OxLDL sensitizes platelets for increased formation of extracellular vesicles capable of finetuning macrophage gene expression

Aatonen, 2012, Platelet-derived microvesicles: multitalented participants in intercellular communication, Semin Thromb. Hemost., 38, 102, 10.1055/s-0031-1300956 Aatonen, 2014, Isolation and characterization of platelet-derived extracellular vesicles, J. Extracell Vesicles, 3, 10.3402/jev.v3.24692 Ardlie, 1989, Platelet activation by oxidatively modified low density lipoproteins, Atherosclerosis, 76, 117, 10.1016/0021-9150(89)90094-4 Assarsson, 2014, Homogenous 96-plex PEA immunoassay exhibiting high sensitivity, specificity, and excellent scalability, PLoS One, 9, 10.1371/journal.pone.0095192 Bäck, 2019, Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities, Nat. Rev. Cardiol., 16, 389 Badimon, 2022, Extracellular vesicles in atherothrombosis: From biomarkers and precision medicine to therapeutic targets, Immunol. Rev., 312, 6, 10.1111/imr.13127 Badrnya, 2014, Platelets mediate oxidized low-density lipoprotein-induced monocyte extravasation and foam cell formation, Arterioscler. Thromb. Vasc. Biol., 34, 571, 10.1161/ATVBAHA.113.302919 Baj-Krzyworzeka, 2002, Platelet-derived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells, Exp. Hematol., 30, 450, 10.1016/S0301-472X(02)00791-9 Barrett, 2020, Macrophages in atherosclerosis regression, Arterioscler. Thromb. Vasc. Biol., 40, 20, 10.1161/ATVBAHA.119.312802 Barrett, 2019, Platelet regulation of myeloid suppressor of cytokine signaling 3 accelerates atherosclerosis, Sci. Transl. Med, 11, 10.1126/scitranslmed.aax0481 Berger, 2020, Atherogenic lipid stress induces platelet hyperactivity through CD36-mediated hyposensitivity to prostacyclin: the role of phosphodiesterase 3A, Haematologica, 105, 808, 10.3324/haematol.2018.213348 Biswas, 2017, TLR2 Plays a Key Role in Platelet Hyperreactivity and Accelerated Thrombosis Associated With Hyperlipidemia, Circ. Res, 121, 951, 10.1161/CIRCRESAHA.117.311069 Boilard, 2018, Extracellular vesicles and their content in bioactive lipid mediators: more than a sack of microRNA, J. Lipid Res, 59, 2037, 10.1194/jlr.R084640 Boilard, 2015, The diversity of platelet microparticles, Curr. Opin. Hematol., 22, 437, 10.1097/MOH.0000000000000166 Boren, 2020, Low-density lipoproteins cause atherosclerotic cardiovascular disease: pathophysiological, genetic, and therapeutic insights: a consensus statement from the European Atherosclerosis Society Consensus Panel, Eur. Heart J., 41, 2313, 10.1093/eurheartj/ehz962 Calvo, 1998, Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL, J. Lipid Res, 39, 777, 10.1016/S0022-2275(20)32566-9 Carvalho, 1974, Platelet function in hyperlipoproteinemia, N. Engl. J. Med, 290, 434, 10.1056/NEJM197402212900805 Colas, 2011, LDL from obese patients with the metabolic syndrome show increased lipid peroxidation and activate platelets, Diabetologia, 54, 2931, 10.1007/s00125-011-2272-8 Coly, 2022, Role of extracellular vesicles in atherosclerosis: An update, J. Leukoc. Biol., 111, 51, 10.1002/JLB.3MIR0221-099R Connelly, 1999, Comparison of class B scavenger receptors, CD36 and scavenger receptor BI (SR-BI), shows that both receptors mediate high density lipoprotein-cholesteryl ester selective uptake but SR-BI exhibits a unique enhancement of cholesteryl ester uptake, J. Biol. Chem., 274, 41, 10.1074/jbc.274.1.41 Davi, 1998, Increased levels