Coordinated Molecular Cross-Talk between Staphylococcus aureus, Endothelial Cells and Platelets in Bloodstream Infection
Abstract
:1. Bloodstream Infection
1.1. Localised Bloodstream Infection: Infective Endocarditis
1.2. Generalised Bloodstream Infection: Sepsis
2. Common Mechanisms of S. aureus Binding Platelets and Endothelial Cells
3. Staphylococcus aureus Interactions with Endothelial Cells
4. Staphylococcus aureus Interactions with Platelets
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Foster, T.J. Colonization and infection of the human host by staphylococci: Adhesion, survival and immune evasion. Vet. Dermatol. 2009, 20, 456–470. [Google Scholar] [CrossRef] [PubMed]
- Lowy, F.D. Staphylococcus aureus infections. N. Engl. J. Med. 1998, 339, 520–532. [Google Scholar] [CrossRef] [PubMed]
- Cahill, T.J.; Prendergast, B.D. Infective endocarditis. Lancet 2015. [Google Scholar] [CrossRef]
- Murdoch, D.R.; Corey, G.R.; Hoen, B.; Miró, J.M.; Fowler, V.G., Jr.; Bayer, A.S.; Karchmer, A.W.; Olaison, L.; Pappas, P.A.; Moreillon, P.; et al. Clinical presentation, etiology, and outcome of infective endocarditis in the 21st century: The International Collaboration on Endocarditis-Prospective Cohort Study. Arch. Intern. Med. 2009, 169, 463–473. [Google Scholar] [CrossRef] [PubMed]
- Selton-Suty, C.; Celard, M.; Le Moing, V.; Doco-Lecompte, T.; Chirouze, C.; Iung, B.; Strady, C.; Revest, M.; Vandenesch, F.; Bouvet, A.; et al. Preeminence of Staphylococcus aureus in infective endocarditis: A 1-year population-based survey. Clin. Infect. Dis. 2012, 54, 1230–1239. [Google Scholar] [CrossRef] [PubMed]
- Kerrigan, S.W. The expanding field of platelet-bacterial interconnections. Platelets 2015, 26, 293–301. [Google Scholar] [CrossRef] [PubMed]
- Petersen, H.; Reynolds, K.; Newman, D.K.; Cox, D.; Jenkinson, H.F.; Newman, P.J.; Kerrigan, S.W. 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. [Google Scholar]
- Alla, F.; Fowler, V.G., Jr.; Sexton, D.J.; Corey, G.R.; Chu, V.H.; Wang, A.; Erpelding, M.L.; Durante-Mangoni, E.; Fernandez-Hidalgo, N.; et al. Impact of early valve surgery on outcome of Staphylococcus aureus prosthetic valve infective endocarditis: Analysis in the International Collaboration of Endocarditis-Prospective Cohort Study. Clin. Infect. Dis. 2015, 60, 741–749. [Google Scholar]
- Wang, A.; Athan, E.; Pappas, P.A.; Fowler, V.G., Jr.; Olaison, L.; Pare, C.; Almirante, B.; Munoz, P.; Rizzi, M.; Naber, C.; et al. Contemporary clinical profile and outcome of prosthetic valve endocarditis. J. Am. Med. Assoc. 2007, 297, 1354–1361. [Google Scholar] [CrossRef] [PubMed]
- Tong, S.Y.; Davis, J.S.; Eichenberger, E.; Holland, T.L.; Fowler, V.G., Jr. Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management. Clin. Microbiol. Rev. 2015, 28, 603–661. [Google Scholar] [CrossRef] [PubMed]
- Sidhu, P.; O'Kane, H.; Ali, N.; Gladstone, D.J.; Sarsam, M.A.; Campalani, G.; MacGowan, S.W. Mechanical or bioprosthetic valves in the elderly: A 20-year comparison. Ann. Thorac. Surg. 2001, 71, S257–S260. [Google Scholar] [CrossRef]
