NOD2 contributes to porphyromonas gingivalis-induced bone resorption

Journal of Dental Research

Volumn 93, Issue 11, 2014, Pages 1155-1162

  Prates, T P ^a   Taira, T M ^a   Holanda, M C ^a   Bignardi, L A ^a   Salvador, S L ^a   Zamboni, D S ^a   Cunha, F Q ^a   Fukada, S Y ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

cathepsin K; NOD receptors; oral infection; osteoclasts; osteoimmunology; periodontitis

Indexed keywords

CARD15 PROTEIN, MOUSE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CATHEPSIN K; COLONY STIMULATING FACTOR 1; CTSK PROTEIN, MOUSE; GELATINASE B; IMMUNOLOGICAL ADJUVANT; MMP9 PROTEIN, MOUSE; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; TNFRSF11B PROTEIN, MOUSE; TNFSF11 PROTEIN, MOUSE;

AGONISTS; ALVEOLAR BONE LOSS; ANIMAL; C57BL MOUSE; CELL COUNT; CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; COMPARATIVE STUDY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GINGIVA; HEMATOPOIETIC STEM CELL; KNOCKOUT MOUSE; MALE; MICROBIOLOGY; MOUSE; OSTEOCLAST; PATHOLOGY; PHYSIOLOGY; PORPHYROMONAS GINGIVALIS; TIME;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ADJUVANTS, IMMUNOLOGIC; ALVEOLAR BONE LOSS; ANIMALS; CATHEPSIN K; CELL COUNT; CELL DIFFERENTIATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GINGIVA; HEMATOPOIETIC STEM CELLS; MACROPHAGE COLONY-STIMULATING FACTOR; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NOD2 SIGNALING ADAPTOR PROTEIN; OSTEOCLASTS; OSTEOPROTEGERIN; PORPHYROMONAS GINGIVALIS; RANK LIGAND; TIME FACTORS;

EID: 84910065963     PISSN: 00220345     EISSN: 15440591     Source Type: Journal    
DOI: 10.1177/0022034514551770     Document Type: Article

References (42)

