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Neutrophil-Delivered Myeloperoxidase Dampens the Hydrogen Peroxide Burst after Tissue Wounding in Zebrafish
Open accessAbstract
Prompt neutrophil arrival is critical for host defense immediately after injury [1-3]. Following wounding, a hydrogen peroxide (H(2)O(2)) burst generated in injured tissues is the earliest known leukocyte chemoattractant [4]. Generating this tissue-scale H(2)O(2) gradient uses dual oxidase [4] and neutrophils sense H(2)O(2) by a mechanism involving the LYN Src-family kinase [5], but the molecular mechanisms responsible for H(2)O(2) clearance are unknown [6]. Neutrophils carry abundant amounts of myeloperoxidase, an enzyme catalyzing an H(2)O(2)-consuming reaction [7, 8]. We hypothesized that this neutrophil-delivered myeloperoxidase downregulates the high tissue H(2)O(2) concentrations that follow wounding. This was tested in zebrafish using simultaneous fluorophore-based imaging of H(2)O(2) concentrations and leukocytes [4, 9-11] and a new neutrophil-replete but myeloperoxidase-deficient mutant (durif). Leukocyte-depleted zebrafish had an abnormally sustained wound H(2)O(2) burst, indicating that leukocytes themselves were required for H(2)O(2) downregulation. Myeloperoxidase-deficient zebrafish also had abnormally sustained high wound H(2)O(2) concentrations despite similar numbers of arriving neutrophils. A local H(2)O(2)/myeloperoxidase interaction within wound-recruited neutrophils was demonstrated. These data demonstrate that leukocyte-delivered myeloperoxidase cell-autonomously downregulates tissue-generated wound H(2)O(2) gradients in vivo, defining a new requirement for myeloperoxidase during inflammation. Durif provides a new animal model of myeloperoxidase deficiency closely phenocopying the prevalent human disorder [7, 12, 13], offering unique possibilities for investigating its clinical consequences.
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“For example, neutrophils may be partly responsible for their own resolution by clearance of the attractants that first drew them to the wound (128).”
From Wound repair and regeneration: Mechanisms, signaling, and translation (2014) · cites this paper as [128]
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Metadata
- Authors
- Pase, L., Layton, J. E., Wittmann, C., Ellett, F., Nowell, C. J., Reyes-Aldasoro, C. C., Varma, S., Rogers, K. L., Hall, C. J., Keightley, M. C., Crosier, P. S., Grabher, C., Heath, J. K., Renshaw, S. A., & Lieschke, G. J.
- Affiliations
- The University of Melbourne (AU)
- Walter and Eliza Hall Institute of Medical Research (AU)
- Karlsruhe Institute of Technology (DE)
- Ludwig Cancer Research (BE)
- Australian Regenerative Medicine Institute (AU)
- University of Auckland (NZ)
- University of Sheffield (GB)
- Corresponding author
- Lieschke, Graham J.
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 22
- Issue
- 19
- Pages
- 1818-1824
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2171239786
- Cited by
- 118
- References
- 32
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 4 · 2023: 8 · 2022: 3 · 2021: 10 · 2020: 13 · 2019: 11 · 2018: 13 · 2017: 5 · 2016: 7 · 2015: 12 · 2014: 16 · 2013: 8 · 2012: 1
- FWCI
- 5.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- City Research Online (City University London) (acceptedVersion)
- Figshare (submittedVersion, cc-by)
- ResearchSpace (University of Auckland) (submittedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL079545)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Keywords
- myeloperoxidase, neutrophils, hydrogen peroxide, wound healing, tissue damage, dual oxidase, Lyn kinase, myeloperoxidase deficiency, inflammation, leukocyte recruitment, zebrafish
- MeSH terms
- Animals, Hydrogen Peroxide, Leukocytes, Mutation, Peroxidase, Neutrophils, Zebrafish, Neutrophil Infiltration, Animals, Genetically Modified
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