Abstract
We investigated porcine dental follicle cells at the early crown-formation stage and examined the behavior of cells grown in a collagen type I (Col-I) matrix. Clone-porcine dental follicle cells (DFC-I) and controls, viz., dental follicle itself, nonclone-dental follicle cells, periodontal ligament cells (PDLC), and bone marrow stromal cells, were obtained from 6-month-old pigs. DFC-I showed a different gene expression pattern from controls by reverse-transcription polymerase chain reaction analysis. In addition, Col-I treatment enhanced DFC-I proliferation and increased their alkaline phosphatase activity compared with nontreated DFC-I. The expression of periostin, biglycan, and osteocalcin (OCN) in cells growing on collagen was upregulated, similar to the pattern seen in PDLC. DFC-I with and without Col-I treatment were combined with β-tricalcium phosphate particles and implanted into immunodeficient mice. Significant differences were found in the gene expression patterns of bone sialoprotein, OCN, and periostin in both treated and non-treated implants at 2 and/or 4 weeks. The results showed that Col-I induced the mineralization pathway in these cells. Hard tissue formation was observed in both implant types at 8 weeks. Our results suggest that Col-I facilitates the differentiation of DFC-I along the mineralization process.
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Akintoye SO, Lam T, Shi S, Brahim J, Collins MT, Robey PG (2006) Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 38:758–768
Akizuki T, Oda S, Komaki M, Tsuchioka H, Kawakatsu N, Kikuchi A, Yamato M, Okano T, Ishikawa I (2005) Application of periodontal ligament cell sheet for periodontal regeneration: a pilot study in beagle dogs. J Periodontal Res 40:245–251
Alliot-Licht B, Bluteau G, Magne D, Lopez-Cazaux S, Lieubeau B, Daculsi G, Guicheux J (2005) Dexamethasone stimulates differentiation of odontoblast-like cells in human dental pulp cultures. Cell Tissue Res 321:391–400
Aubin JE (2001) Regulation of osteoblast formation and function. Rev Endocr Metab Disord 2:81–94
Bartold PM, Miki Y, McAllister B, Narayanan AS, Page RC (1988) Glycosaminoglycans of human cementum. J Periodontal Res 23:13–17
Bianco P, Fisher LW, Young MF, Termine JD, Robey PG (1991) Expression of bone sialoprotein (BSP) in developing human tissues. Calcif Tissue Int 49:421–426
Bianco P, Riminucci M, Gronthos S, Robey PG (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19:180–192
Boskey AL, Spevak L, Doty SB, Rosenberg L (1997) Effects of bone CS-proteoglycans, DS-decorin, and DS-biglycan on hydroxyapatite formation in a gelatin gel. Calcif Tissue Int 61:298–305
Chen J, Zhang Q, McCulloch CA, Sodek J (1991a) Immunohistochemical localization of bone sialoprotein in foetal porcine bone tissues: comparisons with secreted phosphoprotein 1 (SPP-1, osteopontin) and SPARC (osteonectin). Histochem J 23:281–289
Chen JK, Shapiro HS, Wrana JL, Reimers S, Heersche JN, Sodek J (1991b) Localization of bone sialoprotein (BSP) expression to sites of mineralized tissue formation in fetal rat tissues by in situ hybridization. Matrix 11:133–143
Chen J, Shapiro HS, Sodek J (1992) Development expression of bone sialoprotein mRNA in rat mineralized connective tissues. J Bone Miner Res 7:987–997
Diekwisch TG (2001) The developmental biology of cementum. Int J Dev Biol 45:695–706
Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Amling M, Karsenty G (1999) A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 13:1025–1036
Giannopoulou C, Cimasoni G (1996) Functional characteristics of gingival and periodontal ligament fibroblasts. J Dent Res 75:895–902
Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 97:13625–13630
Hakki SS, Berry JE, Somerman MJ (2001) The effect of enamel matrix protein derivative on follicle cells in vitro. J Periodontol 72:679–687
Han X, Amar S (2003) IGF-1 signaling enhances cell survival in periodontal ligament fibroblasts vs. gingival fibroblasts. J Dent Res 82:454–459
Handa K, Saito M, Tsunoda A, Yamauchi M, Hattori S, Sato S, Toyoda M, Teranaka T, Narayanan AS (2002) Progenitor cells from dental follicle are able to form cementum matrix in vivo. Connect Tissue Res 43:406–408
