Plasmin is essential in preventing periodontitis in mice

American Journal of Pathology

Volumn 179, Issue 2, 2011, Pages 819-828

  Sulniute, Rima ^a   Lindh, Tomas ^a   Wilczynska, Malgorzata ^a   Li, Jinan ^a   Ny, Tor ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRIN; GLUPLASMINOGEN; PLASMIN; PLASMINOGEN; UNCLASSIFIED DRUG; UROKINASE;

ABSORPTION; ALVEOLAR BONE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEFECT; CELL INFILTRATION; CEMENTUM; CONTROLLED STUDY; DENTAL HEALTH; DISEASE COURSE; GINGIVA; IMMUNOHISTOCHEMISTRY; MOUSE; NECROSIS; NEUTROPHIL; NONHUMAN; OSTEOBLAST; PERIODONTITIS; PERIODONTIUM; PRIORITY JOURNAL; TISSUE REGENERATION;

ALKALINE PHOSPHATASE; ANIMALS; DISEASE MODELS, ANIMAL; FIBRIN; FIBRINOLYSIN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, GENETIC; NEUTROPHILS; PERIODONTAL DISEASES; PERIODONTITIS; TIME FACTORS;

EID: 80052454901     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.05.003     Document Type: Article

References (69)

1. B.L. Pihlstrom, B.S. Michalowicz, and N.W. Johnson Periodontal diseases Lancet 366 2005 1809 1820 (Pubitemid 41642647)
2. J.M. Albandar, and T.E. Rams Global epidemiology of periodontal diseases: an overview Periodontol 29 2002 7 10 2000
3. A. Sheiham, and G.S. Netuveli Periodontal diseases in Europe Periodontol 29 2002 104 121 2000
4. J.M. Albandar Periodontal diseases in North America Periodontol 29 2002 31 69 2000
5. S.P. Nair, S. Meghji, M. Wilson, K. Reddi, P. White, and B. Henderson Bacterially induced bone destruction: mechanisms and misconceptions Infect Immun 64 1996 2371 2380 (Pubitemid 26226792)
6. J. Liu, S. Wang, P. Zhang, N. Said-Al-Naief, S.M. Michalek, and X. Feng Molecular mechanism of the bifunctional role of lipopolysaccharide in osteoclastogenesis J Biol Chem 284 2009 12512 12523
7. M. Fujihara, M. Muroi, K. Tanamoto, T. Suzuki, H. Azuma, and H. Ikeda Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex Pharmacol Ther 100 2003 171 194 (Pubitemid 37377912)
8. F.O. Martinez, A. Sica, A. Mantovani, and M. Locati Macrophage activation and polarization Front Biosci 13 2008 453 461 (Pubitemid 351599757)
9. W.B. Clark, and H. Löe Mechanisms of initiation and progression of periodontal disease Periodontol 2 1993 72 82 2000
10. D.E. Deas, S.A. Mackey, and H.T. McDonnell Systemic disease and periodontitis: manifestations of neutrophil dysfunction Periodontol 32 2003 82 104 2000 (Pubitemid 37487572)
11. L. Zhang, D. Seiffert, B.J. Fowler, G.R. Jenkins, T.C. Thinnes, D.J. Loskutoff, R.J. Parmer, and L.A. Miles Plasminogen has a broad extrahepatic distribution Thromb Haemost 87 2002 493 501 (Pubitemid 34232492)
12. J. Arnout, M.F. Hoylaerts, and H.R. Lijnen Haemostasis Handb Exp Pharmacol Pt 2 2006 1 41
13. D. Collen Ham-Wasserman lecture: role of the plasminogen system in fibrin-homeostasis and tissue remodeling Hematology Am Soc Hematol Educ Program 2001 1 91
14. P. Mignatti, and D.B. Rifkin Biology and biochemistry of proteinases in tumor invasion Physiol Rev 73 1993 161 195 (Pubitemid 23065437)
15. D.B. Rifkin, R. Mazzieri, J.S. Munger, I. Noguera, and J. Sung Proteolytic control of growth factor availability Apmis 107 1999 80 85 (Pubitemid 29133526)
16. A. Santala, J. Saarinen, P. Kovanen, and P. Kuusela Activation of interstitial collagenase, MMP-1, by Staphylococcus aureus cells having surface-bound plasmin: a novel role of plasminogen receptors of bacteria FEBS Lett 461 1999 153 156 (Pubitemid 29533324)
17. G. Murphy, R. Ward, J. Gavrilovic, and S. Atkinson Physiological mechanisms for metalloproteinase activation Matrix 1 Suppl 1992 224 230
