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The divergent expression of periostin mRNA in the periodontal ligament during experimental tooth movement

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Abstract

A novel 90-kDa protein named periostin, which is preferentially expressed in the periosteum and the periodontal ligament (PDL), may play a role in bone metabolism and remodeling. However, the precise role of periostin in the PDL remains unclear. Therefore, we examined the expression of periostin mRNA during experimental tooth movement. Experimental tooth movement was achieved in 7-week-old male Sprague-Dawley rats. In control specimens without tooth movement, the expression of periostin mRNA was uniformly observed in the PDL surrounding the mesial and distal roots of the upper molars and was weak in the PDL of the root furcation area. The periostin mRNA-expressing cells were mainly fibroblastic cells in the PDL and osteoblastic cells on the alveolar bone surfaces. The divergent expression of periostin mRNA in the PDL began to be observed at 3 h and continued up to 96 h after tooth movement. The maximum changes, which showed stronger staining in the pressure sites than in the tension sites, were observed at 24 h. The expression of periostin mRNA in the PDL 168 h after tooth movement exhibited a similar distribution to that of the control specimens. These results suggest that periostin is one of the local contributing factors in bone and periodontal tissue remodeling following mechanical stress during experimental tooth movement.

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Fig. 1a, b.
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References

  • Alhashimi N, Frithiof L, Brudvik P, Bakhiet M (1999) Chemokines are upregulated during orthodontic tooth movement. J Interferon Cytokine Res 19:1047–1052

    Article  CAS  PubMed  Google Scholar 

  • Alhashimi N, Frithiof L, Brudvik P, Bakhiet M (2000) Orthodontic movement induces high numbers of cells expressing IFN-gamma at mRNA and protein levels. J Interferon Cytokine Res 20:7–12

    Article  CAS  PubMed  Google Scholar 

  • Alhashimi N, Frithiof L, Brudvik P, Bakhiet M (2001) Orthodontic tooth movement and de novo synthesis of proinflammatory cytokines. Am J Orthod Dentofacial Orthop 119:307–312

    Article  CAS  PubMed  Google Scholar 

  • Azuma M (1970) Study on histologic changes of periodontal membrane incident to experimental tooth movement. Bull Tokyo Med Dent Univ 17:149–178

    CAS  PubMed  Google Scholar 

  • Beertsen W, McCulloch CA, Sodek J (1997) The periodontal ligament: a unique, multifunctional connective tissue. Periodontology 2000 13:20–40

    CAS  PubMed  Google Scholar 

  • Domon S, Shimokawa H, Matsumoto Y, Yamaguchi S, Soma K (1999) In situ hybridization for matrix metalloproteinase-1 and cathepsin K in rat root-resorbing tissue induced by tooth movement. Arch Oral Biol 44:907–915

    Article  CAS  PubMed  Google Scholar 

  • Domon S, Shimokawa H, Yamaguchi S, Soma K (2001) Temporal and spatial mRNA expression of bone sialoprotein and type I collagen during rodent tooth movement. Eur J Orthod 23:339–348

    CAS  PubMed  Google Scholar 

  • Gao J, Symons AL, Bartold PM (1998) Expression of transforming growth factor-beta 1 (TGF-beta1) in the developing periodontium of rats. J Dent Res 77:170817–170816

    Google Scholar 

  • Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, Ozawa H, Toyama Y, Bonewald LF, Kudo A (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14:1239–1249

    CAS  PubMed  Google Scholar 

  • Ji X, Chen D, Xu C, Harris SE, Mundy GR, Yoneda T (2000) Patterns of gene expression associated with BMP-2-induced osteoblast and adipocyte differentiation of mesenchymal progenitor cell 3T3-F442A. J Bone Miner Metab 18:132–139

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Boskey A, Spevak L, Dallas M, Hori M, Bonewald LF (2001) Establishment of an osteoid preosteocyte-like cell MLO-A5 that spontaneously mineralizes in culture. J Bone Miner Res 16:1622–1633.

