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Osteoimmunological Aspects of Periodontal Diseases

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Principles of Osteoimmunology

Abstract

Osteoimmunology describes the cross-talk of cells of the musculoskeletal and the immune system during the pathogenesis of various diseases; among the most prevalent ones is periodontitis, a chronic infectious inflammatory disease of the tooth-supporting structures, i.e., the periodontium consisting of the gingiva, alveolar bone, periodontal ligament, and root cementum. Periodontal disease is initiated by oral pathogens that accumulate at the gingival margin of the teeth and thereby trigger a response of the innate and adaptive immunity. In contrast to other osteoimmunological disorders (e.g., osteoporosis, rheumatoid arthritis), the immune system plays a two-sided role in the pathogenesis of periodontitis: it controls the infection and protects the organism from bacterial invasion but also propagates the destruction of the soft and hard tissues surrounding the tooth. Periodontitis, if left untreated, finally results in tooth loss.

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Abbreviations

AgP:

Aggressive periodontitis

C3:

Complement component 3

CP:

Chronic periodontitis

IFN:

Interferon

Ig:

Immunoglobulin

IL:

Interleukin

iNOS:

Inducible NO-synthases

LPS:

Lipopolysaccharide

M-CSF:

Macrophage colony-stimulating factor

MMP:

Matrix metalloproteinases

NO:

Nitric oxide

OPG:

Osteoprotegerin

RANK:

Receptor activator of NF-kB

RANKL:

Receptor activator of nuclear factor “kappa-light-chain-enhancer” of the activated B cell ligand

TGF:

Transforming growth factor

Th:

T helper cells

TIMP:

Tissue inhibitors of metalloproteinase

TLR:

Toll-like receptors

TNF:

Tumor necrosis factor

Treg:

Regulatory T cells

References

  • Abbas AK, Murphy KM, Sher A (1996) Functional diversity of helper T lymphocytes. Nature 383:787–793

    Article  CAS  PubMed  Google Scholar 

  • Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511

    Article  CAS  PubMed  Google Scholar 

  • Alayan J, Ivanovski S, Gemmell E, Ford P, Hamlet S, Farah CS (2006) Deficiency of iNOS contributes to Porphyromonas gingivalis-induced tissue damage. Oral Microbiol Immunol 21:360–365

    Article  CAS  PubMed  Google Scholar 

  • Anderson DM, Maraskovsky E, Billingsley WL et al (1997) A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature 390:175–179

    Article  CAS  PubMed  Google Scholar 

  • Appay V, van Lier RA, Sallusto F, Roederer M (2008) Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytometry A 73:975–983

    Article  PubMed  Google Scholar 

  • Arabacı T, Kermen E, Özkanlar S et al (2015) Therapeutic effects of melatonin on alveolar bone resorption after experimental periodontitis in rats: a biochemical and immunohistochemical study. J Periodontol 86:874–881

    Article  PubMed  CAS  Google Scholar 

  • Araújo AA, Lopes de Souza G, Souza TO et al (2013a) Olmesartan decreases IL-1β and TNF-α levels; downregulates MMP-2, MMP-9, COX-2, and RANKL; and upregulates OPG in experimental periodontitis. Naunyn Schmiedebergs Arch Pharmacol 386:875–884

    Article  PubMed  CAS  Google Scholar 

  • Araújo AA, Souza TO, Moura LM et al (2013b) Effect of telmisartan on levels of IL-1, TNF-α, down-regulated COX-2, MMP-2, MMP-9 and RANKL/RANK in an experimental periodontitis model. J Clin Periodontol 40:1104–1111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Araújo AA, Varela H, Brito GA et al (2014) Azilsartan increases levels of IL-10, down-regulates MMP-2, MMP-9, RANKL/RANK, Cathepsin K and up-regulates OPG in an experimental periodontitis model. PLoS One 9, e96750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4:1–6

    Article  CAS  PubMed  Google Scholar 

  • Armitage GC, Cullinan MP (2010) Comparison of the clinical features of chronic and aggressive periodontitis. Periodontol 2000 53:12–27

    Article  PubMed  Google Scholar 

  • Aurer A, Aleksic J, Ivic-Kardum M, Aurer J, Culo F (2001) Nitric oxide synthesis is decreased in periodontitis. J Clin Periodontol 28:565–568

    Article  CAS  PubMed  Google Scholar 

  • Baker PJ, Dixon M, Evans RT, Dufour L, Johnson E, Roopenian DC (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baker PJ, Boutaugh NR, Tiffany M, Roopenian DC (2009) B cell IgD deletion prevents Alveolar bone loss following murine oral infection. Interdiscip Perspect Infect Dis 2009:864359

    PubMed  PubMed Central  Google Scholar 

  • Banu S, Jabir NR, Mohan R et al (2015) Correlation of Toll-like receptor 4, interleukin-18, transaminases, and uric acid in patients with chronic periodontitis and healthy adults. J Periodontol 86:431–439

    Article  CAS  PubMed  Google Scholar 

  • Bar-Shavit Z (2008) Taking a toll on the bones: regulation of bone metabolism by innate immune regulators. Autoimmunity 41:195–203

    Article  CAS  PubMed  Google Scholar 

  • Bartold PM, Cantley MD, Haynes DR (2010) Mechanisms and control of pathologic bone loss in periodontitis. Periodontol 2000 53:55–69

    Article  PubMed  Google Scholar 

  • Beklen A, Sorsa T, Konttinen YT (2009) Toll-like receptors 2 and 5 in human gingival epithelial cells co-operate with T-cell cytokine interleukin-17. Oral Microbiol Immunol 24:38–42

    Article  CAS  PubMed  Google Scholar 

  • Belibasakis GN, Bostanci N, Hashim A et al (2007) Regulation of RANKL and OPG gene expression in human gingival fibroblasts and periodontal ligament cells by Porphyromonas gingivalis: a putative role of the Arg-gingipains. Microb Pathog 43:46–53

