Hemolysis is associated with altered heparan sulfate of the endothelial glycocalyx and with local complement activation in thrombotic microangiopathies.


Journal

Kidney international
ISSN: 1523-1755
Titre abrégé: Kidney Int
Pays: United States
ID NLM: 0323470

Informations de publication

Date de publication:
08 2023
Historique:
received: 22 05 2022
revised: 03 03 2023
accepted: 24 03 2023
medline: 24 7 2023
pubmed: 11 5 2023
entrez: 10 5 2023
Statut: ppublish

Résumé

The complement system plays a key role in the pathophysiology of kidney thrombotic microangiopathies (TMA), as illustrated by atypical hemolytic uremic syndrome. But complement abnormalities are not the only drivers of TMA lesions. Among other potential pathophysiological actors, we hypothesized that alteration of heparan sulfate (HS) in the endothelial glycocalyx could be important. To evaluate this, we analyzed clinical and histological features of kidney biopsies from a monocentric, retrospective cohort of 72 patients with TMA, particularly for HS integrity and markers of local complement activation. The role of heme (a major product of hemolysis) as an HS-degrading agent in vitro, and the impact of altering endothelial cell (ECs) HS on their ability to locally activate complement were studied. Compared with a positive control, glomerular HS staining was lower in 57 (79%) patients with TMA, moderately reduced in 20 (28%), and strongly reduced in 37 (51%) of these 57 cases. Strongly reduced HS density was significantly associated with both hemolysis at the time of biopsy and local complement activation (C3 and/or C5b-9 deposits). Using primary endothelial cells (HUVECs, Glomerular ECs), we observed decreased HS expression after short-term exposure to heme, and that artificial HS degradation by exposure to heparinase was associated with local complement activation. Further, prolonged exposure to heme modulated expression of several key genes of glycocalyx metabolism involved in coagulation regulation (C5-EPI, HS6ST1, HS3ST1). Thus, our study highlights the impact of hemolysis on the integrity of endothelial HS, both in patients and in endothelial cell models. Hence, acute alteration of HS may be a mechanism of heme-induced complement activation.

Identifiants

pubmed: 37164260
pii: S0085-2538(23)00327-7
doi: 10.1016/j.kint.2023.03.039
pii:
doi:

Substances chimiques

Complement System Proteins 9007-36-7
Heparitin Sulfate 9050-30-0
Heme 42VZT0U6YR

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

353-366

Informations de copyright

Copyright © 2023 International Society of Nephrology. Published by Elsevier Inc. All rights reserved.

Auteurs

Timothée Laboux (T)

University of Lille, CHU Lille, Nephrology Department, Lille, France; University of Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1167-RID-AGE, Lille, France. Electronic address: tlaboux@gmail.com.

Mehdi Maanaoui (M)

University of Lille, CHU Lille, Nephrology Department, Lille, France; University of Lille, Inserm, Institut Pasteur de Lille, U1190 - EGID, Lille, France.

Fabrice Allain (F)

University of Lille, CNRS, UMR 8576 - UGSF, Lille, France.

Eric Boulanger (E)

University of Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1167-RID-AGE, Lille, France.

Agnès Denys (A)

University of Lille, CNRS, UMR 8576 - UGSF, Lille, France.

Jean-Baptiste Gibier (JB)

University of Lille, Pathology Department, Lille, France; University of Lille, Inserm, US1172, Lille, France.

François Glowacki (F)

University of Lille, CHU Lille, Nephrology Department, Lille, France.

Gaëlle Grolaux (G)

University of Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1167-RID-AGE, Lille, France.

Anne Grunenwald (A)

Centre de Recherche des Cordeliers, INSERM, Sorbonne Université, Université de Paris, Paris, France.

Mike Howsam (M)

University of Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1167-RID-AGE, Lille, France.

Steve Lancel (S)

University of Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1167-RID-AGE, Lille, France.

Céline Lebas (C)

University of Lille, CHU Lille, Nephrology Department, Lille, France.

Benjamin Lopez (B)

University of Lille, Institut of Immunology, Lille, France.

Lubka Roumenina (L)

Centre de Recherche des Cordeliers, INSERM, Sorbonne Université, Université de Paris, Paris, France.

François Provôt (F)

University of Lille, CHU Lille, Nephrology Department, Lille, France.

Viviane Gnemmi (V)

University of Lille, Pathology Department, Lille, France; University of Lille, CNRS, Inserm, U9020-UMR-S 1277, Lille, France.

Marie Frimat (M)

University of Lille, CHU Lille, Nephrology Department, Lille, France; University of Lille, Inserm, CHU Lille, Institut Pasteur de Lille, U1167-RID-AGE, Lille, France. Electronic address: marie.frimat@chru-lille.fr.

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Classifications MeSH