Human platelets and their capacity of binding viruses: meaning and challenges?

BMC Immunology

Olivier Garraud⁵  Ricardo M Gomez³  Mirta Schattner⁴  Fabrice Cognasse⁶  Bruno Pozzetto²  Hind Hamzeh-Cognasse¹  Adrien Chabert¹ 

[1] EA3064—GIMAP, Université de Lyon, Saint-Etienne, 42023, France;Service des Agents infectieux et d’Hygiène, CHU de Saint-Etienne, Saint-Etienne, 42055, France;Laboratorio de Virus Animales, Instituto de Biotecnología y Biología Molecular, UNLP-CONICET, La Plata, Argentina;Laboratorio de Trombosis Experimental, Instituto de Medicina Experimental, ANM-CONICET, Buenos Aires, Argentina;INTS, 6 rue Alexandre-Cabanel, Paris, 75015, France;EFS Auvergne-Loire, Saint-Etienne, 42023, France

关键词: Hemostasis;    Infection;    Viruses;    Receptors;    Platelets;   

Others  :  1177278
DOI  :  10.1186/s12865-015-0092-1

 received in 2015-01-13, accepted in 2015-04-03,  发布年份 2015

【 摘 要 】

Blood platelets are first aimed at ensuring primary hemostasis. Beyond this role, they have been acknowledged as having functions in the maintenance of the vascular arborescence and, more recently, as being also innate immune cells, devoted notably to the detection of danger signals, of which infectious ones. Platelets express pathogen recognition receptors that can sense bacterial and viral moieties. Besides, several molecules that bind epithelial or sub-endothelial molecules and, so forth, are involved in hemostasis, happen to be able to ligate viral determinants, making platelets capable of either binding viruses or even to be infected by some of them. Further, as platelets express both Fc-receptors for Ig and complement receptors, they also bind occasionally virus-Ig or virus-Ig-complement immune complexes. Interplays of viruses with platelets are very complex and viral infections often interfere with platelet number and functions. Through a few instances of viral infections, the present review aims at presenting some of the most important interactions from pathophysiological and clinical points of view, which are observed between human viruses and platelets.

