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Special Review Section: Platelet Secretion

Platelet secretion in inflammatory and infectious diseases

, &
Pages 155-164 | Received 25 May 2016, Accepted 14 Sep 2016, Published online: 16 Nov 2016

References

  • White JG. Platelets and atherosclerosis. Eur J Clin Invest 1994;24(Suppl 1):25–29.
  • del Zoppo GJ. The role of platelets in ischemic stroke. Neurology 1998;51:S9–S14.
  • Boilard E, Blanco P, Nigrovic PA. Platelets: Active players in the pathogenesis of arthritis and SLE. Nat Rev Rheumatol 2012;8:534–542. 10.1038/nrrheum.2012.118.
  • Morowitz DA, Allen LW, Kirsner JB. Thrombocytosis in chronic inflammatory bowel disease. Ann Intern Med 1968;68:1013–1021.
  • Mannaioni PF, Di Bello MG, Masini E. Platelets and inflammation: Role of platelet-derived growth factor, adhesion molecules and histamine. Inflamm Res 1997;46:4–18.
  • Danese S, Scaldaferri F, Papa A, Pola R, Sans M, Gasbarrini G, Pola P, Gasbarrini A. Platelets: New players in the mucosal scenario of inflammatory bowel disease. Eur Rev Med Pharm Sci 2004;8:193–198.
  • Chen C, Li Y, Yu Z, Liu Z, Shi Y, Lewandowska U, Sobczak M, Fichna J, Kreis M. Platelet activity in the pathophysiology of inflammatory bowel diseases. Curr Drug Targets 2015;16:219–225.
  • Kraemer BF, Campbell RA, Schwertz H, Franks ZG, Vieira de Abreu A, Grundler K, Kile BT, Dhakal BK, Rondina MT, Kahr WH, et al. Bacteria differentially induce degradation of Bcl-xL, a survival protein, by human platelets. Blood 2012;120:5014–5020. 10.1182/blood-2012-04-420661.
  • Jenne CN, Urrutia R, Kubes P. Platelets: Bridging hemostasis, inflammation, and immunity. Int J Lab Hematol 2013;35:254–261. 10.1111/ijlh.12084.
  • Maynard DM, Heijnen HF, Horne MK, White JG, Gahl WA. Proteomic analysis of platelet alpha-granules using mass spectrometry. J Thromb Haemost 2007;5:1945–1955. 10.1111/j.1538-7836.2007.02690.x.
  • Flaumenhaft R. Platelet secretion. In: Michelson AD, editor. Platelets, 3rd edn. Elsevier, The Netherlands; 2013. pp. 343–366.
  • Evangelista A, Smyth SS. Interactions Between Platelets, Leukocytes, and the Endothelium. In: Michaels AD, editor. Platelets, 3rd edn. Elsevier, The Netherlands; 2013. pp. 295–307.
  • Frojmovic MM, Milton JG. Human platelet size, shape, and related functions in health and disease. Physiolog Rev 1982;62:185–261.
  • Italiano JE, Jr., Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL. Angiogenesis is regulated by a novel mechanism: Pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 2008;111:1227–1233. 10.1182/blood-2007-09-113837.
  • 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. 10.1111/j.1538-7836.2007.02698.x.
  • van Nispen tot Pannerden H, de Haas F, Geerts W, Posthuma G, van Dijk S, Heijnen HF. The platelet interior revisited: Electron tomography reveals tubular alpha-granule subtypes. Blood 2010;116:1147–1156. 10.1182/blood-2010-02-268680.
  • Koseoglu S, Flaumenhaft R. Advances in platelet granule biology. Curr Opin Hematol 2013 20:464–471. 10.1097/MOH.0b013e3283632e6b.
  • Kahr WH, Lo RW, Li L, Pluthero FG, Christensen H, Ni R, Vaezzadeh N, Hawkins CE, Weyrich AS, Di Paola J, et al. Abnormal megakaryocyte development and platelet function in Nbeal2(−/−) mice. Blood 2013;122:3349–3358. 10.1182/blood-2013-04-499491.
