Cell and Tissue Research

, Volume 331, Issue 1, pp 359–372 | Cite as

Stem cells and tooth tissue engineering

Review

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.

Keywords

Teeth Stem cells Tissue engineering Odontogenesis Epithelial-mesenchymal interaction 

References

  1. About I, Bottero MJ, Denato P de, Camps J, Franquin JC, Mitsiadis TA (2000) Human dentin production in vitro. Exp Cell Res 258:33–41PubMedGoogle Scholar
  2. Amar S, Chung KM (1994) Clinical implications of cellular biologic advances in periodontal regeneration. Curr Opin Periodontol 18:128–140Google Scholar
  3. 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 342:718–724PubMedGoogle Scholar
  4. Arias AM (2001) Epithelial mesenchymal interactions in cancer and development. Cell 105:425–431PubMedGoogle Scholar
  5. 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 275:964–967PubMedGoogle Scholar
  6. 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 105:599–608PubMedGoogle Scholar
  7. Aukhil I, Pettersson E, Suggs C (1986) Guided tissue regeneration: an experimental procedure in beagle dogs. J Periodontol 57:727–734PubMedGoogle Scholar
  8. 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 82:976–981PubMedGoogle Scholar
  9. Bei M, Kratochwil K, Maas RL (2000) BMP4 rescues a non-cell-autonomous function of Msx1 in tooth development. Development 127:4711–4718PubMedGoogle Scholar
  10. 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 283:534–537PubMedGoogle Scholar
  11. Braut A, Kalajzic I, Kalajzic Z, Rowe DW, Kollar EJ, Mina M (2002) Col1a1-GFP transgene expression in developing incisors. Connect Tissue Res 43:216–219PubMedGoogle Scholar
  12. 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 47:281–292PubMedGoogle Scholar
  13. Caplan AI, Bruder SP (2001) Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7:259–264PubMedGoogle Scholar
  14. Chen Y, Bei M, Woo I, Satokata I, Maas R (1996) Msx1 controls inductive signaling in mammalian tooth morphogenesis. Development 122:3035–3044PubMedGoogle Scholar
  15. 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 97:10044–10049PubMedGoogle Scholar
  16. Chiba M (1965) Cellular proliferation in the tooth germ of the rat incisor. Arch Oral Biol 10:707–718PubMedGoogle Scholar
  17. 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 107:639–646PubMedGoogle Scholar
  18. Cobourne MT, Sharpe PT (2003) Tooth and jaw: molecular mechanisms of patterning in the first branchial arch. Arch Oral Biol 48:1–14PubMedGoogle Scholar
  19. Cobourne MT, Sharpe PT (2005) Sonic hedgehog signaling and the developing tooth. Curr Top Dev Biol 65:255–287PubMedGoogle Scholar
  20. Crubezy E, Murail P, Girard L, Bernadou JP (1998) False teeth of the Roman world. Nature 391:29PubMedGoogle Scholar
  21. Cutler LS, Gremski W (1991) Epithelial-mesenchymal interactions in the development of salivary glands. Crit Rev Oral Biol Med 2:1–12PubMedGoogle Scholar
  22. 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 14:1162–1171Google Scholar
  23. 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 25:39–47PubMedGoogle Scholar
  24. 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 71:63–72PubMedGoogle Scholar
  25. 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 126:2911–2920PubMedGoogle Scholar
  26. Dassule HR, McMahon AP (1998) Analysis of epithelial-mesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev Biol 202:215–227PubMedGoogle Scholar
  27. Dassule HR, Lewis P, Bei M, Maas R, McMahon AP (2000) Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127:4775–4785PubMedGoogle Scholar
  28. 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 13:828–838PubMedGoogle Scholar
  29. Duailibi MT, Duailibi SE, Young CS, Bartlett JD, Vacanti JP, Yelick PC (2004) Bioengineered teeth from cultured rat tooth bud cells. J Dent Res 83:523–528PubMedGoogle Scholar
  30. Eames BF, Schneider RA (2005) Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development. Development 132:1499–1509PubMedGoogle Scholar
  31. Eastoe JE (1960) Organic matrix of tooth enamel. Nature 187:411–412PubMedGoogle Scholar
  32. Esposito M, Hirsch JM, Lekholm U, Thomsen P (1998) Biological factors contributing to failures of osseointegrated oral implants. II. Etiopathogenesis. Eur J Oral Sci 106:721–764PubMedGoogle Scholar
