Archives of Oral Biology
Volume 54, Issue 8 , Pages 723-729 , August 2009

A single application of hydrogen sulphide induces a transient osteoclast differentiation with RANKL expression in the rat model

  • Koichiro Irie

      Affiliations

    • Department of Preventive Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Okayama 700-8525, Japan
  • ,
  • Daisuke Ekuni

      Affiliations

    • Department of Preventive Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Okayama 700-8525, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 86 235 6712; fax: +81 86 235 6714.
  • ,
  • Tatsuo Yamamoto

      Affiliations

    • Department of Dental Sociology, Division of Sociological Approach in Dentistry, Kanagawa Dental College, 82 Inaoka-cho, Yokosuka 238-8580, Japan
  • ,
  • Manabu Morita

      Affiliations

    • Department of Preventive Dentistry, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, 2-5-1 Shikata-cho, Okayama 700-8525, Japan
  • ,
  • Ken Yaegaki

      Affiliations

    • Department of Oral Biological and Medical Sciences, Faculty of Dentistry, University of British Columbia, Canada
    • Department of Oral Health, School of Life Dentistry, Nippon Dental University, Japan
  • ,
  • Hisataka Ii

      Affiliations

    • Department of Oral Health, School of Life Dentistry, Nippon Dental University, Japan
  • ,
  • Toshio Imai

      Affiliations

    • Department of Oral Health, School of Life Dentistry, Nippon Dental University, Japan

,Accepted 14 May 2009.