    Article  CAS  PubMed  Google Scholar 

  • Bertl K, Schoiber A, Haririan H et al (2013) Non-surgical periodontal therapy influences salivary melatonin levels. Clin Oral Investig 17:1219–1225

    Article  PubMed  Google Scholar 

  • Bertl K, Bruckmann C, Isberg PE, Klinge B, Gotfredsen K, Stavropoulos A (2015) Hyaluronan in non-surgical and surgical periodontal therapy: a systematic review. J Clin Periodontol 42:236–246

    Article  CAS  PubMed  Google Scholar 

  • Bickel M (1993) The role of interleukin-8 in inflammation and mechanisms of regulation. J Periodontol 64:456–460

    CAS  PubMed  Google Scholar 

  • Bloemen V, Schoenmaker T, de Vries TJ, Everts V (2010) Direct cell-cell contact between periodontal ligament fibroblasts and osteoclast precursors synergistically increases the expression of genes related to osteoclastogenesis. J Cell Physiol 222:565–573

    CAS  PubMed  Google Scholar 

  • Boyle WJ, Simonet WS, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423:337–342

    Article  CAS  PubMed  Google Scholar 

  • Bradshaw DJ, Marsh PD, Watson GK, Allison C (1998) Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration. Infect Immun 66:4729–4732

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan PA, Thomas GJ, Langdon JD (2003) The role of nitric oxide in oral diseases. Arch Oral Biol 48:93–100

    Article  CAS  PubMed  Google Scholar 

  • Brook I (2003) Microbiology and management of periodontal infections. Gen Dent 51:424–428

    PubMed  Google Scholar 

  • Brunetti G, Colucci S, Pignataro P et al (2005) T cells support osteoclastogenesis in an in vitro model derived from human periodontitis patients. J Periodontol 76:1675–1680

    Article  CAS  PubMed  Google Scholar 

  • Cardoso CR, Garlet GP, Moreira AP, Junior WM, Rossi MA, Silva JS (2008) Characterization of CD4 + CD25+ natural regulatory T cells in the inflammatory infiltrate of human chronic periodontitis. J Leukoc Biol 84:311–318

    Article  CAS  PubMed  Google Scholar 

  • Castro ML, Franco GC, Branco-de-Almeida LS et al (2016) Down-Regulation of protease activated receptor 2, interleukin-17 and other pro-inflammatory genes by subantimicrobial doxycycline dose in a rat periodontitis model. J Periodontol 87:203–210

    Google Scholar 

  • Chakravarti A, Raquil MA, Tessier P, Poubelle PE (2009) Surface RANKL of Toll-like receptor 4-stimulated human neutrophils activates osteoclastic bone resorption. Blood 114:1633–1644

    Article  CAS  PubMed  Google Scholar 

  • Chalifour A, Jeannin P, Gauchat JF et al (2004) Direct bacterial protein PAMP recognition by human NK cells involves TLRs and triggers alpha-defensin production. Blood 104:1778–1783

    Article  CAS  PubMed  Google Scholar 

  • Chang PC, Chong LY, Tsai SC, Lim LP (2014) Aminoguanidine inhibits the AGE-RAGE axis to modulate the induction of periodontitis but has limited effects on the progression and recovery of experimental periodontitis: a preliminary study. J Periodontol 85:729–739

    Article  CAS  PubMed  Google Scholar 

  • Cheng WC, Hughes FJ, Taams LS (2014) The presence, function and regulation of IL-17 and Th17 cells in periodontitis. J Clin Periodontol 41:541–549

    Article  CAS  PubMed  Google Scholar 

  • Claudino M, Trombone AP, Cardoso CR et al (2008) The broad effects of the functional IL-10 promoter-592 polymorphism: modulation of IL-10, TIMP-3, and OPG expression and their association with periodontal disease outcome. J Leukoc Biol 84:1565–1573

    Article  CAS  PubMed  Google Scholar 

  • Claudino M, Garlet TP, Cardoso CR et al (2010) Down-regulation of expression of osteoblast and osteocyte markers in periodontal tissues associated with the spontaneous alveolar bone loss of interleukin-10 knockout mice. Eur J Oral Sci 118:19–28

    Article  CAS  PubMed  Google Scholar 

  • Cochran DL (2008) Inflammation and bone loss in periodontal disease. J Periodontol 79:1569–1576

    Article  CAS  PubMed  Google Scholar 

  • Cronstein BN (2007) Interleukin-6--a key mediator of systemic and local symptoms in rheumatoid arthritis. Bull NYU Hosp Jt Dis 65(Suppl 1):S11–S15

    PubMed  Google Scholar 

  • Crotti T, Smith MD, Hirsch R et al (2003) Receptor activator NF kappaB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. J Periodontal Res 38:380–387

    Article  CAS  PubMed  Google Scholar 

  • Daghigh F, Borghaei RC, Thornton RD, Bee JH (2002) Human gingival fibroblasts produce nitric oxide in response to proinflammatory cytokines. J Periodontol 73:392–400

    Article  CAS  PubMed  Google Scholar 

  • Damgaard C, Holmstrup P, Van Dyke TE, Nielsen CH (2015) The complement system and its role in the pathogenesis of periodontitis: current concepts. J Periodontal Res 50:283–293

    Article  CAS  PubMed  Google Scholar 

  • De Almeida J, Ervolino E, Bonfietti LH et al (2015) Adjuvant therapy with sodium alendronate for the treatment of experimental periodontitis in rats. J Periodontol 86:1166–1175

    Article  PubMed  Google Scholar 

  • de Vries TJ, Yousovich J, Schoenmaker T, Scheres N, Everts V (2016) Tumor necrosis factor-α antagonist infliximab inhibits osteoclast formation of peripheral blood mononuclear cells but does not affect periodontal ligament fibroblast-mediated osteoclast formation. J Periodontal Res 51:186–195

    Google Scholar 

  • de Waal Malefyt R, Figdor CG, Huijbens R et al (1993) Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J Immunol 151:6370–6381

