Host Pathways of Hemostasis that Regulate Group A Streptococcus pyogenes Pathogenicity

Author(s): Victoria A. Ploplis*, Francis J. Castellino

Journal Name: Current Drug Targets

Volume 21 , Issue 2 , 2020


DOI : 10.2174/1389450120666190926152914

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Graphical Abstract:


Abstract:

A hallmark feature of severe Group A Streptococcus pyogenes (GAS) infection is dysregulated hemostasis. Hemostasis is the primary pathway for regulating blood flow through events that contribute towards clot formation and its dissolution. However, a number of studies have identified components of hemostasis in regulating survival and dissemination of GAS. Several proteins have been identified on the surface of GAS and they serve to either facilitate invasion to host distal sites or regulate inflammatory responses to the pathogen. GAS M-protein, a surface-exposed virulence factor, appears to be a major target for interactions with host hemostasis proteins. These interactions mediate biochemical events both on the surface of GAS and in the solution when M-protein is released into the surrounding environment through shedding or regulated proteolytic processes that dictate the fate of this pathogen. A thorough understanding of the mechanisms associated with these interactions could lead to novel approaches for altering the course of GAS pathogenicity.

Keywords: Group A Streptococcus, hemostasis, inflammation, pyogenes, pathogen, M-protein.

[1]
Cunningham MW. Pathogenesis of group a streptococcal infections. Clin Microbiol Rev 2000; 13(3): 470-511.
[http://dx.doi.org/10.1128/CMR.13.3.470] [PMID: 10885988]
[2]
Walker MJ, Barnett TC, McArthur JD, et al. Disease manifestations and pathogenic mechanisms of Group A Streptococcus. Clin Microbiol Rev 2014; 27(2): 264-301.
[http://dx.doi.org/10.1128/CMR.00101-13] [PMID: 24696436]
[3]
Navarre WW, Schneewind O. Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria 1994; 14: 115-21.
[http://dx.doi.org/10.1111/j.1365-2958.1994.tb01271.x]
[4]
Swoboda JG, Campbell J, Meredith TC, Walker S. Wall teichoic acid function, biosynthesis, and inhibition. ChemBioChem 2010; 11(1): 35-45.
[http://dx.doi.org/10.1002/cbic.200900557] [PMID: 19899094]
[5]
Winram SB, Lottenberg R. The plasmin-binding protein Plr of group A streptococci is identified as glyceraldehyde-3-phosphate dehydrogenase. Microbiology 1996; 142(Pt 8): 2311-20.
[http://dx.doi.org/10.1099/13500872-142-8-2311] [PMID: 8760943]
[6]
Pancholi V, Fischetti VA. alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem 1998; 273(23): 14503-15.
[http://dx.doi.org/10.1074/jbc.273.23.14503] [PMID: 9603964]
[7]
Sutcliffe IC, Russell RR. Lipoproteins of gram-positive bacteria. J Bacteriol 1995; 177(5): 1123-8.
[http://dx.doi.org/10.1128/jb.177.5.1123-1128.1995] [PMID: 7868582]
[8]
Biagini M, Garibaldi M, Aprea S, et al. The human pathogen Streptococcus pyogenes releases lipoproteins as lipoprotein-rich membrane vesicles. Mol Cell Proteomics 2015; 14(8): 2138-49.
[http://dx.doi.org/10.1074/mcp.M114.045880] [PMID: 26018414]
[9]
Bober M, Mörgelin M, Olin AI, von Pawel-Rammingen U, Collin M. The membrane bound LRR lipoprotein Slr, and the cell wall-anchored M1 protein from Streptococcus pyogenes both interact with type I collagen. PLoS One 2011; 6(5)e20345
[http://dx.doi.org/10.1371/journal.pone.0020345] [PMID: 21655249]
[10]
Beachey EH, Simpson WA. The adherence of group A streptococci to oropharyngeal cells: the lipoteichoic acid adhesin and fibronectin receptor. Infection 1982; 10(2): 107-11.
