Complement and platelets: Mutual interference in the immune network

Molecular Immunology

Volumn 67, Issue 1, 2015, Pages 108-118

  Speth, Cornelia ^a   Rambach, Günter ^a   Würzner, Reinhard ^a   Lass Flörl, Cornelia ^a   Kozarcanin, Huda ^b   Hamad, Osama A ^b   Nilsson, Bo ^b   Ekdahl, Kristina N ^b,c  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UPPSALA UNIVERSITY   (Sweden)

^c LINNAEUS UNIVERSITY   (Sweden)

Author keywords

Autoimmunity and inflammatory disorders; Biomaterials; Complement; Immune network; Infectious diseases; Innate immunity; Platelets

Indexed keywords

BIOMATERIAL; COMPLEMENT; COMPLEMENT FACTOR; COMPLEMENT RECEPTOR; COMPLEMENT FACTOR I;

AUTOIMMUNE DISEASE; AUTOIMMUNITY; BACTERIAL INFECTION; CELL FUNCTION; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; ENZYME REGULATION; HEMOLYTIC UREMIC SYNDROME; HUMAN; IDIOPATHIC THROMBOCYTOPENIC PURPURA; INFLAMMATION; MOLECULAR INTERACTION; MYCOSIS; NONHUMAN; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOTIC THROMBOCYTOPENIC PURPURA; VIRUS INFECTION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; PATHOLOGY; VIROLOGY;

AUTOIMMUNE DISEASES; BACTERIAL INFECTIONS; BLOOD PLATELETS; COMPLEMENT ACTIVATION; COMPLEMENT C3B INACTIVATOR PROTEINS; COMPLEMENT SYSTEM PROTEINS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; MYCOSES; RECEPTORS, COMPLEMENT; SIGNAL TRANSDUCTION; VIRUS DISEASES;

EID: 84936986317     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2015.03.244     Document Type: Review

References (149)

1. Abbal C., Lambelet M., Bertaggia D., Gerbex C., Martinez M., Arcaro A., Schapira M., Spertini O. Lipid raft adhesion receptors and Syk regulate selectin-dependent rolling under flow conditions. Blood 2006, 108:3352-3359.
2. Ahmad A., Menezes J. Binding of the Epstein-Barr virus to human platelets causes the release of transforming growth factor-beta. J. Immunol. 1997, 159:3984-3988.
3. Arvand M., Bhakdi S., Dahlback B., Preissner K.T. Staphylococcus aureus alpha-toxin attack on human platelets promotes assembly of the prothrombinase complex. J. Biol. Chem. 1990, 265:14377-14381.
4. Assinger A., Laky M., Schabbauer G., Hirschl A.M., Buchberger E., Binder B.R., Volf I. Efficient phagocytosis of periodontopathogens by neutrophils requires plasma factors, platelets and TLR2. J. Thromb. Haemost. 2011, 9:799-809.
5. Ayesh Haj Yousef M.H., Alawneh K.M. Candida albicans-induced chronic thrombocytopenic purpura. Acta Haematol. 2011, 126:202-204.
6. Berman H., Rodriguez-Pinto I., Cervera R., Morel N., Costedoat-Chalumeau N., Erkan D., Shoenfeld Y., Espinosa G. Rituximab use in the catastrophic antiphospholipid syndrome: descriptive analysis of the CAPS registry patients receiving rituximab. Autoimmun. Rev. 2013, 12:1085-1090. Catastrophic Antiphospholipid Syndrome Registry Project G.
7. Bertling A., Niemann S., Uekotter A., Fegeler W., Lass-Florl C., von Eiff C., Kehrel B.E. Candida albicans and its metabolite gliotoxin inhibit platelet function via interaction with thiols. Thromb. Haemost. 2010, 104:270-278.
8. Bessler M., Mason P.J., Hillmen P., Miyata T., Yamada N., Takeda J., Luzzatto L., Kinoshita T. Paroxysmal nocturnal haemoglobinuria (PNH) is caused by somatic mutations in the PIG-A gene. EMBO J. 1994, 13:110-117.
9. Bidula S., Kenawy H., Ali Y.M., Sexton D., Schwaeble W.J., Schelenz S. Role of ficolin-A and lectin complement pathway in the innate defense against pathogenic Aspergillus species. Infect. Immun. 2013, 81:1730-1740.
10. Carter A.M. Complement activation: an emerging player in the pathogenesis of cardiovascular disease. Scientifica 2012, 2012:402783.
11. Celi A., Pellegrini G., Lorenzet R., De Blasi A., Ready N., Furie B.C., Furie B. P-selectin induces the expression of tissue factor on monocytes. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:8767-8771.