【 授权许可】

   
2015 Chabert et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Danon D, Jerushalmy Z, De Vries A. Incorporation of influenza virus in human blood platelets in vitro. Electron microscopical observation. Virology. 1959; 9:719-22.
• [2]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):1490-5.
• [3]Flaujac C, Boukour S, Cramer-Borde E. Platelets and viruses: an ambivalent relationship. Cell Mol Life Sci. 2010; 67(4):545-56.
• [4]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):1920-3.
• [5]Youssefian T, Drouin A, Masse 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):4021-9.
• [6]Boukour S, Masse JM, Benit L, Dubart-Kupperschmitt A, Cramer EM. Lentivirus degradation and DC-SIGN expression by human platelets and megakaryocytes. J Thromb Haemost. 2006; 4(2):426-35.
• [7]Holme PA, Muller F, Solum NO, Brosstad F, Froland SS, Aukrust P. Enhanced activation of platelets with abnormal release of RANTES in human immunodeficiency virus type 1 infection. FASEB J. 1998; 12(1):79-89.
• [8]Basch RS, Dolzhanskiy A, Zhang XM, Karpatkin S. The development of human megakaryocytes. II. CD4 expression occurs during haemopoietic differentiation and is an early step in megakaryocyte maturation. Br J Haematol. 1996; 94(3):433-42.
• [9]Rozmyslowicz T, Majka M, Kijowski J, Murphy SL, Conover DO, Poncz M et al.. Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS. 2003; 17(1):33-42.
• [10]Riviere C, Subra F, Cohen-Solal K, Cordette-Lagarde V, Letestu R, Auclair C et al.. Phenotypic and functional evidence for the expression of CXCR4 receptor during megakaryocytopoiesis. Blood. 1999; 93(5):1511-23.
• [11]Kouri YH, Borkowsky W, Nardi M, Karpatkin S, Basch RS. Human megakaryocytes have a CD4 molecule capable of binding human immunodeficiency virus-1. Blood. 1993; 81(10):2664-70.
• [12]Lee B, Ratajczak J, Doms RW, Gewirtz AM, Ratajczak MZ. Coreceptor/chemokine receptor expression on human hematopoietic cells: biological implications for human immunodeficiency virus-type 1 infection. Blood. 1999; 93(4):1145-56.
• [13]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):4046-54.
• [14]Chaipan C, Soilleux EJ, Simpson P, Hofmann H, Gramberg T, Marzi A et al.. DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol. 2006; 80(18):8951-60.
• [15]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(3):562-73.
• [16]Cognasse F, Hamzeh-Cognasse H, Berthet J, Damien P, Lucht F, Pozzetto B et al.. Altered release of regulated upon activation, normal T-cell expressed and secreted protein from human, normal platelets: contribution of distinct HIV-1MN gp41 peptides. AIDS. 2009; 23(15):2057-9.
• [17]Sui SJ, Ren MY, Xu FY, Zhang Y. A high association of aortic valve sclerosis detected by transthoracic echocardiography with coronary arteriosclerosis. Cardiology. 2007; 108(4):322-30.
• [18]Singh MV, Davidson DC, Jackson JW, Singh VB, Silva J, Ramirez SH et al.. Characterization of platelet-monocyte complexes in HIV-1-infected individuals: possible role in HIV-associated neuroinflammation. J Immunol. 2014; 192(10):4674-84.
• [19]Auerbach DJ, Lin Y, Miao H, Cimbro R, Difiore MJ, Gianolini ME et al.. Identification of the platelet-derived chemokine CXCL4/PF-4 as a broad-spectrum HIV-1 inhibitor. Proc Natl Acad Sci USA. 2012; 109(24):9569-74.
• [20]Solomon Tsegaye T, Gnirss K, Rahe-Meyer N, Kiene M, Kramer-Kuhl A, Behrens G et al.. Platelet activation suppresses HIV-1 infection of T cells. Retrovirology. 2013; 10:48. BioMed Central Full Text
• [21]Schwartzkopff F, Grimm TA, Lankford CS, Fields K, Wang J, Brandt E et al.. Platelet factor 4 (CXCL4) facilitates human macrophage infection with HIV-1 and potentiates virus replication. Innate Immun. 2009; 15(6):368-79.
