Schmitz, Gerd, Ballabio, Andrea, Florquin, Sandrine, Aerts, Johannes MFG, Leemans, Jaklien C
Format: Journal Article
Language:English
Published: Chichester, UK John Wiley & Sons, Ltd 01.12.2018
Wiley Subscription Services, Inc
Subjects:
Cholesterol
chronic kidney disease
diet
Dietary intake
Dyslipidemia
Epidermis
Epithelial cells
Epithelium
Fibrosis
Inflammation
kidney
Kidney diseases
Kidneys
Lipids
Lipoproteins
lysosomal storage disease
Lysosomal storage diseases
lysosome
Lysosomes
Metabolic syndrome
metabolism
multilamellar bodies
Obesity
Overnutrition
Phospholipids
Proteomics
Risk factors
Transcription
Urine
Vacuoles
Well being
kidney
chronic kidney disease
lipids
inflammation
lysosomal storage disease
multilamellar bodies
fibrosis
metabolism
diet
lysosome
ISSN:0022-3417, 1096-9896, 1096-9896
Online Access:Get full text
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Abstract Obesity and dyslipidaemia are features of the metabolic syndrome and risk factors for chronic kidney disease. The cellular mechanisms connecting metabolic syndrome with chronic kidney disease onset and progression remain largely unclear. We show that proximal tubular epithelium is a target site for lipid deposition upon overnutrition with a cholesterol‐rich Western‐type diet. Affected proximal tubule epithelial cells displayed giant vacuoles of lysosomal or autophagosomal origin, harbouring oxidised lipoproteins and concentric membrane layer structures (multilamellar bodies), reminiscent of lysosomal storage diseases. Additionally, lipidomic analysis revealed renal deposition of cholesterol and phospholipids, including lysosomal phospholipids. Proteomic profiles of renal multilamellar bodies were distinct from those of epidermis or lung multilamellar bodies and of cytoplasmic lipid droplets. Tubular multilamellar bodies were observed in kidney biopsies of obese hypercholesterolaemic patients, and the concentration of the phospholipidosis marker di‐docosahexaenoyl (22:6)‐bis(monoacylglycerol) phosphate was doubled in urine from individuals with metabolic syndrome and chronic kidney disease. The enrichment of proximal tubule epithelial cells with phospholipids and multilamellar bodies was accompanied by enhanced inflammation, fibrosis, tubular damage markers, and higher urinary electrolyte content. Concomitantly to the intralysosomal lipid storage, a renal transcriptional response was initiated to enhance lysosomal degradation and lipid synthesis. In cultured proximal tubule epithelial cells, inhibition of cholesterol efflux transport or oxysterol treatment induced effects very similar to the in vivo situation, such as multilamellar body and phospholipid amassing, and induction of damage, inflammatory, fibrotic, and lipogenic molecules. The onset of phospholipidosis in proximal tubule epithelial cells is a novel pathological trait in metabolic syndrome‐related chronic kidney disease, and emphasises the importance of healthy lysosomes and nutrition for kidney well‐being. Copyright © 2018 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
AbstractList Obesity and dyslipidaemia are features of the metabolic syndrome and risk factors for chronic kidney disease. The cellular mechanisms connecting metabolic syndrome with chronic kidney disease onset and progression remain largely unclear. We show that proximal tubular epithelium is a target site for lipid deposition upon overnutrition with a cholesterol‐rich Western‐type diet. Affected proximal tubule epithelial cells displayed giant vacuoles of lysosomal or autophagosomal origin, harbouring oxidised lipoproteins and concentric membrane layer structures (multilamellar bodies), reminiscent of lysosomal storage diseases. Additionally, lipidomic analysis revealed renal deposition of cholesterol and phospholipids, including lysosomal phospholipids. Proteomic profiles of renal multilamellar bodies were distinct from those of epidermis or lung multilamellar bodies and of cytoplasmic lipid droplets. Tubular multilamellar bodies were observed in kidney biopsies of obese hypercholesterolaemic patients, and the concentration of the phospholipidosis marker di‐docosahexaenoyl (22:6)‐bis(monoacylglycerol) phosphate was doubled in urine from individuals with metabolic syndrome and chronic kidney disease. The enrichment of proximal tubule epithelial cells with phospholipids and multilamellar bodies was accompanied by enhanced inflammation, fibrosis, tubular damage markers, and higher urinary electrolyte content. Concomitantly to the intralysosomal lipid storage, a renal transcriptional response was initiated to enhance lysosomal degradation and lipid synthesis. In cultured proximal tubule epithelial cells, inhibition of cholesterol efflux transport or oxysterol treatment induced effects very similar to the in vivo situation, such as multilamellar body and phospholipid amassing, and induction of damage, inflammatory, fibrotic, and lipogenic molecules. The onset of phospholipidosis in proximal tubule epithelial cells is a novel pathological trait in metabolic syndrome‐related chronic kidney disease, and emphasises the importance of healthy lysosomes and nutrition for kidney well‐being. Copyright © 2018 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
Obesity and dyslipidaemia are features of the metabolic syndrome and risk factors for chronic kidney disease. The cellular mechanisms connecting metabolic syndrome with chronic kidney disease onset and progression remain largely unclear. We show that proximal tubular epithelium is a target site for lipid deposition upon overnutrition with a cholesterol-rich Western-type diet. Affected proximal tubule epithelial cells displayed giant vacuoles of lysosomal or autophagosomal origin, harbouring oxidised lipoproteins and concentric membrane layer structures (multilamellar bodies), reminiscent of lysosomal storage diseases. Additionally, lipidomic analysis revealed renal deposition of cholesterol and phospholipids, including lysosomal phospholipids. Proteomic profiles of renal multilamellar bodies were distinct from those of epidermis or lung multilamellar bodies and of cytoplasmic lipid droplets. Tubular multilamellar bodies were observed