Constitutive and inflammation-dependent antimicrobial peptides produced by epithelium are differentially processed and inactivated by the commensal Finegoldia magna and the pathogen Streptococcus pyogenes

Journal of Immunology

Volumn 187, Issue 8, 2011, Pages 4300-4309

  Frick, Inga Maria ^a   Nordin, Sara L ^a   Baumgarten, Maria ^a   Mörgelin, Matthias ^a   Sørensen, Ole E ^a   Olin, Anders I ^a   Egesten, Arne ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BACTERIAL ENZYME; BACTERIAL PROTEIN; BETA DEFENSIN 2; BETA DEFENSIN 3; CXCL14 CHEMOKINE; FAF PROTEIN; LYSINE; MIDKINE; POLYPEPTIDE ANTIBIOTIC AGENT; SIC PROTEIN; SPEB ENZYME; SUFA ENZYME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM EXAMINATION; COMMENSAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME RELEASE; EPITHELIUM; ERYSIPELAS; EX VIVO STUDY; FINEGOLDIA MAGNA; GRAM POSITIVE COCCI; HOST RESISTANCE; HUMAN; HUMAN TISSUE; IMMUNOMODULATION; IN VIVO STUDY; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; SKIN BIOPSY; STREPTOCOCCUS PYOGENES; UPREGULATION;

ANTIMICROBIAL CATIONIC PEPTIDES; CELLS, CULTURED; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPITHELIUM; GRAM-POSITIVE BACTERIA; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MASS SPECTROMETRY; MICROSCOPY, ELECTRON, TRANSMISSION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STREPTOCOCCUS PYOGENES; SURFACE PLASMON RESONANCE;

EID: 80054725632     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1004179     Document Type: Article

References (49)