of soluble P-selectin in hypercholesterolemic patients, Circulation, 97, 953, 10.1161/01.CIR.97.10.953 Davizon-Castillo, 2019, TNF-alpha-driven inflammation and mitochondrial dysfunction define the platelet hyperreactivity of aging, Blood, 134, 727, 10.1182/blood.2019000200 De Sousa, 2019, Functional aspects, phenotypic heterogeneity, and tissue immune response of macrophages in infectious diseases, Infect. Drug Resist, 12, 2589, 10.2147/IDR.S208576 Dean, 2009, Proteomic and functional characterisation of platelet microparticle size classes, Thromb. Haemost., 102, 711, 10.1160/TH09-04-243 Dickhout, 2018, Extracellular vesicles as biomarkers in cardiovascular disease; chances and risks, Front Cardiovasc Med, 5, 113, 10.3389/fcvm.2018.00113 Durinck, 2009, Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt, Nat. Protoc., 4, 1184, 10.1038/nprot.2009.97 Erbel, 2015, Prevalence of M4 macrophages within human coronary atherosclerotic plaques is associated with features of plaque instability, Int J. Cardiol., 186, 219, 10.1016/j.ijcard.2015.03.151 Faria, 2020, Platelets in aging and cancer-“double-edged sword”, Cancer Metastasis Rev., 39, 1205, 10.1007/s10555-020-09926-2 Ference, 2017, Low-density lipoproteins cause atherosclerotic cardiovascular disease. 1. Evidence from genetic, epidemiologic, and clinical studies. A consensus statement from the European Atherosclerosis Society Consensus Panel, Eur. Heart J., 38, 2459, 10.1093/eurheartj/ehx144 Ferreira, 2020, Mode of induction of platelet-derived extracellular vesicles is a critical determinant of their phenotype and function, Sci. Rep., 10, 18061, 10.1038/s41598-020-73005-3 Gasecka, 2019, Platelet extracellular vesicles, 401 Gleissner, 2010, CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages, J. Immunol., 184, 4810, 10.4049/jimmunol.0901368 Harmon, 1986, Thrombin binding and response in platelets from patients with dyslipoproteinemias: increased stimulus-response coupling in type II hyperlipoproteinemia, Blood, 68, 498, 10.1182/blood.V68.2.498.498 Havel, 1955, The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum, J. Clin. Invest, 34, 1345, 10.1172/JCI103182 Hessler, 1983, Lipoprotein oxidation and lipoprotein-induced cytotoxicity, Arteriosclerosis, 3, 215, 10.1161/01.ATV.3.3.215 Hulten, 2005, Human macrophages limit oxidation products in low density lipoprotein, Lipids Health Dis., 4, 6, 10.1186/1476-511X-4-6 Hyvärinen, 2018, Mesenchymal Stromal Cells and Their Extracellular Vesicles Enhance the Anti-Inflammatory Phenotype of Regulatory Macrophages by Downregulating the Production of Interleukin (IL)-23 and IL-22, Front Immunol., 9, 771, 10.3389/fimmu.2018.00771 Konkoth, 2021, Multifaceted role of extracellular vesicles in atherosclerosis, Atherosclerosis, 319, 121, 10.1016/j.atherosclerosis.2020.11.006 Korporaal, 2005, Effect of oxidation on the platelet-activating properties of low-density lipoprotein, Arterioscler. Thromb. Vasc. Biol., 25, 867, 10.1161/01.ATV.0000158381.02640.4b Korporaal, 2007, Platelet activation by oxidized low density lipoprotein is mediated by CD36 and scavenger receptor-A, Arterioscler. Thromb. Vasc. Biol., 27, 2476, 10.1161/ATVBAHA.107.150698 Kuiper, 2021, Reliable measurements of extracellular vesicles by clinical flow cytometry, Am. J. Reprod. Immunol., 85, 10.1111/aji.13350 Kumar, 2017, The impact of RNA sequence library construction protocols on transcriptomic profiling