Interaction of streptococcal plasminogen binding proteins with the host fibrinolytic system

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue NOV, 2013, Pages

  Fulde, Marcus ^a   Bergmann, Simone ^b   Steinert, Michael ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Enolase; M protein; Phagocytosis; Plasminogen; SCM; Streptococcus; Transmigration

Indexed keywords

COMPLEMENT COMPONENT C4B; ENOLASE; FIBRINOGEN; M PROTEIN; OXIDOREDUCTASE; PHOSPHOGLYCERATE MUTASE; PLASMINOGEN; PROTEINASE; BACTERIAL PROTEIN; CARRIER PROTEIN; PLASMIN; PLASMINOGEN-BINDING PROTEIN, BACTERIA; PROTEIN BINDING; PLASMINOGEN BINDING PROTEIN, BACTERIA;

BACTERIAL VIRULENCE; CELL ADHESION; CELL PHAGOCYTOSIS; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FIBRINOLYSIS; IMMUNE EVASION; NONHUMAN; PROTEIN BINDING; PROTEIN INTERACTION; SHORT SURVEY; STREPTOCOCCUS; ANIMAL; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGY; M-PROTEIN; PHAGOCYTOSIS; REVIEW; SCM; TRANSMIGRATION;

ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; FIBRINOLYSIN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; PLASMINOGEN; PROTEIN BINDING; STREPTOCOCCUS;

ENOLASE; M-PROTEIN; PHAGOCYTOSIS; PLASMINOGEN; SCM; STREPTOCOCCUS; TRANSMIGRATION;

EID: 84897928634     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00085     Document Type: Short Survey

References (92)

1. Abraham, E. (2000). Coagulation abnormalities in acute lung injury and sepsis. Am. J. Respir. Cell Mol. Biol. 22, 401-404. doi: 10.1165/ajrcmb.22.4.f184
2. Agarwal, V., Hammerschmidt, S., Malm, S., Bergmann, S., Riesbeck, K., and Blom, A. M. (2012). Enolase of Streptococcus pneumoniae binds human complement inhibitor C4b-binding protein and contributes to complement evasion. J. Immunol. 189, 3575-3584. doi: 10.4049/jimmunol.1102934
3. Agarwal, V., Kuchipudi, A., Fulde, M., Riesbeck, K., Bergmann, S., and Blom, A. M. (2013). Streptococcus pneumoniae Endopeptidase, O (PepO) Is a Multifunctional Plasminogen- and fibronectin-binding protein, facilitating evasion of innate immunity and invasion of host cells. J. Biol. Chem. 288, 6849-6863. doi: 10.1074/jbc.M112.405530
4. Attali, C., Frolet, C., Durmort, C., Offant, J., Vernet, T., and Di Guilmi, A. M. (2008a). Streptococcus pneumoniae choline-binding protein E interaction with plasminogen/plasmin stimulates migration across the extracellular matrix. Infect. Immun. 76, 466-476. doi: 10.1128/IAI.01261-07
5. Attali, C., Durmort, C., Vernet, T., and Di Guilmi, A. M. (2008b). The interaction of Streptococcus pneumoniae with plasmin mediates transmigration across endothelial and epithelial monolayers by intercellular junction cleavage. Infect. Immun. 76, 5350-5356. doi: 10.1128/IAI.00184-08
6. Berge, A., Sjöbring, U. (1993). PAM, a novel plasminogen-binding protein from Streptococcus pyogenes. J. Biol. Chem. 268, 25417-25424.
