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Circulating mitochondrial DAMPs cause inflammatory responses to injury
Open accessAbstract
Injury causes a systemic inflammatory response syndrome (SIRS) that is clinically much like sepsis. Microbial pathogen-associated molecular patterns (PAMPs) activate innate immunocytes through pattern recognition receptors. Similarly, cellular injury can release endogenous 'damage'-associated molecular patterns (DAMPs) that activate innate immunity. Mitochondria are evolutionary endosymbionts that were derived from bacteria and so might bear bacterial molecular motifs. Here we show that injury releases mitochondrial DAMPs (MTDs) into the circulation with functionally important immune consequences. MTDs include formyl peptides and mitochondrial DNA. These activate human polymorphonuclear neutrophils (PMNs) through formyl peptide receptor-1 and Toll-like receptor (TLR) 9, respectively. MTDs promote PMN Ca(2+) flux and phosphorylation of mitogen-activated protein (MAP) kinases, thus leading to PMN migration and degranulation in vitro and in vivo. Circulating MTDs can elicit neutrophil-mediated organ injury. Cellular disruption by trauma releases mitochondrial DAMPs with evolutionarily conserved similarities to bacterial PAMPs into the circulation. These signal through innate immune pathways identical to those activated in sepsis to create a sepsis-like state. The release of such mitochondrial 'enemies within' by cellular injury is a key link between trauma, inflammation and SIRS.
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“these organelles express biomolecules that resemble those expressed by prokaryotes, such as cardiolipin, double-stranded-hypomethylated DNA and N-formylated peptides12,13”
From The role of mitochondria in rheumatic diseases (2022) · cites this paper as [13]
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“In human neutrophils, the binding of FPR1 and FPR2 to N-formylated peptides triggers the release of Ca2+ into the cytosol and ultimately leads to the migration and activation of neutrophils13”
From The role of mitochondria in rheumatic diseases (2022) · cites this paper as [13]
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“Mitochondria are considered as deriving from the endosymbiosis of an α-synfular; proteobacterium (3, 4), providing the organelles many bacterial features (3, 5–9).”
From Autoantibodies in Systemic Lupus Erythematosus Target Mitochondrial RNA (2019) · cites this paper as [9]
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“Cardiolipin, N-formylated peptides, mtDNA, ATP and reactive oxygen species are known mitochondrial damage-associated molecular patterns (9, 28–30).”
From Autoantibodies in Systemic Lupus Erythematosus Target Mitochondrial RNA (2019) · cites this paper as [9]
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“Mitochondrial debris were observed in blood in the Twin Study (Garrett-Bakelman et al., 2019) and mitochondrial damage-associated molecular patterns (DAMPs) activate innate immune pathways (Banoth and Cassel, 2018; Zhang et al., 2010).”
From Comprehensive Multi-omics Analysis Reveals Mitochondrial Stress as a Central Biological Hub for Spaceflight Impact (2020) · cites this paper as Zhang et al., 2010
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“In an extreme example such as massive trauma, mito-DAMPs, identified as mtDNA and formyl peptides, are acutely released from damaged tissues and cause a sepsis-like systemic inflammatory response syndrome by activating polymorphonuclear cells via TLR9 and formyl peptide receptor-129.”
From Hepatocyte mitochondria-derived danger signals directly activate hepatic stellate cells and drive progression of liver fibrosis (2020) · cites this paper as [29]
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“Like bacteria, mitochondria are formed of an outer and an inner membrane (inner contains cardiolipin)4,5, express formylated peptides6,7, and contain a circular genome with hypomethylated DNA CpG motifs, referred to as mitochondrial DNA (mtDNA)8,9.”
From Anti-mitochondrial autoantibodies in systemic lupus erythematosus and their association with disease manifestations (2019) · cites this paper as [6]
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“Mitochondria and their components (e.g. N-formylated peptides and mtDNA) are recognized as damage-associated molecular patterns (DAMPs), which activate the innate immune system and elicit an inflammatory response6,21–23.”
From Anti-mitochondrial autoantibodies in systemic lupus erythematosus and their association with disease manifestations (2019) · cites this paper as [6]
In the citing paper
“MtDNA has been reported to activate immunity through two distinct pathways, namely Toll-like receptor 9 (TLR9; Zhang et al, 2010;Oka et al, 2012;Liu et al, 2015), and cGAS activation (White et al, 2014;West et al, 2015).”
From Mitochondrial DNA and TLR9 drive muscle inflammation upon Opa1 deficiency (2018) · cites this paper as Zhang et al, 2010
In the citing paper
“Mitochondria are a source of damage-associated molecular patterns (DAMPs), and among others, mtDNA has been shown to induce a pro-inflammatory state (Zhang et al, 2010;Oka et al, 2012;Wenceslau et al, 2014).”
From Mitochondrial DNA and TLR9 drive muscle inflammation upon Opa1 deficiency (2018) · cites this paper as Zhang et al, 2010
In the citing paper
“MtDNA is recognized as foreign when found outside of mitochondria and can trigger inflammation (Maekawa et al., 2019; Shimada et al., 2012; Zhang et al., 2010).”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Zhang et al., 2010
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“mtDNA is known to localize to endosomes”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Zhang et al., 2010
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“activate DNA sensor and pro-inflammatory mediator TLR9 (Zhang et al., 2010)”
From Cytoplasmic DNA: sources, sensing, and role in aging and disease (2021) · cites this paper as Zhang et al., 2010
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Metadata
- Authors
- Zhang, Q., Raoof, M., Chen, Y., Sumi, Y., Sursal, T., Junger, W., Brohi, K., Itagaki, K., & Hauser, C. J.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- Queen Mary University of London (GB)
- Corresponding author
- Hauser, Carl J.
- ORCID
- Venue
- Nature
- Published
- 2010-03
- Volume
- 464
- Issue
- 7285
- Pages
- 104-107
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2843437
- OpenAlex
- W2134219545
- Cited by
- 3,812
- References
- 34
- Citations by year
- 2026: 253 · 2025: 254 · 2024: 268 · 2023: 266 · 2022: 267 · 2021: 294 · 2020: 275 · 2019: 243 · 2018: 246 · 2017: 252 · 2016: 248 · 2015: 230 · 2014: 196 · 2013: 176 · 2012: 148
- FWCI
- 70.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- U.S. Department of Defense
- National Institute of General Medical Sciences (R01GM051477, R01GM059179)
- Congressionally Directed Medical Research Programs
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Sepsis Diagnosis and Treatment
- Keywords
- mitochondrial DAMPs, mitochondrial damage-associated molecular patterns, mitochondrial DNA, formyl peptides, FPR1, TLR9, neutrophils, systemic inflammatory response syndrome, trauma (physical injury), innate immunity, neutrophil degranulation, MAPK signaling, target organ damage
- MeSH terms
- Animals, Cells, Cultured, DNA, Mitochondrial, Femur, Humans, Immunity, Innate, Liver, Male, Mitochondria, N-Formylmethionine Leucyl-Phenylalanine, Neutrophils, Phosphorylation, Wounds and Injuries, Rats, Sprague-Dawley, Muscle, Skeletal, Systemic Inflammatory Response Syndrome, Sepsis, CpG Islands, Calcium Signaling, Mitogen-Activated Protein Kinases, Receptors, Formyl Peptide, Fractures, Bone, Toll-Like Receptor 9, Rats, Acute Lung Injury
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