• [22]Lima RG, Van Weyenbergh J, Saraiva EM, Barral-Netto M, Galvao-Castro B, Bou-Habib DC. The replication of human immunodeficiency virus type 1 in macrophages is enhanced after phagocytosis of apoptotic cells. J Infect Dis. 2002; 185(11):1561-6.
• [23]Maugeri N, Rovere-Querini P, Evangelista V, Covino C, Capobianco A, Bertilaccio MT et al.. Neutrophils phagocytose activated platelets in vivo: a phosphatidylserine, P-selectin, and {beta}2 integrin-dependent cell clearance program. Blood. 2009; 113(21):5254-65.
• [24]Franzetti M, Adorni F, Oreni L, Van Den Bogaart L, Resnati C, Milazzo L, et al. Changes in the Incidence of Severe Thrombocytopenia and Its Predisposing Conditions in Hiv-Infected Patients since the Introduction of Highly Active Antiretroviral Therapy. J Acquir Immune Defic Syndr. 2014;67:493–8.
• [25]Wolf K, Tsakiris DA, Weber R, Erb P, Battegay M. Antiretroviral therapy reduces markers of endothelial and coagulation activation in patients infected with human immunodeficiency virus type 1. J Infect Dis. 2002; 185(4):456-62.
• [26]Damien P, Cognasse F, Lucht F, Suy F, Pozzetto B, Garraud O et al.. Highly active antiretroviral therapy alters inflammation linked to platelet cytokines in HIV-1-infected patients. J Infect Dis. 2013; 208(5):868-70.
• [27]Karasu Z, Tekin F, Ersoz G, Gunsar F, Batur Y, Ilter T et al.. Liver fibrosis is associated with decreased peripheral platelet count in patients with chronic hepatitis B and C. Dig Dis Sci. 2007; 52(6):1535-9.
• [28]Puoti C, Guarisco R, Bellis L, Spilabotti L. Diagnosis, management, and treatment of hepatitis C. Hepatology. 2009; 50(1):322.
• [29]Weksler BB. Review article: the pathophysiology of thrombocytopenia in hepatitis C virus infection and chronic liver disease. Aliment Pharmacol Ther. 2007; 26 Suppl 1:13-9.
• [30]Peck-Radosavljevic M, Wichlas M, Pidlich J, Sims P, Meng G, Zacherl J et al.. Blunted thrombopoietin response to interferon alfa-induced thrombocytopenia during treatment for hepatitis C. Hepatology. 1998; 28(5):1424-9.
• [31]Adinolfi LE, Giordano MG, Andreana A, Tripodi MF, Utili R, Cesaro G et al.. Hepatic fibrosis plays a central role in the pathogenesis of thrombocytopenia in patients with chronic viral hepatitis. Br J Haematol. 2001; 113(3):590-5.
• [32]Koruk M, Onuk MD, Akcay F, Savas MC. Serum thrombopoietin levels in patients with chronic hepatitis and liver cirrhosis, and its relationship with circulating thrombocyte counts. Hepatogastroenterology. 2002; 49(48):1645-8.
• [33]Afdhal N, McHutchison J, Brown R, Jacobson I, Manns M, Poordad F et al.. Thrombocytopenia associated with chronic liver disease. J Hepatol. 2008; 48(6):1000-7.
• [34]Danish FA, Koul SS, Subhani FR, Rabbani AE, Yasmin S. Role of hematopoietic growth factors as adjuncts in the treatment of chronic hepatitis C patients. Saudi J Gastroenterol. 2008; 14(3):151-7.
• [35]Bordin G, Ballare M, Zigrossi P, Bertoncelli MC, Paccagnino L, Baroli A et al.. A laboratory and thrombokinetic study of HCV-associated thrombocytopenia: a direct role of HCV in bone marrow exhaustion? Clin Exp Rheumatol. 1995; 13 Suppl 13:S39-43.
• [36]Ballard HS. The hematological complications of alcoholism. Alcohol Health Res World. 1997; 21(1):42-52.
• [37]McCormick PA, Murphy KM. Splenomegaly, hypersplenism and coagulation abnormalities in liver disease. Baillieres Best Pract Res Clin Gastroenterol. 2000; 14(6):1009-31.
• [38]Pockros PJ, Duchini A, McMillan R, Nyberg LM, McHutchison J, Viernes E. Immune thrombocytopenic purpura in patients with chronic hepatitis C virus infection. Am J Gastroenterol. 2002; 97(8):2040-5.
• [39]Hamaia S, Li C, Allain JP. The dynamics of hepatitis C virus binding to platelets and 2 mononuclear cell lines. Blood. 2001; 98(8):2293-300.
• [40]Nagamine T, Ohtuka T, Takehara K, Arai T, Takagi H, Mori M. Thrombocytopenia associated with hepatitis C viral infection. J Hepatol. 1996; 24(2):135-40.