    PubMed  Google Scholar 

  • Deas DE, Mealey BL (2010) Response of chronic and aggressive periodontitis to treatment. Periodontol 2000 53:154–166

    Article  PubMed  Google Scholar 

  • Di Paola R, Marzocco S, Mazzon E et al (2004) Effect of aminoguanidine in ligature-induced periodontitis in rats. J Dent Res 83:343–348

    Article  PubMed  Google Scholar 

  • Di Paola R, Mazzon E, Muià C et al (2007) Effects of etanercept, a tumour necrosis factor-alpha antagonist, in an experimental model of periodontitis in rats. Br J Pharmacol 150:286–297

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Donati M, Liljenberg B, Zitzmann NU, Berglundh T (2009) B-1a cells and plasma cells in periodontitis lesions. J Periodontal Res 44:683–688

    Article  CAS  PubMed  Google Scholar 

  • Duarte PM, de Oliveira MC, Tambeli CH, Parada CA, Casati MZ, Nociti FH (2007) Overexpression of interleukin-1beta and interleukin-6 may play an important role in periodontal breakdown in type 2 diabetic patients. J Periodontal Res 42:377–381

    Article  CAS  PubMed  Google Scholar 

  • Ebersole JL, Schuster JL, Stevens J et al (2013) Patterns of salivary analytes provide diagnostic capacity for distinguishing chronic adult periodontitis from health. J Clin Immunol 33:271–279

    Article  PubMed  Google Scholar 

  • Eke PI, Page RC, Wei L, Thornton-Evans G, Genco RJ (2012) Update of the case definitions for population-based surveillance of periodontitis. J Periodontol 83:1449–1454

    Article  PubMed  Google Scholar 

  • Ertugrul AS, Sahin H, Dikilitas A, Alpaslan N, Bozoglan A (2013) Comparison of CCL28, interleukin-8, interleukin-1β and tumor necrosis factor-alpha in subjects with gingivitis, chronic periodontitis and generalized aggressive periodontitis. J Periodontal Res 48:44–51

    Article  CAS  PubMed  Google Scholar 

  • Fajardo ME, Rocha ML, Sánchez-Marin FJ, Espinosa-Chávez EJ (2010) Effect of atorvastatin on chronic periodontitis: a randomized pilot study. J Clin Periodontol 37:1016–1022

    Article  CAS  PubMed  Google Scholar 

  • Faust J, Lacey DL, Hunt P et al (1999) Osteoclast markers accumulate on cells developing from human peripheral blood mononuclear precursors. J Cell Biochem 72:67–80

    Article  CAS  PubMed  Google Scholar 

  • Ferrari-Lacraz S, Ferrari S (2011) Do RANKL inhibitors (denosumab) affect inflammation and immunity? Osteoporos Int 22:435–46

    Google Scholar 

  • Flemmig TF (1999) Periodontitis. Ann Periodontol 4:32–38

    Article  CAS  PubMed  Google Scholar 

  • Ford PJ, Gamonal J, Seymour GJ (2010) Immunological differences and similarities between chronic periodontitis and aggressive periodontitis. Periodontol 2000 53:111–123

    Article  PubMed  Google Scholar 

  • Foster JS, Kolenbrander PE (2004) Development of a multispecies oral bacterial community in a saliva-conditioned flow cell. Appl Environ Microbiol 70:4340–4348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukada SY, Silva TA, Saconato IF et al (2008) iNOS-derived nitric oxide modulates infection-stimulated bone loss. J Dent Res 87:1155–1159

    Article  CAS  PubMed  Google Scholar 

  • Fuller K, Wong B, Fox S, Choi Y, Chambers TJ (1998) TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts. J Exp Med 188:997–1001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furlaneto FA, Nunes NL, Oliveira Filho IL et al (2014) Effects of locally administered tiludronic acid on experimental periodontitis in rats. J Periodontol 85:1291–1301

    Article  CAS  PubMed  Google Scholar 

  • Gaffen SL, Hajishengallis G (2008) A new inflammatory cytokine on the block: re-thinking periodontal disease and the Th1/Th2 paradigm in the context of Th17 cells and IL-17. J Dent Res 87:817–828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamonal J, Acevedo A, Bascones A, Jorge O, Silva A (2000) Levels of interleukin-1 beta, −8, and −10 and RANTES in gingival crevicular fluid and cell populations in adult periodontitis patients and the effect of periodontal treatment. J Periodontol 71:1535–1545

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Grassi F, Ryan MR et al (2007) IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J Clin Invest 117:122–132

    Article  CAS  PubMed  Google Scholar 

  • Garcia MN, Hildebolt CF, Miley DD et al (2011) One-year effects of vitamin D and calcium supplementation on chronic periodontitis. J Periodontol 82:25–32

    Article  CAS  PubMed  Google Scholar 

  • Garlet GP (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

    Article  CAS  PubMed  Google Scholar 

  • Garlet GP, Martins WJ, Ferreira BR, Milanezi CM, Silva JS (2003) Patterns of chemokines and chemokine receptors expression in different forms of human periodontal disease. J Periodontal Res 38:210–217

    Article  CAS  PubMed  Google Scholar 

  • Garlet GP, Martins WJ, Fonseca BA, Ferreira BR, Silva JS (2004) Matrix metalloproteinases, their physiological inhibitors and osteoclast factors are differentially regulated by the cytokine profile in human periodontal disease. J Clin Periodontol 31:671–679

    Article  CAS  PubMed  Google Scholar 

  • Garlet GP, Cardoso CR, Silva TA et al (2006) 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 21:12–20

    Article  CAS  PubMed  Google Scholar 

  • Garlet GP, Cardoso CR, Campanelli AP et al (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garlet GP, Cardoso CR, Campanelli AP et al (2008) The essential role of IFN-gamma in the control of lethal Aggregatibacter actinomycetemcomitans infection in mice. Microbes Infect 10:489–496