7. Bergmann, R., Dinkla, K., Nitsche-Schmitz, D. P., Graham, R. M., Luttge, M., Sanderson-Smith, M. L., et al. (2011). Biological functions of GCS3, a novel plasminogen-binding protein of Streptococcus dysgalactiae ssp. equisimilis. Int. J. Med. Microbiol. 301, 157-164. doi: 10.1016/j.ijmm.2010.06.007
8. Bergmann, S., and Hammerschmidt, S. (2006). Versatility of pneumococcal surface proteins. Microbiology 152, 295-303. doi: 10.1099/mic.0.28610-0
9. Bergmann, S., and Hammerschmidt, S. (2007). Fibrinolysis and host response in bacterial infections. Thromb. Haemost. 98, 512-520. doi: 10.1160/TH07-02-0117
10. Bergmann, S., Rohde, M., Chhatwal, G. S., and Hammerschmidt, S. (2001). alpha-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol. Microbiol. 40, 1273-1287. doi: 10.1046/j.1365-2958.2001.02448.x
11. Bergmann, S., Rohde, M., and Hammerschmidt, S. (2004). Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect. Immun. 72, 2416-2419. doi: 10.1128/IAI.72.4.2416-2419.2004
12. Bergmann, S., Rohde, M., Preissner, K. T., and Hammerschmidt, S. (2005). The nine residue plasminogen-binding motif of the pneumococcal enolase is the major cofactor of plasmin-mediated degradation of extracellular matrix, dissolution of fibrin and transmigration. Thromb. Haemost. 94, 304-311. doi: 10.1160/TH05-05-0369
13. Bergmann, S., Schoenen, H., and Hammerschmidt, S. (2013). The interaction between bacterial enolase and plasminogen promotes adherence of Streptococcus pneumoniae to epithelial and endothelial cells. Int. J. Med. Microbiol. doi: 10.1016/j.ijmm.2013.06.002. [Epub ahead of print].
14. Bergmann, S., Wild, D., Diekmann, O., Frank, R., Bracht, D., Chhatwal, G. S., et al. (2003). Identification of a novel plasmin(ogen)-binding motif in surface displayed alpha-enolase of Streptococcus pneumoniae. Mol. Microbiol. 49, 411-423. doi: 10.1046/j.1365-2958.2003.03557.x
15. Bernardo-Garcia, N., Bartual, S. G., Fulde, M., Bergmann, S., and Hermoso, J. A. (2011). Crystallization and preliminary X-ray diffraction analysis of phosphoglycerate kinase from Streptococcus pneumoniae. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 1285-1289. doi: 10.1107/S1744309111030922
16. Boel, G., Jin, H., and Pancholi, V. (2005). Inhibition of cell surface export of group A streptococcal anchorless surface dehydrogenase affects bacterial adherence and antiphagocytic properties. Infect. Immun. 73, 6237-6248. doi: 10.1128/IAI.73.10.6237-6248.2005
17. Boone, T. J., Burnham, C. A., and Tyrrell, G. J. (2011).Binding of group B streptococcal phosphoglycerate kinase to plasminogen and actin. Microb. Pathog. 51, 255-261. doi: 10.1016/j.micpath.2011.06.005
18. Boone, T. J., and Tyrrell, G. J. (2012).Identification of the actin and plasminogen binding regions of group B streptococcal phosphoglycerate kinase. J. Biol. Chem. 287, 29035-29044. doi: 10.1074/jbc.M112.361261
19. Boxrud, P. D., and Bock, P. E. (2000). Streptokinase binds preferentially to the extended conformation of plasminogen through lysine binding site and catalytic domain interactions. Biochemistry 39, 13974-13981. doi: 10.1021/bi000594i
20. Boxrud, P. D., Verhamme, I. M., and Bock, P. E. (2004). Resolution of conformational activation in the kinetic mechanism of plasminogen activation by streptokinase. J. Biol. Chem. 279, 36633-36641. doi: 10.1074/jbc.M405264200