12. Cerletti C., Tamburrelli C., Izzi B., Gianfagna F., de Gaetano G. Platelet-leukocyte interactions in thrombosis. Thromb. Res. 2012, 129:263-266.
13. Cervera R. Update on the diagnosis, treatment, and prognosis of the catastrophic antiphospholipid syndrome. Curr. Rheumatol. Rep. 2010, 12:70-76.
14. Chang F.Y., Singh N., Gayowski T., Wagener M.M., Mietzner S.M., Stout J.E., Marino I.R. Thrombocytopenia in liver transplant recipients: predictors, impact on fungal infections, and role of endogenous thrombopoietin. Transplantation 2000, 69:70-75.
15. Chaturvedi S., McCrae K.R. Recent advances in the antiphospholipid antibody syndrome. Curr. Opin. Hematol. 2014, 21:371-379.
16. Cheng S.C., Sprong T., Joosten L.A., van der Meer J.W., Kullberg B.J., Hube B., Schejbel L., Garred P., van Deuren M., Netea M.G. Complement plays a central role in Candida albicans-induced cytokine production by human PBMCs. Eur. J. Immunol. 2012, 42:993-1004.
17. Christin L., Wysong D.R., Meshulam T., Hastey R., Simons E.R., Diamond R.D. Human platelets damage Aspergillus fumigatus hyphae and may supplement killing by neutrophils. Infect. Immun. 1998, 66:1181-1189.
18. Coller B.S. Binding of abciximab to alpha V beta 3 and activated alpha M beta 2 receptors: with a review of platelet-leukocyte interactions. Thromb. Haemost. 1999, 82:326-336.
19. Cosgrove L.J., d'Apice A.J., Haddad A., Pedersen J., McKenzie I.F. CR3 receptor on platelets and its role in the prostaglandin metabolic pathway. Immunol. Cell Biol. 1987, 65(Pt 6):453-460.
20. Cox D., Kerrigan S.W., Watson S.P. Platelets and the innate immune system: mechanisms of bacterial-induced platelet activation. J. Thromb. Haemost. 2011, 9:1097-1107.
21. Del Conde I., Cruz M.A., Zhang H., Lopez J.A., Afshar-Kharghan V. Platelet activation leads to activation and propagation of the complement system. J. Exp. Med. 2005, 201:871-879.
22. Devine D.V., Rosse W.F. Regulation of the activity of platelet-bound C3 convertase of the alternative pathway of complement by platelet factor H. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:5873-5877.
23. Dinh A., Anathasayanan A., Rubin L.M. Safe and effective use of eculizumab in the treatment of severe Shiga toxin Escherichia coli-associated hemolytic uremic syndrome. Am. J. Health-Syst. Pharm. 2015, 72:117-120.
24. Dyke M.P., Ott K. Severe thrombocytopenia in extremely low birthweight infants with systemic candidiasis. J. Paediatr. Child Health 1993, 29:298-301.
25. Ehlers R., Ustinov V., Chen Z., Zhang X., Rao R., Luscinskas F.W., Lopez J., Plow E., Simon D.I. Targeting platelet-leukocyte interactions: identification of the integrin Mac-1 binding site for the platelet counter receptor glycoprotein Ibalpha. J. Exp. Med. 2003, 198:1077-1088.
26. Ehrlenbach S., Rosales A., Posch W., Wilflingseder D., Hermann M., Brockmeyer J., Karch H., Satchell S.C., Wurzner R., Orth-Holler D. Shiga toxin 2 reduces complement inhibitor CD59 expression on human renal tubular epithelial and glomerular endothelial cells. Infect. Immun. 2013, 81:2678-2685.
27. Ekdahl K.N., Ronnblom L., Sturfelt G., Nilsson B. Increased phosphate content in complement component C3, fibrinogen, vitronectin, and other plasma proteins in systemic lupus erythematosus: covariation with platelet activation and possible association with thrombosis. Arthritis Rheum. 1997, 40:2178-2186.
28. Feng S., Liang X., Kroll M.H., Chung D.W., Afshar-Kharghan V. Von Willebrand factor is a cofactor in complement regulation. Blood 2014.
29. Fitzgerald J.R., Foster T.J., Cox D. The interaction of bacterial pathogens with platelets. Nat. Rev. Microbiol. 2006, 4:445-457.
30. Flaujac C., Boukour S., Cramer-Borde E. Platelets and viruses: an ambivalent relationship. Cell. Mol. Life Sci. 2010, 67:545-556.