of leukemia, BMC Genom., 18, 629, 10.1186/s12864-017-4039-1 Kuriyama, 2010, Evaluation of factors associated with elevated levels of platelet-derived microparticles in the acute phase of cerebral infarction, Clin. Appl. Thromb. Hemost., 16, 26, 10.1177/1076029609338047 Lara-Guzman, 2018, Oxidized LDL triggers changes in oxidative stress and inflammatory biomarkers in human macrophages, Redox Biol., 15, 1, 10.1016/j.redox.2017.11.017 Larssen, 2017, Tracing Cellular Origin of Human Exosomes Using Multiplex Proximity Extension Assays, Mol. Cell Proteom., 16, 1547, 10.1074/mcp.A116.064725 Larsson, 2015, The effects of age and gender on plasma levels of 63 cytokines, J. Immunol. Methods, 425, 58, 10.1016/j.jim.2015.06.009 Lehti, 2018, Extracellular Lipids Accumulate in Human Carotid Arteries as Distinct Three-Dimensional Structures and Have Proinflammatory Properties, Am. J. Pathol., 188, 525, 10.1016/j.ajpath.2017.09.019 Levitan, 2010, Oxidized LDL: diversity, patterns of recognition, and pathophysiology, Antioxid. Redox Signal, 13, 39, 10.1089/ars.2009.2733 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Lukasik, 2013, Enhanced platelet-derived microparticle formation is associated with carotid atherosclerosis in convalescent stroke patients, Platelets, 24, 63, 10.3109/09537104.2011.654292 Ma, 2021, Platelet-derived extracellular vesicles to target plaque inflammation for effective anti-atherosclerotic therapy, J. Control Release, 329, 445, 10.1016/j.jconrel.2020.11.064 Magwenzi, 2015, Oxidized LDL activates blood platelets through CD36/NOX2-mediated inhibition of the cGMP/protein kinase G signaling cascade, Blood, 125, 2693, 10.1182/blood-2014-05-574491 Martinez, 2014, The M1 and M2 paradigm of macrophage activation: time for reassessment, F1000Prime Rep., 6, 13, 10.12703/P6-13 Massberg, 2002, A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation, J. Exp. Med, 196, 887, 10.1084/jem.20012044 Milioli, 2015, Quantitative proteomics analysis of platelet-derived microparticles reveals distinct protein signatures when stimulated by different physiological agonists, J. Proteom., 121, 56, 10.1016/j.jprot.2015.03.013 Nergiz-Unal, 2011, Signaling role of CD36 in platelet activation and thrombus formation on immobilized thrombospondin or oxidized low-density lipoprotein, J. Thromb. Haemost., 9, 1835, 10.1111/j.1538-7836.2011.04416.x Nguyen, 2020, Functional assays to assess the therapeutic potential of extracellular vesicles, J. Extracell Vesicles, 10, 10.1002/jev2.12033 Nielsen, 2015, In vitro Incubation of Platelets with oxLDL Does Not Induce Microvesicle Release When Measured by Sensitive Flow Cytometry, Front Cardiovasc Med, 2, 37, 10.3389/fcvm.2015.00037 Oggero, 2021, Extracellular vesicles from monocyte/platelet aggregates modulate human atherosclerotic plaque reactivity, J. Extracell Vesicles, 10, 12084, 10.1002/jev2.12084 Palviainen, 2020, Extracellular vesicles from human plasma and serum are carriers of extravesicular cargo-Implications for biomarker discovery, PLoS One, 15, 10.1371/journal.pone.0236439 Panigrahi, 2013, Engagement of platelet toll-like receptor 9 by novel endogenous ligands promotes platelet hyperreactivity and thrombosis, Circ. Res, 112, 103, 10.1161/CIRCRESAHA.112.274241 Pienimaeki-Roemer, 2014, High-density lipoprotein 3 and apolipoprotein A-I alleviate platelet storage lesion and release of platelet extracellular vesicles, Transfusion, 