Streptococcus sanguis-induced platelet activation involves two waves of tyrosine phosphorylation mediated by FcγRIIA and αIIbβ3

Caroline Pampolina; Archibald McNicol

doi:10.1160/TH04-08-0482

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2005; 93(05): 932-939
DOI: 10.1160/TH04-08-0482

Platelets and Blood Cells

Schattauer GmbH

Streptococcus sanguis-induced platelet activation involves two waves of tyrosine phosphorylation mediated by FcγRIIA and α_IIbβ₃

Caroline Pampolina

,

Archibald McNicol

Abstract

Summary

The low-affinity IgG receptor, FcγRIIA, has been implicated in Streptococcus sanguis-induced platelet aggregation. Therefore, it is likely that signal transduction is at least partly mediated by FcγRIIA activation and a tyrosine kinase-dependent pathway. In this study the signal transduction mechanisms associated with platelet activation in response to the oral bacterium, S. sanguis were characterised. In the presence of IgG, S. sanguis strain 2017–78 caused the tyrosine phosphorylation of FcγRIIA 30s following stimulation, which led to the phosphorylation of Syk, LAT, and PLCγ2. These early events were dependent on Src family kinases but independent of either TxA₂ or the engagement of the α_IIbβ₃ integrin. During the lag phase prior to platelet aggregation, FcγRIIA, Syk, LAT, and PLCγ2 were each dephosphorylated, but were re-phosphorylated as aggregation occurred. Platelet stimulation by 2017–78 also induced the tyrosine phosphorylation of PECAM-1, an ITIM-containing receptor that recruits protein tyrosine phosphatases. PECAM-1 co-precipitated with the protein tyrosine phosphatase SHP-1 in the lag phase. SHP-1 was also maximally tyrosine phosphorylated during this phase, suggesting a possible role for SHP-1 in the observed dephosphorylation events. As aggregation occurred, SHP-1 was dephosphorylated, while FcγRIIA, Syk, LAT, and PLCγ2 were rephosphorylated in an RGDS-sensitive, and therefore α_IIbβ₃-dependent, manner. Additionally, TxA₂ release, 5-hydro-xytryptamine secretion and phosphatidic acid formation were all blocked by RGDS. Aspirin also abolished these events, but only partially inhibited α_IIbβ₃-mediated re-phosphorylation. Therefore, S.sanguis-bound IgG cross links FcγRIIA and initiates a signaling pathway that is down-regulated by PECAM-1-bound SHP-1. Subsequent engagement of α_IIbβ₃ leads to SHP-1 dephosphorylation permiting a second wave of signaling leading to TxA₂ release and consequent platelet aggregation.