- Varstela, E. Personal follow-up of 100 aortic valve replacement patients for 1081 patient years. Ann. Chir. Gynaecol. 1998, 87, 205–212. [Google Scholar] [PubMed]
- Widmer, E.; Que, Y.A.; Entenza, J.M.; Moreillon, P. New concepts in the pathophysiology of infective endocarditis. Curr. Infect. Dis. Rep. 2006, 8, 271–279. [Google Scholar] [CrossRef] [PubMed]
- Moreillon, P.; Que, Y.A. Infective endocarditis. Lancet 2004, 363, 139–149. [Google Scholar] [CrossRef]
- Kerrigan, S.W.; Clarke, N.; Loughman, A.; Meade, G.; Foster, T.J.; Cox, D. Molecular basis for Staphylococcus aureus-mediated platelet aggregate formation under arterial shear in vitro. Arterioscler. Thromb. Vasc. Biol. 2008, 28, 335–340. [Google Scholar] [CrossRef] [PubMed]
- Yvorchuk, K.J.; Chan, K.L. Application of transthoracic and transesophageal echocardiography in the diagnosis and management of infective endocarditis. J. Am. Soc. Echocardiogr. 1994, 7, 294–308. [Google Scholar] [CrossRef]
- Prendergast, B.D.; Tornos, P. Surgery for infective endocarditis: Who and when? Circulation 2010, 121, 1141–1152. [Google Scholar] [CrossRef] [PubMed]
- Angus, D.C.; van der Poll, T. Severe sepsis and septic shock. N. Engl. J. Med. 2013. [Google Scholar] [CrossRef] [PubMed]
- Glik, J.; M., Gazdzik, T.; Nowak, M. The impact of the types of microorganisms isolated from blood and wounds on the results of treatment in burn patients with sepsis. Pol. J. Surg. 2012, 84, 6–16. [Google Scholar]
- Li, J.; Carr, B.; Goyal, M.; Gaieski, D.F. Sepsis: The inflammatory foundation of pathophysiology and therapy. Hosp. Pract. (1995) 2011, 39, 99–112. [Google Scholar] [CrossRef] [PubMed]
- Lemichez, E.; Lecuit, M.; Nassif, X.; Bourdoulous, S. Breaking the wall: Targeting of the endothelium by pathogenic bacteria. Nat. Rev. Microbiol. 2010, 8, 93–104. [Google Scholar] [CrossRef] [PubMed]
- Mouncey, P.R.; Osborn, T.M.; Power, G.S.; Harrison, D.A.; Sadique, M.Z.; Grieve, R.D.; Jahan, R.; Harvey, S.E.; Bell, D.; Bion, J.F.; et al. Trial of early, goal-directed resuscitation for septic shock. N. Engl. J. Med. 2015, 372, 1301–111. [Google Scholar] [CrossRef] [PubMed]
- Dellinger, R.P.; Levy, M.M.; Rhodes, A.; Annane, D.; Gerlach, H.; Opal, S.M.; Sevransky, J.E.; Sprung, C.L.; Douglas, I.S.; Jaeschke, R.; et al. Surviving Sepsis Campaign: International guidelines for management of severe sepsis and septic shock 2012. Intensive Care Med. 2013, 39, 165–228. [Google Scholar] [CrossRef] [PubMed]
- Buchan, C.A.; Bravi, A.; Seely, A.J. Variability analysis and the diagnosis, management, and treatment of sepsis. Curr. Infect. Dis. Rep. 2012, 14, 512–521. [Google Scholar] [CrossRef] [PubMed]
- Patti, J.M.; Allen, B.L.; McGavin, M.J.; Hook, M. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 1994, 48, 585–617. [Google Scholar] [CrossRef] [PubMed]
- Edwards, A.M.; Bowden, M.G.; Brown, E.L.; Laabei, M.; Massey, R.C. Staphylococcus aureus extracellular adherence protein triggers TNFalpha release, promoting attachment to endothelial cells via protein A. PLoS One 2012. [Google Scholar] [CrossRef] [PubMed]
- Miajlovic, H.; Zapotoczna, M.; Geoghegan, J.A.; Kerrigan, S.W.; Speziale, P.; Foster, T.J. Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 2010, 156, 920–928. [Google Scholar] [CrossRef] [PubMed]
