|
Sign In to gain access to subscriptions and/or personal tools.
|
Tumor Necrosis Factor Modulates Fibroblast Apoptosis, PMN Recruitment, and Osteoclast Formation in Response to P. gingivalis Infection
D.T. Graves
Department of Peri odontology and Oral Biology, dgraves{at}bu.edu
M. Oskoui
Department of Endodontics, Boston University School of Dental Medicine, Division of Oral Biology, 700 Albany Street, Rm. W-202, Boston, MA 02118
S. Voleinikova
Department of Peri odontology and Oral Biology
G. Naguib
Department of Peri odontology and Oral Biology
S. Cai
Department of Peri odontology and Oral Biology
T. Desta
Department of Peri odontology and Oral Biology
A. Kakouras
Department of Peri odontology and Oral Biology
Y. Jiang
Department of Endodontics, Boston University School of Dental Medicine, Division of Oral Biology, 700 Albany Street, Rm. W-202, Boston, MA 02118
P. gingivalis is an important oral pathogen, which has been closely linked to periodontal disease as well as lesions of endodontic origin. Both infections are associated with a decrease in fibroblast numbers, formation of an inflammatory infiltrate, and bone resorption. The goal of this study was to investigate the role that the host response plays in the capacity of P. gingivalis to stimulate fibroblast apoptosis, PMN recruitment, and osteoclastogenesis. This was accomplished by the use of an in vivo calvarial model in mice with targeted deletion of TNF receptors p55 and p75 and matched wild-type mice. The results indicate that P. gingivalis induces fibroblast apoptosis in vivo and establish for the first time that this involves the stimulation of a host response. Moreover, bacteria-stimulated PMN recruitment and osteoclastogenesis were also dependent upon the host response. The results suggest that much of the damage caused by P. gingivalis infection, including fibroblast apoptosis, at least under some circumstances, results from stimulation of the host response rather than the direct effect of bacterial products. Furthermore, this may represent a more general mechanism by which bacterial challenge induces apoptosis of matrix-producing cells through the induction of TNF.
Key Words: cytokine • bacteria • inflammation • cell death.
REFERENCES
- Assuma R., Oates T., Cochran D., Amar S., Graves D. (1998). IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immun 160:403-409.[Abstract/Free Full Text]
- Baker P., Dixon M., Evans R., Dufour L., Johnson E., Roopenian D. (1999). CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67:2804-2809.[Abstract/Free Full Text]
- Baumgartner J., Watkins B., Bae K., Xia T. (1999). Association of black-pigmented bacteria with endodontic infections. J Endod 25:413-415.[Medline]
[Order article via Infotrieve]
- Boyce B., Aufdemorte T., Garrett I., Yates A., Mundy G. (1989). Effects of interleukin-1 on bone turnover in normal mice. Endocrinology 125:1142-1150.[Abstract/Free Full Text]
- Chen CP, Hertzberg M., Jiang Y., Graves DT (1999). Interleukin-1 and tumor necrosis factor receptor signaling is not required for bacteria-induced osteoclastogenesis and bone loss but is essential for protecting the host from a mixed anaerobic infection. Am J Pathol 155:2145-2152.[Medline]
[Order article via Infotrieve]
- Chiang C., Kyritsis G., Graves D., Amar S. ( 1999). Interleukin-1 and tumor necrosis factor activities partially account for calvarial bone resorption induced by local injection of lipopolysaccharide. Infect Immun 67:4231-4236.[Abstract/Free Full Text]
- Denecker G., Vercammen D., Declercq W., Vandenabeele P. (2001). Apoptotic and necrotic cell death induced by death domain receptors. Cell Mol Life Sci 58:356-370.[CrossRef][Medline]
[Order article via Infotrieve]
- Gamonal J., Bascones A., Acevedo A., Blanco E., Silva A. (2001). Apoptosis in chronic adult periodontitis analyzed by in situ DNA breaks, electron microscopy and immunohistochemistry. J Periodontol 72:517-525.[CrossRef][Medline]
[Order article via Infotrieve]
- Graves DT (1999). The potential role of chemokines and inflammatory cytokines in periodontal disease progression. Clin Infect Dis 28:482-490.[Medline]
[Order article via Infotrieve]
- Graves D., Jiang Y., Genco C. (2000). Periodontal disease: bacterial virulence factors, host response and impact on systemic health. Curr Opin Infect Dis 13:227-232.[Medline]
[Order article via Infotrieve]
- Holt S., Ebersole J., Felton J., Brunsvold M., Kornman K. (1988). Implantation of Bacteroides gingivalis in non-human primates initiates progression of periodontitis. Science 239:55-57.[Abstract/Free Full Text]
- Isogai E., Isogal H., Kimura K., Fujii N., Takagi S., Hirose K., et al. (1996). In vivo induction of apoptosis and immune responses in mice by administration of lipopolysaccharide from Porphyromonas gingivalis. Infect Immun 64:1461-1466.[Abstract]
- Jiang Y., Magli L., Russo M. (1999). Bacterium-dependent induction of cytokines in mononuclear cells and their pathologic consequences in vivo. Infect Immun 67:2125-2130.[Abstract/Free Full Text]
- Kobayashi K., Takahashi N., Jimi E., Udagawa N., Takami M., Kotake S., et al. (2000). Tumor necrosis factory alpha stimulates osteoclast differentiation mechanism independent of the ODF/RANKL-RANK interaction. J Exp Med 191:275-286.[Abstract/Free Full Text]
- Kollias G., Douni E., Kassiotis G., Kontoyiannis D. (1999). The function of tumour necrosis factor and receptors in models of multi-organ inflammation, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Ann Rheum Dis 58:132-139.