• [41]Stasi R, Chia LW, Kalkur P, Lowe R, Shannon MS. Pathobiology and treatment of hepatitis virus-related thrombocytopenia. Mediterr J Hematol Infect Dis. 2009; 1(3):e2009023.
• [42]Rajan SK, Espina BM, Liebman HA. Hepatitis C virus-related thrombocytopenia: clinical and laboratory characteristics compared with chronic immune thrombocytopenic purpura. Br J Haematol. 2005; 129(6):818-24.
• [43]Vizcaino G, Diez-Ewald M, Vizcaino-Carruyo J. Treatment of chronic immune thrombocytopenic purpura. Looking for something better. Review. Invest Clin. 2009; 50(1):95-108.
• [44]Erickson-Miller CL, Delorme E, Tian SS, Hopson CB, Landis AJ, Valoret EI et al.. Preclinical activity of eltrombopag (SB-497115), an oral, nonpeptide thrombopoietin receptor agonist. Stem Cells. 2009; 27(2):424-30.
• [45]Erickson-Miller CL, DeLorme E, Tian SS, Hopson CB, Stark K, Giampa L et al.. Discovery and characterization of a selective, nonpeptidyl thrombopoietin receptor agonist. Exp Hematol. 2005; 33(1):85-93.
• [46]Danish FI, Yasmin S. The role of eltrombopag in the management of hepatitis C virus-related thrombocytopenia. Hepat Med. 2013; 5:17-30.
• [47]Burness CB. Eltrombopag: a review of its use in the treatment of thrombocytopenia in patients with chronic hepatitis C. Drugs. 2014; 74(16):1961-71.
• [48]Faraji A, Egizi A, Fonseca DM, Unlu I, Crepeau T, Healy SP et al.. Comparative host feeding patterns of the Asian tiger mosquito, Aedes albopictus, in urban and suburban Northeastern USA and implications for disease transmission. PLoS Negl Trop Dis. 2014; 8(8):e3037.
• [49]Lambrechts L, Scott TW, Gubler DJ. Consequences of the expanding global distribution of Aedes albopictus for dengue virus transmission. PLoS Negl Trop Dis. 2010; 4(5):e646.
• [50]Zapata JC, Cox D, Salvato MS. The role of platelets in the pathogenesis of viral hemorrhagic fevers. PLoS Negl Trop Dis. 2014; 8(6):e2858.
• [51]Guilarde AO, Turchi MD, Siqueira JB, Feres VC, Rocha B, Levi JE et al.. Dengue and dengue hemorrhagic fever among adults: clinical outcomes related to viremia, serotypes, and antibody response. J Infect Dis. 2008; 197(6):817-24.
• [52]Nachman RL, Rafii S. Platelets, petechiae, and preservation of the vascular wall. N Engl J Med. 2008; 359(12):1261-70.
• [53]Ho-Tin-Noe B, Demers M, Wagner DD. How platelets safeguard vascular integrity. J Thromb Haemost. 2011; 9 Suppl 1:56-65.
• [54]Wills B, Tran VN, Nguyen TH, Truong TT, Tran TN, Nguyen MD et al.. Hemostatic changes in Vietnamese children with mild dengue correlate with the severity of vascular leakage rather than bleeding. Am J Trop Med Hyg. 2009; 81(4):638-44.
• [55]Michels M, van der Ven AJ, Djamiatun K, Fijnheer R, de Groot PG, Griffioen AW et al.. Imbalance of angiopoietin-1 and angiopoetin-2 in severe dengue and relationship with thrombocytopenia, endothelial activation, and vascular stability. Am J Trop Med Hyg. 2012; 87(5):943-6.
• [56]Hottz ED, Lopes JF, Freitas C, Valls-de-Souza R, Oliveira MF, Bozza MT et al.. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation. Blood. 2013; 122(20):3405-14.
• [57]Hottz ED, Oliveira MF, Nunes PC, Nogueira RM, Valls-de-Souza R, Da Poian AT et al.. Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases. J Thromb Haemost. 2013; 11(5):951-62.
• [58]Mitrakul C, Poshyachinda M, Futrakul P, Sangkawibha N, Ahandrik S. Hemostatic and platelet kinetic studies in dengue hemorrhagic fever. Am J Trop Med Hyg. 1977; 26(5 Pt 1):975-84.
• [59]Srichaikul T, Nimmannitya S, Sripaisarn T, Kamolsilpa M, Pulgate C. Platelet function during the acute phase of dengue hemorrhagic fever. Southeast Asian J Trop Med Public Health. 1989; 20(1):19-25.
