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Stem cells and tooth tissue engineering

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Abstract

The notion that teeth contain stem cells is based on the well-known repairing ability of dentin after injury. Dental stem cells have been isolated according to their anatomical locations, colony-forming ability, expression of stem cell markers, and regeneration of pulp/dentin structures in vivo. These dental-derived stem cells are currently under increasing investigation as sources for tooth regeneration and repair. Further attempts with bone marrow mesenchymal stem cells and embryonic stem cells have demonstrated the possibility of creating teeth from non-dental stem cells by imitating embryonic development mechanisms. Although, as in tissue engineering of other organs, many challenges remain, stem-cell-based tissue engineering of teeth could be a choice for the replacement of missing teeth in the future.

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References

  • About I, Bottero MJ, Denato P de, Camps J, Franquin JC, Mitsiadis TA (2000) Human dentin production in vitro. Exp Cell Res 258:33–41

    PubMed  CAS  Google Scholar 

  • Amar S, Chung KM (1994) Clinical implications of cellular biologic advances in periodontal regeneration. Curr Opin Periodontol 18:128–140

    Google Scholar 

  • Arany S, Nakata A, Kameda T, Koyota S, Ueno Y, Sugiyama T (2006) Phenotype properties of a novel spontaneously immortalized odontoblast-lineage cell line. Biochem Biophys Res Commun 342:718–724

    PubMed  CAS  Google Scholar 

  • Arias AM (2001) Epithelial mesenchymal interactions in cancer and development. Cell 105:425–431

    PubMed  CAS  Google Scholar 

  • Asahara T, Murohara T, Sullivan A, Silver M, Zee R van der, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967

    PubMed  CAS  Google Scholar 

  • Aufderheide E, Chiquet-Ehrismann R, Ekblom P (1987) Epithelial-mesenchymal interactions in the developing kidney lead to expression of tenascin in the mesenchyme. J Cell Biol 105:599–608

    PubMed  CAS  Google Scholar 

  • Aukhil I, Pettersson E, Suggs C (1986) Guided tissue regeneration: an experimental procedure in beagle dogs. J Periodontol 57:727–734

    PubMed  CAS  Google Scholar 

  • Batouli S, Miura M, Brahim J, Tsutsui TW, Fisher LW, Gronthos S, Robey PG, Shi S (2003) Comparison of stem-cell-mediated osteogenesis and dentinogenesis. J Dent Res 82:976–981

    PubMed  CAS  Google Scholar 

  • Bei M, Kratochwil K, Maas RL (2000) BMP4 rescues a non-cell-autonomous function of Msx1 in tooth development. Development 127:4711–4718

    PubMed  CAS  Google Scholar 

  • Bjornson CR, Rietze RL, Reynolds BA, Magli MC, Vescovi AL (1999) Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 283:534–537

    PubMed  CAS  Google Scholar 

  • Braut A, Kalajzic I, Kalajzic Z, Rowe DW, Kollar EJ, Mina M (2002) Col1a1-GFP transgene expression in developing incisors. Connect Tissue Res 43:216–219

    PubMed  CAS  Google Scholar 

  • Braut A, Kollar EJ, Mina M (2003) Analysis of the odontogenic and osteogenic potentials of dental pulp in vivo using a Col1a1-2.3-GFP transgene. Int J Dev Biol 47:281–292

    PubMed  CAS  Google Scholar 

  • Caplan AI, Bruder SP (2001) Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7:259–264

    PubMed  CAS  Google Scholar 

  • Chen Y, Bei M, Woo I, Satokata I, Maas R (1996) Msx1 controls inductive signaling in mammalian tooth morphogenesis. Development 122:3035–3044

    PubMed  CAS  Google Scholar 

  • Chen Y, Zhang Y, Jiang TX, Barlow AJ, St Amand TR, Hu Y, Heaney S, Francis-West P, Chuong CM, Maas R (2000) Conservation of early odontogenic signaling pathways in Aves. Proc Natl Acad Sci USA 97:10044–10049

    PubMed  CAS  Google Scholar 

  • Chiba M (1965) Cellular proliferation in the tooth germ of the rat incisor. Arch Oral Biol 10:707–718

    PubMed  CAS  Google Scholar 

  • Chuong CM, Widelitz RB, Ting-Berreth S, Jiang TX (1996) Early events during avian skin appendage regeneration: dependence on epithelial-mesenchymal interaction and order of molecular reappearance. J Invest Dermatol 107:639–646

    PubMed  CAS  Google Scholar 

  • Cobourne MT, Sharpe PT (2003) Tooth and jaw: molecular mechanisms of patterning in the first branchial arch. Arch Oral Biol 48:1–14