21. Castellino, F. J., and Violand, B. N. (1979). The fibrinolytic system-basic considerations. Prog. Cardiovasc. Dis. 21, 241-254. doi: 10.1016/0033-0620(79)90012-4
22. Chen, C., Tang, J., Dong, W., Wang, C., Feng, Y., Wang, J., et al. (2007). A glimpse of streptococcal toxic shock syndrome from comparative genomics of S. suis 2 Chinese isolates. PLoS ONE. 2:e315. doi: 10.1371/journal.pone.0000315
23. Cook, S. M., Skora, A., Gillen, C. M., Walker, M. J., and McArthur, J. D. (2012). Streptokinase variants from Streptococcus pyogenes isolates display altered plasminogen activation characteristics - implications for pathogenesis. Mol. Microbiol. 86, 1052-1062. doi: 10.1111/mmi.12037
24. Courtney, H. S., Hasty, D. L., and Dale, J. B. (2006). Anti-phagocytic mechanisms of Streptococcus pyogenes: binding of fibrinogen to M-related protein. Mol. Microbiol. 59, 936-947. doi: 10.1111/j.1365-2958.2005.04977.x
25. Dano, K., Andreasen, P. A., Grondahl-Hansen, J., Kristensen, P., Nielsen, L. S., and Skriver, L. (1985). Plasminogen activators, tissue degradation, and cancer. Adv. Cancer Res. 44, 139-266. doi: 10.1016/S0065-230X(08)60028-7
26. Devriese, L. A., Hommez, J., Klipper-Bälz, R., and Schleifer, K.-H. (1986). Streptococcus canis sp. nov.: a species of Group G streptococci from animals. Int. J. Syst. Bacteriol. 36, 422-425. doi: 10.1099/00207713-36-3-422
27. Eberhard, T., Kronvall, G., and Ullberg, M. (1999). Surface bound plasmin promotes migration of Streptococcus pneumoniae through reconstituted basement membranes. Microb. Pathog. 26, 175-181. doi: 10.1006/mpat.1998.0262
28. Ehinger, S., Schubert, W. D., Bergmann, S., Hammerschmidt, S., and Heinz, D. W. (2004). Plasmin(ogen)-binding alpha-enolase from Streptococcus pneumoniae: crystal structure and evaluation of plasmin(ogen)-binding sites. J. Mol. Biol. 343, 997-1005. doi: 10.1016/j.jmb.2004.08.088
29. Esgleas, M., Li, Y., Hancock, M. A., Harel, J., Dubreuil, J. D., and Gottschalk, M. (2008). Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154, 2668-2679. doi: 10.1099/mic.0.2008/017145-0
30. Fischetti, V. A. (1991). Streptococcal M protein. Sci. Am. 264, 58-65. doi: 10.1038/scientificamerican0691-58
31. Fittipaldi, N., Segura, M., Grenier, D., and Gottschalk, M. (2012). Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol. 7, 259-279. doi: 10.2217/fmb.11.149
32. Fu, Q., Figuera-Losada, M., Ploplis, V. A., Cnudde, S., Geiger, J. H., Prorok, M., et al. (2008). 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. 283, 1580-1587. doi: 10.1074/jbc.M705063200
33. Fulde, M., Rohde, M., Hitzmann, A., Preissner, K. T., Nitsche-Schmitz, D. P., Nerlich, A., et al. (2011). SCM, a novel M-like protein from Streptococcus canis, binds (mini)-plasminogen with high affinity and facilitates bacterial transmigration. Biochem. J. 434, 523-535. doi: 10.1042/BJ20101121
34. Fulde, M., Rohde, M., Polok, A., Preissner, K. T., Chhatwal, G. S., and Bergmann, S. (2013a). Cooperative plasminogen recruitment to the surface of Streptococcus canis via M protein and enolase enhances bacterial survival. mBio 4, e00629-e00612. doi: 10.1128/mBio.00629-12
35. Fulde, M., Bernardo-Garcĺa, N., Rohde, M., Nachtigall, N., Frank, R., Preissner, K. T., et al. (2013b). Pneumococcal phosphoglycerate kinase interacts with plasminogen and its tissue activator. Thromb. Haemost. 111. doi: 10.1160/TH13-05-0421. [Epub ahead of print].
