Roles of receptor activator of nuclear factor‐ κ B ligand (RANKL) and osteoprotegerin in periodontal health and disease
2007; Wiley; Volume: 43; Issue: 1 Linguagem: Inglês
10.1111/j.1600-0757.2006.00185.x
ISSN1600-0757
AutoresToshiyuki Nagasawa, Makoto Kiji, Reiko Yashiro, Doosadee Hormdee, Lu He, Melanie Kunze, Tomonari Suda, Geena Koshy, Hiroaki Kobayashi, Shigeru Oda, Hiroshi Nitta, Isao Ishikawa,
Tópico(s)NF-κB Signaling Pathways
ResumoPeriodontology 2000Volume 43, Issue 1 p. 65-84 Roles of receptor activator of nuclear factor-κB ligand (RANKL) and osteoprotegerin in periodontal health and disease Toshiyuki Nagasawa, Toshiyuki NagasawaSearch for more papers by this authorMakoto Kiji, Makoto KijiSearch for more papers by this authorReiko Yashiro, Reiko YashiroSearch for more papers by this authorDoosadee Hormdee, Doosadee HormdeeSearch for more papers by this authorHe Lu, He LuSearch for more papers by this authorMelanie Kunze, Melanie KunzeSearch for more papers by this authorTomonari Suda, Tomonari SudaSearch for more papers by this authorGeena Koshy, Geena KoshySearch for more papers by this authorHiroaki Kobayashi, Hiroaki KobayashiSearch for more papers by this authorShigeru Oda, Shigeru OdaSearch for more papers by this authorHiroshi Nitta, Hiroshi NittaSearch for more papers by this authorIsao Ishikawa, Isao IshikawaSearch for more papers by this author Toshiyuki Nagasawa, Toshiyuki NagasawaSearch for more papers by this authorMakoto Kiji, Makoto KijiSearch for more papers by this authorReiko Yashiro, Reiko YashiroSearch for more papers by this authorDoosadee Hormdee, Doosadee HormdeeSearch for more papers by this authorHe Lu, He LuSearch for more papers by this authorMelanie Kunze, Melanie KunzeSearch for more papers by this authorTomonari Suda, Tomonari SudaSearch for more papers by this authorGeena Koshy, Geena KoshySearch for more papers by this authorHiroaki Kobayashi, Hiroaki KobayashiSearch for more papers by this authorShigeru Oda, Shigeru OdaSearch for more papers by this authorHiroshi Nitta, Hiroshi NittaSearch for more papers by this authorIsao Ishikawa, Isao IshikawaSearch for more papers by this author First published: 04 January 2007 https://doi.org/10.1111/j.1600-0757.2006.00185.xCitations: 84Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat References 1 Abiko Y, Ogura N, Matsuda U, Yanagi K, Takiguchi H. A human monoclonal antibody which inhibits the coaggregation activity of Porphyromonas gingivalis. Infect Immun 1997: 65: 3966–3969. 10.1128/IAI.65.9.3966-3969.1997 CASPubMedWeb of Science®Google Scholar 2 Akbar AN, Lord JM, Salmon M. IFN-alpha and IFN-beta: a link between immune memory and chronic inflammation. Immunol Today 2000: 21: 337–342. 10.1016/S0167-5699(00)01652-2 CASPubMedWeb of Science®Google Scholar 3 Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001: 2: 675–680. 10.1038/90609 CASPubMedWeb of Science®Google Scholar 4 Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, Teepe MC, DuBose RF, Cosman D, Galibert L. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature 1997: 390: 175–179. 10.1038/36593 CASPubMedWeb of Science®Google Scholar 5 Aramaki M, Nagasawa T, Koseki T, Ishikawa I. Presence of activated B-1 cells in chronic inflamed gingival tissue. J Clin Immunol 1998: 18: 421–429. 