in kidney biopsies of obese hypercholesterolaemic patients, and the concentration of the phospholipidosis marker di-docosahexaenoyl (22:6)-bis(monoacylglycerol) phosphate was doubled in urine from individuals with metabolic syndrome and chronic kidney disease. The enrichment of proximal tubule epithelial cells with phospholipids and multilamellar bodies was accompanied by enhanced inflammation, fibrosis, tubular damage markers, and higher urinary electrolyte content. Concomitantly to the intralysosomal lipid storage, a renal transcriptional response was initiated to enhance lysosomal degradation and lipid synthesis. In cultured proximal tubule epithelial cells, inhibition of cholesterol efflux transport or oxysterol treatment induced effects very similar to the in vivo situation, such as multilamellar body and phospholipid amassing, and induction of damage, inflammatory, fibrotic, and lipogenic molecules. The onset of phospholipidosis in proximal tubule epithelial cells is a novel pathological trait in metabolic syndrome-related chronic kidney disease, and emphasises the importance of healthy lysosomes and nutrition for kidney well-being. Copyright © 2018 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.Obesity and dyslipidaemia are features of the metabolic syndrome and risk factors for chronic kidney disease. The cellular mechanisms connecting metabolic syndrome with chronic kidney disease onset and progression remain largely unclear. We show that proximal tubular epithelium is a target site for lipid deposition upon overnutrition with a cholesterol-rich Western-type diet. Affected proximal tubule epithelial cells displayed giant vacuoles of lysosomal or autophagosomal origin, harbouring oxidised lipoproteins and concentric membrane layer structures (multilamellar bodies), reminiscent of lysosomal storage diseases. Additionally, lipidomic analysis revealed renal deposition of cholesterol and phospholipids, including lysosomal phospholipids. Proteomic profiles of renal multilamellar bodies were distinct from those of epidermis or lung multilamellar bodies and of cytoplasmic lipid droplets. Tubular multilamellar bodies were observed in kidney biopsies of obese hypercholesterolaemic patients, and the concentration of the phospholipidosis marker di-docosahexaenoyl (22:6)-bis(monoacylglycerol) phosphate was doubled in urine from individuals with metabolic syndrome and chronic kidney disease. The enrichment of proximal tubule epithelial cells with phospholipids and multilamellar bodies was accompanied by enhanced inflammation, fibrosis, tubular damage markers, and higher urinary electrolyte content. Concomitantly to the intralysosomal lipid storage, a renal transcriptional response was initiated to enhance lysosomal degradation and lipid synthesis. In cultured proximal tubule epithelial cells, inhibition of cholesterol efflux transport or oxysterol treatment induced effects very similar to the in vivo situation, such as multilamellar body and phospholipid amassing, and induction of damage, inflammatory, fibrotic, and lipogenic molecules. The onset of phospholipidosis in proximal tubule epithelial cells is a novel pathological trait in metabolic syndrome-related chronic kidney disease, and emphasises the importance of healthy lysosomes and nutrition for kidney well-being. Copyright © 2018 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
Author Kors, Lotte
Leemans, Jaklien C
Rampanelli, Elena
Claessen, Nike
Butter, Loes M
Calcagni, Alessia
Aten, Jan
Steenbergen, Eric
Aerts, Johannes MFG
Gethings, Lee A
Ochodnicky, Peter
Navis, Gerjan J
Vissers, Johannes PC
Speijer, Dave
Ballabio, Andrea
van den Bergh Weerman, Marius A
Jung, Bettina
Schmitz, Gerd
Florquin, Sandrine
Bakker, Stephan JL
Liebisch, Gerhard
de Borst, Martin H
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  organization: University Medical Center Groningen, University of Groningen
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  organization: Academic Medical Center, University of Amsterdam
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  surname: van den Bergh Weerman
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  organization: Academic Medical Center, University of Amsterdam
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  surname: Leemans
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  organization: Academic Medical Center, University of Amsterdam
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30073645$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright Copyright © 2018 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
Copyright © 2018 Pathological Society of Great Britain and Ireland
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ISSN 0022-3417
1096-9896
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Issue 4
Keywords kidney
chronic kidney disease
lipids
inflammation
lysosomal storage disease
multilamellar bodies
fibrosis
metabolism
diet
lysosome
Language English
License Copyright © 2018 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.
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SSID ssj0009955
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Snippet Obesity and dyslipidaemia are features of the metabolic syndrome and risk factors for chronic kidney disease. The cellular mechanisms connecting metabolic...
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StartPage 470
SubjectTerms Cholesterol
chronic kidney disease
diet
Dietary intake
Dyslipidemia
Epidermis
Epithelial cells
Epithelium
Fibrosis
Inflammation
kidney
Kidney diseases
Kidneys
Lipids
Lipoproteins
lysosomal storage disease
Lysosomal storage diseases
lysosome
Lysosomes
Metabolic syndrome
metabolism
multilamellar bodies
Obesity
Overnutrition
Phospholipids
Proteomics
Risk factors
Transcription
Urine
Vacuoles
Well being
Title Excessive dietary lipid intake provokes an acquired form of lysosomal lipid storage disease in the kidney
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fpath.5150
https://www.ncbi.nlm.nih.gov/pubmed/30073645
https://www.proquest.com/docview/2133796007
https://www.proquest.com/docview/2083713550
Volume 246
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