- Agerer, F.; Michel, A.; Ohlsen, K.; Hauck, C.R. Integrin-mediated invasion of Staphylococcus aureus into human cells requires Src family protein-tyrosine kinases. J. Biol. Chem. 2003, 278, 42524–42531. [Google Scholar] [CrossRef] [PubMed]
- 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. [Google Scholar] [PubMed]
- Gould, K.; Ramirez-Ronda, C.H.; Holmes, R.K.; Sanford, J.P. Adherence of bacteria to heart valves in vitro. J. Clin. Invest. 1975, 56, 1364–1370. [Google Scholar] [CrossRef] [PubMed]
- Johnson, C.M.; Hancock, G.A.; Goulin, G.D. Specific binding of Staphylococcus aureus to cultured porcine cardiac valvular endothelial cells. J. Lab. Clin. Med. 1988, 112, 16–22. [Google Scholar] [PubMed]
- Ogawa, S.K.; Yurberg, E.R.; Hatcher, V.B.; Levitt, M.A.; Lowy, F.D. Bacterial adherence to human endothelial cells in vitro. Infect. Immun. 1985, 50, 218–224. [Google Scholar] [PubMed]
- Cheung, A.L.; Fischetti, V.A. The role of fibrinogen in staphylococcal adherence to catheters in vitro. J. Infect. Dis. 1990, 161, 1177–1186. [Google Scholar] [CrossRef] [PubMed]
- Cheung, A.L.; Krishnan, M.; Jaffe, E.A.; Fischetti, V.A. Fibrinogen acts as a bridging molecule in the adherence of Staphylococcus aureus to cultured human endothelial cells. J. Clin. Invest. 1991, 87, 2236–2245. [Google Scholar] [CrossRef] [PubMed]
- Cheung, A.L.; Fischetti, V.A. The role of fibrinogen in mediating staphylococcal adherence to fibers. J. Surg. Res. 1991, 50, 150–155. [Google Scholar] [CrossRef]
- Cheung, A.L.; Koomey, J.M.; Lee, S.; Jaffe, E.A.; Fischetti, V.A. Recombinant human tumor necrosis factor alpha promotes adherence of Staphylococcus aureus to cultured human endothelial cells. Infect. Immun. 1991, 59, 3827–3831. [Google Scholar] [PubMed]
- Shenkman, B.; Rubinstein, E.; Tamarin, I.; Dardik, R.; Savion, N.; Varon, D. Staphylococcus aureus adherence to thrombin-treated endothelial cells is mediated by fibrinogen but not by platelets. J. Lab. Clin. Med. 2000, 135, 43–51. [Google Scholar] [CrossRef]
- Tompkins, D.C.; Blackwell, L.J.; Hatcher, V.B.; Elliott, D.A.; O'Hagan-Sotsky, C.; Lowy, F.D. Staphylococcus aureus proteins that bind to human endothelial cells. Infect. Immun. 1992, 60, 965–969. [Google Scholar] [PubMed]
- Cheung, A.L.; Koomey, J.M.; Butler, C.A.; Projan, S.J.; Fischetti, V.A. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. Proc. Natl. Acad. Sci. USA 1992, 89, 6462–6646. [Google Scholar] [CrossRef] [PubMed]
- Shenkman, B.; Varon, D.; Tamarin, I.; Dardik, R.; Peisachov, M.; Savion, N.; Rubinstein, E. Role of agr (RNAIII) in Staphylococcus aureus adherence to fibrinogen, fibronectin, platelets and endothelial cells under static and flow conditions. J. Med. Microbiol. 2002, 51, 747–754. [Google Scholar] [CrossRef] [PubMed]
- Pohlmann-Dietze, P.; Ulrich, M.; Kiser, K.B.; Doring, G.; Lee, J.C.; Fournier, J.M.; Botzenhart, K.; Wolz, C. Adherence of Staphylococcus aureus to endothelial cells: Influence of capsular polysaccharide, global regulator agr, and bacterial growth phase. Infect. Immun. 2000, 68, 4865–4871. [Google Scholar] [CrossRef] [PubMed]
