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Semin Thromb Hemost 2021; 47(04): 419-426
DOI: 10.1055/s-0041-1726033
Review Article

Platelet Function in Viral Immunity and SARS-CoV-2 Infection

Afaf Allaoui
1   Department of Biology, Faculty of Sciences, Mohammed V University, Rabat, Morocco
,
Akif A. Khawaja
2   National Heart and Lung Institute, Imperial College London, London, United Kingdom
,
Oussama Badad
1   Department of Biology, Faculty of Sciences, Mohammed V University, Rabat, Morocco
3   Department of Plant, Southern Illinois University, Carbondale, Illinois
,
Mariam Naciri
1   Department of Biology, Faculty of Sciences, Mohammed V University, Rabat, Morocco
,
Marie Lordkipanidzé
4   Research Center, Montreal Heart Institute, Montréal, Quebec, Canada
5   Faculty of pharmacy, Université de Montréal, Montréal, Québec, Canada
,
Fadila Guessous
6   Microbiology, Immunology and Cancer Biology, School of Medicine, University of Virginia, Charlottesville, Virginia
7   Department of Biological Sciences, Faculty of Medicine, Mohammed VI University of Health Sciences, Casablanca, Morocco
,
Younes Zaid
1   Department of Biology, Faculty of Sciences, Mohammed V University, Rabat, Morocco
8   Research Center of Abulcasis University of Health Sciences, Cheikh Zaïd Hospital, Rabat, Morocco
› Author Affiliations Funding None.
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Abstract

Platelets, as nonnucleated blood components, are classically recognized for their pivotal role in hemostasis. In recent years, however, accumulating evidence points to a nonhemostatic role for platelets, as active participants in the inflammatory and immune responses to microbial organisms in infectious diseases. This stems from the ability of activated platelets to secrete a plethora of immunomodulatory cytokines and chemokines, as well as directly interplaying with viral receptors. While much attention has been given to the role of the cytokine storm in the severity of the coronavirus disease 2019 (COVID-19), less is known about the contribution of platelets to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection. Here, we give a brief overview on the platelet contribution to antiviral immunity and response during SARS-CoV-2 infection.

Keywords

platelets - hemostasis - inflammation - SARS-CoV-2 - COVID-19 - viral infections

Authors' Contributions

A.A., A.A.K., O.B., M.N., M.L., F.G., and Y.Z. contributed to literature search and writing of this review. A.A.K., M.L., F.G., and Y.Z. designed the structure and content of this review. Y.Z. provided the figure. All authors approved the submitted version of the manuscript.




Publication History

Article published online:
13 April 2021

© 2021. Thieme. All rights reserved.

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  • References

  • 1 World Health Organization.. Disease outbreaks. Accessed February 5, 2021 at: https://www.who.int/emergencies/diseases/en/
  • 2 Howard DH, Scott II RD, Packard R, Jones D. The global impact of drug resistance. Clin Infect Dis 2003; 36 (Suppl. 01) S4-S10
    CrossrefPubMedSearch in Google Scholar
  • 3 Delamou A, Delvaux T, El Ayadi AM. et al. Public health impact of the 2014-2015 Ebola outbreak in West Africa: seizing opportunities for the future. BMJ Glob Health 2017; 2 (02) e000202
    CrossrefPubMedSearch in Google Scholar
  • 4 Piot P, Bartos M, Ghys PD, Walker N, Schwartländer B. The global impact of HIV/AIDS. Nature 2001; 410 (6831): 968-973
    CrossrefPubMedSearch in Google Scholar
  • 5 Hiscott J, Alexandridi M, Muscolini M. et al. The global impact of the coronavirus pandemic. Cytokine Growth Factor Rev 2020; 53: 1-9
    CrossrefPubMedSearch in Google Scholar
