Site-restricted plasminogen activation mediated by group A streptococcal streptokinase variants

Biochemical Journal

Volumn 458, Issue 1, 2014, Pages 23-31

  Cook, Simon M ^a   Skora, Amanda ^a   Walker, Mark J ^b   Sanderson Smith, Martina L ^a   McArthur, Jason D ^a  

^a UNIVERSITY OF WOLLONGONG   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Fibrinogen; Plasminogen; Streptococcus pyogenes; Streptokinase; Thrombolytic therapy

Indexed keywords

ALPHA 2 ANTIPLASMIN; BACTERIAL PROTEIN; FIBRIN; FIBRINOGEN FRAGMENT D; PLASMINOGEN; PLASMINOGEN BINDING GROUP A STREPTOCOCCAL M PROTEIN; STREPTOKINASE; STREPTOKINASE TYPE 1; STREPTOKINASE TYPE 2A; STREPTOKINASE TYPE 2B; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CELL SURFACE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; LIGAND BINDING; NONHUMAN; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; STREPTOCOCCUS GROUP A;

CATALYTIC DOMAIN; PLASMINOGEN; STREPTOCOCCUS PYOGENES; STREPTOKINASE;

EID: 84892946255     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131305     Document Type: Article

References (48)

1. McArthur, J. D., Cook, S. M., Venturini, C. and Walker, M. J. (2012) The role of streptokinase as a virulence determinant of Streptococcus pyogenes: Potential for therapeutic targeting. Curr. Drug Targets 13, 297-307
2. Boxrud, P. D., Fay, W. P. and Bock, P. E. (2000) Streptokinase binds to human plasmin with high affinity, perturbs the plasmin active site, and induces expression of a substrate recognition exosite for plasminogen. J. Biol. Chem. 275, 14579-14589
3. 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
4. Ponting, C. P., Marshall, J. M. and Cederholm-Williams, S. A. (1992) Plasminogen: A structural review. Blood Coagul. Fibrinolysis 3, 605-614
5. Law, R. H., Caradoc-Davies, T., Cowieson, N., Horvath, A. J., Quek, A. J., Encarnacao, J. A., Steer, D., Cowan, A., Zhang, Q., Lu, B. G. et al. (2012) The X-ray crystal structure of full-length human plasminogen. Cell Rep. 1, 185-190
6. Xue, Y., Bodin, C. and Olsson, K. (2012) Crystal structure of the native plasminogen reveals an activation-resistant compact conformation. J. Thromb. Haemost. 10, 1385-1396
7. Brown, P. J., Gill, A. C., Nugent, P. G., McVey, J. H. and Tomley, F. M. (2001) Domains of invasion organelle proteins from apicomplexan parasites are homologous with the Apple domains of blood coagulation factor XI and plasma pre-kallikrein and are members of the PAN module superfamily. FEBS Lett. 497, 31-38
8. Brown, P. J., Mulvey, D., Potts, J. R., Tomley, F. M. and Campbell, I. D. (2003) Solution structure of a PAN module from the apicomplexan parasite Eimeria tenella . J. Struct. Funct. Genomics 4, 227-234
9. Castellino, F. J. and Ploplis, V. A. (2005) Structure and function of the plasminogen/plasmin system. Thromb. Haemost. 93, 647-654
10. Irigoyen, J. P., Munoz-Canoves, P., Montero, L., Koziczak, M. and Nagamine, Y. (1999) The plasminogen activator system: Biology and regulation. Cell. Mol. Life Sci. 56, 104-132
11. Cederholm-Williams, S. A. (1979) Kinetics of the reactions between streptokinase, plasmin and α2-antiplasmin. Eur. J. Biochem. 100, 125-132
12. Parry, M. A., Zhang, X. C. and Bode, I. (2000) Molecular mechanisms of plasminogen activation: Bacterial cofactors provide clues. Trends Biochem. Sci. 25, 53-59
13. 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
14. Sun, H., Ringdahl, U., Homeister, J., Fay, W. P., Engleberg, C., Yang, A., Rozek, X., Wang, L., Sjobring, U. and Ginsberg, D. (2004) Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305, 1283-1286
15. Khil, J., Im, M., Heath, A., Ringdahl, U., Mundada, L., Cary Engleberg, N. and Fay, W. P. (2003) Plasminogen enhances virulence of group A streptococci by streptokinase-dependent and streptokinase-independent mechanisms. J. Infect. Dis. 188, 497-505
16. 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
17. Zhang, Y., Liang, Z., Hsueh, H.-T., Ploplis, V. A. and Castellino, F. J. (2012) Characterization of streptokinases from group A streptococci reveals a strong functional relationship that supports the coinheritance of plasminogen-binding M protein and cluster 2b streptokinase. J. Biol. Chem. 287, 42093-42103
18. 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
19. McArthur, J. D., McKay, F. C., Ramachandran, V., Shyam, P., Cork, A. J., Sanderson-Smith, M. L., Cole, J. N., Ringdahl, U., Sjobring, U., Ranson, M. and Walker, M. J. (2008) Allelic variants of streptokinase from Streptococcus pyogenes display functional differences in plasminogen activation. FASEB J. 22, 3146-3153
20. Kapur, V., Kanjilal, S., Hamrick, M. R., Li, L. L., Whittam, T. S., Sawyer, S. A. and Musser, J. M. (1995) Molecular population genetic analysis of the streptokinase gene of Streptococcus pyogenes: Mosaic alleles generated by recombination. Mol. Microbiol. 16, 509-519
