A novel secreted protease from Pseudomonas aeruginosa activates NF-KB through protease-activated receptors

Cellular Microbiology

Volumn 10, Issue 7, 2008, Pages 1491-1504

  Kida, Yutaka ^a   Higashimoto, Yuichiro ^a   Inoue, Hiroyoshi ^a   Shimizu, Takashi ^a   Kuwano, Koichi ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PROTEINASE; BACTERIAL ENZYME; ELASTASE; ELASTASE A; ELASTASE B; EXOPEPTIDASE; GINGIPAIN R; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 4;

ANIMAL CELL; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; NONHUMAN; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS; SERRATIA MARCESCENS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CATTLE; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOPEPTIDASES; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-8; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PEPTIDES; PROMOTER REGIONS (GENETICS); PSEUDOMONAS AERUGINOSA; RECEPTORS, PROTEINASE-ACTIVATED; THROMBIN; TRYPSIN;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS; PSEUDOMONAS AERUGINOSA; SERRATIA MARCESCENS;

EID: 45249083027     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2008.01142.x     Document Type: Article

References (72)

1. Abraham, L.A., Chinni, C., Jenkins, A.L., Lourbakos, A., Ally, N., Pike, R.N., and Mackie, E.J. (2000) Expression of protease-activated receptor-2 by osteoblasts. Bone 26: 7-14.
2. Al-Ani, B., Saifeddine, M., Wijesuriya, S.J., and Hollenberg, M.D. (2002) Modified proteinase-activated receptor-1 and -2 derived peptides inhibit proteinase-activated receptor-2 activation by trypsin. J Pharmacol Exp Ther 300: 702-708.
3. Caballero, A., Thibodeaux, B., Marquart, M., Traidej, M., and O'Callaghan, R. (2004) Pseudomonas keratitis: Protease IV gene conservation, distribution, and production relative to virulence and other Pseudomonas proteases. Invest Ophthalmol Vis Sci 45: 522-530.
4. Caballero, A.R., Moreau, J.M., Engel, L.S., Marquart, M.E., Hill, J.M., and O'Callaghan, R.J. (2001) Pseudomonas aeruginosa protease IV enzyme assays and comparison to other Pseudomonas proteases. Anal Biochem 290: 330-337.
5. Chung, W.O., Hansen, S.R., Rao, D., and Dale, B.A. (2004) Protease-activated receptor signaling increases epithelial antimicrobial peptide expression. J Immunol 173: 5165-5170.
6. Coburn, J., and Frank, D.W. (1999) Macrophages and epithelial cells respond differently to the Pseudomonas aeruginosa type III secretion system. Infect Immun 67: 3151-3154.
7. Coin, D., Louis, D., Bernillon, J., Guinand, M., and Wallach, J. (1997) LasA, alkaline protease and elastase in clinical strains of Pseudomonas aeruginosa: Quantification by immunochemical methods. FEMS Immunol Med Microbiol 18: 175-184.
8. Compton, S.J., Renaux, B., Wijesuriya, S.J., and Hollenberg, M.D. (2001) Glycosylation and the activation of proteinase-activated receptor 2 (PAR(2)) by human mast cell tryptase. Br J Pharmacol 134: 705-718.
9. Compton, S.J., Sandhu, S., Wijesuriya, S.J., and Hollenberg, M.D. (2002) Glycosylation of human proteinase-activated receptor-2 (hPAR2): Role in cell surface expression and signalling. Biochem J 368: 495-505.
10. Dawid, S., Grass, S., and St Geme, J.W., 3rd (2001) Mapping of binding domains of nontypeable Haemophilus influenzae HMW1 and HMW2 adhesins. Infect Immun 69: 307-314.
11. Dommisch, H., Chung, W.O., Rohani, M.G., Williams, D., Rangarajan, M., Curtis, M.A., and Dale, B.A. (2007) Protease-activated receptor 2 mediates human beta-defensin 2 and CC chemokine ligand 20 mRNA expression in response to proteases secreted by Porphyromonas gingivalis. Infect Immun 75: 4326-4333.
12. Dulon, S., Leduc, D., Cottrell, G.S., D'Alayer, J., Hansen, K.K., Bunnett, N.W., et al. (2005) Pseudomonas aeruginosa elastase disables proteinase-activated receptor 2 in respiratory epithelial cells. Am J Respir Cell Mol Biol 32: 411-419.
