Caught at the Scene of the Crime: Platelets and Neutrophils Are Conspirators in Thrombosis
2021; Lippincott Williams & Wilkins; Volume: 42; Issue: 1 Linguagem: Inglês
10.1161/atvbaha.121.317187
ISSN1524-4636
AutoresMitchell J. Moon, James D. McFadyen, Karlheinz Peter,
Tópico(s)Neutrophil, Myeloperoxidase and Oxidative Mechanisms
ResumoHomeArteriosclerosis, Thrombosis, and Vascular BiologyVol. 42, No. 1Caught at the Scene of the Crime: Platelets and Neutrophils Are Conspirators in Thrombosis Free AccessResearch ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyRedditDiggEmail Jump toFree AccessResearch ArticlePDF/EPUBCaught at the Scene of the Crime: Platelets and Neutrophils Are Conspirators in Thrombosis Mitchell J. Moon, James D. McFadyen and Karlheinz Peter Mitchell J. MoonMitchell J. Moon https://orcid.org/0000-0001-9345-5001 Atherothrombosis and Vascular Biology, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia (M.J.M., J.D.M., K.P.). Baker Department of Cardiometabolic Health, University of Melbourne, Victoria, Australia (M.J.M., J.D.M., K.P.). , James D. McFadyenJames D. McFadyen Atherothrombosis and Vascular Biology, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia (M.J.M., J.D.M., K.P.). Baker Department of Cardiometabolic Health, University of Melbourne, Victoria, Australia (M.J.M., J.D.M., K.P.). Department of Clinical Hematology (J.D.M.), The Alfred Hospital, Melbourne, Victoria, Australia. Departments of Medicine (J.D.M., K.P.), Central Clinical School, Monash University, Melbourne, Victoria, Australia. and Karlheinz PeterKarlheinz Peter The opinions expressed in this article are not necessarily those of the editors or of the American Heart Association. Correspondence to: Karlheinz Peter, MD, PhD, Baker Heart and Diabetes Institute, 75 Commercial Rd, Melbourne, 3004 Victoria, Australia. Email E-mail Address: [email protected] https://orcid.org/0000-0002-8040-2258 Atherothrombosis and Vascular Biology, Baker Heart and Diabetes Institute, Melbourne, Victoria, Australia (M.J.M., J.D.M., K.P.). Baker Department of Cardiometabolic Health, University of Melbourne, Victoria, Australia (M.J.M., J.D.M., K.P.). Department of Cardiology (K.P.), The Alfred Hospital, Melbourne, Victoria, Australia. Departments of Medicine (J.D.M., K.P.), Central Clinical School, Monash University, Melbourne, Victoria, Australia. Immunology (K.P.), Central Clinical School, Monash University, Melbourne, Victoria, Australia. Originally published2 Dec 2021https://doi.org/10.1161/ATVBAHA.121.317187Arteriosclerosis, Thrombosis, and Vascular Biology. 2022;42:63–66is related toNeutrophil-Derived Protein S100A8/A9 Alters the Platelet Proteome in Acute Myocardial Infarction and Is Associated With Changes in Platelet ReactivityOther version(s) of this articleYou are viewing the most recent version of this article. Previous versions: December 2, 2021: Ahead of Print Cardiovascular diseases represent the complex intersection between multiple biological systems, including the hemostatic/thrombotic and the immune/inflammatory system. Indeed, recent studies of retrieved thrombi from patients with stroke have demonstrated abundant neutrophils at the scene of the crime and suggested a culprit role of neutrophils and their interaction with platelets in arterial thromboinflammation.1–4See accompanying article on page 49In this issue of ATVB, Joshi et al5 describe a new mechanism of interaction between neutrophils and platelets, namely the transfer of the alarmin S100A8/A9 