    CAS  PubMed  Google Scholar 

  • Kim JE, Kim EH, Han EH, Park RW, Park IH, Jun SH, Kim JC, Young MF, Kim IS (2000) A TGF-beta-inducible cell adhesion molecule, betaig-h3, is downregulated in melorheostosis and involved in osteogenesis. J Cell Biochem 77:169–178

    CAS  PubMed  Google Scholar 

  • Kobayashi Y, Hashimoto F, Miyamoto H, Kanaoka K, Miyazaki-Kawashita Y, Nakashima T, Shibata M, Kobayashi K, Kato Y, Sakai H (2000) Force-induced osteoclast apoptosis in vivo is accompanied by elevation in transforming growth factor beta and osteoprotegerin expression. J Bone Miner Res 15:1924–1934

    CAS  PubMed  Google Scholar 

  • Kruzynska-Frejtag A, Machnicki M, Rogers R, Markwald RR, Conway SJ (2001) Periostin (an osteoblast-specific factor) is expressed within the embryonic mouse heart during valve formation. Mech Dev 103:183–188

    Article  CAS  PubMed  Google Scholar 

  • LeBaron RG, Bezverkov KI, Zimber MP, Pavelec R, Skonier J, Purchio AF (1995) Beta IG-H3, a novel secretory protein inducible by transforming growth factor-beta, is present in normal skin and promotes the adhesion and spreading of dermal fibroblasts in vitro. J Invest Dermatol 104:844–849

    CAS  PubMed  Google Scholar 

  • Macapanpan LC, Weinmann JP, Brodie AG (1954) Early tissue changes following tooth movement in rats. Angle Orthod 24:79–95

    Google Scholar 

  • McCulloch CA, Lekic P, McKee MD (2000) Role of physical forces in regulating the form and function of the periodontal ligament. Periodontology 2000 24:56–72

    Article  CAS  Google Scholar 

  • Mohammed AH, Tatakis DN, Dziak R (1989) Leukotrienes in orthodontic tooth movement. Am J Orthod Dentofacial Orthop 95:231–237

    CAS  PubMed  Google Scholar 

  • Nakagawa M, Kukita T, Nakasima A, Kurisu K (1994) Expression of the type I collagen gene in rat periodontal ligament during tooth movement as revealed by in situ hybridization. Arch Oral Biol 39:289–294

    Google Scholar 

  • Nicolay OF, Davidovitch Z, Shanfeld JL, Alley K (1990) Substance P immunoreactivity in periodontal tissues during orthodontic tooth movement. Bone Miner 11:19–29

    CAS  PubMed  Google Scholar 

  • Ohba Y, Ohba T, Terai K, Moriyama K (2000) Expression of cathepsin K mRNA during experimental tooth movement in rat as revealed by in situ hybridization. Arch Oral Biol 45:63–69

    Article  CAS  PubMed  Google Scholar 

  • Reitan K (1960) Tissue behavior during orthodontic tooth movement. Am J Orthod 46:881–900

    Google Scholar 

  • Saito I, Ishii K, Hanada K, Sato O, Maeda T (1991a) Responses of calcitonin gene-related peptide-immunopositive nerve fibres in the periodontal ligament of rat molars to experimental tooth movement. Arch Oral Biol 36:689–692

    CAS  PubMed  Google Scholar 

  • Saito M, Saito S, Ngan PW, Shanfeld J, Davidovitch Z (1991b) Interleukin 1 beta and prostaglandin E are involved in the response of periodontal cells to mechanical stress in vivo and in vitro. Am J Orthod Dentofacial Orthop 99:226–240

    CAS  PubMed  Google Scholar 

  • Sasaki H, Auclair D, Fukai I, Kiriyama M, Yamakawa Y, Fujii Y, Chen LB (2001a) Serum level of the periostin, a homologue of an insect cell adhesion molecule, as a prognostic marker in nonsmall cell lung carcinomas. Cancer 92:843–848

    Article  CAS  PubMed  Google Scholar 

  • Sasaki H, Lo KM, Chen LB, Auclair D, Nakashima Y, Moriyama S, Fukai I, Tam C, Loda M, Fujii Y (2001b) Expression of periostin, homologous with an insect cell adhesion molecule, as a prognostic marker in non-small cell lung cancers. Jpn J Cancer Res 92:869–873