Keywords

FcγRIIA - platelet - PECAM-1 - SHP-1 - Streptococcus sanguis

Full Text

References

References
1 Mattila KJ, Nieminen MS, Valtonen VV. et al. Association between dental health and acute myocardial infarction. Br Med J 1989; 298: 779-82.
2 Beck J, Garcia R, Heiss G. et al. Periodontal disease and cardiovascular disease. J Periodontol 1996; 67: 1123-37.
3 Morrison I H, Ellison LF, Taylor GW. Periodontal disease and risk of fatal coronary heart and cerebrovascular diseases. J Cardiovasc Risk 1999; 6: 7-11.
4 Lusis AJ. Atherosclerosis. Nature 2000; 407: 233-41.
5 Gupta S, Camm AJ. Is there an infective aetiology to atherosclerosis?. Drugs Aging 1998; 13: 1-7.
6 Danesh J. Is there a link between chronic Helicobacter pylori infection and coronary heart disease?. Eur J Surg Suppl 1998; 582: 27-31.
7 Griffiths PD, Hannington G, Booth JC. Coxsackie B virus infections and myocardial infarction. Results from a prospective, epidemiologically controlled study. Lancet 1980; 1: 1387-9.
8 Herzberg MC, Brintzenhofe KL, Clawson CC. Aggregation of human platelets and adhesion of Streptococcus sanguis. Infect Immun 1983; 39: 1457-69.
9 Sullam PM, Valone FH, Mills J. Mechanisms of platelet aggregation by viridans group streptococci. Infect Immun 1987; 55: 1743-50.
10 Ford I, Douglas I CW, Preston FE. et al. Mechanisms of platelet aggregation by Streptococcus sanguis, a causative organismin infective endocarditis. Br J Haematol 1993; 84: 95-100.
11 Herzberg MC, Meyer MW. Effects of oral flora on platelets: possible consequences in cardiovascular disease. J Periodontol 1996; 67: 1138-42.
12 Herzberg MC, Meyer MW. Dental plaque, platelets, and cardiovascular diseases. Ann Periodontol 1998; 3: 151-60.
13 Meyer MW, Gong K, Herzberg MC. Streptococcus sanguis-induced platelet clotting in rabbits and hemodynamic and cardiopulmonary consequences. Infect Immun 1998; 66: 5906-14.
14 Soberay AH, Herzberg MC, Rudney JD. et al. Responses of platelets to strains of Streptococcus sanguis: findings in healthy subjects, Bernard-Soulier, Glanzmann's, and collagen-unresponsive patients. Thromb Haemost 1987; 57: 222-5.
15 Douglas CW, Brown PR, Preston FE. Platelet aggregation by oral streptococci. FEMS Micrbiol Lett 1990; 60: 63-7.
16 Kerrigan SW, Douglas I, Wray A. et al. A role for glycoprotein Ib in Streptococcus sanguis-induced platelet aggregation. Blood 2002; 100: 509-16.
17 Ford I, Douglas CW, Heath J. et al. Evidence for the involvement of complement proteins in platelet aggregationby Streptococcus sanguis NCTC 7863. Br JHaematol 1996; 94: 729-39.
18 Ford I, Douglas CW, Cox D. et al. The role of immunoglobulin G and fibrinogen in platelet aggregation by Streptococcus sanguis. Br J Haematol 1997; 97: 737-46.
19 Sjobring U, Ringdahl U, Ruggeri ZM. Induction of platelet thrombi by bacteria and antibodies. Blood 2002; 100: 4470-7.
20 Anderson GP, Anderson CL. Signal transduction by the platelet Fc receptor. Blood 1990; 76: 1165-72.
21 Daëron M. Structural bases of Fc gamma R functions. Annu Rev Immunol 1997; 15: 203-34.
22 Huang M-M, Indik Z, Brass LF. et al. Activation of Fc?RII induces tyrosine phosphorylation of multiple proteins including FcγRII. J Biol Chem 1992; 267: 5467-73.
23 Chacko GW, Duchemin A, Coggeshall KM. et al. Clustering of the platelet Fcγreceptor induces noncovalent association with the tyrosine kinase p72syk. J Biol Chem 1994; 269: 32435-40.
24 Keely PJ, Parise LV. The α2 β1 integrin is a necessary co-receptor for collagen-induced activation of Syk and the subsequent phosphorylation of phospholipase Cγin platelets. J Biol Chem 1996; 271: 26668-76.
25 Yanaga F, Poole A, Asselin J. et al. Syk interacts with tyrosine-phosphorylated proteins in human platelets activated by collagen and cross-linking of the Fcγ-IIA receptor. Biochem J 1995; 311: 471-8.
