Pseudomonas aeruginosa elastase cleaves a C-terminal peptide from human thrombin that inhibits host inflammatory responses

Nature Communications

Volumn 7, Issue , 2016, Pages

  Van Der Plas, Mariena J A ^a   Bhongir, Ravi K V ^a   Kjellström, Sven ^b   Siller, Helena ^a   Kasetty, Gopinath ^a   Mörgelin, Matthias ^a   Schmidtchen, Artur ^a,c,d  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c LUND UNIVERSITY HOSPITAL   (Sweden)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

AP 1 PROTEIN; BACTERIAL ENZYME; CARBOXY TERMINAL FYT21 PEPTIDE; ELASTASE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PEPTIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PHOSPHOLIPASE C; POLYMYXIN B; PSEUDOMONAS AERUGINOSA ELASTASE; THROMBIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TRYPSIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYTOKINE; METALLOPROTEINASE; PROTEIN BINDING; PSEUDOLYSIN, PSEUDOMONAS AERUGINOSA; TRANSCRIPTION FACTOR AP 1;

BACTERIUM; DEGRADATION; HOST-PATHOGEN INTERACTION; HUMAN ACTIVITY; IMMUNE RESPONSE; PATHOGEN; PEPTIDE; PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL SURVIVAL; CELL ACTIVATION; CELL INTERACTION; CELL MEMBRANE; CONTROLLED STUDY; DIMERIZATION; ELECTRON MICROSCOPY; ESCHERICHIA COLI; EUKARYOTIC CELL; FEMALE; FLOW CYTOMETRY; HEMOLYSIS ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LIQUID CHROMATOGRAPHY; LYMPHOCYTE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WOUND FLUID; AGONISTS; ANIMAL; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; LEUKOCYTE; METABOLISM; MICROBIAL VIABILITY; PATHOLOGY; ULTRASTRUCTURE;

PSEUDOMONAS AERUGINOSA;

ANIMALS; BACTERIAL PROTEINS; CELL MEMBRANE; CYTOKINES; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; LEUKOCYTES; LIPOPOLYSACCHARIDES; METALLOENDOPEPTIDASES; MICE; MICROBIAL VIABILITY; NF-KAPPA B; PEPTIDES; PROTEIN BINDING; THROMBIN; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP-1;

EID: 84968883567     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11567     Document Type: Article

References (41)