  33. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156PubMedGoogle Scholar
  34. 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 279:1528–1530PubMedGoogle Scholar
  35. 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 12:414–421PubMedGoogle Scholar
  36. Fitzgerald M, Chiego DJ Jr, Heys DR (1990) Autoradiographic analysis of odontoblast replacement following pulp exposure in primate teeth. Arch Oral Biol 35:707–715PubMedGoogle Scholar
  37. Fleischmajer R (1967) Epithelial-mesenchymal interactions. Science 157:1472–1482PubMedGoogle Scholar
  38. 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 2:83–92PubMedGoogle Scholar
  39. 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 324:117–125PubMedGoogle Scholar
  40. Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438PubMedGoogle Scholar
  41. Gould TR (1983) Ultrastructural characteristics of progenitor cell populations in the periodontal ligament. J Dent Res 62:873–876PubMedGoogle Scholar
  42. Gould TR, Melcher AH, Brunette DM (1977) Location of progenitor cells in periodontal ligament of mouse molar stimulated by wounding. Anat Rec 188:133–141PubMedGoogle Scholar
  43. Gould TR, Melcher AH, Brunette DM (1980) Migration and division of progenitor cell populations in periodontal ligament after wounding. J Periodontal Res 15:20–42PubMedGoogle Scholar
  44. 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 125:2063–2074PubMedGoogle Scholar
  45. 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 97:13625–13630PubMedGoogle Scholar
  46. 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 81:531–535PubMedGoogle Scholar
  47. 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 43:406–408PubMedGoogle Scholar
  48. 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 31:606–611PubMedGoogle Scholar
  49. 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 147:105–120PubMedGoogle Scholar
  50. 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 129:1533–1541PubMedGoogle Scholar
  51. Hay MF (1961) The development in vivo and in vitro of the lower incisor and molars of the mouse. Arch Oral Biol 3:86–109PubMedGoogle Scholar
  52. Honda MJ, Sumita Y, Kagami H, Ueda M (2005) Histological and immunohistochemical studies of tissue engineered odontogenesis. Arch Histol Cytol 68:89–101PubMedGoogle Scholar
  53. 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 64:283–289PubMedGoogle Scholar
  54. 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 28:680–689PubMedGoogle Scholar
  55. Hu B, Nadiri A, Bopp-Kuchler S, Perrin-Schmitt F, Lesot H (2005a) Dental epithelial histomorphogenesis in vitro. J Dent Res 84:521–525PubMedGoogle Scholar
  56. 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 50:131–136PubMedGoogle Scholar
  57. 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 12:2069-2075PubMedGoogle Scholar
  58. 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 85:416–421PubMedGoogle Scholar
  59. Ivanovski S, Haase HR, Bartold PM (2001) Isolation and characterization of fibroblasts derived from regenerating human periodontal defects. Arch Oral Biol 46:679–688PubMedGoogle Scholar
  60. Jernvall J, Thesleff I (2000) Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev 92:19–29PubMedGoogle Scholar
  61. 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 38:463–469PubMedGoogle Scholar
  62. 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 13:767–773PubMedGoogle Scholar
  63. 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 11:415–421PubMedGoogle Scholar
  64. 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 83:129–133PubMedGoogle Scholar
  65. 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 329:283–294PubMedGoogle Scholar
  66. 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 209:495–506PubMedGoogle Scholar
  67. 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 211:256–268PubMedGoogle Scholar
  68. 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 418:50–56PubMedGoogle Scholar
  69. 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 11:181–190PubMedGoogle Scholar
  70. Kollar EJ (1970) The induction of hair follicles by embryonic dermal papillae. J Invest Dermatol 55:374–378PubMedGoogle Scholar
  71. Kollar EJ, Baird GR (1970) Tissue interactions in embryonic mouse tooth germs. II. The inductive role of the dental papilla. J Embryol Exp Morphol 24:173–186PubMedGoogle Scholar