  • Kahr WH, Hinckley J, Li L, Schwertz H, Christensen H, Rowley JW, Pluthero FG, Urban D, Fabbro S, Nixon B, et al. Mutations in NBEAL2, encoding a BEACH protein, cause gray platelet syndrome. Nat Genet 2011;43:738–740. 10.1038/ng.884.
  • Gunay-Aygun M, Falik-Zaccai TC, Vilboux T, Zivony-Elboum Y, Gumruk F, Cetin M, Khayat M, Boerkoel CF, Kfir N, Huang Y, et al. NBEAL2 is mutated in gray platelet syndrome and is required for biogenesis of platelet alpha-granules. Nat Genet 2011;43:732–734. 10.1038/ng.883.
  • Albers CA, Cvejic A, Favier R, Bouwmans EE, Alessi MC, Bertone P, Jordan G, Kettleborough RN, Kiddle G, Kostadima M, et al. Exome sequencing identifies NBEAL2 as the causative gene for gray platelet syndrome. Nat Genet 2011;43:735–737. 10.1038/ng.885.
  • Cullinane AR, Curry JA, Carmona-Rivera C, Summers CG, Ciccone C, Cardillo ND, Dorward H, Hess RA, White JG, Adams D, et al. A BLOC-1 mutation screen reveals that PLDN is mutated in Hermansky-Pudlak Syndrome type 9. Am J Hum Genet 2011;88:778–787. 10.1016/j.ajhg.2011.05.009.
  • Lemons PP, Chen D, Bernstein AM, Bennett MK, Whiteheart SW. Regulated secretion in platelets: Identification of elements of the platelet exocytosis machinery. Blood 1997;90:1490–1500.
  • Sudhof TC, Rothman JE. Membrane fusion: Grappling with SNARE and SM proteins. Science 2009;323:474–477. 10.1126/science.1161748.
  • Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993;362:318–324. 10.1038/362318a0.
  • Ren Q, Barber HK, Crawford GL, Karim ZA, Zhao C, Choi W, Wang CC, Hong W, Whiteheart SW. Endobrevin/VAMP-8 is the primary v-SNARE for the platelet release reaction. Mol Biol Cell 2007;18:24–33. 10.1091/mbc.E06-09-0785.
  • Graham GJ, Ren Q, Dilks JR, Blair P, Whiteheart SW, Flaumenhaft R. Endobrevin/VAMP-8-dependent dense granule release mediates thrombus formation in vivo. Blood 2009;114:1083–1090. 10.1182/blood-2009-03-210211.
  • Ye S, Karim ZA, Al Hawas R, Pessin JE, Filipovich AH, Whiteheart SW. Syntaxin-11, but not syntaxin-2 or syntaxin-4, is required for platelet secretion. Blood 2012;120:2484–2492. 10.1182/blood-2012-05-430603.
  • Murata Y, Yasumi T, Shirakawa R, Izawa K, Sakai H, Abe J, Tanaka N, Kawai T, Oshima K, Saito M, et al. Rapid diagnosis of FHL3 by flow cytometric detection of intraplatelet Munc13-4 protein. Blood 2011;118:1225–1230. 10.1182/blood-2011-01-329540.
  • Savage JS, Williams CM, Konopatskaya O, Hers I, Harper MT, Poole AW. Munc13-4 is critical for thrombosis through regulating release of ADP from platelets. J Thromb Haemost 2013;11:771–775. 10.1111/jth.12138.
  • Harper MT, van den Bosch MT, Hers I, Poole AW. Platelet dense granule secretion defects may obscure alpha-granule secretion mechanisms: Evidence from Munc13-4-deficient platelets. Blood 2015;125:3034–3036. 10.1182/blood-2014-12-618439.
  • Ren Q, Wimmer C, Chicka MC, Ye S, Ren Y, Hughson FM, Whiteheart SW. Munc13-4 is a limiting factor in the pathway required for platelet granule release and hemostasis. Blood 2010;116:869–877. 10.1182/blood-2010-02-270934.
  • Houng A, Polgar J, Reed GL. Munc18-syntaxin complexes and exocytosis in human platelets. J Biol Chem 2003;278:19627–1933. 10.1074/jbc.M212465200.
