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Alveolar Bone Protective Effect of Hiziki Extracts on the Progression of Periodontitis

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Abstract

The purpose of this study was to evaluate the effects of hiziki extract on alveolar bone loss, inflammation, and osteo-biomarker expression in hPDL cells (10, 50, 100 μg/ml final concentrations in culture medium) and on a ligature-induced periodontitis rat model (50, 100, 200 mg/kg with oral administration). Hiziki extract increased alkaline phosphatase activity and mineralized nodule formation in hPDL cell. In western blot analysis, hiziki extract resulted in increased expression of osteoblast markers, including transforming growth factor beta (TGF-β), SMAD anchor for receptor activation (SARA) and runt-related transcription factor 2 (RUNX2) in hDPL cells. Additionally, expression of osteoclast markers and inflammatory cytokines was inhibited, which were receptor activator of NF-κB (RANK), RANK receptor (RANKL) and nuclear factor of activated T cells, cytoplasmic 1 (NFATc1). Hiziki extract also prevented alveolar bone loss in a ligature-induced periodontitis rat model through reducing the distance between cementoenamel junction and alveolar bone crest (CBJ-ABC) and furcation involvement. These findings suggested that hiziki extract has prophylactic potential for the prevention of periodontitis through anti-inflammation and, anti-bone resorption effects and the inhibition of alveolar bone destruction.

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References

  • Anusaksathien O, Giannobile WV (2002) Growth factor delivery to reengineer periodontal tissues. Curr Pharm Biotechnol 3:129–139

    Article  PubMed  CAS  Google Scholar 

  • Bezerra MM, Brito GA, Ribeiro RA, Rocha FA (2002) Low-dose doxycycline prevents inflammatory bone resorption in rats. Braz J Med Biol Res 35:613–616

    Article  PubMed  CAS  Google Scholar 

  • Bezerra JP, da Silva LR, de Alvarenga Lemos VA, Duarte PM, Bastos MF (2008) Administration of high doses of caffeine increases alveolar bone loss in ligature-induced periodontitis in rats. J Periodontol 79:2356–2360

    Article  PubMed  Google Scholar 

  • Chen X, Nie W, Fan S, Zhang J, Wang Y, Lu J, Jin L (2012) A polysaccharide from Sargassum fusiforme protects against immunosuppression in cyclophosphamide-treated mice. Carbohydr Polym 90:1114–1119

    Article  PubMed  CAS  Google Scholar 

  • Dereka XE, Markopoulou CE, Vrotsos IA (2006) Role of growth factors on periodontal repair. Growth Factors 24:260–267

    Article  PubMed  CAS  Google Scholar 

  • Ernst CW, Lee JE, Nakanishi T, Karimbux NY, Rezende TM, Stashenko P, Seki M, Taubman MA, Kawai T (2007) Diminished forkhead box P3/CD25 double-positive T regulatory cells are associated with the increased nuclear factor-κB ligand (RANKL+) T cells in bone resorption lesion of periodontal disease. Clin Exp Immunol 148:271–280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fujii S, Maeda H, Tomokiyo A, Monnouchi S, Hori K, Wada N, Akamine A (2010) Effects of TGF-β1 on the proliferation and differentiation of human periodontal ligament cells and a human periodontal ligament stem/progenitor cell line. Cell Tissue Res 342:233–242

    Article  PubMed  CAS  Google Scholar 

  • Holanda Pinto SA, Pinto LM, Cunha GM, Chaves MH, Santos FA, Rao VS (2008) Anti-inflammatory effect of α, β-Amyrin, a pentacyclic triterpene from Protium heptaphyllum in rat model of acute periodontitis. Inflammopharmacology 16:48–52

    Article  PubMed  CAS  Google Scholar 

  • Honda T, Aoki Y, Takahashi N, Maekawa T, Nakajima T, Ito H, Tabeta K, Okui T, Kajita K, Domon H, Yamazaki K (2008) Elevated expression of IL-17 and IL-12 genes in chronic inflammatory periodontal disease. Clin Chim Acta 395:137–141

