A Champion of Host Defense: A Generic Large-Scale Cause for Platelet Dysfunction and Depletion in Infection

Abstract

Thrombocytopenia is commonly associated with sepsis and infections, which in turn are characterized by a profound immune reaction to the invading pathogen. Platelets are one of the cellular entities that exert considerable immune, antibacterial, and antiviral actions, and are therefore active participants in the host response. Platelets are sensitive to surrounding inflammatory stimuli and contribute to the immune response by multiple mechanisms, including endowing the endothelium with a proinflammatory phenotype, enhancing and amplifying leukocyte recruitment and inflammation, promoting the effector functions of immune cells, and ensuring an optimal adaptive immune response. During infection, pathogens and their products influence the platelet response and can even be toxic. However, platelets are able to sense and engage bacteria and viruses to assist in their removal and destruction. Platelets greatly contribute to host defense by multiple mechanisms, including forming immune complexes and aggregates, shedding their granular content, and internalizing pathogens and subsequently being marked for removal. These processes, and the nature of platelet function in general, cause the platelet to be irreversibly consumed in the execution of its duty. An exaggerated systemic inflammatory response to infection can drive platelet dysfunction, where platelets are inappropriately activated and face immunological destruction. While thrombocytopenia may arise by condition-specific mechanisms that cause an imbalance between platelet production and removal, this review evaluates a generic large-scale mechanism for platelet depletion as a repercussion of its involvement at the nexus of responses to infection.

Keywords

platelets - virus - bacteria - thrombocytopenia - immune response

Author Contribution Statement

M.P.: wrote paper, prepared figures; E.P.: wrote parts of the paper, study leader, and corresponding author. Both authors edited and reviewed the manuscript.

Publication History

Publication Date:
12 April 2020 (online)

• References

• 1 Semple JW, Freedman J. Platelets and innate immunity. Cell Mol Life Sci 2010; 67 (04) 499-511
• 2 Semple JW, Italiano Jr JE, Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011; 11 (04) 264-274
• 3 Speth C, Löffler J, Krappmann S, Lass-Flörl C, Rambach G. Platelets as immune cells in infectious diseases. Future Microbiol 2013; 8 (11) 1431-1451
• 4 Weyrich AS, Zimmerman GA. Platelets: signaling cells in the immune continuum. Trends Immunol 2004; 25 (09) 489-495
• 5 Jenne CN, Kubes P. Platelets in inflammation and infection. Platelets 2015; 26 (04) 286-292
• 6 Assinger A. Platelets and infection - an emerging role of platelets in viral infection. Front Immunol 2014; 5: 649
• 7 Hottz ED, Bozza FA, Bozza PT. Platelets in immune response to virus and immunopathology of viral infections. Front Med (Lausanne) 2018; 5: 121
• 8 Yeaman MR. Platelets in defense against bacterial pathogens. Cell Mol Life Sci 2010; 67 (04) 525-544
• 9 Yeaman MR. Platelets: at the nexus of antimicrobial defence. Nat Rev Microbiol 2014; 12 (06) 426-437
• 10 Fitzgerald JR, Foster TJ, Cox D. The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006; 4 (06) 445-457
• 11 Hamzeh-Cognasse H, Damien P, Chabert A, Pozzetto B, Cognasse F, Garraud O. Platelets and infections - complex interactions with bacteria. Front Immunol 2015; 6: 82
• 12 Cox D, Kerrigan SW, Watson SP. Platelets and the innate immune system: mechanisms of bacterial-induced platelet activation. J Thromb Haemost 2011; 9 (06) 1097-1107
• 13 Wong CHY, Jenne CN, Petri B, Chrobok NL, Kubes P. Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat Immunol 2013; 14 (08) 785-792
• 14 Sullam PM, Frank U, Yeaman MR, Täuber MG, Bayer AS, Chambers HF. Effect of thrombocytopenia on the early course of streptococcal endocarditis. J Infect Dis 1993; 168 (04) 910-914
• 15 Zhang X, Liu Y, Gao Y. et al. Inhibiting platelets aggregation could aggravate the acute infection caused by Staphylococcus aureus. Platelets 2011; 22 (03) 228-236
• 16 Claushuis TAM, van Vught LA, Scicluna BP. et al; Molecular Diagnosis and Risk Stratification of Sepsis Consortium. Thrombocytopenia is associated with a dysregulated host response in critically ill sepsis patients. Blood 2016; 127 (24) 3062-3072
• 17 Dewitte A, Lepreux S, Villeneuve J. et al. Blood platelets and sepsis pathophysiology: a new therapeutic prospect in critically ill patients?. Ann Intensive Care 2017; 7 (01) 115
• 18 Iannacone M, Sitia G, Isogawa M. et al. Platelets prevent IFN-α/β-induced lethal hemorrhage promoting CTL-dependent clearance of lymphocytic choriomeningitis virus. Proc Natl Acad Sci U S A 2008; 105 (02) 629-634
• 19 Loria GD, Romagnoli PA, Moseley NB, Rucavado A, Altman JD. Platelets support a protective immune response to LCMV by preventing splenic necrosis. Blood 2013; 121 (06) 940-950
• 20 Solomon Tsegaye T, Gnirß K, Rahe-Meyer N. et al. Platelet activation suppresses HIV-1 infection of T cells. Retrovirology 2013; 10: 48
• 21 D' Atri LP, Schattner M. Platelet toll-like receptors in thromboinflammation. Front Biosci 2017; 22: 1867-1883
• 22 Jenne CN. Platelets: crossroads of immunity and hemostasis. Blood 2014; 124 (05) 671-672
• 23 Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 2010; 30 (12) 2341-2349
