Proteolysis of human monocyte CD14 by cysteine proteinases (gingipains) from Porphyromonas gingivalis leading to lipopolysaccharide hyporesponsiveness

Journal of Immunology

Volumn 165, Issue 1, 2000, Pages 411-418

  Sugawara, Shunji ^a   Nemoto, Eiji ^a   Tada, Hiroyuki ^a   Miyake, Kensuke ^b   Imamura, Takahisa ^c   Takada, Haruhiko ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b SAGA UNIVERSITY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CYSTEINE PROTEINASE; GINGIPAIN R; LIPOPOLYSACCHARIDE;

ANTIGEN BINDING; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MONOCYTE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN DEGRADATION;

PORPHYROMONAS GINGIVALIS;

EID: 0034235313     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.165.1.411     Document Type: Article

References (53)

1. Holt, S. C., and T. E. Bramanti. 1991. Factors in virulence expression and their role in periodontal disease pathogenesis. Crit. Rev. Oral Biol. Med. 2:177.
2. Shah, H. N., D. Mayrand, and R. Genco, eds. 1993. Biology of the Species Porphyromonas gingivalis. CRC Press, Boca Raton.
3. Cutler, C. W., J. R. Kalmar, and C. A. Genco. 1995. Pathogenic strategies of oral anaerobe Porphyromonas gingivalis. Trends Microbiol 3:45.
4. Potempa, J., R. Pike, and J. Travis. 1995. The multiple forms of trypsin-like activity present in various strains of Porphyromonas gingivalis are due to the presence of either Arg-gingipain or Lys-gingipain. Infect. Immun. 63:1176.
5. Chen, Z., J. Potempa, A. Polanowski, M. Wikstrom, and J. Travis. 1992. Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis. J. Biol. Chem. 267:18896.
6. Pike, R., W. McGraw, J. Potempa, and J. Travis. 1994. Lysine- and arginine-specific proteinases from Porphyromonas gingivalis: isolation, characterization, and evidence for the existence of complexes with hemagglutinins. J. Biol. Chem. 269:406.
7. Imamura, T., R. N. Pike, J. Potempa, and J. Travis. 1994. Pathogenesis of periodontitis: a major arginine-specifie cysteine proteinase from Porphyromonas gingivalis induces vascular permeability enhancement through activation of the kallikrein/kinin pathway. J. Clin. Invest. 94:361.
8. Imamura, T., J. Potempa, R. N. Pike, and J. Travis. 1995. Dependence of vascular permeability enhancement on cysteine proteinases in vesicles of Porphyromonas gingivalis. Infect. Immun. 63:1999.
9. Scott, C. F., E. J. Whitaker, B. J. Hammond, and R. C. Colman. 1993. Purification and characterization of a potent 70-kDa thiol lysyl-proteinase (Lys-gingipain) from Porphyromonas gingivalis that cleaves kininogens and fibrinogen. J. Biol. Chem. 268:7935.
10. Imamura, T., J. Potempa, R. N. Pike, J. N. Moore, M. H. Barton, and J. Travis. 1995. Effect of free and vesicle-bound cysteine proteinases of Porphyromonas gingivalis on plasma clot formation: implications for bleeding tendency at periodontitis sites. Infect. Immun. 63:4877.
11. Imamura, T., J. Potempa, S. Tanase, and J. Travis. 1997. Activation of blood coagulation factor X by arginine-specific cysteine proteinases (gingipain-Rs) from Porphyromonas gingivalis. J. Biol. Chem. 272:16062.
12. Wingrove, J. A., R. G. DiScipio, Z. Chen, J. Potempa, J. Travis, and T. E. Hugh. 1992. Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J. Biol. Chem. 267: 18902.
13. Jagels, M. A., J. Travis, J. Potempa, R. Pike, and T. E. Hugh. 1996. Proteolytic inactivation of the leukocyte C5a receptor by proteinases derived from Porphyromonas gingivalis. Infect. Immun. 64:1984.