    PubMed  CAS  Google Scholar 

  • Cobourne MT, Sharpe PT (2005) Sonic hedgehog signaling and the developing tooth. Curr Top Dev Biol 65:255–287

    PubMed  CAS  Google Scholar 

  • Crubezy E, Murail P, Girard L, Bernadou JP (1998) False teeth of the Roman world. Nature 391:29

    PubMed  CAS  Google Scholar 

  • Cutler LS, Gremski W (1991) Epithelial-mesenchymal interactions in the development of salivary glands. Crit Rev Oral Biol Med 2:1–12

    PubMed  CAS  Google Scholar 

  • d’Aquino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De Rosa A, Papaccio G (2007) Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ 14:1162–1171

    CAS  Google Scholar 

  • D’Errico JA, Ouyang H, Berry JE, MacNeil RL, Strayhorn C, Imperiale MJ, Harris NL, Goldberg H, Somerman MJ (1999) Immortalized cementoblasts and periodontal ligament cells in culture. Bone 25:39–47

    PubMed  CAS  Google Scholar 

  • D’Errico JA, Berry JE, Ouyang H, Strayhorn CL, Windle JJ, Somerman MJ (2000) Employing a transgenic animal model to obtain cementoblasts in vitro. J Periodontol 71:63–72

    PubMed  CAS  Google Scholar 

  • D’Souza RN, Aberg T, Gaikwad J, Cavender A, Owen M, Karsenty G, Thesleff I (1999) Cbfa1 is required for epithelial-mesenchymal interactions regulating tooth development in mice. Development 126:2911–2920

    PubMed  CAS  Google Scholar 

  • Dassule HR, McMahon AP (1998) Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev Biol 202:215–227

    PubMed  CAS  Google Scholar 

  • Dassule HR, Lewis P, Bei M, Maas R, McMahon AP (2000) Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127:4775–4785

    PubMed  CAS  Google Scholar 

  • Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, Canfield AE (1998) Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res 13:828–838

    PubMed  CAS  Google Scholar 

  • Duailibi MT, Duailibi SE, Young CS, Bartlett JD, Vacanti JP, Yelick PC (2004) Bioengineered teeth from cultured rat tooth bud cells. J Dent Res 83:523–528

    PubMed  CAS  Google Scholar 

  • Eames BF, Schneider RA (2005) Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development. Development 132:1499–1509

    PubMed  CAS  Google Scholar 

  • Eastoe JE (1960) Organic matrix of tooth enamel. Nature 187:411–412

    PubMed  CAS  Google Scholar 

  • Esposito M, Hirsch JM, Lekholm U, Thomsen P (1998) Biological factors contributing to failures of osseointegrated oral implants. II. Etiopathogenesis. Eur J Oral Sci 106:721–764

    PubMed  CAS  Google Scholar 

  • Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156

    PubMed  CAS  Google Scholar 

  • Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528–1530

    PubMed  CAS  Google Scholar 

  • Filshie RJ, Zannettino AC, Makrynikola V, Gronthos S, Henniker AJ, Bendall LJ, Gottlieb DJ, Simmons PJ, Bradstock KF (1998) MUC18, a member of the immunoglobulin superfamily, is expressed on bone marrow fibroblasts and a subset of hematological malignancies. Leukemia 12:414–421

    PubMed  CAS  Google Scholar 

  • Fitzgerald M, Chiego DJ Jr, Heys DR (1990) Autoradiographic analysis of odontoblast replacement following pulp exposure in primate teeth. Arch Oral Biol 35:707–715

    PubMed  CAS  Google Scholar 

  • Fleischmajer R (1967) Epithelial-mesenchymal interactions. Science 157:1472–1482

    PubMed  CAS  Google Scholar 

  • Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, Ruadkow IA (1974) Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 2:83–92

    PubMed  CAS  Google Scholar 

  • Fujii S, Maeda H, Wada N, Kano Y, Akamine A (2006) Establishing and characterizing human periodontal ligament fibroblasts immortalized by SV40T-antigen and hTERT gene transfer. Cell Tissue Res 324:117–125

    PubMed  CAS  Google Scholar 

  • Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438

    PubMed  CAS  Google Scholar 

  • Gould TR (1983) Ultrastructural characteristics of progenitor cell populations in the periodontal ligament. J Dent Res 62:873–876

    PubMed  CAS  Google Scholar 

  • Gould TR, Melcher AH, Brunette DM (1977) Location of progenitor cells in periodontal ligament of mouse molar stimulated by wounding. Anat Rec 188:133–141