  • 6 Machlus KR, Italiano Jr JE. The incredible journey: from megakaryocyte development to platelet formation. J Cell Biol 2013; 201 (06) 785-796
    CrossrefPubMedSearch in Google Scholar
  • 7 Liu X, Gorzelanny C, Schneider SW. Platelets in skin autoimmune diseases. Front Immunol 2019; 10: 1453
    CrossrefPubMedSearch in Google Scholar
  • 8 Haemmerle M, Stone RL, Menter DG, Afshar-Kharghan V, Sood AK. The platelet lifeline to cancer: challenges and opportunities. Cancer Cell 2018; 33 (06) 965-983
    CrossrefPubMedSearch in Google Scholar
  • 9 Middleton E, Rondina MT. Platelets in infectious disease. Hematology (Am Soc Hematol Educ Program) 2016; 2016 (01) 256-261
    CrossrefPubMedSearch in Google Scholar
  • 10 Guo L, Rondina MT. The era of thromboinflammation: platelets are dynamic sensors and effector cells during infectious diseases. Front Immunol 2019; 10: 2204
    Search in Google Scholar
  • 11 Ribeiro LS, Migliari Branco L, Franklin BS. Regulation of innate immune responses by platelets. Front Immunol 2019; 10: 1320
    CrossrefPubMedSearch in Google Scholar
  • 12 Liu JZ, van Sommeren S, Huang H. et al; International Multiple Sclerosis Genetics Consortium, International IBD Genetics Consortium. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet 2015; 47 (09) 979-986
    CrossrefPubMedSearch in Google Scholar
  • 13 Riaz AH, Tasma BE, Woodman ME, Wooten RM, Worth RG. Human platelets efficiently kill IgG-opsonized E. coli. FEMS Immunol Med Microbiol 2012; 65 (01) 78-83
    CrossrefPubMedSearch in Google Scholar
  • 14 Martel C, Cointe S, Maurice P. et al. Requirements for membrane attack complex formation and anaphylatoxins binding to collagen-activated platelets. PLoS One 2011; 6 (04) e18812
    CrossrefPubMedSearch in Google Scholar
  • 15 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
    CrossrefPubMedSearch in Google Scholar
  • 16 Rivière C, Subra F, Cohen-Solal K. et al. Phenotypic and functional evidence for the expression of CXCR4 receptor during megakaryocytopoiesis. Blood 1999; 93 (05) 1511-1523
    CrossrefPubMedSearch in Google Scholar
  • 17 Shiraki R, Inoue N, Kawasaki S. et al. Expression of toll-like receptors on human platelets. Thromb Res 2004; 113 (06) 379-385
    CrossrefPubMedSearch in Google Scholar
  • 18 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
    CrossrefPubMedSearch in Google Scholar
  • 19 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
    CrossrefPubMedSearch in Google Scholar
  • 20 D'Atri LP, Etulain J, Rivadeneyra L. et al. Expression and functionality of toll-like receptor 3 in the megakaryocytic lineage. J Thromb Haemost 2015; 13 (05) 839-850
    CrossrefPubMedSearch in Google Scholar
  • 21 Clark SR, Ma AC, Tavener SA. et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13 (04) 463-469
    CrossrefPubMedSearch in Google Scholar
  • 22 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
    CrossrefPubMedSearch in Google Scholar
  • 23 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
    CrossrefPubMedSearch in Google Scholar
  • 24 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
    CrossrefPubMedSearch in Google Scholar
  • 25 Panigrahi S, Ma Y, Hong L. et al. Engagement of platelet toll-like receptor 9 by novel endogenous ligands promotes platelet hyperreactivity and thrombosis. Circ Res 2013; 112 (01) 103-112
    CrossrefPubMedSearch in Google Scholar
  • 26 Ojha A, Nandi D, Batra H. et al. Platelet activation determines the severity of thrombocytopenia in dengue infection. Sci Rep 2017; 7: 41697
    CrossrefPubMedSearch in Google Scholar
  • 27 Baker JV. Chronic HIV disease and activation of the coagulation system. Thromb Res 2013; 132 (05) 495-499