26 Gratacap M, Payrastre B, Viala C. et al. Phosphatidyl 3,4,5-trisphosphate-dependent stimulation of phospholipase Cγ-2 is an early key event in FcγRIIAmediated activation of human platelets. J Biol Chem 1998; 273: 24314-21.
27 Watson SP, Reep B, McConnell RT. et al. Collagen stimulates [3H] inositol trisphosphate formation in indomethacin- treated human platelets. Biochem J 1985; 226: 831-7.
28 Gergely J, Pecht I, Sarmay G. Immunoreceptor tyrosine- based inhibition motif-bearing receptors regulate the immunoreceptor tyrosine-based activation motif-induced activation of immune competent cells. Immunol Lett 1999; 68: 3-15.
29 Gibbins JM. The negative regulation of platelet function: extending the role of the ITIM. Trends Cardiovasc Med 2002; 12: 213-9.
30 Patil S, Newman DK, Newman PJ. Platelet endothelial cell adhesion molecule-1 serves as an inhibitory receptor that modulates platelet responses to collagen. Blood 2001; 97: 1727-32.
31 Jones KL, Hughan SC, Dopheide SM. et al. Platelet endothelial cell adhesionmolecule-1 is a negative regulator of platelet-collagen interactions. Blood 2001; 98: 1456-63.
32 Cicmil M, Thomas JM, Leduc M. et al. Platelet endothelial cell adhesion molecule-1 signaling inhibits the activation of human platelets. Blood 2002; 99: 137-44.
33 Thai LM, Ashman LK, Harbour SN. et al. Physical proximity and functional interplay of PECAM-1 with the Fc receptor FcγRIIa on the platelet plasma membrane. Blood 2003; 102: 3637-45.
34 McNicol A. Platelet preparation and estimation of functional responses. In: Platelets: A Practical Approach. Watson SP, Authi KS. eds Oxford: Oxford Univ. Press; 1996: 1-26.
35 Nguyen A, Packham MA, Rand ML. Effects of ethanol on platelet responses associated with adhesion to collagen. Thromb Res 1999; 95: 303-14.
36 Clark EA, Brugge JS. Tyrosine phosphorylation. In: Platelets: A Practical Approach. Watson SP, Authi KS. eds Oxford: Oxford Univ. Press; 1996: 199-215.
37 Cicmil M, Thomas JM, Sage T. et al. Collagen, convulxin, and thrombin stimulate aggregation-independent tyrosine phosphorylation of CD31 in platelets. Evidence for the involvement of Src family kinases. J Biol Chem 2000; 275: 27339-47.
38 Holmsen H, Dangelmaier CA, Rongved S. Tight coupling of thrombin-induced hydrolase secretion and phosphatidate synthesis to receptor occupancy in human platelets. Biochem J 1984; 222: 157-67.
39 Lockhart LK, McNicol A. The phospholipase Cinhibitor U73122 inhibits phorbol ester-induced platelet activation. J Pharmacol Exp Therap 1999; 289: 721-8.
40 Karni R, Mizrachi S, Reiss-Sklan E. et al. The pp60 (c-Src) inhibitor PP1 is non-competitive against ATP. FEBS Lett 2003; 537: 47-52.
41 Bodin S, Viala C, Ragab A. et al. A critical role of lipid rafts in the organization of a key FcγRIIa-mediated signaling pathway in human platelets. Thromb Haemost 2003; 89: 318-30.
42 Hua CT, Gamble JR, Vadas MA. et al. Recruitment and activation of SHP-1 protein-tyrosine phosphatase by human platelet endothelial cell adhesionmolecule-1 (PECAM-1). Identification of immunoreceptor tyrosine- based inhibitory motif-like binding motifs and substrates. J Biol Chem 1998; 273: 28332-40.
43 Jackson DE, Ward CM, Wang R. et al. The proteintyrosine phosphatase SHP-2 binds platelet/endothelial cell adhesionmolecule-1 (PECAM-1) and forms a distinct signaling complex during platelet aggregation. J Biol Chem 1997; 272: 6986-93.
44 Jackson DE, Kupcho KR, Newman PJ. Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase, SHP-2. J Biol Chem 1997; 272: 24868-75.
45 Kullo IJ, Gau GT, Tajik AJ. Novel risk factors for atherosclerosis. Mayo Clin Proc 2000; 75: 369-80.
46 Fong IW. Emerging relations between infectious diseases and coronary artery disease and atherosclerosis. CMAJ 2000; 163: 49-56.