during ST-segment–elevation myocardial infarction (STEMI) from neutrophils to platelets. S100A8 and S100A9 are typically released from cells as a heterodimer (also termed calprotectin) and plasma levels correlate with adverse outcomes following percutaneous coronary interventions,6 increased atherosclerotic plaque instability,7 and thromboxane synthesis in acute coronary syndromes.8 Using a proteomics-based approach, Joshi et al5 demonstrate upregulation of S100A8/A9 in platelets from patients at the time of STEMI, which was largely abrogated 3 days post-STEMI. To investigate the source of the increased S100A8/A9, platelet protein synthesis was assessed in LC-MS/MS (liquid chromatography with tandem mass spectrometry) using 13C6-labeled lysine/arginine. Contrary to other reports,9,10 the authors were not able to detect de novo protein synthesis in platelets, however, they do acknowledge that their approach is not as sensitive as the [35]methionine-incorporation method typically used. The authors concluded that S100A8/A9 in platelets is derived from other cell types. Given S100A8 and S100A9 are signature proteins of neutrophils and comprise ≈45% of the cytoplasmic proteins in neutrophils,11 coupled with the key observations that neutrophil counts correlate with increased plasma S100A8/A9 levels during STEMI, neutrophils obviously were the prime suspects to be investigated as the potential source.12 Using fluorescence confocal microscopy, S100A8 was only detected in activated platelets when coincubated with neutrophils. The uptake of S100A8/A9 by platelets has been described before, as Wang et al13 have shown that platelet uptake of S100A9 is CD36-dependent in mice and that blocking this uptake was thromboprotective in vivo. However, the precise role of S100A8/A9 in modulating human platelet function requires further investigation. In the current study, a weak negative correlation between S100A8/A9 plasma levels and platelet function was observed, and while S100A8/A9 has been shown to induce low levels of platelet activation in human platelets,14 the biological relevance and pathways by which alarmins modulate platelet function have yet to be elucidated. Further detailed platelet studies are therefore required to properly examine if S100A8/A9 is incriminated as a culprit in STEMI, or whether it is merely an innocent bystander and biomarker of inflammation and thrombosis.There is growing evidence that platelets physically interact with leukocytes. They have been shown to interact directly with T-cells, to activate different T-cell subtypes and to play a role in antigen presentation.15,16 Thrombotic and inflammatory diseases have typically been associated with platelet-monocyte aggregates.17,18 These aggregates can be used as a marker of platelet activation status as recently shown in patients with peripheral artery disease,19 thromboinflammation associated with COVID-19,20,21 and vaccine-induced thrombotic thrombocytopenia.22 In fact, antiplatelet drugs, such as P2Y12 inhibitors, may exert anti-inflammatory effects via the direct physical and signaling interaction between platelets and monocytes.23,24 One of the least studied interactions recognized as an important mediator of thrombosis and inflammation are platelet-neutrophil interactions. These aggregates were initially described in the setting of sepsis, where LPS (lipopolysaccharide) activation of the TLR4 (Toll-like receptor 4) on platelets can induce platelet binding to neutrophils and neutrophil