    CrossrefPubMedSearch in Google Scholar
  • 28 Satchell CS, O'Halloran JA, Cotter AG. et al. Increased platelet reactivity in HIV-1-infected patients receiving abacavir-containing antiretroviral therapy. J Infect Dis 2011; 204 (08) 1202-1210
    CrossrefPubMedSearch in Google Scholar
  • 29 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
    CrossrefPubMedSearch in Google Scholar
  • 30 Jansen AJG, Spaan T, Low HZ. et al. Influenza-induced thrombocytopenia is dependent on the subtype and sialoglycan receptor and increases with virus pathogenicity. Blood Adv 2020; 4 (13) 2967-2978
    CrossrefPubMedSearch in Google Scholar
  • 31 Ackermann M, Verleden SE, Kuehnel M. et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med 2020; 383 (02) 120-128
    CrossrefPubMedSearch in Google Scholar
  • 32 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
    CrossrefPubMedSearch in Google Scholar
  • 33 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
    CrossrefPubMedSearch in Google Scholar
  • 34 Banerjee M, Huang Y, Joshi S. et al. Platelets endocytose viral particles and are activated via TLR (toll-like receptor) signaling. Arterioscler Thromb Vasc Biol 2020; 40 (07) 1635-1650
    CrossrefPubMedSearch in Google Scholar
  • 35 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
    Search in Google Scholar
  • 36 Torre D, Pugliese A. Platelets and HIV-1 infection: old and new aspects. Curr HIV Res 2008; 6 (05) 411-418
    CrossrefPubMedSearch in Google Scholar
  • 37 Solomon Tsegaye T, Gnirß K, Rahe-Meyer N. et al. Platelet activation suppresses HIV-1 infection of T cells. Retrovirology 2013; 10: 48
    CrossrefPubMedSearch in Google Scholar
  • 38 Auerbach DJ, Lin Y, Miao H. et al. Identification of the platelet-derived chemokine CXCL4/PF-4 as a broad-spectrum HIV-1 inhibitor. Proc Natl Acad Sci U S A 2012; 109 (24) 9569-9574
    CrossrefPubMedSearch in Google Scholar
  • 39 Parker ZF, Rux AH, Riblett AM. et al. Platelet factor 4 inhibits and enhances HIV-1 infection in a concentration-dependent manner by modulating viral attachment. AIDS Res Hum Retroviruses 2016; 32 (07) 705-717
    CrossrefPubMedSearch in Google Scholar
  • 40 Mohan KV, Rao SS, Atreya CD. Antiviral activity of selected antimicrobial peptides against vaccinia virus. Antiviral Res 2010; 86 (03) 306-311
    CrossrefPubMedSearch in Google Scholar
  • 41 Schrottmaier WC, Salzmann M, Badrnya S. et al. Platelets mediate serological memory to neutralize viruses in vitro and in vivo. Blood Adv 2020; 4 (16) 3971-3976
    CrossrefPubMedSearch in Google Scholar
  • 42 George JN, Saucerman S, Levine SP, Knieriem LK, Bainton DF. Immunoglobulin G is a platelet alpha granule-secreted protein. J Clin Invest 1985; 76 (05) 2020-2025
    CrossrefPubMedSearch in Google Scholar
  • 43 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
    CrossrefPubMedSearch in Google Scholar
  • 44 Chapman LM, Aggrey AA, Field DJ. et al. Platelets present antigen in the context of MHC class I. J Immunol 2012; 189 (02) 916-923
    CrossrefPubMedSearch in Google Scholar
  • 45 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
    CrossrefPubMedSearch in Google Scholar
  • 46 Barbosa-Lima G, Hottz ED, de Assis EF. et al. Dengue virus-activated platelets modulate monocyte immunometabolic response through lipid droplet biogenesis and cytokine signaling. J Leukoc Biol 2020; 108 (04) 1293-1306
    CrossrefPubMedSearch in Google Scholar
  • 47 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
    CrossrefPubMedSearch in Google Scholar
  • 48 Chelucci C, Federico M, Guerriero R. et al. Productive human immunodeficiency virus-1 infection of purified megakaryocytic progenitors/precursors and maturing megakaryocytes. Blood 1998; 91 (04) 1225-1234
