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

Journal of Biological Chemistry

Volumn 287, Issue 50, 2012, Pages 42093-42103

  Zhang, Yueling ^a   Liang, Zhong ^a   Hsueh, Hsing Tse ^a   Ploplis, Victoria A ^a   Castellino, Francis J ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIRECT ACTIVATION; FUNCTIONAL RELATIONSHIP; GAS CELL; INVASIVENESS; PROTEOLYTIC ACTIVITIES;

PROTEINS;

CHEMICAL ACTIVATION;

BACTERIAL PROTEIN; FIBRINOGEN; M PROTEIN; PLASMINOGEN; PLASMINOGEN BINDING M PROTEIN; STREPTOKINASE; STREPTOKINASE 2B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BINDING AFFINITY; CELL INVASION; DROSOPHILA; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME PURIFICATION; HUMAN; INHERITANCE; INSECT CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; STREPTOCOCCUS GROUP A; TROPISM;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; CELL LINE; ENZYME ACTIVATION; HUMANS; MOLECULAR SEQUENCE DATA; PLASMINOGEN; PROTEIN BINDING; PROTEOLYSIS; SHEEP; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; STREPTOKINASE;

STREPTOCOCCUS SP. 'GROUP A';

EID: 84871325888     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.417808     Document Type: Article

References (42)