Hasegawa M, Yamato M, Kikuchi A, Okano T, Ishikawa I (2005) Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng 11:469–478
Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580
Iohara K, Nakashima M, Ito M, Ishikawa M, Nakasima A, Akamine A (2004) Dentin regeneration by dental pulp stem cell therapy with recombinant human bone morphogenetic protein 2. J Dent Res 83:590-595
Jin QM, Zhao M, Webb SA, Berry JE, Somerman MJ, Giannobile WV (2003) Cementum engineering with three-dimensional polymer scaffolds. J Biomed Mater Res [A] 67:54–60
Klees RF, Salasznyk RM, Kingsley K, Williams WA, Boskey A, Plopper GE (2005) Laminin-5 induces osteogenic gene expression in human mesenchymal stem cells through an ERK-dependent pathway. Mol Biol Cell 16:881–890
Lekic P, Sodek J, McCulloch CA (1996) Relationship of cellular proliferation to expression of osteopontin and bone sialoprotein in regenerating rat periodontium. Cell Tissue Res 285:491–500
Lekic P, Rojas J, Birek C, Tenenbaum H, McCulloch CA (2001) Phenotypic comparison of periodontal ligament cells in vivo and in vitro. J Periodontal Res 36:71–79
Liu F, Malaval L, Aubin JE (2003) Global amplification polymerase chain reaction reveals novel transitional stages during osteoprogenitor differentiation. J Cell Sci 116:1787–1796
Luan X, Ito Y, Dangaria S, Diekwisch TG (2006) Dental follicle progenitor cell heterogeneity in the developing mouse periodontium. Stem Cells Dev 15:595–608
Marcopoulou CE, Vavouraki HN, Dereka XE, Vrotsos IA (2003) Proliferative effect of growth factors TGF-beta1, PDGF-BB and rhBMP-2 on human gingival fibroblasts and periodontal ligament cells. J Int Acad Periodontol 5:63–70
Mizuno M, Kuboki Y (2001) Osteoblast-related gene expression of bone marrow cells during the osteoblastic differentiation induced by type I collagen. J Biochem (Tokyo) 129:133–138
Mizuno M, Miyamoto T, Wada K, Watatani S, Zhang GX (2003) Type I collagen regulated dentin matrix protein-1 (Dmp-1) and osteocalcin (OCN) gene expression of rat dental pulp cells. J Cell Biochem 88:1112–1119
Morsczeck C, Gotz W, Schierholz J, Zeilhofer F, Kuhn U, Mohl C, Sippel C, Hoffmann KH (2005) Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24:155–165
Murakami Y, Kojima T, Nagasawa T, Kobayashi H, Ishikawa I (2003) Novel isolation of alkaline phosphatase-positive subpopulation from periodontal ligament fibroblasts. J Periodontol 74:780–786
Nakao K, Itoh M, Tomita Y, Tomooka Y, Tsuji T (2004) FGF-2 potently induces both proliferation and DSP expression in collagen type I gel cultures of adult incisor immature pulp cells. Biochem Biophys Res Commun 325:1052–1059
Nakashima M (1994) Induction of dentin formation on canine amputated pulp by recombinant human bone morphogenetic proteins (BMP)-2 and -4. J Dent Res 73:1515–1522
Nohutcu RM, McCauley LK, Koh AJ, Somerman MJ (1997) Expression of extracellular matrix proteins in human periodontal ligament cells during mineralization in vitro. J Periodontol 68:320–327
Ogata Y, Niisato N, Sakurai T, Furuyama S, Sugiya H (1995) Comparison of the characteristics of human gingival fibroblasts and periodontal ligament cells. J Periodontol 66:1025–1031
Ouyang H, McCauley LK, Berry JE, D’Errico JA, Strayhorn CL, Somerman MJ (2000) Response of immortalized murine cementoblasts/periodontal ligament cells to parathyroid hormone and parathyroid hormone-related protein in vitro. Arch Oral Biol 45:293–303
Palmer RM, Lumsden AG (1987) Development of periodontal ligament and alveolar bone in homografted recombinations of enamel organs and papillary, pulpal and follicular mesenchyme in the mouse. Arch Oral Biol 32:281–289
Pavasant P, Yongchaitrakul T, Pattamapun K, Arksornnukit M (2003) The synergistic effect of TGF-beta and 1,25-dihydroxyvitamin D3 on SPARC synthesis and alkaline phosphatase activity in human pulp fibroblasts. Arch Oral Biol 48:717–722
Piattelli A, Trisi P, Passi P, Piattelli M, Cordioli GP (1994) Histochemical and confocal laser scanning microscopy study of the bone-titanium interface: an experimental study in rabbits. Biomaterials 15:194–200
