Bacterial infection increases periodontal bone loss in diabetic rats through enhanced apoptosis

American Journal of Pathology

Volumn 183, Issue 6, 2013, Pages 1928-1935

  Pacios, Sandra ^a   Andriankaja, Oelisoa ^a,b   Kang, Jun ^c   Alnammary, Maher ^a   Bae, Jason ^a   De Brito Bezerra, Beatriz ^d   Schreiner, Helen ^e   Fine, Daniel H ^e   Graves, Dana T ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

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

^d UNIVERSITY OF CAMPINAS   (Brazil)

^e RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CASPASE 3 INHIBITOR; MESSENGER RNA; OSTEOCALCIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ALVEOLAR BONE LOSS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL INFECTION; CELL COUNT; DIABETES MELLITUS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; NICK END LABELING; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; PERIODONTITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ALVEOLAR BONE LOSS; ANIMALS; APOPTOSIS; DIABETES COMPLICATIONS; DIABETES MELLITUS, EXPERIMENTAL; FEMALE; HUMANS; MALE; OSTEOCLASTS; PASTEURELLACEAE INFECTIONS; PERIODONTITIS; RATS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84888223748     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.08.017     Document Type: Article

References (47)

1. Z. Gong, and R.H. Muzumdar Pancreatic function, type 2 diabetes, and metabolism in aging Int J Endocrinol 2012 2012 320482
2. I.B. Lamster, E. Lalla, W.S. Borgnakke, and G.W. Taylor The relationship between oral health and diabetes mellitus J Am Dent Assoc 139 Suppl 2008 19S 24S
3. E. Lalla, and P.N. Papapanou Diabetes mellitus and periodontitis: a tale of two common interrelated diseases Nat Rev Endocrinol 7 2011 738 748
4. A. Bascones-Martinez, S. Arias-Herrera, E. Criado-Camara, J. Bascones-Ilundain, and C. Bascones-Ilundain Periodontal disease and diabetes Adv Exp Med Biol 771 2012 76 87
5. A.N. Gurav Periodontitis and insulin resistance: casual or causal relationship? Diabetes Metab J 36 2012 404 411
6. J. Otomo-Corgel, J.J. Pucher, M.P. Rethman, and M.A. Reynolds State of the science: chronic periodontitis and systemic health J Evid Based Dent Pract 12 Suppl 2012 20 28
7. H. Nassar, A. Kantarci, and T.E. van Dyke Diabetic periodontitis: a model for activated innate immunity and impaired resolution of inflammation Periodontol 2000 43 2007 233 244
8. Q. Li, M.S. Valerio, and K.L. Kirkwood MAPK usage in periodontal disease progression J Signal Transduct 2012 2012 308943
9. G.P. Garlet Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints J Dent Res 89 2010 1349 1363
10. D.T. Graves, J. Li, and D.L. Cochran Inflammation and uncoupling as mechanisms of periodontal bone loss J Dent Res 90 2011 143 153
11. M. Croft, C.A. Benedict, and C.F. Ware Clinical targeting of the TNF and TNFR superfamilies Nat Rev Drug Discov 12 2013 147 168
12. Y. Behl, P. Krothapalli, T. Desta, A. Dipiazza, S. Roy, and D.T. Graves Diabetes-enhanced tumor necrosis factor-{alpha} production promotes apoptosis and the loss of retinal microvascular cells in type 1 and type 2 models of diabetic retinopathy Am J Pathol 172 2008 1411 1418
13. S. Pacios, J. Kang, J. Galicia, K. Gluck, H. Patel, A. Ovaydi-Mandel, S. Petrov, F. Alawi, and D.T. Graves Diabetes aggravates periodontitis by limiting repair through enhanced inflammation FASEB J 26 2012 1423 1430
14. R.A. Kayal, M. Siqueira, J. Alblowi, J. McLean, N. Krothapalli, D. Faibish, T.A. Einhorn, L.C. Gerstenfeld, and D.T. Graves TNF-alpha mediates diabetes-enhanced chondrocyte apoptosis during fracture healing and stimulates chondrocyte apoptosis through FOXO1 J Bone Miner Res 25 2010 1604 1615
15. I. Chowdhury, B. Tharakan, and G.K. Bhat Caspases: an update Comp Biochem Physiol B Biochem Mol Biol 151 2008 10 27
16. H.A. Al-Mashat, S. Kandru, R. Liu, Y. Behl, T. Desta, and D.T. Graves Diabetes enhances mRNA levels of proapoptotic genes and caspase activity, which contribute to impaired healing Diabetes 55 2006 487 495
17. 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 278 2003 52901 52908
18. B. Ponugoti, G. Dong, and D.T. Graves Role of forkhead transcription factors in diabetes-induced oxidative stress Exp Diabetes Res 2012 2012 939751
19. B.A. Callus, and D.L. Vaux Caspase inhibitors: viral, cellular and chemical Cell Death Differ 14 2007 73 78
20. N.O. Concha, and S.S. Abdel-Meguid Controlling apoptosis by inhibition of caspases Curr Med Chem 9 2002 713 726
21. S.E. Wilson, R.R. Mohan, J. Hong, J. Lee, R. Choi, and J.J. Liu Apoptosis in the cornea in response to epithelial injury: significance to wound healing and dry eye Adv Exp Med Biol 506 2002 821 826