  • Schraw TD, Lemons PP, Dean WL, Whiteheart SW. A role for Sec1/Munc18 proteins in platelet exocytosis. Biochem J 2003;374:207–217. 10.1042/BJ20030610.
  • Al Hawas R, Ren Q, Ye S, Karim ZA, Filipovich AH, Whiteheart SW. Munc18b/STXBP2 is required for platelet secretion. Blood 2012;120:2493–2500. 10.1182/blood-2012-05-430629.
  • Shirakawa R, Higashi T, Tabuchi A, Yoshioka A, Nishioka H, Fukuda M, Kita T, Horiuchi H. Munc13-4 is a GTP-Rab27-binding protein regulating dense core granule secretion in platelets. J Biol Chem 2004;279:10730–1077. 10.1074/jbc.M309426200.
  • Shirakawa R, Higashi T, Kondo H, Yoshioka A, Kita T, Horiuchi H. Purification and functional analysis of a Rab27 effector munc 13-4 using a semi-intact platelet dense-granule secretion assay. Methods Enzymol 2005;403:778–788. 10.1016/S0076-6879(05)03067-3.
  • Quinton TM, Kim S, Dangelmaier C, Dorsam RT, Jin J, Daniel JL, Kunapuli SP. Protein kinase C- and calcium-regulated pathways independently synergize with Gi pathways in agonist-induced fibrinogen receptor activation. Biochem J 2002;368:535–543. 10.1042/BJ20020226.
  • Gilio K, Harper MT, Cosemans JM, Konopatskaya O, Munnix IC, Prinzen L, Leitges M, Liu Q, Molkentin JD, Heemskerk JW, et al. Functional divergence of platelet protein kinase C (PKC) isoforms in thrombus formation on collagen. J Biol Chem 2010;285:23410–9. 10.1074/jbc.M110.136176.
  • Chari R, Getz T, Nagy B, Jr., Bhavaraju K, Mao Y, Bynagari YS, Murugappan S, Nakayama K, Kunapuli SP. Protein kinase C[delta] differentially regulates platelet functional responses. Arterioscler Thromb Vasc Biol 2009;29:699–705. 10.1161/ATVBAHA.109.184010.
  • Manne BK, Getz TM, Hughes CE, Alshehri O, Dangelmaier C, Naik UP, Watson SP, Kunapuli SP. Fucoidan is a novel platelet agonist for the C-type lectin-like receptor 2 (CLEC-2). J Biol Chem 2013;288:7717–7726. 10.1074/jbc.M112.424473.
  • Reed GL, Houng AK, Fitzgerald ML. Human platelets contain SNARE proteins and a Sec1p homologue that interacts with syntaxin 4 and is phosphorylated after thrombin activation: Implications for platelet secretion. Blood 1999;93:2617–2626.
  • Karim ZA, Zhang J, Banerjee M, Chicka MC, Al Hawas R, Hamilton TR, Roche PA, Whiteheart SW. IkappaB kinase phosphorylation of SNAP-23 controls platelet secretion. Blood 2013;121:4567–4574. 10.1182/blood-2012-11-470468.
  • Polgar J, Lane WS, Chung SH, Houng AK, Reed GL. Phosphorylation of SNAP-23 in activated human platelets. J Biol Chem 2003;278:44369–4476. 10.1074/jbc.M307864200.
  • Zucker-Franklin D. Endocytosis by human platelets: Metabolic and freeze-fracture studies. J Cell Biol 1981;91:706–715.
  • Handagama PJ, Shuman MA, Bainton DF. Incorporation of intravenously injected albumin, immunoglobulin G, and fibrinogen in guinea pig megakaryocyte granules. J Clin Invest 1989;84:73–82. 10.1172/JCI114173.
  • Handagama P, Scarborough RM, Shuman MA, Bainton DF. Endocytosis of fibrinogen into megakaryocyte and platelet alpha-granules is mediated by alpha IIb beta 3 (glycoprotein IIb-IIIa). Blood 1993;82:135–138.