36. Fulde, M., and Valentin-Weigand, P. (2013).Epidemiology and pathogenicity of zoonotic streptococci. Curr. Top. Microbiol. Immunol. 368, 49-81. doi: 10.1007/82_2012_277
37. Gase, K., Gase, A., Schirmer, H., and Malke, H. (1996). Cloning, sequencing and functional overexpression of the Streptococcus equisimilis H46A gapC gene encoding a glyceraldehyde-3-phosphate dehydrogenase that also functions as a plasmin(ogen)-binding protein. Purification and biochemical characterization of the protein. Eur. J. Biochem. 239, 42-51. doi: 10.1111/j.1432-1033.1996.0042u.x
38. Gunther, A., Mosavi, P., Heinemann, S., Ruppert, C., Muth, H., Markart, P., et al. (2000). Alveolar fibrin formation caused by enhanced procoagulant and depressed fibrinolytic capacities in severe pneumonia. Comparison with the acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 161, 454-462. doi: 10.1164/ajrccm.161.2.9712038
39. Hall, S. W., Humphries, J. E., and Gonias, S. L. (1991).Inhibition of cell surface receptor-bound plasmin by alpha 2-antiplasmin and alpha 2-macroglobulin. J. Biol. Chem. 266, 12329-12336.
40. Hoffmann, C., Berking, A., Agerer, F., Buntru, A., Neske, F., Chhatwal, G. S., et al. (2010). Caveolin limits membrane microdomain mobility and integrin-mediated uptake of fibronectin-binding pathogens. J. Cell. Sci. 15 123, 4280-4291. doi: 10.1242/jcs.064006
41. Hollands, A., Gonzalez, D., Leire, E., Donald, C., Gallo, R. L., Sanderson-Smith, M., et al. (2012). A bacterial pathogen co-opts host plasmin to resist killing by cathelicidin antimicrobial peptides. J. Biol. Chem. 287, 40891-40897. doi: 10.1074/jbc.M112.404582
42. Itzek, A., Gillen, C. M., Fulde, M., Friedrichs, C., Rodloff, A. C., Chhatwal, G. S., et al. (2010). Contribution of plasminogen activation towards the pathogenic potential of oral streptococci. PLoS ONE. 5:e13826. doi: 10.1371/journal.pone.0013826
43. Jensch, I., Gamez, G., Rothe, M., Ebert, S., Fulde, M., Somplatzki, D., et al. (2010). PavB is a surface-exposed adhesin of Streptococcus pneumoniae contributing to nasopharyngeal colonization and airways infections. Mol. Microbiol. 77, 22-43. doi: 10.1111/j.1365-2958.2010.07189.x
44. Jin, H., Song, Y. P., Boel, G., Kochar, J., and Pancholi, V. (2005). Group A streptococcal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells. J. Mol. Biol. 350, 27-41. doi: 10.1016/j.jmb.2005.04.063
45. Jones, M. N., and Holt, R. G. (2007). Cloning and characterization of an alpha-enolase of the oral pathogen Streptococcus mutans that binds human plasminogen. Biochem. Biophys. Res. Commun. 364, 924-929. doi: 10.1016/j.bbrc.2007.10.098
46. Kalia, A., and Bessen, D. E. (2004). Natural selection and evolution of streptococcal virulence genes involved in tissue-specific adaptations. J. Bacteriol. 186, 110-121. doi: 10.1128/JB.186.1.110-121.2004
47. Kinnby, B., Booth, N. A., and Svensater, G. (2008).Plasminogen binding by oral streptococci from dental plaque and inflammatory lesions. Microbiology 154, 924-931. doi: 10.1099/mic.0.2007/013235-0
48. Lahteenmaki, K., Edelman, S., and Korhonen, T. K. (2005). Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol. 13, 79-85. doi: 10.1016/j.tim.2004.12.003
49. Lahteenmaki, K., Kuusela, P., and Korhonen, T. K. (2001). Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25, 531-552. doi: 10.1016/S0168-6445(01)00067-5
50. Linke, C., Siemens, N., Oehmcke, S., Radjainia, M., Law, R. H., Whisstock, J. C., et al. (2012). The extracellular protein factor Epf from Streptococcus pyogenes is a cell surface adhesin that binds to cells through an N-terminal domain containing a carbohydrate-binding module. J. Biol. Chem. 287, 38178-38189. doi: 10.1074/jbc.M112.376434
51. Liotta, L. A., Goldfarb, R. H., Brundage, R., Siegal, G. P., Terranova, V., and Garbisa, S. (1981). Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res. 41, 4629-4636.