18. P. Carmeliet, L. Moons, R. Lijnen, M. Baes, V. Lemaitre, P. Tipping, A. Drew, Y. Eeckhout, S. Shapiro, F. Lupu, and D. Collen Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation Nat Genet 17 1997 439 444 (Pubitemid 27518393)
19. T. Syrovets, and T. Simmet Novel aspects and new roles for the serine protease plasmin Cell Mol Life Sci 61 2004 873 885 (Pubitemid 38651004)
20. V.A. Ploplis, E.L. French, P. Carmeliet, D. Collen, and E.F. Plow Plasminogen deficiency differentially affects recruitment of inflammatory cell populations in mice Blood 91 1998 2005 2009 (Pubitemid 28185501)
21. K. Shanmukhappa, U. Matte, J.L. Degen, and J.A. Bezerra Plasmin-mediated proteolysis is required for hepatocyte growth factor activation during liver repair J Biol Chem 284 2009 12917 12923
22. J. Romer, T.H. Bugge, C. Pyke, L.R. Lund, M.J. Flick, J.L. Degen, and K. Dano Impaired wound healing in mice with a disrupted plasminogen gene Nat Med 2 1996 287 292 (Pubitemid 26080649)
23. C.C. Broder, R. Lottenberg, G.O. von Mering, K.H. Johnston, and M.D. Boyle Isolation of a prokaryotic plasmin receptor: relationship to a plasminogen activator produced by the same micro-organism J Biol Chem 266 1991 4922 4928 (Pubitemid 21909443)
24. A. Berge, and U. Sjobring PAM, a novel plasminogen-binding protein from Streptococcus pyogenes J Biol Chem 268 1993 25417 25424 (Pubitemid 23358145)
25. P. Brandtzaeg, G.B. Joo, B. Brusletto, and P. Kierulf Plasminogen activator inhibitor 1 and 2, alpha-2-antiplasmin, plasminogen, and endotoxin levels in systemic meningococcal disease Thromb Res 57 1990 271 278 (Pubitemid 20071076)
26. Y. Guo, J. Li, E. Hagstrom, and T. Ny Protective effects of plasmin(ogen) in a mouse model of Staphylococcus aureus-induced arthritis Arthritis Rheum 58 2008 764 772 (Pubitemid 351364874)
27. O. Gunhan, M. Gunhan, E. Berker, C.A. Gurgan, and H. Yildirim Destructive membranous periodontal disease (Ligneous periodontitis) J Periodontol 70 1999 919 925
28. C. Scully, A.Y. Gokbuget, C. Allen, J.V. Bagan, A. Efeoglu, G. Erseven, C. Flaitz, S. Cintan, T. Hodgson, S.R. Porter, and P. Speight Oral lesions indicative of plasminogen deficiency (hypoplasminogenemia) Oral Surg Oral Med Oral Pathol Oral Radiol Endod 91 2001 334 337 (Pubitemid 33608854)
29. K. Tefs, M. Gueorguieva, J. Klammt, C.M. Allen, D. Aktas, F.Y. Anlar, S.D. Aydogdu, D. Brown, E. Ciftci, P. Contarini, C.E. Dempfle, M. Dostalek, S. Eisert, A. Gokbuget, O. Gunhan, A.A. Hidayat, B. Hugle, M. Isikoglu, M. Irkec, S.K. Joss, S. Klebe, C. Kneppo, I. Kurtulus, R.P. Mehta, K. Ornek, R. Schneppenheim, S. Seregard, E. Sweeney, S. Turtschi, G. Veres, P. Zeitler, M. Ziegler, and V. Schuster Molecular and clinical spectrum of type I plasminogen deficiency: a series of 50 patients Blood 108 2006 3021 3026
30. E. Baltacioglu, F.A. Akalin, E. Topaloglu, E. Sukuroglu, and U. Cobanoglu Ligneous periodontitis and gingival antioxidant status: report of two cases Oral Surg Oral Med Oral Pathol Oral Radiol Endod 104 2007 803 808
31. V. Schuster, B. Hugle, and K. Tefs Plasminogen deficiency J Thromb Haemost 5 2007 2315 2322 (Pubitemid 350154337)
32. J. Klammt, L. Kobelt, D. Aktas, I. Durak, A. Gokbuget, Q. Hughes, M. Irkec, I. Kurtulus, E. Lapi, H. Mechoulam, R. Mendoza-Londono, J.S. Palumbo, H. Steitzer, K.F. Tabbara, Z. Ozbek, N. Pucci, T. Sotomayor, M. Sturm, T. Drogies, M. Ziegler, and V. Shuster Identification of three novel plasminogen (Plg) gene mutations in a series of 23 patients with low Plg activity Thromb Haemost 105 2011 454 460
33. V.A. Ploplis, P. Carmeliet, S. Vazirzadeh, I. Van Vlaenderen, L. Moons, E.F. Plow, and D. Collen Effects of disruption of the plasminogen gene on thrombosis, growth, and health in mice Circulation 92 1995 2585 2593