    CAS  PubMed  Google Scholar 

  • Sasaki H, Roberts J, Lykins D, Fujii Y, Auclair D, Chen LB (2002) Novel chemiluminescence assay for serum periostin levels in women with preeclampsia and in normotensive pregnant women. Am J Obstet Gynecol 186:103–108

    Article  CAS  PubMed  Google Scholar 

  • Sicher H, Weinmann JP (1944) Bone growth and physiologic tooth movement. Am J Orthod Oral Surg 30:109–132

    Google Scholar 

  • Su M, Borke JL, Donahue HJ, Li Z, Warshawsky NM, Russell CM, Lewis JE (1997) Expression of connexin 43 in rat mandibular bone and periodontal ligament (PDL) cells during experimental tooth movement. J Dent Res 76:1357–1366

    CAS  PubMed  Google Scholar 

  • Sugiura T, Takamatsu H, Kudo A, Amann E (1995) Expression and characterization of murine osteoblast-specific factor 2 (OSF-2) in a baculovirus expression system. Protein Expr Purif 6:305–311

    CAS  PubMed  Google Scholar 

  • Takano-Yamamoto T, Takemura T, Kitamura Y, Nomura S (1994) Site-specific expression of mRNAs for osteonectin, osteocalcin, and osteopontin revealed by in situ hybridization in rat periodontal ligament during physiological tooth movement. J Histochem Cytochem 42:885–896

    CAS  PubMed  Google Scholar 

  • Takeshita S, Kikuno R, Tezuka K, Amann E (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294:271–278

    CAS  PubMed  Google Scholar 

  • Terai K, Takano-Yamamoto T, Ohba Y, Hiura K, Sugimoto M, Sato M, Kawahata H, Inaguma N, Kitamura Y, Nomura S (1999) Role of osteopontin in bone remodeling caused by mechanical stress. J Bone Miner Res 14:839–849

    CAS  PubMed  Google Scholar 

  • Tsuji Y, Yamaza T, Kido MA, Goto T, Nakata S, Akamine A, Nakasima A, Tanaka T (2001) Expression of cathepsin K mRNA and protein in odontoclasts after experimental tooth movement in the mouse maxilla by in situ hybridization and immunoelectron microscopy. Cell Tissue Res 303:359–369

    Article  CAS  PubMed  Google Scholar 

  • Waldo CM, Rothblatt JM (1954) Histologic response to tooth movement in the laboratory rat bone. J Dent Res 33:481–486

    Google Scholar 

  • Yamasaki K (1983) The role of cyclic AMP, calcium, and prostaglandins in the induction of osteoclastic bone resorption associated with experimental tooth movement. J Dent Res 62:877–881

    CAS  PubMed  Google Scholar 

  • Zaki AE, Van Huysen G (1960) Histology of the periodontium following tooth movement. J Dent Res 42:1373–1379

    Google Scholar 

  • Zinn K, McAllister L, Goodman CS (1988) Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell 53:577-587

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. K. Hiura for special technical advice and gratefully acknowledge the members of the Department of Orthodontics, University of Tokushima, for their helpful discussion.

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Authors and Affiliations

  1. Department of Orthodontics, School of Dentistry, University of Tokushima, 3–18–15 Kuramoto-cho, Tokushima 770–8504, Japan,

    Javier Wilde, Masahiko Yokozeki, Kunihiro Terai & Keiji Moriyama

  2. Department of Life Science, Tokyo Institute of Technology, 4259 Nagatsuda, Midori-ku, Yokohama 226–8501, Japan,

    Akira Kudo

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  1. Javier Wilde
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  2. Masahiko Yokozeki
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  3. Kunihiro Terai
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  4. Akira Kudo
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  5. Keiji Moriyama
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Corresponding author

Correspondence to Keiji Moriyama.

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This work was supported in part by the Grants-in Aid for Scientific Research from the Japanese Ministry of Education nos. 13470452 and 13771263

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Wilde, J., Yokozeki, M., Terai, K. et al. The divergent expression of periostin mRNA in the periodontal ligament during experimental tooth movement. Cell Tissue Res 312, 345–351 (2003). https://doi.org/10.1007/s00441-002-0664-2

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  • DOI: https://doi.org/10.1007/s00441-002-0664-2

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