1. Hromas, R., H. E. Broxmeyer, C. Kim, H. Nakshatri, K. Christopherson, II, M. Azam, and Y. H. Hou. 1999. Cloning of BRAK, a novel divergent CXC chemokine preferentially expressed in normal versus malignant cells. Biochem. Biophys. Res. Commun. 255: 703-706. (Pubitemid 29294862)
2. Kurth, I., K. Willimann, P. Schaerli, T. Hunziker, I. Clark-Lewis, and B. Moser. 2001. Monocyte selectivity and tissue localization suggests a role for breast and kidney-expressed chemokine (BRAK) in macrophage development. J. Exp. Med. 194: 855-861. (Pubitemid 32983020)
3. Maerki, C., S. Meuter, M. Liebi, K. Mühlemann, M. J. Frederick, N. Yawalkar, B. Moser, and M. Wolf. 2009. Potent and broad-spectrum antimicrobial activity of CXCL14 suggests an immediate role in skin infections. J. Immunol. 182: 507-514.
4. Inazumi, T., S. Tajima, T. Nishikawa, K. Kadomatsu, H. Muramatsu, and T. Muramatsu. 1997. Expression of the retinoid-inducible polypeptide, midkine, in human epidermal keratinocytes. Arch. Dermatol. Res. 289: 471-475. (Pubitemid 27371053)
5. Svensson, S. L., M. Pasupuleti, B. Walse, M. Malmsten, M. Mörgelin, C. Sjögren, A. I. Olin, M. Collin, A. Schmidtchen, R. Palmer, and A. Egesten. 2010. Midkine and pleiotrophin have bactericidal properties: preserved antibacterial activity in a family of heparin-binding growth factors during evolution. J. Biol. Chem. 285: 16105-16115.
6. Harder, J., J. Bartels, E. Christophers, and J. M. Schröder. 1997. A peptide antibiotic from human skin. Nature 387: 861.
7. Harder, J., J. Bartels, E. Christophers, and J. M. Schröder. 2001. Isolation and characterization of human beta -defensin-3, a novel human inducible peptide antibiotic. J. Biol. Chem. 276: 5707-5713.
8. Higaki, S., and M. Morohashi. 2003. Characteristics of anaerobes from skin specimens. Drugs Exp. Clin. Res. 29: 153-155. (Pubitemid 38282343)
9. Dowd, S. E., Y. Sun, P. R. Secor, D. D. Rhoads, B. M. Wolcott, G. A. James, and R. D. Wolcott. 2008. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol. 8: 43.
10. Dowd, S. E., R. D. Wolcott, Y. Sun, T. McKeehan, E. Smith, and D. Rhoads. 2008. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS ONE 3: e3326.
11. Gontcharova, V., E. Youn, Y. Sun, R. D. Wolcott, and S. E. Dowd. 2010. A comparison of bacterial composition in diabetic ulcers and contralateral intact skin. The Open Microbiol. J. 4: 8-19.
12. Frick, I.-M., C. Karlsson, M. Mö rgelin, A. I. Olin, R. Janjusevic, C. Hammarström, E. Holst, M. de Château, and L. Björck. 2008. Identification of a novel protein promoting the colonization and survival of Finegoldia magna, a bacterial commensal and opportunistic pathogen. Mol. Microbiol. 70: 695-708.
13. Karlsson, C., M.-L. Andersson, M. Collin, A. Schmidtchen, L. Bjö rck, and I.-M. Frick. 2007. SufA - a novel subtilisin-like serine proteinase of Finegoldia magna. Microbiology 153: 4208-4218.
14. Karlsson, C., M. Eliasson, A. I. Olin, M. Mörgelin, A. Karlsson, M. Malmsten, A. Egesten, and I. M. Frick. 2009. SufA of the opportunistic pathogen finegoldia magna modulates actions of the antibacterial chemokine MIG/CXCL9, promoting bacterial survival during epithelial inflammation. J. Biol. Chem. 284: 29499-29508.
15. Cunningham, M. W. 2000. Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13: 470-511. (Pubitemid 30452618)
16. Potempa, J., and R. N. Pike. 2009. Corruption of innate immunity by bacterial proteases. J. Innate Immun. 1: 70-87.
17. Egesten, A., M. Eliasson, H. M. Johansson, A. I. Olin, M. Mörgelin, A. Mueller, J. E. Pease, I.-M. Frick, and L. Björck. 2007. The CXC chemokine MIG/CXCL9 is important in innate immunity against Streptococcus pyogenes. J. Infect. Dis. 195: 684-693.
18. Fernie-King, B. A., D. J. Seilly, A. Davies, and P. J. Lachmann. 2002. Streptococcal inhibitor of complement inhibits two additional components of the mucosal innate immune system: secretory leukocyte proteinase inhibitor and lysozyme. Infect. Immun. 70: 4908-4916.
19. Fernie-King, B. A., D. J. Seilly, and P. J. Lachmann. 2004. The interaction of streptococcal inhibitor of complement (SIC) and its proteolytic fragments with the human beta defensins. Immunology 111: 444-452. (Pubitemid 38482497)
20. Frick, I. M., P. Åkesson, M. Rasmussen, A. Schmidtchen, and L. Björck. 2003. SIC, a secreted protein of Streptococcus pyogenes that inactivates antibacterial peptides. J. Biol. Chem. 278: 16561-16566.
21. Åkesson, P., A. G. Sjöholm, and L. Björck. 1996. Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J. Biol. Chem. 271: 1081-1088. (Pubitemid 26034969)
22. Shelburne, S. A., III, C. Granville, M. Tokuyama, I. Sitkiewicz, P. Patel, and J. M. Musser. 2005. Growth characteristics of and virulence factor production by group A Streptococcus during cultivation in human saliva. Infect. Immun. 73: 4723-4731. (Pubitemid 41105628)
23. Frick, I.-M., O. Shannon, P. Åkesson, M. Mörgelin, M. Collin, A. Schmidtchen, and L. Björck. 2011. Antibacterial activity of the contact and complement systems is blocked by SIC, a protein secreted by Streptococcus pyogenes. J. Biol. Chem. 286: 1331-1340.
24. Lukomski, S., C. A. Montgomery, J. Rurangirwa, R. S. Geske, J. P. Barrish, G. J. Adams, and J. M. Musser. 1999. Extracellular cysteine protease produced by Streptococcus pyogenes participates in the pathogenesis of invasive skin infection and dissemination in mice. Infect. Immun. 67: 1779-1788. (Pubitemid 29144397)