extracellular trap (NET) formation.25 In fact, platelet-neutrophil aggregates have been described as a potential therapeutic target in sepsis.26 Interactions between platelets and neutrophils can eventuate on different levels and complexities. This can be in the form of physical interactions (Figure [A]) between platelet bound P-selectin (CD62P) and neutrophil PSGL-1 (P-selectin glycoprotein ligand-1) or between neutrophil αMβ2 (Mac-1, CD11b/CD18) binding directly to platelet GPIbα, or via fibrinogen to αIIbβ3 (GPIIb/IIIa, CD41/CD61). Neutrophils have also been shown to release extracellular vesicles containing arachidonic acid, which platelets use as a substrate for thromboxane A2 production, which is, in turn, released via platelet-derived extracellular vesicles and is important for full activation of neutrophils (Figure [B]).27 In keeping with the significance of platelet-leukocyte cross talk, while neutrophils release the alarmin S100A8/A9, activated platelets can release the alarmin HMGB1 (high-mobility group box protein 1), which directly activates neutrophils through the receptor for advanced glycation end products and induces the formation of NETs (NETosis) in acute MI28,29 and sepsis30 (Figure [C]). NETs as a sequela of platelet-neutrophil interactions are typically decorated with proinflammatory and prothrombotic molecules (eg, HMGB1, S100A8/A9, myeloperoxidase, histones, and negatively charged DNA; Figure [D]), promoting coagulation and platelet adhesion/aggregation,31 further potentiating thrombosis (containing platelets, neutrophils, red blood cells stabilized by NETs, and fibrin; Figure [E]).32 Recently, a major focus of platelet-neutrophil interactions has been in the setting of COVID-19, where platelet-neutrophil interactions are implicated as main drivers of thrombosis. SARS-CoV-2 infection activates the endothelium, resulting in platelet adhesion/activation and neutrophil adhesion, activation and NETosis.33 Furthermore NETs themselves, by providing a network for platelet adhesion and coagulation, are major facilitators of (micro)vascular thrombosis34 and exacerbate damage in the lungs, heart and kidneys of patients with COVID-19.35Download figureDownload PowerPointFigure. Platelet-neutrophil interactions via membrane receptors, interchange of soluble signals and neutrophil extracellular traps (NETs) are central mediators of thrombosis. A, Platelet-neutrophil aggregates form through physical interactions between P-selectin and PSGL-1 (P-selectin glycoprotein ligand-1), GPIbα and αMβ2, or αIIbβ3 and αMβ2 via fibrinogen. B, Activated neutrophils release extracellular vesicles (EVs) rich in arachidonic acid (AA) for platelets to use as a substrate. Platelets convert AA to thromboxane A2 (TxA2), which is, in turn, is released in platelet-derived EVs directed at neutrophils where TxA2 is required for full activation of neutrophils and increased neutrophil recruitment. C, Platelets release HMGB1 (high-mobility group box protein 1) which activates neutrophils via the receptor for advanced glycation end products (RAGE) and induces NET formation. Neutrophils release S100A8/A9 which is taken up by platelets, possibly through CD36, during ST-segment–elevation myocardial infarction (STEMI). D, Activated neutrophils undergo chromatin decondensation and release of NETs rich in alarmins, histones, and myeloperoxidase (MPO), which provide a surface for the assembly of coagulation factors and platelet attachment. E, These mechanisms of interaction