54, 2301, 10.1111/trf.12640 Podrez, 2007, Platelet CD36 links hyperlipidemia, oxidant stress and a prothrombotic phenotype, Nat. Med, 13, 1086, 10.1038/nm1626 Puhka, 2017, KeepEX, a simple dilution protocol for improving extracellular vesicle yields from urine, Eur. J. Pharm. Sci., 98, 30, 10.1016/j.ejps.2016.10.021 Puhm, 2021, Platelet extracellular vesicles: beyond the blood, Arterioscler. Thromb. Vasc. Biol., 41, 87 Radding, 1960, Studies on the synthesis and secretion of serum lipoproteins by rat liver slices, J. Clin. Invest, 39, 1560, 10.1172/JCI104177 Robert, 2009, Standardization of platelet-derived microparticle counting using calibrated beads and a Cytomics FC500 routine flow cytometer: a first step towards multicenter studies?, J. Thromb. Haemost., 7, 190, 10.1111/j.1538-7836.2008.03200.x Rubic, 2006, Downregulated CD36 and oxLDL uptake and stimulated ABCA1/G1 and cholesterol efflux as anti-atherosclerotic mechanisms of interleukin-10, Cardiovasc Res, 69, 527, 10.1016/j.cardiores.2005.10.018 Saboor, 2013, Platelet receptors; an instrumental of platelet physiology, Pak. J. Med Sci., 29, 891, 10.12669/pjms.293.3497 Sachais, 2007, Elimination of platelet factor 4 (PF4) from platelets reduces atherosclerosis in C57Bl/6 and apoE-/- mice, Thromb. Haemost., 98, 1108, 10.1160/TH07-04-0271 Sadallah, 2011, Microparticles (ectosomes) shed by stored human platelets downregulate macrophages and modify the development of dendritic cells, J. Immunol., 186, 6543, 10.4049/jimmunol.1002788 Sadallah, 2014, Ectosomes released by platelets induce differentiation of CD4+T cells into T regulatory cells, Thromb. Haemost., 112, 1219, 10.1160/th14-03-0281 Scheuerer, 2000, The CXC-chemokine platelet factor 4 promotes monocyte survival and induces monocyte differentiation into macrophages, Blood, 95, 1158, 10.1182/blood.V95.4.1158.004k31_1158_1166 Shastri, 1980, Platelet function and platelet lipid composition in the dyslipoproteinemias, J. Lipid Res, 21, 467, 10.1016/S0022-2275(20)39797-2 Siljander, 1999, Studies of adhesion-dependent platelet activation: distinct roles for different participating receptors can be dissociated by proteolysis of collagen, Arterioscler. Thromb. Vasc. Biol., 19, 3033, 10.1161/01.ATV.19.12.3033 Soldano, 2018, Increase in circulating cells coexpressing M1 and M2 macrophage surface markers in patients with systemic sclerosis, Ann. Rheum. Dis., 77, 1842, 10.1136/annrheumdis-2018-213648 Steinberg, 2010, Oxidized low-density lipoprotein and atherosclerosis, Arterioscler. Thromb. Vasc. Biol., 30, 2311, 10.1161/ATVBAHA.108.179697 Suades, 2015, High levels of TSP1+/CD142+ platelet-derived microparticles characterise young patients with high cardiovascular risk and subclinical atherosclerosis, Thromb. Haemost., 114, 1310, 10.1160/TH15-04-0325 Suades, 2019, Liquid Biopsy of Extracellular Microvesicles Predicts Future Major Ischemic Events in Genetically Characterized Familial Hypercholesterolemia Patients, Arterioscler. Thromb. Vasc. Biol., 39, 1172, 10.1161/ATVBAHA.119.312420 Suades, 2022, Platelet-released extracellular vesicles: the effects of thrombin activation, Cell Mol. Life Sci., 79, 190, 10.1007/s00018-022-04222-4 Takahashi, 1996, Native lipoproteins inhibit platelet activation induced by oxidized lipoproteins, Biochem Biophys. Res Commun., 222, 453, 10.1006/bbrc.1996.0765 Tan, 2005, Clinically apparent atherosclerotic disease in diabetes is associated