21. Svensson, M. D., Scaramuzzino, D. A., Sjobring, U., Olsen, A., Frank, C. and Bessen, D. E. (2000) Role for a secreted cysteine proteinase in the establishment of host tissue tropism by group A streptococci. Mol. Microbiol. 38, 242-253
22. McKay, F. C., McArthur, J. D., Sanderson-Smith, M. L., Gardam, S., Currie, B. J., Sriprakash, K. S., Fagan, P. K., Towers, R. J., Batzloff, M. R., Chhatwal, G. S. et al. (2004) Plasminogen binding by group A streptococcal isolates from a region of hyperendemicity for streptococcal skin infection and a high incidence of invasive infection. Infect. Immun. 72, 364-370
23. Sanderson-Smith, M. L., Dinkla, K., Cole, J. N., Cork, A. J., Maamary, P. G., McArthur, J. D., Chhatwal, G. S. and Walker, M. J. (2008) M protein-mediated plasminogen binding is essential for the virulence of an invasive Streptococcus pyogenes isolate. FASEB J. 22, 2715-2722
24. Sanderson-Smith, M., Batzloff, M., Sriprakash, K. S., Dowton, M., Ranson, M. and Walker, M. J. (2006) 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
25. Derbise, A., Song, Y. P., Parikh, S., Fischetti, V. A. and Pancholi, V. (2004) Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect. Immun. 72, 94-105
26. Cole, J. N., Sanderson-Smith, M. L., Cork, A. J., Henningham, A., Conlan, F., Ranson, M., McArthur, J. D. and Walker, M. J. (2006) Gene expression and tagging of streptococcal proteins. In Molecular Biology of Streptococci (Hakenbeck, R. and Chhatwal, G. S., eds), pp. 359-378, Horizon Bioscience, Norfolk
27. Rampling, M. W. and Gaffney, P. J. (1976) Sulfite precipitation method for fibrinogen measurement: Use on small samples in presence of fibrinogen degradation products. Clin. Chim. Acta 67, 43-52
28. Lahteenmaki, K., Kuusela, P. and Korhonen, T. K. (2001) Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25, 531-552
29. Plow, E. F., Herren, T., Redlitz, A., Miles, L. A. and Hoover-Plow, J. L. (1995) The cell biology of the plasminogen activation system. FASEB J. 9, 939-945
30. Gladysheva, I. P., Sazonova, I. Y., Houng, A., Hedstrom, L. and Reed, G. L. (2007) Regulation of nonproteolytic active site formation in plasminogen. Biochemistry 46, 8879-8887
31. Rijken, D. C. and Lijnen, H. R. (2009) New insights into the molecular mechanisms of the fibrinolytic system. J. Thromb. Haemost. 7, 4-13
32. Chibber, B. A., Morris, J. P. and Castellino, F. J. (1985) Effects of human fibrinogen and its cleavage products on activation of human plasminogen by streptokinase. Biochemistry 24, 3429-3434
33. Cesarman-Maus, G. and Hajjar, K. A. (2005) Molecular mechanisms of fibrinolysis. Br. J. Haematol. 129, 307-321
34. Yakovlev, S., Makogonenko, E., Kurochkina, N., Nieuwenhuizen, W., Ingham, K. and Medved, L. (2000) Conversion of fibrinogen to fibrin: Mechanism of exposure of tPA- and plasminogen-binding sites. Biochemistry 39, 15730-15741
35. Varadi, A. and Patthy, L. (1983) Location of plasminogen-binding sites in human fibrin(ogen). Biochemistry 22, 2440-2446
36. Medved, L. and Nieuwenhuizen, W. (2003) Molecular mechanisms of initiation of fibrinolysis by fibrin. Thromb. Haemost. 89, 409-419
37. Takada, Y. and Takada, A. (1989) Evidence for the formation of a trimolecular complex between streptokinase, plasminogen and fibrinogen. Thromb. Res. 53, 409-415
38. Wang, H., Lottenberg, R. and Boyle, M. D. (1995) A role for fibrinogen in the streptokinase-dependent acquisition of plasmin(ogen) by group A streptococci. J. Infect. Dis. 171, 85-92
39. Svensson, M. D., Sjobring, U. and Bessen, D. E. (1999) Selective distribution of a high-affinity plasminogen-binding site among group A streptococci associated with impetigo. Infect. Immun. 67, 3915-3920
40. Sanderson-Smith, M. L., De Oliveira, D. M. P., Ranson, M. and McArthur, J. D. (2012) Bacterial plasminogen receptors: Mediators of a multifaceted relationship. J. Biomed. Biotechnol. 2012, 14
41. 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
42. 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
43. Gerber, S., Lejon, S., Locher, M. and Schaller, J. (2010) The human α2-plasmin inhibitor: Functional characterization of the unique plasmin(ogen)-binding region. Cell. Mol. Life Sci. 67, 1505-1518
44. Wang, S., Reed, G. L. and Hedstrom, L. (1999) Deletion of Ile1 changes the mechanism of streptokinase: Evidence for the molecular sexuality hypothesis. Biochemistry 38, 5232-5240
45. Lu, P., Takai, K., Weaver, V. M. and Werb, Z. (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb. Perspect. Biol. 3, a005058
46. Bessen, D. E. and Tengra, F. K. (2010) Wiring the streptococcal network for alternative lifestyles. J. Infect. Dis. 201, 800-802
47. Reed, G. L., Houng, A. K., Liu, L., Parhami-Seren, B., Matsueda, L. H., Wang, S. and Hedstrom, L. (1999) A catalytic switch and the conversion of streptokinase to a fibrin-targeted plasminogen activator. Proc. Natl. Acad. Sci. U.S.A. 96, 8879-8883
48. Collen, D. and Lijnen, H. R. (1994) Staphylokinase, a fibrin-specific plasminogen activator with therapeutic potential? Blood 84, 680-686