A bacterial pathogen co-opts host plasmin to resist killing by cathelicidin antimicrobial peptides

Journal of Biological Chemistry

Volumn 287, Issue 49, 2012, Pages 40891-40897

  Hollands, Andrew ^a   Gonzalez, David ^a   Leire, Emma ^a   Donald, Cortny ^d   Gallo, Richard L ^a,c   Sanderson Smith, Martina ^d   Dorrestein, Pieter C ^b   Nizet, Victor ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GASES; MAMMALS; MASS SPECTROMETRY; MICROORGANISMS; PEPTIDES;

ANTIMICROBIAL PEPTIDE; BACTERIAL PATHOGENS; BACTERIAL SURFACES; CLEAVAGE PRODUCTS; EVASION STRATEGY; MATRIX-ASSISTED LASER DESORPTION IONIZATION MASS SPECTROMETRY; PLASMINOGEN ACTIVATORS; PROTEASE ACTIVITIES;

IONIZATION OF GASES;

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; PLASMIN; PROTEINASE; STREPTOKINASE;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL IMMUNITY; BACTERIAL VIRULENCE; ENZYME ACTIVITY; HOST RESISTANCE; IMMUNE EVASION; INNATE IMMUNITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; STREPTOCOCCUS AGALACTIAE;

EID: 84870342677     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.404582     Document Type: Article

References (28)