    Article  CAS  PubMed  Google Scholar 

  • Gemmell E, Seymour GJ (1994) Cytokines and T cell switching. Crit Rev Oral Biol Med 5:249–279

    CAS  PubMed  Google Scholar 

  • Genco RJ, Borgnakke WS (2013) Risk factors for periodontal disease. Periodontol 2000 62:59–94

    Article  PubMed  Google Scholar 

  • Giannobile WV (2008) Host-response therapeutics for periodontal diseases. J Periodontol 79:1592–1600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonçalves DC, Evangelista RC, da Silva RR et al (2014) Infliximab attenuates inflammatory osteolysis in a model of periodontitis in Wistar rats. Exp Biol Med (Maywood) 239:442–453

    Article  CAS  Google Scholar 

  • Gonzales JR (2015) T- and B-cell subsets in periodontitis. Periodontol 2000 69:181–200

    Article  PubMed  Google Scholar 

  • Graves D (2008) Cytokines that promote periodontal tissue destruction. J Periodontol 79:1585–1591

    Article  CAS  PubMed  Google Scholar 

  • Graves DT, Cochran D (2003) The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J Periodontol 74:391–401

    Article  CAS  PubMed  Google Scholar 

  • Graves DT, Li J, Cochran DL (2011) Inflammation and uncoupling as mechanisms of periodontal bone loss. J Dent Res 90:143–153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guentsch A, Puklo M, Preshaw PM et al (2009) Neutrophils in chronic and aggressive periodontitis in interaction with Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans. J Periodontal Res 44:368–377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gursoy UK, Könönen E, Uitto VJ et al (2009) Salivary interleukin-1beta concentration and the presence of multiple pathogens in periodontitis. J Clin Periodontol 36:922–927

    Article  CAS  PubMed  Google Scholar 

  • Gursoy UK, Könönen E, Huumonen S et al (2013) Salivary type I collagen degradation end-products and related matrix metalloproteinases in periodontitis. J Clin Periodontol 40:18–25

    Article  CAS  PubMed  Google Scholar 

  • Gustafsson A, Ito H, Asman B, Bergstrom K (2006) Hyper-reactive mononuclear cells and neutrophils in chronic periodontitis. J Clin Periodontol 33:126–129

    Article  CAS  PubMed  Google Scholar 

  • Hajishengallis G (2014) Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 35:3–11

    Article  CAS  PubMed  Google Scholar 

  • Hajishengallis G, Lamont RJ (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27:409–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hajishengallis G, Liang S, Payne MA et al (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10:497–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hajishengallis G, Darveau RP, Curtis MA (2012) The keystone-pathogen hypothesis. Nat Rev Microbiol 10:717–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han X, Kawai T, Eastcott JW, Taubman MA (2006) Bacterial-responsive B lymphocytes induce periodontal bone resorption. J Immunol 176:625–631

    Article  CAS  PubMed  Google Scholar 

  • Han X, Lin X, Seliger AR, Eastcott J, Kawai T, Taubman MA (2009) Expression of receptor activator of nuclear factor-kappaB ligand by B cells in response to oral bacteria. Oral Microbiol Immunol 24:190–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao L, Chen J, Zhu Z et al (2015) Odanacatib, a cathepsin K-Specific inhibitor, inhibits inflammation and bone loss caused by periodontal diseases. J Periodontol 86:972–983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasturk H, Kantarci A, Goguet-Surmenian E et al (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J Immunol 179:7021–7029

    Article  CAS  PubMed  Google Scholar 

  • Hayami T, Kapila YL, Kapila S (2008) MMP-1 (collagenase-1) and MMP-13 (collagenase-3) differentially regulate markers of osteoblastic differentiation in osteogenic cells. Matrix Biol 27:682–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Himani GS, Prabhuji ML, Karthikeyan BV (2014) Gingival crevicular fluid and interleukin-23 concentration in systemically healthy subjects: their relationship in periodontal health and disease. J Periodontal Res 49:237–245

    Article  CAS  PubMed  Google Scholar 

  • Holt SC, Ebersole JL (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38:72–122

    Article  PubMed  Google Scholar 

  • Holtfreter B, Kocher T, Hoffmann T, Desvarieux M, Micheelis W (2010) Prevalence of periodontal disease and treatment demands based on a German dental survey (DMS IV). J Clin Periodontol 37:211–219

    Article  PubMed  Google Scholar 

  • Honda T, Domon H, Okui T, Kajita K, Amanuma R, Yamazaki K (2006) Balance of inflammatory response in stable gingivitis and progressive periodontitis lesions. Clin Exp Immunol 144:35–40

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ihn H, Yamane K, Asano Y, Kubo M, Tamaki K (2002) IL-4 up-regulates the expression of tissue inhibitor of metalloproteinase-2 in dermal fibroblasts via the p38 mitogen-activated protein kinase dependent pathway. J Immunol 168:1895–1902

    Article  CAS  PubMed  Google Scholar 

  • Irwin CR, Myrillas TT (1998) The role of IL-6 in the pathogenesis of periodontal disease. Oral Dis 4:43–47

    Article  CAS  PubMed  Google Scholar 

  • Isaza-Guzmán DM, Cardona-Vélez N, Gaviria-Correa DE, Martínez-Pabón MC, Castaño-Granada MC, Tobón-Arroyave SI (2015) Association study between salivary levels of interferon (IFN)-gamma, interleukin (IL)-17, IL-21, and IL-22 with chronic periodontitis. Arch Oral Biol 60:91–99

    Article  PubMed  CAS  Google Scholar 

  • Jarnicki AG, Fallon PG (2003) T helper type-2 cytokine responses: potential therapeutic targets. Curr Opin Pharmacol 3:449–455

    Article  CAS  PubMed  Google Scholar 

  • Jenkinson HF, Lamont RJ (2005) Oral microbial communities in sickness and in health. Trends Microbiol 13:589–595

