1932

Abstract

Platelets have dual physiologic roles as both cellular mediators of thrombosis and immune modulatory cells. Historically, the thrombotic function of platelets has received significant research and clinical attention, but emerging research indicates that the immune regulatory roles of platelets may be just as important. We now know that in addition to their role in the acute thrombotic event at the time of myocardial infarction, platelets initiate and accelerate inflammatory processes that are part of the pathogenesis of atherosclerosis and myocardial infarction expansion. Furthermore, it is increasingly apparent from recent studies that platelets impact the pathogenesis of many vascular inflammatory processes such as autoimmune diseases, sepsis, viral infections, and growth and metastasis of many types of tumors. Therefore, we must consider platelets as immune cells that affect all phases of immune responses.

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2019-04-26
2024-04-25
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Literature Cited

  1. 1.
    Karshovska E, Zhao Z, Blanchet X, Schmitt MM, Bidzhekov K et al. 2015. Hyperreactivity of junctional adhesion molecule A-deficient platelets accelerates atherosclerosis in hyperlipidemic mice. Circ. Res. 116:587–99
    [Google Scholar]
  2. 2.
    Cameron SJ, Ture SK, Mickelsen D, Chakrabarti E, Modjeski KL et al. 2015. Platelet extracellular regulated protein kinase 5 is a redox switch and triggers maladaptive platelet responses and myocardial infarct expansion. Circulation 132:47–58
    [Google Scholar]
  3. 3.
    Schmidt RA, Morrell CN, Ling FS, Simlote P, Fernandez G et al. 2018. The platelet phenotype in patients with ST-segment elevation myocardial infarction is different from non-ST-segment elevation myocardial infarction. Transl. Res. 195:1–12
    [Google Scholar]
  4. 4.
    Rong MY, Wang CH, Wu ZB, Zeng W, Zheng ZH et al. 2014. Platelets induce a proinflammatory phenotype in monocytes via the CD147 pathway in rheumatoid arthritis. Arthritis Res. Ther. 16:478
    [Google Scholar]
  5. 5.
    Zamora C, Canto E, Nieto JC, Bardina J, Diaz-Torne C et al. 2017. Binding of platelets to lymphocytes: a potential anti-inflammatory therapy in rheumatoid arthritis. J. Immunol. 198:3099–108
    [Google Scholar]
  6. 6.
    Habets KL, Trouw LA, Levarht EW, Korporaal SJ, Habets PA et al. 2015. Anti-citrullinated protein antibodies contribute to platelet activation in rheumatoid arthritis. Arthritis Res. Ther. 17:209
    [Google Scholar]
  7. 7.
    Sacharidou A, Chambliss KL, Ulrich V, Salmon JE, Shen YM et al. 2018. Antiphospholipid antibodies induce thrombosis by PP2A activation via apoER2-Dab2-SHC1 complex formation in endothelium. Blood 131:2097–110
    [Google Scholar]
  8. 8.
    Haemmerle M, Taylor ML, Gutschner T, Pradeep S, Cho MS et al. 2017. Platelets reduce anoikis and promote metastasis by activating YAP1 signaling. Nat. Commun. 8:310
    [Google Scholar]
  9. 9.
    Michael JV, Wurtzel JGT, Mao GF, Rao AK, Kolpakov MA et al. 2017. Platelet microparticles infiltrating solid tumors transfer miRNAs that suppress tumor growth. Blood 130:567–80
    [Google Scholar]
  10. 10.
    Jiang L, Luan Y, Miao X, Sun C, Li K et al. 2017. Platelet releasate promotes breast cancer growth and angiogenesis via VEGF-integrin cooperative signalling. Br. J. Cancer 117:695–703
    [Google Scholar]
  11. 11.
    Rachidi S, Metelli A, Riesenberg B, Wu BX, Nelson MH et al. 2017. Platelets subvert T cell immunity against cancer via GARP-TGFβ axis. Sci. Immunol. 2:eaai7911
  12. 12.