34. A. Ny, G. Leonardsson, A.C. Hagglund, P. Hagglof, V.A. Ploplis, P. Carmeliet, and T. Ny Ovulation in plasminogen-deficient mice Endocrinology 140 1999 5030 5035
35. P. Carmeliet, L. Schoonjans, L. Kieckens, B. Ream, J. Degen, R. Bronson, R. De Vos, J.J. van den Oord, D. Collen, and R.C. Mulligan Physiological consequences of loss of plasminogen activator gene function in mice Nature 368 1994 419 424 (Pubitemid 24115347)
36. A. Ny, L. Nordstrom, P. Carmeliet, and T. Ny Studies of mice lacking plasminogen activator gene function suggest that plasmin production prior to ovulation exceeds the amount needed for optimal ovulation efficiency Eur J Biochem 244 1997 487 493 (Pubitemid 27110752)
37. D. Miao, and A. Scutt Histochemical localization of alkaline phosphatase activity in decalcified bone and cartilage J Histochem Cytochem 50 2002 333 340 (Pubitemid 34171058)
38. J.A. Bezerra, A.R. Currier, H. Melin-Aldana, G. Sabla, T.H. Bugge, K.W. Kombrinck, and J.L. Degen Plasminogen activators direct reorganization of the liver lobule after acute injury Am J Pathol 158 2001 921 929 (Pubitemid 32221784)
39. L.R. Lund, K.A. Green, A.A. Stoop, M. Ploug, K. Almholt, J. Lilla, B.S. Nielsen, I.J. Christensen, C.S. Craik, Z. Werb, K. Dano, and J. Romer Plasminogen activation independent of uPA and tPA maintains wound healing in gene-deficient mice EMBO J 25 2006 2686 2697 (Pubitemid 43980377)
40. W. Beertsen, M. Willenborg, V. Everts, A. Zirogianni, R. Podschun, B. Schroder, E.L. Eskelinen, and P. Saftig Impaired phagosomal maturation in neutrophils leads to periodontitis in lysosomal-associated membrane protein-2 knockout mice J Immunol 180 2008 475 482
41. T.H. Bugge, M.J. Flick, C.C. Daugherty, and J.L. Degen Plasminogen deficiency causes severe thrombosis but is compatible with development and reproduction Genes Dev 9 1995 794 807
42. M. El-Darouti, A.A. Zayed, G.Y. El-Kamah, and M.I. Mostafa Ligneous conjunctivitis with oral mucous membrane involvement and decreased plasminogen level Pediatr Dermatol 26 2009 448 451
43. H. Toker, M.I. Toker, F. Goze, M. Turgut, and A. Yilmaz A ligneous periodontitis and conjunctival lesions in a patient with plasminogen deficiency Oral Surg Oral Med Oral Pathol Oral Radiol Endod 103 2007 e35 e38
44. V.S. Pierro, R. Vazquez-Sullca, A.S. Vieira, C.M. Takiya, G. Carakushansky, and E.J. Feres-Filho Ligneous periodontitis and Ehlers-Danlos syndrome J Periodontol 77 2006 123 128 (Pubitemid 43949666)
45. T. Baykul, and Y. Bozkurt Destructive membranous periodontal disease (ligneous periodontitis): a case report and 3 years follow-up Br Dent J 197 2004 467 468 (Pubitemid 39472127)
46. T. Herren, T.A. Burke, M. Jardi, J. Felez, and E.F. Plow Regulation of plasminogen binding to neutrophils Blood 97 2001 1070 1078 (Pubitemid 32154295)
47. T.H. Price, H.D. Ochs, R. Gershoni-Baruch, J.M. Harlan, and A. Etzioni In vivo neutrophil and lymphocyte function studies in a patient with leukocyte adhesion deficiency type II Blood 84 1994 1635 1639 (Pubitemid 24273035)
48. R. Niederman, T. Westernoff, C. Lee, L.L. Mark, N. Kawashima, M. Ullman-Culler, F.E. Dewhirst, B.J. Paster, D.D. Wagner, T. Mayadas, R.O. Hynes, and P. Stashenko Infection-mediated early-onset periodontal disease in P/E-selectin-deficient mice J Clin Periodontol 28 2001 569 575 (Pubitemid 33761333)
49. D.D. Bosshardt, and A. Sculean Does periodontal tissue regeneration really work? Periodontol 51 2009 208 219 2000
50. F.J. Castellino, and V.A. Ploplis Structure and function of the plasminogen/plasmin system Thromb Haemost 93 2005 647 654 (Pubitemid 40485399)
51. S. Garrett, and G. Bogle Periodontal regeneration: a review of flap management Periodontol 1 1993 100 108 2000
