Streptococcus sanguinis-induced cytokine and matrix metalloproteinase-1 release from platelets

BMC Immunology

Archie McNicol¹  Olivier Garraud²  Charles-Antoine Arthaud³  Elke Jackson¹  Adrien Chabert²  Hind Hamzeh-Cognasse²  Fabrice Cognasse² 

[1] International Centre for Oral Systemic Health, University of Manitoba, Winnipeg, MB, Canada;GIMAP-EA3064, Université de Lyon, Saint-Étienne 42023, France;Etablissement Français du Sang (EFS) Auvergne-Loire, Saint-Etienne, France

关键词: Streptococcus sanguinis;    Inflammation;    Oral cavity;    Signalling;    Cytokines;    Platelets;   

Others  :  1077717
DOI  :  10.1186/1471-2172-15-15

 received in 2013-10-30, accepted in 2014-04-07,  发布年份 2014

【 摘 要 】

Background

Streptococcus sanguinis (S.sanguinis), a predominant bacterium in the human oral cavity, has been widely associated with the development of infective endocarditis. Platelets play both a haemostatic function and can influence both innate and adaptive immune responses. Previous studies have shown that S.sanguinis can interact with, and activate, platelets.

Results

The aim of this study was to determine whether S.sanguinis stimulates the release of matrix metalloproteinases (MMPs) 1, 2 and 9 and the pro-inflammatory mediators SDF-1, VEGF and sCD40L, from platelets and to subsequently pharmacologically address the release mechanism (s). S.sanguinis stimulated the release of MMP-1, SDF-1, VEGF and sCD40L from platelets and inhibitors of cyclooxygenase and phosphatidylinositol 3-kinase, and antagonists of the αIIbβ3 integrin and glycoprotein Ib, each inhibited the secretion of all factors.

Conclusions

Therefore the release of MMP-1, SDF-1, VEGF and sCD40L occurs late in the platelet response to S.sanguinis and highlights the complex intracellular signalling pathways stimulated in response to S.sanguinis which lead to haemostasis, MMP and pro-inflammatory mediator secretion.

