Bacteria-induced intracellular signalling in platelets

Platelets

Volumn 26, Issue 4, 2015, Pages 309-316

  McNicol, Archie ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Bacillus; Bacteria; Platelets; Porphyromonas; Signalling; Streptococcus

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENYLATE CYCLASE; ALPHA IIB BETA3 INTEGRIN; COMPLEMENT; FC GAMMA RECEPTOR IIIA; FC RECEPTOR; GLYCOPROTEIN IB; IMMUNOGLOBULIN G; INTEGRIN; LAT PROTEIN; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C BETA; PHOSPHOLIPASE C GAMMA2; PROTEIN KINASE SYK; PROTEINASE ACTIVATED RECEPTOR; THROMBOCYTE FACTOR 4; THROMBOXANE A2; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

BACILLUS ANTHRACIS; BACTERIUM TRANSDUCTION; ENZYME INHIBITION; EXOCYTOSIS; NONHUMAN; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STREPTOCOCCUS GORDONII; STREPTOCOCCUS ORALIS; STREPTOCOCCUS SANGUINIS; THROMBOCYTE ACTIVATION; BACTERIUM; HUMAN; IMMUNOLOGY; THROMBOCYTE;

PORPHYROMONAS; PORPHYROMONAS GINGIVALIS; STREPTOCOCCUS; STREPTOCOCCUS GORDONII; STREPTOCOCCUS ORALIS; STREPTOCOCCUS SANGUINIS;

BACTERIA; BLOOD PLATELETS; HUMANS; SIGNAL TRANSDUCTION;

EID: 84929336896     PISSN: 09537104     EISSN: 13691635     Source Type: Journal    
DOI: 10.3109/09537104.2015.1014470     Document Type: Review

References (90)

