References
- Koupenova M, Clancy L, Corkrey HA, Freedman JE. 2018. Circulating platelets as mediators of immunity, inflammation, and thrombosis. Circ Res. 122:337–351. https://doi.org/10.1161/CIRCRESAHA.117.310795.
- Dib PRB, Quirino-Teixeira AC, Merij LB, Pinheiro MBM, Rozini SV, Andrade FB, et al. 2020. Innate immune receptors in platelets and platelet-leukocyte interactions [Internet]. J Leukoc Biol. 108:1157–1182. https://doi.org/10.1002/JLB.4MR0620-701R.
- Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. 2007. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 13:463–469. https://doi.org/10.1038/nm1565
- Bournazos S, Rennie J, Hart SP, Fox KAA, Dransfield I. 2008. Monocyte functional responsiveness after PSGL-1-mediated platelet adhesion is dependent on platelet activation status. Arterioscler Thromb Vasc Biol. 28:1491–1498. https://doi.org/10.1161/ATVBAHA.108.167601.
- Moore KL, Stults NL, Diaz S, Smith DF, Cummings RD, Varki A, et al. 1992. Identification of a specific glycoprotein ligand for P-selectin (CD62) on myeloid cells. J Cell Biol. 118:445–456. https://doi.org/10.1083/jcb.118.2.445
- Simon DI, Chen Z, Xu H, Li CQ, Dong JF, McIntire LV, et al. 2000. Platelet glycoprotein Ibα is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J Exp Med. 192:193–204. https://doi.org/10.1084/jem.192.2.193
- Ehlers R, Ustinov V, Chen Z, Zhang X, Rao R, Luscinskas FW, et al. 2003. Targeting platelet-leukocyte interactions: identification of the integrin Mac-1 binding site for the platelet counter receptor glycoprotein Ibα. J Exp Med. 198:1077–1088. https://doi.org/10.1084/jem.20022181
- Flick MJ, LaJeunesse CM, Talmage KE, Witte DP, Palumbo JS, Pinkerton MD, et al. 2007. Fibrin(ogen) exacerbates inflammatory joint disease through a mechanism linked to the integrin αMβ2 binding motif. J Clin Invest. 117:3224–3235. https://doi.org/10.1172/JCI30134
- Koupenova M, Vitseva O, MacKay CR, Beaulieu LM, Benjamin EJ, Mick E, et al. 2014. Platelet-TLR7 mediates host survival and platelet count during viral infection in the absence of platelet-dependent thrombosis. Blood. 124:791–802. https://doi.org/10.1182/blood-2013-11-536003
- Koupenova M, Corkrey HA, Vitseva O, Manni G, Pang CJ, Clancy L, et al. 2019. The role of platelets in mediating a response to human influenza infection. Nat Commun. 10:1780. https://doi.org/10.1038/s41467-019-09607-x
- Etulain J, Martinod K, Wong SL, Cifuni SM, Schattner M, Wagner DD. 2015. P-selectin promotes neutrophil extracellular trap formation in mice. Blood. 126:242–246. https://doi.org/10.1182/blood-2015-01-624023.
- Hurley SM, Kahn F, Nordenfelt P, Mörgelin M, Sørensen OE, Shannon O. 2015. Platelet-dependent neutrophil function is dysregulated by M protein from Streptococcus pyogenes. Infect Immun. 83:3515–3525. https://doi.org/10.1128/IAI.00508-15.