between neutrophils and platelets result in formation of platelet and NET-rich thrombi.The proteomics approach used by Joshi et al5 has identified S100A8/A9 as a biomarker of neutrophil-platelet interactions during STEMI. This exemplifies the potential of omics in identifying biomarkers and novel therapeutic targets for thromboinflammatory disorders. Proteomics-based thrombosis research provides large, robust data sets, in the case of platelets consisting of up to 5200 proteins,36,37 which in combination with other omics can be used to identify pathways (eg, driven by microRNAs) upregulated in prothrombotic disease states38–40 and to gain detailed insights into cellular responses to antithrombotic drugs.41 This use of omics as a discovery tool holds great promise and will hopefully translate into the identification of novel disease biomarkers that will allow the provision of personalized therapy.42 With increased understanding into the importance of platelet-leukocyte interactions in cardiovascular disease, it is hoped that further studies coupling omics-based approaches with classical in vitro and in vivo research will shed further insight into the interaction between platelets and neutrophils to ultimately identify biomarkers and therapeutic targets for the treatment of thrombotic and inflammatory diseases.Article InformationSources of FundingThis work was supported by the National Health and Medical Research Council of Australia.Disclosures None.FootnotesFor Sources of Funding and Disclosures, see page 65.The opinions expressed in this article are not necessarily those of the editors or of the American Heart Association. Correspondence to: Karlheinz Peter, MD, PhD, Baker Heart and Diabetes Institute, 75 Commercial Rd, Melbourne, 3004 Victoria, Australia. Email karlheinz.[email protected]edu.auReferences1. Ducroux C, Di Meglio L, Loyau S, Delbosc S, Boisseau W, Deschildre C, Ben Maacha M, Blanc R, Redjem H, Ciccio G, et al.. Thrombus neutrophil extracellular traps content impair tPA-induced thrombolysis in acute ischemic stroke.Stroke. 2018; 49:754–757. doi: 10.1161/STROKEAHA.117.019896LinkGoogle Scholar2. Laridan E, Denorme F, Desender L, François O, Andersson T, Deckmyn H, Vanhoorelbeke K, De Meyer SF. Neutrophil extracellular traps in ischemic stroke thrombi.Ann Neurol. 2017; 82:223–232. doi: 10.1002/ana.24993CrossrefMedlineGoogle Scholar3. Blanch-Ruiz MA, Ortega-Luna R, Martínez-Cuesta MÁ, Álvarez Á. The neutrophil secretome as a crucial link between inflammation and thrombosis.Int J Mol Sci. 2021; 22:4170. doi: 10.3390/ijms22084170CrossrefMedlineGoogle Scholar4. Thålin C, Hisada Y, Lundström S, Mackman N, Wallén H. Neutrophil extracellular traps: villains and targets in arterial, venous, and cancer-associated thrombosis.Arterioscler Thromb Vasc Biol. 2019; 39:1724–1738. doi: 10.1161/ATVBAHA.119.312463LinkGoogle Scholar5. Joshi A, Schmidt LE, Burnap SA, Lu R, Chan MV, Armstrong PC, Baig F, Gutmann C, Willeit P, Santer P, et al.. Neutrophil-derived protein S100A8/A9 alters the platelet proteome in acute myocardial infarction and is associated with changes in platelet reactivity.Arterioscler Thromb Vasc Biol. 2022; 42:49–62. doi: 10.1161/ATVBAHA.121.317113LinkGoogle Scholar6. Song NP, Zhen XW, Li LD, Zhong L, Wang H, An Y. Plasma calprotectin was associated with platelet activation and no-reflow phenomenon in acute coronary syndrome.BMC Cardiovasc Disord. 