10.1023/A:1023234823783 CASPubMedWeb of Science®Google Scholar 6 Arron JR, Choi Y. Bone versus immune system. Nature 2000: 408: 535–536. 10.1038/35046196 CASPubMedWeb of Science®Google Scholar 7 Arvin AM, Greenberg HB. New viral vaccines. Virology 2006: 344: 240–249. 10.1016/j.virol.2005.09.057 CASPubMedWeb of Science®Google Scholar 8 Bandeira A, Mota-Santos T, Itohara S, Degermann S, Heusser C, Tonegawa S, Coutinho A. Localization of gamma/delta T cells to the intestinal epithelium is independent of normal microbial colonization. J Exp Med 1990: 172: 239–244. 10.1084/jem.172.1.239 CASPubMedWeb of Science®Google Scholar 9 Barros SP, Silva MA, Somerman MJ, Nociti FH Jr. Parathyroid hormone protects against periodontitis-associated bone loss. J Dent Res 2003: 82: 791–795. 10.1177/154405910308201006 CASPubMedWeb of Science®Google Scholar 10 Baumgarth N, Tung JW, Herzenberg LA. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin Immunopathol 2005: 26: 347–362. 10.1007/s00281-004-0182-2 CASPubMedWeb of Science®Google Scholar 11 Beck JD, Eke P, Heiss G, Madianos P, Couper D, Lin D, Moss K, Elter J, Offenbacher S. Periodontal disease and coronary heart disease: a reappraisal of the exposure. Circulation 2005: 112: 19–24. 10.1161/CIRCULATIONAHA.104.511998 CASPubMedWeb of Science®Google Scholar 12 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: 342–351. 10.1128/IAI.73.1.342-351.2005 CASPubMedWeb of Science®Google Scholar 13 Belibasakis GN, Johansson A, Wang Y, Chen C, Lagergard T, Kalfas S, Lerner UH. Cytokine responses of human gingival fibroblasts to Actinobacillus actinomycetemcomitans cytolethal distending toxin. Cytokine 2005: 30: 56–63. 10.1016/j.cyto.2004.11.008 CASPubMedWeb of Science®Google Scholar 14 Berglundh T, Liljenberg B, Tarkowski A, Lindhe J. The presence of local and circulating autoreactive B cells in patients with advanced periodontitis. J Clin Periodontol 2002: 29: 281–286. 10.1034/j.1600-051X.2002.290402.x CASPubMedWeb of Science®Google Scholar 15 Berland R, Wortis HH. Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol 2002: 20: 253–300. 10.1146/annurev.immunol.20.100301.064833 CASPubMedWeb of Science®Google Scholar 16 Bharadwaj M, Moss DJ. Epstein–Barr virus vaccine: a cytotoxic T-cell-based approach. Expert Rev Vaccines 2002: 1: 467–476. 10.1586/14760584.1.4.467 CASPubMedGoogle Scholar 17 Booth V, Ashley FP, Lehner T. Passive immunization with monoclonal antibodies against Porphyromonas gingivalis in patients with periodontitis. Infect Immun 1996: 64: 422–427. 10.1128/IAI.64.2.422-427.1996 CASPubMedWeb of Science®Google Scholar 18 Bosshardt DD, Lang NP. The junctional epithelium: from health to disease. J Dent Res 2005: 84: 9–20. 10.1177/154405910508400102 CASPubMedWeb of Science®Google Scholar 19 Boutsi EA, Umeda M, Nagasawa T, Laosrisin N, Ishikawa I. Follow-up of two cases of Papillon–Lefèvre syndrome and presentation of two new cases. Int J Periodontics Restorative Dent 1997: 17: 334–347. CASPubMedGoogle Scholar 20 Brandtzaeg P, Johansen FE. Mucosal B cells: phenotypic characteristics, transcriptional regulation, and homing properties. Immunol Rev 2005: 206: 32–63. 