Cysteine proteinase from Streptococcus pyogenes enables evasion of innate immunity via degradation of complement factors

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15854-15864

  Honda Ogawa, Mariko ^a   Ogawa, Taiji ^a   Terao, Yutaka ^b   Sumitomo, Tomoko ^a   Nakata, Masanobu ^a   Ikebe, Kazunori ^a   Maeda, Yoshinobu ^a   Kawabata, Shigetada ^a  

^a OSAKA UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CULTURE SUPERNATANT; CYSTEINE PROTEINASE; FLOW-CYTOMETRIC ANALYSIS; HOSTILE ENVIRONMENTS; HUMAN COMPLEMENT SYSTEMS; MEMBRANE ATTACK COMPLEXES; N-TERMINAL SEQUENCES; STREPTOCOCCUS PYOGENES;

AMINO ACIDS; FISH; SCANNING ELECTRON MICROSCOPY;

BODY FLUIDS;

COMPLEMENT COMPONENT C1S INHIBITOR; COMPLEMENT COMPONENT C9; COMPLEMENT FACTOR; CYSTEINE PROTEINASE; VIRULENCE FACTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM CULTURE; CELL MEMBRANE; COMPLEMENT DEPOSITION; COMPLEMENT SYSTEM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME STRUCTURE; HUMAN; HUMAN CELL; IMMUNE EVASION; INNATE IMMUNITY; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECRETION; SPEB GENE; STREPTOCOCCUS PYOGENES; SURVIVAL RATE; TOXIC SHOCK SYNDROME;

C1-ESTERASE INHIBITOR; COMPLEMENT SYSTEM; CYSTEINE PROTEASE; INNATE IMMUNITY; MEMBRANE ATTACK COMPLEX; PROTEASE INHIBITOR; SPEB; STREPTOCOCCUS PYOGENES;

BACTERIAL PROTEINS; COMPLEMENT C1 INHIBITOR PROTEIN; COMPLEMENT C9; COMPLEMENT MEMBRANE ATTACK COMPLEX; CYSTEINE ENDOPEPTIDASES; EXOTOXINS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; STREPTOCOCCUS PYOGENES;

STREPTOCOCCUS PYOGENES;

EID: 84878423155     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.469106     Document Type: Article

References (34)

