Elongated neutrophil-derived structures are blood-borne microparticles formed by rolling neutrophils during sepsis

Márki, Alex; Buscher, Konrad; Lorenzini, Cristina B; Meyer, Matthew; Saigusa, Ryosuke; Fan, Zhichao; Yeh, Yi‐Ting; Hartmann, N; Dan, Jennifer M.; Kiosses, William B.; Golden, Gregory J.; Ganesan, Rajee; Winkels, Holger; Orecchioni, Marco; McArdle, Sara; Mikulski, Zbigniew; Altman, Yoav; Bui, Jack D.; Kronenberg, Mitchell; Chien, Shu; Esko, Jeffrey D.; Nizet, Victor; Smalley, David M.; Roth, Johannes; Ley, Klaus

doi:10.1084/jem.20200551

Cited by 31 publications

(45 citation statements)

References 56 publications

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“…A recent study discovered a new type of neutrophil membrane deposit that results from tether formation and called the deposits elongated neutrophil-derived structures (ENDS). They showed that ENDS do not contain DNA, mitochondria or endoplasmic reticulum (ER) and that they slowly degrade over time (Marki et al, 2021). Another study observed similar particles, but referred to the remnants that migrating neutrophils leave behind on the endothelium and in the interstitium of infected tracheal tissue as neutrophil 'trails' (Lim et al, 2015).…”

Section: Neutrophil Trails As Cues For Subsequent Temmentioning

confidence: 98%

“…However, this may not be the only reason for neutrophil-induced successive TEM. It has been shown that neutrophils can form tethers and deposit microparticles on the endothelium (Schmidtke and Diamond, 2000;Marki et al, 2017Marki et al, , 2021). An interesting hypothesis could be that these deposits contain cues for other leukocytes to aid in their TEM.…”

Section: Neutrophil Trails As Cues For Subsequent Temmentioning

confidence: 99%

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Neutrophil transendothelial migration hotspots – mechanisms and implications

Grönloh

Arts

Buul

2021

Journal of Cell Science

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During inflammation, leukocytes circulating in the blood stream exit the vasculature in a process called leukocyte transendothelial migration (TEM). The current paradigm of this process comprises several well-established steps, including rolling, adhesion, crawling, diapedesis and sub-endothelial crawling. Nowadays, the role of the endothelium in transmigration is increasingly appreciated. It has been established that leukocyte exit sites on the endothelium and in the pericyte layer are in fact not random but instead may be specifically recognized by migrating leukocytes. Here, we review the concept of transmigration hotspots, specific sites in the endothelial and pericyte layer where most transmigration events take place. Chemokine cues, adhesion molecules and membrane protrusions as well as physical factors, such as endothelial junction stability, substrate stiffness, the presence of pericytes and basement membrane composition, may all contribute to local hotspot formation to facilitate leukocytes exiting the vasculature. In this Review, we discuss the biological relevance of such hotspots and put forward multiple mechanisms and factors that determine a functional TEM hotspot.

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Section: Neutrophil Trails As Cues For Subsequent Temmentioning

confidence: 98%

Section: Neutrophil Trails As Cues For Subsequent Temmentioning

confidence: 99%

Neutrophil transendothelial migration hotspots – mechanisms and implications

Grönloh

Arts

Buul

2021

Journal of Cell Science

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“…This may be related to a recent report which demonstrated that rolling neutrophils on the vessel wall form tethers that, when detached, form elongated neutrophil‐derived structures (ENDS). These novel types of neutrophil‐derived microparticles do not express tetraspanins but represent another specific type of EVs originating from cellular extensions (Marki et al., 2021 ).…”

Section: Association Of Protrusion Derived Evs With Cell Migrationmentioning

confidence: 99%

Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

Rilla

2021

J of Extracellular Vesicle

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Plasma membrane curvature is an important factor in the regulation of cellular phenotype and is critical for various cellular activities including the shedding of extracellular vesicles (EV). One of the most striking morphological features of cells is different plasma membrane‐covered extensions supported by actin core such as filopodia and microvilli. Despite the various functions of these extensions are partially unexplained, they are known to facilitate many crucial cellular functions such as migration, adhesion, absorption, and secretion. Due to the rapid increase in the research activity of EVs, there is raising evidence that one of the general features of cellular plasma membrane protrusions is to act as specialized platforms for the budding of EVs. This review will focus on early observations and recent findings supporting this hypothesis, discuss the putative budding and shedding mechanisms of protrusion‐derived EVs and their biological significance.

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“…28 Notably, while tethers appear to engage in more stable interactions, at very high shear rates such as during septic conditions, they rupture from neutrophils, forming so called S100A8/A9-rich "elongated neutrophil-derived structures". 29 These structures release S100A8/A9 into the environment depending on calcium levels which may actively promote the inflammatory milieu at the endothelial surface.…”

Section: A Capturing and Rollingmentioning

confidence: 99%

Neutrophils in acute inflammation: current concepts and translational implications

Margraf

Lowell

Zarbock

2022

Blood

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Modulation of neutrophil recruitment and function is crucial for targeting inflammatory cells to sites of infection to combat invading pathogens while at the same time limiting host tissue injury or autoimmunity. The underlying mechanisms regulating recruitment of neutrophils, one of the most abundant inflammatory cells, have gained increasing interest over the years. The previously described classical recruitment cascade of leukocytes has been extended to include not only capturing, rolling, adhesion, crawling and transmigration but furthermore a reverse-transmigration step that is crucial for balancing immune defense and control of remote organ endothelial leakage. Current developments in the field emphasize the importance of cellular interplay, tissue-environmental cues, circadian rhythmicity, detection of neutrophil phenotypes, differential chemokine sensing, and contribution of distinct signaling components to receptor activation and integrin conformations. Use of therapeutics modulating neutrophil activation responses as well as mutations causing dysfunctional neutrophil receptors and impaired signaling cascades have been defined in translational animal models. Human correlates of such mutations result in increased susceptibility to infections or organ damage. This review focuses on current advances in the understanding of the regulation of neutrophil recruitment and functionality and translational implications of current discoveries in the field with a focus on acute inflammation and sepsis.

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Elongated neutrophil-derived structures are blood-borne microparticles formed by rolling neutrophils during sepsis

Cited by 31 publications

References 56 publications

Neutrophil transendothelial migration hotspots – mechanisms and implications

Neutrophil transendothelial migration hotspots – mechanisms and implications

Diverse plasma membrane protrusions act as platforms for extracellular vesicle shedding

Neutrophils in acute inflammation: current concepts and translational implications

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