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

Abstract

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.

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102. 102.

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     Not in our library10.1038/sj.jid.5700824

103. 103.

     de las Casas‐Engel M, Dominguez‐Soto A, Sierra‐Filardi E, Bragado R, Nieto C, Puig‐Kroger A, et al. Serotonin skews human macrophage polarization through HTR2B and HTR7. J Immunol. 2013;190:2301–10.

     Not in our library10.4049/jimmunol.1201133

104. 104.

     Cloutier N, Allaeys I, Marcoux G, Machlus KR, Mailhot B, Zufferey A, et al. Platelets release pathogenic serotonin and return to circulation after immune complex‐mediated sequestration. Proc Natl Acad Sci USA. 2018;115:E1550–E1559.

     Not in our library10.1073/pnas.1720553115

105. 105.

     Merhi Y, Guidoin R, Provost P, Leung TK, Lam JY. Increase of neutrophil adhesion and vasoconstriction with platelet deposition after deep arterial injury by angioplasty. Am Heart J. 1995;129:445–51.

     Not in our library10.1016/0002-8703(95)90266-x

106. 106.

     Massberg S, Brand K, Grüner S, Page S, Müller E, Müller I, et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med. 2002;196:887–96.

     Not in our library10.1084/jem.20012044

107. 107.

     Drechsler M, Megens RT, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia‐triggered neutrophilia promotes early atherosclerosis. Circulation. 2010;122:1837–45.

     Not in our library10.1161/circulationaha.110.961714

108. 108.

     Ylitalo R, Oksala O, Yla‐Herttuala S, Ylitalo P. Effects of clodronate (dichloromethylene bisphosphonate) on the development of experimental atherosclerosis in rabbits. J Lab Clin Med. 1994;123:769–76.

     Not in our library

109. 109.

     Bültmann A, Li Z, Wagner S, Peluso M, Schönberger T, Weis C, et al. Impact of glycoprotein VI and platelet adhesion on atherosclerosis–a possible role of fibronectin. J Mol Cell Cardiol. 2010;49:532–42.

     Not in our library10.1016/j.yjmcc.2010.04.009

110. 110.

     Jamasbi J, Megens R, Bianchini M, Münch G, Ungerer M, Faussner A, et al. Differential inhibition of human atherosclerotic plaque‐induced platelet activation by dimeric GPVI‐Fc and anti‐GPVI antibodies: functional and imaging studies. J Am Coll Cardiol. 2015;65:2404–15.

     Not in our library10.1016/j.jacc.2015.03.573

111. 111.

     Busygina K, Jamasbi J, Seiler T, Deckmyn H, Weber C, Brandl R, et al. Oral Bruton tyrosine kinase inhibitors selectively block atherosclerotic plaque‐triggered thrombus formation in humans. Blood. 2018;131:2605–16.

     Not in our library10.1182/blood-2017-09-808808

112. 112.

     Badrnya S, Schrottmaier WC, Kral JB, Yaiw K‐C, Volf I, Schabbauer G, et al. Platelets mediate oxidized low‐density lipoprotein‐induced monocyte extravasation and foam cell formation. Arterioscler Thromb Vasc Biol. 2014;34:571–80.

     Not in our library10.1161/atvbaha.113.302919

113. 113.

     Wolf D, Hohmann J‐D, Wiedemann A, Bledzka K, Blankenbach H, Marchini T, et al. Binding of CD40L to Mac‐1's I‐domain involves the EQLKKSKTL motif and mediates leukocyte recruitment and atherosclerosis–but does not affect immunity and thrombosis in mice. Circ Res. 2011;109:1269–79.

     Not in our library10.1161/circresaha.111.247684

114. 114.

     Donners M, Beckers L, Lievens D, Munnix I, Heemskerk J, Janssen BJ, et al. The CD40‐TRAF6 axis is the key regulator of the CD40/CD40L system in neointima formation and arterial remodeling. Blood. 2008;111:4596–604.

     Not in our library10.1182/blood-2007-05-088906

115. 115.

     Lievens D, Zernecke A, Seijkens T, Soehnlein O, Beckers L, Munnix I, et al. Platelet CD40L mediates thrombotic and inflammatory processes in atherosclerosis. Blood. 2010;116:4317–27.

     Not in our library10.1182/blood-2010-01-261206

116. 116.

     Mach F, Schonbeck U, Sukhova GK, Atkinson E, Libby P. Reduction of atherosclerosis in mice by inhibition of CD40 signalling. Nature. 1998;394:200–3.

     Not in our library10.1038/28204

117. 117.

     Mause SF, von Hundelshausen P, Zernecke A, Koenen RR, Weber C. Platelet microparticles: a transcellular delivery system for RANTES promoting monocyte recruitment on endothelium. Arterioscler Thromb Vasc Biol. 2005;25:1512–8.