    Zara M, Canobbio I, Visconte C, Canino J, Torti M, Guidetti GF 2018. Molecular mechanisms of platelet activation and aggregation induced by breast cancer cells. Cell Signal 48:45–53
    [Google Scholar]
  13. 13.
    Claushuis TA, van Vught LA, Scicluna BP, Wiewel MA, Klein Klouwenberg PM et al. 2016. Thrombocytopenia is associated with a dysregulated host response in critically ill sepsis patients. Blood 127:3062–72
    [Google Scholar]
  14. 14.
    Rayes J, Lax S, Wichaiyo S, Watson SK, Di Y et al. 2017. The podoplanin-CLEC-2 axis inhibits inflammation in sepsis. Nat. Commun. 8:2239
    [Google Scholar]
  15. 15.
    McDonald B, Davis RP, Kim SJ, Tse M, Esmon CT et al. 2017. Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood 129:1357–67
    [Google Scholar]
  16. 16.
    Hottz ED, Oliveira MF, Nunes PC, Nogueira RM, Valls-de-Souza R et al. 2013. Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases. J. Thromb. Haemost. 11:951–62
    [Google Scholar]
  17. 17.
    Sridharan A, Chen Q, Tang KF, Ooi EE, Hibberd ML, Chen J 2013. Inhibition of megakaryocyte development in the bone marrow underlies dengue virus-induced thrombocytopenia in humanized mice. J. Virol. 87:11648–58
    [Google Scholar]
  18. 18.
    Hottz ED, Lopes JF, Freitas C, Valls-de-Souza R, Oliveira MF et al. 2013. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation. Blood 122:3405–14
    [Google Scholar]
  19. 19.
    Trugilho MRO, Hottz ED, Brunoro GVF, Teixeira-Ferreira A, Carvalho PC et al. 2017. Platelet proteome reveals novel pathways of platelet activation and platelet-mediated immunoregulation in dengue. PLOS Pathog 13:e1006385
    [Google Scholar]
  20. 20.
    Hottz ED, Medeiros-de-Moraes IM, Vieira-de-Abreu A, de Assis EF, Vals-de-Souza R et al. 2014. Platelet activation and apoptosis modulate monocyte inflammatory responses in dengue. J. Immunol. 193:1864–72
    [Google Scholar]
  21. 21.
    Sugiyama MG, Gamage A, Zyla R, Armstrong SM, Advani S et al. 2016. Influenza virus infection induces platelet-endothelial adhesion which contributes to lung injury. J. Virol. 90:1812–23
    [Google Scholar]
  22. 22.
    Boilard E, Pare G, Rousseau M, Cloutier N, Dubuc I et al. 2014. Influenza virus H1N1 activates platelets through FcγRIIA signaling and thrombin generation. Blood 123:2854–63
    [Google Scholar]
  23. 23.
    Guo L, Feng K, Wang YC, Mei JJ, Ning RT et al. 2017. Critical role of CXCL4 in the lung pathogenesis of influenza (H1N1) respiratory infection. Mucosal Immunol 10:1529–41
    [Google Scholar]
  24. 24.
    Junt T, Schulze H, Chen Z, Massberg S, Goerge T et al. 2007. Dynamic visualization of thrombopoiesis within bone marrow. Science 317:1767–70
    [Google Scholar]
  25. 25.
    Nishimura S, Nagasaki M, Kunishima S, Sawaguchi A, Sakata A et al. 2015. IL-1α induces thrombopoiesis through megakaryocyte rupture in response to acute platelet needs. J. Cell Biol. 209:453–66
    [Google Scholar]
  26. 26.
    Cerutti A, Custodi P, Mduranti, Cazzola M, Balduini CL 1999. Circulating thrombopoietin in reactive conditions behaves like an acute phase reactant. Clin. Lab. Haematol. 21:271–75
    [Google Scholar]
  27. 27.
    Lefrançais E, Ortiz-Muñoz G, Caudrillier A, Mallavia B, Liu F et al. 2017. The lung is a site of platelet biogenesis and a reservoir for haematopoietic progenitors. Nature 544:105–9
    [Google Scholar]
  28. 28.