• 24 van Gils JM, Zwaginga JJ, Hordijk PL. Molecular and functional interactions among monocytes, platelets, and endothelial cells and their relevance for cardiovascular diseases. J Leukoc Biol 2009; 85 (02) 195-204
• 25 Shannon O. Platelet interaction with bacterial toxins and secreted products. Platelets 2015; 26 (04) 302-308
• 26 Zhang W, Nardi MA, Borkowsky W, Li Z, Karpatkin S. Role of molecular mimicry of hepatitis C virus protein with platelet GPIIIa in hepatitis C-related immunologic thrombocytopenia. Blood 2009; 113 (17) 4086-4093
• 27 Aref S, Sleem T, El Menshawy N. et al. Antiplatelet antibodies contribute to thrombocytopenia associated with chronic hepatitis C virus infection. Hematology 2009; 14 (05) 277-281
• 28 Olumuyiwa-Akeredolu OO, Page MJ, Soma P, Pretorius E. Platelets: emerging facilitators of cellular crosstalk in rheumatoid arthritis. Nat Rev Rheumatol 2019; 15 (04) 237-248
• 29 Franchini M, Veneri D, Lippi G. Thrombocytopenia and infections. Expert Rev Hematol 2017; 10 (01) 99-106
• 30 Flaujac C, Boukour S, Cramer-Bordé E. Platelets and viruses: an ambivalent relationship. Cell Mol Life Sci 2010; 67 (04) 545-556
• 31 Larkin CM, Santos-Martinez M-J, Ryan T, Radomski MW. Sepsis-associated thrombocytopenia. Thromb Res 2016; 141: 11-16
• 32 Tosi MF. Innate immune responses to infection. J Allergy Clin Immunol 2005; 116 (02) 241-249 , quiz 250
• 33 McNicol A, Agpalza A, Jackson EC, Hamzeh-Cognasse H, Garraud O, Cognasse F. Streptococcus sanguinis-induced cytokine release from platelets. J Thromb Haemost 2011; 9 (10) 2038-2049
• 34 Page AV, Liles WC. Biomarkers of endothelial activation/dysfunction in infectious diseases. Virulence 2013; 4 (06) 507-516
• 35 Yeaman MR. The role of platelets in antimicrobial host defense. Clin Infect Dis 1997; 25 (05) 951-968 , quiz 969–970
• 36 Sugiyama MG, Gamage A, Zyla R. et al. Influenza virus infection induces platelet-endothelial adhesion which contributes to lung injury. J Virol 2015; 90 (04) 1812-1823
• 37 Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005; 115 (12) 3378-3384
• 38 Assinger A, Laky M, Schabbauer G. et al. Efficient phagocytosis of periodontopathogens by neutrophils requires plasma factors, platelets and TLR2. J Thromb Haemost 2011; 9 (04) 799-809
• 39 Miedzobrodzki J, Panz T, Płonka PM. et al. Platelets augment respiratory burst in neutrophils activated by selected species of gram-positive or gram-negative bacteria. Folia Histochem Cytobiol 2008; 46 (03) 383-388
• 40 Peters MJ, Dixon G, Kotowicz KT, Hatch DJ, Heyderman RS, Klein NJ. Circulating platelet-neutrophil complexes represent a subpopulation of activated neutrophils primed for adhesion, phagocytosis and intracellular killing. Br J Haematol 1999; 106 (02) 391-399
• 41 Nagata K, Tsuji T, Todoroki N. et al. Activated platelets induce superoxide anion release by monocytes and neutrophils through P-selectin (CD62). J Immunol 1993; 151 (06) 3267-3273
• 42 Jin R, Yu S, Song Z. et al. Soluble CD40 ligand stimulates CD40-dependent activation of the β2 integrin Mac-1 and protein kinase C zeda (PKCζ) in neutrophils: implications for neutrophil-platelet interactions and neutrophil oxidative burst. PLoS One 2013; 8 (06) e64631
• 43 Haselmayer P, Grosse-Hovest L, von Landenberg P, Schild H, Radsak MP. TREM-1 ligand expression on platelets enhances neutrophil activation. Blood 2007; 110 (03) 1029-1035
• 44 Bouchon A, Facchetti F, Weigand MA, Colonna M. TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 2001; 410 (6832): 1103-1107
• 45 Mohamadzadeh M, Coberley SS, Olinger GG. et al. Activation of triggering receptor expressed on myeloid cells-1 on human neutrophils by marburg and ebola viruses. J Virol 2006; 80 (14) 7235-7244
• 46 Brinkmann V, Reichard U, Goosmann C. et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303 (5663): 1532-1535
• 47 McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 2012; 12 (03) 324-333
• 48 Ma AC, Kubes P. Platelets, neutrophils, and neutrophil extracellular traps (NETs) in sepsis. J Thromb Haemost 2008; 6 (03) 415-420
• 49 Jenne CN, Wong CH, Zemp FJ. et al. Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host Microbe 2013; 13 (02) 169-180
• 50 Urban CF, Ermert D, Schmid M. et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5 (10) e1000639
• 51 Saitoh T, Komano J, Saitoh Y. et al. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 2012; 12 (01) 109-116
• 52 Assinger A, Laky M, Badrnya S, Esfandeyari A, Volf I. Periodontopathogens induce expression of CD40L on human platelets via TLR2 and TLR4. Thromb Res 2012; 130 (03) e73-e78
• 53 Elzey BD, Tian J, Jensen RJ. et al. Platelet-mediated modulation of adaptive immunity. A communication link between innate and adaptive immune compartments. Immunity 2003; 19 (01) 9-19
• 54 Sowa JM, Crist SA, Ratliff TL, Elzey BD. Platelet influence on T- and B-cell responses. Arch Immunol Ther Exp (Warsz) 2009; 57 (04) 235-241
• 55 Elzey BD, Schmidt NW, Crist SA. et al. Platelet-derived CD154 enables T-cell priming and protection against Listeria monocytogenes challenge. Blood 2008; 111 (07) 3684-3691
• 56 Kaneider NC, Kaser A, Tilg H, Ricevuti G, Wiedermann CJ. CD40 ligand-dependent maturation of human monocyte-derived dendritic cells by activated platelets. Int J Immunopathol Pharmacol 2003; 16 (03) 225-231
• 57 Czapiga M, Kirk AD, Lekstrom-Himes J. Platelets deliver costimulatory signals to antigen-presenting cells: a potential bridge between injury and immune activation. Exp Hematol 2004; 32 (02) 135-139
