Archives of Oral Biology
Volume 54, Issue 8 , Pages 749-756 , August 2009

Trehalose inhibits inflammatory cytokine production by protecting IκB-α reduction in mouse peritoneal macrophages

  • Kahoru Taya

      Affiliations

    • Division of Dental Pharmacology, Department of Oral Medical Science, Ohu University School of Dentistry, Koriyama, Fukushima 963-8611, Japan
  • ,
  • Kimiharu Hirose

      Affiliations

    • Division of Preventive Dentistry, Department of Oral Health, Ohu University School of Dentistry, Koriyama, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 24 932 8982; fax: +81 24 932 8983.
  • ,
  • Setsuo Hamada

      Affiliations

    • Division of Dental Pharmacology, Department of Oral Medical Science, Ohu University School of Dentistry, Koriyama, Fukushima 963-8611, Japan

,Accepted 3 May 2009.

References 

  1. Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000. 1994;5:78–111
  2. Slots J, Bragd L, Wikstrom M, Dahlen G. The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Bacteroides intermedius in destructive periodontal disease in adults. J Clin Periodontol. 1986;13:570–577
  3. Dzink JL, Socransky SS, Haffajee AD. The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol. 1988;15:316–323
  4. Birkedal-Hansen H. Role of cytokines and inflammatory mediator in tissue destruction. J Periodontal Res. 1993;28:500–510
  5. Henderson B, Poole S, Wilson M. Bacterial modulins: a novel class of virulence factor which cause host tissue pathology by inducing cytokine synthesis. Microbial Rev. 1996;60:316–341
  6. Tobias PS, Gegner J, Tapping R, Orr S, Mathison J, Lee JD, et al. Lipopolysaccharide dependent cellular activation. J Periodontal Res. 1997;32:99–103
  7. Zappa U, Reinking-Zappa M, Graf H, Espeland M. Cell populations and episodic periodontal attachment loss in humans. J Clin Periodontol. 1991;18:508–515
  8. Kornman KS, Page RC, Tonetti MS. The host response to the microbial challenge in periodontitis: assembling the players. Periodontol 2000. 1997;14:33–53
  9. McFarlane CG, Reynolds JJ, Meikle MC. The release of interleukin-1 beta, tumor necrosis factor-alpha and interferon-gamma by cultured peripheral blood mononuclear cells from patients with periodontitis. J Periodontal Res. 1990;25:207–214
  10. Wilson M, Reddi K, Henderson B. Cytokine-induced components of periodontopathogenic bacteria. J Periodontal Res. 1996;31:393–407
  11. Lindemann RA, Economou JS, Rothermel H. Production of interleukin-1 and tumor necrosis factor by human peripheral monocytes activated by periodontal bacteria and extracted lipopolysaccharides. J Dent Res. 1988;67:1131–1135
  12. Chiang CY, Kyritsis G, Graves DT, Amar S. Interleukin-1 and tumor necrosis factor activities partially account for calvarial bone resorption induced by local injection of lipopolysaccharide. Infect Immun. 1999;67:4231–4236
  13. Miyauchi M, Sato S, Kitagawa S, Hiraoka M, Kudo Y, Ogawa I, et al. Cytokine expression in rat molar gingival periodontal tissues after topical application of lipopolysaccharide. Histochem Cell Biol. 2001;116:57–62
  14. Okada H, Murakami S. Cytokine expression in periodontal health and disease. Crit Rev Oral Biol Med. 1998;9:248–266
  15. 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;191:275–285
  16. Baldwin AS. The NF-κB and IκB proteins: new discoveries and insights. Annu Rev Immunol. 1996;14:649–683
  17. Chen F, Castranova V, Shi X, Demers LM. New insights into the role of nuclear factor-κB, a ubiquitous transcription factor in the initiation of disease. Clin Chem. 1999;45:7–17
  18. Baeuerle PA, Baltimore D. NF-κB: ten years after. Cell. 1996;87:13–20
  19. Hayden MS, Ghosh S. Signaling to NF-κB. Genes Dev. 2004;18:2195–2224
  20. Mukaida N, Mahe Y, Matsushima K. Cooperative interaction of nuclear factor-κB- and cis-regulatory enhancer binding protein-like factor binding elements in activating the interleukin-8 gene by pro-inflammatory cytokines. J Biol Chem. 1990;265:21128–21133