1. Gjodsbol, K. et al. Multiple bacterial species reside in chronic wounds: a longitudinal study. Int. Wound J. 3, 225-231 (2006).
2. Hogsberg, T., Bjarnsholt, T., Thomsen, J. S. & Kirketerp-Moller, K. Success rate of split-thickness skin grafting of chronic venous leg ulcers depends on the presence of Pseudomonas aeruginosa: a retrospective study. PLoS ONE 6, e20492 (2011).
3. Vincent, J. L. et al. Sepsis in European intensive care units: results of the SOAP study. Crit. Care Med. 34, 344-353 (2006).
4. Lyczak, J. B., Cannon, C. L. & Pier, G. B. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15, 194-222 (2002).
5. Emerson, J., Rosenfeld, M., McNamara, S., Ramsey, B. & Gibson, R. L. Pseudomonas aeruginosa and other predictors of mortality and morbidity in young children with cystic fibrosis. Pediatr. Pulmonol. 34, 91-100 (2002).
6. Le Berre, R. et al. Relative contribution of three main virulence factors in Pseudomonas aeruginosa pneumonia. Crit. Care Med. 39, 2113-2120 (2011).
7. Kaminishi, H. et al. Activation of blood clotting factors by microbial proteinases. FEMS Microbiol. Lett. 121, 327-332 (1994).
8. Wretlind, B. & Pavlovskis, O. R. Pseudomonas aeruginosa elastase and its role in pseudomonas infections. Rev. Infect. Dis. 5(Suppl 5): S998-S1004 (1983).
9. Schmidtchen, A., Holst, E., Tapper, H. & Bjorck, L. Elastase-producing Pseudomonas aeruginosa degrade plasma proteins and extracellular products of human skin and fibroblasts, and inhibit fibroblast growth. Microb. Pathog. 34, 47-55 (2003).
10. Parmely, M., Gale, A., Clabaugh, M., Horvat, R. & Zhou, W. W. Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect. Immun. 58, 3009-3014 (1990).
11. Matsumoto, K. Role of bacterial proteases in pseudomonal and serratial keratitis. Biol. Chem. 385, 1007-1016 (2004).
12. Papareddy, P. et al. The TFPI-2 derived peptide EDC34 improves outcome of gram-negative sepsis. PLoS Pathog. 9, e1003803 (2013).
13. Kalle, M. et al. Proteolytic activation transforms heparin cofactor II into a host defense molecule. J. Immunol. 190, 6303-6310 (2013).
14. Papareddy, P. et al. Proteolysis of human thrombin generates novel host defense peptides. PLoS Pathog. 6, e1000857 (2010).
15. Kalle, M. et al. Host defense peptides of thrombin modulate inflammation and coagulation in endotoxin-mediated shock and Pseudomonas aeruginosa sepsis. PLoS ONE 7, e51313 (2012).
16. Choi, K. Y., Chow, L. N. & Mookherjee, N. Cationic host defence peptides: multifaceted role in immune modulation and inflammation. J. Innate Immun. 4, 361-370 (2012).
17. Hilchie, A. L., Wuerth, K. & Hancock, R. E. Immune modulation by multifaceted cationic host defense (antimicrobial) peptides. Nat. Chem. Biol. 9, 761-768 (2013).
18. Pasupuleti, M., Schmidtchen, A. & Malmsten, M. Antimicrobial peptides: key components of the innate immune system. Crit. Rev. Biotechnol. 32, 143-171 (2011).
19. Hancock, R. E. & Sahl, H. G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24, 1551-1557 (2006).
20. Bowdish, D. M. et al. Impact of LL-37 on anti-infective immunity. J. Leukoc. Biol. 77, 451-459 (2005).
21. Sato, S. et al. Synergy and cross-tolerance between toll-like receptor (TLR) 2- and TLR4-mediated signaling pathways. J. Immunol. 165, 7096-7101 (2000).
22. Penc, S. F. et al. Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function. J. Biol. Chem. 273, 28116-28121 (1998).
23. Baranska-Rybak, W., Sonesson, A., Nowicki, R. & Schmidtchen, A. Glycosaminoglycans inhibit the antibacterial activity of LL-37 in biological fluids. J. Antimicrob. Chemother. 57, 260-265 (2006).
24. Kielland, A. et al. In vivo imaging of reactive oxygen and nitrogen species in inflammation using the luminescent probe L-012. Free Radic. Biol. Med. 47, 760-766 (2009).
25. Butenas, S. & Mann, K. G. Blood coagulation. Biochemistry (Mosc) 67, 3-12 (2002).
26. Bardoel, B. W. et al. Pseudomonas evades immune recognition of flagellin in both mammals and plants. PLoS Pathog. 7, e1002206 (2011).
27. Madani, F., Lindberg, S., Langel, U., Futaki, S. & Graslund, A. Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys. 2011, 414729 (2011).
28. Yeaman, M. R. & Yount, N. Y. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55, 27-55 (2003).
29. Kasetty, G. et al. Structure-activity studies and therapeutic potential of host defense peptides of human thrombin. Antimicrob. Agents Chemother. 55, 2880-2890 (2011).
30. Marples, M. The Ecology of the Human Skin (Thomas, 1965).
31. Grice, E. A. et al. A diversity profile of the human skin microbiota. Genome Res. 18, 1043-1050 (2008).
32. Grice, E. A. & Segre, J. A. The skin microbiome. Nat. Rev. Microbiol. 9, 244-253 (2011).
33. Kasetty, G. et al. The C-terminal sequence of several human serine proteases encodes host defense functions. J. Innate Immun. 3, 471-482 (2011).
34. Snitkin, E. S. & Segre, J. A. Pseudomonas aeruginosa adaptation to human hosts. Nat. Genet. 47, 2-3 (2015).
35. Adekoya, O. A. & Sylte, I. The thermolysin family (M4) of enzymes: therapeutic and biotechnological potential. Chem. Biol. Drug. Des. 73, 7-16 (2009).
36. Schmidtchen, A., Frick, I. M., Andersson, E., Tapper, H. & Bjorck, L. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 46, 157-168 (2002).
37. Schmidtchen, A. Degradation of antiproteinases, complement and fibronectin in chronic leg ulcers. Acta Derm. Venereol. 80, 179-184 (2000).
38. Toder, D. S., Gambello, M. J. & Iglewski, B. H. Pseudomonas aeruginosa LasA: a second elastase under the transcriptional control of lasR. Mol. Microbiol. 5, 2003-2010 (1991).
39. Lehrer, R. I., Rosenman, M., Harwig, S. S., Jackson, R. & Eisenhauer, P. Ultrasensitive assays for endogenous antimicrobial polypeptides. J. Immunol. Methods 137, 167-173 (1991).
40. Ulevitch, R. J. The preparation and characterization of a radioiodinated bacterial lipopolysaccharide. Immunochemistry 15, 157-164 (1978).
41. Schmidtchen, A., Frick, I. M. & Bjorck, L. Dermatan sulphate is released by proteinases of common pathogenic bacteria and inactivates antibacterial alpha-defensin. Mol. Microbiol. 39, 708-713 (2001).