1. Baker PJ. The role of immune responses in bone loss during periodontal disease. Microbes Infect. 2000 ; 2: 1181-1192
2. Belibasakis GN, Johansson A, Wang Y, Chen C, Kalfas S, Lerner UH. The cytolethal distending toxin induces receptor activator of NF-kappaB ligand expression in human gingival fibroblasts and periodontal ligament cells. Infect Immun. 2005 ; 73: 342-51
3. Belibasakis GN, Bostanci N, Hashim A, Johansson A, Aduse-Opoku J, Curtis MA, et al. Regulation of RANKL and OPG gene expression in human gingival fibroblasts and periodontal ligament cells by Porphyromonas gingivalis: a putative role of the Arg-gingipain. Microb Pathog. 2007 ; 43: 46-53
4. Belibasakis GN, Guggenheim B, Bostanci N. Down-regulation of NLRP3 inflammasome in gingival fibroblasts by subgingival biofilms: involvement of Porphyromonas gingivalis. Innate Immun. 2013 ; 19: 3-9
5. Bostanci N, Meier A, Guggenheim B, Belibasakis GN. Regulation of NLRP3 and AIM2 inflammasome gene expression levels in gingival fibroblasts by oral biofilms. Cell Immunol. 2011 ; 270: 88-93
6. Cantley MD, Haynes DR, Marino V, Bartold PM. Pre-existing periodontitis exacerbates experimental arthritis in a mouse model. J Clin Periodontol. 2011 ; 38: 532-541
7. Chauhan VS, Marriott I. Differential roles for NOD2 in osteoblast inflammatory immune responses to bacterial pathogens of bone tissue. J Med Microbiol. 2010 ; 59 (Pt 7). 755-62
8. Chung WO, An JY, Yin L, Hacker BM, Rohani MG, Dommisch H, et al. Interplay of protease-activated receptors and NOD pattern recognition receptors in epithelial innate immune responses to bacteria. Immunol Lett. 2010 ; 131: 113-119
9. Delaisse JM, Andersen TL, Engsig MT, Henriksen K, Troen T, Blavier L. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc Res Tech. 2003 ; 61: 504-513
10. Everts V, Delaisse JM, Korper W, Niehof A, Vaes G, Beertsen W. Degradation of collagen in the bone-resorbing compartment underlying the osteoclast involves both cysteine-proteinases and matrix metalloproteinases. J Cell Physiol. 1992 ; 150: 221-231
11. Garg G, Pradeep AR, Thorat MK. Effect of nonsurgical periodontal therapy on crevicular fluid levels of Cathepsin K in periodontitis. Arch Oral Biol. 2009 ; 54: 1046-1051
12. Garlet GP, Cardoso CR, Silva TA, Ferreira BR, Avila-Campos MJ, Cunha FQ, et al. Cytokine pattern determines the progression of experimental periodontal disease induced by Actinobacillus actinomycetemcomitans through the modulation of MMPs, RANKL, and their physiological inhibitors. Oral Microbiol Immunol. 2006 ; 21: 12-20
13. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem. 2003 ; 278: 8869-8872
14. Gowen M, Lazner F, Dodds R, Kapadia R, Feild J, Tavaria M, et al. Cathepsin K knockout mice develop osteopetrosis due to a deficit in matrix degradation but not demineralization. J Bone Miner Res. 1999 ; 14: 1654-1663
15. Grimes CL, Ariyananda Lde Z, Melnyk JE, O'Shea EK. The innate immune protein Nod2 binds directly to MDP, a bacterial cell wall fragment. J Am Chem Soc. 2012 ; 134: 13535-13537
16. Hie M, Shimono M, Fujii K, Tsukamoto I. Increased cathepsin K and tartrate-resistant acid phosphatase expression in bone of streptozotocin-induced diabetic rats. Bone. 2007 ; 41: 1045-1050
17. Hirao K, Yumoto H, Takahashi K, Mukai K, Nakanishi T, Matsuo T. Roles of TLR2, TLR4, NOD2, and NOD1 in pulp fibroblasts. J Dent Res. 2009 ; 88: 762-767
18. Hosokawa I, Hosokawa Y, Ozaki K, Yumoto H, Nakae H, Matsuo T. Proinflammatory effects of muramyldipeptide on human gingival fibroblasts. J Periodontal Res. 2010 ; 45: 193-199
19. Inohara N, Koseki T, del Peso L, Hu Y, Yee C, Chen S, et al. Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-kappaB. J Biol Chem. 1999 ; 274: 14560-14567
20. Inohara N, Chamaillard M, McDonald C, Nunez G. NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu Rev Biochem. 2005 ; 74: 355-383
21. Jeon DI, Park SR, Ahn MY, Ahn SG, Park JH, Yoon JH. NOD1 and NOD2 stimulation triggers innate immune responses of human periodontal ligament cells. Int J Mol Med. 2012 ; 29: 699-703