    CrossrefPubMedSearch in Google Scholar
  • 49 Crapnell K, Zanjani ED, Chaudhuri A, Ascensao JL, St Jeor S, Maciejewski JP. In vitro infection of megakaryocytes and their precursors by human cytomegalovirus. Blood 2000; 95 (02) 487-493
    CrossrefPubMedSearch in Google Scholar
  • 50 Li X, Jeffers LJ, Garon C. et al. Persistence of hepatitis C virus in a human megakaryoblastic leukaemia cell line. J Viral Hepat 1999; 6 (02) 107-114
    CrossrefPubMedSearch in Google Scholar
  • 51 Terada H, Baldini M, Ebbe S, Madoff MA. Interaction of influenza virus with blood platelets. Blood 1966; 28 (02) 213-228
    CrossrefPubMedSearch in Google Scholar
  • 52 Simpson SR, Singh MV, Dewhurst S, Schifitto G, Maggirwar SB. Platelets function as an acute viral reservoir during HIV-1 infection by harboring virus and T-cell complex formation. Blood Adv 2020; 4 (18) 4512-4521
    CrossrefPubMedSearch in Google Scholar
  • 53 Baumer Y, Weatherby TM, Mitchell BI. et al. Hiding in plain sight - platelets, the silent carriers of HIV-1. Platelets 2020; (e-pub ahead of print)
    CrossrefPubMedSearch in Google Scholar
  • 54 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
    CrossrefPubMedSearch in Google Scholar
  • 55 Larsen JB, Pasalic L, Hvas AM. Platelets in coronavirus disease 2019. Semin Thromb Hemost 2020; 46 (07) 823-825
    Thieme ConnectPubMedSearch in Google Scholar
  • 56 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
    CrossrefPubMedSearch in Google Scholar
  • 57 Stenberg PE, Levin J, Baker G, Mok Y, Corash L. Neuraminidase-induced thrombocytopenia in mice: effects on thrombopoiesis. J Cell Physiol 1991; 147 (01) 7-16
    CrossrefPubMedSearch in Google Scholar
  • 58 Isomura H, Yoshida M, Namba H. et al. Suppressive effects of human herpesvirus-6 on thrombopoietin-inducible megakaryocytic colony formation in vitro. J Gen Virol 2000; 81 (Pt 3): 663-673
    CrossrefPubMedSearch in Google Scholar
  • 59 Gonelli A, Mirandola P, Grill V, Secchiero P, Zauli G. Human herpesvirus 7 infection impairs the survival/differentiation of megakaryocytic cells. Haematologica 2002; 87 (11) 1223-1225
    PubMedSearch in Google Scholar
  • 60 Zapata JC, Cox D, Salvato MS. The role of platelets in the pathogenesis of viral hemorrhagic fevers. PLoS Negl Trop Dis 2014; 8 (06) e2858
    Search in Google Scholar
  • 61 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
    CrossrefPubMedSearch in Google Scholar
  • 62 Hottz ED, Medeiros-de-Moraes IM, Vieira-de-Abreu A. et al. Platelet activation and apoptosis modulate monocyte inflammatory responses in dengue. J Immunol 2014; 193 (04) 1864-1872
    CrossrefPubMedSearch in Google Scholar
  • 63 Trugilho MRO, Hottz ED, Brunoro GVF. et al. Platelet proteome reveals novel pathways of platelet activation and platelet-mediated immunoregulation in dengue. PLoS Pathog 2017; 13 (05) e1006385
    CrossrefPubMedSearch in Google Scholar
  • 64 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
    CrossrefPubMedSearch in Google Scholar
  • 65 Pastori D, Esposito A, Carnevale R. et al. HIV-1 induces in vivo platelet activation by enhancing platelet NOX2 activity. J Infect 2015; 70 (06) 651-658
    CrossrefPubMedSearch in Google Scholar
  • 66 Page MJ, Pretorius E. A champion of host defense: a generic large-scale cause for platelet dysfunction and depletion in infection. Semin Thromb Hemost 2020; 46 (03) 302-319
    Thieme ConnectPubMedSearch in Google Scholar
  • 67 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
    CrossrefPubMedSearch in Google Scholar