    PubMed  CAS  Google Scholar 

  • Gould TR, Melcher AH, Brunette DM (1980) Migration and division of progenitor cell populations in periodontal ligament after wounding. J Periodontal Res 15:20–42

    PubMed  CAS  Google Scholar 

  • Grigoriou M, Tucker AS, Sharpe PT, Pachnis V (1998) Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. Development 125:2063–2074

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81:531–535

    PubMed  CAS  Google Scholar 

  • Handa K, Saito M, Tsunoda A, Yamauchi M, Hattori S, Sato S, Toyoda M, Teranaka T, Narayanan AS (2002a) Progenitor cells from dental follicle are able to form cementum matrix in vivo. Connect Tissue Res 43:406–408

    PubMed  Google Scholar 

  • Handa K, Saito M, Yamauchi M, Kiyono T, Sato S, Teranaka T, Sampath Narayanan A (2002b) Cementum matrix formation in vivo by cultured dental follicle cells. Bone 31:606–611

    PubMed  CAS  Google Scholar 

  • Harada H, Kettunen P, Jung HS, Mustonen T, Wang YA, Thesleff I (1999) Localization of putative stem cells in dental epithelium and their association with Notch and FGF signaling. J Cell Biol 147:105–120

    PubMed  CAS  Google Scholar 

  • Harada H, Toyono T, Toyoshima K, Yamasaki M, Itoh N, Kato S, Sekine K, Ohuchi H (2002) FGF10 maintains stem cell compartment in developing mouse incisors. Development 129:1533–1541

    PubMed  CAS  Google Scholar 

  • Hay MF (1961) The development in vivo and in vitro of the lower incisor and molars of the mouse. Arch Oral Biol 3:86–109

    PubMed  CAS  Google Scholar 

  • Honda MJ, Sumita Y, Kagami H, Ueda M (2005) Histological and immunohistochemical studies of tissue engineered odontogenesis. Arch Histol Cytol 68:89–101

    PubMed  Google Scholar 

  • Honda MJ, Ohara T, Sumita Y, Ogaeri T, Kagami H, Ueda M (2006) Preliminary study of tissue-engineered odontogenesis in the canine jaw. J Oral Maxillofac Surg 64:283–289

    PubMed  Google Scholar 

  • Honda MJ, Tsuchiya S, Sumita Y, Sagara H, Ueda M (2007) The sequential seeding of epithelial and mesenchymal cells for tissue-engineered tooth regeneration. Biomaterials 28:680–689

    PubMed  CAS  Google Scholar 

  • Hu B, Nadiri A, Bopp-Kuchler S, Perrin-Schmitt F, Lesot H (2005a) Dental epithelial histomorphogenesis in vitro. J Dent Res 84:521–525

    PubMed  CAS  Google Scholar 

  • Hu B, Nadiri A, Bopp-Kuchler S, Perrin-Schmitt F, Wang S, Lesot H (2005b) Dental epithelial histo-morphogenesis in the mouse: positional information versus cell history. Arch Oral Biol 50:131–136

    PubMed  Google Scholar 

  • Hu B, Nadiri A, Kuchler-Bopp S, Perrin-Schmitt F, Peters H, Lesot H (2006a) Tissue engineering of tooth crown, root, and periodontium. Tissue Eng 12:2069-2075

    PubMed  CAS  Google Scholar 

  • Hu B, Unda F, Bopp-Kuchler S, Jimenez L, Wang XJ, Haikel Y, Wang SL, Lesot H (2006b) Bone marrow cells can give rise to ameloblast-like cells. J Dent Res 85:416–421

    PubMed  CAS  Google Scholar 

  • Ivanovski S, Haase HR, Bartold PM (2001) Isolation and characterization of fibroblasts derived from regenerating human periodontal defects. Arch Oral Biol 46:679–688

    PubMed  CAS  Google Scholar 

  • Jernvall J, Thesleff I (2000) Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev 92:19–29

    PubMed  CAS  Google Scholar 

  • Jernvall J, Kettunen P, Karavanova I, Martin LB, Thesleff I (1994) Evidence for the role of the enamel knot as a control center in mammalian tooth cusp formation: non-dividing cells express growth stimulating FGF-4 gene. Int J Dev Biol 38:463–469

    PubMed  CAS  Google Scholar 

  • Jo YY, Lee HJ, Kook SY, Choung HW, Park JY, Chung JH, Choung YH, Kim ES, Yang HC, Choung PH (2007) Isolation and characterization of postnatal stem cells from human dental tissues. Tissue Eng 13:767–773

    PubMed  CAS  Google Scholar 

  • Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N, Groffen J (1995) Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 11:415–421