    Article  CAS  PubMed  Google Scholar 

  • Ji JD, Park-Min KH, Shen Z et al (2009) Inhibition of RANK expression and osteoclastogenesis by TLRs and IFN-gamma in human osteoclast precursors. J Immunol 183:7223–7233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Q, Cirelli JA, Park CH et al (2007) RANKL inhibition through osteoprotegerin blocks bone loss in experimental periodontitis. J Periodontol 78:1300–1308

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson RB, Serio FG (2007) The contribution of interleukin-13 and −15 to the cytokine network within normal and diseased gingiva. J Periodontol 78:691–695

    Article  CAS  PubMed  Google Scholar 

  • Joseph J, Kapila YL, Hayami T, Kapila S (2010) Disease-associated extracellular matrix suppresses osteoblastic differentiation of human periodontal ligament cells via MMP-1. Calcif Tissue Int 86:154–162

    Article  CAS  PubMed  Google Scholar 

  • Jovanovic DV, Di Battista JA, Martel-Pelletier J et al (1998) IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J Immunol 160:3513–3521

    CAS  PubMed  Google Scholar 

  • Kadono H, Kido J, Kataoka M, Yamauchi N, Nagata T (1999) Inhibition of osteoblastic cell differentiation by lipopolysaccharide extract from Porphyromonas gingivalis. Infect Immun 67:2841–2846

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kara A, Akman S, Ozkanlar S et al (2013) Immune modulatory and antioxidant effects of melatonin in experimental periodontitis in rats. Free Radic Biol Med 55:21–26

    Article  CAS  PubMed  Google Scholar 

  • Kawai T, Matsuyama T, Hosokawa Y et al (2006) B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 169:987–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kikkert R, Laine ML, Aarden LA, van Winkelhoff AJ (2007) Activation of toll-like receptors 2 and 4 by gram-negative periodontal bacteria. Oral Microbiol Immunol 22:145–151

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi T, Hahn CL, Tanaka S, Barbour SE, Schenkein HA, Tew JG (2004) Dendritic cells stimulated with Actinobacillus actinomycetemcomitans elicit rapid gamma interferon responses by natural killer cells. Infect Immun 72:5089–5096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JH, Lee DE, Cha JH, Bak EJ, Yoo YJ (2014) Receptor activator of nuclear factor-kB ligand and sclerostin expression in osteocytes of alveolar bone in rats with ligature-induced periodontitis. J Periodontol 85:e370–e378

    Article  PubMed  Google Scholar 

  • Kim JH, Lee DE, Woo GH, Cha JH, Bak EJ, Yoo YJ (2015) Osteocytic sclerostin expression in alveolar bone in rats with diabetes mellitus and ligature-induced periodontitis. J Periodontol 86:1005–1011

    Article  CAS  PubMed  Google Scholar 

  • Kirkwood KL, Li F, Rogers JE et al (2007) A p38alpha selective mitogen-activated protein kinase inhibitor prevents periodontal bone loss. J Pharmacol Exp Ther 320:56–63

    Article  CAS  PubMed  Google Scholar 

  • Klein DC, Raisz LG (1970) Prostaglandins: stimulation of bone resorption in tissue culture. Endocrinology 86:1436–1440

    Article  CAS  PubMed  Google Scholar 

  • Kong YY, Yoshida H, Sarosi I et al (1999) OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397:315–323

    Article  CAS  PubMed  Google Scholar 

  • Kook YA, Lee SK, Son DH et al (2009) Effects of substance P on osteoblastic differentiation and heme oxygenase-1 in human periodontal ligament cells. Cell Biol Int 33:424–428

    Article  CAS  PubMed  Google Scholar 

  • Kotake S, Udagawa N, Takahashi N et al (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103:1345–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koutouzis T, Haber D, Shaddox L, Aukhil I, Wallet SM (2009) Autoreactivity of serum immunoglobulin to periodontal tissue components: a pilot study. J Periodontol 80:625–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulkarni C, Kinane DF (2014) Host response in aggressive periodontitis. Periodontol 2000 65:79–91

    Article  PubMed  Google Scholar 

  • Kuziel WA, Greene WC (1990) Interleukin-2 and the IL-2 receptor: new insights into structure and function. J Invest Dermatol 94:27S–32S

    Article  CAS  PubMed  Google Scholar 

  • Lacey DL, Timms E, Tan HL et al (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165–176

    Article  CAS  PubMed  Google Scholar 

  • Lacey DC, Simmons PJ, Graves SE, Hamilton JA (2009) Proinflammatory cytokines inhibit osteogenic differentiation from stem cells: implications for bone repair during inflammation. Osteoarthritis Cartilage 17:735–742

    Article  CAS  PubMed  Google Scholar 

  • Lappin DF, Kjeldsen M, Sander L, Kinane DF (2000) Inducible nitric oxide synthase expression in periodontitis. J Periodontal Res 35:369–373

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Pi SH, Kim Y et al (2009) Effects of nicotine on antioxidant defense enzymes and RANKL expression in human periodontal ligament cells. J Periodontol 80:1281–1288

    Article  CAS  PubMed  Google Scholar 

  • Leppilahti JM, Hernández-Ríos PA, Gamonal JA et al (2014) Matrix metalloproteinases and myeloperoxidase in gingival crevicular fluid provide site-specific diagnostic value for chronic periodontitis. J Clin Periodontol 41:348–356

    Article  CAS  PubMed  Google Scholar 

  • Lin X, Han X, Kawai T, Taubman MA (2011) Antibody to RANKL Ameliorates T cell-mediated Periodontal Bone Resorption. Infect Immun 79:911–7

    Google Scholar 

  • Listgarten MA (1994) The structure of dental plaque. Periodontol 2000 5:52–65

    Article  CAS  PubMed  Google Scholar 

  • Liu YC, Lerner UH, Teng YT (2010) Cytokine responses against periodontal infection: protective and destructive roles. Periodontol 2000 52:163–206

    Article  PubMed  Google Scholar 

  • Loe H, Theilade E, Jensen SB (1965) Experimental gingivitis in man. J Periodontol 36:177–187