2020; 20:443. doi: 10.1186/s12872-020-01717-5CrossrefMedlineGoogle Scholar7. Ionita MG, Vink A, Dijke IE, Laman JD, Peeters W, van der Kraak PH, Moll FL, de Vries JP, Pasterkamp G, de Kleijn DP. High levels of myeloid-related protein 14 in human atherosclerotic plaques correlate with the characteristics of rupture-prone lesions.Arterioscler Thromb Vasc Biol. 2009; 29:1220–1227. doi: 10.1161/ATVBAHA.109.190314LinkGoogle Scholar8. Santilli F, Paloscia L, Liani R, Di Nicola M, Di Marco M, Lattanzio S, La Barba S, Pascale S, Mascellanti M, Davì G. Circulating myeloid-related protein-8/14 is related to thromboxane-dependent platelet activation in patients with acute coronary syndrome, with and without ongoing low-dose aspirin treatment.J Am Heart Assoc. 2014; 3:e000903. doi: 10.1161/JAHA.114.000903LinkGoogle Scholar9. Kieffer N, Guichard J, Farcet JP, Vainchenker W, Breton-Gorius J. Biosynthesis of major platelet proteins in human blood platelets.Eur J Biochem. 1987; 164:189–195. doi: 10.1111/j.1432-1033.1987.tb11010.xCrossrefMedlineGoogle Scholar10. Nassa G, Giurato G, Cimmino G, Rizzo F, Ravo M, Salvati A, Nyman TA, Zhu Y, Vesterlund M, Lehtiö J, et al.. Splicing of platelet resident pre-mRNAs upon activation by physiological stimuli results in functionally relevant proteome modifications.Sci Rep. 2018; 8:498. doi: 10.1038/s41598-017-18985-5CrossrefMedlineGoogle Scholar11. Wang S, Song R, Wang Z, Jing Z, Wang S, Ma J. S100A8/A9 in Inflammation.Front Immunol. 2018; 9:1298. doi: 10.3389/fimmu.2018.01298CrossrefMedlineGoogle Scholar12. Tardif MR, Chapeton-Montes JA, Posvandzic A, Pagé N, Gilbert C, Tessier PA. Secretion of S100A8, S100A9, and S100A12 by neutrophils involves reactive oxygen species and potassium efflux.J Immunol Res. 2015; 2015:296149. doi: 10.1155/2015/296149CrossrefMedlineGoogle Scholar13. Wang Y, Fang C, Gao H, Bilodeau ML, Zhang Z, Croce K, Liu S, Morooka T, Sakuma M, Nakajima K, et al.. Platelet-derived S100 family member myeloid-related protein-14 regulates thrombosis.J Clin Invest. 2014; 124:2160–2171. doi: 10.1172/JCI70966CrossrefMedlineGoogle Scholar14. Zhan Y, Lu R, Meng H, Wang X, Hou J. Platelet activation and platelet-leukocyte interaction in generalized aggressive periodontitis.J Leukoc Biol. 2016; 100:1155–1166. doi: 10.1189/jlb.4A1115-526RRCrossrefMedlineGoogle Scholar15. Chapman LM, Aggrey AA, Field DJ, Srivastava K, Ture S, Yui K, Topham DJ, Baldwin WM, Morrell CN. Platelets present antigen in the context of MHC class I.J Immunol. 2012; 189:916–923. doi: 10.4049/jimmunol.1200580CrossrefMedlineGoogle Scholar16. Portier I, Campbell RA. Role of platelets in detection and regulation of infection.Arterioscler Thromb Vasc Biol. 2021; 41:70–78. doi: 10.1161/ATVBAHA.120.314645LinkGoogle Scholar17. Shih L, Kaplan D, Kraiss LW, Casper TC, Pendleton RC, Peters CL, Supiano MA, Zimmerman GA, Weyrich AS, Rondina MT. Platelet-monocyte aggregates and C-reactive protein are associated with VTE in older surgical patients.Sci Rep. 2016; 6:27478. doi: 10.1038/srep27478CrossrefMedlineGoogle Scholar18. Furman MI, Barnard MR, Krueger LA, Fox ML, Shilale EA, Lessard DM, Marchese P, Frelinger AL, Goldberg RJ, Michelson AD. Circulating monocyte-platelet aggregates are an early marker of acute myocardial infarction.J Am Coll Cardiol. 2001; 38:1002–1006. doi: 10.1016/s0735-1097(01)01485-1CrossrefMedlineGoogle Scholar19. Allen N, Barrett TJ, Guo Y, Nardi M, Ramkhelawon B, Rockman CB, Hochman JS, Berger JS. Circulating monocyte-platelet aggregates are a robust marker of platelet activity in cardiovascular disease.Atherosclerosis. 