[http://dx.doi.org/10.1007/BF01816738] [PMID: 7047404]
[11]
Morath S, von Aulock S, Hartung T. Structure/function relationships of lipoteichoic acids. J Endotoxin Res 2005; 11(6): 348-56.
[http://dx.doi.org/10.1177/09680519050110061001] [PMID: 16303090]
[12]
Courtney HS, Ofek I, Penfound T, et al. Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes. PLoS One 2009; 4(1)e4166
[http://dx.doi.org/10.1371/journal.pone.0004166] [PMID: 19132104]
[13]
Ofek I, Simpson WA, Beachey EH. Formation of molecular complexes between a structurally defined M protein and acylated or deacylated lipoteichoic acid of Streptococcus pyogenes. J Bacteriol 1982; 149(2): 426-33.
[PMID: 7035430]
[14]
Simpson WA, Beachey EH. Adherence of group A streptococci to fibronectin on oral epithelial cells. Infect Immun 1983; 39(1): 275-9.
[PMID: 6337097]
[15]
Farnell MB, Crippen TL, He H, Swaggerty CL, Kogut MH. Oxidative burst mediated by toll like receptors (TLR) and CD14 on avian heterophils stimulated with bacterial toll agonists. Dev Comp Immunol 2003; 27(5): 423-9.
[http://dx.doi.org/10.1016/S0145-305X(02)00115-5] [PMID: 12631524]
[16]
Thapa S, Nagy E, Abdul-Careem MF. In ovo delivery of Toll-like receptor 2 ligand, lipoteichoic acid induces pro-inflammatory mediators reducing post-hatch infectious laryngotracheitis virus infection. Vet Immunol Immunopathol 2015; 164(3-4): 170-8.
[http://dx.doi.org/10.1016/j.vetimm.2015.02.006] [PMID: 25764942]
[17]
Vega LA, Malke H, McIver KS. Virulence-related transcriptional regulators of Streptococcus pyogenesPulmonary Fibrosis. New York: Marcel Dekker 2016; pp. 135-71.
[18]
Hondorp ER, McIver KS. The Mga virulence regulon: infection where the grass is greener. Mol Microbiol 2007; 66(5): 1056-65.
[http://dx.doi.org/10.1111/j.1365-2958.2007.06006.x] [PMID: 18001346]
[19]
Churchward G. The two faces of Janus: virulence gene regulation by CovR/S in group A streptococci. Mol Microbiol 2007; 64(1): 34-41.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05649.x] [PMID: 17376070]
[20]
Bao YJ, Liang Z, Mayfield JA, Lee SW, Ploplis VA, Castellino FJ. CovRS regulated transcriptome analysis of a hypervirulent M23 strain of Group A Streptococcus pyogenes provides new insights on virulence determinants. J Bacteriol 2015; 197(19): 3191-205.
[http://dx.doi.org/10.1128/JB.00511-15] [PMID: 26216843]
[21]
Wu Y. Contact pathway of coagulation and inflammation. Thromb J 2015; 13: 17.
[http://dx.doi.org/10.1186/s12959-015-0048-y] [PMID: 25949215]
[22]
Golias C, Charalabopoulos A, Stagikas D, Charalabopoulos K, Batistatou A. The kinin system – bradykinin: biological effects and clinical implications. 2007; 11: 124-8.
[23]
Sriskandan S, Cohen J. Gram-positive sepsis. Mechanisms and differences from gram-negative sepsis. Infect Dis Clin North Am 1999; 13(2): 397-412.
[http://dx.doi.org/10.1016/S0891-5520(05)70082-9] [PMID: 10340174]
[24]
Oehmcke S, Mörgelin M, Malmström J, et al. Stimulation of blood mononuclear cells with bacterial virulence factors leads to the release of pro-coagulant and pro-inflammatory microparticles. Cell Microbiol 2012; 14(1): 107-19.