52. Lottenberg, R., Broder, C. C., Boyle, M. D., Kain, S. J., Schroeder, B. L., and Curtiss, R. 3rd. (1992). Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor. J. Bacteriol. 174, 5204-5210.
53. Lottenberg, R., Minning-Wenz, D., and Boyle, M. D. (1994). Capturing host plasmin(ogen): a common mechanism for invasive pathogens. Trends Microbiol. 2, 20-24. doi: 10.1016/0966-842X(94)90340-9
54. Lu, Q., Lu, H., Qi, J., Lu, G., and Gao, G. F. (2012). An octamer of enolase from Streptococcus suis. Protein Cell 3, 769-780. doi: 10.1007/s13238-012-2040-7
55. Marshall, J. M., Brown, A. J., and Ponting, C. P. (1994). Conformational studies of human plasminogen and plasminogen fragments: evidence for a novel third conformation of plasminogen. Biochemistry 33, 3599-3606. doi: 10.1021/bi00178a017
56. Marti, D. N., Hu, C. K., An, S. S., von Haller, P., Schaller, J., and Llinas, M. (1997). Ligand preferences of kringle 2 and homologous domains of human plasminogen: canvassing weak, intermediate, and high-affinity binding sites by 1H-NMR. Biochemistry 36, 11591-11604. doi: 10.1021/bi971316v
57. Miles, L. A., Dahlberg, C. M., Plescia, J., Felez, J., Kato, K., and Plow, E. F. (1991). Role of cell-surface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry 30, 1682-1691. doi: 10.1021/bi00220a034
58. Miles, L. A., and Plow, E. F. (1985). Binding and activation of plasminogen on the platelet surface. J. Biol. Chem. 260, 4303-4311.
59. Miyashita, C., Wenzel, E., and Heiden, M. (1988). Plasminogen: a brief introduction into its biochemistry and function. Haemostasis 18(Suppl. 1), 7-13.
60. Olsen, R. J., Shelburne, S. A., and Musser, J. M. (2009). Molecular mechanisms underlying group A streptococcal pathogenesis. Cell. Microbiol. 11, 1-12. doi: 10.1111/j.1462-5822.2008.01225.x
61. Pancholi, V. (2001). Multifunctional alpha-enolase: its role in diseases. Cell. Mol. Life Sci. 58, 902-920. doi: 10.1007/PL00000910
62. Pancholi, V., and Chhatwal, G. S. (2003). Housekeeping enzymes as virulence factors for pathogens. Int. J. Med. Microbiol. 293, 391-401. doi: 10.1078/1438-4221-00283
63. Pancholi, V., and Fischetti, V. A. (1992). A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 176, 415-426. doi: 10.1084/jem.176.2.415
64. Pancholi, V., and Fischetti, V. A. (1993). Glyceraldehyde-3-phosphate dehydrogenase on the surface of group A streptococci is also an ADP-ribosylating enzyme. Proc. Natl. Acad. Sci. U.S.A. 90, 8154-8158. doi: 10.1073/pnas.90.17.8154
65. Pancholi, V., and Fischetti, V. A. (1997). A novel plasminogen/plasmin binding protein on the surface of group A streptococci. Adv. Exp. Med. Biol. 418, 597-599. doi: 10.1007/978-1-4899-1825-3_138
66. Pancholi, V., and Fischetti, V. A. (1998). alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273, 14503-14515. doi: 10.1074/jbc.273.23.14503
67. Pancholi, V., Fontan, P., and Jin, H. (2003). Plasminogen-mediated group A streptococcal adherence to and pericellular invasion of human pharyngeal cells. Microb. Pathog. 35, 293-303. doi: 10.1016/j.micpath.2003.08.004