10.1111/j.0105-2896.2005.00283.x CASPubMedWeb of Science®Google Scholar 21 Brouty-Boye D, Doucet C, Clay D, Le Bousse-Kerdiles MC, Lampidis TJ, Azzarone B. Phenotypic diversity in human fibroblasts from myelometaplasic and non-myelometaplasic hematopoietic tissues. Int J Cancer 1998: 76: 767–773. 10.1002/(SICI)1097-0215(19980529)76:5 3.0.CO;2-# CASPubMedWeb of Science®Google Scholar 22 Brouty-Boye D, Magnien V. Myofibroblast and concurrent ED-B fibronectin phenotype in human stromal cells cultured from non-malignant and malignant breast tissue. Eur J Cancer 1994: 30A: 66–73. 10.1016/S0959-8049(05)80021-8 CASPubMedWeb of Science®Google Scholar 23 Brouty-Boye D, Pottin-Clemenceau C, Doucet C, Jasmin C, Azzarone B. Chemokines and CD40 expression in human fibroblasts. Eur J Immunol 2000: 30: 914–919. 10.1002/1521-4141(200003)30:3 3.0.CO;2-D CASPubMedWeb of Science®Google Scholar 24 Castigli E, Fuleihan R, Ramesh N, Tsitsikov E, Tsytsykova A, Geha RS. CD40 ligand/CD40 deficiency. Int Arch Allergy Immunol 1995: 107: 37–39. 10.1159/000236923 CASPubMedWeb of Science®Google Scholar 25 Choi BK, Moon SY, Cha JH, Kim KW, Yoo YJ. Prostaglandin E(2) is a main mediator in receptor activator of nuclear factor-kappaB ligand-dependent osteoclastogenesis induced by Porphyromonas gingivalis, Treponema denticola, and Treponema socranskii. J Periodontol 2005: 76: 813–820. 10.1902/jop.2005.76.5.813 CASPubMedWeb of Science®Google Scholar 26 Choi Y, Woo KM, Ko SH, Lee YJ, Park SJ, Kim HM, Kwon BS. Osteoclastogenesis is enhanced by activated B cells but suppressed by activated CD8(+) T cells. Eur J Immunol 2001: 31: 2179–2188. 10.1002/1521-4141(200107)31:7 3.0.CO;2-X CASPubMedWeb of Science®Google Scholar 27 Colombo AP, Teles RP, Torres MC, Rosalem W, Mendes MC, Souto RM, Uzeda M. Effects of non-surgical mechanical therapy on the subgingival microbiota of Brazilians with untreated chronic periodontitis: 9-month results. J Periodontol 2005: 76: 778–784. 10.1902/jop.2005.76.5.778 PubMedWeb of Science®Google Scholar 28 Crawford JM. Distribution of ICAM-1, LFA-3 and HLA-DR in healthy and diseased gingival tissues. J Periodontal Res 1992: 27: 291–298. 10.1111/j.1600-0765.1992.tb01680.x PubMedWeb of Science®Google Scholar 29 Crotti T, Smith MD, Hirsch R, Soukoulis S, Weedon H, Capone M, Ahern MJ, Haynes D. Receptor activator NF kappaB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. J Periodontal Res 2003: 38: 380–387. 10.1034/j.1600-0765.2003.00615.x CASPubMedWeb of Science®Google Scholar 30 Das G, Janeway CA Jr. MHC specificity of iIELs. Trends Immunol 2003: 24: 88–93. 10.1016/S1471-4906(02)00036-4 CASPubMedWeb of Science®Google Scholar 31 De Brito RB Jr, Scarel-Caminaga RM, Trevilatto PC, De Souza AP, Barros SP. Polymorphisms in the vitamin D receptor gene are associated with periodontal disease. J Periodontol 2004: 75: 1090–1095. 10.1902/jop.2004.75.8.1090 CASPubMedWeb of Science®Google Scholar 32 Dennison DK, Van Dyke TE. The acute inflammatory response and the role of phagocytic cells in periodontal health and disease. Periodontol 2000 1997: 14: 54–78. 10.1111/j.1600-0757.1997.tb00192.x CASPubMedWeb of Science®Google Scholar 33 Dongari-Bagtzoglou AI, Warren WD, Berton MT, Ebersole JL. CD40 expression by gingival fibroblasts: correlation of phenotype with function. Int Immunol 1997: 9: 1233–1241. 