Collagenase-2 (MMP-8) and collagenase-3 (MMP-13) in adult periodontitis: Molecular forms and levels in gingival crevicular fluid and immunolocalisation in gingival tissue

Journal of Clinical Periodontology

Volumn 29, Issue 3, 2002, Pages 224-232

  Kiili, M ^a   Cox, S W ^b   Chen, H W ^b,e   Wahlgren, J ^c   Maisi, P ^a   Eley, B M ^b   Salo, T ^d   Sorsa, T ^a,c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF OULU   (Finland)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

Collagenase; Gingival crevicular fluid; Immunohistochemistry; Matrix metalloproteinase; Periodontium; Western blotting

Indexed keywords

COLLAGENASE; COLLAGENASE 3; ENZYME PRECURSOR; MMP13 PROTEIN, HUMAN; NEUTROPHIL COLLAGENASE;

ADULT; ARTICLE; CHRONIC DISEASE; ENZYME IMMUNOASSAY; ENZYMOLOGY; FEMALE; FIBROBLAST; GINGIVA; GINGIVITIS; HUMAN; MACROPHAGE; MALE; METABOLISM; MIDDLE AGED; NEUTROPHIL; NONPARAMETRIC TEST; PERIODONTITIS; PLASMA CELL; WESTERN BLOTTING;

ADULT; BLOTTING, WESTERN; CHRONIC DISEASE; COLLAGENASES; ENZYME PRECURSORS; FEMALE; FIBROBLASTS; GINGIVA; GINGIVAL CREVICULAR FLUID; HUMANS; IMMUNOENZYME TECHNIQUES; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 8; MIDDLE AGED; NEUTROPHILS; PERIODONTITIS; PLASMA CELLS; STATISTICS, NONPARAMETRIC;

EID: 0036512085     PISSN: 03036979     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-051x.2002.290308.x     Document Type: Article

References (49)

