Whole blood coagulation in an ex vivo thrombus is sufficient to induce clot neutrophils to adopt a myeloid-derived suppressor cell signature and shed soluble Lox-1.

Blood Clot RNA immunity innate myeloid-derived suppressor cells polymorphonuclear neutrophils sequence analysis

Journal

Journal of thrombosis and haemostasis : JTH
ISSN: 1538-7836
Titre abrégé: J Thromb Haemost
Pays: England
ID NLM: 101170508

Informations de publication

Date de publication:
20 Dec 2023
Historique:
received: 12 07 2023
revised: 04 12 2023
accepted: 06 12 2023
medline: 23 12 2023
pubmed: 23 12 2023
entrez: 22 12 2023
Statut: aheadofprint

Résumé

Blood clots are living tissues that release inflammatory mediators including IL-8/CXCL8 and MCP-1/CCL2. A deeper understanding of blood clots is needed to develop new therapies for pro-thrombotic disease states and regenerative medicine. Identify a common transcriptional shift in cultured blood clot leukocytes. Differential gene expression of whole blood and cultured clots (4h 37°C) was assessed by RNA sequencing (RNAseq), RT-PCR, proteomics, and histology (23 diverse healthy human donors). Cultured clot serum bioactivity was tested in endothelial barrier functional assays. All cultured clots developed a polymorphonuclear myeloid-derived suppressor cell (PMN-MDSC) signature, including upregulation of OLR1 (mRNA encoding lectin-like oxidized low density lipoprotein receptor 1, Lox-1), IL-8/CXCL8, CXCL2, CCL2, IL10, IL1A, SPP1, TREM1 and DUSP4/MKP. Lipopolysaccharide enhanced PMN-MDSC gene expression and specifically induced a Type II interferon response with IL-6 production. Lox-1 was specifically expressed by cultured clot CD15+ neutrophils. Cultured clot neutrophils, but not activated platelets, shed copious amounts of soluble Lox-1 (sLox-1) with a donor-dependent amplitude. sLox-1 shedding was enhanced by phorbol ester and suppressed by heparin and by beta-glycerol phosphate, a phosphatase inhibitor. Cultured clot serum significantly enhanced endothelial cell monolayer barrier function, consistent with a pro-resolving bioactivity. This study suggests that PMN-MDSC activation is part of the innate immune response to coagulation which may have a protective role in inflammation. The cultured blood clot is an innovative thrombus model that can be used to study both sterile and nonsterile inflammatory states and could be used as a personalized medicine tool for drug screening.

Sections du résumé

BACKGROUND BACKGROUND
Blood clots are living tissues that release inflammatory mediators including IL-8/CXCL8 and MCP-1/CCL2. A deeper understanding of blood clots is needed to develop new therapies for pro-thrombotic disease states and regenerative medicine.
OBJECTIVES OBJECTIVE
Identify a common transcriptional shift in cultured blood clot leukocytes.
METHODS METHODS
Differential gene expression of whole blood and cultured clots (4h 37°C) was assessed by RNA sequencing (RNAseq), RT-PCR, proteomics, and histology (23 diverse healthy human donors). Cultured clot serum bioactivity was tested in endothelial barrier functional assays.
RESULTS RESULTS
All cultured clots developed a polymorphonuclear myeloid-derived suppressor cell (PMN-MDSC) signature, including upregulation of OLR1 (mRNA encoding lectin-like oxidized low density lipoprotein receptor 1, Lox-1), IL-8/CXCL8, CXCL2, CCL2, IL10, IL1A, SPP1, TREM1 and DUSP4/MKP. Lipopolysaccharide enhanced PMN-MDSC gene expression and specifically induced a Type II interferon response with IL-6 production. Lox-1 was specifically expressed by cultured clot CD15+ neutrophils. Cultured clot neutrophils, but not activated platelets, shed copious amounts of soluble Lox-1 (sLox-1) with a donor-dependent amplitude. sLox-1 shedding was enhanced by phorbol ester and suppressed by heparin and by beta-glycerol phosphate, a phosphatase inhibitor. Cultured clot serum significantly enhanced endothelial cell monolayer barrier function, consistent with a pro-resolving bioactivity.
CONCLUSIONS CONCLUSIONS
This study suggests that PMN-MDSC activation is part of the innate immune response to coagulation which may have a protective role in inflammation. The cultured blood clot is an innovative thrombus model that can be used to study both sterile and nonsterile inflammatory states and could be used as a personalized medicine tool for drug screening.

Identifiants

pubmed: 38135253
pii: S1538-7836(23)00912-1
doi: 10.1016/j.jtha.2023.12.014
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Auteurs

Julia Leonard (J)

Department of Bioengineering, George Mason University.

David Kepplinger (D)

Department of Statistics, George Mason University.

Virginia Espina (V)

Department of Systems Biology, George Mason University.

Pat Gillevet (P)

Department of Biology, George Mason University.

Yunbo Ke (Y)

Department of Anesthesiology, School of Medicine, University of Maryland at Baltimore.

Konstantin G Birukov (KG)

Department of Anesthesiology, School of Medicine, University of Maryland at Baltimore.

Allan Doctor (A)

Departments of Pediatrics & Bioengineering and Center for Blood Oxygen Transport and Hemostasis, School of Medicine, University of Maryland.

Caroline D Hoemann (CD)

Department of Bioengineering, George Mason University. Electronic address: choemann@gmu.edu.

Classifications MeSH