1. Wei AH, Schoenwaelder SM, Andrews RK, Jackson SP. New insights into the haemostatic function of platelets. Br J Haematol 2009;147(4):415-430.
2. Michelson AD. Antiplatelet therapies for the treatment of cardiovascular disease. Nat Rev Drug Discov 2010;9(2):154-169.
3. Jennings LK. Role of platelets in atherothrombosis. Am J Cardiol 2009;103(3 Suppl):4A-10A.
4. McNicol A, Israels SJ. Beyond hemostasis: The role of platelets in inflammation, malignancy and infection. Cardiovasc Hematol Disord Drug Targets 2008;8(2):99-117.
5. Seizer P, Gawaz M, May AE. Platelet-monocyte interactions - A dangerous liaison linking thrombosis, inflammation and atherosclerosis. Curr Med Chem 2008;15(20):1976-1980.
6. Gleissner CA, von Hundelshausen P, Ley K. Platelet chemokines in vascular disease. Arterioscler Thromb Vasc Biol 2008; 28(11):1920-1927.
7. Smyth SS, McEver RP, Weyrich AS, Morrell CN, Hoffman MR, Arepally GM, French PA, Dauerman HL, Becker RC. Platelet functions beyond hemostasis. J Thromb Haemost 2009; 7(11):1759-1766.
8. Semple JW, Freedman J. Platelets and innate immunity. Cell Mol Life Sci 2010;67(4):499-511.
9. Erpenbeck L, Schon MP. Deadly allies: The fatal interplay between platelets and metastasizing cancer cells. Blood 2010;115(17): 3427-3436.
10. Nurden AT. Platelets, inflammation and tissue regeneration. Thromb Haemost 2011;105(Suppl 1):S13-S33.
11. Semple JW, Italiano Jr JE, Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011;11(4):264-274.
12. Corrales-Medina VF, Madjid M, Musher DM. Role of acute infection in triggering acute coronary syndromes. Lancet Infect Dis 2010;10(2):83-92.
13. Ott SJ, El Mokhtari NE, Musfeldt M, Hellmig S, Freitag S, Rehman A, Kühbacher T, Nikolaus S, Namsolleck P, Blaut M, et al. Detection of diverse bacterial signatures in atherosclerotic lesions of patients with coronary heart disease. Circulation 2006; 113(7):929-937.
14. Nakano K, Nemoto H, Nomura R, Inaba H, Yoshioka H, Taniguchi K, Amano A, Ooshima T. Detection of oral bacteria in cardiovascular specimens. Oral Microbiol Immunol 2009;24(1):64-68.
15. Fitzgerald JR, Foster TJ, Cox D. The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006;4(6):445-457.
16. 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(5):836-849.
17. 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(20):3166-3174.
18. Ford I, 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(4):729-739.
19. Erickson PR, Herzberg MC. Purification and partial characterization of a 65-kDa platelet aggregation-associated protein antigen from the surface of Streptococcus sanguis. J Biol Chem 1990;265(24): 14080-14087.
20. 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(2):509-516.
21. Douglas CW, Brown PR, Preston FE. Platelet aggregation by oral streptococci. FEMS Microbiol Lett 1990;60(1-2):63-67.
22. 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(1):95-100.
23. Ford I, Douglas CW. The role of platelets in infective endocarditis. Platelets 1997;8(5):285-294.
24. Soberay AH, Herzberg MC, Rudney JD, Nieuwenhuis HK, Sixma JJ, Seligsohn U. Responses of platelets to strains of Streptococcus sanguis: Findings in healthy subjects, Bernard-Soulier, Glanzmann's, and collagen-unresponsive patients. Thromb Haemost 1987;57(2):222-225.
25. Kerrigan SW, Cox D. Platelet-bacterial interactions. Cell Mol Life Sci 2010;67(4):513-523.
26. Erickson PR, Herzberg MC. The Streptococcus sanguis platelet aggregation-associated protein. Identification and characterization of the minimal platelet-interactive domain. J Biol Chem 1993; 268(3):1646-1649.
27. Herzberg MC, Meyer MW. Effects of oral flora on platelets: Possible consequences in cardiovascular disease. J Periodontol 1996;67(10 Suppl):1138-1142.
28. Legrand YJ, Karniguian A, Le Francier P, Fauvel F, Caen JP. Evidence that a collagen-derived nonapeptide is a specific inhibitor of platelet-collagen interaction. Biochem Biophys Res Commun 1980;96(4):1579-1585.
29. Pintigny D, Legrand C, Karniguian A, Legrand YJ, Caen JP. Evidence that a collagen derived octapeptide inhibits fibrinogen binding to platelets stimulated by collagen and not by ADP. Biochem Biophys Res Commun 1985;128(2):547-553.
30. Herzberg MC, Nobbs A, Tao L, Kilic A, Beckman E, Khammanivong A, Zhang Y. Oral streptococci and cardiovascular disease: Searching for the platelet aggregation-associated protein gene and mechanisms of Streptococcus sanguis-induced thrombosis. J Periodontol 2005;76(11 Suppl):2101-2105.
31. Kerrigan SW, Cox D. The thrombotic potential of oral pathogens. J Oral Microbiol 2009;1:1-10.
32. McNicol A, Israels SJ. Mechanisms of oral bacteria-induced platelet activation. Can J Physiol Pharm 2010;88(5):510-524.
33. McNicol A, Zhu R, Pesun R, Pampolina C, Jackson EC, Bowden GH, Zelinski T. A role for immunoglobulin G in donor-specific Streptococcus sanguis-induced platelet aggregation. Thromb Haemost 2006;95(2):288-293.