31. Ford I., Douglas C.W., Cox D., Rees D.G., Heath J., Preston F.E. The role of immunoglobulin G and fibrinogen in platelet aggregation by Streptococcus sanguis. Br. J. Haematol. 1997, 97:737-746.
32. George J.N. Platelets. Lancet 2000, 355:1531-1539.
33. Ghasemzadeh M., Hosseini E. Platelet-leukocyte crosstalk: linking proinflammatory responses to procoagulant state. Thromb. Res. 2013, 131:191-197.
34. Gnatenko D.V., Dunn J.J., McCorkle S.R., Weissmann D., Perrotta P.L., Bahou W.F. Transcript profiling of human platelets using microarray and serial analysis of gene expression. Blood 2003, 101:2285-2293.
35. Gushiken F.C., Han H., Li J., Rumbaut R.E., Afshar-Kharghan V. Abnormal platelet function in C3-deficient mice. J. Thromb. Haemost. 2009, 7:865-870.
36. Hamad O.A., Ekdahl K.N., Nilsson P.H., Andersson J., Magotti P., Lambris J.D., Nilsson B. Complement activation triggered by chondroitin sulfate released by thrombin receptor-activated platelets. J. Thromb. Haemost. 2008, 6:1413-1421.
37. Hamad O.A., Nilsson P.H., Lasaosa M., Ricklin D., Lambris J.D., Nilsson B., Ekdahl K.N. Contribution of chondroitin sulfate A to the binding of complement proteins to activated platelets. PLoS ONE 2010, 5:e12889.
38. Hamad O.A., Nilsson P.H., Wouters D., Lambris J.D., Ekdahl K.N., Nilsson B. Complement component C3 binds to activated normal platelets without preceding proteolytic activation and promotes binding to complement receptor 1. J. Immunol. 2010, 184:2686-2692.
39. Harboe M., Garred P., Lindstad J.K., Pharo A., Müller F., Stahl G.L., Lambris J.D., Mollnes T.E. The role of properdin in zymosan- and Escherichia coli-induced complement activation. J. Immunol. 2012, 189:2606-2613.
40. Harrison P., Cramer E.M. Platelet alpha-granules. Blood Rev. 1993, 7:52-62.
41. Heinekamp T., Schmidt H., Lapp K., Pahtz V., Shopova I., Koster-Eiserfunke N., Kruger T., Kniemeyer O., Brakhage A.A. Interference of Aspergillus fumigatus with the immune response. Semin. Immunopathol. 2014.
42. Hillmen P., Muus P., Duhrsen U., Risitano A.M., Schubert J., Luzzatto L., Schrezenmeier H., Szer J., Brodsky R.A., Hill A., Socie G., Bessler M., Rollins S.A., Bell L., Rother R.P., Young N.S. Effect of the complement inhibitor eculizumab on thromboembolism in patients with paroxysmal nocturnal hemoglobinuria. Blood 2007, 110:4123-4128.
43. Holmsen H. Platelet Secretion and Energy Metabolism 1994, Lippincott Williams & Walins, Philadelphia.
44. Honda S., Saito M., Dimaano E.M., Morales P.A., Alonzo M.T., Suarez L.A., Koike N., Inoue S., Kumatori A., Matias R.R., Natividad F.F., Oishi K. Increased phagocytosis of platelets from patients with secondary dengue virus infection by human macrophages. Am. J. Tropic. Med. Hyg. 2009, 80:841-845.
45. Hottz E.D., Lopes J.F., Freitas C., Valls-de-Souza R., Oliveira M.F., Bozza M.T., Da Poian A.T., Weyrich A.S., Zimmerman G.A., Bozza F.A., Bozza P.T. Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation. Blood 2013, 122:3405-3414.
46. Houle J.J., Leddy J.P., Rosenfeld S.I. Secretion of the terminal complement proteins, C5-C9, by human platelets. Clin. Immunol. Immunopathol. 1989, 50:385-393.
47. Humphrey J.H. Origin of blood platelets. Nature 1955, 176:38.
48. Hymes K., Nardi M., Leaf A., Karpatkin S. Role of leuCAM integrins and complement in platelet-monocyte rosette formation induced by immune complexes of human immunodeficiency virus-type 1-immune thrombocytopenic purpura patients. Blood 1993, 81:2375-2380.
49. Johnsen J. Pathogenesis in immune thrombocytopenia: new insights. Hematology/the education program of the American Society of Hematology. Am. Soc. Hematol. Educ. Program 2012, 2012:306-312.
50. Johnson M.K., Boese-Marrazzo D., Pierce W.A. Effects of pneumolysin on human polymorphonuclear leukocytes and platelets. Infect. Immun. 1981, 34:171-176.
