Periodontal pathogens affect the level of protease inhibitors in gingival crevicular fluid

Molecular Oral Microbiology

Volumn 27, Issue 1, 2012, Pages 45-56

  Laugisch, O ^a   Schacht, M ^b   Guentsch, A ^b   Kantyka, T ^c   Sroka, A ^c   Stennicke, H R ^d   Pfister, W ^b   Sculean, A ^a   Potempa, J ^c,e   Eick, S ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d NOVO NORDISK A S   (Denmark)

^e UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Elafin; Neutrophil elastase; Periodontal disease; Porphyromonas gingivalis; Proteinase 3; Secretory leukocyte protease inhibitor

Indexed keywords

ELAFIN; ELASTASE; MYELOBLASTIN; PROTEINASE INHIBITOR; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR;

ADULT; AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ARTICLE; BACTERIAL LOAD; BACTERIUM; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; FEMALE; GINGIVITIS; HUMAN; HUMAN TISSUE; MALE; NONHUMAN; PORPHYROMONAS GINGIVALIS; TANNERELLA FORSYTHENSIS; TREPONEMA DENTICOLA;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ADHESINS, BACTERIAL; ADULT; AGGRESSIVE PERIODONTITIS; BACTEROIDES; CASE-CONTROL STUDIES; CHRONIC PERIODONTITIS; CYSTEINE ENDOPEPTIDASES; ELAFIN; FEMALE; GINGIVAL CREVICULAR FLUID; GINGIVITIS; HUMANS; MALE; MIDDLE AGED; PORPHYROMONAS GINGIVALIS; PROTEINASE INHIBITORY PROTEINS, SECRETORY; SECRETORY LEUKOCYTE PEPTIDASE INHIBITOR; SERINE PROTEASES; SERINE PROTEINASE INHIBITORS; STATISTICS, NONPARAMETRIC; TREPONEMA DENTICOLA;

EID: 84855753846     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2011.00631.x     Document Type: Article

References (59)