  21. Oku K, Sawatani I, Chaen H, Fukuda S, Kurimoto M. Trehalose content in food. Nippon Shokuhin Kagaku Kougaku Kaishi. 1998;45:381–384
  22. Sugimoto T. Production of trehalose by starch-glication method with enzymes and its use. Food Industry. 1995;38:34–39
  23. Hirata T, Yokomise H, Fukuse T, Muro K, Inui K, Yagi K, et al. Effects of trehalose in preservation of canine lung for transplants. Thorac Cardiovasc Surg. 1993;41:59–63
  24. Neta T, Takada K, Hirasawa M. Low-cariogenicity of treholose as a substate. J Dent. 2000;28:571–576
  25. Taya K, Sugashima S, Setsuo H. Osteogenic effect of trehalose on ovariectomized mice. Jpn J Conser Dent. 2007;50:52–61
  26. Taya K, Hirose K, Setsuo H. Preventive effects of trehalose on bone mineral loss in ovariectomized rats. J Dent Hlth. 2008;58:534–541
  27. Nishizaki Y, Yoshizane C, Toshimori Y, Arai N, Akamatsu S, Hanaya T, et al. Disaccharide-trehalose inhibits bone resorption in ovariectomized mice. Nutr Res. 2000;20:653–664
  28. Arai C, Kohguchi M, Akamatsu S, Arai N, Yoshizane C, Hasegawa N, et al. Trehalose suppresses lipopolysaccharide-induced osteoclastogenesis bone marrow in mice. Nutr Res. 2001;21:993–999
  29. Yoshizane C, Arai N, Arai C, Yamamoto M, Nishizaki Y, Hanaya T, et al. Trehalose suppresses osteoclast differentiation in ovariectomized mice: correlation with decreased in vitro interleukin-6 production by bone marrow cells. Nutr Res. 2000;20:1485–1491
  30. Hanazawa S, Murakami Y, Hirose K, Amano S, Ohmori Y, Higuchi H, et al. Bacteroides (Porphyromonas) gingivalis fimbriae activate mouse peritoneal macrophages and induce gene expression and production of interleukin-1. Infect Immun. 1991;59:1972–1977
  31. Ohmori Y, Hanazawa S, Amano S, Miyoshi T, Hirose K, Kitano S. Functional roles of macrophages in periodontal disease. II. Macrophages produce a factor stimulating growth and differentiation of an osteoblastic cell line (MC3T3-E1). Jpn J Oral Biol. 1986;28:646–653
  32. Kobayashi-Sakamoto M, Hirose K, Isogai E, Chiba I. NF-κB-dependent induction of osteoprotegerin by Porphyromonas gingivalis in endothelial cells. Biochem Biophys Res Commun. 2004;315:107–112
  33. Ariyasu T, Matsumoto S, Kyono F, Hanaya T, Arai S, Ikeda M, et al. Taste receptor T1R3 is an essential molecule for the celluar recognition of the disaccharide trehalose. In vitro Cell Dev Biol Anim. 2003;39:80–88
  34. Bodet C, Chandad F, Grenier D. Anti-inflammatory activity of a high-molecular-weight cranberry fraction on macrophages stimulated by lipopolysaccharides from periodontopathogens. J Dent Res. 2006;85:235–239
  35. Chen LL, Yan J. Porphyromonas gingivalis lipopolysaccharide activated bone resorption of osteoclasts by inducing IL-1, TNF, and PGE. Acta Pharmacol Sin. 2001;22:614–618
  36. Nishida E, Hara Y, Kaneko T, Ikeda Y, Ukai T, Kato I. Bone resorption and local interleukin-1α and interleukin-1β synthesis induced by Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis lipopolysaccharide. J Periodontal Res. 2001;36:1–8
  37. Gowen M, Wood DD, Russell RGG. Stimulation of the proliferation of human bone cells in vitro by human monocyte products with interleukin-1 activity. J Clin Invest. 1985;75:1223–1229
  38. Canalis E. Interleukin-1 has independent effects on deoxyribonucleic acid and collagen synthesis in cultures of rat calvariae. Endocrinology. 1986;118:74–81
  39. Ishihara Y, Nishihara T, Maki E, Noguchi T, Koga T. Role of interleukin-1 and prostaglandin in in vitro bone resorption induced by Actinobacillus actinomycetemcomitans lipopolysaccharide. J Periodontal Res. 1991;26:155–160
  40. Agarwal S, Piesco NP, Johns LP, Riccelli AE. Differential expression of IL-1β, TNF-α, IL-6, and IL-8 in human monocytes in response to lipopolysaccharides from different microbes. J Dent Res. 1995;74:1057–1065