  • Salgado R, Benoy I, Bogers J, Weytjens R, Vermeulen P, Dirix L, Van Marck E. Platelets and vascular endothelial growth factor (VEGF): A morphological and functional study. Angiogenesis 2001;4:37–43.
  • Huang Y, Joshi S, Xiang B, Kanaho Y, Li Z, Bouchard BA, Moncman CL, Whiteheart SW. Arf6 controls platelet spreading and clot retraction via integrin alphaIIbbeta3 trafficking. Blood 2016;127:1459–1467. 10.1182/blood-2015-05-648550.
  • Kanamarlapudi V, Owens SE, Saha K, Pope RJ, Mundell SJ. ARF6-dependent regulation of P2Y receptor traffic and function in human platelets. PloS one 2012;7:e43532. 10.1371/journal.pone.0043532.
  • Richards-Smith B, Novak EK, Jang EK, He P, Haslam RJ, Castle D, Whiteheart SW, Swank RT. Analyses of proteins involved in vesicular trafficking in platelets of mouse models of Hermansky Pudlak syndrome. Mol Genet Metab 1999;68:14–23. 10.1006/mgme.1999.2891.
  • Evangelista V, Manarini S, Sideri R, Rotondo S, Martelli N, Piccoli A, Totani L, Piccardoni P, Vestweber D, de Gaetano G, et al. Platelet/polymorphonuclear leukocyte interaction: P-selectin triggers protein-tyrosine phosphorylation-dependent CD11b/CD18 adhesion: Role of PSGL-1 as a signaling molecule. Blood 1999;93:876–885.
  • Nomura S, Okamae F, Abe M, Hosokawa M, Yamaoka M, Ohtani T, Onishi S, Matsuzaki T, Teraoka A, Ishida T, et al. Platelets expressing P-selectin and platelet-derived microparticles in stored platelet concentrates bind to PSGL-1 on filtrated leukocytes. Clin Appl Thromb Hemost Off J Int Acad Clin Appl Thromb Hemostasis 2000;6:213–221.
  • Furie B, Furie BC, Flaumenhaft R. A journey with platelet P-selectin: The molecular basis of granule secretion, signalling and cell adhesion. Thromb Haemost 2001;86:214–221.
  • Michelson AD, Barnard MR, Krueger LA, Valeri CR, Furman MI. Circulating monocyte-platelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin: Studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation 2001;104:1533–1537.
  • Rondina MT, Carlisle M, Fraughton T, Brown SM, Miller RR, 3rd, Harris ES, Weyrich AS, Zimmerman GA, Supiano MA, Grissom CK. Platelet-monocyte aggregate formation and mortality risk in older patients with severe sepsis and septic shock. J Gerontol A Biol Sci Med Sci 2015;70:225–231. 10.1093/gerona/glu082.
  • Rondina MT, Brewster B, Grissom CK, Zimmerman GA, Kastendieck DH, Harris ES, Weyrich AS. In Vivo Platelet Activation in Critically Ill Patients With Primary 2009 Influenza A(H1N1). Chest 2012;141:1490–1495. 10.1378/chest.11-2860.
  • Freedman JE, Loscalzo J. Platelet-monocyte aggregates: Bridging thrombosis and inflammation. Circulation 2002;105:2130–2132.
  • Palabrica T, Lobb R, Furie BC, Aronovitz M, Benjamin C, Hsu YM, Sajer SA, Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature 1992;359:848–851. 10.1038/359848a0.
  • Hrachovinova I, Cambien B, Hafezi-Moghadam A, Kappelmayer J, Camphausen RT, Widom A, Xia L, Kazazian HH, Jr., Schaub RG, McEver RP, et al. Interaction of P-selectin and PSGL-1 generates microparticles that correct hemostasis in a mouse model of hemophilia A. Nat Med 2003;9:1020–1025. 10.1038/nm899.
  • Falati S, Liu Q, Gross P, Merrill-Skoloff G, Chou J, Vandendries E, Celi A, Croce K, Furie BC, Furie B. Accumulation of tissue factor into developing thrombi in vivo is dependent upon microparticle P-selectin glycoprotein ligand 1 and platelet P-selectin. J Exp Med 2003;197:1585–1598. 10.1084/jem.20021868.
