Porphyromonas gingivalis suppresses differentiation and increases apoptosis of osteoblasts from New Zealand obese mice

Journal of Periodontology

Volumn 86, Issue 9, 2015, Pages 1095-1102

  Dittmann, Cora ^a   Doueiri, Salim ^a   Kluge, Reinhart ^b   Dommisch, Henrik ^a   Gaber, Timo ^a   Pischon, Nicole ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

Author keywords

Alveolar bone loss; Metabolic syndrome X; Mice; Obesity; Osteoblasts; Porphyromonas gingivalis

Indexed keywords

CASP3 PROTEIN, MOUSE; CASPASE 3; COLLAGEN TYPE 1; COLLAGEN TYPE I, ALPHA 1 CHAIN; GLYCOPROTEIN; LACTATE DEHYDROGENASE; NEPHROCALCIN; OSTEOCALCIN; RUNX2 PROTEIN, RAT; TRANSCRIPTION FACTOR RUNX2;

ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL CYCLE G2 PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPARATIVE STUDY; DISEASE MODEL; DOWN REGULATION; FEMALE; INBRED MOUSE STRAIN; MALE; METABOLIC SYNDROME X; MICROBIOLOGY; MOUSE; MOUSE MUTANT; OSTEOBLAST; PERIODONTITIS; PHYSIOLOGY; PORPHYROMONAS GINGIVALIS; TIME FACTOR;

ANIMALS; APOPTOSIS; CASPASE 3; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE I; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; G2 PHASE; GLYCOPROTEINS; L-LACTATE DEHYDROGENASE; MALE; METABOLIC SYNDROME X; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, OBESE; OSTEOBLASTS; OSTEOCALCIN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; TIME FACTORS;

EID: 84940398015     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2015.150032     Document Type: Article

References (51)