1. Birkedal-Hansen, H. (1993) Role of matrix metalloproteinases in human periodontal diseases. J. Periodontol. 64, 474-484.
2. 2-macroglobulin and cystatin levels in gingival crevicular fluid from chronic periodontitis patients. J. Clin. Periodontol. 25, 34-41.
3. Chen, H. Y., Cox, S. W., Eley, B. M., Mäntylä, P., Rönkä, H. & Sorsa, T. (2000) Matrix metalloproteinase-8 levels and elastase activities in gingival crevicular fluid from chronic adult periodontitis patients. J. Clin. Periodontol. 27, 366-369.
4. Cole, A. A., Chubinskaya, S., Schumacher, B., Huch, K., Szabo, G., Yao, J., Mikecz, K., Hasty, K. A. & Kuettner, K. E. (1996) Chondrocyte matrix metalloproteinase-8. Human articular chondrocytes express neutrophil collagenase. J. Biol. Chem. 271, 11023-11026.
5. Collin, H-L., Sorsa, T., Meurman, J. H., Niskanen, L., Salo, T., Rönkä., H., Konttinen, Y. T., Koivisto, A-M. & Uusitupa, M. (2000) Salivary matrix metalloproteinase (MMP-8) levels and gelatinase (MMP-9) activities in patients with type 2 diabetes mellitus. J. Periodontal. Res. 35, 259-265.
6. Ding, Y., Uitto, V. J., Firth, J., Salo, T., Haapasalo, M., Konttinen, Y. T. & Sorsa, T. (1995) Modulation of host matrix metalloproteinases by bacterial virulence factors relevant in human periodontal diseases. Oral Dis. 1, 279-286.
7. Ding, Y., Uitto, V. J., Haapasalo, M., Lounatmaa, K., Konttinen, Y. T., Salo, T., Grenier, D. & Sorsa, T. (1996) Membrane components of Treponema denticola trigger proteinase release from human polymorphonuclear leukocytes. J. Dent. Res. 75, 1986-1993.
8. Ding, Y., Haapasalo, M., Kerosuo, E., Lounatmaa, K., Kotiranta, A. & Sorsa, T. (1997) Release and activation of human neutrophil matrix metallo- and serine proteinases during phagocytosis of Fusobacterium nucleatum, Porphyromonas gingivalis and Treponema denticola. J. Clin. Periodontol. 24, 237-248.
9. Freije, J. M., Diez-Itza, I., Balbin, M., Sanchez, L. M., Blasco, R., Tolivia, J. & Lopez-Otin, C. (1994) Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J. Biol. Chem. 269, 16766-16773.
10. Gangbar, S., Overall, C. M., McCulloch, C. A. & Sodek, J. (1990) Identification of polymorphonuclear leukocyte collagenase and gelatinase activities in mouthrinse samples: correlation with periodontal disease activity in adult and juvenile periodontitis. J. Periodontal. Res. 25, 257-267.
11. Golub, L. M., Sorsa, T., Lee, H. M., Ciancio, S., Sorbi, D., Ramamurthy, N. S., Gruber, B., Salo, T. & Konttinen, Y. T. (1995) Doxycycline inhibits neutrophil (PMN)-type matrix metalloproteinases in human adult periodontitis gingiva. J. Clin. Periodontol. 22, 100-109.
12. Golub, L. M., Lee, H. M., Greenwald, R. A., Ryan, M. E., Sorsa, T., Salo, T. & Giannobile, W. V. (1997) A matrix metalloproteinase inhibitor reduces bone-type collagen degradation fragments and specific collagenases in gingival crevicular fluid during adult periodontitis. Inflamm. Res. 46, 310-319.
13. Golub, L. M., Lee, H. M., Ryan, M. E., Giannobile, W. V., Payne, J. & Sorsa, T. (1998) Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms. Adv. Dent. Res. 12, 12-26.
14. Golub, L. M., McNamara, T. F., Ryan, M. E., Kohut, B., Blienden, T., Payonk, G. P., Sipos, T. & Baron, H. J. (2001) Adjunctive treatment with subantimicrobial doses of doxycycline: Effects on gingival fluid collagenase activity and attachement loss in adult periodontitis. J. Clin. Periodontol. 28, 146-156.
15. Hanemaaijer, R., Sorsa, T., Konttinen, Y. T., Ding, Y., Sutinen, M., Visser, H., van Hinsbergh, V. W., Helaakoski, T., Kainulainen, T., Rönkä, H., Tschesche, H. & Salo, T. (1997) Matrix metalloproteinase-8 is expressed in human rheumatoid synovial fibroblasts and endothelial cells. Regulation by TNF-α and doxycycline. J. Biol. Chem. 272, 31504-31509.
16. Ingman, T., Sorsa, T., Lindy, O., Koski, H. & Konttinen, Y. T. (1994a) Multiple forms of gelatinases/type IV collagenases in saliva and gingival crevicular fluid of periodontitis patients. J. Clin. Periodontol. 21, 26-31.
17. Ingman, T., Sorsa, T., Michaelis, J. & Konttinen, Y. T. (1994b) Immunohistochemical study of neutrophil- and fibroblast-type collagenases and stromeolysin-1 in adult periodontitis. Scand. J. Dent. Res. 102, 342-349.