References 

  1. Tonzetich J. Production and origin of oral malodor: a review of mechanisms and methods of analysis. J Periodontol. 1977;48:13–20
  2. Yaegaki K, Sanada K. Biochemical and clinical factors influencing oral malodor in periodontal patients. J Periodontol. 1992;63:783–789
  3. Genco RJ, Zambon JJ, Christersson LA. The origin of periodontal infections. Adv Dent Res. 1988;2:245–259
  4. Ratcliff PA, Johson PW. The relationship between oral malodour, gingivitis, and periodontitis. A review. J Periodontol. 1999;70:485–489
  5. Ng W, Tonzetich J. Effect of hydrogen sulfide and methyl mercaptan on the permeability of oral mucosa. J Dent Res. 1984;63:994–997
  6. Ratkay LG, Waterfield JD, Tonzetich J. Stimulation of enzyme and cytokine production by methyl mercaptan in human gingival fibroblast and monocyte cell cultures. Arch Oral Biol. 1995;40:337–344
  7. Johnson P, Yaegaki K, Tonzetich J. Effect of methyl mercaptan on synthesis and degradation of collagen. J Periodontal Res. 1996;31:323–329
  8. Yaegaki K, Qian W, Murata T, Imai T, Sato T, Tanaka T, et al. Oral malodorous compound causes apoptosis and genomic DNA damage in human gingival fibroblasts. J Periodontal Res. 2008;43:391–399
  9. Yaegaki K. Oral malodor and periodontal disease. In:  Rosenberg M editors. Bad breath; research perspectives. Tel Aviv: Ramot Publishing-Tel Aviv University; 1995;p. 87–108
  10. Takeuchi H, Setoguchi T, Machigashira M, Kanbara K, Izumi Y. Hydrogen sulfide inhibits cell proliferation and induces cell cycle arrest via an elevated p21 Cip1 level in Ca9-22 cells. J Periodontal Res. 2008;43:90–95
  11. Bhatia M, Sidhapuriwala J, Moochhala SM, Moore PK. Hydrogen sulphide is a mediator of carrageenan-induced hindpaw oedema in the rat. Br J Pharmacol. 2005;145:141–144
  12. Dal-Secco D, Cunha TM, Freitas A, Alves-Filho JC, Souto FO, Fukada SY, et al. Hydrogen sulfide augments neutrophil migration through enhancement of adhesion molecule expression and prevention of CXCR2 internalization: role of ATP-sensitive potassium channels. J Immunol. 2008;181:4287–4298
  13. Zhi L, Ang AD, Zhang H, Moore PK, Bhatia M. Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-kappaB pathway. J Leukoc Biol. 2007;81:1322–1332
  14. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397:315–323
  15. Ekuni D, Tomofuji T, Yamanaka R, Tachibana K, Yamamoto T, Watanabe T. Initial apical migration of junctional epithelium in rats following application of lipopolysaccharide and proteases. J Periodontol. 2005;76:43–48
  16. Irie K, Tomofuji T, Tamaki N, Sanbe T, Ekuni D, Azuma T, et al. Effects of ethanol consumption on periodontal inflammation in rats. J Dent Res. 2008;87:456–460
  17. Kawamoto S, Ejiri S, Hoshi K, Nagaoka E, Ozawa H. Immunolocalization of osteoclast differentiation factor in rat periodontium. Arch Oral Biol. 2000;47:55–58
  18. Tomofuji T, Kusano H, Azuma T, Ekuni D, Yamamoto T, Watanabe T. Effects of a high-cholesterol diet on cell behavior in rat periodontitis. J Dent Res. 2005;84:752–756
  19. Sanbe T, Tomofuji T, Ekuni D, Azuma T, Tamaki N, Yamamoto T. Oral administration of vitamin C prevents alveolar bone resorption induced by high dietary cholesterol in rats. J Periodontol. 2007;78:2165–2170
  20. Yu H, Wu SD. Activation of TLR-4 and liver injury via NF-kappa B in rat with acute cholangitis. Hepatobiliary Pancreat Dis Int. 2008;7:185–191
  21. de Amorim FP, Ornelas SS, Diniz SF, Batista AC, da Silva TA. Imbalance of RANK, RANKL and OPG expression during tibial fracture repair in diabetic rats. J Mol Histol. 2008;39:401–408
  22. Sadi G, Yilmaz O, Güray T. Effect of vitamin C and lipoic acid on streptozotocin-induced diabetes gene expression: mRNA and protein expressions of Cu–Zn SOD and catalase. Mol Cell Biochem. 2008;309:109–116
  23. Ekuni D, Firth JD, Putnins EE. RNA integrity and in situ RT-PCR in dento-alveolar tissues after microwave accelerated demineralisation. Arch Oral Biol. 2006;51:164–169
  24. Nakajima K, Hamada N, Takahashi Y, Sasaguri K, Tsukinoki K, Umemoto T, et al. Restraint stress enhances alveolar bone loss in an experimental rat model. J Periodontal Res. 2006;41:527–534
  25. Ekuni D, Tomofuji T, Tamaki N, Sanbe T, Azuma T, Yamanaka R, et al. Mechanical stimulation of gingiva reduces plasma 8-OHdG level in rat periodontitis. Arch Oral Biol. 2008;53:324–329
  26. Persson S. Hydrogen sulfide and methyl mercaptan in periodontal pockets. Oral Microbiol Immunol. 1992;7:378–379
  27. Kobayashi K, Takahashi N, Jimi E, Udagawa N, Takami M, Kotake S, et al. Tumor necrosis factor alpha stimulates osteoclast differentiation by a mechanism independent of the ODF/RANKL–RANK interaction. J Exp Med. 2000;191:275–286
  28. Li L, Bhatia M, Zhu YZ, Zhu YC, Ramnath RD, Wang ZJ, et al. Hydrogen sulfide is a novel mediator of lipopolysaccharide-induced inflammation in the mouse. FASEB J. 2005;19:1196–1198
  29. Boyce BF, Xing L. Functions of RANKL/RANK/OPG in bone modeling and remodeling. Arch Biochem Biophys. 2008;473:139–146
  30. Zhang H, Zhi L, Moochhala S, Moore PK, Bhatia M. Hydrogen sulfide acts as an inflammatory mediator in cecal ligation and puncture-induced sepsis in mice by upregulating the production of cytokines and chemokines via NF-kappaB. Am J Physiol Lung Cell Mol Physiol. 2007;292:L960–L971
  31. Suda K, Woo JT, Takami M, Sexton PM, Nagai K. Lipopolysaccharide supports survival and fusion of preosteoclasts independent of TNF-alpha, IL-1, and RANKL. J Cell Physiol. 2002;190:101–108
  32. Udagawa N. Mechanisms involved in bone resorption. Biogerontology. 2002;3:79–83
  33. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, et al. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA. 1998;95:3597–3602
  34. Kieslinger M, Folberth S, Dobreva G, Dorn T, Croci L, Erben R, et al. EBF2 regulates osteoblast-dependent differentiation of osteoclasts. Dev Cell. 2005;9:757–767
  35. Florin T, Neale G, Gibson GR, Christl SU, Cummings JH. Metabolism of dietary sulphate: absorption and excretion in humans. Gut. 1991;32:766–773
  36. Morita M, Wang HL. Relationship of sulcular sulfide level to severity of periodontal disease and BANA test. J Periodontol. 2001;72:74–78
  37. Deplancke B, Gaskins HR. Hydrogen sulfide induces serum-independent cell cycle entry in nontransformed rat intestinal epithelial cells. FASEB J. 2003;17:1310–1312
  38. Hongfang J, Cong B, Zhao B, Zhang C, Liu X, Zhou W, et al. Effects of hydrogen sulfide on hypoxic pulmonary vascular structural remodeling. Life Sci. 2006;78:1299–1309
  39. Blom HJ, Tangerman A. Methanethiol metabolism in whole blood. J Lab Clin Med. 1988;111:606–610

PII: S0003-9969(09)00126-5

doi: 10.1016/j.archoralbio.2009.05.006

Archives of Oral Biology
Volume 54, Issue 8 , Pages 723-729 , August 2009