[http://dx.doi.org/10.1111/j.1462-5822.2011.01705.x] [PMID: 21951918]
[25]
Soult MC, Dobrydneva Y, Wahab KH, Britt LD, Sullivan CJ. Outer membrane vesicles alter inflammation and coagulation mediators. J Surg Res 2014; 192(1): 134-42.
[http://dx.doi.org/10.1016/j.jss.2014.05.007] [PMID: 24909870]
[26]
Mackman N. Role of tissue factor in hemostasis and thrombosis. Blood Cells Mol Dis 2006; 36(2): 104-7.
[http://dx.doi.org/10.1016/j.bcmd.2005.12.008] [PMID: 16466951]
[27]
Coughlin SR. Protease-activated receptors in vascular biology. Thromb Haemost 2001; 86(1): 298-307.
[PMID: 11487018]
[28]
Coughlin SR. How the protease thrombin talks to cells. Proc Natl Acad Sci USA 1999; 96(20): 11023-7.
[http://dx.doi.org/10.1073/pnas.96.20.11023] [PMID: 10500117]
[29]
Lopes-Bezerra LM, Filler SG. Endothelial cells, tissue factor and infectious diseases. Braz J Med Biol Res 2003; 36(8): 987-91.
[http://dx.doi.org/10.1590/S0100-879X2003000800004] [PMID: 12886452]
[30]
Biemond BJ, Levi M, Ten Cate H, et al. Plasminogen activator and plasminogen activator inhibitor I release during experimental endotoxaemia in chimpanzees: effect of interventions in the cytokine and coagulation cascades. Clin Sci (Lond) 1995; 88(5): 587-94.
[http://dx.doi.org/10.1042/cs0880587] [PMID: 7614818]
[31]
Faust SN, Levin M, Harrison OB, et al. Dysfunction of endothelial protein C activation in severe meningococcal sepsis. N Engl J Med 2001; 345(6): 408-16.
[http://dx.doi.org/10.1056/NEJM200108093450603] [PMID: 11496851]
[32]
Yang X, Li L, Liu J, Lv B, Chen F. Extracellular histones induce tissue factor expression in vascular endothelial cells via TLR and activation of NF-κB and AP-1. Thromb Res 2016; 137: 211-8.
[http://dx.doi.org/10.1016/j.thromres.2015.10.012] [PMID: 26476743]
[33]
DeLa Cadena RA, Laskin KJ, Pixley RA, et al. Role of kallikrein-kinin system in pathogenesis of bacterial cell wall-induced inflammation. Am J Physiol 1991; 260(2 Pt 1): G213-9.
[PMID: 1996642]
[34]
Sriskandan S, Kemball-Cook G, Moyes D, Canvin J, Tuddenham E, Cohen J. Contact activation in shock caused by invasive group A Streptococcus pyogenes. Crit Care Med 2000; 28(11): 3684-91.
[http://dx.doi.org/10.1097/00003246-200011000-00025] [PMID: 11098974]
[35]
Oehmcke S, Herwald H. Contact system activation in severe infectious diseases. J Mol Med (Berl) 2010; 88(2): 121-6.
[http://dx.doi.org/10.1007/s00109-009-0564-y] [PMID: 20232512]
[36]
Herwald H, Mörgelin M, Dahlbäck B, Björck L. Interactions between surface proteins of Streptococcus pyogenes and coagulation factors modulate clotting of human plasma. J Thromb Haemost 2003; 1(2): 284-91.
[http://dx.doi.org/10.1046/j.1538-7836.2003.00105.x] [PMID: 12871502]
[37]
Miller G, Silverberg M, Kaplan AP. Autoactivatability of human Hageman factor (factor XII). Biochem Biophys Res Commun 1980; 92(3): 803-10.