1. Cunningham, M. W. (2000) Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13, 470-511
2. Brosnahan, A. J., and Schlievert, P. M. (2011) Gram-positive bacterial superantigen outside-in signaling causes toxic shock syndrome. FEBS J. 278, 4649-4667
3. Lappin, E., and Ferguson, A. J. (2009) Gram-positive toxic shock syndromes. Lancet Infect. Dis. 9, 281-290
4. Fronhoffs, S., Luyken, J., Steuer, K., Hansis, M., Vetter, H., and Walger, P. (2000) The effect of C1-esterase inhibitor in definite and suspected streptococcal toxic shock syndrome. Report of seven patients. Intensive Care Med. 26, 1566-1570
5. Pixley, R. A., De La Cadena, R., Page, J. D., Kaufman, N., Wyshock, E. G., Chang, A., Taylor, F. B., Jr., and Colman, R. W. (1993) The contact system contributes to hypotension but not disseminated intravascular coagulation in lethal bacteremia. In vivo use of a monoclonal anti-factor XII antibody to block contact activation in baboons. J. Clin. Invest. 91, 61-68 (Pubitemid 23037253)
6. Schapira, M., Despland, E., Scott, C. F., Boxer, L. A., and Colman, R. W. (1982) Purified human plasma kallikrein aggregates human blood neutrophils. J. Clin. Invest. 69, 1199-1202 (Pubitemid 12115685)
7. van der Graaf, F., Koedam, J. A., and Bouma, B. N. (1983) Inactivation of kallikrein in human plasma. J. Clin. Invest. 71, 149-158
8. Castelli, R., Zanichelli, A., and Cugno, M. (2013) Therapeutic options for patients with angioedema due to C1-inhibitor deficiencies: from pathophysiology to the clinic. Immunopharmacol. Immunotoxicol. 35, 181-190
9. Müller-Eberhard, H. J., and Schreiber, R. D. (1980) Molecular biology and chemistry of the alternative pathway of complement. Adv. Immunol. 29, 1-53
10. Terao, Y., Mori, Y., Yamaguchi, M., Shimizu, Y., Ooe, K., Hamada, S., and Kawabata, S. (2008) Group A streptococcal cysteine protease degrades C3 (C3b) and contributes to evasion of innate immunity. J. Biol. Chem. 283, 6253-6260
11. Tsao, N., Tsai, W. H., Lin, Y. S., Chuang, W. J., Wang, C. H., and Kuo, C. F. (2006) Streptococcal pyrogenic exotoxin B cleaves properdin and inhibits complement-mediated opsonophagocytosis. Biochem. Biophys. Res. Commun. 339, 779-784 (Pubitemid 41772881)
12. Terao, Y., Kawabata, S., Kunitomo, E., Murakami, J., Nakagawa, I., and Hamada, S. (2001) Fba, a novel fibronectin-binding protein from Streptococcus pyogenes, promotes bacterial entry into epithelial cells, and the fba gene is positively transcribed under the Mga regulator. Mol. Microbiol. 42, 75-86 (Pubitemid 34212162)
13. Okamoto, S., Kawabata, S., Terao, Y., Fujitaka, H., Okuno, Y., and Hamada, S. (2004) The Streptococcus pyogenes capsule is required for adhesion of bacteria to virus-infected alveolar epithelial cells and lethal bacterial-viral superinfection. Infect. Immun. 72, 6068-6075 (Pubitemid 39303722)
14. 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, 14215-24223
15. Kunitomo, E., Terao, Y., Okamoto, S., Rikimaru, T., Hamada, S., and Kawabata, S. (2008) Molecular and biological characterization of histidine triad protein in group A streptococci. Microbes Infect. 10, 414-423
16. Murakami, J., Kawabata, S., Terao, Y., Kikuchi, K., Totsuka, K., Tamaru, A., Katsukawa, C., Moriya, K., Nakagawa, I., Morisaki, I., and Hamada, S. (2002) Distribution of emm genotypes and superantigen genes of Streptococcus pyogenes isolated in Japan, 1994-9. Epidemiol. Infect. 128, 397-404 (Pubitemid 34716367)
17. Terao, Y., Kawabata, S., Nakata, M., Nakagawa, I., and Hamada, S. (2002) Molecular characterization of a novel fibronectin-binding protein of Streptococcus pyogenes strains isolated from toxic shock-like syndrome patients. J. Biol. Chem. 277, 47428-47435 (Pubitemid 36159259)
18. 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
19. Lancefield, R. C. (1957) Differentiation of group A streptococci with a common R antigen into three serological types, with special reference to the bactericidal test. J. Exp. Med. 106, 525-544
20. Ogawa, T., Terao, Y., Okuni, H., Ninomiya, K., Sakata, H., Ikebe, K., Maeda, Y., and Kawabata, S. (2011) Biofilm formation or internalization into epithelial cells enable Streptococcus pyogenes to evade antibiotic eradication in patients with pharyngitis. Microb. Pathog. 51, 58-68
21. Bohach, G. A., Hauser, A. R., and Schlievert, P. M. (1988) Cloning of the gene, speB, for streptococcal pyrogenic exotoxin type B in Escherichia coli. Infect. Immun. 56, 1665-1667
22. Chen, C. C., and Cleary, P. P. (1990) Complete nucleotide sequence of the streptococcal C5a peptidase gene of Streptococcus pyogenes. J. Biol. Chem. 265, 3161-3167
23. Bos, I. G., Lubbers, Y. T., Roem, D., Abrahams, J. P., Hack, C. E., and Eldering, E. (2003) The functional integrity of the serpin domain of C1-inhibitor depends on the unique N-terminal domain, as revealed by a pathological mutant. J. Biol. Chem. 278, 29463-29470 (Pubitemid 36962325)
24. Cockerill, F. R., 3rd, Thompson, R. L., Musser, J. M., Schlievert, P. M., Talbot, J., Holley, K. E., Harmsen, W. S., Ilstrup, D. M., Kohner, P. C., Kim, M. H., Frankfort, B., Manahan, J. M., Steckelberg, J. M., Roberson, F., and Wilson, W. R. (1998) Molecular, serological, and clinical features of 16 consecutive cases of invasive streptococcal disease. Clin. Infect. Dis. 26, 1448-1458 (Pubitemid 28270180)
25. Hidalgo-Grass, C., Dan-Goor, M., Maly, A., Eran, Y., Kwinn, L. A., Nizet, V., Ravins, M., Jaffe, J., Peyser, A., Moses, A. E., and Hanski, E. (2004) Effect of a bacterial pheromone peptide on host chemokine degradation in group A streptococcal necrotising soft-tissue infections. Lancet 363, 696-703 (Pubitemid 38296556)
26. Collin, M., and Olsén, A. (2001) EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J. 20, 3046-3055 (Pubitemid 32611992)
27. Yang, D., Chen, Q., Hoover, D. M., Staley, P., Tucker, K. D., Lubkowski, J., and Oppenheim, J. J. (2003) Many chemokines including CCL20/MIP-3α display antimicrobial activity. J. Leukoc. Biol. 74, 448-455 (Pubitemid 38040406)
28. Egesten, A., Olin, A. I., Linge, H. M., Yadav, M., Mörgelin, M., Karlsson, A., and Collin, M. (2009) SpeB of Streptococcus pyogenes differentially modulates antibacterial and receptor activating properties of human chemokines. PLoS One 4, e4769
29. Fiedler, T., Sugareva, V., Patenge, N., and Kreikemeyer, B. (2010) Insights into Streptococcus pyogenes pathogenesis from transcriptome studies. Future Microbiol. 5, 1675-1694
30. von Pawel-Rammingen, U., and Björck, L. (2003) IdeS and SpeB: immunoglobulin-degrading cysteine proteinases of Streptococcus pyogenes. Curr. Opin. Microbiol. 6, 50-55
31. Sim, R. B., and Tsiftsoglou, S. A. (2004) Proteases of the complement system. Biochem. Soc. Trans. 32, 21-27 (Pubitemid 38283006)
32. Sjöberg, A. P., Trouw, L. A., and Blom, A. M. (2009) Complement activation and inhibition: a delicate balance. Trends Immunol. 30, 83-90
33. Collin, M., and Olsén, A. (2001) Effect of SpeB and EndoS from Streptococcus pyogenes on human immunoglobulins. Infect. Immun. 69, 7187-7189 (Pubitemid 32995485)
34. Eriksson, A., and Norgren, M. (2003) Cleavage of antigen-bound immunoglobulin G by SpeB contributes to streptococcal persistence in opsonizing blood. Infect. Immun. 71, 211-217 (Pubitemid 36026022)