- Koulouri 0, Lappin DF, Radvar M., Kinane DF (1999). Cell division, synthetic capacity and apoptosis in periodontal lesions analyzed by in situ hybridization and immunohistochemistry. J Clin Periodontol 26:552-559.[CrossRef][Medline]
[Order article via Infotrieve]
- Lacey DL, Timms E., Tan HL, Kelley MJ, Dunstan CR, Burgess T., et al. (1998). Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176.[CrossRef][Medline]
[Order article via Infotrieve]
- Matsuda T., Saito H., Inoue T., Fukatsu K., Lin M., Han I., et al. (1999). Ratio of bacteria to polymorphonuclear neutrophils (PMNs) determines PMN fate. Shock 12:365-372.[Medline]
[Order article via Infotrieve]
- Page RC ( 1991). The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodontal Res 26:230-242.[CrossRef][Medline]
[Order article via Infotrieve]
- Perera L., Waldmann TA (1998). Activation of human monocytes induces differential resistance to apoptosis with rapid down regulation of caspase-8/FLICE. Proc Natl Acad Sci USA 95:14308-14313.[Abstract/Free Full Text]
- Peschon J., Torrance D., Stocking K., Glaccum M., Otten C., Willis C., et al. (1998). TNF receptor-deficient mice reveal divergent roles for p55 and p75 in several models of inflammation. J Immunol 160:943-942.[Abstract/Free Full Text]
- Preshaw P., Schifferle R., Walters J. (1999). Porphyromonas gingivalis lipopolysaccharide delays human polymorphonuclear leukocyte apoptosis in vitro. J Periodontal Res 34:197-202.[CrossRef][Medline]
[Order article via Infotrieve]
- Rothe J., Lesslauer W., Lotscher H., Lang Y., Koebel P., Kontgen F., et al. (1993). Mice lacking the tumour necrosis factor receptor I are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364:798-802.[CrossRef][Medline]
[Order article via Infotrieve]
- Seltzer S., Farber P. (1994). Microbiologic factors in endodontology. Oral Surg Oral Med Oral Pathol 78:634-645.[CrossRef][Medline]
[Order article via Infotrieve]
- Socransky S., Haffajee A., Cugini M., Smith C., Kent RJ ( 1998). Microbial complexes in subgingival plaque. J Clin Periodontol 25:134-144.[CrossRef][Medline]
[Order article via Infotrieve]
- Teng Y., Nguyen H., Gao X., Kong Y., Gorczynski R., Singh B., et al. (2000). Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J Clin Invest 106:R59-67.[Medline]
[Order article via Infotrieve]
- Tonetti MS, Cortellini D., Lang NP ( 1998). In situ detection of apoptosis at sites of chronic bacterially induced inflammation in human gingiva. Infect Immun 66:5190-5195.[Abstract/Free Full Text]
- Uy HL, Mundy GR, Boyce BF, Story BM, Dunstan CR, Yin JJ, et al. (1997). Tumor necrosis factor enhances parathyroid hormone-related protein-induced hypercalcemia and bone resorption without inhibiting bone formation in vivo. Cancer Res 57:3194-3199.[Abstract/Free Full Text]
- Wang C., Tani-Ishii N., Stashenko P. (1997). Bone-resorptive cytokine gene expression in periapical lesions in the rat. Oral Microbiol Immunol 12:65-71.[Medline]
[Order article via Infotrieve]
- Williams R. (1999). Non-steroidal anti-inflammatory drugs for altering periodontal bone loss. J Dent Res 78:638-642.