• 58 Kissel K, Berber S, Nockher A, Santoso S, Bein G, Hackstein H. Human platelets target dendritic cell differentiation and production of proinflammatory cytokines. Transfusion 2006; 46 (05) 818-827
• 59 Hamzeh-Cognasse H, Cognasse F, Palle S. et al. Direct contact of platelets and their released products exert different effects on human dendritic cell maturation. BMC Immunol 2008; 9: 54
• 60 Iannacone M, Sitia G, Isogawa M. et al. Platelets mediate cytotoxic T lymphocyte-induced liver damage. Nat Med 2005; 11 (11) 1167-1169
• 61 Lang PA, Contaldo C, Georgiev P. et al. Aggravation of viral hepatitis by platelet-derived serotonin. Nat Med 2008; 14 (07) 756-761
• 62 Verschoor A, Neuenhahn M, Navarini AA. 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 (12) 1194-1201
• 63 Ogura H, Kawasaki T, Tanaka H. et al. Activated platelets enhance microparticle formation and platelet-leukocyte interaction in severe trauma and sepsis. J Trauma 2001; 50 (05) 801-809
• 64 Ge S, Hertel B, Emden SH. et al. Microparticle generation and leucocyte death in Shiga toxin-mediated HUS. Nephrol Dial Transplant 2012; 27 (07) 2768-2775
• 65 Wang J, Zhang W, Nardi MA, Li Z. HIV-1 Tat-induced platelet activation and release of CD154 contribute to HIV-1-associated autoimmune thrombocytopenia. J Thromb Haemost 2011; 9 (03) 562-573
• 66 Mayne E, Funderburg NT, Sieg SF. et al. Increased platelet and microparticle activation in HIV infection: upregulation of P-selectin and tissue factor expression. J Acquir Immune Defic Syndr 2012; 59 (04) 340-346
• 67 Boilard E, Nigrovic PA, Larabee K. et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327 (5965): 580-583
• 68 Nomura S. Function and clinical significance of platelet-derived microparticles. Int J Hematol 2001; 74 (04) 397-404
• 69 Barry OP, Praticò D, Savani RC, FitzGerald GA. Modulation of monocyte-endothelial cell interactions by platelet microparticles. J Clin Invest 1998; 102 (01) 136-144
• 70 Lo S-C, Hung C-Y, Lin D-T, Peng H-C, Huang T-F. Involvement of platelet glycoprotein Ib in platelet microparticle mediated neutrophil activation. J Biomed Sci 2006; 13 (06) 787-796
• 71 Forlow SB, McEver RP, Nollert MU. Leukocyte-leukocyte interactions mediated by platelet microparticles under flow. Blood 2000; 95 (04) 1317-1323
• 72 Merten M, Pakala R, Thiagarajan P, Benedict CR. Platelet microparticles promote platelet interaction with subendothelial matrix in a glycoprotein IIb/IIIa-dependent mechanism. Circulation 1999; 99 (19) 2577-2582
• 73 Sprague DL, Elzey BD, Crist SA, Waldschmidt TJ, Jensen RJ, Ratliff TL. Platelet-mediated modulation of adaptive immunity: unique delivery of CD154 signal by platelet-derived membrane vesicles. Blood 2008; 111 (10) 5028-5036
• 74 Nomura S, Fujita S, Nakanishi T. et al. Platelet-derived microparticles cause CD154-dependent activation of dendritic cells. Platelets 2012; 23 (01) 81-82
• 75 Brown GT, McIntyre TM. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles. J Immunol 2011; 186 (09) 5489-5496
• 76 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 (07) 1512-1518
• 77 Yin W, Ghebrehiwet B, Peerschke EI. Expression of complement components and inhibitors on platelet microparticles. Platelets 2008; 19 (03) 225-233
• 78 Clawson CC, White JG. Platelet interaction with bacteria. I. Reaction phases and effects of inhibitors. Am J Pathol 1971; 65 (02) 367-380
• 79 Clawson CC, Rao GH, White JG. Platelet interaction with bacteria. IV. Stimulation of the release reaction. Am J Pathol 1975; 81 (02) 411-420
• 80 Ali RA, Wuescher LM, Worth RG. Platelets: essential components of the immune system. Curr Trends Immunol 2015; 16: 65-78
• 81 Kerrigan SW. The expanding field of platelet-bacterial interconnections. Platelets 2015; 26 (04) 293-301
• 82 Mirlashari MR, Hagberg IA, Lyberg T. Platelet-platelet and platelet-leukocyte interactions induced by outer membrane vesicles from N. meningitidis. Platelets 2002; 13 (02) 91-99
• 83 McNicol A. Bacteria-induced intracellular signalling in platelets. Platelets 2015; 26 (04) 309-316
• 84 Arman M, Krauel K, Tilley DO. et al. Amplification of bacteria-induced platelet activation is triggered by FcγRIIA, integrin αIIbβ3, and platelet factor 4. Blood 2014; 123 (20) 3166-3174
• 85 Naik UP. Bacteria exploit platelets. Blood 2014; 123 (20) 3067-3068
• 86 Clemetson KJ, Clemetson JM, Proudfoot AE, Power CA, Baggiolini M, Wells TN. Functional expression of CCR1, CCR3, CCR4, and CXCR4 chemokine receptors on human platelets. Blood 2000; 96 (13) 4046-4054
• 87 Gear AR, Camerini D. Platelet chemokines and chemokine receptors: linking hemostasis, inflammation, and host defense. Microcirculation 2003; 10 (3–4): 335-350
• 88 Del Conde I, Crúz MA, Zhang H, López JA, Afshar-Kharghan V. Platelet activation leads to activation and propagation of the complement system. J Exp Med 2005; 201 (06) 871-879
• 89 Peerschke EIB, Yin W, Ghebrehiwet B. Platelet mediated complement activation. Adv Exp Med Biol 2008; 632: 81-91
• 90 Cognasse F, Hamzeh H, Chavarin P, Acquart S, Genin C, Garraud O. Evidence of Toll-like receptor molecules on human platelets. Immunol Cell Biol 2005; 83 (02) 196-198
• 91 Aslam R, Speck ER, Kim M. et al. Platelet Toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-alpha production in vivo. Blood 2006; 107 (02) 637-641
