The expanding field of platelet-bacterial interconnections

Platelets

Volumn 26, Issue 4, 2015, Pages 293-301

  Kerrigan, Steven W ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

Bacteria; Immune; Infection; Platelets; Staphylococcus; Streptococcus

Indexed keywords

COMPLEMENT COMPONENT C1Q; COMPLEMENT RECEPTOR; GLYCOPROTEIN IIB; GLYCOPROTEIN IIBIIIA; THROMBOCYTE RECEPTOR; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

BACTERIUM; HEMOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; REVIEW; THROMBOCYTE; THROMBOSIS; BLOOD; IMMUNOLOGY; INFECTION; INFLAMMATION;

ANIMALIA; BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS; STREPTOCOCCUS;

BACTERIA; BLOOD PLATELETS; HUMANS; INFECTION; INFLAMMATION;

EID: 84929325674     PISSN: 09537104     EISSN: 13691635     Source Type: Journal    
DOI: 10.3109/09537104.2014.997690     Document Type: Review

References (93)

1. Nieswandt B, Varga-Szabo D, Elvers M. Integrins in platelet activation. J Thromb Haemost 2009;7 Suppl 1:206-209.
2. Aird WC. Spatial and temporal dynamics of the endothelium. J Thromb Haemost 2005;3:1392-1406.
3. Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005;115:3378-3384.
4. 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: 4046-4054.
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;99:4021-4029.
6. Antczak AJ, Singh N, Gay SR, Worth RG. IgG-complex stimulated platelets: A source of sCD40L and RANTES in initiation of inflammatory cascade. Cell Immunol 2010;263:129-133.
7. Gleissner CA, von Hundelshausen P, Ley K. Platelet chemokines in vascular disease. Arterioscler Thromb Vasc Biol 2008;28: 1920-1927.
8. Yeaman MR. Bacterial-platelet interactions: Virulence meets host defense. Future Microbiol 2010;5:471-506.
9. Levaditi C. Et des organisms vaccines contre le vibron cholerique. Ann Inst Pasteur 1901;15:894-924.
10. Speth C, Rambach G, Lass-Florl C. Platelet immunology in fungal infections. Thromb Haemost 2014;112:632-639.
11. Flaujac C, Boukour S, Cramer-Borde E. Platelets and viruses: An ambivalent relationship. Cell Mol Life Sci 2010;67:545-556.
12. Kerrigan SW, Cox D. Platelet-bacterial interactions. Cell Mol Life Sci 2010;67:513-523.
13. Kerrigan SW, Douglas I, Wray A, Heath J, Byrne MF, Fitzgerald D, Cox D. A role for glycoprotein Ib in Streptococcus sanguis-induced platelet aggregation. Blood 2002;100:509-516.
14. Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, Foster TJ. Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 2010;156:920-928.
15. Loughman A, Fitzgerald JR, Brennan MP, Higgins J, Downer R, Cox D, Foster TJ. Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol Microbiol 2005;57:804-818.
16. Fitzgerald JR, Loughman A, Keane F, Brennan M, Knobel M, Higgins J, Speziale P, Cox D, Foster TJ. Fibronectin-binding proteins of Staphylococcus aureus mediate activation of human platelets via fibrinogen and fibronectin bridges to integrin GPIIb/IIIa and IgG binding to the FcgammaRIIa receptor. Mol Microbiol 2006; 59:212-230.
17. Siauw C, Kobsar A, Dornieden C, Beyrich C, Schinke B, Schubert-Unkmeir A, Abele-Horn M, Speer CP, Eigenthaler M. Group B streptococcus isolates from septic patients and healthy carriers differentially activate platelet signaling cascades. Thromb Haemost 2006;95:836-849.
18. Lourbakos A, Yuan YP, Jenkins AL, Travis J, Andrade-Gordon P, Santulli R, Potempa J, Pike RN. Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: A new trait in microbial pathogenicity. Blood 2001;97:3790-3797.
19. Stahl AL, Svensson M, Morgelin M, Svanborg C, Tarr PI, Mooney JC, Watkins SL, Johnson R, Karpman D. Lipopolysaccharide from enterohemorrhagic Escherichia coli binds to platelets through TLR4 and CD62 and is detected on circulating platelets in patients with hemolytic uremic syndrome. Blood 2006;108:167-176.