    Rowley JW, Oler AJ, Tolley ND, Hunter BN, Low EN et al. 2011. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood 118:e101–11. Erratum. 2014. Blood 123:3843
    [Google Scholar]
  29. 29.
    Clancy L, Beaulieu LM, Tanriverdi K, Freedman JE 2017. The role of RNA uptake in platelet heterogeneity. Thromb. Haemost. 117:948–61
    [Google Scholar]
  30. 30.
    Zufferey A, Schvartz D, Nolli S, Reny JL, Sanchez JC, Fontana P 2014. Characterization of the platelet granule proteome: evidence of the presence of MHC1 in alpha-granules. J. Proteom. 101:130–40
    [Google Scholar]
  31. 31.
    McManus DD, Beaulieu LM, Mick E, Tanriverdi K, Larson MG et al. 2013. Relationship among circulating inflammatory proteins, platelet gene expression, and cardiovascular risk. Arterioscler. Thromb. Vasc. Biol. 33:2666–73
    [Google Scholar]
  32. 32.
    Walther DJ, Peter JU, Winter S, Holtje M, Paulmann N et al. 2003. Serotonylation of small GTPases is a signal transduction pathway that triggers platelet alpha-granule release. Cell 115:851–62
    [Google Scholar]
  33. 33.
    Huang Y, Joshi S, Xiang B, Kanaho Y, Li Z et al. 2016. Arf6 controls platelet spreading and clot retraction via integrin αIIbβ3 trafficking. Blood 127:1459–67
    [Google Scholar]
  34. 34.
    Handagama PJ, Amrani DL, Shuman MA 1995. Endocytosis of fibrinogen into hamster megakaryocyte α granules is dependent on a dimeric γA configuration. Blood 85:1790–95
    [Google Scholar]
  35. 35.
    Kahr WH, Hinckley J, Li L, Schwertz H, Christensen H et al. 2011. Mutations in NBEAL2, encoding a BEACH protein, cause gray platelet syndrome. Nat. Genet. 43:738–40
    [Google Scholar]
  36. 36.
    Deppermann C, Cherpokova D, Nurden P, Schulz JN, Thielmann I et al. 2013. Gray platelet syndrome and defective thrombo-inflammation in Nbeal2-deficient mice. J. Clin. Investig. 123:3331–42
    [Google Scholar]
  37. 37.
    Sherman A, Genuth L, Hazzi CG, Balthazar EJ, Schinella RA 1989. Perirectal abscess in the Hermansky-Pudlak syndrome. Am. J. Gastroenterol. 84:552–56
    [Google Scholar]
  38. 38.
    Weyrich AS, Denis MM, Schwertz H, Tolley ND, Foulks J et al. 2007. mTOR-dependent synthesis of Bcl-3 controls the retraction of fibrin clots by activated human platelets. Blood 109:1975–83
    [Google Scholar]
  39. 39.
    Cameron SJ, Mix DS, Ture SK, Schmidt RA, Mohan A et al. 2018. Hypoxia and ischemia promote a maladaptive platelet phenotype. Arterioscler. Thromb. Vasc. Biol. 38:1594–1606
    [Google Scholar]
  40. 40.
    Alhasan AA, Izuogu OG, Al-Balool HH, Steyn JS, Evans A et al. 2016. Circular RNA enrichment in platelets is a signature of transcriptome degradation. Blood 127:e1–11
    [Google Scholar]
  41. 41.
    Mills EW, Green R, Ingolia NT 2017. Slowed decay of mRNAs enhances platelet specific translation. Blood 129:e38–48
    [Google Scholar]
  42. 42.
    Mills EW, Wangen J, Green R, Ingolia NT 2016. Dynamic regulation of a ribosome rescue pathway in erythroid cells and platelets. Cell Rep 17:1–10
    [Google Scholar]
  43. 43.
    Shashkin PN, Brown GT, Ghosh A, Marathe GK, McIntyre TM 2008. Lipopolysaccharide is a direct agonist for platelet RNA splicing. J. Immunol. 181:3495–502
    [Google Scholar]
  44. 44.