  • 68 Bik T, Sarov I, Livne A. Interaction between vaccinia virus and human blood platelets. Blood 1982; 59 (03) 482-487
    CrossrefPubMedSearch in Google Scholar
  • 69 Sottnek HM, Campbell Jr WG, Cassel WA. The pathogenesis of Vaccinia virus toxicity. II. An electron microscopic study. Lab Invest 1975; 33 (05) 522-532
    PubMedSearch in Google Scholar
  • 70 Tymvios C, Moore C, Jones S, Solomon A, Sanz-Rosa D, Emerson M. Platelet aggregation responses are critically regulated in vivo by endogenous nitric oxide but not by endothelial nitric oxide synthase. Br J Pharmacol 2009; 158 (07) 1735-1742
    CrossrefPubMedSearch in Google Scholar
  • 71 Moore C, Tymvios C, Emerson M. Functional regulation of vascular and platelet activity during thrombosis by nitric oxide and endothelial nitric oxide synthase. Thromb Haemost 2010; 104 (02) 342-349
    Thieme ConnectPubMedSearch in Google Scholar
  • 72 Bouwman JJ, Visseren FL, Bosch MC, Bouter KP, Diepersloot RJ. Procoagulant and inflammatory response of virus-infected monocytes. Eur J Clin Invest 2002; 32 (10) 759-766
    CrossrefPubMedSearch in Google Scholar
  • 73 Goeijenbier M, van Wissen M, van de Weg C. et al. Review: viral infections and mechanisms of thrombosis and bleeding. J Med Virol 2012; 84 (10) 1680-1696
    CrossrefPubMedSearch in Google Scholar
  • 74 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
    CrossrefPubMedSearch in Google Scholar
  • 75 Hottz ED, Lopes JF, Freitas C. et al. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation. Blood 2013; 122 (20) 3405-3414
    CrossrefPubMedSearch in Google Scholar
  • 76 Choi AI, Vittinghoff E, Deeks SG, Weekley CC, Li Y, Shlipak MG. Cardiovascular risks associated with abacavir and tenofovir exposure in HIV-infected persons. AIDS 2011; 25 (10) 1289-1298
    CrossrefPubMedSearch in Google Scholar
  • 77 Sabin CA, Reiss P, Ryom L. et al; D:A:D Study Group. Is there continued evidence for an association between abacavir usage and myocardial infarction risk in individuals with HIV? A cohort collaboration. BMC Med 2016; 14: 61
    CrossrefPubMedSearch in Google Scholar
  • 78 Collado-Diaz V, Andujar I, Sanchez-Lopez A. et al. Abacavir induces arterial thrombosis in a murine model. J Infect Dis 2018; 218 (02) 228-233
    CrossrefPubMedSearch in Google Scholar
  • 79 Taylor KA, Smyth E, Rauzi F. et al. Pharmacological impact of antiretroviral therapy on platelet function to investigate human immunodeficiency virus-associated cardiovascular risk. Br J Pharmacol 2019; 176 (07) 879-889
    CrossrefPubMedSearch in Google Scholar
  • 80 Alvarez A, Rios-Navarro C, Blanch-Ruiz MA. et al. Abacavir induces platelet-endothelium interactions by interfering with purinergic signalling: a step from inflammation to thrombosis. Antiviral Res 2017; 141: 179-185
    CrossrefPubMedSearch in Google Scholar
  • 81 Khawaja AA, Taylor KA, Lovell AO. et al. HIV antivirals affect endothelial activation and endothelial-platelet crosstalk. Circ Res 2020; 127 (11) 1365-1380
    CrossrefPubMedSearch in Google Scholar
  • 82 Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013; 13 (01) 34-45
    CrossrefPubMedSearch in Google Scholar
  • 83 Mason RJ. Pathogenesis of COVID-19 from a cell biology perspective. Eur Respir J 2020; 55 (04) 2000607
    CrossrefPubMedSearch in Google Scholar
  • 84 Schurink B, Roos E, Radonic T. et al. Viral presence and immunopathology in patients with lethal COVID-19: a prospective autopsy cohort study. Lancet Microbe 2020; 1 (07) e290-e299
    Search in Google Scholar
  • 85 Bradley BT, Maioli H, Johnston R. et al. Histopathology and ultrastructural findings of fatal COVID-19 infections in Washington state: a case series. Lancet 2020; 396 (10247): 320-332