18. Ingman, T., Tervahartiala, T., Ding, Y., Tschesche, H., Haerian, A., Kinane, D. F., Konttinen, Y. T. & Sorsa, T. (1996) Matrix metalloproteinases and their inhibitors in gingival crevicular fluid and saliva of periodontitis patients. J. Clin. Periodontol. 23, 1127-1132.
19. Lauhio, A., Salo, T., Ding, Y., Konttinen, Y. T., Nordstrom, D., Tschesche, H., Lahdevirta, J., Golub, L. M. & Sorsa, T. (1994) In vivo inhibition of human neutrophil collagenase (MMP-8) activity during long-term combination therapy of doxycycline and non-steroidal anti-inflammatory drugs (NSAID) in acute reactive arthritis. Clin. Exp. Immunol. 98, 21-28.
20. Lee, W., Aitken, S., Sodek, J. & McCulloch, C. A. (1995) Evidence of a direct relationship between neutrophil collagenase activity and periodontal tissue destruction in vivo role of active enzyme in human periodontitis. J. Periodontal. Res. 30, 23-33.
21. Liede, K. E., Haukka, J. K., Hietanen, J. H., Mattila, M. H., Rönkä, H. & Sorsa, T. (1999) The association between smoking cessation and periodontal status and salivary proteinase levels. J. Periodontol. 70, 1361-1368.
22. Lindy, O., Konttinen, Y. T., Sorsa, T., Ding, Y., Santavirta, S., Ceponis, A. & Lopez-Otin, C. (1997) Matrix metalloproteinase-13 (collagenase-3) in human rheumatoid synovium. Arthrit. Rheum. 40, 1391-1399.
23. Llano, E., Pendas, A. M., Knauper, V., Sorsa, T., Salo, T., Salido, E., Murphy, G., Simmer, J. P., Bartlett, J. D. & Lopez-Otin, C. (1997) Identification and structural and functional characterization of human enamelysin (MMP-20). Biochemistry 36, 15101-15108.
24. Ma, J., Kitti, U., Teronen, O., Sorsa, T., Husa, V., Laine, P., Rönkä, H., Salo, T., Lindqvist, C. & Konttinen, Y. T. (2000) Collagenases in different categories of peri-implant vertical bone loss. J. Dent. Res. 79, 1870-1873.
25. Mancini, S., Romanelli, R., Laschinger, C. A., Overall, C. M., Sodek, J. & McCulloch, C. A. (1999) Assesment of a novel screening test for neutrophil collagenase activity in the diagnosis of periodontal diseases. J. Periodontol. 70, 1292-1302.
26. Mäkelä, M., Larjava, H., Pirilä, E., Maisi, P., Salo, T., Sorsa, T. & Uitto, V-J. (1999) Matrix metalloproteinase 2 (gelatinase A) is related to migration of keratinocytes. Exp. Cell Res. 251, 67-78.
27. Mäntylä, P., Kinane, D., Luoto, H., Tikanoja, S. & Sorsa, T. (2000) MMP (matrix metalloproteinase) -8 in monitoring periodontal health and disease from gingival crevicular fluid (GCF). J Clin Periodontol 27 (suppl. 1), 97, abstr. #317.
28. Meikle, M. C., Hembry, R. M., Holley, J., Horton, C., McFarlane, C. G. & Reynolds, J. J. (1994) Immunolocalization of matrix metalloproteinases and TIMP-1 (tissue inhibitor of metalloproteinases) in human gingival tissues from periodontitis patients. J. Periodont. Res. 29, 118-126.
29. Mellanen, L., Ingman, T., Lähdevirta, J., Lauhio, A., Ainamo, A., Konttinen, Y. T., Sukura, A., Salo, T. & Sorsa, T. (1996) Matrix metalloproteinases-1, -3 and -8 and myeloperoxidase in saliva of patients with human immunodeficiency virus infection. Oral Dis. 2, 263-71.
30. Nomura, T., Ishii, A., Oishi, Y., Kohma, H. & Hara, K. (1998) Tissue inhibitors of metalloproteinases level and collagenase activity in gingival crevicular fluid: the relevance to periodontal diseases. Oral Dis. 4, 231-240.
31. Palosaari, H., Wahlgren, J., Larmas, M., Rönkä, H., Sorsa, T., Salo, T. & Tjäderhane, L. (2000) The expression of MMP-8 in human odontoblasts and dental pulp cells is down-regulated by TGF-β1. J. Dent. Res. 79, 77-84.
32. Pirilä, E., Ramamurthy, N., Maisi, P., McClain, S., Kucine, A., Wahlgren, J., Golub, L. M., Salo, T. & Sorsa, T. (2001) Wound healing in ovariectomiced rats. Effects of chemically modified tetracycline (CMT-8) and estrogen on matrix metalloproteinases -8 and -13 and type I collagen expression. Curr. Med. Chem. 8, 281-294.
33. Prikk, K., Pirilä, E., Sepper, R., Maisi, P., Salo, T., Wahlgren, J. & Sorsa, T. (2001) In vivo collagenase-2 (MMP-8) expression by human bronchial epithelial cells and monocytes/macrophages in bronchiectasis. J. Pathol. 194, 232-238.