[http://dx.doi.org/10.1016/0006-291X(80)90774-3] [PMID: 7362605]
[38]
Silverberg M, Diehl SV. The autoactivation of factor XII (Hageman factor) induced by low-Mr heparin and dextran sulphate. The effect of the Mr of the activating polyanion. Biochem J 1987; 248(3): 715-20.
[http://dx.doi.org/10.1042/bj2480715] [PMID: 2449171]
[39]
Ben Nasr AB, Herwald H, Müller-Esterl W, Björck L. Human kininogens interact with M protein, a bacterial surface protein and virulence determinant. Biochem J 1995; 305(Pt 1): 173-80.
[http://dx.doi.org/10.1042/bj3050173] [PMID: 7826326]
[40]
Kaplan AP, Joseph K, Shibayama Y, et al. Bradykinin formation. Plasma and tissue pathways and cellular interactions. Clin Rev Allergy Immunol 1998; 16(4): 403-29.
[http://dx.doi.org/10.1007/BF02737659] [PMID: 9926288]
[41]
Herwald H, Collin M, Müller-Esterl W, Björck L. Streptococcal cysteine proteinase releases kinins: a virulence mechanism. J Exp Med 1996; 184(2): 665-73.
[http://dx.doi.org/10.1084/jem.184.2.665] [PMID: 8760820]
[42]
Smith-Erichsen N, Aasen AO, Gallimore MJ, Amundsen E. Studies of components of the coagulation systems in normal individuals and septic shock patients. Circ Shock 1982; 9(5): 491-7.
[PMID: 7172424]
[43]
Matsuda Y, Osaki T, Hashii T, Koshiba T, Kawabata S. A cysteine-rich protein from an arthropod stabilizes clotting mesh and immobilizes bacteria at injury sites. J Biol Chem 2007; 282(46): 33545-52.
[http://dx.doi.org/10.1074/jbc.M705854200] [PMID: 17855345]
[44]
Ploplis VA, Carmeliet P, Vazirzadeh S, et al. Effects of disruption of the plasminogen gene on thrombosis, growth, and health in mice. Circulation 1995; 92(9): 2585-93.
[http://dx.doi.org/10.1161/01.CIR.92.9.2585] [PMID: 7586361]
[45]
Ploplis VA, Castellino FJ. Gene targeting of components of the fibrinolytic system. Methods 2000; 21: 103-10.
[http://dx.doi.org/10.1006/meth.2000.0981] [PMID: 10816371]
[46]
Ploplis VA, Castellino FJ. Gene targeting of components of the fibrinolytic system. Thromb Haemost 2002; 87(1): 22-31.
[http://dx.doi.org/10.1055/s-0037-1612938] [PMID: 11848453]
[47]
Dressler DK. Death by clot: acute coronary syndromes, ischemic stroke, pulmonary embolism, and disseminated intravascular coagulation. AACN Adv Crit Care 2009; 20(2): 166-76.
[http://dx.doi.org/10.1097/NCI.0b013e3181a0b5e8] [PMID: 19411875]
[48]
Fisher MJ. Brain regulation of thrombosis and hemostasis. From Theory to practice. Stroke 2013; 44:3275-3285. Int J Immunopharmacol 2019; 72: 473-8.
[49]
Li X, Zhu Z, Gao S, et al. Inhibition of fibrin formation reduces neuroinflammation and improves long-term outcome after intracerebral hemorrhage. Int Immunopharmacol 2019; 72: 473-8.
[http://dx.doi.org/10.1016/j.intimp.2019.04.029] [PMID: 31039464]
[50]
McCance SG, Castellino FJ. Contributions of individual kringle domains toward maintenance of the chloride-induced tight conformation of human glutamic acid-1 plasminogen. Biochemistry 1995; 34(29): 9581-6.
[http://dx.doi.org/10.1021/bi00029a035] [PMID: 7626628]
[51]
Urano T, Chibber BAK, Castellino FJ. The reciprocal effects of epsilon-aminohexanoic acid and chloride ion on the activation of human [Glu1]plasminogen by human urokinase. Proc Natl Acad Sci USA 1987; 84(12): 4031-4.
