Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stress

Cancer is associated with systemic pathologies that contribute to mortality, such as thrombosis and distant organ failure. The aim of this study was to investigate the potential role of neutrophil extracellular traps (NETs) in myocardial inflammation and tissue damage in treatment-naïve individuals...

Full description

Saved in:
Bibliographic Details
Main Authors: J. Cedervall, M. Herre, A. Dragomir, F. Rabelo-Melo, A. Svensson, C. Thålin, A. Rosell, V. Hjalmar, H. Wallén, H. Lindman, G. Pejler, E. Hagström, M. Hultström, A. Larsson, AK. Olsson
Format: Article
Language:English
Published: Taylor & Francis Group 2022-12-01
Series:OncoImmunology
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/2162402X.2022.2049487
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849774122514513920
author J. Cedervall
M. Herre
A. Dragomir
F. Rabelo-Melo
A. Svensson
C. Thålin
A. Rosell
V. Hjalmar
H. Wallén
H. Lindman
G. Pejler
E. Hagström
M. Hultström
A. Larsson
AK. Olsson
author_facet J. Cedervall
M. Herre
A. Dragomir
F. Rabelo-Melo
A. Svensson
C. Thålin
A. Rosell
V. Hjalmar
H. Wallén
H. Lindman
G. Pejler
E. Hagström
M. Hultström
A. Larsson
AK. Olsson
author_sort J. Cedervall
collection DOAJ
description Cancer is associated with systemic pathologies that contribute to mortality, such as thrombosis and distant organ failure. The aim of this study was to investigate the potential role of neutrophil extracellular traps (NETs) in myocardial inflammation and tissue damage in treatment-naïve individuals with cancer. Mice with mammary carcinoma (MMTV-PyMT) had increased plasma levels of NETs measured as H3Cit-DNA complexes, paralleled with elevated coagulation, compared to healthy littermates. MMTV-PyMT mice displayed upregulation of pro-inflammatory markers in the heart, myocardial hypertrophy and elevated cardiac disease biomarkers in the blood, but not echocardiographic heart failure. Moreover, increased endothelial proliferation was observed in hearts from tumor-bearing mice. Removal of NETs by DNase I treatment suppressed the myocardial inflammation, expression of cardiac disease biomarkers and endothelial proliferation. Compared to a healthy control group, treatment-naïve cancer patients with different malignant disorders had increased NET formation, which correlated to plasma levels of the inflammatory marker CRP and the cardiac disease biomarkers NT-proBNP and sTNFR1, in agreement with the mouse data. Altogether, our data indicate that NETs contribute to inflammation and myocardial stress during malignancy. These findings suggest NETs as potential therapeutic targets to prevent cardiac inflammation and dysfunction in cancer patients.
format Article
id doaj-art-34187af0dbf445fb9bafb39e14648dd2
institution DOAJ
issn 2162-402X
language English
publishDate 2022-12-01
publisher Taylor & Francis Group
record_format Article
series OncoImmunology
spelling doaj-art-34187af0dbf445fb9bafb39e14648dd22025-08-20T03:01:50ZengTaylor & Francis GroupOncoImmunology2162-402X2022-12-0111110.1080/2162402X.2022.2049487Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stressJ. Cedervall0M. Herre1A. Dragomir2F. Rabelo-Melo3A. Svensson4C. Thålin5A. Rosell6V. Hjalmar7H. Wallén8H. Lindman9G. Pejler10E. Hagström11M. Hultström12A. Larsson13AK. Olsson14Department of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, Biomedical Center, Uppsala, SwedenDepartment of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, Biomedical Center, Uppsala, SwedenDepartment of Immunology, Genetics and Pathology, Uppsala University, Rudbeck Laboratory, Uppsala, SwedenDepartment of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, Biomedical Center, Uppsala, SwedenDepartment of Medical Cell Biology, Integrative Physiology, Uppsala University, Uppsala, SwedenDepartment of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Stockholm, SwedenDepartment of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Stockholm, SwedenDepartment of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Stockholm, SwedenDepartment of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Stockholm, SwedenDepartment of Immunology, Genetics and Pathology, Uppsala University, Rudbeck Laboratory, Uppsala, SwedenDepartment of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, Biomedical Center, Uppsala, SwedenDepartment of Medical Sciences, Uppsala University, Uppsala, SwedenDepartment of Medical Cell Biology, Integrative Physiology, Uppsala University, Uppsala, SwedenDepartment of Medical Sciences, Uppsala University, Uppsala, SwedenDepartment of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, Biomedical Center, Uppsala, SwedenCancer is associated with systemic pathologies that contribute to mortality, such as thrombosis and distant organ failure. The aim of this study was to investigate the potential role of neutrophil extracellular traps (NETs) in myocardial inflammation and tissue damage in treatment-naïve individuals with cancer. Mice with mammary carcinoma (MMTV-PyMT) had increased plasma levels of NETs measured as H3Cit-DNA complexes, paralleled with elevated coagulation, compared to healthy littermates. MMTV-PyMT mice displayed upregulation of pro-inflammatory markers in the heart, myocardial hypertrophy and elevated cardiac disease biomarkers in the blood, but not echocardiographic heart failure. Moreover, increased endothelial proliferation was observed in hearts from tumor-bearing mice. Removal of NETs by DNase I treatment suppressed the myocardial inflammation, expression of cardiac disease biomarkers and endothelial proliferation. Compared to a healthy control group, treatment-naïve cancer patients with different malignant disorders had increased NET formation, which correlated to plasma levels of the inflammatory marker CRP and the cardiac disease biomarkers NT-proBNP and sTNFR1, in agreement with the mouse data. Altogether, our data indicate that NETs contribute to inflammation and myocardial stress during malignancy. These findings suggest NETs as potential therapeutic targets to prevent cardiac inflammation and dysfunction in cancer patients.https://www.tandfonline.com/doi/10.1080/2162402X.2022.2049487Neutrophil extracellular trapsNETscancercardiachypertrophyinflammation
spellingShingle J. Cedervall
M. Herre
A. Dragomir
F. Rabelo-Melo
A. Svensson
C. Thålin
A. Rosell
V. Hjalmar
H. Wallén
H. Lindman
G. Pejler
E. Hagström
M. Hultström
A. Larsson
AK. Olsson
Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stress
OncoImmunology
Neutrophil extracellular traps
NETs
cancer
cardiac
hypertrophy
inflammation
title Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stress
title_full Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stress
title_fullStr Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stress
title_full_unstemmed Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stress
title_short Neutrophil extracellular traps promote cancer-associated inflammation and myocardial stress
title_sort neutrophil extracellular traps promote cancer associated inflammation and myocardial stress
topic Neutrophil extracellular traps
NETs
cancer
cardiac
hypertrophy
inflammation
url https://www.tandfonline.com/doi/10.1080/2162402X.2022.2049487
work_keys_str_mv AT jcedervall neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT mherre neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT adragomir neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT frabelomelo neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT asvensson neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT cthalin neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT arosell neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT vhjalmar neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT hwallen neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT hlindman neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT gpejler neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT ehagstrom neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT mhultstrom neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT alarsson neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress
AT akolsson neutrophilextracellulartrapspromotecancerassociatedinflammationandmyocardialstress