  • Zwicker JI, Trenor CC, 3rd, Furie BC, Furie B. Tissue factor-bearing microparticles and thrombus formation. Arterioscler Thromb Vasc Biol 2011;31:728–733. 10.1161/ATVBAHA.109.200964.
  • Zarbock A, Ley K. The role of platelets in acute lung injury (ALI). Front Biosci (Landmark Ed). 2009;14:150–158.
  • Kiefmann R, Heckel K, Schenkat S, Dorger M, Goetz AE. Role of p-selectin in platelet sequestration in pulmonary capillaries during endotoxemia. J Vasc Res 2006;43:473–481. 10.1159/000095247.
  • Gear AR, Camerini D. Platelet chemokines and chemokine receptors: Linking hemostasis, inflammation, and host defense. Microcirculation 2003;10:335–350. 10.1038/sj.mn.7800198.
  • Eriksson EE. Mechanisms of leukocyte recruitment to atherosclerotic lesions: Future prospects. Curr Opin Lipidol 2004;15:553–558.
  • Kameyoshi Y, Dorschner A, Mallet AI, Christophers E, Schroder JM. Cytokine RANTES released by thrombin-stimulated platelets is a potent attractant for human eosinophils. J Exp Med 1992; 176:587–592.
  • von Hundelshausen P, Weber KS, Huo Y, Proudfoot AE, Nelson PJ, Ley K, Weber C. RANTES deposition by platelets triggers monocyte arrest on inflamed and atherosclerotic endothelium. Circulation 2001;103:1772–1777.
  • Gilat D, Hershkoviz R, Mekori YA, Vlodavsky I, Lider O. Regulation of adhesion of CD4+ T lymphocytes to intact or heparinase-treated subendothelial extracellular matrix by diffusible or anchored RANTES and MIP-1 beta. J Immunol 1994;153:4899–4906.
  • 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;25:1512–1518. 10.1161/01.ATV.0000170133.43608.37.
  • Schober A, Manka D, von Hundelshausen P, Huo Y, Hanrath P, Sarembock IJ, Ley K, Weber C. Deposition of platelet RANTES triggering monocyte recruitment requires P-selectin and is involved in neointima formation after arterial injury. Circulation 2002;106:1523–1529.
  • Schober A, Zernecke A. Chemokines in vascular remodeling. Thromb Haemost 2007;97:730–737.
  • Slungaard A. Platelet factor 4: A chemokine enigma. Int J Biochem Cell Biol 2005;37:1162–1167. 10.1016/j.biocel.2004.12.003.
  • Petersen F, Ludwig A, Flad HD, Brandt E. TNF-alpha renders human neutrophils responsive to platelet factor 4. Comparison of PF-4 and IL-8 reveals different activity profiles of the two chemokines. J Immunol 1996;156:1954–1962.
  • Kasper B, Brandt E, Bulfone-Paus S, Petersen F. Platelet factor 4 (PF-4)-induced neutrophil adhesion is controlled by src-kinases, whereas PF-4-mediated exocytosis requires the additional activation of p38 MAP kinase and phosphatidylinositol 3-kinase. Blood 2004;103:1602–1610. 10.1182/blood-2003-08-2802.
  • Kasper B, Brandt E, Ernst M, Petersen F. Neutrophil adhesion to endothelial cells induced by platelet factor 4 requires sequential activation of Ras, Syk, and JNK MAP kinases. Blood 2006;107:1768–1775. 10.1182/blood-2005-06-2501.
  • Pervushina O, Scheuerer B, Reiling N, Behnke L, Schroder JM, Kasper B, Brandt E, Bulfone-Paus S, Petersen F. Platelet factor 4/CXCL4 induces phagocytosis and the generation of reactive oxygen metabolites in mononuclear phagocytes independently of Gi protein activation or intracellular calcium transients. J Immunol 2004;173:2060–2067.
  • von Hundelshausen P, Koenen RR, Sack M, Mause SF, Adriaens W, Proudfoot AE, Hackeng TM, Weber C. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005;105:924–930. 10.1182/blood-2004-06-2475.