[http://dx.doi.org/10.1073/pnas.84.12.4031] [PMID: 3473492]
[52]
Robbins KC, Summaria L, Hsieh B, Shah RJ. The peptide chains of human plasmin. Mechanism of activation of human plasminogen to plasmin. J Biol Chem 1967; 242(10): 2333-42.
[PMID: 4226004]
[53]
Wistedt AC, Kotarsky H, Marti D, et al. Kringle 2 mediates high affinity binding of plasminogen to an internal sequence in streptococcal surface protein PAM. J Biol Chem 1998; 273(38): 24420-4.
[http://dx.doi.org/10.1074/jbc.273.38.24420] [PMID: 9733732]
[54]
Rios-Steiner JL, Schenone M, Mochalkin I, Tulinsky A, Castellino FJ. Structure and binding determinants of the recombinant kringle-2 domain of human plasminogen to an internal peptide from a group A Streptococcal surface protein. J Mol Biol 2001; 308(4): 705-19.
[http://dx.doi.org/10.1006/jmbi.2001.4646] [PMID: 11350170]
[55]
Fu Q, Figuera-Losada M, Ploplis VA, et al. The lack of binding of VEK-30, an internal peptide from the group A streptococcal M-like protein, PAM, to murine plasminogen is due to two amino acid replacements in the plasminogen kringle-2 domain. J Biol Chem 2008; 283(3): 1580-7.
[http://dx.doi.org/10.1074/jbc.M705063200] [PMID: 18039665]
[56]
Wang M, Zajicek J, Geiger JH, Prorok M, Castellino FJ. Solution structure of the complex of VEK-30 and plasminogen kringle 2. J Struct Biol 2010; 169(3): 349-59.
[http://dx.doi.org/10.1016/j.jsb.2009.09.011] [PMID: 19800007]
[57]
Chandrahas V, Glinton K, Liang Z, Donahue DL, Ploplis VA, Castellino FJ. Direct host plasminogen binding to bacterial surface M-protein pattern D strains of Streptococcus pyogenes is required for activation by natural coinherited SK2b protein. J Biol Chem 2015; 290(30): 18833-42.
[http://dx.doi.org/10.1074/jbc.M115.655365] [PMID: 26070561]
[58]
Hall SW, Humphries JE, Gonias SL. Inhibition of cell surface receptor-bound plasmin by alpha 2-antiplasmin and alpha 2-macroglobulin. J Biol Chem 1991; 266(19): 12329-36.
[PMID: 1712017]
[59]
Macheboeuf P, Buffalo C, Fu CY, et al. Streptococcal M1 protein constructs a pathological host fibrinogen network. Nature 2011; 472(7341): 64-8.
[http://dx.doi.org/10.1038/nature09967] [PMID: 21475196]
[60]
Sumitomo T, Nakata M, Higashino M, Yamaguchi M, Kawabata S, Group A. Group A Streptococcus exploits human plasminogen for bacterial translocation across epithelial barrier via tricellular tight junctions. Sci Rep 2016; 7: 20069.
[http://dx.doi.org/10.1038/srep20069] [PMID: 26822058]
[61]
Magalhães V, Andrade EB, Alves J, et al. Group B Streptococcus hijacks the host plasminogen system to promote brain endothelial cell invasion. PLoS One 2013; 8(5)e63244
[http://dx.doi.org/10.1371/journal.pone.0063244] [PMID: 23658816]
[62]
Lijnen HR. Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost 2001; 86(1): 324-33.
[http://dx.doi.org/10.1055/s-0037-1616230] [PMID: 11487021]
[63]
Siemens N, Patenge N, Otto J, Fiedler T, Kreikemeyer B. Streptococcus pyogenes M49 plasminogen/plasmin binding facilitates keratinocyte invasion via integrin-integrin-linked kinase (ILK) pathways and protects from macrophage killing. J Biol Chem 2011; 286(24): 21612-22.