14. Kadowaki, T., K. Nakayama, F. Yoshimura, K. Okamoto, N. Abe, and K. Yamamoto. 1998. Arg-gingipain acts as a major processing enzyme for various cell surface proteins in Porphyromonas gingivalis. J. Biol. Chem. 273:29072.
15. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431.
16. Ulevitch, R. J., and P. S. Tobias. 1995. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol. 13:437.
17. Frey, E. A., D. S. Miller, T. G. Jahr, A. Sundan, V. Bazil, T. Espevik, B. B. Finlay, and S. D. Wright. 1992. Soluble CD14 participates in the response of cells to lipopolysaccharide. J. Exp. Med. 176:1665.
18. Pugin, J., C.-C. Schürer-Maly, D. Letureq, A. Moriarty, R. J. Ulevitch, and P. S. Tobias. 1993. Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc. Natl. Acad. Sci. USA 90:2744.
19. Sugawara, S., A. Sugiyama, E. Nemoto, H. Rikiishi, and H. Takada. 1998. Heterogeneous expression and release of CD14 by human gingival fibroblasts: characterization and CD14-mediated interleukin-8 secretion in response to lipopolysaccharide. Infect. Immun. 66:3043.
20. Sugawara, S., R. Arakaki, H. Rikiishi, and H. Takada. 1999. Lipoteichoic acid acts as an antagonist and an agonist of lipopolysaccharide on human gingival fibroblasts and monocytes in a CD14-dependent manner. Infect. Immun. 67:1623.
21. Pugin, J., D. Heumann, A. Tomasz, V. V. Kravchenko, Y. Akamatsu, M. Nishijima, M. P. Glauser, P. S. Tobias, and R. J. Ulevitch. 1994. CD14 is a pattern recognition receptor. Immunity 1:509.
22. Wright, S. D. 1995. CD14 and innate recognition of bacteria. J. Immunol. 155:6.
23. Haziot, A., S. Chen, E. Ferrero, M. G. Low, R. Silber, and S. M. Goyert. 1988. The monocyte differentiation antigen. CD14, is anchored to the cell membrane by a phosphatidylinositol linkage. J. Immunol. 141:547.
24. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway Jr. 1997. A human homologue of the Drosophilia Toll protein signals activation of adaptive immunity. Nature 388:394.
25. Yang, R.-B., M. R. Mark, A. Gray, A. Huang, M. H. Xie, M. Zhang, A. Goddard, W. I. Wood, A. L. Gurney, and P. J. Godowski. 1998. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395:284.
26. Kirschning, C. J., H. Wesche, T. M. Ayres, and M. Rothe. 1998. Human Toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J. Exp. Med. 188:2091.
27. Poltorak, A., X. He, I. Smirnova, M.-Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085.
28. Qureshi, S. T., L. Larivière, G. Leveque, S. Clermont, K. J. Moore, P. Gros, and D. Malo. 1999. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J. Exp. Med. 189:615.
29. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162:3749.
30. Shimazu, R., S. Akashi, H. Ogata, Y. Nagai, K. Fukudome, K. Miyake, and M. Kimoto. 1999. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 189:1777.
31. Galanos, C., O. Lüderitz, and O. Westphal. 1979. Preparation and properties of a standardized lipopolysaccharide from Salmonella abortus equi (Novo-Pyexal). Zentralbl. Bakteriol. Mikrobiol. Hyg. Abt. 1 Orig. Reiche A 243:226.
32. Potempa, J., R. Pike, and J. Travis. 1997. Titration and mapping of the active site of cysteine proteinases from Porphyromonas gingivalis (gingipains) using peptidyl chloromethanes. Biol. Chem. 378:223.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680.
34. Le-Barillec, K., M. Si-Tahar, V. Balloy, and M. Chignard. 1999. Proteolysis of monocyte CD14 by human leukocyte elastase inhibits lipopolysaccharide-mediated cell activation. J. Clin. Invest. 103:1039.
