Diabetes aggravates periodontitis by limiting repair through enhanced inflammation

FASEB Journal

Volumn 26, Issue 4, 2012, Pages 1423-1430

  Pacios, Sandra ^a,b   Kang, Jun ^a,c   Galicia, Johnah ^a   Gluck, Kenneth ^d   Patel, Hemal ^a   Ovaydi Mandel, Amy ^d   Petrov, Sophia ^d   Alawi, Faizan ^a   Graves, Dana T ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITAT INTERNACIONAL DE CATALUNYA   (Spain)

^c PEKING UNIVERSITY SCHOOL AND HOSPITAL OF STOMATOLOGY   (China)

^d RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Bone formation; Cytokine; Growth factor; Inhibitor

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; FIBROBLAST GROWTH FACTOR 2; GAMMA INTERFERON; INTERLEUKIN 1BETA; MESSENGER RNA; PEGSUNERCEPT; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GOTO KAKIZAKI RAT; HISTOPATHOLOGY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLASTOGENESIS; OSTEOID; OSTEOLYSIS; PERIODONTITIS; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 6; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; FIBROBLAST GROWTH FACTOR 2; INFLAMMATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKOCYTES; MALE; OSTEOBLASTS; OSTEOCLASTS; PERIODONTITIS; PROLIFERATING CELL NUCLEAR ANTIGEN; RATS; RATS, INBRED STRAINS; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA; RATTUS;

EID: 84860898192     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-196279     Document Type: Article

References (32)