     Not in our library10.1161/01.atv.0000170133.43608.37

118. 118.

     Nassar T, Sachais BS, Akkawi Sa'ed, Kowalska MA, Bdeir K, Leitersdorf E, et al. Platelet factor 4 enhances the binding of oxidized low‐density lipoprotein to vascular wall cells. J Biol Chem. 2003;278:6187–93.

     Not in our library10.1074/jbc.m208894200

119. 119.

     Gleissner CA. Macrophage phenotype modulation by CXCL4 in atherosclerosis. Front Physiol. 2012;3:1.

     Not in our library10.3389/fphys.2012.00001

120. 120.

     Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA, Sarabi A, et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med. 2009;15:97–103.

     Not in our library10.1038/nm.1898

121. 121.

     Fan Y, Xiong X, Zhang Y, Yan D, Jian Z, Xu B, et al. A peptide inhibitor of CXCL4‐CCL5 heterodimer formation, protects against stroke in mice. J Am Heart Assoc. 2016;5(9): e003615

     Not in our library10.1161/jaha.116.003615

122. 122.

     Galt SW, Lindemann S, Medd D, Allen LL, Kraiss LW, Harris ES, et al. Differential regulation of matrix metalloproteinase‐9 by monocytes adherent to collagen and platelets. Circ Res. 2001;89:509–16.

     Not in our library10.1161/hh1801.096339

123. 123.

     Patrono C, Andreotti F, Arnesen H, Badimon L, Baigent C, Collet J‐P, et al. Antiplatelet agents for the treatment and prevention of atherothrombosis. Eur Heart J. 2011;32:2922–32.

     Not in our library10.1093/eurheartj/ehr373

124. 124.
     Immune Factors in Deep Vein Thrombosis Initiation · 2018

     No notice
125. 125.

     Ponomaryov T, Payne H, Fabritz L, Wagner DD, Brill A. Mast cells granular contents are crucial for deep vein thrombosis in mice. Circ Res. 2017;121:941–50.

     Not in our library10.1161/circresaha.117.311185

126. 126.

     Brill A, Fuchs TA, Chauhan AK, Yang JJ, De Meyer SF, Kollnberger M, et al. von Willebrand factor‐mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood. 2011;117:1400–7.

     Not in our library10.1182/blood-2010-05-287623

127. 127.

     Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De meyer SF, et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost. 2012;10:136–44.

     Not in our library10.1111/j.1538-7836.2011.04544.x

128. 128.

     Etulain J, Martinod K, Wong SL, Cifuni SM, Schattner M, Wagner DD. P‐selectin promotes neutrophil extracellular trap formation in mice. Blood. 2015;126:242–6.

     Not in our library10.1182/blood-2015-01-624023

129. 129.

     Stark K, Philippi V, Stockhausen S, Busse J, Antonelli A, Miller M, et al. Disulfide HMGB1 derived from platelets coordinates venous thrombosis in mice. Blood. 2016;128:2435–49.

     Not in our library10.1182/blood-2016-04-710632

130. 130.
     Deep vein thrombosis in mice is regulated by platelet HMGB1 through release of neutrophil-extracellular traps and DNA · 2018

     No notice
131. 131.

     Subramaniam S, Jurk K, Hobohm L, Jäckel S, Saffarzadeh M, Schwierczek K, et al. Distinct contributions of complement factors to platelet activation and fibrin formation in venous thrombus development. Blood. 2017;129:2291–302.

     Not in our library10.1182/blood-2016-11-749879

132. 132.

     Zhou J, Xu E, Shao K, Shen W, Gu YI, Li M, et al. Circulating platelet‐neutrophil aggregates as risk factor for deep venous thrombosis. Clin Chem Lab Med. 2019;57:707–15.

     Not in our library10.1515/cclm-2018-0909

133. 133.

     Shih L, Kaplan D, Kraiss LW, Casper TC, Pendleton RC, Peters CL, et al. Platelet‐monocyte aggregates and c‐reactive protein are associated with VTE in older surgical patients. Sci Rep. 2016;6:27478.

     Not in our library10.1038/srep27478

134. 134.

     Becattini C, Agnelli G, Schenone A, Eichinger S, Bucherini E, Silingardi M, et al. Aspirin for preventing the recurrence of venous thromboembolism. N Engl J Med. 2012;366:1959–67.

     Not in our library10.1056/nejmoa1114238

135. 135.

     Weitz JI, Lensing A, Prins MH, Bauersachs R, Beyer‐Westendorf J, Bounameaux H, et al. Rivaroxaban or aspirin for extended treatment of venous thromboembolism. N Engl J Med. 2017;376:1211–22.

     Not in our library10.1056/nejmoa1700518

136. 136.

     Castellucci LA, Cameron C, Le Gal G, Rodger MA, Coyle D, Wells PS, et al. Efficacy and safety outcomes of oral anticoagulants and antiplatelet drugs in the secondary prevention of venous thromboembolism: systematic review and network meta‐analysis. BMJ. 2013;347:f5133.