34. Ravanti, L., Häkkinen, L., Larjava, H., Saarialho-Kere, U., Foschi, M., Han, J. & Kähäri, V. M. (1999) Transforming growth factor-beta induces collagenase-3 expression by human gingival fibroblasts via p38 mitogen-activated protein kinase. J. Biol. Chem. 274, 37292-37300.
35. Romanelli, R., Mancini, S., Laschinger, C., Overall, C. M., Sodek, J. & McCulloch, C. A. (1999) Activation of neutrophil collagenase in periodontitis. Infect Immun. 67, 2319-2326.
36. Said, S., Mohd, H., Sander, L., Rönkä, H., Sorsa, T. & Kinane, D. F. (1999) GCF levels of MMP-3 and MMP-8 following placement of bioresorbable membranes. J. Clin. Periodontol. 26, 757-763.
37. Salo, T., Mäkelä, M., Kylmäniemi, M., Autio-Harmainen, H. & Larjava, H. (1994) Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab. Invest. 70, 176-182.
38. Sepper, R., Konttinen, Y. T., Ding, Y., Tagaki, M. & Sorsa, T. (1995) Human neutrophil collagenase (MMP-8), identified in bronchiectasis lavage fluid, correlates with severity of disease. Chest 107, 1641-1647.
39. Sorsa, T., Uitto, V-J., Suomalainen, K., Vauhkonen, M. & Lindy, S. (1988) Comparison of interstitial collagenases from human gingiva, sulcular fluid and polymorphonuclear leukocytes. J. Periodontal. Res. 23, 386-393.
40. Sorsa, T., Ingman, T., Suomalainen, K., Haapasalo, M., Konttinen, Y. T., Lindy, O., Saari, H. & Uitto, V-J. (1992) Identification of proteases from periodontopathogenic bacteria as activators of latent human neutrophil and fibroblast-type interstitial collagenases. Infect. Immun. 60, 4491-4495.
41. Sorsa, T., Ding, Y., Salo, T., Lauhio, A., Teronen, O., Ingman, T., Ohtani, H., Andoh, N., Takeha, S. & Konttinen, Y. T. (1994) Effects of tetracylines on neutrophil, gingival and salivary collagenases. A functional and Western-blot assessment with special reference to their cellular sources in periodontal diseases. Ann. NY Acad. Sci. 732, 112-131.
42. Sorsa, T., Ding, Y. L., Ingman, T., Salo, T., Westerlund, U., Haapasalo, M., Tschesche, H. & Konttinen, Y. T. (1995) Cellular source, activation and inhibition of dental plaque collagenase. J. Clin. Periodontol. 22, 709-717.
43. Sorsa, T., Lukinmaa, P. L., Westerlund, U., Ingman, T., Ding, Y., Tschesche, H., Konttinen, Y. T., Hellaakoski, T. & Salo, T. (1996) The expression, activation and chemotherapeutic inhibition of matrix metalloproteinase-8 (neutrophil collagenase/collagenase-2) in inflammation. In: Biological mechanism of tooth eruption, resorption and replacement by implants, ed. Davidovitch, Z., pp. 317-323. Boston, MA: Harvard Society for the Advancement of Orthodontics.
44. Sorsa, T., Mäntylä, P., Rönkä, H., Kallio, P., Kallis, G. B., Lundqvist, C., Kinane, D. F., Salo, T., Golub, L. M., Teronen, O. & Tikanoja, S. (1999a) Scientific basis of a matrix metalloproteinase-8 specific chair-side test for monitoring periodontal and periimplant health and disease. Ann. NY Acad. Sci. 878, 130-140.
45. Sorsa, T., Golub, L. M., Lee, L. M., Kallis, G. S., Husa, V., Laine, P., Rönkä, H., Salo, T., Mäntylä, P. & Tikanoja, S. (1999b) The anti-collagenolytic effect of low-dose doxycycline (LDD) regimen in adult human periodontitis from gingival crevicular fluid can be monitored by the immunological test for neutrophil collagenase (MMP-8). Fibrinolysis and Proteolysis 13 (suppl. 1), 30-31.
46. Tervahartiala, T., Pirilä, E., Ceponis, A., Maisi, P., Salo, T., Tuter, G., Kallio, P., Törnwall, J., Srinivas, R., Konttinen, Y. T. & Sorsa, T. (2000) The in vivo expression of the collagenolytic matrix metalloproteinases (MMP-2, -8, -13, and -14) and matrilysin (MMP-7) in adult and localized juvenile periodontitis. J. Dent. Res. 79, 1969-1977.
47. Tjäderhane, L., Larjava, H., Sorsa, T., Uitto, V-J., Larmas, M. & Salo, T. (1998) The activation and function of host matrix metalloproteinases in dentin matrix breakdown in caries lesions. J. Dent. Res. 77, 1622-1629.
48. Wahlgren, J., Maisi, P., Sorsa, T., Sutinen, M., Tervahartiala, T., Pirilä, E., Teronen, O., Hietanen, J., Tjäderhane, L. & Salo, T. (2001) Expression and induction of collagenases (MMP-8 and MMP-13) in plasma cells associated with bone destructive lesions. J. Pathol. 194, 217-224.
49. Woessner, J. (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 5, 2145-2154.