Neutrophil extracellular trap fragments stimulate innate immune responses that prevent lung transplant tolerance

Scozzi, Davide; Wang, Xingan; Liao, Fuyi; Liu, Zhiyi; Zhu, Jihong; Pugh, Katy; Ibrahim, Mohsen; Hsiao, Hsi-Min; Miller, Mark J.; Yizhan, Guo; Mohanakumar, Thalachallour; Krupnick, Alexander S.; Kreisel, Daniel; Gelman, Andrew E.

doi:10.1111/ajt.15163

Cited by 58Transplantation: Methods and OutcomesNeutrophil, Myeloperoxidase and Oxidative MechanismsT-cell and B-cell Immunology

Neutrophil extracellular trap fragments stimulate innate immune responses that prevent lung transplant tolerance

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Scozzi, Davide, Wang, Xingan, Liao, Fuyi, Liu, Zhiyi, Zhu, Jihong, Pugh, Katy, Ibrahim, Mohsen, Hsiao, Hsi-Min +6 more·2019·American Journal of Transplantation

DOI 10.1111/ajt.15163PMC PMC6438629

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Abstract

Neutrophil extracellular traps (NETs) have been shown to worsen acute pulmonary injury including after lung transplantation. The breakdown of NETs by DNAse-1 can help restore lung function, but whether there is an impact on allograft tolerance remains less clear. Using intravital 2-photon microscopy, we analyzed the effects of DNAse-1 on NETs in mouse orthotopic lung allografts damaged by ischemia-reperfusion injury. Although DNAse-1 treatment rapidly degrades intragraft NETs, the consequential release of NET fragments induces prolonged interactions between infiltrating CD4+ T cells and donor-derived antigen presenting cells. DNAse-1 generated NET fragments also promote human alveolar macrophage inflammatory cytokine production and prime dendritic cells for alloantigen-specific CD4+ T cell proliferation through activating toll-like receptor (TLR) — Myeloid Differentiation Primary Response 88 (MyD88) signaling pathways. Furthermore, and in contrast to allograft recipients with a deficiency in NET generation due to a neutrophil-specific ablation of Protein Arginine Deiminase 4 (PAD4), DNAse-1 administration to wild-type recipients promotes the recognition of allo- and self-antigens and prevents immunosuppression-mediated lung allograft acceptance through a MyD88-dependent pathway. Taken together, these data show that the rapid catalytic release of NET fragments promotes innate immune responses that prevent lung transplant tolerance.

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The degradation process of NETs leaves behind fragments of NETs that could still be biologically active.
“research shows that the degradation process leaves behind fragments of NETs which could still be biologically active [94]”
From A novel tumor-immune microenvironment (TIME)-on-Chip mimics three dimensional neutrophil-tumor dynamics and neutrophil extracellular traps (NETs)-mediated collective tumor invasion (2021) · cites this paper as [94]

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American Journal of Transplantation: Volume 19, Number 4, April 2019
(2019) · American Journal of Transplantation · doi:10.1111/ajt.15332
The Real Time Visualization of Neutrophil Extracellular Trap Formation in Lung Transplants Reveals a Critical Role in Tolerance
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Authors: Scozzi, D., Wang, X., Liao, F., Liu, Z., Zhu, J., Pugh, K., Ibrahim, M., Hsiao, H.-M., Miller, M. J., Yizhan, G., Mohanakumar, T., Krupnick, A. S., Kreisel, D., & Gelman, A. E.
Affiliations: Washington University in St. Louis (US)
University of Virginia (US)
St. Joseph's Hospital and Medical Center (US)
Corresponding author: Gelman, Andrew E.
ORCID: Scozzi, Davide
Wang, Xingan
Liao, Fuyi
Liu, Zhiyi
Ibrahim, Mohsen
Hsiao, Hsi-Min
Miller, Mark J.
Mohanakumar, Thalachallour
Krupnick, Alexander S.
Kreisel, Daniel
Gelman, Andrew E.
Venue: American Journal of Transplantation
Publisher: Elsevier BV
Published: 2019-04
Volume: 19
Issue: 4
Pages: 1011-1023
ISSN: 1600-6135 (ISSN-L)
DOI: 10.1111/ajt.15163
PMC: PMC6438629
OpenAlex: W2899203237
Cited by: 58
References: 51
Citations by year: 2026: 7 · 2025: 5 · 2024: 10 · 2023: 7 · 2022: 12 · 2021: 4 · 2020: 6 · 2019: 7
FWCI: 4.42
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor, 1327 d)
Locations: American Journal of Transplantation (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, other-oa)
Funders: National Institutes of Health (2RHL094601, P01AI116501‐01, R01HL113436‐01A1, R21AI119506)
Topics: Health Sciences › Medicine › Surgery › Transplantation: Methods and Outcomes
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: neutrophil extracellular traps, lung transplantation, allograft tolerance, DNase1, PAD4, MyD88 signaling, Toll-like receptors, dendritic cells, CD4+ T cells, alveolar macrophages, ischemia-reperfusion injury, innate immunity, immunosuppression
MeSH terms: Animals, Cells, Cultured, Dendritic Cells, Deoxyribonucleases, Enzyme-Linked Immunosorbent Assay, Humans, Immunity, Innate, Mice, Inbred BALB C, Reperfusion Injury, Lung Transplantation, Macrophages, Alveolar, Inflammation Mediators, Transplantation Tolerance, Mice, Extracellular Traps

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Neutrophil extracellular trap fragments stimulate innate immune responses that prevent lung transplant tolerance

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