    Denis MM, Tolley ND, Bunting M, Schwertz H, Jiang H et al. 2005. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 122:379–91
    [Google Scholar]
  45. 45.
    Aggrey AA, Srivastava K, Ture S, Field DJ, Morrell CN 2013. Platelet induction of the acute-phase response is protective in murine experimental cerebral malaria. J. Immunol. 190:4685–91
    [Google Scholar]
  46. 46.
    Cooney KA, Nichols WC, Bruck ME, Bahou WF, Shapiro AD et al. 1991. The molecular defect in type IIB von Willebrand disease: identification of four potential missense mutations within the putative GpIb binding domain. J. Clin. Investig. 87:1227–33
    [Google Scholar]
  47. 47.
    Kroll MH, Harris TS, Moake JL, Handin RI, Schafer AI 1991. von Willebrand factor binding to platelet GpIb initiates signals for platelet activation. J. Clin. Investig. 88:1568–73
    [Google Scholar]
  48. 48.
    Weyrich AS, McIntyre TM, McEver RP, Prescott SM, Zimmerman GA 1995. Monocyte tethering by P-selectin regulates monocyte chemotactic protein-1 and tumor necrosis factor-α secretion: signal integration and NF-κB translocation. J. Clin. Investig. 95:2297–303
    [Google Scholar]
  49. 49.
    Bennewitz MF, Jimenez MA, Vats R, Tutuncuoglu E, Jonassaint J et al. 2017. Lung vaso-occlusion in sickle cell disease mediated by arteriolar neutrophil-platelet microemboli. JCI Insight 2:e89761
    [Google Scholar]
  50. 50.
    Ott I, Neumann FJ, Gawaz M, Schmitt M, Schomig A 1996. Increased neutrophil-platelet adhesion in patients with unstable angina. Circulation 94:1239–46
    [Google Scholar]
  51. 51.
    Hidalgo A, Chang J, Jang JE, Peired AJ, Chiang EY, Frenette PS 2009. Heterotypic interactions enabled by polarized neutrophil microdomains mediate thromboinflammatory injury. Nat. Med. 15:384–91
    [Google Scholar]
  52. 52.
    Sreeramkumar V, Adrover JM, Ballesteros I, Cuartero MI, Rossaint J et al. 2014. Neutrophils scan for activated platelets to initiate inflammation. Science 346:1234–38
    [Google Scholar]
  53. 53.
    Ruggeri ZM, De Marco L, Gatti L, Bader R, Montgomery RR 1983. Platelets have more than one binding site for von Willebrand factor. J. Clin. Investig. 72:1–12
    [Google Scholar]
  54. 54.
    Wang Y, Sakuma M, Chen Z, Ustinov V, Shi C et al. 2005. Leukocyte engagement of platelet glycoprotein Ibα via the integrin Mac-1 is critical for the biological response to vascular injury. Circulation 112:2993–3000
    [Google Scholar]
  55. 55.
    Fuchs TA, Brill A, Wagner DD 2012. Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler. Thromb. Vasc. Biol. 32:1777–83
    [Google Scholar]
  56. 56.
    Phillipson M, Kubes P 2011. The neutrophil in vascular inflammation. Nat. Med. 17:1381–90
    [Google Scholar]
  57. 57.
    Yost CC, Cody MJ, Harris ES, Thornton NL, McInturff AM et al. 2009. Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 113:6419–27
    [Google Scholar]
  58. 58.
    Vong L, Yeung CW, Pinnell LJ, Sherman PM 2016. Adherent-invasive Escherichia coli exacerbates antibiotic-associated intestinal dysbiosis and neutrophil extracellular trap activation. Inflamm. Bowel Dis. 22:42–54
    [Google Scholar]
  59. 59.
    Yipp BG, Petri B, Salina D, Jenne CN, Scott BN et al. 2012. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med. 18:1386–93
    [Google Scholar]
  60. 60.
    de Stoppelaar SF, van ’t Veer C, Claushuis TA, Albersen BJ, Roelofs JJ, van der Poll T 2014. Thrombocytopenia impairs host defense in gram-negative pneumonia-derived sepsis in mice. Blood 124:3781–90
    [Google Scholar]
  61. 61.
    Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z et al. 2007. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13:463–69
    [Google Scholar]
  62. 62.
    Chow OA, von Kockritz-Blickwede M, Bright AT, Hensler ME, Zinkernagel AS et al. 2010. Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe 8:445–54
    [Google Scholar]
  63. 63.
    Okubo K, Kurosawa M, Kamiya M, Urano Y, Suzuki A et al. 2018. Macrophage extracellular trap formation promoted by platelet activation is a key mediator of rhabdomyolysis-induced acute kidney injury. Nat. Med. 24:232–38
    [Google Scholar]
  64. 64.
    Kraemer BF, Campbell RA, Schwertz H, Cody MJ, Franks Z et al. 2011. Novel anti-bacterial activities of β-defensin 1 in human platelets: suppression of pathogen growth and signaling of neutrophil extracellular trap formation. PLOS Pathog 7:e1002355
    [Google Scholar]
  65. 65.
    Yount NY, Yeaman MR 2004. Multidimensional signatures in antimicrobial peptides. PNAS 101:7363–68
    [Google Scholar]
  66. 66.
    Tang YQ, Yeaman MR, Selsted ME 2002. Antimicrobial peptides from human platelets. Infect. Immun. 70:6524–33
    [Google Scholar]
  67. 67.
    Love MS, Millholland MG, Mishra S, Kulkarni S, Freeman KB et al. 2012. Platelet factor 4 activity against P. falciparum and its translation to nonpeptidic mimics as antimalarials. Cell Host Microbe 12:815–23
    [Google Scholar]
  68. 68.
    Wong CH, Jenne CN, Petri B, Chrobok NL, Kubes P 2013. Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat. Immunol. 14:785–92
    [Google Scholar]
  69. 69.
    Gaertner F, Ahmad Z, Rosenberger G, Fan S, Nicolai L et al. 2017. Migrating platelets are mechano-scavengers that collect and bundle bacteria. Cell 171:1368–82.e23
    [Google Scholar]
  70. 70.
    Walz A, Baggiolini M 1990. Generation of the neutrophil-activating peptide NAP-2 from platelet basic protein or connective tissue-activating peptide III through monocyte proteases. J. Exp. Med. 171:449–54
    [Google Scholar]
  71. 71.
    Walz A, Dewald B, von Tscharner V, Baggiolini M 1989. Effects of the neutrophil-activating peptide NAP-2, platelet basic protein, connective tissue-activating peptide III and platelet factor 4 on human neutrophils. J. Exp. Med. 170:1745–50
    [Google Scholar]
  72. 72.
    Ghasemzadeh M, Kaplan ZS, Alwis I, Schoenwaelder SM, Ashworth KJ et al. 2013. The CXCR1/2 ligand NAP-2 promotes directed intravascular leukocyte migration through platelet thrombi. Blood 121:4555–66
    [Google Scholar]
  73. 73.
    Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC et al. 2003. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat. Med. 9:61–67
    [Google Scholar]
  74. 74.
    Massberg S, Brand K, Gruner S, Page S, Muller E et al. 2002. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J. Exp. Med. 196:887–96
    [Google Scholar]
  75. 75.
    Srivastava K, Field DJ, Aggrey A, Yamakuchi M, Morrell CN 2010. Platelet factor 4 regulation of monocyte KLF4 in experimental cerebral malaria. PLOS ONE 5:e10413
    [Google Scholar]
  76. 76.
    Domschke G, Gleissner CA 2017. CXCL4-induced macrophages in human atherosclerosis. Cytokine In press. https://doi.org/10.1016/j.cyto.2017.08.021
    [Crossref]
  77. 77.
    Gleissner CA, Shaked I, Erbel C, Bockler D, Katus HA, Ley K 2010. CXCL4 downregulates the atheroprotective hemoglobin receptor CD163 in human macrophages. Circ. Res. 106:203–11
    [Google Scholar]
  78. 78.