1. Wood N, Johnson RB, Streckfus CF. Comparison of body composition and periodontal disease using nutritional assessment techniques: Third National Health and Nutrition Examination Survey (NHANES III). J Clin Periodontol 2003;30:321-327.
2. Genco RJ, Grossi SG, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol 2005; 76(Suppl. 11):2075-2084.
3. Saito T, Shimazaki Y, Sakamoto M. Obesity and periodontitis. N Engl J Med 1998;339:482-483.
4. Linden GJ, Herzberg MC; working group 4 of the joint EFP/AAPworkshop. Periodontitis and systemic diseases: A record of discussions of working group 4 of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Periodontol 2013;84(Suppl. 4):S20-S23.
5. Nibali L, Tatarakis N, Needleman I, et al. Clinical review: Association between metabolic syndrome and periodontitis: A systematic review and meta-analysis. J Clin Endocrinol Metab 2013;98:913-920.
6. Pischon N, Heng N, Bernimoulin JP, Kleber BM, Willich SN, Pischon T. Obesity, inflammation, and periodontal disease. J Dent Res 2007;86:400-409.
7. Montebugnoli L, Servidio D, Miaton RA, et al. Periodontal health improves systemic inflammatory and haemostatic status in subjects with coronary heart disease. J Clin Periodontol 2005;32:188-192.
8. Gurav AN. The association of periodontitis and metabolic syndrome. Dent Res J (Isfahan) 2014;11:1-10.
9. Forner L, Larsen T, Kilian M, Holmstrup P. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol 2006;33:401-407.
10. Waghmare AS, Vhanmane PB, Savitha B, Chawla RL, Bagde HS. Bacteremia following scaling and root planing: A clinico-microbiological study. J Indian Soc Periodontol 2013;17:725-730.
11. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet 2005;365:1415-1428.
12. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive summary of the third report of the National Cholesterol Education Program (NCEP) Expert Panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 2001;285: 2486-2497.
13. Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic syndrome among US adults: Findings from the third National Health and Nutrition Examination Survey. JAMA 2002;287:356-359.
14. Tu YK, D'Aiuto F, Lin HJ, Chen YW, Chien KL. Relationship between metabolic syndrome and diagnoses of periodontal diseases among participants in a large Taiwanese cohort. J Clin Periodontol 2013;40:994-1000.
15. Mottillo S, Filion KB, Genest J, et al. The metabolic syndrome and cardiovascular risk: A systematic review and meta-analysis. J Am Coll Cardiol 2010;56:1113-1132.
16. Ohnishi T, Bandow K, Kakimoto K, Machigashira M, Matsuyama T, Matsuguchi T. Oxidative stress causes alveolar bone loss in metabolic syndrome model mice with type 2 diabetes. J Periodontal Res 2009;44:43-51.
17. Xu F, Du Y, Hang S, Chen A, Guo F, Xu T. Adipocytes regulate the bonemarrowmicroenvironment in a mouse model of obesity. Mol Med Rep 2013;8:823-828.
18. Wang D, Haile A, Jones LC. Dexamethasone-induced lipolysis increases the adverse effect of adipocytes on osteoblasts using cells derived from human mesenchymal stem cells. Bone 2013;53:520-530.
19. Li H, Yang H, Ding Y, et al. Experimental periodontitis induced by Porphyromonas gingivalis does not alter the onset or severity of diabetes in mice. J Periodontal Res 2013;48:582-590.
20. He H, Liu R, Desta T, Leone C, Gerstenfeld LC, Graves DT. Diabetes causes decreased osteoclastogenesis, reduced bone formation, and enhanced apoptosis of osteoblastic cells in bacteria stimulated bone loss. Endocrinology 2004;145:447-452.
21. Fu YW, He HB, Ou JG. Osteoblast apoptosis in experimental diabetic periodontitis in rats (in Chinese). Hua Xi Kou Qiang Yi Xue Za Zhi 2009;27:252-255, 259.
22. Kluge R, Scherneck S, Schürmann A, Joost HG. Pathophysiology and genetics of obesity and diabetes in the New Zealand Obese mouse: A model of the human metabolic syndrome. Methods Mol Biol 2012; 933:59-73.
23. Bielschowsky M, Goodall CM. Origin of inbred NZ mouse strains. Cancer Res 1970;30:834-836.
24. Bakker AD, Klein-Nulend J. Osteoblast isolation from murine calvaria and long bones. Methods Mol Biol 2012;816:19-29.
25. Pischon N, Mäki JM, Weisshaupt P, et al. Lysyl oxidase (lox) gene deficiency affects osteoblastic phenotype. Calcif Tissue Int 2009;85:119-126.