35. Bazil, V., and J. L. Strominger. 1991. Shedding as a mechanism of down-regulation of CD14 on stimulated human monocytes. J. Immunol. 147:1567.
36. Beatty, K., J. Bieth, and J. Travis. 1980. Kinetics of association of serine proteinases with native and oxidized α-1-proteinase inhibitor and α-1-antichymotrypsin. J. Biol. Chem. 255:3931.
37. 2-macroglobulin in the control of cysteine proteinases (gingipains) from Porphyromonas gingivalis. J. Periodont. Res. 32:61.
38. Mikolajczyk-Pawlinska, J., J. Travis, and J. Potempa. 1998. Modulation of interleukin-8 activity by gingipains from Porphyromonas gingivalis: implications for pathogenicity of periodontal disease. FEBS Lett. 440:282.
39. Viriyakosol, S., and T. N. Kirkland. 1995. A region of human CD14 required for lipopolysaccharide binding. J. Biol. Chem. 270:361.
40. Juan, T. S.-C., E. Hailman, M. J. Kelley, L. A. Busse, E. Davy, C. J. Empig, L. O. Narhi, S. D. Wright, and H. S. Lichenstein. 1995. Identification of a lipopolysaccharide binding domain in CD14 between amino acids 57 and 64. J. Biol. Chem. 270:5219.
41. Pike, R. N., J. Potempa, W. McGraw, T. H. Coetzer, and J. Travis. 1996. Characterization of the binding activities of proteinase-adhesin complexes from Porphyromonas gingivalis. J. Bacteriol. 178:2876.
42. Davies, A., D. L. Simmons, G. Hale, R. A. Harrison, H. Tighe, P. J. Lachmann, and H. Waldmann. 1989. CD59, an LY6-like protein expressed in human lymphoid cells, regulates the action of the complement membrane attack complex on homologous cells. J. Exp. Med. 170:637.
43. Okada, H., Y. Nagami, K. Takahashi, N. Okada, T. Hideshima, H. Takizawa, and J. Kondo. 1989. 20 kDa homologous restriction factor of complement resembles T-cell activating protein. Biochem. Biophys. Res. Commun. 162:1553.
44. Chow, J. C., D. W. Young, D. T. Golenbock, W. J. Christ, and F. Gusovsky. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274:10689.
45. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gramnegative and Gram-positive bacterial cell wall components. Immunity 11:443.
46. Calkins, C. C., K. Platt, J. Potempa, and J. Travis. 1998. Inactivation of tumor necrosis factor-α by proteinases (gingipains) from the periodontal pathogen, Porphyromonas gingivalis: implications of immune evasion. J. Biol. Chem. 273:6611.
47. Grunwald, U., X. Fan, R. S. Jack, G. Workalemahu, A. Kallies, F. Stelter, and C. Schütt. 1996. Monocytes can phagocytose Gram-negative bacteria by a CD14-dependent mechanism. J. Immunol. 157:4119.
48. Schiff, D. E., L. Kline, K. Soldau, J. D. Lee, J. Pugin, P. S. Tobias, and R. J. Ulevitch. 1997. Phagocytosis of Gram-negative bacteria by a unique CD14-dependent mechanism. J. Leukocyte Biol. 62:786.
49. Griffin, J. D., J. Ritz, L. M. Nadler, and S. F. Schlossman. 1981. Expression of myeloid differentiation antigens on normal and malignant myeloid cells. J. Clin. Invest. 68:932.
50. Todd, R. F., L. M. Nadler, and S. F. Schlossman. 1981. Antigens on human monocytes identified by monoclonal antibodies. J. Immunol. 126:1435.
51. Haziot, A., B.-Z. Tsuberi, and S. M. Goyert. 1993. Neutrophil CD14: biochemical properties and role in the secretion of tumor necrosis factor-α in response to lipopolysaccharide. J Immunol. 150:5556.
52. 1-proteinase inhibitor. J. Biol. Chem. 274:12245.
53. Genco, C. A., J. Polempa, J. Mikolajczyk-Pawlinska, and J. Travis. 1999. Role of gingipains R in the pathogenesis of Porphyromonas gingivalis-mediated periodontal disease. Clin. Infect. Dis 28:456.