[http://dx.doi.org/10.1074/jbc.M110.202671] [PMID: 21521694]
[64]
Agrahari G, Liang Z, Mayfield JA, Balsara RD, Ploplis VA, Castellino FJ. Complement-mediated opsonization of invasive group A Streptococcus pyogenes strain AP53 is regulated by the bacterial two-component cluster of virulence responder/sensor (CovRS) system. J Biol Chem 2013; 288(38): 27494-504.
[http://dx.doi.org/10.1074/jbc.M113.494864] [PMID: 23928307]
[65]
Agrahari G, Liang Z, Glinton K, Lee SW, Ploplis VA, Castellino FJ. Streptococcus pyogenes employs strain-dependent mechanisms of C3b inactivation to inhibit phagocytosis and killing of bacteria. J Biol Chem 2016; 291(17): 9181-9.
[http://dx.doi.org/10.1074/jbc.M115.704221] [PMID: 26945067]
[66]
Sun H, Ringdahl U, Homeister JW, et al. Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 2004; 305(5688): 1283-6.
[http://dx.doi.org/10.1126/science.1101245] [PMID: 15333838]
[67]
Kurpiewski GE, Forrester LJ, Campbell BJ, Barrett JT. Platelet aggregation by Streptococcus pyogenes. Infect Immun 1983; 39(2): 704-8.
[PMID: 6403459]
[68]
Cox D, Kerrigan SW, Watson SP. Platelets and the innate immune system: mechanisms of bacterial-induced platelet activation. J Thromb Haemost 2011; 9(6): 1097-107.
[http://dx.doi.org/10.1111/j.1538-7836.2011.04264.x] [PMID: 21435167]
[69]
Shannon O, Hertzén E, Norrby-Teglund A, Mörgelin M, Sjöbring U, Björck L. Severe streptococcal infection is associated with M protein-induced platelet activation and thrombus formation. Mol Microbiol 2007; 65(5): 1147-57.
[http://dx.doi.org/10.1111/j.1365-2958.2007.05841.x] [PMID: 17662041]
[70]
Berge A, Björck L. Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins. J Biol Chem 1995; 270(17): 9862-7.
[http://dx.doi.org/10.1074/jbc.270.17.9862] [PMID: 7730368]
[71]
Palm F, Sjöholm K, Malmström J, Shannon O. Complement activation occurs at the surface of platelets activated by streptococcal M1 protein and this results in phagocytosis of platelets. J Immunol 2019; 202(2): 503-13.
[http://dx.doi.org/10.4049/jimmunol.1800897] [PMID: 30541884]
[72]
Hurley SM, Lutay N, Holmqvist B, Shannon O. The dynamics of platelet activation during progression of streptococcal sepsis. PLoS One 2016; 11(9)e0163531
[http://dx.doi.org/10.1371/journal.pone.0163531] [PMID: 27656898]
[73]
Cunningham MW. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 2000; 13(3): 470-511.
[http://dx.doi.org/10.1128/CMR.13.3.470] [PMID: 10885988]
[74]
Dale JB, Penfound TA, Chiang EY, Walton WJ. New 30-valent M protein-based vaccine evokes cross-opsonic antibodies against non-vaccine serotypes of group A streptococci. Vaccine 2011; 29(46): 8175-8.
[http://dx.doi.org/10.1016/j.vaccine.2011.09.005] [PMID: 21920403]
[75]
Dale JB, Penfound TA, Tamboura B, et al. Potential coverage of a multivalent M protein-based group A streptococcal vaccine. Vaccine 2013; 31(12): 1576-81.
[http://dx.doi.org/10.1016/j.vaccine.2013.01.019] [PMID: 23375817]
[76]
Bessen D, Fischetti VA. Influence of intranasal immunization with synthetic peptides corresponding to conserved epitopes of M protein on mucosal colonization by group A streptococci. Infect Immun 1988; 56(10): 2666-72.