    Gleissner CA, Shaked I, Little KM, Ley K 2010. CXC chemokine ligand 4 induces a unique transcriptome in monocyte-derived macrophages. J. Immunol. 184:4810–18
    [Google Scholar]
  79. 79.
    Alard JE, Ortega-Gomez A, Wichapong K, Bongiovanni D, Horckmans M et al. 2015. Recruitment of classical monocytes can be inhibited by disturbing heteromers of neutrophil HNP1 and platelet CCL5. Sci. Transl. Med. 7:317ra196
    [Google Scholar]
  80. 80.
    Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA et al. 2009. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat. Med. 15:97–103
    [Google Scholar]
  81. 81.
    Duerschmied D, Suidan GL, Demers M, Herr N, Carbo C et al. 2013. Platelet serotonin promotes the recruitment of neutrophils to sites of acute inflammation in mice. Blood 121:1008–15
    [Google Scholar]
  82. 82.
    Cloutier N, Allaeys I, Marcoux G, Machlus KR, Mailhot B et al. 2018. Platelets release pathogenic serotonin and return to circulation after immune complex-mediated sequestration. PNAS 115:E1550–59
    [Google Scholar]
  83. 83.
    McKenzie SE, Taylor SM, Malladi P, Yuhan H, Cassel DL et al. 1999. The role of the human Fc receptor FcγRIIA in the immune clearance of platelets: a transgenic mouse model. J. Immunol. 162:4311–18
    [Google Scholar]
  84. 84.
    Lesurtel M, Graf R, Aleil B, Walther DJ, Tian Y et al. 2006. Platelet-derived serotonin mediates liver regeneration. Science 312:104–7
    [Google Scholar]
  85. 85.
    Morrell CN, Sun H, Ikeda M, Beique JC, Swaim AM et al. 2008. Glutamate mediates platelet activation through the AMPA receptor. J. Exp. Med. 205:575–84
    [Google Scholar]
  86. 86.
    Sun H, Swaim A, Herrera JE, Becker D, Becker L et al. 2009. Platelet kainate receptor signaling promotes thrombosis by stimulating cyclooxygenase activation. Circ. Res. 105:595–603
    [Google Scholar]
  87. 87.
    Morrell CN, Murata K, Swaim AM, Mason E, Martin TV et al. 2008. In vivo platelet-endothelial cell interactions in response to major histocompatibility complex alloantibody. Circ. Res. 102:777–85
    [Google Scholar]
  88. 88.
    Fallarino F, Volpi C, Fazio F, Notartomaso S, Vacca C et al. 2010. Metabotropic glutamate receptor-4 modulates adaptive immunity and restrains neuroinflammation. Nat. Med. 16:897–902
    [Google Scholar]
  89. 89.
    Ganor Y, Besser M, Ben-Zakay N, Unger T, Levite M 2003. Human T cells express a functional ionotropic glutamate receptor GluR3, and glutamate by itself triggers integrin-mediated adhesion to laminin and fibronectin and chemotactic migration. J. Immunol. 170:4362–72
    [Google Scholar]
  90. 90.
    Swaim AM, Field DJ, Fox-Talbot K, Baldwin WM, Morrell CN 2010. Platelets contribute to allograft rejection through glutamate receptor signaling. J. Immunol. 185:6999–7006
    [Google Scholar]
  91. 91.
    Jy W, Horstman LL, Jimenez JJ, Ahn YS, Biro E et al. 2004. Measuring circulating cell-derived microparticles. J. Thromb. Haemost. 2:1842–51
    [Google Scholar]
  92. 92.
    Rautou PE, Vion AC, Amabile N, Chironi G, Simon A et al. 2011. Microparticles, vascular function, and atherothrombosis. Circ. Res. 109:593–606
    [Google Scholar]
  93. 93.
    Boilard E, Nigrovic PA, Larabee K, Watts GF, Coblyn JS et al. 2010. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 327:580–83
    [Google Scholar]
  94. 94.