2019; 282:11–18. doi: 10.1016/j.atherosclerosis.2018.12.029CrossrefMedlineGoogle Scholar20. Taus F, Salvagno G, Canè S, Fava C, Mazzaferri F, Carrara E, Petrova V, Barouni RM, Dima F, Dalbeni A, et al.. Platelets promote thromboinflammation in SARS-CoV-2 pneumonia.Arterioscler Thromb Vasc Biol. 2020; 40:2975–2989. doi: 10.1161/ATVBAHA.120.315175LinkGoogle Scholar21. Hottz ED, Azevedo-Quintanilha IG, Palhinha L, Teixeira L, Barreto EA, Pão CRR, Righy C, Franco S, Souza TML, Kurtz P, et al.. Platelet activation and platelet-monocyte aggregate formation trigger tissue factor expression in patients with severe COVID-19.Blood. 2020; 136:1330–1341. doi: 10.1182/blood.2020007252CrossrefMedlineGoogle Scholar22. McFadyen JD, Sharma P, Moon MJ, Noonan J, Goodall E, Tran HA, Peter K. Activation of circulating platelets in vaccine-induced thrombotic thrombocytopenia and its reversal by intravenous immunoglobulin [published online August 16, 2021].Br J Haematol. doi: 10.1111/bjh.17750Google Scholar23. Siegel PM, Sander L, Fricke A, Stamm J, Wang X, Sharma P, Bassler N, Ying YL, Olivier CB, Eisenhardt SU, et al.. P2Y12 receptor blockers are anti-inflammatory drugs inhibiting both circulating monocytes and macrophages including THP-1 cells.Sci Rep. 2021; 11:17459. doi: 10.1038/s41598-021-95710-3CrossrefMedlineGoogle Scholar24. Thomas MR, Outteridge SN, Ajjan RA, Phoenix F, Sangha GK, Faulkner RE, Ecob R, Judge HM, Khan H, West LE, et al.. Platelet P2Y12 inhibitors reduce systemic inflammation and its prothrombotic effects in an experimental human model.Arterioscler Thromb Vasc Biol. 2015; 35:2562–2570. doi: 10.1161/ATVBAHA.115.306528LinkGoogle Scholar25. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, Patel KD, Chakrabarti S, McAvoy E, Sinclair GD, et al.. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood.Nat Med. 2007; 13:463–469. doi: 10.1038/nm1565CrossrefMedlineGoogle Scholar26. Granja T, Körner A, Glück C, Hohmann JD, Wang X, Köhler D, Streißenberger A, Nandurkar HH, Mirakaj V, Rosenberger P, et al.. Targeting CD39 toward activated platelets reduces systemic inflammation and improves survival in sepsis: a preclinical pilot study.Crit Care Med. 2019; 47:e420–e427. doi: 10.1097/CCM.0000000000003682CrossrefMedlineGoogle Scholar27. Rossaint J, Kühne K, Skupski J, Van Aken H, Looney MR, Hidalgo A, Zarbock A. Directed transport of neutrophil-derived extracellular vesicles enables platelet-mediated innate immune response.Nat Commun. 2016; 7:13464. doi: 10.1038/ncomms13464CrossrefMedlineGoogle Scholar28. Maugeri N, Campana L, Gavina M, Covino C, De Metrio M, Panciroli C, Maiuri L, Maseri A, D'Angelo A, Bianchi ME, et al.. Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps.J Thromb Haemost. 2014; 12:2074–2088. doi: 10.1111/jth.12710CrossrefMedlineGoogle Scholar29. Peter K, Bobik A. HMGB1 signals danger in acute coronary syndrome: emergence of a new risk marker for cardiovascular death?Atherosclerosis. 2012; 221:317–318. doi: 10.1016/j.atherosclerosis.2011.11.039CrossrefMedlineGoogle Scholar30. Zhou H, Deng M, Liu Y, Yang C, Hoffman R, Zhou J, Loughran PA, Scott MJ, Neal MD, Billiar TR. Platelet HMGB1 is required for efficient bacterial clearance in intra-abdominal bacterial sepsis in mice.Blood Adv. 2018; 2:638–648. doi: 10.1182/bloodadvances.2017011817CrossrefMedlineGoogle Scholar31. Döring Y, Soehnlein O, Weber C. Neutrophil extracellular traps in atherosclerosis and atherothrombosis.Circ Res. 2017; 120:736–743. doi: 10.1161/CIRCRESAHA.116.309692LinkGoogle