• [60]Mendes-Ribeiro AC, Moss MB, Siqueira MA, Moraes TL, Ellory JC, Mann GE et al.. Dengue fever activates the L-arginine-nitric oxide pathway: an explanation for reduced aggregation of human platelets. Clin Exp Pharmacol Physiol. 2008; 35(10):1143-6.
• [61]Michels M, Alisjahbana B, De Groot PG, Indrati AR, Fijnheer R, Puspita M et al.. Platelet function alterations in dengue are associated with plasma leakage. Thromb Haemost. 2014; 112(2):352-62.
• [62]Carneiro AM, Cook EH, Murphy DL, Blakely RD. Interactions between integrin alphaIIbbeta3 and the serotonin transporter regulate serotonin transport and platelet aggregation in mice and humans. J Clin Invest. 2008; 118(4):1544-52.
• [63]Noisakran S, Gibbons RV, Songprakhon P, Jairungsri A, Ajariyakhajorn C, Nisalak A et al.. Detection of dengue virus in platelets isolated from dengue patients. Southeast Asian J Trop Med Public Health. 2009; 40(2):253-62.
• [64]Tassaneetrithep B, Burgess TH, Granelli-Piperno A, Trumpfheller C, Finke J, Sun W et al.. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med. 2003; 197(7):823-9.
• [65]Alonzo MT, Lacuesta TL, Dimaano EM, Kurosu T, Suarez LA, Mapua CA et al.. Platelet apoptosis and apoptotic platelet clearance by macrophages in secondary dengue virus infections. J Infect Dis. 2012; 205(8):1321-9.
• [66]Tsai JJ, Jen YH, Chang JS, Hsiao HM, Noisakran S, Perng GC. Frequency alterations in key innate immune cell components in the peripheral blood of dengue patients detected by FACS analysis. J Innate Immun. 2011; 3(5):530-40.
• [67]Onlamoon N, Noisakran S, Hsiao HM, Duncan A, Villinger F, Ansari AA et al.. Dengue virus-induced hemorrhage in a nonhuman primate model. Blood. 2010; 115(9):1823-34.
• [68]Rathakrishnan A, Wang SM, Hu Y, Khan AM, Ponnampalavanar S, Lum LC et al.. Cytokine expression profile of dengue patients at different phases of illness. PLoS One. 2012; 7(12):e52215.
• [69]Prashantha B, Varun S, Sharat D, Murali Mohan BV, Ranganatha R, Shivaprasad, Naveen M. Prophyactic platelet transfusion in stable dengue Fever patients: is it really necessary? Indian J Hematol Blood Transfus. 2014, 30(2):126-129.
• [70]Kerber. Research efforts to control highly pathogenic arenaviruses: a summary of the progress and gaps. J Clin Virol. 2015, in press.
• [71]Iannacone M, Sitia G, Isogawa M, Whitmire JK, Marchese P, Chisari FV et al.. Platelets prevent IFN-alpha/beta-induced lethal hemorrhage promoting CTL-dependent clearance of lymphocytic choriomeningitis virus. Proc Natl Acad Sci USA. 2008; 105(2):629-34.
• [72]Zapata JC, Pauza CD, Djavani MM, Rodas JD, Moshkoff D, Bryant J et al.. Lymphocytic choriomeningitis virus (LCMV) infection of macaques: a model for Lassa fever. Antiviral Res. 2011; 92(2):125-38.
• [73]Pozner RG, Ure AE, Jaquenod De Giusti C, D'Atri LP, Italiano JE, Torres O et al.. Junin virus infection of human hematopoietic progenitors impairs in vitro proplatelet formation and platelet release via a bystander effect involving type I IFN signaling. PLoS Pathog. 2010; 6(4):e1000847.
• [74]Negrotto S, De Giusti CJ, Lapponi MJ, Etulain J, Rivadeneyra L, Pozner RG et al.. Expression and functionality of type I interferon receptor in the megakaryocytic lineage. J Thromb Haemost. 2011; 9(12):2477-85.
• [75]Murray CJ, Ortblad KF, Guinovart C, Lim SS, Wolock TM, Roberts DA et al.. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014; 384(9947):1005-70.
• [76]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(6):940-50.
• [77]Cummins D, Fisher-Hoch SP, Walshe KJ, Mackie IJ, McCormick JB, Bennett D et al.. A plasma inhibitor of platelet aggregation in patients with Lassa fever. Br J Haematol. 1989; 72(4):543-8.
• [78]Marta RF, Heller MV, Maiztegui JI, Molinas FC. Further studies on the plasma inhibitor of platelet activation in Argentine hemorrhagic fever. Thromb Haemost. 1993; 69(5):526-7.