1. Carapetis, J. R., Steer, A. C., Mulholland, E. K., and Weber, M. (2005) The global burden of group A streptococcal diseases. Lancet Infect. Dis. 5, 685-694 (Pubitemid 41505357)
2. Le Hello, S., Doloy, A., Baumann, F., Roques, N., Coudene, P., Rouchon, B., Lacassin, F., and Bouvet, A. (2010) Clinical and microbial characteristics of invasive Streptococcus pyogenes disease in New Caledonia, a region in Oceania with a high incidence of acute rheumatic fever. J. Clin. Microbiol. 48, 526-530
3. Smeesters, P. R., McMillan, D. J., and Sriprakash, K. S. (2010) The streptococcal M protein: a highly versatile molecule. Trends Microbiol. 18, 275-282
4. Beall, B., Facklam, R., and Thompson, T. (1996) Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J. Clin. Microbiol. 34, 953-958 (Pubitemid 26091514)
5. Bisno, A. L., Brito, M. O., and Collins, C. M. (2003) Molecular basis of group A streptococcal virulence. Lancet Infect. Dis. 3, 191-200 (Pubitemid 36389182)
6. Mitchell, T. J. (2003) The pathogenesis of streptococcal infections: from tooth decay to meningitis. Nat. Rev. Microbiol. 1, 219-230
7. Cunningham, M. W. (2008) Pathogenesis of group A streptococcal infections and their sequelae. Adv. Exp. Med. Biol. 609, 29-42
8. Musser, J. M., and Shelburne, S. A. (2009) A decade of molecular pathogenomic analysis of group A Streptococcus. J. Clin. Invest. 119, 2455-2463
9. Cole, J. N., Barnett, T. C., Nizet, V., and Walker, M. J. (2011) Molecular insight into invasive group A streptococcal disease. Nat. Rev. Microbiol. 9, 724-736
10. Sun, H., Ringdahl, U., Homeister, J. W., Fay, W. P., Engleberg, N. C., Yang, A. Y., Rozek, L. S., Wang, X., Sjöbring, U., and Ginsburg, D. (2004) Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305, 1283-1286 (Pubitemid 39129231)
11. 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 (Pubitemid 40884465)
12. Robbins, K. C., Summaria, L., Hsieh, B., and Shah, R. J. (1967) The peptide chains of human plasmin. Mechanism of activation of human plasminogen to plasmin. J. Biol. Chem. 242, 2333-2342
13. Schick, L. A., and Castellino, F. J. (1974) Direct evidence for the generation of an active site in the plasminogen moiety of the streptokinase-human plasminogen activator complex. Biochem. Biophys. Res. Commun. 57, 47-54
14. Berge, A., and Sjöbring, U. (1993) PAM, a novel plasminogen-binding protein from Streptococcus pyogenes. J. Biol. Chem. 268, 25417-25424 (Pubitemid 23358145)
15. 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., Ranson, M., and Walker, M. J. (2004) Plasminogen binding by groupAstreptococcal isolates from a region of hyperendemicity for streptococcal skin infection and a high incidence of invasive infection. Infect. Immun. 72, 364-370 (Pubitemid 38018197)
16. 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 (Pubitemid 38020293)
17. McArthur, J. D., McKay, F. C., Ramachandran, V., Shyam, P., Cork, A. J., Sanderson-Smith, M. L., Cole, J. N., Ringdahl, U., Sjöbring, 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
18. Sjögren, J., Okumura, C. Y., Collin, M., Nizet, V., and Hollands, A. (2011) Study of the IgG endoglycosidase EndoS in group A streptococcal phagocyte resistance and virulence. BMC Microbiol. 11, 120
19. Ward, P. N., and Leigh, J. A. (2002) Characterization of PauB, a novel broad-spectrum plasminogen activator from Streptococcus uberis. J. Bacteriol. 184, 119-125 (Pubitemid 34003291)
20. Iwaki, T., and Castellino, F. J. (2008) A single plasmid transfection that offers a significant advantage associated with puromycin selection in Drosophila Schneider S2 cells expressing heterologous proteins. Cytotechnology 57, 45-49
21. Nilsen, S. L., and Castellino, F. J. (1999) Expression of human plasminogen in Drosophila Schneider S2 cells. Protein Expr. Purif. 16, 136-143 (Pubitemid 29321735)
22. McShan, W. M., Ferretti, J. J., Karasawa, T., Suvorov, A. N., Lin, S., Qin, B., Jia, H., Kenton, S., Najar, F., Wu, H., Scott, J., Roe, B. A., and Savic, D. J. (2008) Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J. Bacteriol. 190, 7773-7785
23. Ringdahl, U., Svensson, M., Wistedt, A. C., Renné, T., Kellner, R., Müller- Esterl, W., and Sjöbring, U. (1998) Molecular co-operation between protein PAM and streptokinase for plasmin acquisition by Streptococcus pyogenes. J. Biol. Chem. 273, 6424-6430 (Pubitemid 28144736)
24. Rios-Steiner, J. L., Schenone, M., Mochalkin, I., Tulinsky, A., and Castellino, F. J. (2001) 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. 308, 705-719 (Pubitemid 32568470)
25. Macheboeuf, P., Buffalo, C., Fu, C. Y., Zinkernagel, A. S., Cole, J. N., Johnson, J. E., Nizet, V., and Ghosh, P. (2011) Streptococcal M1 protein constructs a pathological host fibrinogen network. Nature 472, 64-68
26. Lauth, X., von Köckritz-Blickwede, M., McNamara, C. W., Myskowski, S., Zinkernagel, A. S., Beall, B., Ghosh, P., Gallo, R. L., and Nizet, V. (2009)M1 protein allows group A streptococcal survival in phagocyte extracellular traps through cathelicidin inhibition. J. Innate Immun. 1, 202-214
27. 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
28. Castellino, F. J., Sodetz, J. M., Brockway, W. J., and Siefring, G. E. (1976) Streptokinase. Methods Enzymol. 45, 244-257
29. 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
30. Loy, J. A., Lin, X., Schenone, M., Castellino, F. J., Zhang, X. C., and Tang, J. (2001) Domain interactions between streptokinase and human plasminogen. Biochemistry 40, 14686-14695 (Pubitemid 33111753)
31. Lin, L. F., Houng, A., and Reed, G. L. (2000) Epsilon amino caproic acid inhibits streptokinase-plasminogen activator complex formation and substrate binding through kringle-dependent mechanisms. Biochemistry 39, 4740-4745 (Pubitemid 30225338)
32. Violand, B. N., Sodetz, J. M., and Castellino, F. J. (1975) The effect of ε-amino caproic acid on the gross conformation of plasminogen and plasmin. Arch. Biochem. Biophys. 170, 300-305
33. Chibber, B. A., and Castellino, F. J. (1986) Regulation of the streptokinase-mediated activation of human plasminogen by fibrinogen and chloride ions. J. Biol. Chem. 261, 5289-5295 (Pubitemid 17204334)
34. Chibber, B. A., Radek, J. T., Morris, J. P., and Castellino, F. J. (1986) Rapid formation of an anion-sensitive active site in stoichiometric complexes of streptokinase and human [Glu1]plasminogen. Proc. Natl. Acad. Sci., U.S.A. 83, 1237-1241 (Pubitemid 16016103)
35. Svensson, M. D., Sjöbring, 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 (Pubitemid 29357010)
36. Sanderson-Smith, M. L., Walker, M. J., and Ranson, M. (2006) 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 (Pubitemid 44401802)
37. D'Costa, S. S., Wang, H., Metzger, D. W., and Boyle, M. D. (1997) GroupA streptococcal isolate 64/14 expresses surface plasmin-binding structures in addition to Plr. Res. Microbiol. 148, 559-572 (Pubitemid 27438285)
38. Pancholi, V., and Fischetti, V. A. (1998) α-Enolase, a novel strong plasmin (ogen)-binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273, 14503-14515 (Pubitemid 28319172)
39. Lottenberg, R., Broder, C. C., Boyle, M. D., Kain, S. J., Schroeder, B. L., and Curtiss, R. (1992) Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor. J. Bacteriol. 174, 5204-5210
40. 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 (Pubitemid 46239765)
41. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (Pubitemid 350162903)
42. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599 (Pubitemid 47236692)