    PubMed  CAS  Google Scholar 

  • Kawano S, Saito M, Handa K, Morotomi T, Toyono T, Seta Y, Nakamura N, Uchida T, Toyoshima K, Ohishi M, Harada H (2004) Characterization of dental epithelial progenitor cells derived from cervical-loop epithelium in a rat lower incisor. J Dent Res 83:129–133

    PubMed  CAS  Google Scholar 

  • Kemoun P, Laurencin-Dalicieux S, Rue J, Farges JC, Gennero I, Conte-Auriol F, Briand-Mesange F, Gadelorge M, Arzate H, Narayanan AS, Brunel G, Salles JP (2007) Human dental follicle cells acquire cementoblast features under stimulation by BMP-2/-7 and enamel matrix derivatives (EMD) in vitro. Cell Tissue Res 329:283–294

    PubMed  CAS  Google Scholar 

  • Keranen SV, Kettunen P, Aberg T, Thesleff I, Jernvall J (1999) Gene expression patterns associated with suppression of odontogenesis in mouse and vole diastema regions. Dev Genes Evol 209:495–506

    PubMed  CAS  Google Scholar 

  • Kettunen P, Thesleff I (1998) Expression and function of FGFs-4, -8, and -9 suggest functional redundancy and repetitive use as epithelial signals during tooth morphogenesis. Dev Dyn 211:256–268

    PubMed  CAS  Google Scholar 

  • Kim JH, Auerbach JM, Rodriguez-Gomez JA, Velasco I, Gavin D, Lumelsky N, Lee SH, Nguyen J, Sanchez-Pernaute R, Bankiewicz K, McKay R (2002) Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson’s disease. Nature 418:50–56

    PubMed  CAS  Google Scholar 

  • Klein OD, Minowada G, Peterkova R, Kangas A, Yu BD, Lesot H, Peterka M, Jernvall J, Martin GR (2006) Sprouty genes control diastema tooth development via bidirectional antagonism of epithelial-mesenchymal FGF signaling. Dev Cell 11:181–190

    PubMed  CAS  Google Scholar 

  • Kollar EJ (1970) The induction of hair follicles by embryonic dermal papillae. J Invest Dermatol 55:374–378

    PubMed  CAS  Google Scholar 

  • Kollar EJ, Baird GR (1970) Tissue interactions in embryonic mouse tooth germs. II. The inductive role of the dental papilla. J Embryol Exp Morphol 24:173–186

    PubMed  CAS  Google Scholar 

  • Kollar EJ, Fisher C (1980) Tooth induction in chick epithelium: expression of quiescent genes for enamel synthesis. Science 207:993–995

    PubMed  CAS  Google Scholar 

  • Komine A, Suenaga M, Nakao K, Tsuji T, Tomooka Y (2007) Tooth regeneration from newly established cell lines from a molar tooth germ epithelium. Biochem Biophys Res Commun 355:758–763

    PubMed  CAS  Google Scholar 

  • Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ (2001) Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105:369–377

    PubMed  CAS  Google Scholar 

  • Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M (2000) Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6:1229–1234

    PubMed  CAS  Google Scholar 

  • Laino G, d’Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G (2005) A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 20:1394–1402

    PubMed  Google Scholar 

  • Laino G, Carinci F, Graziano A, d’Aquino R, Lanza V, De Rosa A, Gombos F, Caruso F, Guida L, Rullo R, Menditti D, Papaccio G (2006a) In vitro bone production using stem cells derived from human dental pulp. J Craniofac Surg 17:511–515

    PubMed  Google Scholar 

  • Laino G, Graziano A, d’Aquino R, Pirozzi G, Lanza V, Valiante S, De Rosa A, Naro F, Vivarelli E, Papaccio G (2006b) An approachable human adult stem cell source for hard-tissue engineering. J Cell Physiol 206:693–701

    PubMed  CAS  Google Scholar 

  • Langer R, Folkman J (1976) Polymers for the sustained release of proteins and other macromolecules. Nature 263:797–800

    PubMed  CAS  Google Scholar 

  • Langer R, Tirrell DA (2004) Designing materials for biology and medicine. Nature 428:487–492

    PubMed  CAS  Google Scholar 

  • Langer R, Vacanti JP (1993) Tissue engineering. Science 260:920–926

    PubMed  CAS  Google Scholar 

  • Layer PG, Robitzki A, Rothermel A, Willbold E (2002) Of layers and spheres: the reaggregate approach in tissue engineering. Trends Neurosci 25:131–134