    Risitano A, Beaulieu LM, Vitseva O, Freedman JE 2012. Platelets and platelet-like particles mediate intercellular RNA transfer. Blood 119:6288–95
    [Google Scholar]
  95. 95.
    Gidlof O, van der Brug M, Ohman J, Gilje P, Olde B et al. 2013. Platelets activated during myocardial infarction release functional miRNA, which can be taken up by endothelial cells and regulate ICAM1 expression. Blood 121:3908–17
    [Google Scholar]
  96. 96.
    Boudreau LH, Duchez AC, Cloutier N, Soulet D, Martin N et al. 2014. Platelets release mitochondria serving as substrate for bactericidal group IIA-secreted phospholipase A2 to promote inflammation. Blood 124:2173–83
    [Google Scholar]
  97. 97.
    Verschoor A, Neuenhahn M, Navarini AA, Graef P, Plaumann A et al. 2011. A platelet-mediated system for shuttling blood-borne bacteria to CD8α+ dendritic cells depends on glycoprotein GPIb and complement C3. Nat. Immunol. 12:1194–201
    [Google Scholar]
  98. 98.
    Elzey BD, Schmidt NW, Crist SA, Kresowik TP, Harty JT et al. 2008. Platelet-derived CD154 enables T-cell priming and protection against Listeriamonocytogenes challenge. Blood 111:3684–91
    [Google Scholar]
  99. 99.
    Andre P, Prasad KS, Denis CV, He M, Papalia JM et al. 2002. CD40L stabilizes arterial thrombi by a β3 integrin–dependent mechanism. Nat. Med. 8:247–52
    [Google Scholar]
  100. 100.
    Straw AD, MacDonald AS, Denkers EY, Pearce EJ 2003. CD154 plays a central role in regulating dendritic cell activation during infections that induce Th1 or Th2 responses. J. Immunol. 170:727–34
    [Google Scholar]
  101. 101.
    Duffau P, Seneschal J, Nicco C, Richez C, Lazaro E et al. 2010. Platelet CD154 potentiates interferon-alpha secretion by plasmacytoid dendritic cells in systemic lupus erythematosus. Sci. Transl. Med. 2:47ra63
    [Google Scholar]
  102. 102.
    Xu H, Zhang X, Mannon RB, Kirk AD 2006. Platelet-derived or soluble CD154 induces vascularized allograft rejection independent of cell-bound CD154. J. Clin. Investig. 116:769–74
    [Google Scholar]
  103. 103.
    Xia CQ, Kao KJ 2003. Effect of CXC chemokine platelet factor 4 on differentiation and function of monocyte-derived dendritic cells. Int. Immunol. 15:1007–15
    [Google Scholar]
  104. 104.
    Hamzeh-Cognasse H, Cognasse F, Palle S, Chavarin P, Olivier T et al. 2008. Direct contact of platelets and their released products exert different effects on human dendritic cell maturation. BMC Immunol 9:54
    [Google Scholar]
  105. 105.
    Sozzani S, Longoni D, Bonecchi R, Luini W, Bersani L et al. 1997. Human monocyte-derived and CD34+ cell-derived dendritic cells express functional receptors for platelet activating factor. FEBS Lett 418:98–100
    [Google Scholar]
  106. 106.
    Idzko M, Hammad H, van Nimwegen M, Kool M, Willart MA et al. 2007. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat. Med. 13:913–19
    [Google Scholar]
  107. 107.
    Chapman LM, Aggrey AA, Field DJ, Srivastava K, Ture S et al. 2012. Platelets present antigen in the context of MHC class I. J. Immunol. 189:916–23
    [Google Scholar]
  108. 108.
    Zufferey A, Speck ER, Machlus KR, Aslam R, Guo L et al. 2017. Mature murine megakaryocytes present antigen-MHC class I molecules to T cells and transfer them to platelets. Blood Adv 1:1773–85
    [Google Scholar]
  109. 109.
    Semple JW, Italiano JE, Freedman J 2011. Platelets and the immune continuum. Nat. Rev. Immunol. 11:264–74
    [Google Scholar]
  110. 110.