10.1093/intimm/9.9.1233 CASPubMedWeb of Science®Google Scholar 34 Doucet C, Meazza R, Pottin-Clemenceau C, Scudeletti M, Brouty-Boye D, Ferrini S, Alileche A, Taoufik Y, Jasmin C, Azzarone B, Indiveri F. Role of interleukin (IL)-2 and IL-15 in the tumour progression of a melanoma cell line MELP, derived from an IL-2 progressor patient. Melanoma Res 1997: 7 (Suppl. 2): S7–S17. CASPubMedWeb of Science®Google Scholar 35 Esposito M, Coulthard P, Worthington HV. Enamel matrix derivative (Emdogain) for periodontal tissue regeneration in intrabony defects. Cochrane Database Syst Rev 2003: CD003875. CASPubMedGoogle Scholar 36 Evans RT, Klausen B, Sojar HT, Bedi GS, Sfintescu C, Ramamurthy NS, Golub LM, Genco RJ. Immunization with Porphyromonas (Bacteroides) gingivalis fimbriae protects against periodontal destruction. Infect Immun 1992: 60: 2926–2935. 10.1128/IAI.60.7.2926-2935.1992 CASPubMedWeb of Science®Google Scholar 37 Fan Q, Sims T, Sojar H, Genco R, Page RC. Fimbriae of Porphyromonas gingivalis induce opsonic antibodies that significantly enhance phagocytosis and killing by human polymorphonuclear leukocytes. Oral Microbiol Immunol 2001: 16: 144–152. 10.1034/j.1399-302x.2001.016003144.x CASPubMedWeb of Science®Google Scholar 38 Frankenthal S, Nakhoul F, Machtei EE, Green J, Ardekian L, Laufer D, Peled M. The effect of secondary hyperparathyroidism and hemodialysis therapy on alveolar bone and periodontium. J Clin Periodontol 2002: 29: 479–483. 10.1034/j.1600-051X.2002.290601.x CASPubMedWeb of Science®Google Scholar 39 Fries KM, Sempowski GD, Gaspari AA, Blieden T, Looney RJ, Phipps RP. CD40 expression by human fibroblasts. Clin Immunol Immunopathol 1995: 77: 42–51. 10.1016/0090-1229(95)90135-3 CASPubMedWeb of Science®Google Scholar 40 Fu Q, Jilka RL, Manolagas SC, O'Brien CA. Parathyroid hormone stimulates receptor activator of NFkappa B ligand and inhibits osteoprotegerin expression via protein kinase A activation of cAMP-response element-binding protein. J Biol Chem 2002: 277: 48868–48875. 10.1074/jbc.M208494200 CASPubMedWeb of Science®Google Scholar 41 Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol 1996: 67: 1041–1049. 10.1902/jop.1996.67.10s.1041 CASPubMedWeb of Science®Google Scholar 42 Gestrelius S, Lyngstadaas SP, Hammarstrom L. Emdogain–periodontal regeneration based on biomimicry. Clin Oral Investig 2000: 4: 120–125. 10.1007/s007840050127 CASPubMedGoogle Scholar 43 Guo S, Takahashi K, Kokeguchi S, Takashiba S, Kinane DF, Murayama Y. Antibody responses against Porphyromonas gingivalis infection in patients with early-onset periodontitis. J Clin Periodontol 2000: 27: 769–777. 10.1034/j.1600-051x.2000.027010769.x CASPubMedWeb of Science®Google Scholar 44 Halladay DL, Miles RR, Thirunavukkarasu K, Chandrasekhar S, Martin TJ, Onyia JE. Identification of signal transduction pathways and promoter sequences that mediate parathyroid hormone 1–38 inhibition of osteoprotegerin gene expression. J Cell Biochem 2001: 84: 1–11. 10.1002/jcb.1273 CASPubMedWeb of Science®Google Scholar 45 Han X, Amar S. Identification of genes differentially expressed in cultured human periodontal ligament fibroblasts vs. human gingival fibroblasts by DNA microarray analysis. J Dent Res 2002: 102: 1421–1427. Google Scholar 46 Hasegawa T, Yoshimura Y, Kikuiri T, Yawaka Y, Takeyama S, Matsumoto A, Oguchi H, Shirakawa T. Expression of receptor activator of NF-kappa B ligand and osteoprotegerin in culture of human periodontal ligament cells. J Periodontal Res 2002: 37: 405–411. 