68. Papasergi, S., Garibaldi, M., Tuscano, G., Signorino, G., Ricci, S., Peppoloni, S., et al. (2010). Plasminogen- and fibronectin-binding protein B is involved in the adherence of Streptococcus pneumoniae to human epithelial cells. J. Biol. Chem. 285, 7517-7524. doi: 10.1074/jbc.M109.062075
69. Paterson, G. K., and Orihuela, C. J. (2010). Pneumococcal microbial surface components recognizing adhesive matrix molecules targeting of the extracellular matrix. Mol. Microbiol. 77, 1-5. doi: 10.1111/j.1365-2958.2010.07190.x
70. Plow, E. F., Freaney, D. E., Plescia, J., and Miles, L. A. (1986). The plasminogen system and cell surfaces: evidence for plasminogen and urokinase receptors on the same cell type. J. Cell Biol. 103, 2411-2420. doi: 10.1083/jcb.103.6.2411
71. Pollanen, J., Stephens, R. W., and Vaheri, A. (1991). Directed plasminogen activation at the surface of normal and malignant cells. Adv. Cancer Res. 57, 273-328. doi: 10.1016/S0065-230X(08)61002-7
72. Ponting, C. P., Marshall, J. M., and Cederholm-Williams, S. A. (1992). Plasminogen: a structural review. Blood Coagul. Fibrinolysis 3, 605-614. doi: 10.1097/00001721-199210000-00012
73. Ringdahl, U., and Sjöbring, U. (2000). Analysis of plasminogen-binding M proteins of Streptococcus pyogenes. Methods 21, 143-150. doi: 10.1006/meth.2000.0985
74. Sanderson-Smith, M. L., De Oliveira, D. M., Ranson, M., and McArthur, J. D. (2012). Bacterial plasminogen receptors: mediators of a multifaceted relationship. J. Biomed. Biotechnol. 2012, 272148. doi: 10.1155/2012/272148
75. Sanderson-Smith, M. L., Dinkla, K., Cole, J. N., Cork, A. J., Maamary, P. G., McArthur, J. D., et al. (2008). M protein-mediated plasminogen binding is essential for the virulence of an invasive Streptococcus pyogenes isolate. FASEB J. 22, 2715-2722. doi: 10.1096/fj.07-105643
76. Sanderson-Smith, M. L., Dowton, M., Ranson, M., and Walker, M. J. (2007). The plasminogen-binding group A streptococcal M protein-related protein Prp binds plasminogen via arginine and histidine residues. J. Bacteriol. 189, 1435-1440. doi: 10.1128/JB.01218-06
77. Sanderson-Smith, M., Batzloff, M., Sriprakash, K. S., Dowton, M., Ranson, M., and Walker, M. J. (2006a). Divergence in the plasminogen-binding group a streptococcal M protein family: functional conservation of binding site and potential role for immune selection of variants. J. Biol. Chem. 281, 3217-3226. doi: 10.1074/jbc.M508758200
78. Sanderson-Smith, M. L., Walker, M. J., and Ranson, M. (2006b). The maintenance of high affinity plasminogen binding by group A streptococcal plasminogen-binding M-like protein is mediated by arginine and histidine residues within the a1 and a2 repeat domains. J. Biol. Chem. 281, 25965-25971. doi: 10.1074/jbc.M603846200
79. Seifert, K. N., McArthur, W. P., Bleiweis, A. S., and Brady, L. J. (2003). Characterization of group B streptococcal glyceraldehyde-3-phosphate dehydrogenase: surface localization, enzymatic activity, and protein-protein interactions. Can. J. Microbiol. 49, 350-356. doi: 10.1139/w03-042