     Not in our library10.1136/bmj.f5133

137. 137.
     Platelets in Sepsis: An Update on Experimental Models and Clinical Data · 2019

     No notice
138. 138.

     de Stoppelaar SF, van 't Veer C, Claushuis T, Albersen B, Roelofs J, van der Poll T. Thrombocytopenia impairs host defense in gram‐negative pneumonia‐derived sepsis in mice. Blood. 2014;124:3781–90.

     Not in our library10.1182/blood-2014-05-573915

139. 139.

     Corken A, Russell S, Dent J, Post SR, Ware J. Platelet glycoprotein Ib‐IX as a regulator of systemic inflammation. Arterioscler Thromb Vasc Biol. 2014;34:996–1001.

     Not in our library10.1161/atvbaha.113.303113

140. 140.

     Goncalves R, Zhang X, Cohen H, Debrabant A, Mosser DM. Platelet activation attracts a subpopulation of effector monocytes to sites of Leishmania major infection. J Exp Med. 2011;208:1253–65.

     Not in our library10.1084/jem.20101751

141. 141.

     de Stoppelaar SF, Van't Veer C, Roelofs JJ, Claushuis TA, de Boer OJ, Tanck MW, et al. Platelet and endothelial cell P‐selectin are required for host defense against Klebsiella pneumoniae‐induced pneumosepsis. J Thromb Haemost. 2015;13:1128–38.

     Not in our library10.1111/jth.12893

142. 142.

     Beristain‐Covarrubias N, Perez‐Toledo M, Flores‐Langarica A, Zuidscherwoude M, Hitchcock JR, Channell WM, et al. Salmonella‐induced thrombi in mice develop asynchronously in the spleen and liver and are not effective bacterial traps. Blood. 2019;133:600–4.

     Not in our library10.1182/blood-2018-08-867267

143. 143.

     Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13:463–9.

     Not in our library10.1038/nm1565

144. 144.

     Tadie J‐M, Bae H‐B, Jiang S, Park DW, Bell CP, Yang H, et al. HMGB1 promotes neutrophil extracellular trap formation through interactions with toll‐like receptor 4. Am J Physiol Lung Cell Mol Physiol. 2013;304:L342–L349.

     Not in our library10.1152/ajplung.00151.2012

145. 145.
     Novel Anti-bacterial Activities of β-defensin 1 in Human Platelets: Suppression of Pathogen Growth and Signaling of Neutrophil Extracellular Trap Formation · 2011

     No notice
146. 146.

     Brown GT, McIntyre TM. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL‐1beta‐rich microparticles. J Immunol. 2011;186:5489–96.

     Not in our library10.4049/jimmunol.1001623

147. 147.

     McDonald B, Davis RP, Kim S‐J, Tse M, Esmon CT, Kolaczkowska E, et al. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood. 2017;129:1357–67.

     Not in our library10.1182/blood-2016-09-741298

148. 148.

     Mai S, Khan M, Dwivedi DJ, Ross CA, Zhou JI, Gould TJ, et al. Delayed but not early treatment with DNase reduces organ damage and improves outcome in a murine model of sepsis. Shock. 2015;44:166–72.

     Not in our library10.1097/shk.0000000000000396

149. 149.

     Wong CH, Jenne CN, Petri B, Chrobok NL, Kubes P. Nucleation of platelets with blood‐borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat Immunol. 2013;14:785–92.

     Not in our library10.1038/ni.2631

150. 150.

     Kerrigan AM, Navarro‐nuñez L, Pyz E, Finney BA, Willment JA, Watson SP, et al. Podoplanin‐expressing inflammatory macrophages activate murine platelets via CLEC‐2. J Thromb Haemost. 2012;10:484–6.

     Not in our library10.1111/j.1538-7836.2011.04614.x

151. 151.

     Gawaz M, Fateh‐Moghadam S, Pilz G, Gurland HJ, Werdan K. Platelet activation and interaction with leucocytes in patients with sepsis or multiple organ failure. Eur J Clin Invest. 1995;25:843–51.

     Not in our library10.1111/j.1365-2362.1995.tb01694.x

152. 152.

     Rondina MT, Carlisle M, Fraughton T, Brown SM, Miller RR, Harris ES, et al. Platelet‐monocyte aggregate formation and mortality risk in older patients with severe sepsis and septic shock. J Gerontol A Biol Sci Med Sci. 2015;70:225–31.

     Not in our library10.1093/gerona/glu082

153. 153.

     Gremmel T, Michelson AD, Frelinger AL III, Bhatt DL. Novel aspects of antiplatelet therapy in cardiovascular disease. Res Pract Thromb Haemost. 2018;2:439–49.

     Not in our library10.1002/rth2.12115

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