10.1034/j.1600-0765.2002.01603.x CASPubMedWeb of Science®Google Scholar 47 Hatakeyama J, Sreenath T, Hatakeyama Y, Thyagarajan T, Shum L, Gibson CW, Wright JT, Kulkarni AB. The receptor activator of nuclear factor-kappa B ligand-mediated osteodastogenic pathway is elevated in amelogenin-null mice. J Biol Chem 2003: 278: 35743–35748. 10.1074/jbc.M306284200 Google Scholar 48 Hennig BJ, Parkhill JM, Chapple IL, Heasman PA, Taylor JJ. Association of a vitamin D receptor gene polymorphism with localized early-onset periodontal diseases. J Periodontol 1999: 70: 1032–1038. 10.1902/jop.1999.70.9.1032 CASPubMedWeb of Science®Google Scholar 49 Horibe M, Watanabe H, Ishikawa I. Effect of periodontal treatments on serum IgG antibody titers against periodontopathic bacteria. J Clin Periodontol 1995: 22: 510–515. 10.1111/j.1600-051X.1995.tb00798.x CASPubMedWeb of Science®Google Scholar 50 Hormdee D, Nagasawa T, Kiji M, Yashiro R, Kobayashi H, Koshy G, Noguchi K, Nitta H, Ishikawa I. Protein kinase-A-dependent osteoprotegerin production on IL-1 stimulation in human gingival fibroblasts is distinct from periodontal ligament fibroblasts. Clin Exp Immunol 2005: 142: 490–497. 10.1111/j.1365-2249.2005.02937.x CASPubMedWeb of Science®Google Scholar 51 Horwood NJ, Kartsogannis V, Quinn JMW, Romas E, Martin TJ, Gillespie MT. Activated T lymphocytes support osteoclast formation in vitro. Biochem Biophys Res Commun 1999: 265: 144–150. 10.1006/bbrc.1999.1623 CASPubMedWeb of Science®Google Scholar 52 Huang JC, Sakata T, Pfleger LL, Bencsik M, Halloran BP, Bikle DD, Nissenson RA. Parathyroid hormone differentially regulates expression of RANKL and OPG. J Bone Miner Res 2004: 19: 235–244. 10.1359/JBMR.0301226 CASPubMedWeb of Science®Google Scholar 53 Ishikawa I, Nakashima K, Koseki T, Nagasawa T, Watanabe H, Arakawa S, Nitta H, Nishihara T. Induction of the immune response to periodontopathic bacteria and its role in the pathogenesis of periodontitis. Periodontol 2000 1997: 14: 79–111. 10.1111/j.1600-0757.1997.tb00193.x CASPubMedWeb of Science®Google Scholar 54 Ishikawa I, Umeda M, Laosrisin N. Clinical, bacteriological, and immunological examinations and the treatment process of two Papillon–Lefèvre syndrome patients. J Periodontol 1994: 65: 364–371. 10.1902/jop.1994.65.4.364 CASPubMedWeb of Science®Google Scholar 55 Janeway CA Jr. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today 1992: 13: 11–16. 10.1016/0167-5699(92)90198-G CASPubMedWeb of Science®Google Scholar 56 Joisen R, Wong BR, Li HL, Steinman RM, Choi Y. TRANCE, a TNF family member, is differentially expressed on T cell subsets and induces cytokine production in dendritic cells. J Immunol 1999: 162: 2562–2568. PubMedWeb of Science®Google Scholar 57 Kalpidis CD, Ruben MP. Treatment of intrabony periodontal defects with enamel matrix derivative: a literature review. J Periodontol 2002: 73: 1360–1376. 10.1902/jop.2002.73.11.1360 PubMedWeb of Science®Google Scholar 58 Kanamaru F, Iwai H, Ikeda T, Nakajima A, Ishikawa I, Azuma M. Expression of membrane-bound and soluble receptor activator of NF-kappaB ligand (RANKL) in human T cells. Immunol Lett 2004: 94: 239–246. 