- Cedergren, L.; Andersson, R.; Jansson, B.; Uhlen, M.; Nilsson, B. Mutational analysis of the interaction between staphylococcal protein A and human IgG1. Protein Eng. 1993, 6, 441–448. [Google Scholar] [CrossRef] [PubMed]
- O'Seaghdha, M.; van Schooten, C.J.; Kerrigan, S.W.; Emsley, J.; Silverman, G.J.; Cox, D.; Lenting, P.J.; Foster, T.J. Staphylococcus aureus protein A binding to von Willebrand factor A1 domain is mediated by conserved IgG binding regions. Federation Eur. Biochem. Soc. J. 2006, 273, 4831–4841. [Google Scholar] [CrossRef] [PubMed]
- Gomez, M.I.; O'Seaghdha, M.; Magargee, M.; Foster, T.J.; Prince, A.S. Staphylococcus aureus protein A activates TNFR1 signaling through conserved IgG binding domains. J. Biol. Chem. 2006, 281, 20190–20196. [Google Scholar] [CrossRef] [PubMed]
- Gomez, M.I.; Seaghdha, M.O.; Prince, A.S. Staphylococcus aureus protein A activates TACE through EGFR-dependent signaling. EMBO J. 2007, 26, 701–709. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, T.; Ghebrehiwet, B.; Peerschke, E.I. Staphylococcus aureus protein A recognizes platelet gC1qR/p33: A novel mechanism for staphylococcal interactions with platelets. Infect. Immun. 2000, 68, 2061–2068. [Google Scholar] [CrossRef] [PubMed]
- Peerschke, E.I.; Ghebrehiwet, B. Human blood platelet gC1qR/p33. Immunol. Rev. 2001, 180, 56–64. [Google Scholar] [CrossRef] [PubMed]
- Claes, J.; Vanassche, T.; Peetermans, M.; Liesenborghs, L.; Vandenbriele, C.; Vanhoorelbeke, K.; Missiakas, D.; Schneewind, O.; Hoylaerts, M.F.; Heying, R.; et al. Adhesion of Staphylococcus aureus to the vessel wall under flow is mediated by von Willebrand factor-binding protein. Blood 2014, 124, 1669–1676. [Google Scholar] [CrossRef] [PubMed]
- Chavakis, T.; Hussain, M.; Kanse, S.M.; Peters, G.; Bretzel, R.G.; Flock, J.I.; Herrmann, M.; Preissner, K.T. Staphylococcus aureus extracellular adherence protein serves as anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat. Med. 2002, 8, 687–693. [Google Scholar] [CrossRef] [PubMed]
- Haggar, A.; Hussain, M.; Lonnies, H.; Herrmann, M.; Norrby-Teglund, A.; Flock, J.I. Extracellular adherence protein from Staphylococcus aureus enhances internalization into eukaryotic cells. Infect. Immun. 2003, 71, 2310–7231. [Google Scholar] [CrossRef] [PubMed]
- Lee, L.Y.; Miyamoto, Y.J.; McIntyre, B.W.; Hook, M.; McCrea, K.W.; McDevitt, D.; Brown, E.L. The Staphylococcus aureus Map protein is an immunomodulator that interferes with T cell-mediated responses. J. Clin. Invest. 2002, 110, 1461–1471. [Google Scholar] [CrossRef] [PubMed]
- Sinha, B.; Francois, P.P.; Nusse, O.; Foti, M.; Hartford, O.M.; Vaudaux, P.; Foster, T.J.; Lew, D.P.; Herrmann, M.; Krause, K.H. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell. Microbiol. 1999, 1, 101–117. [Google Scholar] [CrossRef] [PubMed]
- Dziewanowska, K.; Patti, J.M.; Deobald, C.F.; Bayles, K.W.; Trumble, W.R.; Bohach, G.A. Fibronectin binding protein and host cell tyrosine kinase are required for internalization of Staphylococcus aureus by epithelial cells. Infect. Immun. 1999, 67, 4673–4678. [Google Scholar] [PubMed]