Scholar32. Gould TJ, Vu TT, Swystun LL, Dwivedi DJ, Mai SH, Weitz JI, Liaw PC. Neutrophil extracellular traps promote thrombin generation through platelet-dependent and platelet-independent mechanisms.Arterioscler Thromb Vasc Biol. 2014; 34:1977–1984. doi: 10.1161/ATVBAHA.114.304114LinkGoogle Scholar33. Middleton EA, He XY, Denorme F, Campbell RA, Ng D, Salvatore SP, Mostyka M, Baxter-Stoltzfus A, Borczuk AC, Loda M, et al.. Neutrophil extracellular traps contribute to immunothrombosis in COVID-19 acute respiratory distress syndrome.Blood. 2020; 136:1169–1179. doi: 10.1182/blood.2020007008CrossrefMedlineGoogle Scholar34. McFadyen JD, Stevens H, Peter K. The emerging threat of (Micro)thrombosis in COVID-19 and its therapeutic implications.Circ Res. 2020; 127:571–587. doi: 10.1161/CIRCRESAHA.120.317447LinkGoogle Scholar35. Iliadi V, Konstantinidou I, Aftzoglou K, Iliadis S, Konstantinidis TG, Tsigalou C. The emerging role of neutrophils in the pathogenesis of thrombosis in COVID-19.Int J Mol Sci. 2021; 22:5368. doi: 10.3390/ijms22105368CrossrefMedlineGoogle Scholar36. Chiu SK, Orive SL, Moon MJ, Saw J, Ellis S, Kile BT, Huang Y, Chacon D, Pimanda JE, Beck D, et al.. Shared roles for Scl and Lyl1 in murine platelet production and function.Blood. 2019; 134:826–835. doi: 10.1182/blood.2019896175CrossrefMedlineGoogle Scholar37. Dargazanli C, Zub E, Deverdun J, Decourcelle M, de Bock F, Labreuche J, Lefèvre PH, Gascou G, Derraz I, Riquelme Bareiro C, et al.. Machine learning analysis of the cerebrovascular thrombi proteome in human ischemic stroke: an exploratory study.Front Neurol. 2020; 11:575376. doi: 10.3389/fneur.2020.575376CrossrefMedlineGoogle Scholar38. Manne BK, Denorme F, Middleton EA, Portier I, Rowley JW, Stubben C, Petrey AC, Tolley ND, Guo L, Cody M, et al.. Platelet gene expression and function in patients with COVID-19.Blood. 2020; 136:1317–1329. doi: 10.1182/blood.2020007214CrossrefMedlineGoogle Scholar39. Diehl P, Fricke A, Sander L, Stamm J, Bassler N, Htun N, Ziemann M, Helbing T, El-Osta A, Jowett JB, et al.. Microparticles: major transport vehicles for distinct microRNAs in circulation.Cardiovasc Res. 2012; 93:633–644. doi: 10.1093/cvr/cvs007CrossrefMedlineGoogle Scholar40. Garcia A, Dunoyer-Geindre S, Nolli S, Strassel C, Reny JL, Fontana P. miR-204-5p and platelet function regulation: insight into a mechanism mediated by CDC42 and GPIIbIIIa.Thromb Haemost. 2021; 121:1206–1219. doi: 10.1055/a-1497-9649CrossrefMedlineGoogle Scholar41. Marcone S, Dervin F, Fitzgerald DJ. Proteomic signatures of antiplatelet drugs: new approaches to exploring drug effects.J Thromb Haemost. 2015; 13(suppl 1):S323–S331. doi: 10.1111/jth.12943CrossrefMedlineGoogle Scholar42. Moon MJ, Peter K. MicroRNAs as biomarkers for personalized antiplatelet therapy.Thromb Haemost. 2021; 121:1121. doi: 10.1055/a-1559-0690CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsRelated articlesNeutrophil-Derived Protein S100A8/A9 Alters the Platelet Proteome in Acute Myocardial Infarction and Is Associated With Changes in Platelet ReactivityAbhishek Joshi, et al. Arteriosclerosis, Thrombosis, and Vascular Biology. 2022;42:49-62 January 2022Vol 42, Issue 1Article InformationMetrics © 2021 American Heart Association, Inc.https://doi.org/10.1161/ATVBAHA.121.317187PMID: 34852641 Originally publishedDecember 2, 2021 Keywordsblood plateletsEditorialsthrombosisproteomicsneutrophilscardiovascular diseasesPDF download Advertisement
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