  72. Kollar EJ, Fisher C (1980) Tooth induction in chick epithelium: expression of quiescent genes for enamel synthesis. Science 207:993–995PubMedGoogle Scholar
  73. 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 355:758–763PubMedGoogle Scholar
  74. 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 105:369–377PubMedGoogle Scholar
  75. 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 6:1229–1234PubMedGoogle Scholar
  76. 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 20:1394–1402PubMedGoogle Scholar
  77. 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 17:511–515PubMedGoogle Scholar
  78. 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 206:693–701PubMedGoogle Scholar
  79. Langer R, Folkman J (1976) Polymers for the sustained release of proteins and other macromolecules. Nature 263:797–800PubMedGoogle Scholar
  80. Langer R, Tirrell DA (2004) Designing materials for biology and medicine. Nature 428:487–492PubMedGoogle Scholar
  81. Langer R, Vacanti JP (1993) Tissue engineering. Science 260:920–926PubMedGoogle Scholar
  82. Layer PG, Robitzki A, Rothermel A, Willbold E (2002) Of layers and spheres: the reaggregate approach in tissue engineering. Trends Neurosci 25:131–134PubMedGoogle Scholar
  83. 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 189:121–129PubMedGoogle Scholar
  84. Limeback H, Sodek J, Aubin JE (1983) Variation in collagen expression by cloned periodontal ligament cells. J Periodontal Res 18:242–248PubMedGoogle Scholar
  85. 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 236:1307–1312PubMedGoogle Scholar
  86. Liu H, Gronthos S, Shi S (2006) Dental pulp stem cells. Methods Enzymol 419:99–113PubMedGoogle Scholar
  87. Luan X, Ito Y, Dangaria S, Diekwisch TG (2006) Dental follicle progenitor cell heterogeneity in the developing mouse periodontium. Stem Cells Dev 15:595–608PubMedGoogle Scholar
  88. 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 292:1389–1394PubMedGoogle Scholar
  89. 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):155–169PubMedGoogle Scholar
  90. Maas R, Bei M (1997) The genetic control of early tooth development. Crit Rev Oral Biol Med 8:4–39PubMedCrossRefGoogle Scholar
  91. Main JH (1966) Retention of potential to differentiate in long-term cultures of tooth germs. Science 152:778–780PubMedGoogle Scholar
  92. McCulloch CA (1985) Progenitor cell populations in the periodontal ligament of mice. Anat Rec 211:258–262PubMedGoogle Scholar
  93. 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 219:233–242PubMedGoogle Scholar
  94. McKay R (1997) Stem cells in the central nervous system. Science 276:66–71PubMedGoogle Scholar
  95. 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 290:1779–1782PubMedGoogle Scholar
  96. Mina M, Kollar EJ (1987) The induction of odontogenesis in non-dental mesenchyme combined with early murine mandibular arch epithelium. Arch Oral Biol 32:123–127PubMedGoogle Scholar
  97. 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 100:5807–5812PubMedGoogle Scholar
  98. Modino SA, Sharpe PT (2005) Tissue engineering of teeth using adult stem cells. Arch Oral Biol 50:255–258PubMedGoogle Scholar
  99. Morio I (1985) Recombinant study of the mouse molar cervical loop and dental papilla by renal transplantation. Arch Oral Biol 30:557–561PubMedGoogle Scholar
  100. 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 50:695–705PubMedGoogle Scholar
  101. 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 24:155–165PubMedGoogle Scholar
  102. 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 8:268–273PubMedGoogle Scholar
  103. Moscona A, Moscona H (1952) The dissociation and aggregation of cells from organ rudiments of the early chick embryo. J Anat 86:287–301PubMedGoogle Scholar
  104. 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 4:227–230PubMedGoogle Scholar
  105. 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 308:834–839PubMedGoogle Scholar
  106. Nehls V, Drenckhahn D (1993) The versatility of microvascular pericytes: from mesenchyme to smooth muscle? Histochemistry 99:1–12PubMedGoogle Scholar
  107. Niswander L, Martin GR (1992) FGF-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114:755–768PubMedGoogle Scholar