- Ellington, J.K.; Elhofy, A.; Bost, K.L.; Hudson, M.C. Involvement of mitogen-activated protein kinase pathways in Staphylococcus aureus invasion of normal osteoblasts. Infect. Immun. 2001, 69, 5235–5242. [Google Scholar] [CrossRef] [PubMed]
- Fowler, T.; Johansson, S.; Wary, K.K.; Hook, M. Src kinase has a central role in in vitro cellular internalization of Staphylococcus aureus. Cell. Microbiol. 2003, 5, 417–426. [Google Scholar] [CrossRef] [PubMed]
- Conforti, G.; Zanetti, A.; Colella, S.; Abbadini, M.; Marchisio, P.C.; Pytela, R.; Giancotti, F.; Tarone, G.; Languino, L.R.; Dejana, E. Interaction of fibronectin with cultured human endothelial cells: Characterization of the specific receptor. Blood 1989, 73, 1576–1585. [Google Scholar] [PubMed]
- Esen, M.; Schreiner, B.; Jendrossek, V.; Lang, F.; Fassbender, K.; Grassme, H.; Gulbins, E. Mechanisms of Staphylococcus aureus induced apoptosis of human endothelial cells. Apoptosis 2001, 6, 431–439. [Google Scholar] [CrossRef] [PubMed]
- Menzies, B.E.; Kourteva, I. Staphylococcus aureus alpha-toxin induces apoptosis in endothelial cells. FEMS Immunol. Med. Microbiol. 2000, 29, 39–45. [Google Scholar] [PubMed]
- Beekhuizen, H.; van de Gevel, J.S.; Olsson, B.; van Benten, I.J.; van Furth, R. Infection of human vascular endothelial cells with Staphylococcus aureus induces hyperadhesiveness for human monocytes and granulocytes. J. Immunol. 1997, 158, 774–782. [Google Scholar] [PubMed]
- Moreland, J.G.; Bailey, G.; Nauseef, W.M.; Weiss, J.P. Organism-specific neutrophil-endothelial cell interactions in response to Escherichia coli, Streptococcus pneumoniae, and Staphylococcus aureus. J. Immunol. 2004, 172, 426–432. [Google Scholar] [CrossRef] [PubMed]
- Powers, M.E.; Kim, H.K.; Wang, Y.; Bubeck Wardenburg, J. ADAM10 mediates vascular injury induced by Staphylococcus aureus alpha-hemolysin. J. Infect. Dis. 2012, 206, 352–356. [Google Scholar] [CrossRef] [PubMed]
- Wilke, G.A.; Wardenburg, J.B. Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc. Natl. Acad. Sci. USA 2010, 107, 13473–13478. [Google Scholar] [CrossRef] [PubMed]
- Aird, W.C. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ. Res. 2007, 100, 158–173. [Google Scholar] [CrossRef] [PubMed]
- Aird, W.C. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ. Res. 2007, 100, 174–190. [Google Scholar] [CrossRef] [PubMed]
- Siegel, I.; Cohen, S. Action of Staphylococcal Toxin on Human Platelets. J. Infect. Dis. 1964, 114, 488–502. [Google Scholar] [CrossRef] [PubMed]
- Sheu, J.R.; Hsiao, G.; Lee, C.; Chang, W.; Lee, L.W.; Su, C.H.; Lin, C.H. Antiplatelet activity of Staphylococcus aureus lipoteichoic acid is mediated through a cyclic AMP pathway. Thromb. Res. 2000, 99, 249–258. [Google Scholar] [CrossRef]
- Sheu, J.R.; Lee, C.R.; Lin, C.H.; Hsiao, G.; Ko, W.C.; Chen, Y.C.; Yen, M.H. Mechanisms involved in the antiplatelet activity of Staphylococcus aureus lipoteichoic acid in human platelets. Thromb. Haemost. 2000, 83, 777–784. [Google Scholar] [PubMed]