    PubMed  CAS  Google Scholar 

  • Lemus D, Coloma L, Fuenzalida M, Illanes J, Paz de la Vega Y, Ondarza A, Blanquez MJ (1986) Odontogenesis and amelogenesis in interacting lizard-quail tissue combinations. J Morphol 189:121–129

    PubMed  CAS  Google Scholar 

  • Limeback H, Sodek J, Aubin JE (1983) Variation in collagen expression by cloned periodontal ligament cells. J Periodontal Res 18:242–248

    PubMed  CAS  Google Scholar 

  • Lin D, Huang Y, He F, Gu S, Zhang G, Chen Y, Zhang Y (2007) Expression survey of genes critical for tooth development in the human embryonic tooth germ. Dev Dyn 236:1307–1312

    PubMed  CAS  Google Scholar 

  • Liu H, Gronthos S, Shi S (2006) Dental pulp stem cells. Methods Enzymol 419:99–113

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Lumelsky N, Blondel O, Laeng P, Velasco I, Ravin R, McKay R (2001) Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292:1389–1394

    PubMed  CAS  Google Scholar 

  • Lumsden AG (1988) Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103 (Suppl):155–169

    PubMed  Google Scholar 

  • Maas R, Bei M (1997) The genetic control of early tooth development. Crit Rev Oral Biol Med 8:4–39

    Article  PubMed  CAS  Google Scholar 

  • Main JH (1966) Retention of potential to differentiate in long-term cultures of tooth germs. Science 152:778–780

    PubMed  Google Scholar 

  • McCulloch CA (1985) Progenitor cell populations in the periodontal ligament of mice. Anat Rec 211:258–262

    PubMed  CAS  Google Scholar 

  • McCulloch CA, Nemeth E, Lowenberg B, Melcher AH (1987) Paravascular cells in endosteal spaces of alveolar bone contribute to periodontal ligament cell populations. Anat Rec 219:233–242

    PubMed  CAS  Google Scholar 

  • McKay R (1997) Stem cells in the central nervous system. Science 276:66–71

    PubMed  CAS  Google Scholar 

  • Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR (2000) Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290:1779–1782

    PubMed  CAS  Google Scholar 

  • Mina M, Kollar EJ (1987) The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Arch Oral Biol 32:123–127

    PubMed  CAS  Google Scholar 

  • Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S (2003) SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 100:5807–5812

    PubMed  CAS  Google Scholar 

  • Modino SA, Sharpe PT (2005) Tissue engineering of teeth using adult stem cells. Arch Oral Biol 50:255–258

    PubMed  Google Scholar 

  • Morio I (1985) Recombinant study of the mouse molar cervical loop and dental papilla by renal transplantation. Arch Oral Biol 30:557–561

    PubMed  CAS  Google Scholar 

  • Morotomi T, Kawano S, Toyono T, Kitamura C, Terashita M, Uchida T, Toyoshima K, Harada H (2005) In vitro differentiation of dental epithelial progenitor cells through epithelial-mesenchymal interactions. Arch Oral Biol 50:695–705

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Morshead CM, Benveniste P, Iscove NN, Kooy D van der (2002) Hematopoietic competence is a rare property of neural stem cells that may depend on genetic and epigenetic alterations. Nat Med 8:268–273

    PubMed  CAS  Google Scholar 

  • Moscona A, Moscona H (1952) The dissociation and aggregation of cells from organ rudiments of the early chick embryo. J Anat 86:287–301

    PubMed  CAS  Google Scholar 

  • Nakao K, Morita R, Saji Y, Ishida K, Tomita Y, Ogawa M, Saitoh M, Tomooka Y, Tsuji T (2007) The development of a bioengineered organ germ method. Nat Methods 4:227–230

    PubMed  CAS  Google Scholar 

  • Nakata A, Kameda T, Nagai H, Ikegami K, Duan Y, Terada K, Sugiyama T (2003) Establishment and characterization of a spontaneously immortalized mouse ameloblast-lineage cell line. Biochem Biophys Res Commun 308:834–839

    PubMed  CAS  Google Scholar 

  • Nehls V, Drenckhahn D (1993) The versatility of microvascular pericytes: from mesenchyme to smooth muscle? Histochemistry 99:1–12

    PubMed  CAS  Google Scholar 

  • Niswander L, Martin GR (1992) FGF-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114:755–768

    PubMed  CAS  Google Scholar 

  • Ohazama A, Modino SA, Miletich I, Sharpe PT (2004) Stem-cell-based tissue engineering of murine teeth. J Dent Res 83:518–522