  41. Agarwal S, Baran C, Piesco NP, Quintero JC, Langkamp HH, Johns LP, et al. Synthesis of proinflammatory cytokines of human gingival fibroblasts in response to lipopolysaccharides and interleukin-1β. J Periodontal Res. 1995;30:382–389
  42. Hou LT, Liu CM, Rossomando EF. Crevicular interleukin-1β in moderate and severe periodontitis patients and the effect of phase I periodontal treatment. J Clin Periodontol. 1995;22:162–167
  43. Lima V, Vidal FDP, Rocha FAC, Brito GAC, Ribeiro RA. Effects of Tumor necrosis factor-α inhibitors pentoxifylline and thalidomide on alveolar bone loss in short-term experimental periodontal disease in rats. J Periodontol. 2004;75:162–168
  44. Assuma R, Oates T, Cochran D, Amar S, Graves DT. IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol. 1998;160:403–409
  45. Collart MA, Baeuerle P, Vassalli P. Regulation of tumor necrosis factor alpha transcription in macrophages: involvement of four κB-like motifs and of constitutive and inducible forms of NF-κB. Mol cell biol. 1990;10:1498–1506
  46. Shakhov AN, Collart MA, Vassalli P, Nedospasov SA, Jongeneel CV. κB-type enhancers are involved in lipopolysaccharide-mediated transcriptional activation of the tumor necrosis factor α gene in primary macrophages. J Exp Med. 1990;171:35–47
  47. Drouet C, Shakhov AN, Jongeneel CV. Enhancers and transcription factors controlling the inducibility of the tumor necrosis factor-α promoter in primary macrophages. J Immunol. 1991;147:1694–1700
  48. Blank V, Kourilsky P, Israel A. NF-κB and related proteins: Rel/dorsal homologies meet ankyrin-like repeats. Trends Biochem Sci. 1992;17:135–140
  49. Ziegler-Heitbrock HWL, Sternsdorf T, Liese J, Belohradsky B, Weber C, Wedel A, et al. Pyrrolidine dithiocarbamate inhibits NF-κB mobilization and TNF production in human monocytes. J Immunol. 1993;151:6986–6993
  50. Han SJ, Jeong SY, Nam YJ, Yang KH, Lim HS, Chung J. Xylitol inhibits inflammatory cytokine expression induced by lipopolysaccharide from Porphyromonas gingivalis. Clin Diagn Lab Immunol. 2005;12:1285–1291
  51. Hoon MA, Adler E, Lindemeier J, Battey JF, Ryba NJP, Zuker CS. Putative mammalian taste receptors: a class of teste-specific GPCRs with distinct topographic selectivity. Cell. 1999;96:541–551
  52. Bachmanov AA, Li X, Reed DR, Ohmen JD, Li S, Chen Z, et al. Positional cloning of the mouse saccharin preference(Sac) locus. Chem Senses. 2001;26:925–933
  53. Montmayeur JP, Liberles SD, Matsunami H, Buck LB. A candidate taste receptor gene near a sweet taste locus. Nat Neurosci. 2001;4:492–498
  54. MaX M, Shanker YG, Hung L, Rong M, Liu Z, Campagne F, et al. Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet. 2001;28:58–63
  55. Kitagawa M, Kusakabe Y, Miura H, Ninomiya Y, Hino A. Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem Biophys Res Commun. 2001;283:236–242
  56. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. Human receptors for sweet and umami taste. Proc Natl Acad Sci U S A. 2002;99:4692–4696
  57. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJP, Zuker CS. Mammalian sweet taste receptors. Cell. 2001;106:381–390
  58. Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJP, et al. The receptors for mammalian sweet and umami taste. Cell. 2003;115:255–266
  59. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Varadarajan V, Zou S, et al. Detection of sweet and umami taste in the absence of taste receptor T1r3. Science. 2003;301:850–853
  60. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJP, et al. An amino-acid taste receptor. Nature. 2002;416:199–202
  61. Kornman KS. Host modulation as a therapeutic strategy in the treatment of periodontal disease. Clin Infect Dis. 1999;28:520–526

PII: S0003-9969(09)00119-8

doi: 10.1016/j.archoralbio.2009.05.003

Archives of Oral Biology
Volume 54, Issue 8 , Pages 749-756 , August 2009