- Weyrich AS, Elstad MR, McEver RP, McIntyre TM, Moore KL, Morrissey JH, et al. 1996. Activated platelets signal chemokine synthesis by human monocytes. J Clin Invest. 97:1525–1534. https://doi.org/10.1172/JCI118575
- Hottz ED, Medeiros-de-Moraes IM, Vieira-de-Abreu A, de Assis EF, Vals-de-Souza R, Castro-Faria-Neto HC, et al. 2014. Platelet activation and apoptosis modulate monocyte inflammatory responses in dengue. J Immunol. 193:1864–1872. https://doi.org/10.4049/jimmunol.1400091
- Dixon DA, Tolley ND, Bemis-Standoli K, Martinez ML, Weyrich AS, Morrow JD, et al. 2006. Expression of COX-2 in platelet-monocyte interactions occurs via combinatorial regulation involving adhesion and cytokine signaling. J Clin Invest. 116:2727–2738. https://doi.org/10.1172/JCI27209.
- Hottz ED, Bozza FA, Bozza PT. 2018. Platelets in immune response to virus and immunopathology of viral infections. Front Med. 5:121.
- Hottz ED, Azevedo-Quintanilha IG, Palhinha L, Teixeira L, Barreto EA, Pão CRR, et al. 2020. Platelet activation and platelet-monocyte aggregate formation trigger tissue factor expression in patients with severe COVID-19. Blood. 136:1330–1341. https://doi.org/10.1182/blood.2020007252
- Singh MV, Davidson DC, Jackson JW, Singh VB, Silva J, Ramirez SH, et al. 2014. Characterization of platelet–monocyte complexes in HIV-1–infected individuals: possible role in HIV-associated neuroinflammation. J Immunol. 192:4674–4684. https://doi.org/10.4049/jimmunol.1302318
- Elzey BD, Tian J, Jensen RJ, Swanson AK, Lees JR, Lentz SR, et al. 2003. Platelet-mediated modulation of adaptive immunity: a communication link between innate and adaptive immune compartments. Immunity. 19:9–19. https://doi.org/10.1016/S1074-7613(03)00177-8
- Rossaint J, Thomas K, Mersmann S, Skupski J, Margraf A, Tekath T, et al. 2021. Platelets orchestrate the resolution of pulmonary inflammation in mice by T reg cell repositioning and macrophage education. J Exp Med. 218. https://doi.org/10.1084/jem.20201353.
- Rowley JW, Oler AJ, Tolley ND, Hunter BN, Low EN, Nix DA, et al. 2011. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood. 118:e101–11. https://doi.org/10.1182/blood-2011-03-339705
- Klockenbusch C, Walsh GM, Brown LM, Hoffman MD, Ignatchenko V, Kislinger T, et al. 2014. Global proteome analysis identifies active immunoproteasome subunits in human platelets. Mol Cell Proteomics. 13:3308–3319. https://doi.org/10.1074/mcp.M113.031757
- Chapman LM, Aggrey AA, Field DJ, Srivastava K, Ture S, Yui K, et al. 2012. Platelets present antigen in the context of MHC class I. J Immunol. 189:916–923. https://doi.org/10.4049/jimmunol.1200580
- Guo L, Shen S, Rowley JW, Tolley ND, Jia W, Manne BK, et al. 2021. Platelet MHC class I mediates CD8+ T cell suppression during sepsis. Blood. https://doi.org/10.1182/blood.2020008958.
- Chaipan C, Soilleux EJ, Simpson P, Hofmann H, Gramberg T, Marzi A, et al. 2006. DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol. 80:8951–8960. https://doi.org/10.1128/JVI.00136-06
- Simon AY, Sutherland MR, Pryzdial ELG. 2015. Dengue virus binding and replication by platelets. Blood. 126:378–385. https://doi.org/10.1182/blood-2014-09-598029.