10.1016/j.imlet.2004.05.010 CASPubMedWeb of Science®Google Scholar 59 Kanzaki H, Chiba M, Shimizu Y, Mitani H. Periodontal ligament cells under mechanical stress induce osteoclastogenesis by receptor activator of nuclear factor kappaB ligand up-regulation via prostaglandin E2 synthesis. J Bone Miner Res 2002: 17: 210–220. 10.1359/jbmr.2002.17.2.210 CASPubMedWeb of Science®Google Scholar 60 Kanzaki H, Chiba M, Shimizu Y, Mitani H. Dual regulation of osteoclast differentiation by periodontal ligament cells through RANKL stimulation and OPG inhibition. J Dent Res 2001: 80: 887–891. 10.1177/00220345010800030801 CASPubMedWeb of Science®Google Scholar 61 Kennedy JE, Bird WC, Palcanis KG, Dorfman HS. A longitudinal evaluation of varying widths of attached gingiva. J Clin Periodontol 1985: 12: 667–675. 10.1111/j.1600-051X.1985.tb00938.x CASPubMedWeb of Science®Google Scholar 62 Kikuchi T, Yoshikai Y, Miyoshi J, Katsuki M, Musikacharoen T, Mitani A, Tanaka S, Noguchi T, Matsuguchi T. Cot/Tpl2 is essential for RANKL induction by lipid A in osteoblasts. J Dent Res 2003: 82: 546–550. 10.1177/154405910308200712 CASPubMedWeb of Science®Google Scholar 63 Kim S, Koga T, Isobe M, Kern BE, Yokochi T, Chin YE, Karesenty G, Taniguchi T, Takayanagi H. Stat1 functions as a cytoplasmic attenuator of Runx2 in transcriptional program of osteoblast differentiation. Genes Dev 2003: 17: 1979–1991. 10.1101/gad.1119303 CASPubMedWeb of Science®Google Scholar 64 Kinane DF, Lappin DF, Koulouri O, Buckley A. Humoral immune responses in periodontal disease may have mucosal and systemic immune features. Clin Exp Immunol 1999: 115: 534–541. 10.1046/j.1365-2249.1999.00819.x CASPubMedWeb of Science®Google Scholar 65 Kobayashi-Sakamoto M, Hirose K, Isogai E, Chiba I. NF-kappaB-dependent induction of osteoprotegerin by Porphyromonas gingivalis in endothelial cells. Biochem Biophys Res Commun 2004: 315: 107–112. 10.1016/j.bbrc.2004.01.024 CASPubMedWeb of Science®Google Scholar 66 Kojima T, Yano K, Ishikawa I. Relationship between serum antibody levels and subgingival colonization of Porphyromonas gingivalis in patients with various types of periodontitis. J Periodontol 1997: 68: 618–625. 10.1902/jop.1997.68.7.618 CASPubMedWeb of Science®Google Scholar 67 Kondo H, Guo J, Bringhurst FR. Cyclic adenosine monophosphate/protein kinase A mediates parathyroid hormone/parathyroid hormone-related protein receptor regulation of osteoclastogenesis and expression of RANKL and osteoprotegerin mRNAs by marrow stromal cells. J Bone Miner Res 2002: 17: 1667–1679. 10.1359/jbmr.2002.17.9.1667 CASPubMedWeb of Science®Google Scholar 68 Kong Y-Y, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, Moran E, Bogoch ER, Van G, Nguyen LT, Ohashi PS, Lacey DL, Fish E, Boyle W, Penninger JM. Activated T cells regulate bone loss and joint destruction in adjyuvant arthritis through osteoprotegerin ligand. Nature 1999: 402: 304–309. 10.1038/46303 CASPubMedWeb of Science®Google Scholar 69 Kong Y-Y, Yoshida H, Sarosi I, Tan H-L, Timms E, Capparelli C, Morony S, Oliveira-dos-Santos AJ, Van G, Itie A, Khoo W, Wakeham A, Dunstan CR, Lacey DL, Mak TW, Boyle WJ, Penninger JM. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 1999: 397: 315–323. 10.1038/16852 CASPubMedWeb of Science®Google Scholar 70 Kroese FG, Butcher EC, Stall AM, Lalor PA, Adams S, Herzenberg LA. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int Immunol 1989: 1: 75–84. 10.1093/intimm/1.1.75 CASPubMedWeb of Science®Google Scholar 71 Kroese FG, De Waard R, Bos NA. B-1 cells and their reactivity with the murine intestinal microflora. Semin Immunol 1996: 8: 11–18. 10.1006/smim.1996.0003 CASPubMedGoogle Scholar 72 Kronstrom M, Svensson B, Erickson E, Houston L, Braham P, Persson GR. Humoral immunity host factors in subjects with failing or successful titanium dental implants. J Clin Periodontol 2000: 27: 875–882. 10.1034/j.1600-051x.2000.027012875.x CASPubMedWeb of Science®Google Scholar 73 Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 1998: 93: 165–176. 10.1016/S0092-8674(00)81569-X CASPubMedWeb of Science®Google Scholar 74 Lang NP, Loe H. The relationship between the width of keratinized gingiva and gingival health. J Periodontol 1972: 43: 623–627. 10.1902/jop.1972.43.10.623 CASPubMedWeb of Science®Google Scholar 75 Lanske B, Karaplis AC, Lee K, Luz A, Vortkamp A, Pirro A, Karperien M, Defize LH, Ho C, Mulligan RC, Abou-Samra AB, Juppner H, Segre GV, Kronenberg HM. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science 1996: 273: 663–666. 10.1126/science.273.5275.663 CASPubMedWeb of Science®Google Scholar 76 Lappin DF, McGregor AM, Kinane DF. The systemic immune response is more prominent than the mucosal immune response in the pathogenesis of periodontal disease. J Clin Periodontol 2003: 30: 778–786. 10.1034/j.1600-051X.2003.00372.x CASPubMedWeb of Science®Google Scholar 77 Liljenberg B, Lindhe J. Juvenile periodontitis. Some microbiological, histopathological and clinical characteristics. J Clin Periodontol 1980: 7: 48–61. 10.1111/j.1600-051X.1980.tb01948.x PubMedWeb of Science®Google Scholar 78 Liu BY, Guo J, Lanske B, Divieti P, Kronenberg HM, Bringhurst FR. Conditionally immortalized murine bone marrow stromal cells mediate parathyroid hormone-dependent osteoclastogenesis in vitro. Endocrinology 1998: 139: 1952–1964. 10.1210/en.139.4.1952 CASPubMedWeb of Science®Google Scholar 79 Liu D, Xu JK, Figliomeni L, Huang L, Pavlos NJ, Rogers M, Tan A, Price P, Zheng MH. Expression of RANKL and OPG mRNA in periodontal disease: possible involvement in bone destruction. Int J Mol Med 2003: 11: 17–21. PubMedWeb of Science®Google Scholar 80 Lopes V, Young LS, Murray PG. Epstein–Barr virus-associated cancers: aetiology and treatment. Herpes 2003: 10: 78–82. PubMedGoogle Scholar 81 Lu H, Wang M, Gunsolley JC, Schenkein HA, Tew JG. Serum immunoglobulin G subclass concentrations in periodontally healthy and diseased individuals. Infect Immun 1994: 62: 1677–1682. 10.1128/IAI.62.5.1677-1682.1994 CASPubMedWeb of Science®Google Scholar 82 Lundqvist C, Baranov V, Teglund S, Hammarstrom S, Hammarstrom ML. Cytokine profile and ultrastructure of intraepithelial gamma delta T cells in chronically inflamed human gingiva suggest a cytotoxic effector function. J Immunol 1994: 153: 2302–2312. 10.4049/jimmunol.153.5.2302 CASPubMedWeb of Science®Google Scholar 83 Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 2000: 288: 2222–2226. 10.1126/science.288.5474.2222 CASPubMedWeb of Science®Google Scholar 84 Mahanonda R, Seymour GJ, Powell LW, Good MF, Halliday JW. Effect of initial treatment of chronic inflammatory periodontal disease on the frequency of peripheral blood T-lymphocytes specific to periodontopathic bacteria. Oral Microbiol Immunol 1991: 6: 221–227. 