51. Karpman D., Papadopoulou D., Nilsson K., Sjogren A.C., Mikaelsson C., Lethagen S. Platelet activation by Shiga toxin and circulatory factors as a pathogenetic mechanism in the hemolytic uremic syndrome. Blood 2001, 97:3100-3108.
52. Kavanagh D., Goodship T.H., Richards A. Atypical hemolytic uremic syndrome. Semin. Nephrol. 2013, 33:508-530.
53. Kenney D.M., Davis A.E. Association of alternative complement pathway components with human blood platelets: secretion and localization of factor D and beta 1H Globulin. Clin. Immunol. Immunopathol. 1981, 21:351-363.
54. Kozel T.R. Activation of the complement system by pathogenic fungi. Clin. Microbiol. Rev. 1996, 9:34-46.
55. Kozel T.R., Weinhold L.C., Lupan D.M. Distinct characteristics of initiation of the classical and alternative complement pathways by Candida albicans. Infect. Immun. 1996, 64:3360-3368.
56. Kravitz M.S., Shoenfeld Y. Thrombocytopenic conditions-autoimmunity and hypercoagulability: commonalities and differences in ITP, TTP, HIT, and APS. Am. J. Hematol. 2005, 80:232-242.
57. Kusaba G., Ohsawa I., Ishii M., Inoshita H., Ohi H., Horikoshi S., Takase M., Yamaguchi Y., Tomino Y. Evidence of immunopathological traces in mucormycosis: an autopsy case. Clin. Exp. Nephrol. 2010, 14:396-400.
58. Larsson R., Elgue G., Larsson A., Ekdahl K.N., Nilsson U.R., Nilsson B. Inhibition of complement activation by soluble recombinant CR1 under conditions resembling those in a cardiopulmonary circuit: reduced up-regulation of CD11b and complete abrogation of binding of PMNs to the biomaterial surface. Immunopharmacology 1997, 38:119-127.
59. Lewis R.E., Kontoyiannis D.P. Invasive aspergillosis in glucocorticoid-treated patients. Med. Mycol. 2009, 47(Suppl. 1):S271-S281.
60. Li Z., Yang F., Dunn S., Gross A.K., Smyth S.S. Platelets as immune mediators: their role in host defense responses and sepsis. Thromb. Res. 2011, 127:184-188.
61. Lin C.F., Lei H.Y., Liu C.C., Liu H.S., Yeh T.M., Wang S.T., Yang T.I., Sheu F.C., Kuo C.F., Lin Y.S. Generation of IgM anti-platelet autoantibody in dengue patients. J. Med. Virol. 2001, 63:143-149.
62. Lonze B.E., Zachary A.A., Magro C.M., Desai N.M., Orandi B.J., Dagher N.N., Singer A.L., Carter-Monroe N., Nazarian S.M., Segev D.L., Streiff M.B., Montgomery R.A. Eculizumab prevents recurrent antiphospholipid antibody syndrome and enables successful renal transplantation. Am. J. Transpl. 2014, 14:459-465.
63. Lood C., Amisten S., Gullstrand B., Jonsen A., Allhorn M., Truedsson L., Sturfelt G., Erlinge D., Bengtsson A.A. Platelet transcriptional profile and protein expression in patients with systemic lupus erythematosus: up-regulation of the type I interferon system is strongly associated with vascular disease. Blood 2010, 116:1951-1957.
64. Lundquist A.L., Chari R.S., Wood J.H., Miller G.G., Schaefer H.M., Raiford D.S., Wright K.J., Gorden D.L. Serum sickness following rabbit antithymocyte-globulin induction in a liver transplant recipient: case report and literature review. Liver Transpl. 2007, 13:647-650.
65. Luo S., Skerka C., Kurzai O., Zipfel P.F. Complement and innate immune evasion strategies of the human pathogenic fungus Candida albicans. Mol. Immunol. 2013, 56:161-169.
66. Mantadakis E., Samonis G. Clinical presentation of zygomycosis. Clin. Microbiol. Infect. 2009, 15(Suppl. 5):15-20.
67. Martel C., Cointe S., Maurice P., Matar S., Ghitescu M., Theroux P., Bonnefoy A. Requirements for membrane attack complex formation and anaphylatoxins binding to collagen-activated platelets. PLoS ONE 2011, 6:e18812.
68. Masliah-Planchon J., Darnige L., Bellucci S. Molecular determinants of platelet delta storage pool deficiencies: an update. Br. J. Haematol. 2013, 160:5-11.