    PubMed  CAS  Google Scholar 

  • Ohshima H, Kenmotsu S, Harada H (2003) Use of the term apical bud to refer to the apical end of the continuously growing tooth. Arch Comp Biol Tooth Enamel 8:45–49

    Google Scholar 

  • Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P (2001) Bone marrow cells regenerate infarcted myocardium. Nature 410:701–705

    PubMed  CAS  Google Scholar 

  • Papaccio G, Graziano A, d’Aquino R, Graziano MF, Pirozzi G, Menditti D, De Rosa A, Carinci F, Laino G (2006) Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated osteoblasts: a cell source for tissue repair. J Cell Physiol 208:319–325

    PubMed  CAS  Google Scholar 

  • Peters H, Neubuser A, Kratochwil K, Balling R (1998) Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities. Genes Dev 12:2735–2747

    PubMed  CAS  Google Scholar 

  • Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP (1999) Bone marrow as a potential source of hepatic oval cells. Science 284:1168–1170

    PubMed  CAS  Google Scholar 

  • Pierdomenico L, Bonsi L, Calvitti M, Rondelli D, Arpinati M, Chirumbolo G, Becchetti E, Marchionni C, Alviano F, Fossati V, Staffolani N, Franchina M, Grossi A, Bagnara GP (2005) Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 80:836–842

    PubMed  Google Scholar 

  • Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147

    PubMed  CAS  Google Scholar 

  • Potter SW, Morris JE (1985) Development of mouse embryos in hanging drop culture. Anat Rec 211:48–56

    PubMed  CAS  Google Scholar 

  • Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74

    PubMed  CAS  Google Scholar 

  • Reynolds AJ, Jahoda CA (2004) Cultured human and rat tooth papilla cells induce hair follicle regeneration and fiber growth. Differentiation 72:566–575

    PubMed  Google Scholar 

  • Robinson C, Brookes SJ, Shore RC, Kirkham J (1998) The developing enamel matrix: nature and function. Eur J Oral Sci 106 (Suppl 1):282–291

    PubMed  CAS  Google Scholar 

  • Ruch JV (1998) Odontoblast commitment and differentiation. Biochem Cell Biol 76:923–938

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Sanders EJ (1988) The roles of epithelial-mesenchymal cell interactions in developmental processes. Biochem Cell Biol 66:530–540

    Article  PubMed  CAS  Google Scholar 

  • Sarkar L, Sharpe PT (1999) Expression of Wnt signalling pathway genes during tooth development. Mech Dev 85:197–200

    PubMed  CAS  Google Scholar 

  • Satomura K, Krebsbach P, Bianco P, Gehron Robey P (2000) Osteogenic imprinting upstream of marrow stromal cell differentiation. J Cell Biochem 78:391–403

    PubMed  CAS  Google Scholar 

  • Scadden DT (2006) The stem-cell niche as an entity of action. Nature 441:1075–1079

    PubMed  CAS  Google Scholar 

  • Senzaki H (1980) A histological study of reparative dentinogenesis in the rat incisor after colchicine administration. Arch Oral Biol 25:737–743

    PubMed  CAS  Google Scholar 

  • Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, Young M, Robey PG, Wang CY, Shi S (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364:149–155

    PubMed  CAS  Google Scholar 

  • Seo BM, Miura M, Sonoyama W, Coppe C, Stanyon R, Shi S (2005) Recovery of stem cells from cryopreserved periodontal ligament. J Dent Res 84:907–912

    PubMed  Google Scholar 

  • Sharpe PT, Young CS (2005) Test-tube teeth. Sci Am 293:34–41

    Article  PubMed  Google Scholar 

  • Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338–1340

    PubMed  CAS  Google Scholar 

  • Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18:696–704

    PubMed  Google Scholar 

  • Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S (2005) The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res 8:191–199

    PubMed  CAS  Google Scholar 

  • Shigetani Y, Sugahara F, Kawakami Y, Murakami Y, Hirano S, Kuratani S (2002) Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science 296:1316–1319

    PubMed  CAS  Google Scholar 

  • Slavkin HC, Bavetta LA (1968) Odontogenesis in vivo and in xenografts on chick chorio-allantois. I. Collagen and hexosamine biosynthesis. Arch Oral Biol 13:145–154

    PubMed  CAS  Google Scholar 

  • Slavkin HC, Beierle J, Bavetta LA (1968) Odontogenesis: cell-cell interactions in vitro. Nature 217:269–270

    PubMed  CAS  Google Scholar 

  • Slavkin HC, Bringas P Jr, Bessem C, Santos V, Nakamura M, Hsu MY, Snead ML, Zeichner-David M, Fincham AG (1989) Hertwig’s epithelial root sheath differentiation and initial cementum and bone formation during long-term organ culture of mouse mandibular first molars using serumless, chemically-defined medium. J Periodontal Res 24:28–40