- Quirino-Teixeira AC, Rozini SV, Barbosa-Lima G, Coelho DR, Carneiro PH, Mohana-Borges R, et al. 2020. Inflammatory signaling in dengue-infected platelets requires translation and secretion of nonstructural protein 1. Blood Adv. 4:2018–2031. https://doi.org/10.1182/bloodadvances.2019001169
- Real F, Capron C, Sennepin A, Arrigucci R, Zhu A, Sannier G, et al. 2020. Platelets from HIV-infected individuals on antiretroviral drug therapy with poor CD4+ T cell recovery can harbor replication-competent HIV despite viral suppression. Sci Transl Med. 12:eaat6263. https://doi.org/10.1126/scitranslmed.aat6263
- Simpson SR, Singh MV, Dewhurst S, Schifitto G, Maggirwar SB. 2020. Platelets function as an acute viral reservoir during HIV-1 infection by harboring virus and T-cell complex formation. Blood Adv. 4:4512–4521. https://doi.org/10.1182/bloodadvances.2020002420.
- Davidson DC, Hirschman MP, Sun A, Singh MV, Kasischke K, Maggirwar SB. 2012. Excess Soluble CD40L Contributes to Blood Brain Barrier Permeability In Vivo: implications for HIV-Associated Neurocognitive Disorders. PLoS One. 7:e51793. https://doi.org/10.1371/journal.pone.0051793.
- Wang J, Zhang W, Nardi MA, Li Z. 2011. HIV-1 Tat-induced platelet activation and release of CD154 contribute to HIV-1-associated autoimmune thrombocytopenia. J Thromb Haemost. 9:562–573. https://doi.org/10.1111/j.1538-7836.2010.04168.x.
- Auerbach DJ, Lin Y, Miao H, Cimbro R, DiFiore MJ, Gianolini ME, et al. 2012. Identification of the platelet-derived chemokine CXCL4/PF-4 as a broad-spectrum HIV-1 inhibitor. Proc Natl Acad Sci U S A. 109:9569–9574. https://doi.org/10.1073/pnas.1207314109
- Solomon Tsegaye T, Gnirß K, Rahe-Meyer N, Kiene M, Krämer-Kühl A, Behrens G, et al. 2013. Platelet activation suppresses HIV-1 infection of T cells. Retrovirology. 10:1–10. https://doi.org/10.1186/1742-4690-10-48
- Coffey MJ, Woffendin C, Phare SM, Strieter RM, Markovitz DM. 1997. RANTES inhibits HIV-1 replication in human peripheral blood monocytes and alveolar macrophages. Am J Physiol. 272:L1025–9.
- Alonzo MTG, Lacuesta TLV, Dimaano EM, Kurosu T, Suarez LC, Mapua CA, et al. 2012. Platelet Apoptosis and Apoptotic Platelet Clearance by Macrophages in Secondary Dengue Virus Infections. J Infect Dis. 205:1321–1329. https://doi.org/10.1093/infdis/jis180
- Barbosa-Lima G, Hottz ED, Assis EF, Liechocki S, Souza TML, Zimmerman GA, et al. 2020. Dengue virus-activated platelets modulate monocyte immunometabolic response through lipid droplet biogenesis and cytokine signaling. J Leukoc Biol. 108(4):1293–1306. https://doi.org/10.1002/JLB.4MA0620-658R.
- Sung P-S, Huang T-F, Hsieh S-L. 2019. Extracellular vesicles from CLEC2-activated platelets enhance dengue virus-induced lethality via CLEC5A/TLR2. Nat Commun. 10:2402. https://doi.org/10.1038/s41467-019-10360-4.
- Guo L, Feng K, Wang YC, Mei JJ, Ning RT, Zheng HW, et al. 2017. Critical role of CXCL4 in the lung pathogenesis of influenza (H1N1) respiratory infection. Mucosal Immunol. 10:1529–1541. https://doi.org/10.1038/mi.2017.1
- Skendros P, Mitsios A, Chrysanthopoulou A, Mastellos DC, Metallidis S, Rafailidis P, et al. 2020. Complement and tissue factor–enriched neutrophil extracellular traps are key drivers in COVID-19 immunothrombosis. J Clin Invest. 130:6151–6157. https://doi.org/10.1172/JCI141374
- Boukour S, Massé JM, Bénit L, Dubart-Kupperschmitt A, Cramer EM. 2006. Lentivirus degradation and DC-SIGN expression by human platelets and megakaryocytes. J Thromb Haemost. 4:426–435. https://doi.org/10.1111/j.1538-7836.2006.01749.x.