  • Hawrylowicz CM, Santoro SA, Platt FM, Unanue ER. Activated platelets express IL-1 activity. J Immunol 1989;143:4015–4018.
  • Lindemann S, Tolley ND, Dixon DA, McIntyre TM, Prescott SM, Zimmerman GA, Weyrich AS. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J Cell Biol 2001;154:485–490. 10.1083/jcb.200105058.
  • Brown GT, Narayanan P, Li W, Silverstein RL, McIntyre TM. Lipopolysaccharide stimulates platelets through an IL-1beta autocrine loop. J Immunol 2013;191:5196–5203. 10.4049/jimmunol.1300354.
  • Lindemann S, Tolley ND, Dixon DA, McIntyre TM, Prescott SM, Zimmerman GA, Weyrich AS. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J Cell Biol 2001;154:485–490. 10.1083/jcb.200105058.
  • Warkentin TE, Arnold DM, Nazi I, Kelton JG. The platelet serotonin-release assay. Am J Hematol 2015;90:564–572. 10.1002/ajh.24006.
  • Lood C, Tyden H, Gullstrand B, Klint C, Wenglen C, Nielsen CT, Heegaard NH, Jonsen A, Kahn R, Bengtsson AA. Type I interferon-mediated skewing of the serotonin synthesis is associated with severe disease in systemic lupus erythematosus. PloS One 2015;10:e0125109. 10.1371/journal.pone.0125109.
  • Shinohara Y, Nishimaru K, Sawada T, Terashi A, Handa S, Hirai S, Hayashi K, Tohgi H, Fukuuchi Y, Uchiyama S, et al. Sarpogrelate-Aspirin Comparative Clinical Study for Efficacy and Safety in Secondary Prevention of Cerebral Infarction (S-ACCESS): A randomized, double-blind, aspirin-controlled trial. Stroke; a journal of cerebral Circulation 2008;39:1827–1833. 10.1161/STROKEAHA.107.505131.
  • Mach F. The role of chemokines in atherosclerosis. Curr Atherosclerosis Rep 2001;3:243–251.
  • Huo Y, Ley KF. Role of platelets in the development of atherosclerosis. Trends Cardiovasc Med 2004;14:18–22.
  • Shebuski RJ, Kilgore KS. Role of inflammatory mediators in thrombogenesis. J Pharmacol Exp Ther 2002;300:729–735.
  • Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, Littman DR, Weber C, Ley K. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med 2003;9:61–67. 10.1038/nm810.
  • Lievens D, Zernecke A, Seijkens T, Soehnlein O, Beckers L, Munnix IC, Wijnands E, Goossens P, van Kruchten R, Thevissen L, et al. Platelet CD40L mediates thrombotic and inflammatory processes in atherosclerosis. Blood 2010;116:4317–4327. 10.1182/blood-2010-01-261206.
  • Seta N, Okazaki Y, Miyazaki H, Kato T, Kuwana M. Platelet-derived stromal cell-derived factor-1 is required for the transformation of circulating monocytes into multipotential cells. PloS One 2013;8:e74246. 10.1371/journal.pone.0074246.
  • Koenen RR, von Hundelshausen P, Nesmelova IV, Zernecke A, Liehn EA, Sarabi A, Kramp BK, Piccinini AM, Paludan SR, Kowalska MA, et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009;15:97–103. 10.1038/nm.1898.
  • Schober A, Knarren S, Lietz M, Lin EA, Weber C. Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice. Circulation 2003;108:2491–2497. 10.1161/01.CIR.0000099508.76665.9A.
  • Yin Y, Zhao X, Fang Y, Yu S, Zhao J, Song M, Huang L. SDF-1alpha involved in mobilization and recruitment of endothelial progenitor cells after arterial injury in mice. Cardiovasc Pathol Off J Soc Cardiovasc Pathol 2010;19:218–227. 10.1016/j.carpath.2009.04.002.
  • Navarro-Sobrino M, Rosell A, Hernandez-Guillamon M, Penalba A, Boada C, Domingues-Montanari S, Ribo M, Alvarez-Sabin J, Montaner J. A large screening of angiogenesis biomarkers and their association with neurological outcome after ischemic stroke. Atherosclerosis 2011;216:205–211. 10.1016/j.atherosclerosis.2011.01.030.
