The prowess of platelets in immunity and inflammation

Thrombosis and Haemostasis

Volumn 116, Issue 4, 2016, Pages 605-612

  Koenen, Rory R ^a,b  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Adhesion molecules; Chemokines; Inflammation; Platelet immunology

Indexed keywords

ANTITHROMBOCYTIC AGENT; INTERLEUKIN 1BETA; CYTOKINE; SIGNAL PEPTIDE;

ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL INJURY; BRAIN INJURY; CELL INTERACTION; DENGUE; HUMAN; HYPERLIPIDEMIA; IMMUNITY; INFLAMMATION; PLATELET REACTIVITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA SEQUENCE; RNA SPLICING; THROMBOCYTE; THROMBOCYTOPENIA; HEMOSTASIS; IMMUNOLOGY; PHYSIOLOGY;

BLOOD PLATELETS; CYTOKINES; HEMOSTASIS; HUMANS; IMMUNITY; INFLAMMATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS;

EID: 84989170157     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH16-04-0300     Document Type: Article

References (95)

1. Semple JW, et al. Platelets and the immune continuum. Nat Rev Immunol 2011; 11: 264–274.
2. Rondina MT, et al. Platelets as cellular effectors of inflammation in vascular diseases. Circ Res 2013; 112: 1506–1519.
3. Projahn D, Koenen RR. Platelets: key players in vascular inflammation. J Leuk Biol 2012; 92: 1167–1175.
4. Jenne CN, Kubes P. Platelets in inflammation and infection. Platelets 2015; 26: 286–292.
5. Duerschmied D, et al. Immune functions of platelets. Thromb Haemost 2014; 112: 678–691.
6. Thomas MR, Storey RF. The role of platelets in inflammation. Thromb Haemost 2015; 114: 449–458.
7. Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res 2007; 100: 1673–1685.
8. Vajen T, et al. Microvesicles from platelets: novel drivers of vascular inflammation. Thromb Haemost 2015; 114: 228–236.
9. Jurk K, Kehrel BE. Platelets: physiology and biochemistry. Semin Thromb Hemost 2005; 31: 381–392.
10. Heemskerk JWM, et al. Platelet-based coagulation: different populations, different functions. J Thromb Haemost 2013; 11: 2–16.
11. Bye AP, et al. Platelet signaling: a complex interplay between inhibitory and acti-vatory networks. J Thromb Haemost 2016; 14: 918–930.
12. Kehrel B, et al. Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet-activating quaternary structure of collagen, whereas CD36, glycoprotein IIb/IIIa, and von Willebrand factor do not. Blood 1998; 91: 491–499.
13. Golebiewska EM, Poole AW. Platelet secretion: From haemostasis to wound healing and beyond. Blood Rev 2015; 29: 153–162.
14. Deppermann C, et al. Gray platelet syndrome and defective thrombo-inflam-mation in Nbeal2-deficient mice. J Clin Invest 2013; 123: 3331–3342.
15. Konopatskaya O, et al. PKCalpha regulates platelet granule secretion and thrombus formation in mice. J Clin Invest 2009; 119: 399–407.
16. Junt T, Schulze H, Chen Z, et al. Dynamic visualisation of thrombopoiesis within bone marrow. Science 2007; 317: 1767–1770.
17. Machlus KR, Italiano JE. The incredible journey: From megakaryocyte development to platelet formation. J Cell Biol 2013; 201: 785–796.
18. Denis MM, et al. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 2005; 122: 379–391.
19. Schwertz H, et al. Anucleate platelets generate progeny. Blood 2010; 115: 3801–3809.
20. Mason KD, Carpinelli MR, Fletcher JI, et al. Programmed anuclear cell death delimits platelet life span. Cell 2007; 128: 1173–1186.
21. Ouseph MM, et al. Autophagy is induced upon platelet activation and is essential for hemostasis and thrombosis. Blood 2015; 126: 1224–1233.
22. Kieffer N, et al. Biosynthesis of major platelet proteins in human blood platelets. Eur J Biochem 1987; 164: 189–195.
23. Lindemann S, et al. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J Cell Biol 2001; 154: 485–490.
24. Brown GT, et al. Lipopolysaccharide stimulates platelets through an IL-1β auto-crine loop. J Immunol 2013; 191: 5196–5203.
25. Hottz ED, et al. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation. Blood 2013; 122: 3405–3414.
26. Brown GT, McIntyre TM. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles. J Immunol 2011; 186: 5489–5496.
27. Simon AY, et al. Dengue virus binding and replication by platelets. Blood 2015; 126: 378–385.
28. Schwertz H, et al. Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenecity of human platelets. J Exp Med 2006; 203: 2433–2440.
29. Brogren H, et al. Platelets synthesize large amounts of active plasminogen activator inhibitor 1. Blood 2004; 104: 3943–3948.
30. Nilsson RJA, et al. Blood platelets contain tumor-derived RNA biomarkers. Blood 2011; 118: 3680–3683.
31. Zomer A, et al. In vivo imaging reveals extracellular vesicle-mediated pheno-copying of metastatic behavior. Cell 2015; 161: 1046–1057.
32. Skog J, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10: 1470–1476.