[PMID: 2458320]
[77]
Bessen D, Fischetti VA. Passive acquired mucosal immunity to group A streptococci by secretory immunoglobulin A. J Exp Med 1988; 167(6): 1945-50.
[http://dx.doi.org/10.1084/jem.167.6.1945] [PMID: 3290383]
[78]
Bessen D, Fischetti VA. Synthetic peptide vaccine against mucosal colonization by group A streptococci. I. Protection against a heterologous M serotype with shared C repeat region epitopes. J Immunol 1990; 145(4): 1251-6.
[PMID: 1696296]
[79]
Pruksakorn S, Currie B, Brandt E, et al. Towards a vaccine for rheumatic fever: identification of a conserved target epitope on M protein of group A streptococci. Lancet 1994; 344(8923): 639-42.
[http://dx.doi.org/10.1016/S0140-6736(94)92083-4] [PMID: 7520963]
[80]
Pruksakorn S, Galbraith A, Houghten RA, Good MF. Conserved T and B cell epitopes on the M protein of group A streptococci. Induction of bactericidal antibodies. J Immunol 1992; 149(8): 2729-35.
[PMID: 1383324]
[81]
Brandt ER, Hayman WA, Currie B, et al. Opsonic human antibodies from an endemic population specific for a conserved epitope on the M protein of group A streptococci. Immunology 1996; 89(3): 331-7.
[http://dx.doi.org/10.1046/j.1365-2567.1996.d01-754.x] [PMID: 8958044]
[82]
Relf WA, Cooper J, Brandt ER, et al. Mapping a conserved conformational epitope from the M protein of group A streptococci. Pept Res 1996; 9(1): 12-20.
[PMID: 8727479]
[83]
Hayman WA, Brandt ER, Relf WA, Cooper J, Saul A, Good MF. Mapping the minimal murine T cell and B cell epitopes within a peptide vaccine candidate from the conserved region of the M protein of group A streptococcus. Int Immunol 1997; 9(11): 1723-33.
[http://dx.doi.org/10.1093/intimm/9.11.1723] [PMID: 9418133]
[84]
Batzloff MR, Hayman WA, Davies MR, et al. Protection against group A streptococcus by immunization with J8-diphtheria toxoid: contribution of J8- and diphtheria toxoid-specific antibodies to protection. J Infect Dis 2003; 187(10): 1598-608.
[http://dx.doi.org/10.1086/374800] [PMID: 12721940]
[85]
Pandey M, Wykes MN, Hartas J, Good MF, Batzloff MR. Long-term antibody memory induced by synthetic peptide vaccination is protective against Streptococcus pyogenes infection and is independent of memory T cell help. J Immunol 2013; 190(6): 2692-701.
[http://dx.doi.org/10.4049/jimmunol.1202333] [PMID: 23401589]
[86]
Pandey M, Langshaw E, Hartas J, Lam A, Batzloff MR, Good MF. A synthetic M protein peptide synergizes with a CXC chemokine protease to induce vaccine-mediated protection against virulent streptococcal pyoderma and bacteremia. J Immunol 2015; 194(12): 5915-25.
[http://dx.doi.org/10.4049/jimmunol.1500157] [PMID: 25980008]
[87]
Batzloff MR, Yan H, Davies MR, et al. Toward the development of an antidisease, transmission-blocking intranasal vaccine for group a streptococcus. J Infect Dis 2005; 192(8): 1450-5.
[http://dx.doi.org/10.1086/466528] [PMID: 16170764]
[88]
Batzloff MR, Hartas J, Zeng W, Jackson DC, Good MF. Intranasal vaccination with a lipopeptide containing a conformationally constrained conserved minimal peptide, a universal T cell epitope, and a self-adjuvanting lipid protects mice from group A streptococcus challenge and reduces throat colonization. J Infect Dis 2006; 194(3): 325-30.