    Burkhart JM, Vaudel M, Gambaryan S, Radau S, Walter U et al. 2012. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 120:e73–82
    [Google Scholar]
  111. 111.
    Srivastava K, Cockburn IA, Swaim A, Thompson LE, Tripathi A et al. 2008. Platelet factor 4 mediates inflammation in experimental cerebral malaria. Cell Host Microbe 4:179–87
    [Google Scholar]
  112. 112.
    McMorran BJ, Marshall VM, de Graaf C, Drysdale KE, Shabbar M et al. 2009. Platelets kill intraerythrocytic malarial parasites and mediate survival to infection. Science 323:797–800
    [Google Scholar]
  113. 113.
    McMorran BJ, Wieczorski L, Drysdale KE, Chan JA, Huang HM et al. 2012. Platelet factor 4 and Duffy antigen required for platelet killing of Plasmodium falciparum. . Science 338:1348–51
    [Google Scholar]
  114. 114.
    Gramaglia I, Velez J, Combes V, Grau GE, Wree M, van der Heyde HC 2017. Platelets activate a pathogenic response to blood-stage Plasmodium infection but not a protective immune response. Blood 129:1669–79
    [Google Scholar]
  115. 115.
    Lang PA, Contaldo C, Georgiev P, El-Badry AM, Recher M et al. 2008. Aggravation of viral hepatitis by platelet-derived serotonin. Nat. Med. 14:756–61
    [Google Scholar]
  116. 116.
    Danese S, de la Motte C, Reyes BM, Sans M, Levine AD, Fiocchi C 2004. Cutting edge: T cells trigger CD40-dependent platelet activation and granular RANTES release: a novel pathway for immune response amplification. J. Immunol. 172:2011–15
    [Google Scholar]
  117. 117.
    Gerdes N, Zhu L, Ersoy M, Hermansson A, Hjemdahl P et al. 2011. Platelets regulate CD4+ T-cell differentiation via multiple chemokines in humans. Thromb. Haemost. 106:353–62
    [Google Scholar]
  118. 118.
    Shi G, Field DJ, Ko KA, Ture S, Srivastava K et al. 2014. Platelet factor 4 limits Th17 differentiation and cardiac allograft rejection. J. Clin. Investig. 124:543–52
    [Google Scholar]
  119. 119.
    Bruns I, Lucas D, Pinho S, Ahmed J, Lambert MP et al. 2014. Megakaryocytes regulate hematopoietic stem cell quiescence through CXCL4 secretion. Nat. Med. 20:1315–20
    [Google Scholar]
  120. 120.
    Zhao M, Perry JM, Marshall H, Venkatraman A, Qian P et al. 2014. Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat. Med. 20:1321–26
    [Google Scholar]
  121. 121.
    Winter O, Moser K, Mohr E, Zotos D, Kaminski H et al. 2010. Megakaryocytes constitute a functional component of a plasma cell niche in the bone marrow. Blood 116:1867–75
    [Google Scholar]
  122. 122.
    Field DJ, Aggrey-Amable AA, Blick SK, Ture SK, Johanson A et al. 2017. Platelet factor 4 increases bone marrow B cell development and differentiation. Immunol. Res. 65:1089–94
    [Google Scholar]
  123. 123.
    Cognasse F, Hamzeh-Cognasse H, Lafarge S, Chavarin P, Cogne M et al. 2007. Human platelets can activate peripheral blood B cells and increase production of immunoglobulins. Exp. Hematol. 35:1376–87
    [Google Scholar]
  124. 124.
    Elzey BD, Tian J, Jensen RJ, Swanson AK, Lees JR et al. 2003. Platelet-mediated modulation of adaptive immunity: a communication link between innate and adaptive immune compartments. Immunity 19:9–19
    [Google Scholar]
  125. 125.
    Elzey BD, Grant JF, Sinn HW, Nieswandt B, Waldschmidt TJ, Ratliff TL 2005. Cooperation between platelet-derived CD154 and CD4+ T cells for enhanced germinal center formation. J. Leukoc. Biol. 78:80–84
    [Google Scholar]
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