    PubMed  CAS  Google Scholar 

  • Smith CE (1980) Cell turnover in the odontogenic organ of the rat incisor as visualized by graphic reconstructions following a single injection of 3H-thymidine. Am J Anat 158:321–343

    PubMed  CAS  Google Scholar 

  • Smith AJ, Lesot H (2001) Induction and regulation of crown dentinogenesis: embryonic events as a template for dental tissue repair? Crit Rev Oral Biol Med 12:425–437

    PubMed  CAS  Google Scholar 

  • Somerman MJ, Ouyang HJ, Berry JE, Saygin NE, Strayhorn CL, D’Errico JA, Hullinger T, Giannobile WV (1999) Evolution of periodontal regeneration: from the roots’ point of view. J Periodontal Res 34:420–424

    PubMed  CAS  Google Scholar 

  • Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C, Liu H, Gronthos S, Wang CY, Shi S, Wang S (2006) Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 1:e79

    PubMed  Google Scholar 

  • Spangrude GJ, Heimfeld S, Weissman IL (1988) Purification and characterization of mouse hematopoietic stem cells. Science 241:58–62

    PubMed  CAS  Google Scholar 

  • Spradling A, Drummond-Barbosa D, Kai T (2001) Stem cells find their niche. Nature 414:98–104

    PubMed  CAS  Google Scholar 

  • Steele-Perkins G, Butz KG, Lyons GE, Zeichner-David M, Kim HJ, Cho MI, Gronostajski RM (2003) Essential role for NFI-C/CTF transcription-replication factor in tooth root development. Mol Cell Biol 23:1075–1084

    PubMed  CAS  Google Scholar 

  • Steinberg MS, Gilbert SF (2004) Townes and Holtfreter (1955): directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool [A] Comp Exp Biol 301:701–706

    Google Scholar 

  • Sveen OB, Hawes RR (1968) Differentiation of new odontoblasts and dentine bridge formation in rat molar teeth after tooth grinding. Arch Oral Biol 13:1399–1409

    PubMed  CAS  Google Scholar 

  • Tecles O, Laurent P, Zygouritsas S, Burger AS, Camps J, Dejou J, About I (2005) Activation of human dental pulp progenitor/stem cells in response to odontoblast injury. Arch Oral Biol 50:103–108

    PubMed  CAS  Google Scholar 

  • Ten Cate AR (2003) Oral histology: development, structure and function, 6th edn. Elsevier, Amsterdam

    Google Scholar 

  • Thesleff I (2003) Epithelial-mesenchymal signalling regulating tooth morphogenesis. J Cell Sci 116:1647–1648

    PubMed  CAS  Google Scholar 

  • Thesleff I, Sharpe P (1997) Signalling networks regulating dental development. Mech Dev 67:111–123

    PubMed  CAS  Google Scholar 

  • Thesleff I, Keranen S, Jernvall J (2001) Enamel knots as signaling centers linking tooth morphogenesis and odontoblast differentiation. Adv Dent Res 15:14–18

    PubMed  CAS  Google Scholar 

  • Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147

    PubMed  CAS  Google Scholar 

  • Thonemann B, Schmalz G (2000) Immortalization of bovine dental papilla cells with Simian Virus 40 large T antigen. Arch Oral Biol 45:857–869

    PubMed  CAS  Google Scholar 

  • Townes PL, Holtfreter J (1955) Directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool 128:53–120

    Google Scholar 

  • Tucker A, Sharpe P (2004) The cutting-edge of mammalian development; how the embryo makes teeth. Nat Rev Genet 5:499–508

    PubMed  CAS  Google Scholar 

  • Tucker AS, Matthews KL, Sharpe PT (1998) Transformation of tooth type induced by inhibition of BMP signaling. Science 282:1136–1138

    PubMed  CAS  Google Scholar 

  • Tucker AS, Headon DJ, Schneider P, Ferguson BM, Overbeek P, Tschopp J, Sharpe PT (2000) Edar/Eda interactions regulate enamel knot formation in tooth morphogenesis. Development 127:4691–4700

    PubMed  CAS  Google Scholar 

  • Tummers M, Thesleff I (2003) Root or crown: a developmental choice orchestrated by the differential regulation of the epithelial stem cell niche in the tooth of two rodent species. Development 130:1049–1057

    PubMed  CAS  Google Scholar 

  • Tziafas D (1995) Basic mechanisms of cytodifferentiation and dentinogenesis during dental pulp repair. Int J Dev Biol 39:281–290