  • Veillard NR, Kwak B, Pelli G, Mulhaupt F, James RW, Proudfoot AE, Mach F. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res 2004;94:253–261. 10.1161/01.RES.0000109793.17591.4E.
  • Sachais BS, Kuo A, Nassar T, Morgan J, Kariko K, Williams KJ, Feldman M, Aviram M, Shah N, Jarett L, et al. Platelet factor 4 binds to low-density lipoprotein receptors and disrupts the endocytic machinery, resulting in retention of low-density lipoprotein on the cell surface. Blood 2002;99:3613–3622.
  • Nassar T, Sachais BS, Akkawi S, Kowalska MA, Bdeir K, Leitersdorf E, Hiss E, Ziporen L, Aviram M, Cines D, et al. Platelet factor 4 enhances the binding of oxidized low-density lipoprotein to vascular wall cells. J Biol Chem 2003;278:6187–6193. 10.1074/jbc.M208894200.
  • Wiesner T, Bugl S, Mayer F, Hartmann JT, Kopp HG. Differential changes in platelet VEGF, Tsp, CXCL12, and CXCL4 in patients with metastatic cancer. Clin Exp Metastasis 2010;27:141–149. 10.1007/s10585-010-9311-6.
  • Gasic GJ, Gasic TB, Galanti N, Johnson T, Murphy S. Platelet-tumor-cell interactions in mice. The role of platelets in the spread of malignant disease. Int J Cancer J Int du Cancer 1973;11:704–718.
  • Gasic GJ, Koch PA, Hsu B, Gasic TB, Niewiarowski S. Thrombogenic activity of mouse and human tumors: Effects on platelets, coagulation, and fibrinolysis, and possible significance for metastases. Z Krebsforsch Klin Onkol Cancer Res Clin Oncol 1976;86:263–277.
  • Menter DG, Onoda JM, Taylor JD, Honn KV. Effects of prostacyclin on tumor cell-induced platelet aggregation. Cancer Res 1984;44:450–456.
  • Heinmoller E, Schropp T, Kisker O, Simon B, Seitz R, Weinel RJ. Tumor cell-induced platelet aggregation in vitro by human pancreatic cancer cell lines. Scand J Gastroenterol 1995;30:1008–1016.
  • Borsig L. The role of platelet activation in tumor metastasis. Expert Rev Anticancer Ther 2008;8:1247–1255. 10.1586/14737140.8.8.1247.
  • Goubran HA, Stakiw J, Radosevic M, Burnouf T. Platelets effects on tumor growth. Semin Oncol 2014;41:359–369. 10.1053/j.seminoncol.2014.04.006.
  • Honn KV, Tang DG, Crissman JD. Platelets and cancer metastasis: A causal relationship? Cancer Metastasis Rev 1992;11:325–351.
  • Dovizio M, Alberti S, Guillem-Llobat P, Patrignani P. Role of platelets in inflammation and cancer: Novel therapeutic strategies. Basic Clin Pharmacol Toxicol 2014;114:118–127. 10.1111/bcpt.12156.
  • Jia Y, Zhang S, Miao L, Wang J, Jin Z, Gu B, Duan Z, Zhao Z, Ma S, Zhang W, et al. Activation of platelet protease-activated receptor-1 induces epithelial-mesenchymal transition and chemotaxis of colon cancer cell line SW620. Oncology Rep 2015;33:2681–2688. 10.3892/or.2015.3897.
  • Assoian RK, Komoriya A, Meyers CA, Miller DM, Sporn MB. Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization. J Biol Chem 1983;258:7155–7160.
  • Kopp HG, Placke T, Salih HR. Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res 2009;69:7775–7783. 10.1158/0008-5472.CAN-09-2123.
  • Thomas MR, Storey RF. The role of platelets in inflammation. Thromb Haemost 2015;114:449–458. 10.1160/TH14-12-1067.