33. Best MG, Sol N, Kooi I, et al. RNA-Seq of Tumor-Educated Platelets Enables Blood-Based Pan-Cancer, Multiclass, and Molecular Pathway Cancer Diagnostics. Cancer Cell 2015; 28: 666–676.
34. Schubert S, et al. A tour through the transcriptional landscape of platelets. Blood 2014; 124: 493–502.
35. Bray PF, et al. The complex transcriptional landscape of the anucleate human platelet. BMC Genomics 2013; 14: 1.
36. Eicher JD, et al. Characterisation of the platelet transcriptome by RNA sequencing in patients with acute myocardial infarction. Platelets 2016; 27: 230–239.
37. Stakos DA, et al. Platelet microRNAs: From platelet biology to possible disease biomarkers and therapeutic targets. Platelets 2012; 24: 579–589.
38. Nagalla S, et al. Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 2011; 117: 5189–5197.
39. Plé H, et al. The repertoire and features of human platelet microRNAs. PLoS one 2012; 7: e50746.
40. Landry P, et al. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol 2009; 16: 961–966.
41. Edelstein LC, et al. Racial differences in human platelet PAR4 reactivity reflect expression of PCTP and miR-376c. Nat Med 2013; 19: 1609–1616.
42. Rowley JW, et al. Dicer1 mediated miRNA processing shapes the mRNA profile and function of murine platelets. Blood 2016; 127: 1743–1751.
43. Boilard E, et al. Platelets amplify inflammation in arthritis via collagen-depend-ent microparticle production. Science 2010; 327: 580–583.
44. Langer HF, et al. Platelets contribute to the pathogenesis of experimental autoimmune encephalomyelitis. Circ Res 2012; 110: 1202–1210.
45. Hu H, Zhu L, Huang Z, et al. Platelets enhance lymphocyte adhesion and infiltration into arterial thrombus. Thromb Haemost 2010; 104: 1184–1192.
46. da Costa Martins PA, et al. Platelet binding to monocytes increases the adhesive properties of monocytes by up-regulating the expression and functionality of beta1 and beta2 integrins. J Leuk Biol 2006; 79: 499–507.
47. Santoso S, et al. The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J Exp Med 2002; 196: 679–691.
48. Wang Y, et al. Leukocyte engagement of platelet glycoprotein Ibalpha via the integrin Mac-1 is critical for the biological response to vascular injury. Circulation 2005; 112: 2993–3000.
49. Seizer P, et al. EMMPRIN (CD147) is a novel receptor for platelet GPVI and mediates platelet rolling via GPVI-EMMPRIN interaction. Thromb Haemost 2009; 101: 682–686.
50. Schulz C, et al. EMMPRIN (CD147/basigin) mediates platelet-monocyte interactions in vivo and augments monocyte recruitment to the vascular wall. J Thromb Haemost 2011; 9: 1007–1019.
51. Schmidt R, et al. Extracellular matrix metalloproteinase inducer (CD147) is a novel receptor on platelets, activates platelets, and augments nuclear factor kap-paB-dependent inflammation in monocytes. Circ Res 2008; 102: 302–309.
52. Seizer P, et al. Extracellular cyclophilin A activates platelets via EMMPRIN (CD147) and PI3K/Akt signaling, which promotes platelet adhesion and thrombus formation in vitro and in vivo. Arterioscler Thromb Vasc Biol 2015; 35: 655–663.
53. Postea O, et al. Contribution of platelet CX(3)CR1 to platelet-monocyte complex formation and vascular recruitment during hyperlipidemia. Arterioscler Thromb Vasc Biol 2012; 32: 1186–1193.
54. Langer HF, et al. Platelets recruit human dendritic cells via Mac-1/JAM-C interaction and modulate dendritic cell function in vitro. Arterioscler Thromb Vasc Biol 2007; 27: 1463–1470.
55. Schleicher RI, et al. Platelets induce apoptosis via membrane-bound FasL. Blood 2015; 126: 1483–1493.
56. Massberg S, et al. A critical role of platelet adhesion in the initiation of athero-sclerotic lesion formation. J Exp Med 2002; 196: 887–896.
57. Huo Y, et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 2003; 9: 61–67.
58. Frenette PS, et al. P-Selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet-endothelial interactions in vivo. J Exp Med 2000; 191: 1413–1422.
59. Theilmeier G, et al. Endothelial von Willebrand factor recruits platelets to atherosclerosis-prone sites in response to hypercholesterolemia. Blood 2002; 99: 4486–4493.
60. May AE, et al. Engagement of glycoprotein IIb/IIIa (alpha(IIb)beta3) on platelets upregulates CD40L and triggers CD40L-dependent matrix degradation by endothelial cells. Circulation 2002; 106: 2111–2117.
61. Lievens D, et al. Platelet CD40L mediates thrombotic and inflammatory processes in atherosclerosis. Blood 2010; 116: 4317–4327.
62. Gerdes N, et al. Platelet CD40 Exacerbates Atherosclerosis by Transcellular Activation of Endothelial Cells and Leukocytes. Arterioscler Thromb Vasc Biol 2016; 36: 482–490.
63. Weyrich AS, et al. Activated platelets signal chemokine synthesis by human monocytes. J Clin Invest 1996; 97: 1525–1534.