• 92 Garraud O, Cognasse F. Platelet Toll-like receptor expression: the link between “danger” ligands and inflammation. Inflamm Allergy Drug Targets 2010; 9 (05) 322-333
• 93 Andonegui G, Kerfoot SM, McNagny K, Ebbert KV, Patel KD, Kubes P. Platelets express functional Toll-like receptor-4. Blood 2005; 106 (07) 2417-2423
• 94 Zhang G, Han J, Welch EJ. et al. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway. J Immunol 2009; 182 (12) 7997-8004
• 95 Berthet J, Damien P, Hamzeh-Cognasse H. et al. Human platelets can discriminate between various bacterial LPS isoforms via TLR4 signaling and differential cytokine secretion. Clin Immunol 2012; 145 (03) 189-200
• 96 Cognasse F, Hamzeh-Cognasse H, Lafarge S. et al. Toll-like receptor 4 ligand can differentially modulate the release of cytokines by human platelets. Br J Haematol 2008; 141 (01) 84-91
• 97 Cognasse F, Lafarge S, Chavarin P, Acquart S, Garraud O. Lipopolysaccharide induces sCD40L release through human platelets TLR4, but not TLR2 and TLR9. Intensive Care Med 2007; 33 (02) 382-384
• 98 Zielinski T, Wachowicz B, Saluk-Juszczak J, Kaca W. The generation of superoxide anion in blood platelets in response to different forms of Proteus mirabilis lipopolysaccharide: effects of staurosporin, wortmannin, and indomethacin. Thromb Res 2001; 103 (02) 149-155
• 99 Werts C, Tapping RI, Mathison JC. et al. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat Immunol 2001; 2 (04) 346-352
• 100 Darveau RP, Pham TT, Lemley K. et al. Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both toll-like receptors 2 and 4. Infect Immun 2004; 72 (09) 5041-5051
• 101 Erridge C, Pridmore A, Eley A, Stewart J, Poxton IR. Lipopolysaccharides of Bacteroides fragilis, Chlamydia trachomatis and Pseudomonas aeruginosa signal via toll-like receptor 2. J Med Microbiol 2004; 53 (Pt 8): 735-740
• 102 Keane C, Tilley D, Cunningham A. et al. Invasive Streptococcus pneumoniae trigger platelet activation via Toll-like receptor 2. J Thromb Haemost 2010; 8 (12) 2757-2765
• 103 Blair P, Rex S, Vitseva O. et al. Stimulation of Toll-like receptor 2 in human platelets induces a thromboinflammatory response through activation of phosphoinositide 3-kinase. Circ Res 2009; 104 (03) 346-354
• 104 Kälvegren H, Skoglund C, Helldahl C, Lerm M, Grenegård M, Bengtsson T. Toll-like receptor 2 stimulation of platelets is mediated by purinergic P2X1-dependent Ca2+ mobilisation, cyclooxygenase and purinergic P2Y1 and P2Y12 receptor activation. Thromb Haemost 2010; 103 (02) 398-407
• 105 Ward JR, Bingle L, Judge HM. et al. Agonists of toll-like receptor (TLR)2 and TLR4 are unable to modulate platelet activation by adenosine diphosphate and platelet activating factor. Thromb Haemost 2005; 94 (04) 831-838
• 106 Czapiga M, Gao JL, Kirk A, Lekstrom-Himes J. Human platelets exhibit chemotaxis using functional N-formyl peptide receptors. Exp Hematol 2005; 33 (01) 73-84
• 107 Lourbakos A, Yuan YP, Jenkins AL. et al. Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: a new trait in microbial pathogenicity. Blood 2001; 97 (12) 3790-3797
• 108 Pham K, Feik D, Hammond BF, Rams TE, Whitaker EJ. Aggregation of human platelets by gingipain-R from Porphyromonas gingivalis cells and membrane vesicles. Platelets 2002; 13 (01) 21-30
• 109 Bhakdi S, Muhly M, Mannhardt U. et al. Staphylococcal alpha toxin promotes blood coagulation via attack on human platelets. J Exp Med 1988; 168 (02) 527-542
• 110 Arvand M, Bhakdi S, Dahlbäck B, Preissner KT. Staphylococcus aureus alpha-toxin attack on human platelets promotes assembly of the prothrombinase complex. J Biol Chem 1990; 265 (24) 14377-14381
• 111 Hu H, Armstrong PCJ, Khalil E. et al. GPVI and GPIbα mediate staphylococcal superantigen-like protein 5 (SSL5) induced platelet activation and direct toward glycans as potential inhibitors. PLoS One 2011; 6 (04) e19190
• 112 de Haas CJC, Weeterings C, Vughs MM, de Groot PG, Van Strijp JA, Lisman T. Staphylococcal superantigen-like 5 activates platelets and supports platelet adhesion under flow conditions, which involves glycoprotein Ibα and αIIbβ3. J Thromb Haemost 2009; 7 (11) 1867-1874
• 113 Niemann S, Bertling A, Brodde MF. et al. Panton-Valentine leukocidin associated with S. aureus osteomyelitis activates platelets via neutrophil secretion products. Sci Rep 2018; 8 (01) 2185
• 114 Bertling A, Niemann S, Hussain M. et al. Staphylococcal extracellular adherence protein induces platelet activation by stimulation of thiol isomerases. Arterioscler Thromb Vasc Biol 2012; 32 (08) 1979-1990
• 115 Palma M, Shannon O, Quezada HC, Berg A, Flock JI. Extracellular fibrinogen-binding protein, Efb, from Staphylococcus aureus blocks platelet aggregation due to its binding to the alpha-chain. J Biol Chem 2001; 276 (34) 31691-31697
• 116 Shannon O, Flock JI. Extracellular fibrinogen binding protein, Efb, from Staphylococcus aureus binds to platelets and inhibits platelet aggregation. Thromb Haemost 2004; 91 (04) 779-789
• 117 Shannon O, Uekötter A, Flock JI. Extracellular fibrinogen binding protein, Efb, from Staphylococcus aureus as an antiplatelet agent in vivo. Thromb Haemost 2005; 93 (05) 927-931
• 118 Tran U, Boyle T, Shupp JW, Hammamieh R, Jett M. Staphylococcal enterotoxin B initiates protein kinase C translocation and eicosanoid metabolism while inhibiting thrombin-induced aggregation in human platelets. Mol Cell Biochem 2006; 288 (1–2): 171-178