52. S. Pitaru, H. Tal, M. Soldinger, A. Grosskopf, and M. Noff Partial regeneration of periodontal tissues using collagen barriers: initial observations in the canine J Periodontol 59 1988 380 386
53. J. Gottlow, S. Nyman, J. Lindhe, T. Karring, and J. Wennstrom New attachment formation in the human periodontium by guided tissue regeneration: case reports J Clin Periodontol 13 1986 604 616
54. J. Caton, S. Nyman, and H. Zander Histometric evaluation of periodontal surgery, II: connective tissue attachment levels after four regenerative procedures J Clin Periodontol 7 1980 224 231 (Pubitemid 10089885)
55. S. Nyman, J. Lindhe, T. Karring, and H. Rylander New attachment following surgical treatment of human periodontal disease J Clin Periodontol 9 1982 290 296
56. I. Fernández-Tresguerres-Hernandez-Gil, M.A. Alobera-Gracia, M. del-Canto-Pingarrón, and L. Blanco-Jerez Physiological bases of bone regeneration, II: the remodeling process Med Oral Patol Oral Cir Bucal 11 2006 E151 E157
57. E. Daci, V. Everts, S. Torrekens, E. Van Herck, W. Tigchelaar-Gutterr, R. Bouillon, and G. Carmeliet Increased bone formation in mice lacking plasminogen activators J Bone Miner Res 18 2003 1167 1176 (Pubitemid 37294909)
58. E.A. Jaffe, and D.F. Mosher Synthesis of fibronectin by cultured human endothelial cells J Exp Med 147 1978 1779 1791 (Pubitemid 8372968)
59. R. Timpl, H. Rohde, P.G. Robey, S.I. Rennard, J.M. Foidart, and G.R. Martin Laminin: a glycoprotein from basement membranes J Biol Chem 254 1979 9933 9937
60. J.A. Yee, L. Yan, J.C. Dominguez, E.H. Allan, and T.J. Martin Plasminogen-dependent activation of latent transforming growth factor beta (TGF beta) by growing cultures of osteoblast-like cells J Cell Physiol 157 1993 528 534 (Pubitemid 23361181)
61. E.H. Allan, R. Zeheb, T.D. Gelehrter, J.H. Heaton, S. Fukumoto, J.A. Yee, and T.J. Martin Transforming growth factor beta inhibits plasminogen activator (PA) activity and stimulates production of urokinase-type PA: PA inhibitor-1 mRNA, and protein in rat osteoblast-like cells J Cell Physiol 149 1991 34 43 (Pubitemid 21910163)
62. J.F. Novak, J.D. Hayes, and S.K. Nishimoto Plasmin-mediated proteolysis of osteocalcin J Bone Miner Res 12 1997 1035 1042 (Pubitemid 27264216)
63. C. Chenu, S. Colucci, M. Grano, P. Zigrino, R. Barattolo, G. Zambonin, N. Baldini, P. Vergnaud, P.D. Delmas, and A.Z. Zallone Osteocalcin induces chemotaxis, secretion of matrix proteins, and calcium-mediated intracellular signaling in human osteoclast-like cells J Cell Biol 127 1994 1149 1158
64. P.V. Bodine, and B.S. Komm Evidence that conditionally immortalized human osteoblasts express an osteocalcin receptor Bone 25 1999 535 543 (Pubitemid 29469459)
65. E.H. Allan, and T.J. Martin The plasminogen activator inhibitor system in bone cell function Clin Orthop Relat Res 1995 54 63
66. I. Kurtulus, A. Gokbuget, A. Efeoglu, S. Cintan, K. Tefs, V. Schuster, and C. Scully Hypoplasminogenemia with ligneous periodontitis: a failed local therapeutic approach J Periodontol 78 2007 1164 1175
67. G. Fine, K. Bauer, M. Al-Mohaya, and S.B. Woo Successful treatment of ligneous gingivitis with warfarin Oral Surg Oral Med Oral Pathol Oral Radiol Endod 107 2009 77 80
68. D. Schott, C.E. Dempfle, P. Beck, A. Liermann, A. Mohr-Pennert, M. Goldner, P. Mehlem, H. Azuma, V. Schuster, A.M. Mingers, H.P. Schwarz, and M.D. Kramer Therapy with a purified plasminogen concentrate in an infant with ligneous conjunctivitis and homozygous plasminogen deficiency N Engl J Med 339 1998 1679 1686 (Pubitemid 28550693)
69. P. Watts, P. Suresh, E. Mezer, A. Ells, M. Albisetti, L. Bajzar, V. Marzinotto, M. Andrew, P. Massicotle, and D. Rootman Effective treatment of ligneous conjunctivitis with topical plasminogen Am J Ophthalmol 133 2002 451 455 (Pubitemid 34262663)