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. Sumby, P., Whitney, A. R., Graviss, E. A., DeLeo, F. R., and Musser, J. M. (2006) Genome-wide analysis of group A streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog. 2, e5
3. Walker, M. J., Hollands, A., Sanderson-Smith, M. L., Cole, J. N., Kirk, J. K., Henningham, A., McArthur, J. D., Dinkla, K., Aziz, R. K., Kansal, R. G., Simpson, A. J., Buchanan, J. T., Chhatwal, G. S., Kotb, M., and Nizet, V. (2007) DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat. Med. 13, 981-985 (Pubitemid 47222039)
4. 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
5. Cole, J. N., McArthur, J. D., McKay, F. C., Sanderson-Smith, M. L., Cork, A. J., Ranson, M., Rohde, M., Itzek, A., Sun, H., Ginsburg, D., Kotb, M., Nizet, V., Chhatwal, G. S., and Walker, M. J. (2006) Trigger for group A streptococcal M1T1 invasive disease. FASEB J. 20, 1745-1747
6. Ponting, C. P., Marshall, J. M., and Cederholm-Williams, S. A. (1992) Plasminogen: a structural review. Blood Coagul. Fibrinolysis 3, 605-614
7. 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 (Pubitemid 30100366)
8. 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)
9. 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 (Pubitemid 24043631)
10. 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
11. Dürr, U. H., Sudheendra, U. S., and Ramamoorthy, A. (2006) LL-37, the only human member of the cathelicidin family of antimicrobial peptides. Biochim. Biophys. Acta 1758, 1408-1425 (Pubitemid 44436081)
12. Zanetti, M. (2004) Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 75, 39-48
13. Nizet, V., Ohtake, T., Lauth, X., Trowbridge, J., Rudisill, J., Dorschner, R. A., Pestonjamasp, V., Piraino, J., Huttner, K., and Gallo, R. L. (2001) Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 414, 454-457 (Pubitemid 34173727)
14. Bergman, P., Johansson, L., Wan, H., Jones, A., Gallo, R. L., Gudmundsson, G. H., Hökfelt, T., Jonsson, A. B., and Agerberth, B. (2006) Induction of the antimicrobial peptide CRAMP in the blood-brain barrier and meninges after meningococcal infection. Infect. Immun. 74, 6982-6991 (Pubitemid 44913173)
15. Chromek, M., Slamová, Z., Bergman, P., Kovács, L., Podracká, L., Ehrén, I., Hökfelt, T., Gudmundsson, G. H., Gallo, R. L., Agerberth, B., and Brauner, A. (2006) The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat. Med. 12, 636-641 (Pubitemid 43865231)
16. Buchanan, J. T., Simpson, A. J., Aziz, R. K., Liu, G. Y., Kristian, S. A., Kotb, M., Feramisco, J., and Nizet, V. (2006) DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr. Biol. 16, 396-400 (Pubitemid 43259350)
17. Cole, J. N., Pence, M. A., von Köckritz-Blickwede, M., Hollands, A., Gallo, R. L., Walker, M. J., and Nizet, V. (2010) M protein and hyaluronic acid capsule are essential for in vivo selection of covRS mutations characteristic of invasive serotype M1T1 group A Streptococcus. MBio 1, e00191-10
18. Hollands, A., Aziz, R. K., Kansal, R., Kotb, M., Nizet, V., and Walker, M. J. (2008) A naturally occurring mutation in ropB suppresses SpeB expression and reduces M1T1 group A streptococcal systemic virulence. PloS One 3, e4102
19. Yamasaki, K., Schauber, J., Coda, A., Lin, H., Dorschner, R. A., Schechter, N. M., Bonnart, C., Descargues, P., Hovnanian, A., and Gallo, R. L. (2006) Kallikrein-mediated proteolysis regulates the antimicrobial effects of cathelicidins in skin. FASEB J. 20, 2068-2080 (Pubitemid 44953906)
20. Dorschner, R. A., Pestonjamasp, V. K., Tamakuwala, S., Ohtake, T., Rudisill, J., Nizet, V., Agerberth, B., Gudmundsson, G. H., and Gallo, R. L. (2001) Cutaneous injury induces the release of cathelicidin anti-microbial peptides active against group A Streptococcus. J. Invest. Dermatol. 117, 91-97 (Pubitemid 32652444)
21. Lee, P. H., Ohtake, T., Zaiou, M., Murakami, M., Rudisill, J. A., Lin, K. H., and Gallo, R. L. (2005) Expression of an additional cathelicidin antimicrobial peptide protects against bacterial skin infection. Proc. Natl. Acad. Sci. U.S.A. 102, 3750-3755 (Pubitemid 40354683)
22. 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
23. Pence, M. A., Rooijakkers, S. H., Cogen, A. L., Cole, J. N., Hollands, A., Gallo, R. L., and Nizet, V. (2010) Streptococcal inhibitor of complement promotes innate immune resistance phenotypes of invasive M1T1 group A Streptococcus. J. Innate Immun. 2, 587-595
24. Collen, D. (1999) The plasminogen (fibrinolytic) system. Thromb. Haemost. 82, 259-270
25. Gryllos, I., Tran-Winkler, H. J., Cheng, M. F., Chung, H., Bolcome, R., 3rd, Lu, W., Lehrer, R. I., and Wessels, M. R. (2008) Induction of group A Streptococcus virulence by a human antimicrobial peptide. Proc. Natl. Acad. Sci. U.S.A. 105, 16755-16760
26. Jin, T., Bokarewa, M., Foster, T., Mitchell, J., Higgins, J., and Tarkowski, A. (2004) Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J. Immunol. 172, 1169-1176 (Pubitemid 38113778)
27. Braff, M. H., Jones, A. L., Skerrett, S. J., and Rubens, C. E. (2007) Staphylococcus aureus exploits cathelicidin antimicrobial peptides produced during early pneumonia to promote staphylokinase-dependent fibrinolysis. J. Infect Dis. 195, 1365-1372 (Pubitemid 46649625)
28. Sun, H., Xu, Y., Sitkiewicz, I., Ma, Y., Wang, X., Yestrepsky, B. D., Huang, Y., Lapadatescu, M. C., Larsen, M. J., Larsen, S. D., Musser, J. M., and Ginsburg, D. (2012) Inhibitor of streptokinase gene expression improves survival after group A Streptococcus infection in mice. Proc. Natl. Acad. Sci. U.S.A. 109, 3469-3474