25. Pence, M. A., S. H. M. Rooijakkers, A. L. Cogen, J. N. Cole, A. Hollands, R. L. Gallo, and V. Nizet. 2010. Streptococcal inhibitor of complement promotes innate immune resistance phenotypes of invasive M1T1 group A Streptococcus. J. Innate Immun. 2: 587-595.
26. Skattum, L., P. Åkesson, L. Truedsson, and A. G. Sjöholm. 2006. Antibodies against four proteins from a Streptococcus pyogenes serotype M1 strain and levels of circulating mannan-binding lectin in acute poststreptococcal glomerulonephritis. Int. Arch. Allergy Immunol. 140: 9-19.
27. Sørensen, O. E., D. R. Thapa, A. Rosenthal, L. Liu, A. A. Roberts, and T. Ganz. 2005. Differential regulation of beta-defensin expression in human skin by microbial stimuli. J. Immunol. 174: 4870-4879.
28. Berge, A., and L. Björck. 1995. Streptococcal cysteine proteinase releases biologically active fragments of streptococcal surface proteins. J. Biol. Chem. 270: 9862-9867.
29. Linder, A., L. Johansson, P. Thulin, E. Hertzén, M. Mö rgelin, B. Christensson, L. Björck, A. Norrby-Teglund, and P. Åkesson. 2010. Erysipelas caused by group A streptococcus activates the contact system and induces the release of heparinbinding protein. J. Invest. Dermatol. 130: 1365-1372.
30. Roupé, K. M., M. Nybo, U. Sjöbring, P. Alberius, A. Schmidtchen, and O. E. Sørensen. 2010. Injury is a major inducer of epidermal innate immune responses during wound healing. J. Invest. Dermatol. 130: 1167-1177.
31. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368-379. (Pubitemid 18004907)
32. Bengtson, S. H., C. Sandén, M. Mörgelin, P. F. Marx, A. I. Olin, L. M. Leeb- Lundberg, J. C. Meijers, and H. Herwald. 2008. Activation of TAFI on the surface of Streptococcus pyogenes evokes inflammatory reactions by modulating the kallikrein/kinin system. J. Innate Immun. 1: 18-28.
33. Röcken, C., and A. Roessner. 1999. An evaluation of antigen retrieval procedures for immunoelectron microscopic classification of amyloid deposits. J. Histochem. Cytochem. 47: 1385-1394.
34. Stirling, J. W., and P. S. Graff. 1995. Antigen unmasking for immunoelectron microscopy: labeling is improved by treating with sodium ethoxide or sodium metaperiodate, then heating on retrieval medium. J. Histochem. Cytochem. 43: 115-123.
35. Yano, S., K. Kashima, T. Daa, S. Urabe, K. Tsuji, I. Nakayama, and S. Yokoyama. 2003. An antigen retrieval method using an alkaline solution allows immunoelectron microscopic identification of secretory granules in conventional epoxy-embedded tissue sections. J. Histochem. Cytochem. 51: 199-204. (Pubitemid 36160046)
36. Kellenberger, E., M. Dürrenberger, W. Villiger, E. Carlemalm, and M. Wurtz. 1987. The efficiency of immunolabel on Lowicryl sections compared to theoretical predictions. J. Histochem. Cytochem. 35: 959-969. (Pubitemid 17128190)
37. Schmidtchen, A., I.-M. Frick, E. Andersson, H. Tapper, and L. Björck. 2002. Proteinases of common pathogenic bacteria degrade and inactivate the antibacterial peptide LL-37. Mol. Microbiol. 46: 157-168. (Pubitemid 35238020)
38. Egesten, A., A. I. Olin, H. M. Linge, M. Yadav, M. Mörgelin, A. Karlsson, and M. Collin. 2009. SpeB of Streptococcus pyogenes differentially modulates antibacterial and receptor activating properties of human chemokines. PLoS ONE 4: e4769.
39. Fernie-King, B. A., D. J. Seilly, M. J. Binks, K. S. Sriprakash, and P. J. Lachmann. 2007. Streptococcal DRS (distantly related to SIC) and SIC inhibit antimicrobial peptides, components of mucosal innate immunity: a comparison of their activities. Microbes Infect. 9: 300-307. (Pubitemid 46341934)
40. Meuter, S., and B. Moser. 2008. Constitutive expression of CXCL14 in healthy human and murine epithelial tissues. Cytokine 44: 248-255.
41. Ozawa, S., Y. Kato, R. Komori, Y. Maehata, E. Kubota, and R. Hata. 2006. BRAK/CXCL14 expression suppresses tumor growth in vivo in human oral carcinoma cells. Biochem. Biophys. Res. Commun. 348: 406-412. (Pubitemid 44218985)
42. Krzystek-Korpacka, M., K. Neubauer, and M. Matusiewicz. 2010. Circulating midkine in Crohn's disease: clinical implications. Inflamm. Bowel Dis. 16: 208-215.
43. Yoshida, Y., S. Ikematsu, H. Muramatsu, H. Sakakima, N. Mizuma, F. Matsuda, K. Sonoda, F. Umehara, R. Ohkubo, E. Matsuura, et al. 2008. Expression of the heparin-binding growth factor midkine in the cerebrospinal fluid of patients with neurological disorders. Intern. Med. 47: 83-89. (Pubitemid 351377308)
44. Coll, R. C., and L. A. O'Neill. 2010. New insights into the regulation of signalling by toll-like receptors and nod-like receptors. J. Innate Immun. 2: 406-421.
45. You, Z., Y. Dong, X. Kong, L. A. Beckett, R. Gandour-Edwards, and J. Melamed. 2008. Midkine is a NF-kappaB-inducible gene that supports prostate cancer cell survival. BMC Med. Genomics 1: 6.
46. Takada, T., K. Toriyama, H. Muramatsu, X. J. Song, S. Torii, and T. Muramatsu. 1997. Midkine, a retinoic acid-inducible heparin-binding cytokine in inflammatory responses: chemotactic activity to neutrophils and association with inflammatory synovitis. J. Biochem. 122: 453-458. (Pubitemid 27395316)
47. Schröder, J. M., and J. Harder. 2006. Antimicrobial skin peptides and proteins. Cell. Mol. Life Sci. 63: 469-486.
48. Siezen, R. J., and J. A. Leunissen. 1997. Subtilases: the superfamily of subtilisinlike serine proteases. Protein Sci. 6: 501-523. (Pubitemid 27120048)
49. Nizet, V. 2007. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J. Allergy Clin. Immunol. 120: 13-22. (Pubitemid 46990514)