  108. Ohazama A, Modino SA, Miletich I, Sharpe PT (2004) Stem-cell-based tissue engineering of murine teeth. J Dent Res 83:518–522PubMedGoogle Scholar
  109. 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 8:45–49Google Scholar
  110. 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 410:701–705PubMedGoogle Scholar
  111. 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 208:319–325PubMedGoogle Scholar
  112. 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 12:2735–2747PubMedGoogle Scholar
  113. 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 284:1168–1170PubMedGoogle Scholar
  114. 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 80:836–842PubMedGoogle Scholar
  115. 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 284:143–147PubMedGoogle Scholar
  116. Potter SW, Morris JE (1985) Development of mouse embryos in hanging drop culture. Anat Rec 211:48–56PubMedGoogle Scholar
  117. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74PubMedGoogle Scholar
  118. Reynolds AJ, Jahoda CA (2004) Cultured human and rat tooth papilla cells induce hair follicle regeneration and fiber growth. Differentiation 72:566–575PubMedGoogle Scholar
  119. Robinson C, Brookes SJ, Shore RC, Kirkham J (1998) The developing enamel matrix: nature and function. Eur J Oral Sci 106 (Suppl 1):282–291PubMedGoogle Scholar
  120. Ruch JV (1998) Odontoblast commitment and differentiation. Biochem Cell Biol 76:923–938PubMedGoogle Scholar
  121. 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 20:50–57PubMedGoogle Scholar
  122. Sanders EJ (1988) The roles of epithelial-mesenchymal cell interactions in developmental processes. Biochem Cell Biol 66:530–540PubMedCrossRefGoogle Scholar
  123. Sarkar L, Sharpe PT (1999) Expression of Wnt signalling pathway genes during tooth development. Mech Dev 85:197–200PubMedGoogle Scholar
  124. Satomura K, Krebsbach P, Bianco P, Gehron Robey P (2000) Osteogenic imprinting upstream of marrow stromal cell differentiation. J Cell Biochem 78:391–403PubMedGoogle Scholar
  125. Scadden DT (2006) The stem-cell niche as an entity of action. Nature 441:1075–1079PubMedGoogle Scholar
  126. Senzaki H (1980) A histological study of reparative dentinogenesis in the rat incisor after colchicine administration. Arch Oral Biol 25:737–743PubMedGoogle Scholar
  127. 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 364:149–155PubMedGoogle Scholar
  128. Seo BM, Miura M, Sonoyama W, Coppe C, Stanyon R, Shi S (2005) Recovery of stem cells from cryopreserved periodontal ligament. J Dent Res 84:907–912PubMedGoogle Scholar
  129. Sharpe PT, Young CS (2005) Test-tube teeth. Sci Am 293:34–41PubMedCrossRefGoogle Scholar
  130. 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 304:1338–1340PubMedGoogle Scholar
  131. Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18:696–704PubMedGoogle Scholar
  132. 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 8:191–199PubMedGoogle Scholar
  133. Shigetani Y, Sugahara F, Kawakami Y, Murakami Y, Hirano S, Kuratani S (2002) Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science 296:1316–1319PubMedGoogle Scholar
  134. Slavkin HC, Bavetta LA (1968) Odontogenesis in vivo and in xenografts on chick chorio-allantois. I. Collagen and hexosamine biosynthesis. Arch Oral Biol 13:145–154PubMedGoogle Scholar
  135. Slavkin HC, Beierle J, Bavetta LA (1968) Odontogenesis: cell-cell interactions in vitro. Nature 217:269–270PubMedGoogle Scholar
  136. 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 24:28–40PubMedGoogle Scholar
  137. 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 158:321–343PubMedGoogle Scholar
  138. 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 12:425–437PubMedGoogle Scholar
  139. 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 34:420–424PubMedGoogle Scholar
  140. 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:e79PubMedGoogle Scholar
  141. Spangrude GJ, Heimfeld S, Weissman IL (1988) Purification and characterization of mouse hematopoietic stem cells. Science 241:58–62PubMedGoogle Scholar
  142. Spradling A, Drummond-Barbosa D, Kai T (2001) Stem cells find their niche. Nature 414:98–104PubMedGoogle Scholar
  143. 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 23:1075–1084PubMedGoogle Scholar