1. American Academy of Periodontology. (1996) Consensus report. Periodontal diseases: pathogenesis and microbial factors. Ann Periodontol 1: 926-932.
2. Armitage, G.C. (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4: 1-6.
3. Ashcroft, G.S., Lei, K., Jin, W. et al. (2000) Secretory leukocyte protease inhibitor mediates non-redundant functions necessary for normal wound healing. Nat Med 6: 1147-1153.
4. Ashimoto, A., Chen, C., Bakker, I. and Slots, J. (1996) Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 11: 266-273.
5. Bamford, C.V., Francescutti, T., Cameron, C.E., Jenkinson, H.F. and Dymock, D. (2010) Characterization of a novel family of fibronectin-binding proteins with M23 peptidase domains from Treponema denticola. Mol Oral Microbiol 25: 369-383.
6. Baranger, K., Zani, M.L., Chandenier, J., Dallet-Choisy, S. and Moreau, T. (2008) The antibacterial and antifungal properties of trappin-2 (pre-elafin) do not depend on its protease inhibitory function. FEBS J 275: 2008-2020.
7. Baranger, K., Zani, M.L., Labas, V., Dallet-Choisy, S. and Moreau, T. (2011) Secretory leukocyte protease inhibitor (SLPI) is, like its homologue trappin-2 (pre-elafin), a transglutaminase substrate. PLoS ONE 6: e20976.
8. Bergenfeldt, M., Axelsson, L. and Ohlsson, K. (1992) Release of neutrophil proteinase 4(3) and leukocyte elastase during phagocytosis and their interaction with proteinase inhibitors. Scand J Clin Lab Invest 52: 823-829.
9. Binder, T.A., Goodson, J.M. and Socransky, S.S. (1987) Gingival fluid levels of acid and alkaline phosphatase. J Periodontal Res 22: 14-19.
10. Borrell, L.N. and Papapanou, P.N. (2005) Analytical epidemiology of periodontitis. J Clin Periodontol 32(Suppl 6): 132-158.
11. Eick, S., Straube, A., Guentsch, A., Pfister, W. and Jentsch, H. (2011) Comparison of real-time polymerase chain reaction and DNA-strip technology in microbiological evaluation of periodontitis treatment. Diagn Microbiol Infect Dis 69: 12-20.
12. Figueredo, C.M. and Gustafsson, A. (2000) Increased amounts of laminin in GCF from untreated patients with periodontitis. J Clin Periodontol 27: 313-318.
13. Figueredo, C.M., Fischer, R.G. and Gustafsson, A. (2005) Aberrant neutrophil reactions in periodontitis. J Periodontol 76: 951-955.
14. Fong, K.P., Tang, H.Y., Brown, A.C. et al. (2011) Aggregatibacter actinomycetemcomitans leukotoxin is post-translationally modified by addition of either saturated or hydroxylated fatty acyl chains. Mol Oral Microbiol 26: 262-276.
15. Fox, S., Leitch, A.E., Duffin, R., Haslett, C. and Rossi, A.G. (2010) Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J Innate Immun 2: 216-227.
16. Fritz, H., Schiessler, H., Gieger, R., Ohlsson, K. and Hochstrasser, K. (1978) Naturally occurring low molecular weight inhibitors of neutral proteinases from PMN-granulocytes and of kallikreins. Agents Actions 8: 57-64.
17. Gallo, R.L., Murakami, M., Ohtake, T. and Zaiou, M. (2002a) Biology and clinical relevance of naturally occurring antimicrobial peptides. J Allergy Clin Immunol 110: 823-831.
18. Garant, P. (2003) Oral Cells and Tissues. Carol Stream, IL: Quintessence Publishing Co Inc.
19. Guentsch, A., Kramesberger, M., Sroka, A. et al. (2011) Comparison of gingival crevicular fluid sampling methods in patients with severe chronic periodontitis. J Periodontol 82: 1051-1060.
20. Guo, Y., Nguyen, K.A. and Potempa, J. (2010) Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon's knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000 54: 15-44.
21. Guyot, N., Zani, M.L., Maurel, M.C., Dallet-Choisy, S. and Moreau, T. (2005) Elafin and its precursor trappin-2 still inhibit neutrophil serine proteinases when they are covalently bound to extracellular matrix proteins by tissue transglutaminase. Biochemistry 44: 15610-15618.
22. Guyot, N., Bergsson, G., Butler, M.W. et al. (2010) Functional study of elafin cleaved by Pseudomonas aeruginosa metalloproteinases. Biol Chem 391: 705-716.
23. Hiemstra, P.S., Maassen, R.J., Stolk, J. et al. (1996) Antibacterial activity of antileukoprotease. Infect Immun 64: 4520-4524.
24. Holt, S.C. and Ebersole, J.L. (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38: 72-122.
25. Huynh, Q.N., Wang, S., Tafolla, E. et al. (2002) Specific fibronectin fragments as markers of periodontal disease status. J Periodontol 73: 1101-1110.
26. Ichimaru, E., Tanoue, M., Tani, M. et al. (1996) Cathepsin B in gingival crevicular fluid of adult periodontitis patients: identification by immunological and enzymological methods. Inflamm Res 45: 277-282.
27. Into, T., Inomata, M., Kanno, Y. et al. (2006) Arginine-specific gingipains from Porphyromonas gingivalis deprive protective functions of secretory leucocyte protease inhibitor in periodontal tissue. Clin Exp Immunol 145: 545-554.
28. Jin, F., Nathan, C.F., Radzioch, D. and Ding, A. (1998) Lipopolysaccharide-related stimuli induce expression of the secretory leukocyte protease inhibitor, a macrophage-derived lipopolysaccharide inhibitor. Infect Immun 66: 2447-2452.
29. Kachlany, S.C. (2010) Aggregatibacter actinomycetemcomitans leukotoxin: from threat to therapy. J Dent Res 89: 561-570.
30. Kantyka, T., Latendorf, T., Wiedow, O. et al. (2009) Elafin is specifically inactivated by RgpB from Porphyromonas gingivalis by distinct proteolytic cleavage. Biol Chem 390: 1313-1320.
