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Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps
Abstract
Neutrophil extracellular traps (NETs) represent extracellular structures able to bind and kill microorganisms. It is believed that they are generated by neutrophils undergoing cell death, allowing these dying or dead cells to kill microbes. We show that, following priming with granulocyte/macrophage colony-stimulating factor (GM-CSF) and subsequent short-term toll-like receptor 4 (TLR4) or complement factor 5a (C5a) receptor stimulation, viable neutrophils are able to generate NETs. Strikingly, NETs formed by living cells contain mitochondrial, but no nuclear, DNA. Pharmacological or genetic approaches to block reactive oxygen species (ROS) production suggested that NET formation is ROS dependent. Moreover, neutrophil populations stimulated with GM-CSF and C5a showed increased survival compared with resting neutrophils, which did not generate NETs. In conclusion, mitochondrial DNA release by neutrophils and NET formation do not require neutrophil death and do also not limit the lifespan of these cells.
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“Different cellular lineages (10–18) may extrude their mitochondria upon activation.”
From Autoantibodies in Systemic Lupus Erythematosus Target Mitochondrial RNA (2019) · cites this paper as [10]
In the citing paper
“Various cellular lineages are capable of extruding their mitochondria. Activated mast cells10, T-cells11, eosinophils12, hepatocytes13, neutrophils14–16 and platelets17,18, in addition to damaged organs or tissues7,13,19,20, release extracellular mitochondria.”
From Anti-mitochondrial autoantibodies in systemic lupus erythematosus and their association with disease manifestations (2019) · cites this paper as [14]
In the citing paper
“during immune response, neutrophils utilize mtDNA as a structural molecule to bind cytotoxic proteins into neutrophil extracellular traps (NETs), which are then released onto advancing plaque biofilms (Yousefi et al., 2009)”
From Successful enrichment and recovery of whole mitochondrial genomes from ancient human dental calculus (2016) · cites this paper as Yousefi et al., 2009
In the citing paper
“Several reports demonstrate that a considerable fraction of the nucleic acids contained in NETs is of mitochondrial, rather than nuclear, origin [724–728].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [724]
In the citing paper
“both NETotic cell death and NET extrusion in the absence of RCD appears to rely on the activity of NADPH oxidases [724, 736, 737].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [724]
In the citing paper
“NET extrusion per se does not necessarily result in cellular lysis [722, 724, 735].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [724]
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Metadata
- Authors
- Yousefi, S., Mihalache, C., Kozlowski, E., Schmid, I., & Simon, H. U.
- Affiliations
- University of Bern (CH)
- Corresponding author
- Yousefi, S
- ORCID
- Venue
- Cell Death & Differentiation
- Published
- 2009-07-17
- Volume
- 16
- Issue
- 11
- Pages
- 1438-1444
- ISSN
- 1350-9047 (ISSN-L)
- 1476-5403
- OpenAlex
- W2056112680
- Cited by
- 1,036
- References
- 17
- Citations by year
- 2026: 84 · 2025: 82 · 2024: 67 · 2023: 89 · 2022: 92 · 2021: 93 · 2020: 84 · 2019: 79 · 2018: 66 · 2017: 57 · 2016: 66 · 2015: 43 · 2014: 28 · 2013: 36 · 2012: 36
- FWCI
- 9.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cell Death and Differentiation (publishedVersion)
- PubMed (publishedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (107526, 112078)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- neutrophil extracellular traps, mitochondrial DNA release, neutrophil survival, reactive oxygen species, GM-CSF, TLR4, C5a receptor, innate immunity, antimicrobial defense
- MeSH terms
- DNA, Mitochondrial, Humans, Neutrophils, Complement C5a, Granulocyte-Macrophage Colony-Stimulating Factor, Apoptosis, Reactive Oxygen Species, Neutrophil Activation, Toll-Like Receptor 4
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