【 授权许可】

   
2014 Cognasse et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Ford I, Douglas CW: The role of platelets in infective endocarditis. Platelets 1997, 8:285-294.
• [2]Sansonetti PJ: To be or not to be a pathogen: that is the mucosally relevant question. Mucosal Immunol 2011, 4:8-14.
• [3]Forner L, Larsen T, Kilian M, Holmstrup P: Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol 2006, 33:401-407.
• [4]Belstrom D, Damgaard C, Nielsen CH, Holmstrup P: Does a causal relation between cardiovascular disease and periodontitis exist? Microbes Infect 2012, 14:411-418.
• [5]Lockhart PB, Bolger AF, Papapanou PN, Osinbowale O, Trevisan M, Levison ME, Taubert KA, Newburger JW, Gornik HL, Gewitz MH, Wilson WR, Smith SC Jr, Baddour LM, American Heart Association Rheumatic Fever, Endocarditis, and Kawasaki Disease Committee of the Council on Cardiovascular Disease in the Young, Council on Epidemiology and Prevention: Periodontal disease and atherosclerotic vascular disease: does the evidence support an independent association?: a scientific statement from the American Heart Association. Circulation 2012, 125:2520-2544.
• [6]McNicol A, Israels SJ: Mechanisms of oral bacteria-induced platelet activation. Can J Physiol Pharmacol 2010, 88:510-524.
• [7]Wei AH, Schoenwaelder SM, Andrews RK, Jackson SP: New insights into the haemostatic function of platelets. Br J Haematol 2009, 147:415-430.
• [8]Jennings LK: Role of platelets in atherothrombosis. Am J Cardiol 2009, 103:4A-10A.
• [9]Engelmann B, Massberg S: Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol 2013, 13:34-45.
• [10]Rondina MT, Weyrich AS, Zimmerman GA: Platelets as cellular effectors of inflammation in vascular diseases. Circ Res 2013, 112:1506-1519.
• [11]Jenne CN, Urrutia R, Kubes P: Platelets: bridging hemostasis, inflammation, and immunity. Int J Lab Hematol 2013, 35:254-261.
• [12]Davi G, Patrono C: Platelet activation and atherothrombosis. N Engl J Med 2007, 357:2482-2494.
• [13]Andre P, Nannizzi-Alaimo L, Prasad SK, Phillips DR: Platelet-derived CD40L: the switch-hitting player of cardiovascular disease. Circulation 2002, 106:896-899.
• [14]Semple JW, Italiano JE Jr, Freedman J: Platelets and the immune continuum. Nat Rev Immunol 2011, 11:264-274.
• [15]Berthet J, Damien P, Hamzeh-Cognasse H, Arthaud CA, Eyraud MA, Zeni F, Pozzetto B, McNicol A, Garraud O, Cognasse F: Human platelets can discriminate between various bacterial LPS isoforms via TLR4 signaling and differential cytokine secretion. Clin Immunol 2012, 145:189-200.
• [16]Italiano JE Jr, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL: Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 2008, 111:1227-1233.
• [17]Italiano Jr JE, Battinelli EM: Selective sorting of alpha-granule proteins. J Thromb Haemost 2009, 7(1):173-176.
• [18]tot Pannerden H v N, 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, 116:1147-1156.
• [19]Parks WC, Wilson CL, Lopez-Boado YS: Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004, 4:617-629.
• [20]Seizer P, May AE: Platelets and matrix metalloproteinases. Thromb Haemost 2013, 110(5):903-909.
• [21]Trivedi V, Boire A, Tchernychev B, Kaneider NC, Leger AJ, O'Callaghan K, Covic L, Kuliopulos A: Platelet matrix metalloprotease-1 mediates thrombogenesis by activating PAR1 at a cryptic ligand site. Cell 2009, 137:332-343.
• [22]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.
• [23]Lutgens E, Lievens D, Beckers L, Donners M, Daemen M: CD40 and its ligand in atherosclerosis. Trends Cardiovasc Med 2007, 17:118-123.
• [24]McNicol A, Agpalza A, Jackson EC, Hamzeh-Cognasse H, Garraud O, Cognasse F: Streptococcus sanguinis-induced cytokine release from platelets. J Thromb Haemost 2011, 9:2038-2049.
• [25]Pampolina C, McNicol A: Streptococcus sanguis-induced platelet activation involves two waves of tyrosine phosphorylation mediated by FcgammaRIIA and alphaIIbbeta3. Thromb Haemost 2005, 93:932-939.
• [26]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.
• [27]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.
• [28]Sawicki G, Sanders EJ, Salas E, Wozniak M, Rodrigo J, Radomski MW: Localization and translocation of MMP-2 during aggregation of human platelets. Thromb Haemost 1998, 80:836-839.
• [29]Wrzyszcz A, Wozniak M: On the origin of matrix metalloproteinase-2 and −9 in blood platelets. Platelets 2012, 23:467-474.
• [30]Kalvegren H, Jonsson S, Jonasson L: Release of matrix metalloproteinases-1 and −2, but not −9, from activated platelets measured by enzyme-linked immunosorbent assay. Platelets 2011, 22:572-578.
• [31]Fernandez Bello I, Alvarez MT, Lopez-Longo FJ, Arias-Salgado EG, Martin M, Jimenez-Yuste V, de la Rua AR, Butta NV: Platelet soluble CD40L and matrix metalloproteinase 9 activity are proinflammatory mediators in Behcet disease patients. Thromb Haemost 2012, 107:88-98.
• [32]Rahman M, Zhang S, Chew M, Syk I, Jeppsson B, Thorlacius H: Platelet shedding of CD40L is regulated by matrix metalloproteinase-9 in abdominal sepsis. J Thromb Haemost 2013, 11:1385-1398.
• [33]McNicol A, Eyer E, Jackson EC, Israels SJ: A role for von Willebrand factor in Streptococcus sanguis-induced platelet activation. Thromb Haemost 2007, 98:1382-1384.
• [34]Abdulrehman AY, Jackson EC, McNicol A: Platelet activation by Streptococcus sanguinis is accompanied by MAP kinase phosphorylation. Platelets 2013, 24:6-14.
• [35]Nadal F, Levy-Toledano S, Grelac F, Caen JP, Rosa JP, Bryckaert M: Negative regulation of mitogen-activated protein kinase activation by integrin alphaIIbbeta3 in platelets. J Biol Chem 1997, 272:22381-22384.
• [36]Flevaris P, Li Z, Zhang G, Zheng Y, Liu J, Du X: Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPK-dependent integrin outside-in retractile signaling pathway. Blood 2009, 113:893-901.
• [37]Aslan JE, McCarty OJ: Rho GTPases in platelet function. J Thromb Haemost 2013, 11:35-46.
• [38]Herzberg MC, Brintzenhofe KL, Clawson CC: Cell-free released components of Streptococcus sanguis inhibit human platelet aggregation. Infect Immun 1983, 42:394-401.
• [39]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, 141:84-91.