13. Finck-Barbancon, V., Goranson, J., Zhu, L., Sawa, T., Wiener-Kronish, J.P., Fleiszig, S.M., et al. (1997) ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol Microbiol 25: 547-557.
14. Fleiszig, S.M., Wiener-Kronish, J.P., Miyazaki, H., Vallas, V., Mostov, K.E., Kanada, D., et al. (1997) Pseudomonas aeruginosa -mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect Immun 65: 579-586.
15. Frank, D.W. (1997) The exoenzyme S regulon of Pseudomonas aeruginosa. Mol Microbiol 26: 621-629.
16. Frithz-Lindsten, E.Y., Rosqvist, R., and Forsberg, A. (1997) Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol Microbiol 25: 1125-1139.
17. Gentle, I.E., Burri, L., and Lithgow, T. (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58: 1216-1225.
18. Giacaman, R.A., Nobbs, A.H., Ross, K.F., and Herzberg, M.C. (2007) Porphyromonas gingivalis selectively up-regulates the HIV-1 coreceptor CCR5 in oral keratinocytes. J Immunol 179: 2542-2550.
19. Hauser, A.R., Kang, P.J., and Engel, J.N. (1998) PepA, a secreted protein of Pseudomonas aeruginosa, is necessary for cytotoxicity and virulence. Mol Microbiol 27: 807-818.
20. Hauser, A.R., Cobb, E., Bodi, M., Mariscal, D., Valles, J., Engel, J.N., and Rello, J. (2002) Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Crit Care Med 30: 521-528.
21. Hollenberg, M.D., and Compton, S.J. (2002) International union of pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev 54: 203-217.
22. Holzhausen, M., Spolidorio, L.C., Ellen, R.P., Jobin, M.C., Steinhoff, M., Andrade-Gordon, P., and Vergnolle, N. (2006) Protease-activated receptor-2 activation: A major role in the pathogenesis of Porphyromonas gingivalis infection. Am J Pathol 168: 1189-1199.
23. Hong, Y.Q., and Ghebrehiwet, B. (1992) Effect of Pseudomonas aeruginosa elastase and alkaline protease on serum complement and isolated components C1q and C3. Clin Immunol Immunopathol 62: 133-138.
24. Horvat, R.T., and Parmely, M.J. (1988) Pseudomonas aeruginosa alkaline protease degrades human gamma interferon and inhibits its bioactivity. Infect Immun 56: 2925-2932.
25. Inomata, M., Into, T., Ishihara, Y., Nakashima, M., Noguchi, T., and Matsushita, K. (2007) Arginine-specific gingipain A from Porphyromonas gingivalis induces Weibel-Palade body exocytosis and enhanced activation of vascular endothelial cells through protease-activated receptors. Microbes Infect 9: 1500-1506.
26. Jacob-Dubuisson, F., Locht, C., and Antoine, R. (2001) Two-partner secretion in Gram-negative bacteria: A thrifty, specific pathway for large virulence proteins. Mol Microbiol 40: 306-313.
27. Jacob-Dubuisson, F., Fernandez, R., and Coutte, L. (2004) Protein secretion through autotransporter and two-partner pathways. Biochim Biophys Acta 1694: 235-257.
28. Kanke, T., Macfarlane, S.R., Seatter, M.J., Davenport, E., Paul, A., McKenzie, R.C., and Plevin, R. (2001) Proteinase-activated receptor-2-mediated activation of stress-activated protein kinases and inhibitory kappa B kinases in NCTC 2544 keratinocytes. J Biol Chem 276: 31657-31666.
29. Kharazmi, A. (1991) Mechanisms involved in the evasion of the host defence by Pseudomonas aeruginosa. Immunol Lett 30: 201-205.
30. Kida, Y., Shimizu, T., and Kuwano, K. (2006) Sodium butyrate up-regulates cathelicidin gene expression via activator protein-1 and histone acetylation at the promoter region in a human lung epithelial cell line, EBC-1. Mol Immunol 43: 1972-1981.
31. Kida, Y., Inoue, H., Shimizu, T., and Kuwano, K. (2007) Serratia marcescens serralysin induces inflammatory responses through protease-activated receptor 2. Infect Immun 75: 164-174.
32. Leidal, K.G., Munson, K.L., Johnson, M.C., and Denning, G.M. (2003) Metalloproteases from Pseudomonas aeruginosa degrade human RANTES, MCP-1, and ENA-78. J Interferon Cytokine Res 23: 307-318.
33. Locht, C., Bertin, P., Menozzi, F.D., and Renauld, G. (1993) The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol Microbiol 9: 653-660.