  • Gawaz M, Dickfeld T, Bogner C, Fateh-Moghadam S, Neumann FJ. Platelet function in septic multiple organ dysfunction syndrome. Intensive Care Med 1997;23:379–385.
  • 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;25:843–851.
  • de Stoppelaar SF, Van’t Veer C, Roelofs JJ, Claushuis TA, de Boer OJ, Tanck MW, Hoogendijk AJ, van der Poll T. Platelet and endothelial cell P-selectin are required for host defense against Klebsiella pneumoniae-induced pneumosepsis. J Thromb Haemost 2015;13:1128–1138. 10.1111/jth.12893.
  • Zarbock A, Singbartl K, Ley K. Complete reversal of acid-induced acute lung injury by blocking of platelet-neutrophil aggregation. J Clin Invest 2006;116:3211–3219. 10.1172/JCI29499.
  • Parker ZF, Rux AH, Riblett AM, Lee FH, Rauova L, Cines DB, Poncz M, Sachais BS, Doms RW. Platelet factor 4 inhibits and enhances HIV-1 infection in a concentration-dependent manner by modulating viral attachment. AIDS Res Hum Retroviruses 2016. 10.1089/AID.2015.0344.
  • Solomon Tsegaye T, Gnirss K, Rahe-Meyer N, Kiene M, Kramer-Kuhl A, Behrens G, Munch J, Pohlmann S. Platelet activation suppresses HIV-1 infection of T cells. Retrovirology 2013;10:48. 10.1186/1742-4690-10-48.
  • Viskovic K, Zidovec-Lepej S, Gorenec L, Grgic I, Lukas D, Zekan S, Dragobratovic A, Begovac J. Cardiovascular markers of inflammation and serum lipid levels in HIV-infected patients with undetectable viraemia. J Int AIDS Soc 2014;17:19548. 10.7448/IAS.17.4.19548.
  • Miller EA, Gopal R, Valdes V, Berger JS, Bhardwaj N, O’Brien MP. Soluble CD40 ligand contributes to dendritic cell-mediated T-cell dysfunction in HIV-1 infection. AIDS 2015;29:1287–1296. 10.1097/QAD.0000000000000698.
  • Skudowitz RB, Katz J, Lurie A, Levin J, Metz J. Mechanisms of thrombocytopenia in malignant tertian malaria. Br Med J 1973;2:515–518.
  • Singh T, Mirakhur N, Ahuja P. Thrombocytopenia in P. falciparum infection. J Assoc Phys India 1983;31:323–324.
  • Essien EM, Ebhota MI. Platelet secretory activities in acute malaria (Plasmodium falciparum) infection. Acta Haematol 1983;70:183–188.
  • Love MS, Millholland MG, Mishra S, Kulkarni S, Freeman KB, Pan W, Kavash RW, Costanzo MJ, Jo H, Daly TM, et al. Platelet factor 4 activity against P. falciparum and its translation to nonpeptidic mimics as antimalarials. Cell Host Microbe 2012;12:815–823. 10.1016/j.chom.2012.10.017.
  • McMorran BJ, Wieczorski L, Drysdale KE, Chan JA, Huang HM, Smith C, Mitiku C, Beeson JG, Burgio G, Foote SJ. Platelet factor 4 and Duffy antigen required for platelet killing of Plasmodium falciparum. Science 2012;338:1348–1351. 10.1126/science.1228892.
  • Polack B, Peyron F, Sheick Zadiuddin I, Kolodie L, Ambroise-Thomas P. Erythrocytes infected by Plasmodium falciparum activate human platelets. C R Acad Sci III 1990;310:577–582.
  • Srivastava K, Cockburn IA, Swaim A, Thompson LE, Tripathi A, Fletcher CA, Shirk EM, Sun H, Kowalska MA, Fox-Talbot K, et al. Platelet factor 4 mediates inflammation in experimental cerebral malaria. Cell Host Microbe 2008;4:179–187. 10.1016/j.chom.2008.07.003.
  • Vieira-de-Abreu A, Rondina MT, Weyrich AS, Zimmerman GA. Inflammation. In: Michelson AD, editor. Platelets, 3rd edn. New York: Elsevier; 2012. pp. 733–766.

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