    PubMed  CAS  Google Scholar 

  • Vaahtokari A, Aberg T, Jernvall J, Keranen S, Thesleff I (1996) The enamel knot as a signaling center in the developing mouse tooth. Mech Dev 54:39–43

    PubMed  CAS  Google Scholar 

  • Vainio S, Karavanova I, Jowett A, Thesleff I (1993) Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75:45–58

    PubMed  CAS  Google Scholar 

  • Verfaillie CM (2002) Adult stem cells: assessing the case for pluripotency. Trends Cell Biol 12:502–508

    PubMed  CAS  Google Scholar 

  • Wagers AJ, Sherwood RI, Christensen JL, Weissman IL (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297:2256–2259

    PubMed  CAS  Google Scholar 

  • Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches. Science 287:1427–1430

    PubMed  CAS  Google Scholar 

  • Weiss P, Taylor AC (1960) Reconstitution of complete organs from single-cell suspensions of chick embryos in advanced stages of differentiation. Proc Natl Acad Sci USA 46:1177–1185

    PubMed  CAS  Google Scholar 

  • Weissman IL (2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157–168

    PubMed  CAS  Google Scholar 

  • Wilson HV (1907) On some phenomena of coalescence and regeneration in sponges. J Exp Zool 5:245–258

    Google Scholar 

  • Yamada M, Bringas P Jr, Grodin M, MacDougall M, Cummings E, Grimmett J, Weliky B, Slavkin HC (1980) Chemically-defined organ culture of embryonic mouse tooth organs: morphogenesis, dentinogenesis and amelogenesis. J Biol Buccale 8:127–139

    PubMed  CAS  Google Scholar 

  • Yamamura T (1985) Differentiation of pulpal cells and inductive influences of various matrices with reference to pulpal wound healing. J Dent Res 64 (Spec No):530–540

    PubMed  Google Scholar 

  • Yokohama-Tamaki T, Ohshima H, Fujiwara N, Takada Y, Ichimori Y, Wakisaka S, Ohuchi H, Harada H (2006) Cessation of FGF10 signaling, resulting in a defective dental epithelial stem cell compartment, leads to the transition from crown to root formation. Development 133:1359–1366

    PubMed  CAS  Google Scholar 

  • Yokoi T, Saito M, Kiyono T, Iseki S, Kosaka K, Nishida E, Tsubakimoto T, Harada H, Eto K, Noguchi T, Teranaka T (2007) Establishment of immortalized dental follicle cells for generating periodontal ligament in vivo. Cell Tissue Res 327:301–311

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Young CS, Terada S, Vacanti JP, Honda M, Bartlett JD, Yelick PC (2002) Tissue engineering of complex tooth structures on biodegradable polymer scaffolds. J Dent Res 81:695–700

    Article  PubMed  CAS  Google Scholar 

  • Yu J, McMahon AP, Valerius MT (2004) Recent genetic studies of mouse kidney development. Curr Opin Genet Dev 14:550–557

    PubMed  CAS  Google Scholar 

  • Yu J, Wang Y, Deng Z, Tang L, Li Y, Shi J, Jin Y (2007) Odontogenic capability: bone marrow stromal stem cells versus dental pulp stem cells. Biol Cell 99:465–474

    Google Scholar 

  • Zander HA (1939) Reaction of the pulp to calcium hydroxide. J Dent Res 18:373

    CAS  Google Scholar 

  • Zeichner-David M, Oishi K, Su Z, Zakartchenko V, Chen LS, Arzate H, Bringas P Jr (2003) Role of Hertwig’s epithelial root sheath cells in tooth root development. Dev Dyn 228:651–663

    PubMed  CAS  Google Scholar 

  • Zhang W, Walboomers XF, Shi S, Fan M, Jansen JA (2006) Multilineage differentiation potential of stem cells derived from human dental pulp after cryopreservation. Tissue Eng 12:2813–2823

    PubMed  CAS  Google Scholar 

  • Zhou P, Byrne C, Jacobs J, Fuchs E (1995) Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev 9:700–713

    PubMed  CAS  Google Scholar 

  • Zussman WV (1966) Osteogenic activity of odontoblasts in transplanted tooth pulps. J Dent Res 45:144–151

    PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Dr. Puangwan Lapthanasupkul for kindly providing the sections that appear in Fig. 1.

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Correspondence to Paul T. Sharpe.

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Yen, A.HH., Sharpe, P.T. Stem cells and tooth tissue engineering. Cell Tissue Res 331, 359–372 (2008). https://doi.org/10.1007/s00441-007-0467-6

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