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Infection and Immunity, February 2009, p. 850-859, Vol. 77, No. 2
0019-9567/09/$08.00+0     doi:10.1128/IAI.00873-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Local and Systemic Responses in Matrix Metalloproteinase 8-Deficient Mice during Porphyromonas gingivalis-Induced Periodontitis{triangledown}

Heidi Kuula,1* Tuula Salo,2 Emma Pirilä,2 Anita M. Tuomainen,1 Matti Jauhiainen,3 Veli-Jukka Uitto,1 Leo Tjäderhane,1,2 Pirkko J. Pussinen,1 and Timo Sorsa1

Institute of Dentistry, University of Helsinki, Biomedicum, P.O. Box 63, FIN-00014, Helsinki, Finland, and Department of Oral and Maxillofacial Diseases, Helsinki University Central Hospital, Helsinki, Finland,1 Institute of Dentistry, University of Oulu, P.O. Box 5281, 90014 University of Oulu, Oulu, Finland, and Oulu University Central Hospital, Oulu, Finland,2 National Public Health Institute and FIMM, Institute for Molecular Medicine, Biomedicum, Helsinki, Finland3

Received 15 July 2008/ Returned for modification 11 August 2008/ Accepted 13 November 2008

Periodontitis is a bacterium-induced chronic inflammation that destroys tissues that attach teeth to jaw bone. Pathologically excessive matrix metalloproteinase 8 (MMP-8) is among the key players in periodontal destruction by initiating type I collagen degradation. We studied MMP-8 in Porphyromonas gingivalis-induced periodontitis by using MMP-8-deficient (MMP8–/–) and wild-type (WT) mice. Alveolar bone loss, inflammatory mediator expression, serum immunoglobulin, and lipoprotein responses were investigated to clarify the role of MMP-8 in periodontitis and systemic inflammatory responses. P. gingivalis infection induced accelerated site-specific alveolar bone loss in both MMP8–/– and WT mice relative to uninfected mice. The most extensive bone degradation took place in the P. gingivalis-infected MMP8–/– group. Surprisingly, MMP-8 significantly attenuated (P < 0.05) P. gingivalis-induced site-specific alveolar bone loss. Increased alveolar bone loss in P. gingivalis-infected MMP8–/– and WT mice was associated with increase in gingival neutrophil elastase production. Serum lipoprotein analysis demonstrated changes in the distribution of high-density lipoprotein (HDL) and very-low-density lipoprotein (VLDL) particles; unlike the WT mice, the MMP8–/– mice underwent a shift toward a smaller HDL/VLDL particle sizes. P. gingivalis infection increased the HDL/VLDL particle size in the MMP8–/– mice, which is an indicator of lipoprotein responses during systemic inflammation. Serum total lipopolysaccharide activity and the immunoglobulin G-class antibody level in response to P. gingivalis were significantly elevated in both infected mice groups. Thus, MMP-8 appears to act in a protective manner inhibiting the development of bacterium-induced periodontal tissue destruction, possibly through the processing anti-inflammatory cytokines and chemokines. Bacterium-induced periodontitis, especially in MMP8–/– mice, is associated with systemic inflammatory and lipoprotein changes that are likely involved in early atherosclerosis.

* Corresponding author. Mailing address: Biomedicum Helsinki, Institute of Dentistry, P.O. Box 63 (Haartmaninkatu 8), 00014 University of Helsinki, Helsinki, Finland. Phone: 358 443564604. Fax: 358 919125371. E-mail: heidi.kuula{at}helsinki.fi

{triangledown} Published ahead of print on 24 November 2008.

Editor: R. P. Morrison

Infection and Immunity, February 2009, p. 850-859, Vol. 77, No. 2
0019-9567/09/$08.00+0     doi:10.1128/IAI.00873-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



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