69. Mershon-Shier K.L., Vasuthasawat A., Takahashi K., Morrison S.L., Beenhouwer D.O. In vitro C3 deposition on Cryptococcus capsule occurs via multiple complement activation pathways. Mol. Immunol. 2011, 48:2009-2018.
70. Miajlovic H., Loughman A., Brennan M., Cox D., Foster T.J. Both complement- and fibrinogen-dependent mechanisms contribute to platelet aggregation mediated by Staphylococcus aureus clumping factor B. Infect. Immun. 2007, 75:3335-3343.
71. Morgan B.P. Isolation and characterization of the complement-inhibiting protein CD59 antigen from platelet membranes. Biochem. J. 1992, 282(Pt 2):409-413.
72. Nascimento E.J., Hottz E.D., Garcia-Bates T.M., Bozza F., Marques E.T., Barratt-Boyes S.M. Emerging concepts in dengue pathogenesis: interplay between plasmablasts, platelets, and complement in triggering vasculopathy. Crit. Rev. Immunol. 2014, 34:227-240.
73. Nascimento E.J., Silva A.M., Cordeiro M.T., Brito C.A., Gil L.H., Braga-Neto U., Marques E.T. Alternative complement pathway deregulation is correlated with dengue severity. PLoS ONE 2009, 4:e6782.
74. Nicholson-Weller A., March J.P., Rosen C.E., Spicer D.B., Austen K.F. Surface membrane expression by human blood leukocytes and platelets of decay-accelerating factor, a regulatory protein of the complement system. Blood 1985, 65:1237-1244.
75. Nilsson B., Ekdahl K.N. Complement diagnostics: concepts, indications, and practical guidelines. Clin. Dev. Immunol. 2012, 2012:962702.
76. Nilsson B., Ekdahl K.N., Mollnes T.E., Lambris J.D. The role of complement in biomaterial-induced inflammation. Mol. Immunol. 2007, 44:82-94.
77. Nilsson B., Nilsson Ekdahl K. The tick-over theory revisited: is C3 a contact-activated protein?. Immunobiology 2012, 217:1106-1110.
78. Nilsson P.H., Ekdahl K.N., Magnusson P.U., Qu H., Iwata H., Ricklin D., Hong J., Lambris J.D., Nilsson B., Teramura Y. Autoregulation of thromboinflammation on biomaterial surfaces by a multicomponent therapeutic coating. Biomaterials 2013, 34:985-994.
79. Nilsson P.H., Engberg A.E., Back J., Faxalv L., Lindahl T.L., Nilsson B., Ekdahl K.N. The creation of an antithrombotic surface by apyrase immobilization. Biomaterials 2010, 31:4484-4491.
80. Nouer S.A., Nucci M., Kumar N.S., Grazziutti M., Restrepo A., Anaissie E. Baseline platelet count and creatinine clearance rate predict the outcome of neutropenia-related invasive aspergillosis. Clin. Infect. Dis. 2012, 54:e173-e183.
81. Ntefidou M., Elsner C., Spreer A., Weinstock N., Kratzin H.D., Ruchel R. Blood coagulation in domestic deep-seated mycoses. Mycoses 2002, 45(Suppl. 1):53-56.
82. 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, 17:515-520.
83. Nurden A.T. Platelets, inflammation and tissue regeneration. Thromb. Haemost. 2011, 105(Suppl. 1):S13-S33.
84. Orth D., Khan A.B., Naim A., Grif K., Brockmeyer J., Karch H., Joannidis M., Clark S.J., Day A.J., Fidanzi S., Stoiber H., Dierich M.P., Zimmerhackl L.B., Wurzner R. Shiga toxin activates complement and binds factor H: evidence for an active role of complement in hemolytic uremic syndrome. J. Immunol. 2009, 182:6394-6400.
85. Orth-Holler D., Riedl M., Wurzner R. Inhibition of terminal complement activation in severe Shiga toxin-associated HUS - perfect example for a fast track from bench to bedside. EMBO Mol. Med. 2011, 3:617-619.
86. Orth-Holler D., Wurzner R. Role of complement in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Semin. Thromb. Hemost. 2014, 40:503-507.
87. Patzelt J., Mueller K.A., Breuning S., Karathanos A., Schleicher R., Seizer P., Gawaz M., Langer H.F., Geisler T. Expression of anaphylatoxin receptors on platelets in patients with coronary heart disease. Atherosclerosis 2015, 238:289-295.
88. Peerschke E.I., Ghebrehiwet B. Human blood platelets possess specific binding sites for C1q. J. Immunol. 1987, 138:1537-1541.