with an increase in platelet microparticle levels, Diabet. Med, 22, 1657, 10.1111/j.1464-5491.2005.01707.x Tarazona, 2015, Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package, Nucleic Acids Res, 43 Taus, 2019, Platelet-Derived Extracellular Vesicles as Target of Antiplatelet Agents. What Is the Evidence?, Front Pharm., 10, 1256, 10.3389/fphar.2019.01256 Thery, 2018, Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines, J. Extracell Vesicles, 7, 1535750, 10.1080/20013078.2018.1535750 Trombetta, 2018, A circulating cell population showing both M1 and M2 monocyte/macrophage surface markers characterizes systemic sclerosis patients with lung involvement, Respir. Res, 19, 186, 10.1186/s12931-018-0891-z Trpkovic, 2015, Oxidized low-density lipoprotein as a biomarker of cardiovascular diseases, Crit. Rev. Clin. Lab Sci., 52, 70, 10.3109/10408363.2014.992063 Valkonen, 2019, Lipid mediators in platelet concentrate and extracellular vesicles: Molecular mechanisms from membrane glycerophospholipids to bioactive molecules, Biochim Biophys. Acta Mol. Cell Biol. Lipids, 1864, 1168, 10.1016/j.bbalip.2019.03.011 Van Der Meijden, 2019, Platelet biology and functions: new concepts and clinical perspectives, Nat. Rev. Cardiol., 16, 166, 10.1038/s41569-018-0110-0 Van Der Pol, 2018, Standardization of extracellular vesicle measurements by flow cytometry through vesicle diameter approximation, J. Thromb. Haemost., 16, 1236, 10.1111/jth.14009 Van Der Pol, 2022, Minimum information to report about a flow cytometry experiment on extracellular vesicles: Communication from the ISTH SSC subcommittee on vascular biology, J. Thromb. Haemost., 20, 245, 10.1111/jth.15540 Wang, 2012, Oxidized low-density lipoprotein-dependent platelet-derived microvesicles trigger procoagulant effects and amplify oxidative stress, Mol. Med, 18, 159, 10.2119/molmed.2011.00295 Welsh, 2020, MIFlowCyt-EV: a framework for standardized reporting of extracellular vesicle flow cytometry experiments, J. Extracell Vesicles, 9, 1713526, 10.1080/20013078.2020.1713526 Weidtmann, 1995, Mildly oxidized LDL induces platelet aggregation through activation of phospholipase A2, Arterioscler Thromb Vasc Biol, 15, 1131, 10.1161/01.ATV.15.8.1131 Welsh, 2023, A compendium of single extracellular vesicle flow cytometry, J. Extracell Vesicles, 12, 10.1002/jev2.12299 Yang, 2017, Platelet CD36 promotes thrombosis by activating redox sensor ERK5 in hyperlipidemic conditions, Blood, 129, 2917, 10.1182/blood-2016-11-750133 Yang, 2018, Platelet CD36 signaling through ERK5 promotes caspase-dependent procoagulant activity and fibrin deposition in vivo, Blood Adv., 2, 2848, 10.1182/bloodadvances.2018025411 Yla-Herttuala, 1989, Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man, J. Clin. Invest, 84, 1086, 10.1172/JCI114271 Yla-Herttuala, 1990, Lipoproteins in normal and atherosclerotic aorta, Eur. Heart J., 11, 88, 10.1093/eurheartj/11.suppl_E.88 Yu, 2012, clusterProfiler: an R package for comparing biological themes among gene clusters, OMICS, 16, 284, 10.1089/omi.2011.0118 Zaldivia, 2017, Platelet-derived microvesicles in cardiovascular diseases, Front Cardiovasc Med, 4, 74, 10.3389/fcvm.2017.00074 Zhang, 2014, Platelet-derived microparticle count and surface molecule expression differ between subjects with and without type 2 diabetes, independently of obesity status, J. Thromb. Thrombolysis, 37, 455, 10.1007/s11239-013-1000-2