    Article  PubMed  CAS  Google Scholar 

  • Hu YL, Liu Z, Jiao DK, Ma T, Wang CY, Jia CY (2011) The effect of rhoA/rho kinase signal pathway on TGF-beta1-induced phenotypic differentiation of human dermal fibroblasts. Zhonghua Zheng Xing Wai Ke Za Zhi 27:376–380

    PubMed  Google Scholar 

  • Ji YB, Gao SY (2005) Effects and mechanism of Sargassum fusiforme polysaccharide on antitumor in vitro. Chin J Clin Rehabil 34:190–192

    Google Scholar 

  • Jönsson D, Nebel D, Bratthall G, Nilsson BO (2011) The human periodontal ligament cell: a fibroblast-like cell acting as an immune cell. J Periodontal Res 46:153–157

    Article  PubMed  CAS  Google Scholar 

  • Katagiri T, Lee T, Takeshima H, Suda T, Tanaka H, Omura S (1990) Transforming growth factor-beta modulates proliferation and differentiation of mouse clonal osteoblastic MC3T3-E1 cells depending on their maturation stages. Bone Miner 11:285–293

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Kim N (2014) Regulation of NFATc1 in osteoclast differentiation. J Bone Metab 21:233–241

    Article  PubMed  PubMed Central  Google Scholar 

  • Kingsley DM (1994) The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8:133–146

    Article  PubMed  CAS  Google Scholar 

  • Lee JM, Shin ZU, Mavlonov GT, Abdurakhmonov IY, Yi TH (2012) Solid-phase colorimetric method for the quantification of fucoidan. Appl Biochem Biotechnol 168:1019–1024

    Article  PubMed  CAS  Google Scholar 

  • Lee DG, Park SY, Chung WS, Park JH, Shin HS, Hwang E, Kim IH, Yi TH (2014) The bone regenerative effects of fucosterol in in vitro and in vivo models of postmenopausal osteoporosis. Mol Nutr Food Res 58:1249–1257

    Article  PubMed  CAS  Google Scholar 

  • Lee DG, Park SY, Chung WS, Park JH, Hwang E, Mavlonov GT, Kim IH, Kim KY, Yi TH (2015) Fucoidan prevents the progression of osteoarthritis in rats. J Med Food 18:1032–1041

    Article  PubMed  CAS  Google Scholar 

  • Lester SR, Bain JL, Johnson RB, Serio FG (2007) Gingival concentrations of interleukin-23 and -17 at healthy sites and at sites of clinical attachment loss. J Periodontol 78:1545–1550

    Article  PubMed  CAS  Google Scholar 

  • Listgarten MA (1987) Nature of periodontal diseases: pathogenic mechanisms. J Periodontal Res 22:172–178

    Article  PubMed  CAS  Google Scholar 

  • Mao WJ, Li BF, Gu QQ, Fang YC, Xing HT (2004) Preliminary studies on the chemical characterization and antihyperlipidemic activity of polysaccharide from the brown alga Sargassum fusiforme. Hydrobiology 173:263–266

    Article  Google Scholar 

  • Matsumoto T, Abe M (2011) TGF-β-related mechanisms of bone destruction in multiple myeloma. Bone 48:129–134

    Article  PubMed  CAS  Google Scholar 

  • Menezes AM, Rocha FA, Chaves HV, Carvalho CB, Ribeiro RA, Brito GA (2005) Effect of sodium alendronate on alveolar bone resorption in experimental periodontitis in rats. J Periodontol 76:1901–1909

    Article  PubMed  CAS  Google Scholar 

  • Okubo K, Kobayashi M, Takiguchi T, Takada T, Ohazama A, Okamatsu Y, Hasegawa K (2003) Participation of endogenous IGF-I and TGF-beta with enamel matrix derivative-stimulated cell growth in human periodontal ligament cells. J Periodontal Res 38:1–9

    Article  PubMed  CAS  Google Scholar 

  • Ono Y, Sensui H, Okutsu S, Nagatomi R (2007) Notch2 negatively regulates myofibroblastic differentiation of myoblasts. J Cell Physiol 210:358–369

    Article  PubMed  CAS  Google Scholar 

  • Park SY, Hwang E, Shin YK, Lee DG, Yang JE, Park JH, Yi TH (2017) Immunostimulatory effect of enzyme-modified Hizikia fusiforme in a mouse model in vitro and ex vivo. Mar Biotechnol (NY) 19:65–75