89. Peerschke E.I., Ghebrehiwet B. C1q augments platelet activation in response to aggregated Ig. J. Immunol. 1997, 159:5594-5598.
90. Peerschke E.I., Ghebrehiwet B. Platelet receptors for the complement component C1q: implications for hemostasis and thrombosis. Immunobiology 1998, 199:239-249.
91. Peerschke E.I., Ghebrehiwet B. Human blood platelet gC1qR/p33. Immunol. Rev. 2001, 180:56-64.
92. Peerschke E.I., Murphy T.K., Ghebrehiwet B. Activation-dependent surface expression of gC1qR/p33 on human blood platelets. Thromb. Haemost. 2003, 89:331-339.
93. Peerschke E.I., Reid K.B., Ghebrehiwet B. Identification of a novel 33-kDa C1q-binding site on human blood platelets. J. Immunol. 1994, 152:5896-5901.
94. Peerschke E.I., Yin W., Ghebrehiwet B. Complement activation on platelets: implications for vascular inflammation and thrombosis. Mol. Immunol. 2010, 47:2170-2175.
95. Peerschke E.I., Yin W., Grigg S.E., Ghebrehiwet B. Blood platelets activate the classical pathway of human complement. J. Thromb. Haemost. 2006, 4:2035-2042.
96. Perkhofer S., Kainzner B., Kehrel B.E., Dierich M.P., Nussbaumer W., Lass-Florl C. Potential antifungal effects of human platelets against zygomycetes in vitro. J. Infect. Dis. 2009, 200:1176-1179.
97. Perkhofer S., Kehrel B.E., Dierich M.P., Donnelly J.P., Nussbaumer W., Hofmann J., von Eiff C., Lass-Florl C. Human platelets attenuate Aspergillus species via granule-dependent mechanisms. J. Infect. Dis. 2008, 198:1243-1246.
98. Perkhofer S., Niederegger H., Blum G., Burgstaller W., Ledochowski M., Dierich M.P., Lass-Florl C. Interaction of 5-hydroxytryptamine (serotonin) against Aspergillus spp. in vitro. Int. J. Antimicrob. Agents 2007, 29:424-429.
99. Polley M.J., Nachman R.L. Human platelet activation by C3a and C3a des-arg. J. Exp. Med. 1983, 158:603-615.
100. Poolpol K., Orth-Holler D., Speth C., Zipfel P.F., Skerka C., de Cordoba S.R., Brockmeyer J., Bielaszewska M., Wurzner R. Interaction of Shiga toxin 2 with complement regulators of the factor H protein family. Mol. Immunol. 2014, 58:77-84.
101. Punyadee N., Mairiang D., Thiemmeca S., Komoltri C., Pan-Ngum W., Chomanee N., Charngkaew K., Tangthawornchaikul N., Limpitikul W., Vasanawathana S., Malasit P., Avirutnan P. Microparticles provide a novel biomarker to predict severe clinical outcomes of dengue virus infection. J. Virol. 2015, 89:1587-1607.
102. Rambach G., Dum D., Mohsenipour I., Hagleitner M., Wurzner R., Lass-Florl C., Speth C. Secretion of a fungal protease represents a complement evasion mechanism in cerebral aspergillosis. Mol. Immunol. 2010, 47:1438-1449.
103. Richardson J.L., Shivdasani R.A., Boers C., Hartwig J.H., Italiano J.E. Mechanisms of organelle transport and capture along proplatelets during platelet production. Blood 2005, 106:4066-4075.
104. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 2010, 11:785-797.
105. Rinaldi M., Perricone C., Ortega-Hernandez O.D., Perricone R., Shoenfeld Y. Immune thrombocytopaenic purpura: an autoimmune cross-link between infections and vaccines. Lupus 2014, 23:554-567.
106. Risitano A.M. Paroxysmal nocturnal hemoglobinuria and other complement-mediated hematological disorders. Immunobiology 2012, 217:1080-1087.
107. Robert R., Mahaza C., Miegeville M., Ponton J., Marot-Leblond A., Senet J.M. Binding of resting platelets to Candida albicans germ tubes. Infect. Immun. 1996, 64:3752-3757.
108. Robert R., Nail S., Marot-Leblond A., Cottin J., Miegeville M., Quenouillere S., Mahaza C., Senet J.M. Adherence of platelets to Candida species in vivo. Infect. Immun. 2000, 68:570-576.
109. Rodland E.K., Ueland T., Pedersen T.M., Halvorsen B., Muller F., Aukrust P., Froland S.S. Activation of platelets by Aspergillus fumigatus and potential role of platelets in the immunopathogenesis of Aspergillosis. Infect. Immun. 2010, 78:1269-1275.