22. Kawai T, Paster BJ, Komatsuzawa H, Ernst CW, Gonçalves RB, Sasaki H, et al. Cross-reactive adaptive immune response to oral commensal bacteria results in an induction of receptor activator of nuclear factor-kappaB ligand (RANKL)-dependent periodontal bone resorption in a mouse model. Oral Microbiol Immunol. 2007 ; 22: 208-215
23. Kishimoto T, Kaneko T, Ukai T, Yokoyama M, Ayon Haro R, Yoshinaga Y, et al. Peptidoglycan and lipopolysaccharide synergistically enhance bone resorption and osteoclastogenesis. J Periodontal Res. 2012 ; 47: 446-454
24. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nuñez G, et al. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Sicence. 2005 ; 307: 731-734
25. Kornman KS. Mapping the pathogenesis of periodontitis: a new look. J Periodontol. 2008 ; 79 (8). 1560S - 1568S
26. Lee SI, Kim GT, Kim HJ, Park SH, Kim EC. NOD2 mediates odontoblast differentiation and RANKL expression. J Dent Res. 2014 ; 93: 678-684
27. Leppilahti JM, Hernandez-Rios PA, Gamonal JA, Tervahartiala T, Brignardello-Petersen R, Mantyla P, et al. Matrix metalloproteinases and myeloperoxidase in gingival crevicular fluid provide site-specific diagnostic value for chronic periodontitis. J Clin Periodontol. 2014 ; 41: 348-356
28. Liu J, Duan J, Wang Y, Ouyang X. Intracellular adhesion molecule-1 is regulated by porphyromonas gingivalis through nucleotide binding oligomerization domain-containing proteins 1 and 2 molecules in periodontal fibroblasts. J Periodontol. 2014 ; 85: 358-368
29. Liu YC, Lerner UH, Teng YT. Cytokine responses against periodontal infection: protective and destructive roles. Periodontol. 2010 2000 ; 52: 163-206
30. Loesche WJ, Grossman NS. Periodontal disease as a specific, albeit chronic, infection: diagnosis and treatment. Clin Microbiol Rev. 2001 ; 14: 727-752
31. Marriott I, Rati DM, McCall SH, Tranguch SL. Induction of Nod1 and Nod2 intracellular pattern recognition receptors in murine osteoblasts following bacterial challenge. Infect Immun. 2005 ; 73: 2967-2973
32. Mogi M, Otogoto J. Expression of cathepsin-K in gingival crevicular fluid of patients with periodontitis. Arch Oral Biol. 2007 ; 52: 894-898
33. Okugawa T, Kaneko T, Yoshimura A, Silverman N, Hara Y. NOD1 and NOD2 mediate sensing of periodontal pathogens. J Dental Res. 2010 ; 89: 186-191
34. Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS. Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol. 1997 ; 2000: 14 216-248
35. Saftig P, Hunziker E, Wehmeyer O, Jones S, Boyde A, Rommerskirch W, et al. Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc Natl Acad Sci U S A. 1998 ; 95: 13453-13458
36. Sasaki H, Okamatsu Y, Kawai T, Kent R, Taubman M, Stashenko P. The interleukin-10 knockout mouse is highly susceptible to Porphyromonas gingivalis-induced alveolar bone loss. J Periodontal Res. 2004 ; 39: 432-441
37. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998 ; 25: 134-144
38. Strober W, Murray PJ, Kitani A, Watanabe T. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat Rev Immunol. 2006 ; 6: 9-20
39. Stroup GB, Lark MW, Veber DF, Bhattacharyya A, Blake S, Dare LC, et al. Potent and selective inhibition of human cathepsin K leads to inhibition of bone resorption in vivo in a nonhuman primate. J Bone Miner Res. 2001 ; 16: 1739-1746
40. Takahashi S, Fukuda M, Mitani A, Fujimura T, Iwamura Y, Sato S, et al. Follicular dendritic cell-secreted protein is decreased in experimental periodontitis concurrently with the increase of interleukin-17 expression and the Rankl/Opg mRNA ratio. J Periodontal Res. 2013 ; 49: 390-397
41. Tang L, Zhou XD, Wang Q, Zhang L, Wang Y, Li XY, et al. Expression of TRAF6 and pro-inflammatory cytokines through activation of TLR2, TLR4, NOD1, and NOD2 in human periodontal ligament fibroblasts. Arch Oral Biol. 2011 ; 56: 1064-1072
42. Votta BJ, Levy MA, Badger A, Bradbeer J, Dodds RA, James IE, et al. Peptide aldehyde inhibitors of cathepsin K inhibit bone resorption both in vitro and in vivo. J Bone Miner Res. 1997 ; 12: 1396-1406