    CrossrefPubMedSearch in Google Scholar
  • 86 Borczuk AC, Salvatore SP, Seshan SV. et al. COVID-19 pulmonary pathology: a multi-institutional autopsy cohort from Italy and New York City. Mod Pathol 2020; 33 (11) 2156-2168
    Search in Google Scholar
  • 87 Tang N, Li D, Wang X, Sun Z. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J Thromb Haemost 2020; 18 (04) 844-847
    CrossrefPubMedSearch in Google Scholar
  • 88 Hottz ED, Azevedo-Quintanilha IG, Palhinha L. et al. Platelet activation and platelet-monocyte aggregate formation trigger tissue factor expression in patients with severe COVID-19. Blood 2020; 136 (11) 1330-1341
    CrossrefPubMedSearch in Google Scholar
  • 89 Denorme F, Manne BK, Portier I. et al. COVID-19 patients exhibit reduced procoagulant platelet responses. J Thromb Haemost 2020; 18 (11) 3067-3073
    CrossrefPubMedSearch in Google Scholar
  • 90 Gu SX, Tyagi T, Jain K. et al. Thrombocytopathy and endotheliopathy: crucial contributors to COVID-19 thromboinflammation. Nat Rev Cardiol 2021; 18 (03) 194-209
    CrossrefPubMedSearch in Google Scholar
  • 91 Xu Z, Shi L, Wang Y. et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med 2020; 8 (04) 420-422
    CrossrefPubMedSearch in Google Scholar
  • 92 Ciceri F, Beretta L, Scandroglio AM. et al. Microvascular COVID-19 lung vessels obstructive thromboinflammatory syndrome (MicroCLOTS): an atypical acute respiratory distress syndrome working hypothesis. Crit Care Resusc 2020; 22 (02) 95-97
    PubMedSearch in Google Scholar
  • 93 Thwaites RS, Uruchurtu ASS, Siggins M. et al; on behalf of the ISARIC4C investigators. Elevated antiviral, myeloid and endothelial inflammatory markers in severe COVID-19. medRxiv 2020;
    CrossrefPubMedSearch in Google Scholar
  • 94 Zaid Y, Puhm F, Allaeys I. et al. Platelets can associate with SARS-Cov-2 RNA and are hyperactivated in COVID-19. Circ Res 2020; 127 (11) 1404-1418
    CrossrefPubMedSearch in Google Scholar
  • 95 Parra-Izquierdo I, Aslan JE. Perspectives on platelet heterogeneity and host immune response in coronavirus disease 2019 (COVID-19). Semin Thromb Hemost 2020; 46 (07) 826-830
    Thieme ConnectPubMedSearch in Google Scholar
  • 96 Sinha P, Calfee CS, Cherian S. et al. Prevalence of phenotypes of acute respiratory distress syndrome in critically ill patients with COVID-19: a prospective observational study. Lancet Respir Med 2020; 8 (12) 1209-1218
    CrossrefPubMedSearch in Google Scholar
  • 97 Kox M, Waalders NJB, Kooistra EJ, Gerretsen J, Pickkers P. Cytokine levels in critically ill patients with COVID-19 and other conditions. JAMA 2020; 324 (15) 1565-1567
    CrossrefPubMedSearch in Google Scholar
  • 98 Leisman DE, Ronner L, Pinotti R. et al. Cytokine elevation in severe and critical COVID-19: a rapid systematic review, meta-analysis, and comparison with other inflammatory syndromes. Lancet Respir Med 2020; 8 (12) 1233-1244
    CrossrefPubMedSearch in Google Scholar
  • 99 Wang D, Hu B, Hu C. et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 2020; 323 (11) 1061-1069
    CrossrefPubMedSearch in Google Scholar
  • 100 Klok FA, Kruip MJHA, van der Meer NJM. et al. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: an updated analysis. Thromb Res 2020; 191: 148-150
    CrossrefPubMedSearch in Google Scholar
  • 101 Hanley B, Naresh KN, Roufosse C. et al. Histopathological findings and viral tropism in UK patients with severe fatal COVID-19: a post-mortem study. Lancet Microbe 2020; 1 (06) e245-e253
    Search in Google Scholar
  • 102 Huang C, Wang Y, Li X. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395 (10223): 497-506
    CrossrefPubMedSearch in Google Scholar