80. Siemens, N., Patenge, N., Otto, J., Fiedler, T., and Kreikemeyer, B. (2011). Streptococcus pyogenes M49 plasminogen/plasmin binding facilitates keratinocyte invasion via integrin-integrin-linked kinase (ILK) pathways and protects from macrophage killing. J. Biol. Chem. 286, 21612-21622. doi: 10.1074/jbc.M110.202671
81. Staats, J. J., Feder, I., Okwumabua, O., and Chengappa, M. (1997). Streptococcus suis: past and present. Vet. Res. Commun. 21, 831-407. doi: 10.1023/A:1005870317757
82. Sun, H., Ringdahl, U., Homeister, J. W., Fay, W. P., Engleberg, N. C., Yang, A. Y., et al. (2004). Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305, 1283-1286. doi: 10.1126/science.1101245
83. Tang, J., Wang, C., Feng, Y., Yang, W., Song, H., Chen, Z., et al. (2006). Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med. 3:e151. doi: 10.1371/journal.pmed.0030151
84. Teles, C., Smith, A., and Lang, S. (2012). Antibiotic modulation of the plasminogen binding ability of viridans group streptococci. Antimicrobial Agents Chemother. 56, 458-463. doi: 10.1128/AAC.00452-11
85. Terao, Y., Yamaguchi, M., Hamada, S., and Kawabata, S. (2006). Multifunctional glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pyogenes is essential for evasion from neutrophils. J. Biol. Chem. 281, 14215-14223. doi: 10.1074/jbc.M513408200
86. Valenti-Weigand, P., Benkel, P., Rohde, M., and Chhatwal, G. S. (1996). Entry and intracellular survival of group B streptococci in J774 macrophages. Infect. Immun. 64, 2467-2473.
87. van der Linden, M., Al-Lahham, A., Nicklas, W., and Reinert, R. R. (2009). Molecular characterization of pneumococcal isolates from pets and laboratory animals. PLoS ONE. 4:e8286. doi: 10.1371/journal.pone.0008286
88. Voss, S., Gámez, G., and Hammerschmidt, S. (2012). Impact of pneumococcal microbial surface components recognizing adhesive matrix molecules on colonization. Mol. Oral. Microbiol. 27, 246-256. doi: 10.1111/j.2041-1014.2012.00654.x
89. Walker, M. J., McArthur, J. D., McKay, F., and Ranson, M. (2005). Is plasminogen deployed as a Streptococcus pyogenes virulence factor. Trends Microbiol. 13, 308-313. doi: 10.1016/j.tim.2005.05.006
90. Winram, S. B., and Lottenberg, R. (1996). The plasmin-binding protein Plr of group A streptococci is identified as glyceraldehyde-3-phosphate dehydrogenase. Microbiology 142(Pt 8), 2311-2320. doi: 10.1099/13500872-142-8-2311
91. Wistedt, A. C., Ringdahl, U., Muller-Esterl, W., and Sjobring, U. (1995). Identification of a plasminogen-binding motif in PAM, a bacterial surface protein. Mol. Microbiol. 18, 569-578. doi: 10.1111/j.1365-2958.1995.mmi_18030569.x
92. Yamaguchi, M., Terao, Y., Mori, Y., Hamada, S., and Kawabata, S. (2008). PfbA, a novel plasmin- and fibronectin-binding protein of Streptococcus pneumoniae, contributes to fibronectin-dependent adhesion and antiphagocytosis. J. Biol. Chem. 283, 36272-36279. doi: 10.1074/jbc.M807087200