110. Rosenhagen M., Feldhues R., Schmidt J., Hoppe-Tichy T., Geiss H.K. A risk profile for invasive aspergillosis in liver transplant recipients. Infection 2009, 37:313-319.
111. Saggu G., Cortes C., Emch H.N., Ramirez G., Worth R.G., Ferreira V.P. Identification of a novel mode of complement activation on stimulated platelets mediated by properdin and C3(H2O). J. Immunol. 2013, 190:6457-6467.
112. Santoso S., Sachs U.J., Kroll H., Linder M., Ruf A., Preissner K.T., Chavakis T. The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J. Exp. Med. 2002, 196:679-691.
113. Schmaier A.H., Smith P.M., Colman R.W. Platelet C1-inhibitor. A secreted alpha-granule protein. J. Clin. Investig. 1985, 75:242-250.
114. Semple J.W., Italiano J.E., Freedman J. Platelets and the immune continuum. Nat. Rev. Immunol. 2011, 11:264-274.
115. Sims P.J., Faioni E.M., Wiedmer T., Shattil S.J. Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J. Biol. Chem. 1988, 263:18205-18212.
116. Sims P.J., Wiedmer T. Induction of cellular procoagulant activity by the membrane attack complex of complement. Semin. Cell Biol. 1995, 6:275-282.
117. Skoglund C., Wettero J., Bengtsson T. C1q regulates collagen-dependent production of reactive oxygen species, aggregation and levels of soluble P-selectin in whole blood. Immunol. Lett. 2012, 142:28-33.
118. Skoglund C., Wettero J., Tengvall P., Bengtsson T. C1q induces a rapid up-regulation of P-selectin and modulates collagen- and collagen-related peptide-triggered activation in human platelets. Immunobiology 2010, 215:987-995.
119. Speth C., Blum G., Hagleitner M., Hortnagl C., Pfaller K., Posch B., Ott H.W., Wurzner R., Lass-Florl C., Rambach G. Virulence and thrombocyte affectation of two Aspergillus terreus isolates differing in amphotericin B susceptibility. Med. Microbiol. Immunol. (Berl) 2013, 202:379-389.
120. Speth C., Hagleitner M., Ott H.W., Wurzner R., Lass-Florl C., Rambach G. Aspergillus fumigatus activates thrombocytes by secretion of soluble compounds. J. Infect. Dis. 2013, 207:823-833.
121. Speth C., Loffler J., Krappmann S., Lass-Florl C., Rambach G. Platelets as immune cells in infectious diseases. Future Microbiol. 2013, 8:1431-1451.
122. Speth C., Prodinger W., Wurzner R., Stoiber H., Dierich M.P. Complement. Fundamental Immunology 2008, 1047-1078. Lippincott Williams & Wilkins, Philadelphia, PA, USA. W.E. Paul (Ed.).
123. Speth C., Rambach G., Wurzner R., Lass-Florl C. Complement and fungal pathogens: an update. Mycoses 2008, 51:477-496.
124. Spitzer D., Mitchell L.M., Atkinson J.P., Hourcade D.E. Properdin can initiate complement activation by binding specific target surfaces and providing a platform for de novo convertase assembly. J. Immunol. 2007, 179:2600-2608.
125. Srichaikul T., Nimmannitya S. Haematology in dengue and dengue haemorrhagic fever. Bailliere's best practice & research. Clin. Haematol. 2000, 13:261-276.
126. Stahl A.L., Vaziri-Sani F., Heinen S., Kristoffersson A.C., Gydell K.H., Raafat R., Gutierrez A., Beringer O., Zipfel P.F., Karpman D. Factor H dysfunction in patients with atypical hemolytic uremic syndrome contributes to complement deposition on platelets and their activation. Blood 2008, 111:5307-5315.
127. Strakhan M., Hurtado-Sbordoni M., Galeas N., Bakirhan K., Alexis K., Elrafei T. 36-year-old female with catastrophic antiphospholipid syndrome treated with eculizumab: a case report and review of literature. Case Rep. Hematol. 2014, 2014:704371.
128. Sturtevant J.E., Latge J.P. Interactions between conidia of Aspergillus fumigatus and human complement component C3. Infect. Immun. 1992, 60:1913-1918.
129. Sun D.S., King C.C., Huang H.S., Shih Y.L., Lee C.C., Tsai W.J., Yu C.C., Chang H.H. Antiplatelet autoantibodies elicited by dengue virus non-structural protein 1 cause thrombocytopenia and mortality in mice. J. Thromb. Haemost. 2007, 5:2291-2299.