  144. 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 301:701–706Google Scholar
  145. Sveen OB, Hawes RR (1968) Differentiation of new odontoblasts and dentine bridge formation in rat molar teeth after tooth grinding. Arch Oral Biol 13:1399–1409PubMedGoogle Scholar
  146. 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 50:103–108PubMedGoogle Scholar
  147. Ten Cate AR (2003) Oral histology: development, structure and function, 6th edn. Elsevier, AmsterdamGoogle Scholar
  148. Thesleff I (2003) Epithelial-mesenchymal signalling regulating tooth morphogenesis. J Cell Sci 116:1647–1648PubMedGoogle Scholar
  149. Thesleff I, Sharpe P (1997) Signalling networks regulating dental development. Mech Dev 67:111–123PubMedGoogle Scholar
  150. Thesleff I, Keranen S, Jernvall J (2001) Enamel knots as signaling centers linking tooth morphogenesis and odontoblast differentiation. Adv Dent Res 15:14–18PubMedGoogle Scholar
  151. 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 282:1145–1147PubMedGoogle Scholar
  152. Thonemann B, Schmalz G (2000) Immortalization of bovine dental papilla cells with Simian Virus 40 large T antigen. Arch Oral Biol 45:857–869PubMedGoogle Scholar
  153. Townes PL, Holtfreter J (1955) Directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool 128:53–120Google Scholar
  154. Tucker A, Sharpe P (2004) The cutting-edge of mammalian development; how the embryo makes teeth. Nat Rev Genet 5:499–508PubMedGoogle Scholar
  155. Tucker AS, Matthews KL, Sharpe PT (1998) Transformation of tooth type induced by inhibition of BMP signaling. Science 282:1136–1138PubMedGoogle Scholar
  156. 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 127:4691–4700PubMedGoogle Scholar
  157. 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 130:1049–1057PubMedGoogle Scholar
  158. Tziafas D (1995) Basic mechanisms of cytodifferentiation and dentinogenesis during dental pulp repair. Int J Dev Biol 39:281–290PubMedGoogle Scholar
  159. 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 54:39–43PubMedGoogle Scholar
  160. 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 75:45–58PubMedGoogle Scholar
  161. Verfaillie CM (2002) Adult stem cells: assessing the case for pluripotency. Trends Cell Biol 12:502–508PubMedGoogle Scholar
  162. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297:2256–2259PubMedGoogle Scholar
  163. Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches. Science 287:1427–1430PubMedGoogle Scholar
  164. 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 46:1177–1185PubMedGoogle Scholar
  165. Weissman IL (2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell 100:157–168PubMedGoogle Scholar
  166. Wilson HV (1907) On some phenomena of coalescence and regeneration in sponges. J Exp Zool 5:245–258Google Scholar
  167. 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 8:127–139PubMedGoogle Scholar
  168. 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):530–540PubMedGoogle Scholar
  169. 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 133:1359–1366PubMedGoogle Scholar
  170. 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 327:301–311PubMedGoogle Scholar
  171. 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 26:303–307PubMedGoogle Scholar
  172. 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 81:695–700PubMedCrossRefGoogle Scholar
  173. Yu J, McMahon AP, Valerius MT (2004) Recent genetic studies of mouse kidney development. Curr Opin Genet Dev 14:550–557PubMedGoogle Scholar
  174. 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 99:465–474Google Scholar
  175. Zander HA (1939) Reaction of the pulp to calcium hydroxide. J Dent Res 18:373Google Scholar
  176. 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 228:651–663PubMedGoogle Scholar
  177. 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 12:2813–2823PubMedGoogle Scholar
  178. Zhou P, Byrne C, Jacobs J, Fuchs E (1995) Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev 9:700–713PubMedGoogle Scholar
  179. Zussman WV (1966) Osteogenic activity of odontoblasts in transplanted tooth pulps. J Dent Res 45:144–151PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Craniofacial Development, Dental Institute, Floor 27, Guy’s HospitalKings College LondonLondonUK

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