20. Byrne MF, Kerrigan SW, Corcoran PA, Atherton JC, Murray FE, Fitzgerald DJ, Cox DM. Helicobacter pylori binds von Willebrand factor and interacts with GPIba to induce platelet aggregation. Gastroenterology 2003;124:1846-1854.
21. Kerrigan SW, Jakubovics NS, Keane C, Maguire P, Wynne K, Jenkinson HF, Cox D. Role of Streptococcus gordonii surface proteins SspA/SspB and Hsa in platelet function. Infect Immun 2007;75:5740-5747.
22. Lopez JA. The platelet glycoprotein Ib-IX complex. Blood Coag Fibrinolysis: Int J Haemost Thromb 1994;5:97-119.
23. Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood 1996;88:1525-1541.
24. Li R, Emsley J. The organizing principle of the platelet glycoprotein Ib-IX-V complex. J Thromb Haemost 2013;11:605-614.
25. Canobbio I, Balduini C, Torti M. Signalling through the platelet glycoprotein Ib-V-IX complex. Cell Signal 2004;16:1329-1344.
26. Bensing BA, Lopez JA, Sullam PM. The Streptococcus gordonii surface proteins GspB and Hsa mediate binding to sialylated carbohydrate epitopes on the platelet membrane glycoprotein Ibalpha. Infect Immun 2004;72:6528-6537.
27. Takamatsu D, Bensing BA, Cheng H, Jarvis GA, Siboo IR, Lopez JA, Griffiss JM, Sullam PM. Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibalpha. Mol Microbiol 2005;58:380-392.
28. Pyburn TM, Bensing BA, Xiong YQ, Melancon BJ, Tomasiak TM, Ward NJ, Yankovskaya V, Oliver KM, Cecchini G, Sulikowski GA, et al. A structural model for binding of the serine-rich repeat adhesin GspB to host carbohydrate receptors. PLoS Pathogens 2011;7: e1002112.
29. Siboo IR, Chambers HF, Sullam PM. Role of SraP, a serine-rich surface protein of Staphylococcus aureus, in binding to human platelets. Infect Immun 2005;73:2273-2280.
30. O'Seaghdha M, van Schooten CJ, Kerrigan SW, Emsley J, Silverman GJ, Cox D, Lenting PJ, Foster TJ. Staphylococcus aureus protein A binding to von Willebrand factor A1 domain is mediated by conserved IgG binding regions. FEBS J 2006;273: 4831-4841.
31. Corcoran PA, Atherton JC, Kerrigan SW, Wadstrom T, Murray FE, Peek RM, Fitzgerald DJ, Cox DM, Byrne MF. The effect of different strains of Helicobacter pylori on platelet aggregation. Can J Gastroenterol 2007;21:367-370.
32. Fujimura K, Phillips DR. Calcium cation regulation of glycoprotein IIb-IIIa complex formation in platelet plasma membranes. J Biol Chem 1983;258:10247-10252.
33. Wagner CL, Mascelli MA, Neblock DS, Weisman HF, Coller BS, Jordan RE. Analysis of GPIIb/IIIa receptor number by quantification of 7E3 binding to human platelets. Blood 1996;88:907-914.
34. Trikha M, Timar J, Lundy SK, Szekeres K, Tang K, Grignon D, Porter AT, Honn KV. Human prostate carcinoma cells express functional alphaIIb(beta)3 integrin. Cancer Res 1996;56:5071-5078.
35. Ginsberg MH, O'Toole TE, Loftus JC, Plow EF. Ligand binding to integrins: Dynamic regulation and common mechanisms. Cold Spring Harbor Symp Quant Biol 1992;57:221-231.
36. Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 1996;12:697-715.
37. Cierniewski CS, Byzova T, Papierak M, Haas TA, Niewiarowska J, Zhang L, Cieslak M, Plow EF. Peptide ligands can bind to distinct sites in integrin alphaIIbbeta3 and elicit different functional responses. J Biol Chem 1999;274:16923-16932.
38. Duperray A, Berthier R, Chagnon E, Ryckewaert JJ, Ginsberg M, Plow E, Marguerie G. Biosynthesis and processing of platelet GPIIb-IIIa in human megakaryocytes. J Cell Biol 1987;104: 1665-1673.
39. Zimrin AB, Gidwitz S, Lord S, Schwartz E, Bennett JS, White 2nd GC,, Poncz M. The genomic organization of platelet glycoprotein IIIa. J Biol Chem 1990;265:8590-8595.