[http://dx.doi.org/10.1086/505146] [PMID: 16826480]
[89]
Sun H, Wang X, Degen JL, Ginsburg D. Reduced thrombin generation increases host susceptibility to group A streptococcal infection. Blood 2009; 113(6): 1358-64.
[http://dx.doi.org/10.1182/blood-2008-07-170506] [PMID: 19056689]
[90]
Yan SB, Nelson DR. Effect of factor V Leiden polymorphism in severe sepsis and on treatment with recombinant human activated protein C. Crit Care Med 2004; 32(5)(Suppl.): S239-46.
[http://dx.doi.org/10.1097/01.CCM.0000126122.34119.D1] [PMID: 15118525]
[91]
Weiler H, Kerlin B, Lytle MC, Factor V, Factor V. Leiden polymorphism modifies sepsis outcome: evidence from animal studies. Crit Care Med 2004; 32(5)(Suppl.): S233-8.
[http://dx.doi.org/10.1097/01.CCM.0000126126.79861.08] [PMID: 15118524]
[92]
Smith W, Hale JH, Smith MM. The role of coagulase in staphylococcal infections. Br J Exp Pathol 1947; 28(1): 57-67.
[PMID: 20290308]
[93]
Cheng AG, McAdow M, Kim HK, Bae T, Missiakas DM, Schneewind O. Contribution of coagulases towards Staphylococcus aureus disease and protective immunity. PLoS Pathog 2010; 6(8)e1001036
[http://dx.doi.org/10.1371/journal.ppat.1001036] [PMID: 20700445]
[94]
Thomer L, Emolo C, Thammavongsa V, et al. Antibodies against a secreted product of Staphylococcus aureus trigger phagocytic killing. J Exp Med 2016; 213(3): 293-301.
[http://dx.doi.org/10.1084/jem.20150074] [PMID: 26880578]
[95]
Panizzi P, Friedrich R, Fuentes-Prior P, Bode W, Bock PE. The staphylocoagulase family of zymogen activator and adhesion proteins. Cell Mol Life Sci 2004; 61(22): 2793-8.
[http://dx.doi.org/10.1007/s00018-004-4285-7] [PMID: 15558209]
[96]
McAdow M, Missiakas DM, Schneewind O. Staphylococcus aureus secretes coagulase and von Willebrand factor binding protein to modify the coagulation cascade and establish host infections. J Innate Immun 2012; 4(2): 141-8.
[http://dx.doi.org/10.1159/000333447] [PMID: 22222316]
[97]
Panizzi P, Nahrendorf M, Figueiredo JL, et al. In vivo detection of Staphylococcus aureus endocarditis by targeting pathogen-specific prothrombin activation. Nat Med 2011; 17(9): 1142-6.
[http://dx.doi.org/10.1038/nm.2423] [PMID: 21857652]
[98]
Lishko VK, Podolnikova NP, Yakubenko VP, et al. Multiple binding sites in fibrinogen for integrin alphaMbeta2 (Mac-1). J Biol Chem 2004; 279(43): 44897-906.
[http://dx.doi.org/10.1074/jbc.M408012200] [PMID: 15304494]
[99]
Flick MJ, Du X, Witte DP, et al. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 2004; 113(11): 1596-606.
[http://dx.doi.org/10.1172/JCI20741] [PMID: 15173886]
[100]
Oehmcke S, Shannon O, von Köckritz-Blickwede M, et al. Treatment of invasive streptococcal infection with a peptide derived from human high-molecular weight kininogen. Blood 2009; 114(2): 444-51.
[http://dx.doi.org/10.1182/blood-2008-10-182527] [PMID: 19433860]


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VOLUME: 21
ISSUE: 2
Year: 2020
Page: [193 - 201]
Pages: 9
DOI: 10.2174/1389450120666190926152914
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