- Waller, A.K.; Sage, T.; Kumar, C.; Carr, T.; Gibbins, J.M.; Clarke, S.R. Staphylococcus aureus lipoteichoic acid inhibits platelet activation and thrombus formation via the Paf receptor. J. Infect. Dis. 2013, 208, 2046–2057. [Google Scholar] [CrossRef] [PubMed]
- Powers, M.E.; Becker, R.E.; Sailer, A.; Turner, J.R.; Bubeck Wardenburg, J. Synergistic Action of Staphylococcus aureus alpha-Toxin on Platelets and Myeloid Lineage Cells Contributes to Lethal Sepsis. Cell Host Microbe 2015, 17, 775–787. [Google Scholar] [CrossRef] [PubMed]
- Hawiger, J.; Steckley, S.; Hammond, D.; Cheng, C.; Timmons, S.; Glick, A.D.; Des Prez, R.M. Staphylococci-induced human platelet injury mediated by protein A and immunoglobulin G Fc fragment receptor. J. Clin. Invest. 1979, 64, 931–937. [Google Scholar] [CrossRef] [PubMed]
- Andrews, R.K.; Gardiner, E.E.; Shen, Y.; Berndt, M.C. Structure-activity relationships of snake toxins targeting platelet receptors, glycoprotein Ib-IX-V and glycoprotein VI. Curr. Med. Chem. Cardiovasc. Hematol. Agents 2003, 1, 143–149. [Google Scholar] [CrossRef] [PubMed]
- Siboo, I.R.; Cheung, A.L.; Bayer, A.S.; Sullam, P.M. Clumping factor A mediates binding of Staphylococcus aureus to human platelets. Infect. Immun. 2001, 69, 3120–3127. [Google Scholar] [CrossRef] [PubMed]
- O'Brien, L.; Kerrigan, S.W.; Kaw, G.; Hogan, M.; Penades, J.; Litt, D.; Fitzgerald, D.J.; Foster, T.J.; 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. [Google Scholar] [CrossRef] [PubMed]
- Loughman, A.; Fitzgerald, J.R.; Brennan, M.P.; Higgins, J.; Downer, R.; Cox, D.; Foster, T.J. Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol. Microbiol. 2005, 57, 804–818. [Google Scholar] [CrossRef] [PubMed]
- Fitzgerald, J.R.; Loughman, A.; Keane, F.; Brennan, M.; Knobel, M.; Higgins, J.; Visai, L.; Speziale, P.; Cox, D.; Foster, T.J. 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. [Google Scholar] [CrossRef] [PubMed]
- Siboo, I.R.; Chambers, H.F.; Sullam, P.M. Role of SraP, a Serine-Rich Surface Protein of Staphylococcus aureus, in binding to human platelets. Infect. Immun. 2005, 73, 2273–2280. [Google Scholar] [CrossRef] [PubMed]
- Pawar, P.; Shin, P.K.; Mousa, S.A.; Ross, J.M.; Konstantopoulos, K. Fluid shear regulates the kinetics and receptor specificity of Staphylococcus aureus binding to activated platelets. J. Immunol. 2004, 173, 1258–1265. [Google Scholar] [CrossRef] [PubMed]
© 2015 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Garciarena, C.D.; McHale, T.M.; Watkin, R.L.; Kerrigan, S.W. Coordinated Molecular Cross-Talk between Staphylococcus aureus, Endothelial Cells and Platelets in Bloodstream Infection. Pathogens 2015, 4, 869-882. https://doi.org/10.3390/pathogens4040869
Garciarena CD, McHale TM, Watkin RL, Kerrigan SW. Coordinated Molecular Cross-Talk between Staphylococcus aureus, Endothelial Cells and Platelets in Bloodstream Infection. Pathogens. 2015; 4(4):869-882. https://doi.org/10.3390/pathogens4040869
Chicago/Turabian StyleGarciarena, Carolina D., Tony M. McHale, Rebecca L. Watkin, and Steven W. Kerrigan. 2015. "Coordinated Molecular Cross-Talk between Staphylococcus aureus, Endothelial Cells and Platelets in Bloodstream Infection" Pathogens 4, no. 4: 869-882. https://doi.org/10.3390/pathogens4040869