    Article  CAS  Google Scholar 

  • Paskaleva EE, Lin X, Li W, Cotter R, Klein MT, Roberge E, Yu EK, Clark B, Veille JC, Liu Y, Lee DY, Canki M (2006) Inhibition of highly productive HIV-1 infection in T cells, primary human macrophages, microglia, and astrocytes by Sargassum fusiforme. AIDS Res Ther 25:3–15

    Google Scholar 

  • Pierro VS, de Souza IP, Luiz RR (2009) Influence of local factors on cementoenamel junction-alveolar bone crest distance in primary dentition. J Clin Pediatr Dent 33:199–206

    Article  PubMed  Google Scholar 

  • Sallay K, Sanavi F, Ring I, Pham P, Behling UH, Nowotny A (1982) Alveolar bone destruction in the immunosuppressed rat. J Periodontal Res 17:263–274

    Article  PubMed  CAS  Google Scholar 

  • Salvi GE, Lang NP (2005) Host response modulation in the management of periodontal diseases. J Clin Periodontol 32:108–129

    Article  PubMed  CAS  Google Scholar 

  • Samejima Y, Ebisu S, Okada H (1990) Effect of infection with Eikenella corrodens on the progression of ligature-induced periodontitis in rats. J Periodontal Res 25:308–315

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, Tanaka S, Kodama T, Akira S, Iwakura Y, Cua DJ, Takayanagi H (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  PubMed  PubMed Central  CAS  Google Scholar 

  • Seto H, Ninomiya M, Nagata T (2006) Alveolar bone resorption in animal models of periodontitis. Clin Calcium 16:248–254

    PubMed  CAS  Google Scholar 

  • Silva I, Branco JC (2011) Rank/Rankl/opg: literature review. Acta Reumatol Port 36:209–218

    PubMed  CAS  Google Scholar 

  • Tu HP, Fu MM, Kuo PJ, Chin YT, Chiang CY, Chung CL, Fu E (2014) Berberine’s effect on periodontal tissue degradation by matrix metalloproteinases: an in vitro and in vivo experiment. Phytomedicine 20:1203–1210

    Article  CAS  Google Scholar 

  • Xiong H, Wei L, Peng B (2009) Immunohistochemical localization of IL-17 in induced rat periapical lesions. J Endod 35:216–220

    Article  PubMed  Google Scholar 

  • Xu XC, Chen H, Zhang X, Zhai ZJ, Liu XQ, Qin A, Lu EY (2014) Simvastatin prevents alveolar bone loss in an experimental rat model of periodontitis after ovariectomy. J Transl Med 12:284–293

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou J, Hu N, Wu YL, Pan YJ, Sun CR (2008) Preliminary studies on the chemical characterization and antioxidant properties of acidic polysaccharides from Sargassum fusiforme. J Zhejiang Univ Sci B 9:721–727

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

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Author notes

  1. Don-Gil Lee and Yu-Kyong Shin contributed equally to this work.

Authors and Affiliations

  1. Department of Oriental Medicinal Materials & Processing, College of Life Science, Kyung Hee University, Yongin-si, Gyeonggi-do, South Korea

    Don-Gil Lee, Yu-Kyong Shin, Jae-Hee Park, Sang-Yong Park, Eunson Hwang, Jung-Eun Yang, Hae Jo, Ki-Young Kim, Gafurjon T. Mavlonov & Tae-Hoo Yi

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  1. Don-Gil Lee
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  2. Yu-Kyong Shin
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  3. Jae-Hee Park
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  4. Sang-Yong Park
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  5. Eunson Hwang
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  6. Jung-Eun Yang
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  7. Hae Jo
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  9. Gafurjon T. Mavlonov
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  10. Tae-Hoo Yi
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Correspondence to Tae-Hoo Yi.

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Lee, DG., Shin, YK., Park, JH. et al. Alveolar Bone Protective Effect of Hiziki Extracts on the Progression of Periodontitis. Mar Biotechnol 20, 313–323 (2018). https://doi.org/10.1007/s10126-018-9814-8

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  • DOI: https://doi.org/10.1007/s10126-018-9814-8

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