34. 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(5):941-950.
35. Ford I, Douglas CW, Cox D, Rees DG, Heath J, Preston FE. The role of immunoglobulin G and fibrinogen in platelet aggregation by Streptococcus sanguis. Br J Haematol 1997;97(4):737-746.
36. Sullam PM, Jarvis GA, Valone FH. Role of immunoglobulin G in platelet aggregation by viridans group streptococci. Infect Immun 1988;56(11):2907-2911.
37. Pampolina C, McNicol A. Streptococcus sanguis-induced platelet activation involves two waves of tyrosine phosphorylation mediated by FcgammaRIIA and alphaIIbbeta3. Thromb Haemost 2005; 93(5):932-939.
38. Stalker TJ, Newman DK, Ma P, Wannemacher KM, Brass LF. Platelet signaling. Handb Exp Pharmacol 2012;210:59-85.
39. Ragab A, Séverin S, Gratacap MP, Aguado E, Malissen M, Jandrot-Perrus M, Malissen B, Ragab-Thomas J, Payrastre B. Roles of the C-terminal tyrosine residues of LAT in GPVI-induced platelet activation: Insights into the mechanism of PLC gamma 2 activation. Blood 2007;110(7):2466-2474.
40. Moraes LA, Barrett NE, Jones CI, Holbrook LM, Spyridon M, Sage T, Newman DK, Gibbins JM. Platelet endothelial cell adhesion molecule-1 regulates collagen-stimulated platelet function by modulating the association of phosphatidylinositol 3-kinase with Grb-2-associated binding protein-1 and linker for activation of T cells. J Thromb Haemost 2010;8(11):2530-2541.
41. Abdulrehman AY, Jackson EC, McNicol A. Platelet activation by Streptococcus sanguinis is accompanied by MAP kinase phosphor-ylation. Platelets 2013;24(1):6-14.
42. 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(7):2780-2786.
43. Zhi H, Rauova L, Hayes V, Gao C, Boylan B, Newman DK, McKenzie SE, Cooley BC, Poncz M, Newman PJ. Cooperative integrin/ITAM signaling in platelets enhances thrombus formation in vitro and in vivo. Blood 2013;121(10):1858-1867.
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(1):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(12):2408-2415.
46. McNicol A, Agpalza A, Jackson EC, Hamzeh-Cognasse H, Garraud O, Cognasse F. Streptococcus sanguinis-induced cytokine release from platelets. J Thromb Haemost, 2011;9(10):2038-2049.
47. Kasper B, Petersen F. Molecular pathways of platelet factor 4/CXCL4 signaling. Eur J Cell Biol 2011;90(6-7):521-526.
48. van Nispen tot Pannerden H, de Haas F, Geerts W, Posthuma G, van Dijk S, Heijnen HF. The platelet interior revisited: Electron tomography reveals tubular alpha-granule subtypes. Blood 2010; 116(7) 1147-1156.
49. Italiano Jr JE, Battinelli EM. Selective sorting of alpha-granule proteins. J Thromb Haemost 2009;7(Suppl 1):173-176.
50. Borsch-Haubold AG, Kramer RM, Watson SP. Phosphorylation and activation of cytosolic phospholipase A2 by 38-kDa mitogen-activated protein kinase in collagen-stimulated human platelets. Eur J Biochem 1997;245(3):751-759.
51. 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(1):101-109.
52. McNicol A, Eyer E, Jackson EC, Israels SJ. A role for von Willebrand factor in Streptococcus sanguis-induced platelet activation. Thromb Haemost 2007;98(6):1382-1384.
53. Ozaki Y, Asazuma N, Suzuki-Inoue K, Berndt MC. Platelet GPIb-IX-V-dependent signaling. J Thromb Haemost 2005;3(8): 1745-1751.
54. Takahashi Y, Yajima A, Cisar JO, Konishi K. Functional analysis of the Streptococcus gordonii DL1 sialic acid-binding adhesin and its essential role in bacterial binding to platelets. Infect Immun 2004; 72(7):3876-3882.
55. 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(11):6528-6537.
56. Plummer C, Douglas CW. Relationship between the ability of oral streptococci to interact with platelet glycoprotein Ibalpha and with the salivary low-molecular-weight mucin, MG2. FEMS Immunol Med Microbiol 2006;48(3):390-399.
57. Peerschke EI, Murphy TK, Ghebrehiwet B. Activation-dependent surface expression of gC1qR/p33 on human blood platelets. Thromb Haemost 2003;89(2):331-339.
58. Herzberg MC, Brintzenhofe KL. ADP-like platelet aggregation activity generated by viridans streptococci incubated with exogenous ATP. Infect Immun 1983;40(1):120-125.
59. Pierce KL, Premont RT, Lefkowitz RJ. Seven-transmembrane receptors. Nat Rev Mol Cell Biol 2002;3(9):639-650.
60. Lova P, Paganini S, Sinigaglia F, Balduini C, Torti M. A Gi-dependent pathway is required for activation of the small GTPase Rap1B in human platelets. J Biol Chem 2002;277(14):12009-12015.
61. Herzberg MC, Krishnan LK, MacFarlane GD. Involvement of alpha 2-adrenoreceptors and G proteins in the modulation of platelet secretion in response to Streptococcus sanguis. Crit Rev Oral Biol Med 1993;4(3-4):435-442.
62. Nash CA, Séverin S, Dawood BB, Makris M, Mumford A, Wilde J, Senis YA, Watson SP. Src family kinases are essential for primary aggregation by G(i)-coupled receptors. J Thromb Haemost 2010; 8(10):2273-2282.