- Hottz ED, Oliveira MF, Nunes PCG, Nogueira RMR, Valls-de-Souza R, Da Poian AT, et al. 2013. Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases. J Thromb Haemost. 11:951–962. https://doi.org/10.1111/jth.12178
- Chao C-H, Wu W-C, Lai Y-C, Tsai P-J, Perng G-C, Lin Y-S, et al. 2019. Dengue virus nonstructural protein 1 activates platelets via Toll-like receptor 4, leading to thrombocytopenia and hemorrhage. Kuhn RJ, editor. PLOS Pathog. 15:e1007625. https://doi.org/10.1371/journal.ppat.1007625
- Boilard E, Paré G, Rousseau M, Cloutier N, Dubuc I, Lévesque T, et al. 2014. Influenza virus H1N1 activates platelets through FcγRIIA signaling and thrombin generation. Blood. 123:2854–2863. https://doi.org/10.1182/blood-2013-07-515536
- Chabert A, Hamzeh-Cognasse H, Pozzetto B, Cognasse F, Schattner M, Gomez RM, et al. 2015. Human platelets and their capacity of binding viruses: meaning and challenges? BMC Immunol. 16:26. https://doi.org/10.1186/s12865-015-0092-1
- Assinger A. 2014. Platelets and Infection - an Emerging Role of Platelets in Viral Infection. Front Immunol. 5:649. https://doi.org/10.3389/fimmu.2014.00649.
- Deng HK, Liu R, Ellmeier W, Choe S, Unutmaz D, Burkhart M, et al. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 381:661–666. https://doi.org/10.1038/381661a0
- Maartens G, Celum C, Lewin SR. 2014. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet. 384:258–271. https://doi.org/10.1016/S0140-6736(14)60164-1.
- Marin B, Thiébaut R, Bucher HC, Rondeau V, Costagliola D, Dorrucci M, et al. 2009. Non-AIDS-defining deaths and immunodeficiency in the era of combination antiretroviral therapy. Aids. 23:1743–1753. https://doi.org/10.1097/QAD.0b013e32832e9b78
- Goehringer F, Bonnet F, Salmon D, Cacoub P, Paye A, Chêne G, et al. 2017. Causes of Death in HIV-Infected Individuals with Immunovirologic Success in a National Prospective Survey. AIDS Res Hum Retroviruses. 33:187–193. https://doi.org/10.1089/aid.2016.0222
- Geijtenbeek TBH, Kwon DS, Torensma R, Van Vliet SJ, Van Duijnhoven GCF, Middel J, et al. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. 100:587–597. https://doi.org/10.1016/S0092-8674(00)80694-7
- Turville SG, Cameron PU, Handley A, Lin G, Pöhlmann S, Doms RW, et al. 2002. Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol. 3:975–983. https://doi.org/10.1038/ni841
- Youssefian T, Drouin A, Massé JM, Guichard J, Cramer EM. 2002. Host defense role of platelets: engulfment of HIV and Staphylococcus aureus occurs in a specific subcellular compartment and is enhanced by platelet activation. Blood. 99:4021–4029. https://doi.org/10.1182/blood-2001-12-0191.
- Holme PA, Müller F, Solum NO, Brosstad F, FrØland SS, Aukrust P. 1998. Enhanced activation of platelets with abnormal release of RANTES in human immunodeficiency virus type 1 infection. FASEB J. 12:79–90. https://doi.org/10.1096/fasebj.12.1.79.