34. Lomholt, J.A., Poulsen, K., and Kilian, M. (2001) Epidemic population structure of Pseudomonas aeruginosa: Evidence for a clone that is pathogenic to the eye and that has a distinct combination of virulence factors. Infect Immun 69: 6284-6295.
35. Lourbakos, A., Chinni, C., Thompson, P., Potempa, J., Travis, J., Mackie, E.J., and Pike, R.N. (1998) Cleavage and activation of proteinase-activated receptor-2 on human neutrophils by gingipain-R from Porphyromonas gingivalis. FEBS Lett 435: 45-48.
36. Lourbakos, A., Potempa, J., Travis, J., D'Andrea, M.R., Andrade-Gordon, P., Santulli, R., et al. (2001a) Arginine-specific protease from Porphyromonas gingivalis activates protease-activated receptors on human oral epithelial cells and induces interleukin-6 secretion. Infect Immun 69: 5121-5130.
37. Lourbakos, A., Yuan, Y.P., Jenkins, A.L., Travis, J., Andrade-Gordon, P., Santulli, R., et al. (2001b) Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: A new trait in microbial pathogenicity. Blood 97: 3790-3797.
38. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2000) Establishment of Pseudomonas aeruginosa infection: Lessons from a versatile opportunist. Microbes Infect 2: 1051-1060.
39. Ma, Q., Zhai, Y., Schneider, J.C., Ramseier, T.M., and Saier, M.H., Jr. (2003) Protein secretion systems of Pseudomonas aeruginosa and P.fluorescens. Biochim Biophys Acta 1611: 223-233.
40. Macfarlane, S.R., Seatter, M.J., Kanke, T., Hunter, G.D., and Plevin, R. (2001) Proteinase-activated receptors. Pharmacol Rev 53: 245-282.
41. McLaughlin, J.N., Patterson, M.M., and Malik, A.B. (2007) Protease-activated receptor-3 (PAR3) regulates PAR1 signaling by receptor dimerization. Proc Natl Acad Sci USA 104: 5662-5667.
42. Maeda, H., and Morihara, K. (1995) Serralysin and related bacterial proteinases. Methods Enzymol 248: 395-413.
43. Mazar, J., and Cotter, P.A. (2007) New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol 15: 508-515.
44. Molino, M., Barnathan, E.S., Numerof, R., Clark, J., Dreyer, M., Cumashi, A., et al. (1997) Interactions of mast cell tryptase with thrombin receptors and PAR-2. J Biol Chem 272: 4043-4049.
45. Nakanishi-Matsui, M., Zheng, Y.W., Sulciner, D.J., Weiss, E.J., Ludeman, M.J., and Coughlin, S.R. (2000) PAR3 is a cofactor for PAR4 activation by thrombin. Nature 404: 609-613.
46. Oido-Mori, M., Rezzonico, R., Wang, P.L., Kowashi, Y., Dayer, J.M., Baehni, P.C., and Chizzolini, C. (2001) Porphyromonas gingivalis gingipain-R enhances interleukin-8 but decreases gamma interferon-inducible protein 10 production by human gingival fibroblasts in response to T-cell contact. Infect Immun 69: 4493-4501.
47. Ossovskaya, V.S., and Bunnett, N.W. (2004) Protease-activated receptors: contribution to physiology and disease. Physiol Rev 84: 579-621.
48. Parmely, M., Gale, A., Clabaugh, M., Horvat, R., and Zhou, W.W. (1990) Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect Immun 58: 3009-3014.
49. Pavlovskis, O.R., and Wretlind, B. (1979) Assessment of protease (elastase) as a Pseudomonas aeruginosa virulence factor in experimental mouse burn infection. Infect Immun 24: 181-187.
50. Preston, M.J., Seed, P.C., Toder, D.S., Iglewski, B.H., Ohman, D.E., Gustin, J.K., et al. (1997) Contribution of proteases and LasR to the virulence of Pseudomonas aeruginosa during corneal infections. Infect Immun 65: 3086-3090.
51. Reed, C.E., and Kita, H. (2004) The role of protease activation of inflammation in allergic respiratory diseases. J Allergy Clin Immunol 114: 997-1008; quiz 1009.
52. Romling, U., Schmidt, K.D., and Tummler, B. (1997) Large genome rearrangements discovered by the detailed analysis of 21 Pseudomonas aeruginosa clone C isolates found in environment and disease habitats. J Mol Biol 271: 386-404.