40. Carrell NA, Fitzgerald LA, Steiner B, Erickson HP, Phillips DR. Structure of human platelet membrane glycoproteins IIb and IIIa as determined by electron microscopy. J Biol Chem 1985;260: 1743-1749.
41. Vinogradova O, Vaynberg J, Kong X, Haas TA, Plow EF, Qin J. Membrane-mediated structural transitions at the cytoplasmic face during integrin activation. Proc Natl Acad Sci USA 2004;101: 4094-4099.
42. Arciola CR, Campoccia D, Gamberini S, Donati ME, Montanaro L. Presence of fibrinogen-binding adhesin gene in Staphylococcus epidermidis isolates from central venous catheters-associated and orthopaedic implant-associated infections. Biomaterials 2004;25: 4825-4829.
43. Brennan MP, Loughman A, Devocelle M, Arasu S, Chubb AJ, Foster TJ, Cox D. Elucidating the role of Staphylococcus epidermidis serine-aspartate repeat protein G in platelet activation. J Thromb Haemost 2009;7:1364-1372.
44. Petersen HJ, Keane C, Jenkinson HF, Vickerman MM, Jesionowski A, Waterhouse JC, Cox D, Kerrigan SW. Human platelets recognize a novel surface protein, PadA, on Streptococcus gordonii through a unique interaction involving fibrinogen receptor GPIIbIIIa. Infect Immun 2010;78:413-422.
45. Keane C, Petersen H, Reynolds K, Newman DK, Cox D, Jenkinson HF, Newman PJ, Kerrigan SW. Mechanism of outside-in {alpha}IIb{beta}3-mediated activation of human platelets by the colonizing Bacterium, Streptococcus gordonii. Arterioscler Thromb Vasc Biol 2010;30:2408-2415.
46. Keane C, Petersen HJ, Tilley DO, Haworth J, Cox D, Jenkinson HF, Kerrigan SW. Multiple sites on Streptococcus gordonii surface protein PadA bind to platelet GPIIbIIIa. Thromb Haemost 2013;110: 1278-1287.
47. McDevitt D, Francois P, Vaudaux P, Foster TJ. Identification of the ligand-binding domain of the surface-located fibrinogen receptor (clumping factor) of Staphylococcus aureus. Mol Microbiol 1995; 16:895-907.
48. McDevitt D, Nanavaty T, House-Pompeo K, Bell E, Turner N, McIntire L, Foster T, Höök M. Characterization of the interaction between the Staphylococcus aureus clumping factor (ClfA) and fibrinogen. Eur J Biochem/FEBS 1997;247:416-424.
49. Walsh EJ, Miajlovic H, Gorkun OV, Foster TJ. Identification of the Staphylococcus aureus MSCRAMM clumping factor B (ClfB) binding site in the alphaC-domain of human fibrinogen. Microbiology 2008;154:550-558.
50. Signas C, Raucci G, Jonsson K, Lindgren PE, Anantharamaiah GM, Hook M, Lindberg M. Nucleotide sequence of the gene for a fibronectin-binding protein from Staphylococcus aureus: Use of this peptide sequence in the synthesis of biologically active peptides. Proc Natl Acad Sci USA 1989;86:699-703.
51. Wann ER, Gurusiddappa S, Hook M. The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J Biol Chem 2000;275: 13863-13871.
52. Davis SL, Gurusiddappa S, McCrea KW, Perkins S, Hook M. SdrG, a fibrinogen-binding bacterial adhesin of the microbial surface components recognizing adhesive matrix molecules subfamily from Staphylococcus epidermidis, targets the thrombin cleavage site in the Bbeta chain. J Biol Chem 2001;276:27799-27805.
53. Hartford O, O'Brien L, Schofield K, Wells J, Foster TJ. The Fbe (SdrG) protein of Staphylococcus epidermidis HB promotes bacterial adherence to fibrinogen. Microbiology 2001;147:2545-2552.
54. Cunningham MW. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 2000;13:470-511.
55. Andre I, Persson J, Blom AM, Nilsson H, Drakenberg T, Lindahl G, Linse S. Streptococcal M protein: Structural studies of the hypervariable region, free and bound to human C4BP. Biochemistry 2006;45:4559-4568.