Pitaru S, McCulloch CA, Narayanan SA (1994) Cellular origins and differentiation control mechanisms during periodontal development and wound healing. J Periodontal Res 29:81–94
Pitaru S, Pritzki A, Bar-Kana I, Grosskopf A, Savion N, Narayanan AS (2002) Bone morphogenetic protein 2 induces the expression of cementum attachment protein in human periodontal ligament clones. Connect Tissue Res 43:257–264
Ramakrishnan PR, Lin WL, Sodek J, Cho MI (1995) Synthesis of noncollagenous extracellular matrix proteins during development of mineralized nodules by rat periodontal ligament cells in vitro. Calcif Tissue Int 57:52–59
Ruch JV (1998) Odontoblast commitment and differentiation. Biochem Cell Biol 76:923–938
Saito Y, Yoshizawa T, Takizawa F, Ikegame M, Ishibashi O, Okuda K, Hara K, Ishibashi K, Obinata M, Kawashima H (2002) A cell line with characteristics of the periodontal ligament fibroblasts is negatively regulated for mineralization and Runx2/Cbfa1/Osf2 activity, part of which can be overcome by bone morphogenetic protein-2. J Cell Sci 115:4191–4200
Saito M, Handa K, Kiyono T, Hattori S, Yokoi T, Tsubakimoto T, Harada H, Noguchi T, Toyoda M, Sato S, Teranaka T (2005) Immortalization of cementoblast progenitor cells with Bmi-1 and TERT. J Bone Miner Res 20:50–57
Salasznyk RM, Williams WA, Boskey A, Batorsky A, Plopper GE (2004) Adhesion to vitronectin and collagen I promotes osteogenic differentiation of human mesenchymal stem cells. J Biomed Biotechnol 2004:24–34
Sasaki T, Watanabe C, Shimizu T, Debari K, Segawa K (1990) Possible role of cementoblasts in the resorbant organ of human deciduous teeth during root resorption. J Periodontal Res 25:143–151
Saygin NE, Giannobile WV, Somerman MJ (2000) Molecular and cell biology of cementum. Periodontology 24:73–98
Shi S, Robey PG, Gronthos S (2001) Comparison of human dental pulp and bone marrow stromal stem cells by cDNA microarray analysis. Bone 29:532–539
Staatz WD, Fok KF, Zutter MM, Adams SP, Rodriguez BA, Santoro SA (1991) Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1 integrin in collagen. J Biol Chem 266:7363–7367
Ten Cate AR, Mills C (1972) The development of the periodontium: the origin of alveolar bone. Anat Rec 173:69–77
Ten Cate AR, Mills C, Solomon G (1971) The development of the periodontium. A transplantation and autoradiographic study. Anat Rec 170:365–379
Thesleff I, Mikkola M (2002) The role of growth factors in tooth development. Int Rev Cytol 217:93–135
Wise GE, Lin F, Fan W (1992) Culture and characterization of dental follicle cells from rat molars. Cell Tissue Res 267:483–492
Xiao G, Wang D, Benson MD, Karsenty G, Franceschi RT (1998) Role of the alpha2-integrin in osteoblast-specific gene expression and activation of the Osf2 transcription factor. J Biol Chem 273:32988–32994
Xu T, Bianco P, Fisher LW, Longenecker G, Smith E, Goldstein S, Bonadio J, Boskey A, Heegaard AM, Sommer B, Satomura K, Dominguez P, Zhao C, Kulkarni AB, Robey PG, Young MF (1998) Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat Genet 20:78–82
Yoshikawa DK, Kollar EJ (1981) Recombination experiments on the odontogenic roles of mouse dental papilla and dental sac tissues in ocular grafts. Arch Oral Biol 26:303–307
Acknowledgments
We thank Dr. J. Sodek for generously providing the collagen type I and BSP antibodies (University of Toronto, Canada), Dr. H. Irie for the kind gift of the Osferion G1 (Olympus, Japan), and Dr. A. Kamiya (IMSUT, Japan ) for technical support.
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This work was supported in part by grants from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (Kakenhi Kiban B 16390578 and Houga 18659592 to M.J.H.) and by the Hitachi Medical Corporation (Japan) and DENICS International (Japan).
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Tsuchiya, S., Honda, M.J., Shinohara, Y. et al. Collagen type I matrix affects molecular and cellular behavior of purified porcine dental follicle cells. Cell Tissue Res 331, 447–459 (2008). https://doi.org/10.1007/s00441-007-0532-1
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DOI: https://doi.org/10.1007/s00441-007-0532-1