130. Tang Y.Q., Yeaman M.R., Selsted M.E. Antimicrobial peptides from human platelets. Infect. Immun. 2002, 70:6524-6533.
131. Tati R., Kristoffersson A.C., Stahl A.L., Rebetz J., Wang L., Licht C., Motto D., Karpman D. Complement activation associated with ADAMTS13 deficiency in human and murine thrombotic microangiopathy. J. Immunol. 2013, 191:2184-2193.
132. Torres C.S., Dupla A.M., Perez D.R., Aliaga M.Y., Rebage M.V. Nosocomial Candida infections and thrombocytopenia in very low birth weight newborns. An. Pediatr. (Barc.) 2007, 67:544-547.
133. Tschopp J., Jenne D.E., Hertig S., Preissner K.T., Morgenstern H., Sapino A.P., French L. Human megakaryocytes express clusterin and package it without apolipoprotein A-1 into alpha-granules. Blood 1993, 82:118-125.
134. Vaziri-Sani F., Hellwage J., Zipfel P.F., Sjoholm A.G., Iancu R., Karpman D. Factor H binds to washed human platelets. J. Thromb. Haemost. 2005, 3:154-162.
135. Verschoor A., Langer H.F. Crosstalk between platelets and the complement system in immune protection and disease. Thromb. Haemost. 2013, 110:910-919.
136. Verschoor A., Neuenhahn M., Navarini A.A., Graef P., Plaumann A., Seidlmeier A., Nieswandt B., Massberg S., Zinkernagel R.M., Hengartner H., Busch D.H. A platelet-mediated system for shuttling blood-borne bacteria to CD8alpha+ dendritic cells depends on glycoprotein GPIb and complement C3. Nat. Immunol. 2011, 12:1194-1201.
137. Vik D.P., Fearon D.T. Cellular distribution of complement receptor type 4 (CR4): expression on human platelets. J. Immunol. 1987, 138:254-258.
138. Waldorf A.R., Diamond R.D. Neutrophil chemotactic responses induced by fresh and swollen Rhizopus oryzae spores and Aspergillus fumigatus conidia. Infect. Immun. 1985, 48:458-463.
139. Watanabe H., Kuraya M., Kasukawa R., Yanagisawa H., Yanagisawa M., Fujita T. Analysis of C5a receptor by monoclonal antibody. J. Immunol. Methods 1995, 185:19-29.
140. Weber C., Springer T.A. Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to alphaIIbbeta3 and stimulated by platelet-activating factor. J. Clin. Investig. 1997, 100:2085-2093.
141. Wiedmer T., Esmon C.T., Sims P.J. Complement proteins C5b-9 stimulate procoagulant activity through platelet prothrombinase. Blood 1986, 68:875-880.
142. Wiedmer T., Hall S.E., Ortel T.L., Kane W.H., Rosse W.F., Sims P.J. Complement-induced vesiculation and exposure of membrane prothrombinase sites in platelets of paroxysmal nocturnal hemoglobinuria. Blood 1993, 82:1192-1196.
143. Wiedmer T., Sims P.J. Participation of protein kinases in complement C5b-9-induced shedding of platelet plasma membrane vesicles. Blood 1991, 78:2880-2886.
144. Willcox M.D., Webb B.C., Thakur A., Harty D.W. Interactions between Candida species and platelets. J. Med. Microbiol. 1998, 47:103-110.
145. Woth G., Tokes-Fuzesi M., Magyarlaki T., Kovacs G.L., Vermes I., Muhl D. Activated platelet-derived microparticle numbers are elevated in patients with severe fungal (Candida albicans) sepsis. Ann. Clin. Biochem. 2012, 49:554-560.
146. Wright J.F., Blanchette V.S., Wang H., Arya N., Petric M., Semple J.W., Chia W.K., Freedman J. Characterization of platelet-reactive antibodies in children with varicella-associated acute immune thrombocytopenic purpura (ITP). Br. J. Haematol. 1996, 95:145-152.
147. Yeaman M.R., Soldan S.S., Ghannoum M.A., Edwards J.E., Filler S.G., Bayer A.S. Resistance to platelet microbicidal protein results in increased severity of experimental Candida albicans endocarditis. Infect. Immun. 1996, 64:1379-1384.
148. Yin W., Ghebrehiwet B., Peerschke E.I. Expression of complement components and inhibitors on platelet microparticles. Platelets 2008, 19:225-233.
149. Yu G.H., Holers V.M., Seya T., Ballard L., Atkinson J.P. Identification of a third component of complement-binding glycoprotein of human platelets. J. Clin. Investig. 1986, 78:494-501.