- Williams RC, Offenbacher S. (2000). Periodontal medicine: the emergence of a new branch of periodontology. Periodontology 23:9-12.[Medline]
[Order article via Infotrieve]
- Zappa U., Reinking-Zappa M., Graf H., Chase D. (1992). Cell populations associated with active probing attachment loss. J Periodontol 63:748-752.[Medline]
[Order article via Infotrieve]
- Zhao Y., Lajoie G., Zhang H., Chiu B., Payne U., Inman R. (2000). Tumor necrosis factor receptor p55-deficient mice respond to acute Yersinia enterocolitica infection with less apoptosis and more effective host resistance. Infect Immun 68:1243-1251.[Abstract/Free Full Text]
- Zubery Y., Dunstan C., Story B., Kesavalu L., Ebersole J., Holt S., et al. (1998). Bone resorption caused by three periodontal pathogens in vivo in mice is mediated in part by prostaglandin. Infect Immun 66:4158-4162.[Abstract/Free Full Text]
Journal of Dental Research, Vol. 80, No. 10,
1875-1879 (2001)
DOI: 10.1177/00220345010800100301
 CiteULike  Complore  Connotea  Del.icio.us  Digg  Reddit  Technorati  Twitter What's this?
This article has been cited by other articles:
|
|
|
|
 
A. Ghosh, J. Y. Park, C. Fenno, and Y. L. Kapila
Porphyromonas gingivalis, Gamma Interferon, and a Proapoptotic Fibronectin Matrix Form a Synergistic Trio That Induces c-Jun N-Terminal Kinase 1-Mediated Nitric Oxide Generation and Cell Death
Infect. Immun.,
December 1, 2008;
76(12):
5514 - 5523.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Yang, M. F. Siqueira, Y. Behl, M. Alikhani, and D. T. Graves
The transcription factor ST18 regulates proapoptotic and proinflammatory gene expression in fibroblasts
FASEB J,
November 1, 2008;
22(11):
3956 - 3967.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. W. Leone, H. Bokhadhoor, D. Kuo, T. Desta, J. Yang, M. F. Siqueira, S. Amar, and D. T. Graves
Immunization Enhances Inflammation and Tissue Destruction in Response to Porphyromonas gingivalis
Infect. Immun.,
April 1, 2006;
74(4):
2286 - 2292.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Liu, H. S. Bal, T. Desta, Y. Behl, and D. T. Graves
Tumor Necrosis Factor-{alpha} Mediates Diabetes-Enhanced Apoptosis of Matrix-Producing Cells and Impairs Diabetic Healing
Am. J. Pathol.,
March 1, 2006;
168(3):
757 - 764.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Alikhani, Z. Alikhani, and D. T. Graves
FOXO1 Functions as a Master Switch That Regulates Gene Expression Necessary for Tumor Necrosis Factor-induced Fibroblast Apoptosis
J. Biol. Chem.,
April 1, 2005;
280(13):
12096 - 12102.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Mezyk-Kopec, M. Bzowska, J. Potempa, M. Bzowska, N. Jura, A. Sroka, R. A. Black, and J. Bereta
Inactivation of Membrane Tumor Necrosis Factor Alpha by Gingipains from Porphyromonas gingivalis
Infect. Immun.,
March 1, 2005;
73(3):
1506 - 1514.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. M. Sheets, J. Potempa, J. Travis, C. A. Casiano, and H. M. Fletcher
Gingipains from Porphyromonas gingivalis W83 Induce Cell Adhesion Molecule Cleavage and Apoptosis in Endothelial Cells
Infect. Immun.,
March 1, 2005;
73(3):
1543 - 1552.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. T. Graves, G. Naguib, Huafei Lu, T. Desta, and S. Amar
Porphyromonas gingivalis fimbriae are pro-inflammatory but do not play a prominent role in the innate immune response to P. gingivalis
Innate Immunity,
February 1, 2005;
11(1):
13 - 18.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R. Liu, T. Desta, H. He, and D. T. Graves
Diabetes Alters the Response to Bacteria by Enhancing Fibroblast Apoptosis
Endocrinology,
June 1, 2004;
145(6):
2997 - 3003.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Alikhani, Z. Alikhani, H. He, R. Liu, B. I. Popek, and D. T. Graves
Lipopolysaccharides Indirectly Stimulate Apoptosis and Global Induction of Apoptotic Genes in Fibroblasts
J. Biol. Chem.,
December 26, 2003;
278(52):
52901 - 52908.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