- Mesquita EC, Hottz ED, Amancio RT, Carneiro AB, Palhinha L, Coelho LE, et al. 2018. Persistent platelet activation and apoptosis in virologically suppressed HIV-infected individuals. Sci Rep. 8:14999. https://doi.org/10.1038/s41598-018-33403-0
- Nkambule BB, Davison G, Ipp H. 2015. Platelet leukocyte aggregates and markers of platelet aggregation, immune activation and disease progression in HIV infected treatment naive asymptomatic individuals. J Thromb Thrombolysis. 40:458–467. https://doi.org/10.1007/s11239-015-1212-8.
- Singh MV, Davidson DC, Kiebala M, Maggirwar SB. 2012. Detection of circulating platelet-monocyte complexes in persons infected with human immunodeficiency virus type-1. J Virol Methods. 181:170–176. https://doi.org/10.1016/j.jviromet.2012.02.005.
- World Health Organization (WHO) and the Special Programme for Research and Tropical Diseases (TDR). Dengue case classification. In: dengue: guidelines for diagnosis, treatment, prevention and control: new edition. World Health Organization; 2009:10–12.
- Bozza FA, Cruz OG, Zagne SMO, Azeredo EL, Nogueira RMR, Assis EF, et al. 2008. Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect Dis. 8:86. https://doi.org/10.1186/1471-2334-8-86
- Zhao L, Huang X, Hong W, Qiu S, Wang J, Yu L, et al. 2016. Slow resolution of inflammation in severe adult dengue patients. BMC Infect Dis. 16:291. https://doi.org/10.1186/s12879-016-1596-x
- Mpg M, Lacerda MVG, Macedo VO, Santos JB. 2007. Thrombocytopenia in patients with dengue virus infection in the Brazilian Amazon. Platelets. 18:605–612. https://doi.org/10.1080/09537100701426604.
- de O Trugilho MR, Hottz ED, Brunoro GVF, Teixeira-Ferreira A, Carvalho PC, Salazar GA, et al. 2017. Platelet proteome reveals novel pathways of platelet activation and platelet-mediated immunoregulation in dengue. PLoS Pathog. 13:e1006385. https://doi.org/10.1371/journal.ppat.1006385
- Hottz ED, Lopes JF, Freitas C, Valls-de-Souza R, Oliveira MF, Bozza MT, et al. 2013. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation. Blood. 122:3405–3414. https://doi.org/10.1182/blood-2013-05-504449
- Matsuura C, Moraes TL, Barbosa JB, Moss MB, Siqueira MAS, Mann GE, et al. 2012. Nitric oxide activity in platelets of dengue haemorrhagic fever patients: the apparent paradoxical role of ADMA and l-NMMA. Trans R Soc Trop Med Hyg. 106:174–179. https://doi.org/10.1016/j.trstmh.2011.10.009
- Kar M, Singla M, Chandele A, Kabra SK, Lodha R, Medigeshi GR. 2017. Dengue Virus Entry and Replication Does Not Lead to Productive Infection in Platelets. Open Forum Infect Dis. 4:ofx051. https://doi.org/10.1093/ofid/ofx051.
- Ojha A, Nandi D, Batra H, Singhal R, Annarapu GK, Bhattacharyya S, et al. 2017. Platelet activation determines the severity of thrombocytopenia in dengue infection. Sci Rep. 7:41697. https://doi.org/10.1038/srep41697
- Núñez-Avellaneda D, Mosso-Pani M, Sánchez-Torres L, Castro-Mussot M, Corona-de la Peña N, Salazar M. 2018. Dengue virus induces the release of sCD40L and changes in levels of membranal CD42b and CD40L molecules in human platelets. Viruses. 10:357. https://doi.org/10.3390/v10070357.
- Tsai -J-J, Jen Y-H, Chang J-S, Hsiao H-M, Noisakran S, Perng GC. 2011. Frequency alterations in key innate immune cell components in the peripheral blood of dengue patients detected by FACS analysis. J Innate Immun. 3:530–540. https://doi.org/10.1159/000322904.