47 Mealey BL. Influence of periodontal infections on systemic health. Periodontology 2000 1999; 21: 197-209.
48 Kinane DF. Periodontal diseases' contributions to cardiovascular disease: an overviewof potential mechanisms. Ann Periodontol 1998; 3: 142-50.
49 Schuster GS. Oral flora and pathogenic organisms. Infect Dis Clin NAm 1999; 13: 757-74.
50 Gong K, Wen DY, Ouyang T. et al. Platelet receptors for the Streptococcus sanguis adhesin and aggregationassociated antigens are distinguished by anti-idiotypical monoclonal antibodies. Infect Immun 1995; 63: 3628-33.
51 Sullam PM, Hyun WC, Szollosi J. et al. Physical proximity and functional interplay of the glycoprotein Ib-IX-V complex and the Fc receptor FcγRIIA on the platelet plasma membrane. J Biol Chem 1998; 273: 5331-6.
52 Ibarrola I, Vossebeld PJ, Homburg CH. et al. Influence of tyrosine phosphorylation on protein interaction with FcγRIIa. Biochim Biophys Acta 1997; 1357: 348-58.
53 Ragab A, Bodin S, Viala C. et al. The tyrosine phosphatase 1B regulates linker for activation of T-cell phosphorylation and platelet aggregation upon FcγRIIA cross-linking. J Biol Chem 2003; 278: 40923-32.
54 Rathore V, Stapleton MA, Hillery CA. et al. PECAM-1 negatively regulates GPIb/V/IX signaling in murine platelets. Blood 2003; 102: 3658-64.
55 Zhang Z, Shen K, Lu W. et al. The role of C-terminal tyrosine phosphorylation in the regulation of SHP-1 explored via expressed protein ligation. J Biol Chem 2002; 278: 4668-74.
56 Xu F, Xu M, Zhao R. et al. Tyrosine phosphatases SHP-1 and SHP-2 are associatedwith distinct tyrosinephosphorylated proteins. Exp Cell Res 2002; 272: 75-83.
57 Sagawa K, Kimura T, Swieter M. et al. The proteintyrosine phosphatase SHP-2 associates with tyrosinephosphorylated adhesionmolecule PECAM-1 (CD31). J Biol Chem 1997; 272: 31086-91.
58 Masuda M, Osawa M, Shigematsu H. et al. Platelet endothelial cell adhesion molecule-1 is a major SHPTP2 binding protein in vascular endothelial cells. FEBS Lett 1997; 408: 331-6.
59 Zhang J, Somani AK, Siminovitch KA. Roles of the SHP-1 tyrosine phosphatase in the negative regulation of cell signaling. Semin Immunol 2000; 12: 361-78.
60 Qu CK. The SHP-2 tyrosine phosphatase: signaling mechanisms and biological functions. Cell Res 2000; 10: 279-88.
61 Ganesan LP, Fang H, Marsh CB. et al. The proteintyrosine phosphatase SHP-1 associates with the phosphorylated immunoreceptor tyrosine-based activation motif of FcγRIIA tomodulate signaling events in myeloid cells. J Biol Chem 2003; 278: 35710-7.
62 Frank C, Burkhardt C, Imhof D. et al. Effective dephosphorylation of Src substrates by SHP-1. J Biol Chem 2004; 279: 11375-83.
63 Zhang J, Somani AK, Siminovitch KA. Roles of the SHP-1 tyrosine phosphatase in the negative regulation of cell signaling. Semin Immunol 2000; 12: 361-78.
64 Pasquet JM, Quek L, Pasquet S. et al. Evidence of a role for SHP-1 in platelet activation by the collagen receptor glycoprotein VI. J Biol Chem 2000; 275: 28526-31.
65 Cramer EM, Berger G, Berndt MC. Platelet α-granule and plasma membrane share two new components: CD9 and PECAM-1. Blood 1994; 84: 1722-30.
66 Erickson PR, Herzberg MC. Purification and partial characterization of a 65-k Da platelet aggregationassociated protein antigen from the surface of Streptococcus sanguis. J Biol Chem 1990; 265: 14080-7.
67 Erickson PR, Herzberg MC. The Streptococcus sanguis platelet aggregation-associated protein. Identification and characterization of the minimal plateletinteractive domain. J Biol Chem 1993; 268: 1646-9.
68 McRedmond JP, Harriott P, Walker B. et al. Streptokinase- induced platelet activation involves antistreptokinase antibodies and cleavage of protease-activated receptor-1. Blood 2000; 95: 1301-8.