63. Zimmerman TS, Spiegelberg HL. Pneumococcus-induced serotonin release from human platelets. Identification of the participating plasma/serum factor as immunoglobulin. J Clin Invest 1975; 56(4):828-834.
64. 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(12):2757-2765.
65. Cognasse F, Hamzeh H, Chavarin P, Acquart S, Genin C, Garraud O. Evidence of Toll-like receptor molecules on human platelets. Immunol Cell Biol 2005;83(2):196-198.
66. Sullam PM, Bayer AS, Foss WM, Cheung AL. Diminished platelet binding in vitro by Staphylococcus aureus is associated with reduced virulence in a rabbit model of infective endocarditis. Infect Immun 1996;64(12):4915-4921.
67. O'Brien L, Kerrigan SW, Kaw G, Hogan M, Penadés 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(4):1033-1044.
68. de Haas CJ, Weeterings C, Vughs MM, de Groot PG, Van Strijp JA, Lisman T. Staphylococcal superantigen-like 5 activates platelets and supports platelet adhesion under flow conditions, which involves glycoprotein Ibalpha and alpha IIb beta 3. J Thromb Haemost 2009; 7(11):1867-1874.
69. 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(3):804-818.
70. Zhang W, Zhao L, Liu J, Du J, Yan R, Dai K. Role of 14-3-3z in Platelet Glycoprotein Iba-von Willebrand Factor Interaction-Induced Signaling. Int J Mol Sci. 2012;13(5):5364-5374.
71. Andrews RK, Du X, Berndt MC. The 14-3-3zeta-GPIb-IX-V complex as an antiplatelet target. Drug News Perspect 2007;20(5): 285-292.
72. Whitaker EJ, Thomas IS, Falk JA, Obebe A, Hammond BF. Effect of acetylsalicylic acid on aggregation of human platelets by Porphyromonas gingivalis. Gen Dent 2007;55(1):64-69; quiz 70, 79-80.
73. McNicol A, Israels SJ. Mechanisms of oral bacteria-induced platelet activation. Can J Physiol Pharmacol 2010;88(5):510-524.
74. Potempa J, Sroka A, Imamura T, Travis J. Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes. Curr Protein Pept Sci 2003;4(6):397-407.
75. 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(12):3790-3797.
76. 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(1):152-167.
77. Gibson III FC, Ukai T, Genco CA. Engagement of specific innate immune signaling pathways during Porphyromonas gingivalis induced chronic inflammation and atherosclerosis. Front Biosci 2008;13:2041-2059.
78. Shiraki R, Inoue N, Kawasaki S, Takei A, Kadotani M, Ohnishi Y, Ejiri J, Kobayashi S, Hirata K, Kawashima S, Yokoyama M. Expression of Toll-like receptors on human platelets. Thromb Res 2004;113(6):379-385.
79. Ward JR, Bingle L, Judge HM, Brown SB, Storey RF, Whyte MK, Dower SK, Buttle DJ, Sabroe I. Agonists of toll-like receptor (TLR)2 and TLR4 are unable to modulate platelet activation by adenosine diphosphate and platelet activating factor. Thromb Haemost 2005;94(4):831-838.
80. Cognasse F, Hamzeh-Cognasse H, Lafarge S, Delezay O, Pozzetto B, McNicol A, Garraud O. Toll-like receptor 4 ligand can differentially modulate the release of cytokines by human platelets. Br J Haematol 2008;141(1):84-91.
81. Aslam R, Speck ER, Kim M, Crow AR, Bang KW, Nestel FP, Ni H, Lazarus AH, Freedman J, Semple JW. Platelet Toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-alpha production in vivo. Blood 2006; 107(2):637-641.
82. Shashkin PN, Brown GT, Ghosh A, Marathe GK, McIntyre TM. Lipopolysaccharide is a direct agonist for platelet RNA splicing. J Immunol 2008;81(5):3495-3502.
83. Assinger A, Laky M, Badrnya S, Esfandeyari A, Volf I. Periodontopathogens induce expression of CD40L on human platelets via TLR2 and TLR4. Thromb Res 2012;130(3):e73-e78.
84. Troutman TD, Bazan JF, Pasare C. Toll-like receptors, signaling adapters and regulation of the pro-inflammatory response by PI3K. Cell Cycle 2012;11(19):3559-3567.
85. Clark K. Protein kinase networks that limit TLR signalling. Biochem Soc Trans 2014;42(1):11-24.
86. Sun D, Popescu NI, Raisley B, Keshari RS, Dale GL, Lupu F, Coggeshall KM. Bacillus anthracis peptidoglycan activates human platelets through FcgammaRII and complement. Blood 2013; 122(4):571-579.
87. Lhermusier T, Chap H, Payrastre B. Platelet membrane phospholipid asymmetry: From the characterization of a scramblase activity to the identification of an essential protein mutated in Scott syndrome. J Thromb Haemost 2011;9(10):1883-1891.
88. Bergmeier W, Oh-Hora M, McCarl CA, Roden RC, Bray PF, Feske S. R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood 2009;113(3):675-678.
89. Gilio K, van Kruchten R, Braun A, Berna-Erro A, Feijge MA, Stegner D, van der Meijden PE, Kuijpers MJ, Varga-Szabo D, Heemskerk JW, et al. Roles of platelet STIM1 and Orai1 in glycoprotein VI- and thrombin-dependent procoagulant activity and thrombus formation. J Biol Chem 2010;285(31):23629-23638.
90. Vincent JL, Yagushi A, Pradier O. Platelet function in sepsis. Crit Care Med 2002;30(5 Suppl):S313-S317.