22. M.F. Siqueira, J. Li, L. Chehab, T. Desta, T. Chino, N. Krothpali, Y. Behl, M. Alikhani, J. Yang, C. Braasch, and D.T. Graves Impaired wound healing in mouse models of diabetes is mediated by TNF-alpha dysregulation and associated with enhanced activation of forkhead box O1 (FOXO1) Diabetologia 53 2010 378 388
23. H.C. Schreiner, K. Sinatra, J.B. Kaplan, D. Furgang, S.C. Kachlany, P.J. Planet, B.A. Perez, D.H. Figurski, and D.H. Fine Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model Proc Natl Acad Sci U S A 100 2003 7295 7300
24. D.L. Fu, Q.H. Jiang, F.M. He, G.L. Yang, and L. Liu Fluorescence microscopic analysis of bone osseointegration of strontium-substituted hydroxyapatite implants J Zhejiang Univ Sci B 13 2012 364 371
25. N.A. Sims, and J.H. Gooi Bone remodeling: multiple cellular interactions required for coupling of bone formation and resorption Semin Cell Dev Biol 19 2008 444 451
26. J. Kang, B. de Brito Bezerra, S. Pacios, O. Andriankaja, Y. Li, V. Tsiagbe, H. Schreiner, D.H. Fine, and D.T. Graves Aggregatibacter actinomycetemcomitans infection enhances apoptosis in vivo through a caspase-3-dependent mechanism in experimental periodontitis Infect Immun 80 2012 2247 2256
27. D.T. Graves, D. Fine, Y.T. Teng, T.E. Van Dyke, and G. Hajishengallis The use of rodent models to investigate host-bacteria interactions related to periodontal diseases J Clin Periodontol 35 2008 89 105
28. R. Liu, H.S. Bal, T. Desta, N. Krothapalli, M. Alyassi, Q. Luan, and D.T. Graves Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation J Dent Res 85 2006 510 514
29. A.M. Vincent, M. Brownlee, and J.W. Russell Oxidative stress and programmed cell death in diabetic neuropathy Ann N Y Acad Sci 959 2002 368 383
30. L. Cai, W. Li, G. Wang, L. Guo, Y. Jiang, and Y.J. Kang Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway Diabetes 51 2002 1938 1948
31. C.M. Zehendner, L. Librizzi, M. de Curtis, C.R. Kuhlmann, and H.J. Luhmann Caspase-3 contributes to ZO-1 and Cl-5 tight-junction disruption in rapid anoxic neurovascular unit damage PLoS One 6 2011 e16760
32. J.D. Beckham, K.D. Tuttle, and K.L. Tyler Caspase-3 activation is required for reovirus-induced encephalitis in vivo J Neurovirol 16 2010 306 317
33. E.L. Greer, and A. Brunet FOXO transcription factors in ageing and cancer Acta Physiol 192 2008 19 28
34. D.A. Scott, and J. Krauss Neutrophils in periodontal inflammation Front Oral Biol 15 2012 56 83
35. 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 168 2006 757 764
36. S.C. Kachlany Aggregatibacter actinomycetemcomitans leukotoxin: from threat to therapy J Dent Res 89 2010 561 570
37. B.C. Dickinson, C.E. Moffatt, D. Hagerty, S.E. Whitmore, T.A. Brown, D.T. Graves, and R.J. Lamont Interaction of oral bacteria with gingival epithelial cell multilayers Mol Oral Microbiol 26 2011 210 220
38. D. Graves, M. Oskoui, S. Volejnikova, G. Naguib, S. Cai, T. Desta, A. Kakouras, and Y. Jiang Tumor necrosis factor modulates fibroblast apoptosis, PMN recruitment, and osteoclast formation in response to P gingivalis infection J Dent Res 80 2001 1875 1879
39. M. Alikhani, C.M. Maclellan, M. Raptis, S. Vora, P.C. Trackman, and D.T. Graves Advanced glycation end products induce apoptosis in fibroblasts through activation of ROS, MAP kinases, and the FOXO1 transcription factor Am J Physiol Cell Physiol 292 2007 C850 C856
40. R.M. Chen, G.J. Wu, H.C. Chang, J.T. Chen, T.F. Chen, Y.L. Lin, and T.L. Chen 2,6-Diisopropylphenol protects osteoblasts from oxidative stress-induced apoptosis through suppression of caspase-3 activation Ann N Y Acad Sci 1042 2005 448 459
41. N. Okahashi, M. Koide, E. Jimi, T. Suda, and T. Nishihara Caspases (interleukin-1beta-converting enzyme family proteases) are involved in the regulation of the survival of osteoclasts Bone 23 1998 33 41
42. H.L. Benford, N.W. McGowan, M.H. Helfrich, M.E. Nuttall, and M.J. Rogers Visualization of bisphosphonate-induced caspase-3 activity in apoptotic osteoclasts in vitro Bone 28 2001 465 473
43. D. D'Lima, J. Hermida, S. Hashimoto, C. Colwell, and M. Lotz Caspase inhibitors reduce severity of cartilage lesions in experimental osteoarthritis Arthritis Rheum 54 2006 1814 1821
44. P.G. Bradford, K.V. Gerace, R.L. Roland, and B.G. Chrzan Estrogen regulation of apoptosis in osteoblasts Physiol Behav 99 2010 181 185
45. P.M. Bartold, A.H. du Bois, S. Gannon, D.R. Haynes, and R.S. Hirsch Antibacterial and immunomodulatory properties of azithromycin treatment implications for periodontitis Inflammopharmacology 21 2013 321 338
46. M. Mi, H. Jin, B. Wang, K. Yukata, T.J. Sheu, Q.H. Ke, P. Tong, H.J. Im, G. Xiao, and D. Chen Chondrocyte BMP2 signaling plays an essential role in bone fracture healing Gene 512 2013 211 218
47. O.M. Andriankaja, J. Galicia, G. Dong, W. Xiao, F. Alawi, and D.T. Graves Gene expression dynamics during diabetic periodontitis J Dent Res 91 2012 1160 1165