Platelets and Immune Responses During Thromboinflammation

Mezger, Matthias; Nording, Henry; Sauter, Manuela; Graf, Tobias; Heim, Christian; Bubnoff, Nikolas von; Ensminger, Stephan; Langer, Harald F.

doi:10.3389/fimmu.2019.01731

Cited by 103 publications

(113 citation statements)

References 165 publications

(225 reference statements)

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“…Following injury, restoration of vascular integrity, apoptosis, and recruitment of progenitor, stromal and immune cells are crucial for tissue restructuring, remodeling, and functionality. Platelets are involved in many of the stages of wound healing, and this is emphasized by the beneficial use of platelet‐rich plasma and platelet releasate in wound repair . They promote progenitor cell recruitment; promote cytokine, chemokine, proangiogenic, and growth factor release; and support fibrin generation and modulate immune and stromal cell recruitment and activation .…”

Section: Platelets Support Classical and Inflammatory Hemostasismentioning

confidence: 99%

The dual role of platelet‐innate immune cell interactions in thrombo‐inflammation

Rayes

Bourne

Brill

et al. 2020

Research and Practice in Thrombosis and Haemostasis

117

102

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Beyond their role in hemostasis and thrombosis, platelets are increasingly recognized as key regulators of the inflammatory response under sterile and infectious conditions. Both platelet receptors and secretion are critical for these functions and contribute to their interaction with the endothelium and innate immune system. Platelet-leukocyte interactions are increased in thrombo-inflammatory diseases and are sensitive biomarkers for platelet activation and targets for the development of new therapies. The crosstalk between platelets and innate immune cells promotes thrombosis, inflammation, and tissue damage. However, recent studies have shown that these interactions also regulate the resolution of inflammation, tissue repair, and wound healing. Many of the platelet and leukocyte receptors involved in these bidirectional interactions are not selective for a subset of immune cells. However, specific heterotypic interactions occur in different vascular beds and inflammatory conditions, raising the possibility of disease-and organ-specific pathways of intervention. In this review, we highlight and discuss prominent and emerging interrelationships between platelets and innate immune cells and their dual role in the regulation of the inflammatory response in sterile and infectious thrombo-inflammatory diseases. A better understanding of the functional relevance of these interactions in different vascular beds may provide opportunities for successful therapeutic interventions to regulate the development, progression, and chronicity of various pathological processes. K E Y W O R D S immune cells, inflammation, platelets, thrombo-inflammation, thrombosis Essentials • Platelet-innate immune cell interactions regulate the development and outcome of thrombo-inflammatory diseases • Platelet activation potentiates innate immune cell recruitment, activation, and transmigration • Platelets promote the progression and resolution of inflammation in a disease-specific manner • Platelet-leukocyte interactions differentially regulate thrombo-inflammation Handling Editor: Cihan Ay JR, JHB AB, and SPW wrote the manuscript. ORCID Julie Rayes

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Section: Platelets Support Classical and Inflammatory Hemostasismentioning

confidence: 99%

The dual role of platelet‐innate immune cell interactions in thrombo‐inflammation

Rayes

Bourne

Brill

et al. 2020

Research and Practice in Thrombosis and Haemostasis

117

102

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“…Therefore, we believe that platelets play an important role in severe acute lung injury after renal transplantation. Numerous studies have confirmed that platelets play not only a leading role in coagulation and thrombosis but also a key role in inflammation [36][37][38]. Platelets in the blood mainly exert anti-infection effects through the following mechanisms: ① After inflammatory stimulation, platelet Pselectin is transferred from the cytoplasm to the surface of the cell membrane, inducing adhesion of PMNs to endometrial cells and promoting the formation of neutrophil extracellular traps [39,40].…”

mentioning

confidence: 99%

The Inhibition of P-Selectin Reduced Severe Acute Lung Injury in Immunocompromised Mice

Yang

Gao

et al. 2020

Oxidative Medicine and Cellular Longevity

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In an immunocompetent host, excess infiltration of immune cells in the lung is a key factor in infection-induced severe acute lung injury. Kidney transplant patients are immunocompromised by the use of immunosuppressive drugs. Immune cell infiltration in the lung in a renal transplant recipient suffering from pulmonary infection is significantly less than that in an immunocompetent host; however, the extent of lung injury in renal transplant patients is more serious than that in immunocompetent hosts. Therefore, we explored the role of platelet activation in a Klebsiella pneumoniae-induced lung injury model with P-selectin gene knockout mice or wild-type mice. Our study suggested that the inhibition of platelets reduced severe acute lung injury and increased survival after acute lung infection in mice. In addition, P-selectin expression on the surface of platelets in mice increased after administration of immunosuppressive drugs, and the extent of lung injury induced by infection decreased in P-selectin gene knockout mice. In conclusion, p-selectin plays a key role in severe acute lung injury in immunocompromised mice by reducing platelet activation and inflammatory processes.

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“…Of major importance, glycoprotein (GP) Ib-IX-V, which binds VWF as well as P-selectin, Factors XI and XII, leukocyte integrin αMβ2, collagen, thrombin and kininogen, and GPVI, which binds collagen, fibrin and laminin (22), initiate platelet adhesion events. These receptors act in concert (23) to translate cues from the surrounding vascular environment to mediate molecular signaling pathways that lead to platelet activation, platelet adhesion as well as mediating interactions with other cells (24,25). The goal is for platelets to adhere and seal the damaged vessel area, thus maintaining hemostasis (26).…”

Section: Adheso-signaling Receptorsmentioning

confidence: 99%

Imaging Platelet Processes and Function—Current and Emerging Approaches for Imaging in vitro and in vivo

et al. 2020

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Platelets are small anucleate cells that are essential for many biological processes including hemostasis, thrombosis, inflammation, innate immunity, tumor metastasis, and wound healing. Platelets circulate in the blood and in order to perform all of their biological roles, platelets must be able to arrest their movement at an appropriate site and time. Our knowledge of how platelets achieve this has expanded as our ability to visualize and quantify discreet platelet events has improved. Platelets are exquisitely sensitive to changes in blood flow parameters and so the visualization of rapid intricate platelet processes under conditions found in flowing blood provides a substantial challenge to the platelet imaging field. The platelet's size (∼2 µm), rapid activation (milliseconds), and unsuitability for genetic manipulation, means that appropriate imaging tools are limited. However, with the application of modern imaging systems to study platelet function, our understanding of molecular events mediating platelet adhesion from a single-cell perspective, to platelet recruitment and activation, leading to thrombus (clot) formation has expanded dramatically. This review will discuss current platelet imaging techniques in vitro and in vivo, describing how the advancements in imaging have helped answer/expand on platelet biology with a particular focus on hemostasis. We will focus on platelet aggregation and thrombus formation, and how platelet imaging has enhanced our understanding of key events, highlighting the knowledge gained through the application of imaging modalities to experimental models in vitro and in vivo. Furthermore, we will review the limitations of current imaging techniques, and questions in thrombosis research that remain to be addressed. Finally, we will speculate how the same imaging advancements might be applied to the imaging of other vascular cell biological functions and visualization of dynamic cell-cell interactions.

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Platelets and Immune Responses During Thromboinflammation

Cited by 103 publications

References 165 publications

The dual role of platelet‐innate immune cell interactions in thrombo‐inflammation

The dual role of platelet‐innate immune cell interactions in thrombo‐inflammation

The Inhibition of P-Selectin Reduced Severe Acute Lung Injury in Immunocompromised Mice

Imaging Platelet Processes and Function—Current and Emerging Approaches for Imaging in vitro and in vivo

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