31. Korkmaz, B., Moreau, T. and Gauthier, F. (2008) Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions. Biochimie 90: 227-242.
32. Lamster, I.B., Oshrain, R.L., Fiorello, L.A., Celenti, R.S. and Gordon, J.M. (1988) A comparison of 4 methods of data presentation for lysosomal enzyme activity in gingival crevicular fluid. J Clin Periodontol 15: 347-352.
33. Lee, C.W., Kim, T.H., Lee, H.M. et al. (2009) Upregulation of elafin and cystatin C in the ethmoid sinus mucosa of patients with chronic sinusitis. Arch Otolaryngol Head Neck Surg 135: 771-775.
34. Lopez, N.J. (2000) Occurrence of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Prevotella intermedia in progressive adult periodontitis. J Periodontol 71: 948-954.
35. Mayer, M.P., Bueno, L.C., Hansen, E.J. and DiRienzo, J.M. (1999) Identification of a cytolethal distending toxin gene locus and features of a virulence-associated region in Actinobacillus actinomycetemcomitans. Infect Immun 67: 1227-1237.
36. Mihaila, A. and Tremblay, G.M. (2001) Human alveolar macrophages express elafin and secretory leukocyte protease inhibitor. Z Naturforsch C 56: 291-297.
37. Miura, M., Hamachi, T., Fujise, O. and Maeda, K. (2005) The prevalence and pathogenic differences of Porphyromonas gingivalis fimA genotypes in patients with aggressive periodontitis. J Periodontal Res 40: 147-152.
38. Pham, C.T. (2008) Neutrophil serine proteases fine-tune the inflammatory response. Int J Biochem Cell Biol 40: 1317-1333.
39. Potempa, J. and Pike, R.N. (2009) Corruption of innate immunity by bacterial proteases. J Innate Immun 1: 70-87.
40. Potempa, J., Banbula, A. and Travis, J. (2000) Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontol 2000 24: 153-192.
41. Potempa, J., Sroka, A., Imamura, T. and Travis, J. (2003) Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes. Curr Protein Pept Sci 4: 397-407.
42. Reeves, E.P., Lu, H., Jacobs, H.L. et al. (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416: 291-297.
43. Sallenave, J.M., Shulmann, J., Crossley, J., Jordana, M. and Gauldie, J. (1994) Regulation of secretory leukocyte proteinase inhibitor (SLPI) and elastase-specific inhibitor (ESI/elafin) in human airway epithelial cells by cytokines and neutrophilic enzymes. Am J Respir Cell Mol Biol 11: 733-741.
44. Samsom, J.N., van der Marel, A.P., van Berkel, L.A. et al. (2007) Secretory leukoprotease inhibitor in mucosal lymph node dendritic cells regulates the threshold for mucosal tolerance. J Immunol 179: 6588-6595.
45. Schagger, H., Aquila, H. and Von Jagow, G. (1988) Coomassie blue-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for direct visualization of polypeptides during electrophoresis. Anal Biochem 173: 201-205.
46. Sigusch, B., Klinger, G., Holtz, H. and Suss, J. (1992) In vitro phagocytosis by crevicular phagocytes in various forms of periodontitis. J Periodontol 63: 496-501.
47. Sundqvist, G. (1993) Pathogenicity and virulence of black-pigmented gram-negative anaerobes. FEMS Immunol Med Microbiol 6: 125-137.
48. Taggart, C.C., Lowe, G.J., Greene, C.M. et al. (2001) Cathepsin B, L, and S cleave and inactivate secretory leucoprotease inhibitor. J Biol Chem 276: 33345-33352.
49. Takeuchi, Y., Umeda, M., Sakamoto, M. et al. (2001) Treponema socranskii, Treponema denticola, and Porphyromonas gingivalis are associated with severity of periodontal tissue destruction. J Periodontol 72: 1354-1363.
50. Talonpoika, J. (1991) Characterization of fibrin(ogen) fragments in gingival crevicular fluid. Scand J Dent Res 99: 40-43.
51. Talonpoika, J., Soderling, E., Tiekso, J. and Paunio, K. (1991) Gingival crevicular fluid plasmin activity in different clinical conditions and after periodontal treatment. Proc Finn Dent Soc 87: 329-337.
52. 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.
53. Ujiie, Y., Oida, S., Gomi, K., Arai, T. and Fukae, M. (2007) Neutrophil elastase is involved in the initial destruction of human periodontal ligament. J Periodontal Res 42: 325-330.
54. van Wetering, S., van der Linden, A.C., van Sterkenburg, M.A. et al. (2000a) Regulation of SLPI and elafin release from bronchial epithelial cells by neutrophil defensins. Am J Physiol Lung Cell Mol Physiol 278: L51-L58.
55. van Wetering, S., van der Linden, A.C., van Sterkenburg, M.A. et al. (2000b) Regulation of secretory leukocyte proteinase inhibitor (SLPI) production by human bronchial epithelial cells: increase of cell-associated SLPI by neutrophil elastase. J Investig Med 48: 359-366.
56. Williams, S.E., Brown, T.I., Roghanian, A. and Sallenave, J.M. (2006) SLPI and elafin: one glove, many fingers. Clin Sci (Lond) 110: 21-35.
57. Yin, L., Swanson, B., An, J. et al. (2010) Differential effects of periopathogens on host protease inhibitors SLPI, elafin, SCCA1, and SCCA2. J Oral Microbiol 2: doi: 10.3402.
58. Yokota, T., Bui, T., Liu, Y. et al. (2007) Differential regulation of elafin in normal and tumor-derived mammary epithelial cells is mediated by CCAAT/enhancer binding protein beta. Cancer Res 67: 11272-11283.
59. Zani, M.L., Nobar, S.M., Lacour, S.A. et al. (2004) Kinetics of the inhibition of neutrophil proteinases by recombinant elafin and pre-elafin (trappin-2) expressed in Pichia pastoris. Eur J Biochem 271: 2370-2378.