1. Graves, D. T., and Kayal, R. A. (2008) Diabetic complications and dysregulated innate immunity. Front. Biosci. 13, 1227-1239 (Pubitemid 351594707)
2. Lamster, I. B., Lalla, E., Borgnakke, W. S., and Taylor, G. W. (2008) The relationship between oral health and diabetes mellitus. J. Am. Dent. Assoc. 139(Suppl.), 19S-24S
3. Kumar, P. S., Leys, E. J., Bryk, J. M., Martinez, F. J., Moeschberger, M. L., and Griffen, A. L. (2006) Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. J. Clin. Microbiol. 44, 3665-3673 (Pubitemid 46768783)
4. Graves, D. T., Li, J., and Cochran, D. L. (2010) Inflammation and uncoupling as mechanisms of periodontal bone loss. J. Dent. Res. 90, 143-153
5. Williams, R., Jeffcoat, M., Kaplan, M., Goldhaber, P., Johnson, H., and Wechter, W. (1985) Flurbiprofen: a potent inhibitor of alveolar bone resorption in beagles. Science 227, 640-642 (Pubitemid 15157484)
6. Assuma, R., Oates, T., Cochran, D., Amar, S., and Graves, D. (1998) IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J. Immun. 160, 403-409 (Pubitemid 28116755)
7. Yu, H., Li, Q., Herbert, B., Zinna, R., Martin, K., Junior, C. R., and Kirkwood, K. L. (2011) Anti-inflammatory effect of MAPK phosphatase-1 local gene transfer in inflammatory bone loss. Gene Ther. 18, 344-353
8. Hasturk, H., Kantarci, A., Ohira, T., Arita, M., Ebrahimi, N., Chiang, N., Petasis, N. A., Levy, B. D., Serhan, C. N., and Van Dyke, T. E. (2006) RvE1 protects from local inflammation and osteoclast- mediated bone destruction in periodontitis. FASEB J. 20, 401-403 (Pubitemid 46671185)
9. Garlet, G. P. (2010) Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. J. Dent. Res. 89, 1349-1363
10. Baker, P., Dixon, M., Evans, R., Dufour, L., Johnson, E., and 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 (Pubitemid 29244693)
11. Delima, A., Spyros, K., Amar, S., and Graves, D. T. (2002) Inflammation and tissue loss caused by periodontal pathogens is reduced by IL-1 antagonists. J. Infect. Dis. 186, 511-516 (Pubitemid 34876260)
12. Teng, Y., Nguyen, H., Gao, X., Kong, Y., Gorczynski, R., Singh, B., Ellen, R., and Penninger, J. (2000) Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J. Clin. Invest. 106, R59-67
13. Han, X., Kawai, T., Eastcott, J. W., and Taubman, M. A. (2006) Bacterial-responsive B lymphocytes induce periodontal bone resorption. J. Immunol. 176, 625-631 (Pubitemid 43023311)
14. Naguib, G., Al-Mashat, H., Desta, T., and Graves, D. (2004) Diabetes prolongs the inflammatory response to a bacterial stimulus through cytokine dysregulation. J. Invest. Dermatol. 123, 87-92 (Pubitemid 38833468)
15. Spite, M., and Serhan, C. N. (2010) Novel lipid mediators promote resolution of acute inflammation: impact of aspirin and statins. Circ. Res. 107, 1170-1184
16. Salvi, G., Collins, J., Yalda, B., Arnold, R., Lang, N., and Offenbacher, S. (1997) Monocytic TNFalpha secretion patterns in IDDM patients with periodontal diseases. J. Clin. Periodontol. 24, 8-16 (Pubitemid 127731485)
17. Graves, D., Oskoui, M., Volejnikova, S., Naguib, G., Cai, S., Desta, T., Kakouras, A., and Jiang, Y. (2001) Tumor necrosis factor modulates fibroblast apoptosis, PMN recruitment, and osteoclast formation in response to P. gingivalis infection. J. Dent. Res. 80, 1875-1879 (Pubitemid 33038053)
18. Garlet, G. P., Cardoso, C. R., Campanelli, A. P., Ferreira, B. R., Avila-Campos, M. J., Cunha, F. Q., and Silva, J. S. (2007) The dual role of p55 tumour necrosis factor-alpha receptor in Actinobacillus actinomycetemcomitans- induced experimental periodontitis: host protection and tissue destruction. Clin. Exp. Immunol. 147, 128-138 (Pubitemid 44915564)
19. Lalla, E., Lamster, I. B., Feit, M., Huang, L., Spessot, A., Qu, W., Kislinger, T., Lu, Y., Stern, D. M., and Schmidt, A. M. (2000) Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J. Clin. Invest. 105, 1117-1124 (Pubitemid 30217696)
20. Rovin, S., Costich, E. R., and Gordon, H. A. (1966) The influence of bacteria and irritation in the initiation of periodontal disease in germfree and conventional rats. J. Periodontal Res. 1, 193-204
21. Liu, R., Bal, H. S., Desta, T., Krothapalli, N., Alyassi, M., Luan, Q., and Graves, D. T. (2006) Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation. J. Dent. Res. 85, 510-514 (Pubitemid 43945487)
22. Fantuzzi, F., Del Giglio, M., Gisondi, P., and Girolomoni, G. (2008) Targeting tumor necrosis factor alpha in psoriasis and psoriatic arthritis. Expert Opin. Ther. Targets 12, 1085-1096
23. Miheller, P., Muzes, G., Racz, K., Blazovits, A., Lakatos, P., Herszenyi, L., and Tulassay, Z. (2007) Changes of OPG and RANKL concentrations in Crohn's disease after infliximab therapy. Inflamm. Bowel Dis. 13, 1379-1384 (Pubitemid 350206849)
24. Pacifici, R. (2010) The immune system and bone. Arch. Biochem. Biophys. 503, 41-53
25. Gilbert, L., He, X., Farmer, P., Boden, S., Kozlowski, M., Rubin, J., and Nanes, M. S. (2000) Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology 141, 3956-3964
26. Lencel, P., Delplace, S., Hardouin, P., and Magne, D. (2011) TNF-alpha stimulates alkaline phosphatase and mineralization through PPARgamma inhibition in human osteoblasts. Bone 48, 242-249
27. Guo, R., Yamashita, M., Zhang, Q., Zhou, Q., Chen, D., Reynolds, D. G., Awad, H. A., Yanoso, L., Zhao, L., Schwarz, E. M., Zhang, Y. E., Boyce, B. F., and Xing, L. (2008) Ubiquitin ligase Smurf1 mediates tumor necrosis factor-induced systemic bone loss by promoting proteasomal degradation of bone morphogenetic signaling proteins. J. Biol. Chem. 283, 23084-23092
28. Chang, J., Wang, Z., Tang, E., Fan, Z., McCauley, L., Franceschi, R., Guan, K., Krebsbach, P. H., and Wang, C. Y. (2009) Inhibition of osteoblastic bone formation by nuclear factorkappaB. Nat. Med. 15, 682-689
29. Hasturk, H., Kantarci, A., Goguet-Surmenian, E., Blackwood, A., Andry, C., Serhan, C. N., and Van Dyke, T. E. (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J. Immunol. 179, 7021-7029
30. Havell, E. A. (1989) Evidence that tumor necrosis factor has an important role in antibacterial resistance. J. Immunol. 143, 2894-2899
31. Kim, E. Y., Priatel, J. J., Teh, S. J., and Teh, H. S. (2006) TNF receptor type 2 (p75) functions as a costimulator for antigendriven T cell responses in vivo. J. Immunol. 176, 1026-1035 (Pubitemid 43099703)
32. Graves, D. T., Naguib, G., Lu, H., Leone, C., Hsue, H., and Krall, E. (2005) Inflammation is more persistent in Type 1 diabetic mice. J. Dent. Res. 84, 324-328 (Pubitemid 43822013)