    Article  CAS  PubMed  Google Scholar 

  • Lohinai Z, Benedek P, Feher E et al (1998) Protective effects of mercaptoethylguanidine, a selective inhibitor of inducible nitric oxide synthase, in ligature-induced periodontitis in the rat. Br J Pharmacol 123:353–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malcolm J, Awang RA, Oliver-Bell J et al (2015) IL-33 exacerbates periodontal disease through induction of RANKL. J Dent Res 94:968–975

    Article  CAS  PubMed  Google Scholar 

  • Massey HM, Flanagan AM (1999) Human osteoclasts derive from CD14-positive monocytes. Br J Haematol 106:167–170

    Article  CAS  PubMed  Google Scholar 

  • Matejka M, Partyka L, Ulm C, Solar P, Sinzinger H (1998) Nitric oxide synthesis is increased in periodontal disease. J Periodontal Res 33:517–518

    Article  CAS  PubMed  Google Scholar 

  • Mayer Y, Balbir-Gurman A, Machtei EE (2009) Anti-tumor necrosis factor-alpha therapy and periodontal parameters in patients with rheumatoid arthritis. J Periodontol 80:1414–1420

    Article  CAS  PubMed  Google Scholar 

  • Menezes R, Garlet TP, Letra A et al (2008) Differential patterns of receptor activator of nuclear factor kappa B ligand/osteoprotegerin expression in human periapical granulomas: possible association with progressive or stable nature of the lesions. J Endod 34:932–938

    Article  PubMed  PubMed Central  Google Scholar 

  • Miley DD, Garcia MN, Hildebolt CF et al (2009) Cross-sectional study of vitamin D and calcium supplementation effects on chronic periodontitis. J Periodontol 80:1433–1439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mize TW, Sundararaj KP, Leite RS, Huang Y (2015) Increased and correlated expression of connective tissue growth factor and transforming growth factor beta 1 in surgically removed periodontal tissues with chronic periodontitis. J Periodontal Res 50:315–319

    Article  CAS  PubMed  Google Scholar 

  • Mogi M, Otogoto J, Ota N, Inagaki H, Minami M, Kojima K (1999) Interleukin 1 beta, interleukin 6, beta 2-microglobulin, and transforming growth factor-alpha in gingival crevicular fluid from human periodontal disease. Arch Oral Biol 44:535–539

    Article  CAS  PubMed  Google Scholar 

  • Mosmann TR, Schumacher JH, Street NF et al (1991) Diversity of cytokine synthesis and function of mouse CD4+ T cells. Immunol Rev 123:209–229

    Article  CAS  PubMed  Google Scholar 

  • Mostafa NZ, Uludağ H, Varkey M, Dederich DN, Doschak MR, El-Bialy TH (2011) In vitro osteogenic induction of human gingival fibroblasts for bone regeneration. Open Dent J 5:139–145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moussion C, Ortega N, Girard JP (2008) The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel ‘alarmin’. PLoS One 3, e3331

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Murphy KM, Reiner SL (2002) The lineage decisions of helper T cells. Nat Rev Immunol 2:933–944

    Article  CAS  PubMed  Google Scholar 

  • Naundorf S, Schroder M, Hoflich C, Suman N, Volk HD, Grutz G (2009) IL-10 interferes directly with TCR-induced IFN-gamma but not IL-17 production in memory T cells. Eur J Immunol 39:1066–1077

    Article  CAS  PubMed  Google Scholar 

  • Nguyen T, Brunson D, Crespi CL, Penman BW, Wishnok JS, Tannenbaum SR (1992) DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc Natl Acad Sci U S A 89:3030–3034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nile CJ, Barksby E, Jitprasertwong P, Preshaw PM, Taylor JJ (2010) Expression and regulation of interleukin-33 in human monocytes. Immunology 130:172–180

    Article  PubMed  PubMed Central  Google Scholar 

  • Nowak M, Krämer B, Haupt M et al (2013) Activation of invariant NK T cells in periodontitis lesions. J Immunol 190:2282–2291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nussbaum G, Shapira L (2011) How has neutrophil research improved our understanding of periodontal pathogenesis. J Clin Periodontol 38(Suppl 11):49–59

    Article  PubMed  Google Scholar 

  • Offenbacher S, Odle BM, Van Dyke TE (1986) The use of crevicular fluid prostaglandin E2 levels as a predictor of periodontal attachment loss. J Periodontal Res 21:101–112

    Article  CAS  PubMed  Google Scholar 

  • Ozçaka O, Nalbantsoy A, Buduneli N (2011) Interleukin-17 and interleukin-18 levels in saliva and plasma of patients with chronic periodontitis. J Periodontal Res 46:592–598

    PubMed  Google Scholar 

  • Page RC, Eke PI (2007) Case definitions for use in population-based surveillance of periodontitis. J Periodontol 78:1387–1399

    Article  PubMed  Google Scholar 

  • Page RC, Kornman KS (1997) The pathogenesis of human periodontitis: an introduction. Periodontol 2000 14:9–11

    Article  CAS  PubMed  Google Scholar 

  • Park AY, Scott P (2001) Il-12: keeping cell-mediated immunity alive. Scand J Immunol 53:529–532

    Article  CAS  PubMed  Google Scholar 

  • Pelletier M, Maggi L, Micheletti A et al (2010) Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115:335–343

    Article  CAS  PubMed  Google Scholar 

  • Pradeep AR, Roopa Y, Swati PP (2008) Interleukin-4, a T-helper 2 cell cytokine, is associated with the remission of periodontal disease. J Periodontal Res 43:712–716

    Article  CAS  PubMed  Google Scholar 

  • Pradeep AR, Priyanka N, Kalra N, Naik SB, Singh SP, Martande S (2012) Clinical efficacy of subgingivally delivered 1.2-mg simvastatin in the treatment of individuals with Class II furcation defects: a randomized controlled clinical trial. J Periodontol 83:1472–1479