• 119 Waller AK, Sage T, Kumar C, Carr T, Gibbins JM, Clarke SR. Staphylococcus aureus lipoteichoic acid inhibits platelet activation and thrombus formation via the Paf receptor. J Infect Dis 2013; 208 (12) 2046-2057
• 120 Beachey EH, Chiang TM, Ofek I, Kang AH. Interaction of lipoteichoic acid of group A streptococci with human platelets. Infect Immun 1977; 16 (02) 649-654
• 121 Wu BQ, Zhi MJ, Liu H, Huang J, Zhou YQ, Zhang TT. Inhibitory effects of lipoteichoic acid from Staphylococcus aureus on platelet function and platelet-monocyte aggregation. Inflamm Res 2011; 60 (08) 775-782
• 122 Sheu JR, Lee CR, Lin CH. et al. Mechanisms involved in the antiplatelet activity of Staphylococcus aureus lipoteichoic acid in human platelets. Thromb Haemost 2000; 83 (05) 777-784
• 123 Chugh TD, Burns GJ, Shuhaiber HJ, Bahr GM. Adherence of Staphylococcus epidermidis to fibrin-platelet clots in vitro mediated by lipoteichoic acid. Infect Immun 1990; 58 (02) 315-319
• 124 Vanassche T, Kauskot A, Verhaegen J. et al. Fibrin formation by staphylothrombin facilitates Staphylococcus aureus-induced platelet aggregation. Thromb Haemost 2012; 107 (06) 1107-1121
• 125 Suehiro A, Oura Y, Ueda M, Kakishita E. Inhibitory effect of staphylokinase on platelet aggregation. Thromb Haemost 1993; 70 (05) 834-837
• 126 Kraemer BF, Campbell RA, Schwertz H. et al. Bacteria differentially induce degradation of Bcl-xL, a survival protein, by human platelets. Blood 2012; 120 (25) 5014-5020
• 127 Towhid ST, Nega M, Schmidt EM. et al. Stimulation of platelet apoptosis by peptidoglycan from Staphylococcus aureus 113. Apoptosis 2012; 17 (09) 998-1008
• 128 Bhakdi S, Tranum-Jensen J. Alpha-toxin of Staphylococcus aureus. Microbiol Rev 1991; 55 (04) 733-751
• 129 Guo Y-L, Liu D-Q, Bian Z, Zhang C-Y, Zen K. Down-regulation of platelet surface CD47 expression in Escherichia coli O157:H7 infection-induced thrombocytopenia. PLoS One 2009; 4 (09) e7131
• 130 Johnson MK, Boese-Marrazzo D, Pierce Jr WA. Effects of pneumolysin on human polymorphonuclear leukocytes and platelets. Infect Immun 1981; 34 (01) 171-176
• 131 Bayer AS, Ramos MD, Menzies BE, Yeaman MR, Shen AJ, Cheung AL. Hyperproduction of alpha-toxin by Staphylococcus aureus results in paradoxically reduced virulence in experimental endocarditis: a host defense role for platelet microbicidal proteins. Infect Immun 1997; 65 (11) 4652-4660
• 132 Bryant AE, Bayer CR, Chen RY, Guth PH, Wallace RJ, Stevens DL. Vascular dysfunction and ischemic destruction of tissue in Streptococcus pyogenes infection: the role of streptolysin O-induced platelet/neutrophil complexes. J Infect Dis 2005; 192 (06) 1014-1022
• 133 Bryant AE, Chen RY, Nagata Y. et al. Clostridial gas gangrene. II. Phospholipase C-induced activation of platelet gpIIbIIIa mediates vascular occlusion and myonecrosis in Clostridium perfringens gas gangrene. J Infect Dis 2000; 182 (03) 808-815
• 134 Khan SY, Kelher MR, Heal JM. et al. Soluble CD40 ligand accumulates in stored blood components, primes neutrophils through CD40, and is a potential cofactor in the development of transfusion-related acute lung injury. Blood 2006; 108 (07) 2455-2462
• 135 Chakrabarti S, Varghese S, Vitseva O, Tanriverdi K, Freedman JE. CD40 ligand influences platelet release of reactive oxygen intermediates. Arterioscler Thromb Vasc Biol 2005; 25 (11) 2428-2434
• 136 Youssefian T, Drouin A, Massé JM, Guichard J, Cramer EM. Host defense role of platelets: engulfment of HIV and Staphylococcus aureus occurs in a specific subcellular compartment and is enhanced by platelet activation. Blood 2002; 99 (11) 4021-4029
• 137 Li X, Iwai T, Nakamura H. et al. An ultrastructural study of Porphyromonas gingivalis-induced platelet aggregation. Thromb Res 2008; 122 (06) 810-819
• 138 White JG. Platelets are covercytes, not phagocytes: uptake of bacteria involves channels of the open canalicular system. Platelets 2005; 16 (02) 121-131
• 139 Boukour S, Cramer EM. Platelet interaction with bacteria. Platelets 2005; 16 (3–4): 215-217
• 140 Worth RG, Chien CD, Chien P, Reilly MP, McKenzie SE, Schreiber AD. Platelet FcgammaRIIA binds and internalizes IgG-containing complexes. Exp Hematol 2006; 34 (11) 1490-1495
• 141 Antczak AJ, Vieth JA, Singh N, Worth RG. Internalization of IgG-coated targets results in activation and secretion of soluble CD40 ligand and RANTES by human platelets. Clin Vaccine Immunol 2011; 18 (02) 210-216
• 142 Semple JW, Aslam R, Kim M, Speck ER, Freedman J. Platelet-bound lipopolysaccharide enhances Fc receptor-mediated phagocytosis of IgG-opsonized platelets. Blood 2007; 109 (11) 4803-4805
• 143 Huang Z-Y, Chien P, Indik ZK, Schreiber AD. Human platelet FcγRIIA and phagocytes in immune-complex clearance. Mol Immunol 2011; 48 (04) 691-696
• 144 Maugeri N, Rovere-Querini P, Evangelista V. et al. Neutrophils phagocytose activated platelets in vivo: a phosphatidylserine, P-selectin, and β2 integrin-dependent cell clearance program. Blood 2009; 113 (21) 5254-5265
• 145 Manfredi AA, Rovere-Querini P, Maugeri N. Dangerous connections: neutrophils and the phagocytic clearance of activated platelets. Curr Opin Hematol 2010; 17 (01) 3-8
• 146 Maugeri N, Cattaneo M, Rovere-Querini P, Manfredi AA. Platelet clearance by circulating leukocytes: a rare event or a determinant of the “immune continuum”?. Platelets 2014; 25 (03) 224-225
• 147 Terada H, Baldini M, Ebbe S, Madoff MA. Interaction of influenza virus with blood platelets. Blood 1966; 28 (02) 213-228