  • 103 Rapkiewicz AV, Mai X, Carsons SE. et al. Megakaryocytes and platelet-fibrin thrombi characterize multi-organ thrombosis at autopsy in COVID-19: a case series. EClinicalMedicine 2020; 24: 100434
    CrossrefPubMedSearch in Google Scholar
  • 104 Manne BK, Denorme F, Middleton EA. et al. Platelet gene expression and function in patients with COVID-19. Blood 2020; 136 (11) 1317-1329
    CrossrefPubMedSearch in Google Scholar
  • 105 Bury L, Camilloni B, Castronari R. et al. Search for SARS-CoV-2 RNA in platelets from COVID-19 patients. Platelets 2020; 32 (02) 284-287
    CrossrefPubMedSearch in Google Scholar
  • 106 Campbell RA, Boilard E, Rondina MT. Is there a role for the ACE2 receptor in SARS-CoV-2 interactions with platelets?. J Thromb Haemost 2021; 19 (01) 46-50
    CrossrefPubMedSearch in Google Scholar
  • 107 Hoffmann M, Kleine-Weber H, Schroeder S, Kruger N, Herrler T, Erichsen S. et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 2020; 181 (02) 271.e8-280.e8
    Search in Google Scholar
  • 108 Zhang S, Liu Y, Wang X. et al. SARS-CoV-2 binds platelet ACE2 to enhance thrombosis in COVID-19. J Hematol Oncol 2020; 13 (01) 120
    CrossrefPubMedSearch in Google Scholar
  • 109 Sahai A, Bhandari R, Koupenova M. et al. SARS-CoV-2 receptors are expressed on human platelets and the effect of aspirin on clinical outcomes in COVID-19 patients. Res Sq [preprint] 2020;rs.3.rs-119031
    CrossrefPubMed
  • 110 Zini G, Bellesi S, Ramundo F, d'Onofrio G. Morphological anomalies of circulating blood cells in COVID-19. Am J Hematol 2020; 95 (07) 870-872
    CrossrefPubMedSearch in Google Scholar
  • 111 Zaid Y, Guessous F, Puhm F, Elhamdani W. et al. Platelet reactivity to thrombin differs between patients with COVID-19 and those with ARDS unrelated to COVID-19. Blood Adv 2020; 5 (03) 635-639
    CrossrefPubMedSearch in Google Scholar
  • 112 Taus F, Salvagno G, Canè S. et al. Platelets promote thromboinflammation in SARS-CoV-2 pneumonia. Arterioscler Thromb Vasc Biol 2020; 40 (12) 2975-2989
    CrossrefPubMedSearch in Google Scholar
  • 113 Vadasz Z, Brenner B, Toubi E. Immune-mediated coagulopathy in COVID-19 infection. Semin Thromb Hemost 2020; 46 (07) 838-840
    Thieme ConnectPubMedSearch in Google Scholar
  • 114 Lippi G, Plebani M. Cytokine “storm”, cytokine “breeze”, or both in COVID-19?. Clinic Chem Lab Med 2020; (e-pub ahead of print)
  • 115 Archambault ASZY, Rakotoarivelo V, Doré E. et al. Lipid storm within the lungs of severe COVID-19 patients: extensive levels of cyclooxygenase and lipoxygenase-derived inflammatory metabolites. MedRxiv 2021;
    CrossrefPubMedSearch in Google Scholar
  • 116 Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ. HLH Across Speciality Collaboration, UK. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020; 395 (10229): 1033-1034
    CrossrefPubMedSearch in Google Scholar
  • 117 Chow JH, Khanna AK, Kethireddy S. et al. Aspirin use is associated with decreased mechanical ventilation, ICU admission, and in-hospital mortality in hospitalized patients with COVID-19. Anesth Analg 2020; 132 (04) 930-941
    PubMedSearch in Google Scholar
  • 118 Forghani B, Schmidt NJ. Association of herpes simplex virus with platelets of experimentally infected mice. Arch Virol 1983; 76 (03) 269-274
    CrossrefPubMedSearch in Google Scholar
  • 119 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
    PubMedSearch in Google Scholar
  • 120 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
    PubMedSearch in Google Scholar
  • 121 Danon D, Jerushalmy Z, De Vries A. Incorporation of influenza virus in human blood platelets in vitro. Electron microscopical observation. Virology 1959; 9: 719-722
    CrossrefPubMedSearch in Google Scholar