64. + T-cell differentiation via multiple chemokines in humans. Thromb Haemost 2011; 106: 353–362.
65. Tersteeg C, et al. FLow-induced PRotrusions (FLIPRs): a platelet-derived platform for the retrieval of microparticles by monocytes and neutrophils. Circ Res 2014; 114: 780–791.
66. Sadallah S, et al. Microparticles (ectosomes) shed by stored human platelets downregulate macrophages and modify the development of dendritic cells. J Immunol 2011; 186: 6543–6552.
67. Laffont B, et al. Platelet microparticles reprogram macrophage gene expression and function. Thromb Haemost 2016; 115: 311–323.
68. Vasina EM, et al. Microparticles from apoptotic platelets promote resident macrophage differentiation. Cell Death Dis 2011; 2: e211.
69. Clark SR, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13: 463–469.
70. Etulain J, et al. P-selectin promotes neutrophil extracellular trap formation in mice. Blood 2015; 126: 242–246.
71. Maugeri N, 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.
72. Rossaint J, et al. Synchronized integrin engagement and chemokine activation is crucial in neutrophil extracellular trap-mediated sterile inflammation. Blood 2014; 123: 2573–2584.
73. Koenen RR, et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009; 15: 97–103.
74. Hidalgo A, et al. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat Med 2009; 15: 384–391.
75. Sreeramkumar V, et al. Neutrophils scan for activated platelets to initiate inflammation. Science 2014; 346: 1234–1238.
76. Niemann S, et al. Soluble fibrin is the main mediator of Staphylococcus aureus adhesion to platelets. Circulation 2004; 110: 193–200.
77. Verschoor A, et al. A platelet-mediated system for shuttling blood-borne bacteria to CD8α+ dendritic cells depends on glycoprotein GPIb and complement C3. Nat Immunol 2011; 12: 1194–1201.
78. Wong CHY, et al. Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat Immunol 2013; 14: 785–792.
79. Sehgal S, Storrie B. Evidence that differential packaging of the major platelet granule proteins von Willebrand factor and fibrinogen can support their differential release. J Thromb Haemost 2007; 5: 2009–2016.
80. Chatterjee M, et al. Distinct platelet packaging, release, and surface expression of proangiogenic and antiangiogenic factors on different platelet stimuli. Blood 2011; 117: 3907–3911.
81. Kamykowski J, et al. Quantitative immunofluorescence mapping reveals little functional coclustering of proteins within platelet αα-granules. Blood 2011; 118: 1370–1373.
82. Jonnalagadda D, et al. Platelet secretion is kinetically heterogeneous in an agon-ist-responsive manner. Blood 2012; 120: 5209–5216.
83. Burkhart JM, et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 2012; 120: e73–82.
84. Hundelshausen von P, et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005; 105: 924–930.
85. Kramp BK, et al. Exchange of extracellular domains of CCR1 and CCR5 reveals confined functions in CCL5-mediated cell recruitment. Thromb Haemost 2013; 110: 795–806.
86. Grommes J, et al. Disruption of platelet-derived chemokine heteromers prevents neutrophil extravasation in acute lung injury. Am J Respir Crit Care Med 2012; 185: 628–636.
87. Alard J-E, et al. Recruitment of classical monocytes can be inhibited by disturbing heteromers of neutrophil HNP1 and platelet CCL5. Sci Transl Med 2015; 7: 317ra196–6.
88. Projahn D, et al. Controlled intramyocardial release of engineered chemokines by biodegradable hydrogels as a treatment approach of myocardial infarction. J Cell Mol Med 2014; 18: 790–800.
89. Horn M, et al. Human neutrophil alpha-defensins induce formation of fibrinogen and thrombospondin-1 amyloid-like structures and activate platelets via glycoprotein IIb/IIIa. J Thromb Haemost 2012; 10: 647–661.
90. Quinn KL, et al. Human neutrophil peptides mediate endothelial-monocyte interaction, foam cell formation, and platelet activation. Arterioscler Thromb Vasc Biol 2011; 31: 2070–2079.
91. Linden MD, et al. High platelet reactivity and antiplatelet therapy resistance. Semin Thromb Hemost 2012; 38: 200–212.
92. Naik MU, et al. JAM-A protects from thrombosis by suppressing integrin αIIbβ3-dependent outside-in signaling in platelets. Blood 2012; 119: 3352–3360.
93. Karshovska E, et al. Hyperreactivity of junctional adhesion molecule a-deficient platelets accelerates atherosclerosis in hyperlipidemic mice. Circ Res 2015; 116: 587–599.
94. Willecke F, et al. Interruption of classic CD40L-CD40 signalling but not of the novel CD40L-Mac-1 interaction limits arterial neointima formation in mice. Thromb Haemost 2014; 112: 379–389.
95. Weber C, Springer TA. Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to alphaIIbbeta3 and stimulated by platelet-activating factor. J Clin Invest 1997; 100: 2085–2093.