Calpain-1 weakens the nuclear envelope and promotes the release of neutrophil extracellular traps

The inducers of neutrophil extracellular trap (NET) formation are heterogeneous and consequently, there is no specific pathway or signature molecule indispensable for NET formation. But certain events such as histone modification, chromatin decondensation, nuclear envelope breakdown, and NET release are ubiquitous. During NET formation, neutrophils drastically rearrange their cytoplasmic, granular and nuclear content. Yet, the exact mechanism for decoding each step during NET formation still remains elusive. Here, we investigated the mechanism of nuclear envelope breakdown during NET formation. Immunofluorescence microscopic evaluation revealed a gradual disintegration of outer nuclear membrane protein nesprin-1 and alterations in nuclear morphology during NET formation. MALDI-TOF analysis of NETs that had been generated by various inducers detected the accumulation of nesprin-1 fragments. This suggests that nesprin-1 degradation occurs before NET release. In the presence of a calpain-1, inhibitor nesprin-1 degradation was decreased in calcium driven NET formation. Microscopic evaluation confirmed that the disintegration of the lamin B receptor (LBR) and the collapse of the actin cytoskeleton occurs in early and later phases of NET release, respectively. We conclude that the calpain-1 degrades nesprin-1, orchestrates the weakening of the nuclear membrane, contributes to LBR disintegration, and promoting DNA release and finally, NETs formation.

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Publication Details

Journal
Cell Communication and Signaling
Published
2024-09-09
DOI
https://doi.org/10.1186/s12964-024-01785-6
Citations
13
Primary Topic
Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Type
article
Field-Weighted Citation Impact
3.13

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article

Calpain-1 weakens the nuclear envelope and promotes the release of neutrophil extracellular traps

Luis E. Muñoz, Felix Pfister, Christina Janko, Moritz Leppkes et al.
13 citations
Cell Communication and Signaling
Neutrophil, Myeloperoxidase and Oxidative Mechanisms
3.13
article

Calpain-1 weakens the nuclear envelope and promotes the release of neutrophil extracellular traps

Luis E. Muñoz, Felix Pfister, Christina Janko, Moritz Leppkes, Jeeshan Singh, Aparna Mahajan, Leticija Zlatar, Jasmin Knopf, Janina Schoen, Georg Andreas Schett, Martin Herrmann, Günter Lochnit, Marco Muñoz‐Becerra, Christine Schauer, Irmgard Herrmann
article en
13 citations

Abstract

The inducers of neutrophil extracellular trap (NET) formation are heterogeneous and consequently, there is no specific pathway or signature molecule indispensable for NET formation. But certain events such as histone modification, chromatin decondensation, nuclear envelope breakdown, and NET release are ubiquitous. During NET formation, neutrophils drastically rearrange their cytoplasmic, granular and nuclear content. Yet, the exact mechanism for decoding each step during NET formation still remains elusive. Here, we investigated the mechanism of nuclear envelope breakdown during NET formation. Immunofluorescence microscopic evaluation revealed a gradual disintegration of outer nuclear membrane protein nesprin-1 and alterations in nuclear morphology during NET formation. MALDI-TOF analysis of NETs that had been generated by various inducers detected the accumulation of nesprin-1 fragments. This suggests that nesprin-1 degradation occurs before NET release. In the presence of a calpain-1, inhibitor nesprin-1 degradation was decreased in calcium driven NET formation. Microscopic evaluation confirmed that the disintegration of the lamin B receptor (LBR) and the collapse of the actin cytoskeleton occurs in early and later phases of NET release, respectively. We conclude that the calpain-1 degrades nesprin-1, orchestrates the weakening of the nuclear membrane, contributes to LBR disintegration, and promoting DNA release and finally, NETs formation.

Cell Communication and SignalingVol. 22(1)
Friedrich-Alexander-Universität Erlangen-Nürnberg (DE), Justus-Liebig-Universität Gießen (DE), Heidelberg University (DE), University Hospital Heidelberg (DE), Universitätsklinikum Erlangen (DE), Else Kröner-Fresenius-Stiftung (DE), University Medical Centre Mannheim (DE)
European Commission, Friedrich-Alexander-Universität Erlangen-Nürnberg, Deutsche Forschungsgemeinschaft, Volkswagen Foundation, Bundesministerium für Bildung und Forschung, Universitätsklinikum Erlangen, Horizon 2020 Framework Programme
Openalex Percentile: Top 8%
Neutrophil, Myeloperoxidase and Oxidative Mechanisms
3.13
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