53. Roy-Burman, A., Savel, R.H., Racine, S., Swanson, B.L., Revadigar, N.S., Fujimoto, J., et al. (2001) Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis 183: 1767-1774.
54. Sambrano, G.R., Weiss, E.J., Zheng, Y.W., Huang, W., and Coughlin, S.R. (2001) Role of thrombin signalling in platelets in haemostasis and thrombosis. Nature 413: 74-78.
55. Sawa, T., Ohara, M., Kurahashi, K., Twining, S.S., Frank, D.W., Doroques, D.B., et al. (1998) In vitro cellular toxicity predicts Pseudomonas aeruginosa virulence in lung infections. Infect Immun 66: 3242-3249.
56. Schonherr, R., Tsolis, R., Focareta, T., and Braun, V. (1993) Amino acid replacements in the Serratia marcescens haemolysin ShlA define sites involved in activation and secretion. Mol Microbiol 9: 1229-1237.
57. Schweizer, H.P. (1992) Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol Microbiol 6: 1195-1204.
58. Shpacovitch, V., Feld, M., Bunnett, N.W., and Steinhoff, M. (2007) Protease-activated receptors: Novel PARtners in innate immunity. Trends Immunol 28: 535-544.
59. St Geme, J.W., 3rd, and Grass, S. (1998) Secretion of the Haemophilus influenzae HMW1 and HMW2 adhesins involves a periplasmic intermediate and requires the HMWB and HMWC proteins. Mol Microbiol 27: 617-630.
60. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
61. Suter, S. (1994) The role of bacterial proteases in the pathogenesis of cystic fibrosis. Am J Respir Crit Care Med 150: S118-S122.
62. Tancharoen, S., Sarker, K.P., Imamura, T., Biswas, K.K., Matsushita, K., Tatsuyama, S., et al. (2005) Neuropeptide release from dental pulp cells by RgpB via proteinase-activated receptor-2 signaling. J Immunol 174: 5796-5804.
63. Traidej, M., Caballero, A.R., Marquart, M.E., Thibodeaux, B.A., and O'Callaghan, R.J. (2003) Molecular analysis of Pseudomonas aeruginosa protease IV expressed in Pseudomonas putida. Invest Ophthalmol Vis Sci 44: 190-196.
64. Twining, S.S., Kirschner, S.E., Mahnke, L.A., and Frank, D.W. (1993) Effect of Pseudomonas aeruginosa elastase, alkaline protease, and exotoxin A on corneal proteinases and proteins. Invest Ophthalmol Vis Sci 34: 2699-2712.
65. Uehara, A., Muramoto, K., Takada, H., and Sugawara, S. (2003) Neutrophil serine proteinases activate human nonepithelial cells to produce inflammatory cytokines through protease-activated receptor 2. J Immunol 170: 5690-5696.
66. Uehara, A., Muramoto, K., Imamura, T., Nakayama, K., Potempa, J., Travis, J., et al. (2005) Arginine-specific gingipains from Porphyromonas gingivalis stimulate production of hepatocyte growth factor (scatter factor) through protease-activated receptors in human gingival fibroblasts in culture. J Immunol 175: 6076-6084.
67. Ward, C.K., Lumbley, S.R., Latimer, J.L., Cope, L.D., and Hansen, E.J. (1998) Haemophilus ducreyi secretes a filamentous hemagglutinin-like protein. J Bacteriol 180: 6013-6022.
68. Ward, C.K., Latimer, J.L., Nika, J., Vakevainen, M., Mock, J.R., Deng, K., et al. (2003) Mutations in the lspA1 and lspA2 genes of Haemophilus ducreyi affect the virulence of this pathogen in an animal model system. Infect Immun 71: 2478-2486.
69. Ward, C.K., Mock, J.R., and Hansen, E.J. (2004) The LspB protein is involved in the secretion of the LspA1 and LspA2 proteins by Haemophilus ducreyi. Infect Immun 72: 1874-1884.
70. Yen, M.R., Peabody, C.R., Partovi, S.M., Zhai, Y., Tseng, Y.H., and Saier, M.H. (2002) Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 1562: 6-31.
71. Yun, L.W., Decarlo, A.A., and Hunter, N. (2007) Blockade of protease-activated receptors on T cells correlates with altered proteolysis of CD27 by gingipains of Porphyromonas gingivalis. Clin Exp Immunol 150: 217-229.
72. Zhu, H., Conibear, T.C., Bandara, R., Aliwarga, Y., Stapleton, F., and Willcox, M.D. (2006) Type III secretion system-associated toxins, proteases, serotypes, and antibiotic resistance of Pseudomonas aeruginosa isolates associated with keratitis. Curr Eye Res 31: 297-306.