    Article  CAS  PubMed  Google Scholar 

  • Pradeep AR, Kumari M, Rao NS, Martande SS, Naik SB (2013) Clinical efficacy of subgingivally delivered 1.2% atorvastatin in chronic periodontitis: a randomized controlled clinical trial. J Periodontol 84:871–879

    Article  CAS  PubMed  Google Scholar 

  • Pradeep AR, Karvekar S, Nagpal K, Patnaik K, Guruprasad CN, Kumaraswamy KM (2015) Efficacy of locally delivered 1.2% rosuvastatin gel to non-surgical treatment of patients with chronic periodontitis: a randomized, placebo-controlled clinical trial. J Periodontol 86:738–745

    Article  CAS  PubMed  Google Scholar 

  • Quinn JM, Elliott J, Gillespie MT, Martin TJ (1998) A combination of osteoclast differentiation factor and macrophage-colony stimulating factor is sufficient for both human and mouse osteoclast formation in vitro. Endocrinology 139:4424–4427

    Article  CAS  PubMed  Google Scholar 

  • Rams TE, Listgarten MA, Slots J (2006) Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis subgingival presence, species-specific serum immunoglobulin G antibody levels, and periodontitis disease recurrence. J Periodontal Res 41:228–234

    Article  CAS  PubMed  Google Scholar 

  • Ritz HL (1967) Microbial population shifts in developing human dental plaque. Arch Oral Biol 12:1561–1568

    Article  CAS  PubMed  Google Scholar 

  • Roberts HC, Moseley R, Sloan AJ, Youde SJ, Waddington RJ (2008) Lipopolysaccharide alters decorin and biglycan synthesis in rat alveolar bone osteoblasts: consequences for bone repair during periodontal disease. Eur J Oral Sci 116:207–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues TL, Marchesan JT, Coletta RD et al (2007) Effects of enamel matrix derivative and transforming growth factor-beta1 on human periodontal ligament fibroblasts. J Clin Periodontol 34:514–522

    Article  CAS  PubMed  Google Scholar 

  • Rogers JE, Li F, Coatney DD et al (2007) A p38 mitogen-activated protein kinase inhibitor arrests active alveolar bone loss in a rat periodontitis model. J Periodontol 78:1992–1998

    Article  CAS  PubMed  Google Scholar 

  • Ryder MI (2010) Comparison of neutrophil functions in aggressive and chronic periodontitis. Periodontol 2000 53:124–137

    Article  PubMed  Google Scholar 

  • Saidenberg-Kermanac’h N, Bessis N, Lemeiter D, de Vernejoul MC, Boissier MC, Cohen-Solal M (2004) Interleukin-4 cellular gene therapy and osteoprotegerin decrease inflammation-associated bone resorption in collagen-induced arthritis. J Clin Immunol 24:370–378

    Article  PubMed  Google Scholar 

  • Sasaki H, Okamatsu Y, Kawai T, Kent R, Taubman M, Stashenko P (2004) The interleukin-10 knockout mouse is highly susceptible to Porphyromonas gingivalis-induced alveolar bone loss. J Periodontal Res 39:432–441

    Article  CAS  PubMed  Google Scholar 

  • Sato K, Suematsu A, Okamoto K et al (2006) Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 203:2673–2682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schröder HE, Lindhe J (1981) Conditions and pathological features of rapidly destructive, experimental periodontitis in dogs. J Periodontol 51:6–19

    Google Scholar 

  • Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8:349–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sgolastra F, Petrucci A, Gatto R, Giannoni M, Monaco A (2011) Long-term efficacy of subantimicrobial-dose doxycycline as an adjunctive treatment to scaling and root planing: a systematic review and meta-analysis. J Periodontol 82:1570–1581

    Article  CAS  PubMed  Google Scholar 

  • Shaddox L, Wiedey J, Bimstein E et al (2010) Hyper-responsive phenotype in localized aggressive periodontitis. J Dent Res 89:143–148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slots J (2010) Human viruses in periodontitis. Periodontol 2000 53:89–110

    Article  PubMed  Google Scholar 

  • Stabholz A, Soskolne WA, Shapira L (2010) Genetic and environmental risk factors for chronic periodontitis and aggressive periodontitis. Periodontol 2000 53:138–153

    Article  PubMed  Google Scholar 

  • Steinsvoll S, Halstensen TS, Schenck K (1999) Extensive expression of TGF-beta1 in chronically-inflamed periodontal tissue. J Clin Periodontol 26:366–373

    Article  CAS  PubMed  Google Scholar 

  • Tang H, Mattheos N, Yao Y, Jia Y, Ma L, Gong P (2015) In vivo osteoprotegerin gene therapy preventing bone loss induced by periodontitis. J Periodontal Res 50:434–443

    Article  CAS  PubMed  Google Scholar 

  • Taut AD, Jin Q, Chung JH et al (2013) Sclerostin antibody stimulates bone regeneration after experimental periodontitis. J Bone Miner Res 28:2347–2356

    Article  CAS  PubMed  Google Scholar 

  • Teles RP, Likhari V, Socransky SS, Haffajee AD (2009) Salivary cytokine levels in subjects with chronic periodontitis and in periodontally healthy individuals: a cross-sectional study. J Periodontal Res 44:411–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teles R, Teles F, Frias-Lopez J, Paster B, Haffajee A (2013) Lessons learned and unlearned in periodontal microbiology. Periodontol 2000 62:95–162

    Article  PubMed  PubMed Central  Google Scholar 

  • Teng YT (2006a) Protective and destructive immunity in the periodontium: Part 1--innate and humoral immunity and the periodontium. J Dent Res 85:198–208

    Article  CAS  PubMed  Google Scholar 

  • Teng YT (2006b) Protective and destructive immunity in the periodontium: Part 2--T-cell-mediated immunity in the periodontium. J Dent Res 85:209–219