26. Röhner E, Hoff P, Matziolis G, et al. The impact of Porphyromonas gingivalis lipids on apoptosis of primary human chondrocytes. Connect Tissue Res 2012; 53:327-333.
27. Genco RJ, Borgnakke WS. Risk factors for periodontal disease. Periodontol 2000 2013;62:59-94.
28. Falagas ME, Kompoti M. Obesity and infection. Lancet Infect Dis 2006;6:438-446.
29. Kopelman P. Health risks associated with overweight and obesity. Obes Rev 2007;8(Suppl. 1):13-17.
30. Lee KS, Kim EK, Kim JW, et al. The relationship between metabolic conditions and prevalence of periodontal disease in rural Korean elderly. Arch Gerontol Geriatr 2014;58:125-129.
31. Nesbitt MJ, Reynolds MA, Shiau H, Choe K, Simonsick EM, Ferrucci L. Association of periodontitis and metabolic syndrome in the Baltimore Longitudinal Study of Aging. Aging Clin Exp Res 2010;22:238-242.
32. Morita T, Ogawa Y, Takada K, et al. Association between periodontal disease and metabolic syndrome. J Public Health Dent 2009;69:248-253.
33. Borges PK, Gimeno SG, Tomita NE, Ferreira SR. Prevalence and characteristics associated with metabolic syndrome in Japanese-Brazilians with and without periodontal disease (in Portuguese). Cad Saude Publica 2007;23:657-668.
34. Zhang W, Ju J, Rigney T, Tribble G. Integrin a5b1-fimbriae binding and actin rearrangement are essential for Porphyromonas gingivalis invasion of osteoblasts and subsequent activation of the JNK pathway. BMC Microbiol 2013;13:5-15.
35. Zhang W, Swearingen EB, Ju J, Rigney T, Tribble GD. Porphyromonas gingivalis invades osteoblasts and inhibits bone formation.Microbes Infect 2010;12:838-845.
36. Le XK, Laflamme C, Rouabhia M. Porphyromonas gingivalis decreases osteoblast proliferation through IL-6-RANKL/OPG and MMP-9/TIMPs pathways. Indian J Dent Res 2009;20:141-149.
37. Kuboniwa M, Hasegawa Y, Mao S, et al. P. gingivalis accelerates gingival epithelial cell progression through the cell cycle. Microbes Infect 2008;10:122-128.
38. Kato T, Tsuda T, Inaba H, et al. Porphyromonas gingivalis gingipains cause G(1) arrest in osteoblastic/ stromal cells. Oral Microbiol Immunol 2008;23: 158-164.
39. Pischon N, Röhner E, Hocke A, et al. Effects of Porphyromonas gingivalis on cell cycle progression and apoptosis of primary human chondrocytes. Ann Rheum Dis 2009;68:1902-1907.
40. Liu L, Zhu Y, Xu Y, Reiter RJ. Melatonin delays cell proliferation by inducing G1 and G2/M phase arrest in a human osteoblastic cell line hFOB 1.19. J Pineal Res 2011;50:222-231.
41. He J, Qiu W, Zhang Z, Wang Z, Zhang X, He Y. Effects of irradiation on growth and differentiation-related gene expression in osteoblasts. J Craniofac Surg 2011;22: 1635-1640.
42. Baus F, Gire V, Fisher D, Piette J, Dulic V. Permanent cell cycle exit in G2 phase after DNA damage in normal human fibroblasts. EMBO J 2003;22:3992-4002.
43. Nakhjiri SF, Park Y, Yilmaz O, et al. Inhibition of epithelial cell apoptosis by Porphyromonas gingivalis. FEMS Microbiol Lett 2001;200:145-149.
44. Kinane JA, Benakanakere MR, Zhao J, Hosur KB, Kinane DF. Porphyromonas gingivalis influences actin degradation within epithelial cells during invasion and apoptosis. Cell Microbiol 2012;14:1085-1096.
45. Urnowey S, Ansai T, Bitko V, Nakayama K, Takehara T, Barik S. Temporal activation of anti-and proapoptotic factors in human gingival fibroblasts infected with the periodontal pathogen, Porphyromonas gingivalis: Potential role of bacterial proteases in host signalling. BMC Microbiol 2006;6:26-41.
46. Zahlten J, Riep B, Nichols FC, et al. Porphyromonas gingivalis dihydroceramides induce apoptosis in endothelial cells. J Dent Res 2007;86:635-640.
47. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770-776.
48. Zhang J, Fu Y, Song X, Liang M. Expression of integrin alpha5 and beta1 in osteoblast in the process of gingipains-induced apoptosis (in Chinese). Chin J Stomatol 2013;48:653-659.
49. Thanakun S, Watanabe H, Thaweboon S, Izumi Y. Association of untreated metabolic syndrome with moderate to severe periodontitis in Thai population. J Periodontol 2014;85:1502-1514.
50. Blair HC, Zaidi M, Schlesinger PH. Mechanisms balancing skeletal matrix synthesis and degradation. Biochem J 2002;364:329-341.
51. Ikeda T, Nomura S, Yamaguchi A, Suda T, Yoshiki S. In situ hybridization of bone matrix proteins in undecalcified adult rat bone sections. J Histochem Cytochem 1992;40:1079-1088.