• 148 Danon D, Jerushalmy Z, De Vries A. Incorporation of influenza virus in human blood platelets in vitro. Electron microscopical observation. Virology 1959; 9 (04) 719-722
• 149 Zucker-Franklin D, Seremetis S, Zheng ZY. Internalization of human immunodeficiency virus type I and other retroviruses by megakaryocytes and platelets. Blood 1990; 75 (10) 1920-1923
• 150 Beck Z, Jagodzinski LL, Eller MA. et al. Platelets and erythrocyte-bound platelets bind infectious HIV-1 in plasma of chronically infected patients. PLoS One 2013; 8 (11) e81002
• 151 Hamaia S, Li C, Allain J-P. The dynamics of hepatitis C virus binding to platelets and 2 mononuclear cell lines. Blood 2001; 98 (08) 2293-2300
• 152 Pugliese A, Gennero L, Cutufia M. et al. HCV infective virions can be carried by human platelets. Cell Biochem Funct 2004; 22 (06) 353-358
• 153 de Almeida AJ, Campos-de-Magalhães M, Brandão-Mello CE. et al. Detection of hepatitis C virus in platelets: evaluating its relationship to antiviral therapy outcome. Hepatogastroenterology 2009; 56 (90) 429-436
• 154 Forghani B, Schmidt NJ. Association of herpes simplex virus with platelets of experimentally infected mice. Arch Virol 1983; 76 (03) 269-274
• 155 Bik T, Sarov I, Livne A. Interaction between vaccinia virus and human blood platelets. Blood 1982; 59 (03) 482-487
• 156 Wang S, He R, Patarapotikul J, Innis BL, Anderson R. Antibody-enhanced binding of dengue-2 virus to human platelets. Virology 1995; 213 (01) 254-257
• 157 Ghosh K, Gangodkar S, Jain P. et al. Imaging the interaction between dengue 2 virus and human blood platelets using atomic force and electron microscopy. J Electron Microsc (Tokyo) 2008; 57 (03) 113-118
• 158 Noisakran S, Gibbons RV, Songprakhon P. et al. Detection of dengue virus in platelets isolated from dengue patients. Southeast Asian J Trop Med Public Health 2009; 40 (02) 253-262
• 159 Alonso AL, Cox D. Platelet interactions with viruses and parasites. Platelets 2015; 26 (04) 317-323
• 160 Boilard E, Paré G, Rousseau M. et al. Influenza virus H1N1 activates platelets through FcγRIIA signaling and thrombin generation. Blood 2014; 123 (18) 2854-2863
• 161 Moi ML, Lim CK, Takasaki T, Kurane I. Involvement of the Fc gamma receptor IIA cytoplasmic domain in antibody-dependent enhancement of dengue virus infection. J Gen Virol 2010; 91 (Pt 1): 103-111
• 162 Rodenhuis-Zybert IA, van der Schaar HM, da Silva Voorham JM. et al. Immature dengue virus: a veiled pathogen?. PLoS Pathog 2010; 6 (01) e1000718
• 163 Negrotto S, Jaquenod de Giusti C, Rivadeneyra L. et al. Platelets interact with coxsackieviruses B and have a critical role in the pathogenesis of virus-induced myocarditis. J Thromb Haemost 2015; 13 (02) 271-282
• 164 Mackow ER, Gavrilovskaya IN. Cellular receptors and hantavirus pathogenesis. Curr Top Microbiol Immunol 2001; 256: 91-115
• 165 Assinger A, Kral JB, Yaiw KC. et al. Human cytomegalovirus-platelet interaction triggers toll-like receptor 2-dependent proinflammatory and proangiogenic responses. Arterioscler Thromb Vasc Biol 2014; 34 (04) 801-809
• 166 Koupenova M, Vitseva O, MacKay CR. et al. Platelet-TLR7 mediates host survival and platelet count during viral infection in the absence of platelet-dependent thrombosis. Blood 2014; 124 (05) 791-802
• 167 Koupenova M, Corkrey HA, Vitseva O. et al. The role of platelets in mediating a response to human influenza infection. Nat Commun 2019; 10 (01) 1780
• 168 Thon JN, Peters CG, Machlus KR. et al. T granules in human platelets function in TLR9 organization and signaling. J Cell Biol 2012; 198 (04) 561-574
• 169 Mesquita EC, Hottz ED, Amancio RT. et al. Persistent platelet activation and apoptosis in virologically suppressed HIV-infected individuals. Sci Rep 2018; 8 (01) 14999
• 170 Li J, van der Wal DE, Zhu G. et al. Desialylation is a mechanism of Fc-independent platelet clearance and a therapeutic target in immune thrombocytopenia. Nat Commun 2015; 6: 7737
• 171 Sørensen AL, Rumjantseva V, Nayeb-Hashemi S. et al. Role of sialic acid for platelet life span: exposure of beta-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptor-expressing liver macrophages and hepatocytes. Blood 2009; 114 (08) 1645-1654
• 172 Maurice A, Marchand-Arvier M, Edert D, Le Faou A, Gondrexon G, Vigneron C. The virucidal effect of platelet concentrates: preliminary study and first conclusions. Platelets 2002; 13 (04) 219-222
• 173 Chabert A, Hamzeh-Cognasse H, Pozzetto B. et al. Human platelets and their capacity of binding viruses: meaning and challenges?. BMC Immunol 2015; 16: 26
• 174 Boukour S, Massé JM, Bénit L, Dubart-Kupperschmitt A, Cramer EM. Lentivirus degradation and DC-SIGN expression by human platelets and megakaryocytes. J Thromb Haemost 2006; 4 (02) 426-435
• 175 Jansen G, Low H, van den Brand J, van Riel D, van der Vries E. Uptake of influenza virus by platelets occurs via phagocytosis. Blood 2017; 130 (Suppl. 01) 4834
• 176 Jansen AJG, Low HZ, van den Brand J, van Riel D, Osterhaus A, van der Vries E. Platelets can phagocytose influenza virus which may contribute to the occurrence of thrombocytopenia during influenza infection. Blood 2016; 128 (22) 1358
• 177 Kullaya VI, de Mast Q, van der Ven A. et al. Platelets modulate innate immune response against human respiratory syncytial virus in vitro. Viral Immunol 2017; 30 (08) 576-581
• 178 Alonzo MT, Lacuesta TL, Dimaano EM. et al. Platelet apoptosis and apoptotic platelet clearance by macrophages in secondary dengue virus infections. J Infect Dis 2012; 205 (08) 1321-1329