    Article  CAS  PubMed  Google Scholar 

  • Teng YT, Nguyen H, Gao X et al (2000) Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. J Clin Invest 106:R59–R67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teng YT, Mahamed D, Singh B (2005) Gamma interferon positively modulates Actinobacillus actinomycetemcomitans-specific RANKL+ CD4+ Th-cell-mediated alveolar bone destruction in vivo. Infect Immun 73:3453–3461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thumbigere-Math V, Michalowicz BS, Hodges JS et al (2014) Periodontal disease as a risk factor for bisphosphonate-related osteonecrosis of the jaw. J Periodontol 85:226–233

    Article  PubMed  Google Scholar 

  • Thunell DH, Tymkiw KD, Johnson GK et al (2010) A multiplex immunoassay demonstrates reductions in gingival crevicular fluid cytokines following initial periodontal therapy. J Periodontal Res 45:148–152

    Article  CAS  PubMed  Google Scholar 

  • Tjoa ST, de Vries TJ, Schoenmaker T, Kelder A, Loos BG, Everts V (2008) Formation of osteoclast-like cells from peripheral blood of periodontitis patients occurs without supplementation of macrophage colony-stimulating factor. J Clin Periodontol 35:568–575

    Article  CAS  PubMed  Google Scholar 

  • Tomomatsu N, Aoki K, Alles N et al (2009) LPS-induced inhibition of osteogenesis is TNF-alpha dependent in a murine tooth extraction model. J Bone Miner Res 24:1770–1781

    Article  CAS  PubMed  Google Scholar 

  • Tonetti MS, Mombelli A (1999) Early-onset periodontitis. Ann Periodontol 4:39–53

    Article  CAS  PubMed  Google Scholar 

  • Trombone AP, Ferreira SBJ, Raimundo FM et al (2009) Experimental periodontitis in mice selected for maximal or minimal inflammatory reactions: increased inflammatory immune responsiveness drives increased alveolar bone loss without enhancing the control of periodontal infection. J Periodontal Res 44:443–451

    Article  CAS  PubMed  Google Scholar 

  • Tymkiw KD, Thunell DH, Johnson GK et al (2011) Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol 38:219–228

    Article  CAS  PubMed  Google Scholar 

  • Ugar-Cankal D, Ozmeric N (2006) A multifaceted molecule, nitric oxide in oral and periodontal diseases. Clin Chim Acta 366:90–100

    Article  CAS  PubMed  Google Scholar 

  • Van Dyke TE, Hasturk H, Kantarci A et al (2015) Proresolving nanomedicines activate bone regeneration in periodontitis. J Dent Res 94:148–156

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verstappen J, Von den Hoff JW (2006) Tissue inhibitors of metalloproteinases (TIMPs): their biological functions and involvement in oral disease. J Dent Res 85:1074–1084

    Article  CAS  PubMed  Google Scholar 

  • Wang YH, Jiang J, Zhu Q et al (2010) Porphyromonas gingivalis lipids inhibit osteoblastic differentiation and function. Infect Immun 78:3726–3735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei S, Kitaura H, Zhou P, Ross FP, Teitelbaum SL (2005) IL-1 mediates TNF-induced osteoclastogenesis. J Clin Invest 115:282–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolff K (1972) The langerhans cell. Curr Probl Dermatol 4:79–145

    Article  CAS  PubMed  Google Scholar 

  • Yasuda H, Shima N, Nakagawa N et al (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci U S A 95:3597–3602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu JJ, Ruddy MJ, Wong GC et al (2007) An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood 109:3794–3802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zandbergen D, Slot DE, Cobb CM, Van der Weijden FA (2013) The clinical effect of scaling and root planing and the concomitant administration of systemic amoxicillin and metronidazole: a systematic review. J Periodontol 84:332–351

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Teng YT (2006) Interleukin-10 inhibits gram-negative-microbe-specific human receptor activator of NF-kappaB ligand-positive CD4 + −Th1-cell-associated alveolar bone loss in vivo. Infect Immun 74:4927–4931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong Y, Slade GD, Beck JD, Offenbacher S (2007) Gingival crevicular fluid interleukin-1beta, prostaglandin E2 and periodontal status in a community population. J Clin Periodontol 34:285–293

    Article  CAS  PubMed  Google Scholar 

  • Zhong Q, Ding C, Wang M, Sun Y, Xu Y (2012) Interleukin-10 gene polymorphisms and chronic/aggressive periodontitis susceptibility: a meta-analysis based on 14 case–control studies. Cytokine 60:47–54

    Article  CAS  PubMed  Google Scholar 

  • Zwerina J, Hayer S, Tohidast-Akrad M et al (2004) Single and combined inhibition of tumor necrosis factor, interleukin-1, and RANKL pathways in tumor necrosis factor-induced arthritis: effects on synovial inflammation, bone erosion, and cartilage destruction. Arthritis Rheum 50:277–290

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Periodontology, Faculty of Odontology, University of Malmö, Malmö, Sweden

    Kristina Bertl DMD, PhD, MSc & Andreas Stavropoulos DDS, PhD

  2. Division of Oral Surgery, University Clinic of Dentistry, Medical University of Vienna, Vienna, Austria

    Kristina Bertl DMD, PhD, MSc

  3. Department of Pathophysiology and Allergy Research, Center of Pathophysiology, Infectiology and Immunology, Medical University Vienna, Vienna, Austria

    Peter Pietschmann MD

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  1. Kristina Bertl DMD, PhD, MSc
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  2. Peter Pietschmann MD
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Correspondence to Kristina Bertl DMD, PhD, MSc .

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  1. Department of Pathophysiology and Allergy Research, Center for Pathophysiology, Infectiology and Immunology, Medical University of Vienna, Vienna, Austria

    Peter Pietschmann

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Bertl, K., Pietschmann, P., Stavropoulos, A. (2016). Osteoimmunological Aspects of Periodontal Diseases. In: Pietschmann, P. (eds) Principles of Osteoimmunology. Springer, Cham. https://doi.org/10.1007/978-3-319-34238-2_12

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