- Rondina MT, Brewster BA, Grissom CK, Zimmerman GA, Kastendieck DH, Harris ES, et al. 2012. In vivo platelet activation in critically ill patients with primary 2009 influenza A(H1N1). Chest. 141:1490–1495. https://doi.org/10.1378/chest.11-2860
- Lê VB, Schneider JG, Boergeling Y, Berri F, Ducatez M, Guerin J-L, et al. 2015. Platelet activation and aggregation promote lung inflammation and influenza virus pathogenesis. Am J Respir Crit Care Med. 191:804–819. https://doi.org/10.1164/rccm.201406-1031OC
- Tang N, Li D, Wang X, Sun Z. 2020. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost. 18:844–847. https://doi.org/10.1111/jth.14768.
- Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers DAMPJ, Kant KM, et al. 2020. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb Res.
- Nicolai L, Leunig A, Brambs S, Kaiser R, Weinberger T, Weigand M, et al. 2020. Immunothrombotic dysregulation in COVID-19 pneumonia is associated with respiratory failure and coagulopathy. Circulation. 1176–1189;142. https://doi.org/10.1161/CIRCULATIONAHA.120.048488.
- Middleton EA, He XY, Denorme F, Campbell RA, Ng D, Salvatore SP, et al. 2020. Neutrophil extracellular traps contribute to immunothrombosis in COVID-19 acute respiratory distress syndrome. Blood. 136:1169–1179. https://doi.org/10.1182/blood.2020007008
- Ackermann M, Verleden SE, Kuehnel M, Haverich A, Welte T, Laenger F, et al. 2020. Pulmonary Vascular Endothelialitis, Thrombosis, and Angiogenesis in Covid-19. N Engl J Med. NEJMoa2015432.
- Aid M, Busman-Sahay K, Vidal SJ, Maliga Z, Bondoc S, Starke C, et al. 2020. Vascular Disease and Thrombosis in SARS-CoV-2-Infected Rhesus Macaques. Cell. 183:1354–1366.e13. https://doi.org/10.1016/j.cell.2020.10.005
- McMullen PD, Cho JH, Miller JL, Husain AN, Pytel P, Krausz T. 2021. A Descriptive and Quantitative Immunohistochemical Study Demonstrating a Spectrum of Platelet Recruitment Patterns Across Pulmonary Infections Including COVID-19. Am J Clin Pathol. 155:354–363. https://doi.org/10.1093/ajcp/aqaa230.
- Nicolai L, Leunig A, Brambs S, Kaiser R, Joppich M, Hoffknecht ML, et al. 2021. Vascular neutrophilic inflammation and immunothrombosis distinguish severe COVID-19 from influenza pneumonia. J Thromb Haemost. 19:574–581. https://doi.org/10.1111/jth.15179
- Kanth Manne B, Denorme F, Middleton EA, Portier I, Rowley JW, Stubben C, et al. 2020. Platelet gene expression and function in patients with COVID-19. Blood. 136:1317–1329. https://doi.org/10.1182/blood.2020007214
- Canzano P, Brambilla M, Porro B, Cosentino N, Tortorici E, Vicini S, et al. 2021. Platelet and Endothelial Activation as Potential Mechanisms Behind the Thrombotic Complications of COVID-19 Patients. JACC Basic to Transl Sci. 6:202–218. https://doi.org/10.1016/j.jacbts.2020.12.009
- Grover SP, Mackman N. 2018. Tissue Factor: an Essential Mediator of Hemostasis and Trigger of Thrombosis. Arterioscler Thromb Vasc Biol. 38:709–725. https://doi.org/10.1161/ATVBAHA.117.309846.
- Petito E, Falcinelli E, Paliani U, Cesari E, Vaudo G, Sebastiano M, et al. 2021. Association of Neutrophil Activation, More Than Platelet Activation, With Thrombotic Complications in Coronavirus Disease 2019. J Infect Dis. 223:933–944. https://doi.org/10.1093/infdis/jiaa756