10.1111/j.1399-302X.1991.tb00481.x PubMedWeb of Science®Google Scholar 85 Mahanonda R, Seymour GJ, Powell LW, Good MF, Halliday JW. Limit dilution analysis of peripheral blood T lymphocytes specific to periodontopathic bacteria. Clin Exp Immunol 1989: 75: 245–2451. PubMedWeb of Science®Google Scholar 86 Marques MR, De Silva MA, Manzi FR, Cesar-Neto JB, Nociti FH Jr, Barros SP. Effect of intermittent PTH administration in the periodontitis-associated bone loss in ovariectomized rats. Arch Oral Biol 2004: 50: 421–429. 10.1016/j.archoralbio.2004.08.014 CASPubMedWeb of Science®Google Scholar 87 McDermott MR, Bienenstock J. Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J Immunol 1979: 122: 1892–1898. CASPubMedWeb of Science®Google Scholar 88 Mizuno N, Shiba H, Mouri Y, Xu W, Kudoh S, Kawaguchi H, Kurihara H. Characterization of epithelial cells derived from periodontal ligament by gene expression patterns of bone-related and enamel proteins. Cell Biol Int 2005: 29: 111–117. 10.1016/j.cellbi.2004.11.012 CASPubMedWeb of Science®Google Scholar 89 Mogi M, Otogoto J, Ota N, Togari A. Differential expression of RANKL and osteoprotegerin in gingival crevicular fluid of patients with periodontitis. J Dent Res 2004: 83: 166–169. 10.1177/154405910408300216 CASPubMedWeb of Science®Google Scholar 90 Moughal NA, Adonogianaki E, Thornhill MH, Kinane DF. Endothelial cell leukocyte adhesion molecule-1 (ELAM-1) and intercellular adhesion molecule-1 (ICAM-1) expression in gingival tissue during health and experimentally-induced gingivitis. J Periodontal Res 1992: 27: 623–630. 10.1111/j.1600-0765.1992.tb01746.x CASPubMedWeb of Science®Google Scholar 91 Muller-Glauser W, Schroeder HE. The pocket epithelium: a light- and electronmicroscopic study. J Periodontol 1982: 53: 133–144. 10.1902/jop.1982.53.3.133 PubMedWeb of Science®Google Scholar 92 Nagasawa T, Aramaki M, Takamatsu N, Koseki T, Kobayashi H, Ishikawa I. Oral administration of Porphyromonas gingivalis fimbriae with cholera toxin induces anti-fimbriae serum IgG, IgM, IgA and salivary IgA antibodies. J Periodontal Res 1999: 34: 169–174. 10.1111/j.1600-0765.1999.tb02238.x CASPubMedWeb of Science®Google Scholar 93 Nagasawa T, Kobayashi H, Kiji M, Aramaki M, Mahanonda R, Kojima T, Murakami Y, Saito M, Morotome Y, Ishikawa I. LPS-stimulated human gingival fibroblasts inhibit the differentiation of monocytes into osteoclasts through the production of osteoprotegerin. Clin Exp Immunol 2002: 130: 338–344. 10.1046/j.1365-2249.2002.01990.x CASPubMedWeb of Science®Google Scholar 94 Nagasawa T, Sano K, Ike F, Kishimoto H, Nakayama T, Asano Y, Ishikawa I, Tada T. Negative selection of thymus-dependent CD4+8+ intestinal intraepithelial lymphocytes by internal superantigens. Cell Immunol 1993: 147: 158–166. 10.1006/cimm.1993.1056 CASPubMedWeb of Science®Google Scholar 95 Nordin U, Wannfors K, Colque-Navarro P, Mollby R, Heimdahl A. Antibody response in patients with osteomyelitis of the mandible. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995: 79: 429–435. 10.1016/S1079-2104(05)80122-2 CASPubMedWeb of Science®Google Scholar 96
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