56. Carlsson F, Sandin C, Lindahl G. Human fibrinogen bound to Streptococcus pyogenes M protein inhibits complement deposition via the classical pathway. Mol Microbiol 2005;56:28-39.
57. Shannon O, Hertzen E, Norrby-Teglund A, Morgelin M, Sjobring U, Bjorck L. Severe streptococcal infection is associated with M protein-induced platelet activation and thrombus formation. Mol Microbiol 2007;65:1147-1157.
58. Pietrocola G, Schubert A, Visai L, Torti M, Fitzgerald JR, Foster TJ, Reinscheid DJ, Speziale P. FbsA, a fibrinogen-binding protein from Streptococcus agalactiae, mediates platelet aggregation. Blood 2005;105:1052-1059.
59. Schubert A, Zakikhany K, Schreiner M, Frank R, Spellerberg B, Eikmanns BJ, Reinscheid DJ. A fibrinogen receptor from group B Streptococcus interacts with fibrinogen by repetitive units with novel ligand binding sites. Mol Microbiol 2002;46:557-569.
60. Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nature reviews. Immunology 2008;8:34-47.
61. Karas SP, Rosse WF, Kurlander RJ. Characterization of the IgG-Fc receptor on human platelets. Blood 1982;60:1277-1282.
62. McCrae KR, Shattil SJ, Cines DB. Platelet activation induces increased Fc gamma receptor expression. J Immunol 1990;144: 3920-3927.
63. Anderson CL, Chacko GW, Osborne JM, Brandt JT. The Fc receptor for immunoglobulin G (Fc gamma RII) on human platelets. Semin Thromb Hemost 1995;21:1-9.
64. Van den Herik-Oudijk IE, Capel PJ, van der Bruggen T, Van de Winkel JG. Identification of signaling motifs within human Fc gamma RIIa and Fc gamma RIIb isoforms. Blood 1995;85: 2202-2211.
65. Kerrigan SW, Clarke N, Loughman A, Meade G, Foster TJ, Cox D. Molecular basis for Staphylococcus aureus-mediated platelet aggregate formation under arterial shear in vitro. Arterioscler Thromb Vasc Biol 2008;28:335-340.
66. Keane C, Tilley D, Cunningham A, Smolenski A, Kadioglu A, Cox D, Jenkinson HF, Kerrigan SW. Invasive Streptococcus pneumoniae trigger platelet activation via Toll-like receptor 2. J Thromb Haemost 2010;8:2757-2765.
67. Tilley DO, Arman M, Smolenski A, Cox D, O'Donnell JS, Douglas CW, Watson SP, Kerrigan SW. Glycoprotein Ibalpha and FcgammaRIIa play key roles in platelet activation by the colonizing bacterium, Streptococcus oralis. J Thromb Haemost 2013;11: 941-950.
68. Arman M, Krauel K, Tilley DO, Weber C, Cox D, Greinacher A, Kerrigan SW; Watson SP. Amplification of bacteria-induced platelet activation is triggered by FcgammaRIIA, integrin alphaIIbbeta3, and platelet factor 4. Blood 2014;123:3166-3174.
69. Svensson L, Baumgarten M, Morgelin M, Shannon O. Platelet activation by streptococcus pyogenes leads to entrapment in platelet aggregates, from which bacteria subsequently escape. Infect Immun 2014;82:4307-4314.
70. Sullam PM, Hyun WC, Szollosi J, Dong J, Foss WM, Lopez JA. Physical proximity and functional interplay of the glycoprotein Ib- IX-V complex and the Fc receptor FcgammaRIIA on the platelet plasma membrane. J Biol Chem 1998;273:5331-5336.
71. Boylan B, Gao C, Rathore V, Gill JC, Newman DK, Newman PJ. Identification of FcgammaRIIa as the ITAM-bearing receptor mediating alphaIIbbeta3 outside-in integrin signaling in human platelets. Blood 2008;112:2780-2786.
72. Miajlovic H, Loughman A, Brennan M, Cox D, Foster TJ. Both complement- and fibrinogen-dependent mechanisms contribute to platelet aggregation mediated by Staphylococcus aureus clumping factor B. Infect Immun 2007;75:3335-3343.
73. Naito M, Sakai E, Shi Y, Ideguchi H, Shoji M, Ohara N, Yamamoto K, Nakayama K. Porphyromonas gingivalis-induced platelet aggregation in plasma depends on Hgp44 adhesin but not Rgp proteinase. Mol Microbiol 2006;59:152-167.