• 179 Stone D, Liu Y, Shayakhmetov D, Li Z-Y, Ni S, Lieber A. Adenovirus-platelet interaction in blood causes virus sequestration to the reticuloendothelial system of the liver. J Virol 2007; 81 (09) 4866-4871
• 180 Trier DA, Gank KD, Kupferwasser D. et al. Platelet antistaphylococcal responses occur through P2X1 and P2Y12 receptor-induced activation and kinocidin release. Infect Immun 2008; 76 (12) 5706-5713
• 181 White JG. Why human platelets fail to kill bacteria. Platelets 2006; 17 (03) 191-200
• 182 Coburn J, Leong JM, Erban JK. Integrin alpha IIb beta 3 mediates binding of the Lyme disease agent Borrelia burgdorferi to human platelets. Proc Natl Acad Sci U S A 1993; 90 (15) 7059-7063
• 183 Kälvegren H, Majeed M, Bengtsson T. Chlamydia pneumoniae binds to platelets and triggers P-selectin expression and aggregation: a causal role in cardiovascular disease?. Arterioscler Thromb Vasc Biol 2003; 23 (09) 1677-1683
• 184 Byrne MF, Kerrigan SW, Corcoran PA. et al. Helicobacter pylori binds von Willebrand factor and interacts with GPIb to induce platelet aggregation. Gastroenterology 2003; 124 (07) 1846-1854
• 185 Naito M, Sakai E, Shi Y. et al. Porphyromonas gingivalis-induced platelet aggregation in plasma depends on Hgp44 adhesin but not Rgp proteinase. Mol Microbiol 2006; 59 (01) 152-167
• 186 Pietrocola G, Schubert A, Visai L. et al. FbsA, a fibrinogen-binding protein from Streptococcus agalactiae, mediates platelet aggregation. Blood 2005; 105 (03) 1052-1059
• 187 Kerrigan SW, Clarke N, Loughman A, Meade G, Foster TJ, Cox D. Molecular basis for Staphylococcus aureus-mediated platelet aggregate formation under arterial shear in vitro. Arterioscler Thromb Vasc Biol 2008; 28 (02) 335-340
• 188 Loughman A, Fitzgerald JR, Brennan MP. et al. Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol Microbiol 2005; 57 (03) 804-818
• 189 Miajlovic H, Loughman A, Brennan M, Cox D, Foster TJ. Both complement- and fibrinogen-dependent mechanisms contribute to platelet aggregation mediated by Staphylococcus aureus clumping factor B. Infect Immun 2007; 75 (07) 3335-3343
• 190 Fitzgerald JR, Loughman A, Keane F. et al. Fibronectin-binding proteins of Staphylococcus aureus mediate activation of human platelets via fibrinogen and fibronectin bridges to integrin GPIIb/IIIa and IgG binding to the FcgammaRIIa receptor. Mol Microbiol 2006; 59 (01) 212-230
• 191 O'Brien L, Kerrigan SW, Kaw G. et al. Multiple mechanisms for the activation of human platelet aggregation by Staphylococcus aureus: roles for the clumping factors ClfA and ClfB, the serine-aspartate repeat protein SdrE and protein A. Mol Microbiol 2002; 44 (04) 1033-1044
• 192 Herrmann M, Suchard SJ, Boxer LA, Waldvogel FA, Lew PD. Thrombospondin binds to Staphylococcus aureus and promotes staphylococcal adherence to surfaces. Infect Immun 1991; 59 (01) 279-288
• 193 Herrmann M, Lai QJ, Albrecht RM, Mosher DF, Proctor RA. Adhesion of Staphylococcus aureus to surface-bound platelets: role of fibrinogen/fibrin and platelet integrins. J Infect Dis 1993; 167 (02) 312-322
• 194 Bayer AS, Sullam PM, Ramos M, Li C, Cheung AL, Yeaman MR. Staphylococcus aureus induces platelet aggregation via a fibrinogen-dependent mechanism which is independent of principal platelet glycoprotein IIb/IIIa fibrinogen-binding domains. Infect Immun 1995; 63 (09) 3634-3641
• 195 Hawiger J, Steckley S, Hammond D. et al. Staphylococci-induced human platelet injury mediated by protein A and immunoglobulin G Fc fragment receptor. J Clin Invest 1979; 64 (04) 931-937
• 196 Nguyen T, Ghebrehiwet B, Peerschke EIB. Staphylococcus aureus protein A recognizes platelet gC1qR/p33: a novel mechanism for staphylococcal interactions with platelets. Infect Immun 2000; 68 (04) 2061-2068
• 197 Zapotoczna M, Jevnikar Z, Miajlovic H, Kos J, Foster TJ. Iron-regulated surface determinant B (IsdB) promotes Staphylococcus aureus adherence to and internalization by non-phagocytic human cells. Cell Microbiol 2013; 15 (06) 1026-1041
• 198 Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, Foster TJ. Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 2010; 156 (Pt 3): 920-928
• 199 O'Seaghdha M, van Schooten CJ, Kerrigan SW. et al. Staphylococcus aureus protein A binding to von Willebrand factor A1 domain is mediated by conserved IgG binding regions. FEBS J 2006; 273 (21) 4831-4841
• 200 Hartleib J, Köhler N, Dickinson RB. et al. Protein A is the von Willebrand factor binding protein on Staphylococcus aureus. Blood 2000; 96 (06) 2149-2156
• 201 Sjöbring U, Ringdahl U, Ruggeri ZM. Induction of platelet thrombi by bacteria and antibodies. Blood 2002; 100 (13) 4470-4477
• 202 Brennan MP, Loughman A, Devocelle M. et al. Elucidating the role of Staphylococcus epidermidis serine-aspartate repeat protein G in platelet activation. J Thromb Haemost 2009; 7 (08) 1364-1372
• 203 Petersen HJ, Keane C, Jenkinson HF. et al. Human platelets recognize a novel surface protein, PadA, on Streptococcus gordonii through a unique interaction involving fibrinogen receptor GPIIbIIIa. Infect Immun 2010; 78 (01) 413-422
• 204 Keane C, Petersen H, Reynolds K. et al. Mechanism of outside-in αIIbβ3-mediated activation of human platelets by the colonizing Bacterium, Streptococcus gordonii. Arterioscler Thromb Vasc Biol 2010; 30 (12) 2408-2415
• 205 Takamatsu D, Bensing BA, Cheng H. et al. Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibalpha. Mol Microbiol 2005; 58 (02) 380-392