74. Ghebrehiwet B, Jesty J, Peerschke EI. gC1q-R/p33: Structure- function predictions from the crystal structure. Immunobiology 2002;205:421-432.
75. Sarma JV, Ward PA. The complement system. Cell Tissue Res 2011; 343:227-235.
76. Kim KB, Kim BW, Choo HJ, Kwon YC, Ahn BY, Choi JS, Lee JS, Ko YG. Proteome analysis of adipocyte lipid rafts reveals that gC1qR plays essential roles in adipogenesis and insulin signal transduction. Proteomics 2009;9:2373-2382.
77. Ghebrehiwet B, Ji Y, Valentino A, Pednekar L, Ramadass M, Habiel D, Kew RR, Hosszu KH, Galanakis DK, Kishore U. Soluble gC1qR is an autocrine signal that induces B1R expression on endothelial cells. J Immunol 2014;192:377-384.
78. Ghebrehiwet B, Lim BL, Kumar R, Feng X, Peerschke EI. gC1q-R/ p33, a member of a new class of multifunctional and multi-compartmental cellular proteins, is involved in inflammation and infection. Immunol Rev 2001;180:65-77.
79. Peerschke EI, Murphy TK, Ghebrehiwet B. Activation-dependent surface expression of gC1qR/p33 on human blood platelets. Thromb Haemost 2003;89:331-339.
80. Nguyen T, Ghebrehiwet B, Peerschke EI. Staphylococcus aureus protein A recognizes platelet gC1qR/p33: A novel mechanism for staphylococcal interactions with platelets. Infect Immun 2000;68: 2061-2068.
81. O'Brien L, Kerrigan SW, Kaw G, Hogan M, Penades J, Litt D, Fitzgerald DJ, Foster TJ, Cox D. Multiple mechanisms for the activation of human platelet aggregation by Staphylococcus aureus: Roles for the clumping factors ClfA and ClfB, the serine-aspartate repeat protein SdrE and protein A. Mol Microbiol 2002;44: 1033-1044.
82. Ford I, Douglas CW, Preston FE, Lawless A, Hampton KK. Mechanisms of platelet aggregation by Streptococcus sanguis, a causative organism in infective endocarditis. Br J Haematol 1993;84: 95-100.
83. Ford I, Douglas CW, Heath J, Rees C, Preston FE. Evidence for the involvement of complement proteins in platelet aggregation by Streptococcus sanguis NCTC 7863. Br J Haematol 1996;94: 729-739.
84. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, Paik SG, Lee H, Lee JO. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 2007;130:1071-1082.
85. Zahringer U, Lindner B, Inamura S, Heine H, Alexander C. TLR2 - Promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 2008;213: 205-224.
86. Gautam JK, Ashish KS, Comeau LD, Krueger JK, Smith Jr MF. Structural and functional evidence for the role of the TLR2 DD loop in TLR1/TLR2 heterodimerization and signaling. J Biol Chem 2006; 281:30132-30142.
87. Jackson SP, Yap CL, Anderson KE. Phosphoinositide 3-kinases and the regulation of platelet function. Biochem Soc Trans 2004;32: 387-392.
88. Blair P, Rex S, Vitseva O, Beaulieu L, Tanriverdi K, Chakrabarti S, Hayashi C, Genco CA, Iafrati M, Freedman JE. Stimulation of Tolllike receptor 2 in human platelets induces a thromboinflammatory response through activation of phosphoinositide 3-kinase. Circul Res 2009;104:346-354.
89. Baker M. Animal models: Inside the minds of mice and men. Nature 2011; 475: 123-128.
90. Ramsland PA, Farrugia W, Bradford TM, Sardjono CT, Esparon S, Trist HM, Powell MS, Tan PS, Cendron AC, Wines BD. Structural basis for Fc gammaRIIa recognition of human IgG and formation of inflammatory signaling complexes. J Immunol 2011;187: 3208-3217.
91. Varki A. Selectin ligands. Proc Natl Acad Sci USA 1994;91: 7390-7397.
92. Plummer C, Wu H, Kerrigan SW, Meade G, Cox D, Ian Douglas CW. A serine-rich glycoprotein of Streptococcus sanguis mediates adhesion to platelets via GPIb. Br J Haematol 2005;129: 101-109.
93. Sjobring U, Ringdahl U, Ruggeri ZM. Induction of platelet thrombi by bacteria and antibodies. Blood 2002;100: 4470-4477.