• 206 Kerrigan SW, Jakubovics NS, Keane C. et al. Role of Streptococcus gordonii surface proteins SspA/SspB and Hsa in platelet function. Infect Immun 2007; 75 (12) 5740-5747
• 207 Mitchell J, Tristan A, Foster TJ. Characterization of the fibrinogen-binding surface protein Fbl of Staphylococcus lugdunensis. Microbiology 2004; 150 (Pt 11): 3831-3841
• 208 Seo HS, Xiong YQ, Mitchell J, Seepersaud R, Bayer AS, Sullam PM. Bacteriophage lysin mediates the binding of streptococcus mitis to human platelets through interaction with fibrinogen. PLoS Pathog 2010; 6 (08) e1001047
• 209 Mitchell J, Sullam PM. Streptococcus mitis phage-encoded adhesins mediate attachment to alpha2-8-linked sialic acid residues on platelet membrane gangliosides. Infect Immun 2009; 77 (08) 3485-3490
• 210 Tilley DO, Arman M, Smolenski A. et al. Glycoprotein Ibα and FcγRIIa play key roles in platelet activation by the colonizing bacterium, Streptococcus oralis. J Thromb Haemost 2013; 11 (05) 941-950
• 211 Anderson R, Feldman C. Review manuscript: mechanisms of platelet activation by the pneumococcus and the role of platelets in community-acquired pneumonia. J Infect 2017; 75 (06) 473-485
• 212 Binsker U, Kohler TP, Krauel K, Kohler S, Schwertz H, Hammerschmidt S. Pneumococcal adhesins PavB and PspC are important for the interplay with human thrombospondin-1. J Biol Chem 2015; 290 (23) 14542-14555
• 213 Binsker U, Kohler TP, Krauel K. et al. Serotype 3 pneumococci sequester platelet-derived human thrombospondin-1 via the adhesin and immune evasion protein Hic. J Biol Chem 2017; 292 (14) 5770-5783
• 214 Svensson L, Baumgarten M, Mörgelin M, Shannon O. Platelet activation by Streptococcus pyogenes leads to entrapment in platelet aggregates, from which bacteria subsequently escape. Infect Immun 2014; 82 (10) 4307-4314
• 215 Ford I, Douglas CW, Cox D, Rees DG, Heath J, Preston FE. The role of immunoglobulin G and fibrinogen in platelet aggregation by Streptococcus sanguis. Br J Haematol 1997; 97 (04) 737-746
• 216 Plummer C, Wu H, Kerrigan SW, Meade G, Cox D, Ian Douglas CW. A serine-rich glycoprotein of Streptococcus sanguis mediates adhesion to platelets via GPIb. Br J Haematol 2005; 129 (01) 101-109
• 217 Kerrigan SW, Douglas I, Wray A. et al. A role for glycoprotein Ib in Streptococcus sanguis-induced platelet aggregation. Blood 2002; 100 (02) 509-516
• 218 Zhang Y, Bergelson JM. Adenovirus receptors. J Virol 2005; 79 (19) 12125-12131
• 219 Eggerman TL, Mondoro TH, Lozier JN, Vostal JG. Adenoviral vectors do not induce, inhibit, or potentiate human platelet aggregation. Hum Gene Ther 2002; 13 (01) 125-128
• 220 Jin YY, Yu XN, Qu ZY. et al. Adenovirus type 3 induces platelet activation in vitro. Mol Med Rep 2014; 9 (01) 370-374
• 221 Othman M, Labelle A, Mazzetti I, Elbatarny HS, Lillicrap D. Adenovirus-induced thrombocytopenia: the role of von Willebrand factor and P-selectin in mediating accelerated platelet clearance. Blood 2007; 109 (07) 2832-2839
• 222 Simon AY, Sutherland MR, Pryzdial ELG. Dengue virus binding and replication by platelets. Blood 2015; 126 (03) 378-385
• 223 Hottz ED, Oliveira MF, Nunes PC. et al. Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases. J Thromb Haemost 2013; 11 (05) 951-962
• 224 Alvarez CP, Lasala F, Carrillo J, Muñiz O, Corbí AL, Delgado R. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J Virol 2002; 76 (13) 6841-6844
• 225 Nelsen-Salz B, Eggers HJ, Zimmermann H. Integrin alpha(v)beta3 (vitronectin receptor) is a candidate receptor for the virulent echovirus 9 strain Barty. J Gen Virol 1999; 80 (Pt 9): 2311-2313
• 226 Nunez D, Charriaut-Marlangue C, Barel M, Benveniste J, Frade R. Activation of human platelets through gp140, the C3d/EBV receptor (CR2). Eur J Immunol 1987; 17 (04) 515-520
• 227 Gavrilovskaya IN, Gorbunova EE, Mackow ER. Pathogenic hantaviruses direct the adherence of quiescent platelets to infected endothelial cells. J Virol 2010; 84 (09) 4832-4839
• 228 Zahn A, Jennings N, Ouwehand WH, Allain JP. Hepatitis C virus interacts with human platelet glycoprotein VI. J Gen Virol 2006; 87 (Pt 8): 2243-2251
• 229 Kowalska MA, Ratajczak J, Hoxie J. et al. Megakaryocyte precursors, megakaryocytes and platelets express the HIV co-receptor CXCR4 on their surface: determination of response to stromal-derived factor-1 by megakaryocytes and platelets. Br J Haematol 1999; 104 (02) 220-229
• 230 Chaipan C, Soilleux EJ, Simpson P. et al. DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol 2006; 80 (18) 8951-8960
• 231 Gianni T, Leoni V, Chesnokova LS, Hutt-Fletcher LM, Campadelli-Fiume G. αvβ3-integrin is a major sensor and activator of innate immunity to herpes simplex virus-1. Proc Natl Acad Sci U S A 2012; 109 (48) 19792-19797
• 232 Triantafilou K, Triantafilou M, Takada Y, Fernandez N. Human parechovirus 1 utilizes integrins alphavbeta3 and alphavbeta1 as receptors. J Virol 2000; 74 (13) 5856-5862
• 233 Shimojima M, Ströher U, Ebihara H, Feldmann H, Kawaoka Y. Identification of cell surface molecules involved in dystroglycan-independent Lassa virus cell entry. J Virol 2012; 86 (04) 2067-2078
• 234 Coulson BS, Londrigan SL, Lee DJ. Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proc Natl Acad Sci U S A 1997; 94 (10) 5389-5394
• 235 Fleming FE, Graham KL, Takada Y, Coulson BS. Determinants of the specificity of rotavirus interactions with the alpha2beta1 integrin. J Biol Chem 2011; 286 (08) 6165-6174