Advertisement

Dental Pulp Stem Cells: What’s New?

  • Agnieszka Arthur
  • Songtao Shi
  • Stan GronthosEmail author
Chapter
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

Since the discovery of dental pulp stem cells at the beginning of this century, there has been a rapid escalation of published reports describing the different stem/progenitor cells types derived from the oral cavity, the development of novel carrier biomaterials/scaffolds and bioengineering strategies for endodontic regenerative medicine. This chapter will discuss the most current developments utilizing dental pulp stem cells in regenerative dentistry, often employing multidisciplinary approaches. These encompass an understanding of the microenvironment of oral tissues, and highlight the differences between the types of tissues within the oral cavity. Identifying the appropriate bioactive molecules, such as growth factors, transcription factors, signalling molecules and enzymes has also been essential for the regenerative process. Furthermore, the mode of delivery of the dental pulp stem cells has been shown to be dependent on the structure and location of the damaged tissue being targeted. As such, a number of biomaterial used to generate injectable or solid scaffolds have been critically evaluated. The surface structure, extracellular matrix composition of the scaffolds used to deliver the cells, the biodegradability, porosity and release of specific bioactive molecules essential for the survival and maintenance of the dental pulp stem cells have been described. A number of proof-of-principle studies have focused on the efficacy, toxicity, proliferative, adhesive, migratory and differentiation capabilities of dental pulp stem cells within these scaffolds with in vitro, explant and in vivo regenerative experiments. Collectively these findings suggest that the bioengineering and delivery of tissue appropriate biomaterial, bioactive molecules and dental pulp stem cells for the repair or regeneration of the dentin-pulp complex is promising and progressing rapidly.

Keywords

Root Canal Dental Pulp Mineral Trioxide Aggregate Pulp Tissue Dental Pulp Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Lumsden AG. Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development. 1988;103(Suppl):155–69.PubMedGoogle Scholar
  2. 2.
    Buchaille R, Couble ML, Magloire H, Bleicher F. A substractive PCR-based cDNA library from human odontoblast cells: identification of novel genes expressed in tooth forming cells. Matrix Biol. 2000;19:421–30.PubMedCrossRefGoogle Scholar
  3. 3.
    Peters H, Balling R. Teeth. Where and how to make them. Trends Genet. 1999;15:59–65.PubMedCrossRefGoogle Scholar
  4. 4.
    Thesleff I, Aberg T. Molecular regulation of tooth development. Bone. 1999;25:123–5.PubMedCrossRefGoogle Scholar
  5. 5.
    Tucker A, Sharpe P. The cutting-edge of mammalian development; how the embryo makes teeth. Nat Rev Genet. 2004;5:499–508.PubMedCrossRefGoogle Scholar
  6. 6.
    Baume LJ. The biology of pulp and dentine. A historic, terminologic-taxonomic, histologic-biochemical, embryonic and clinical survey. Monogr Oral Sci. 1980;8:1–220.PubMedCrossRefGoogle Scholar
  7. 7.
    Butler WT, Ritchie HH, Bronckers AL. Extracellular matrix proteins of dentine. Ciba Found Symp. 1997;205:107–15. discussion 15–7PubMedGoogle Scholar
  8. 8.
    Bartold PM, Shi S, Gronthos S. Stem cells and periodontal regeneration. Periodontology. 2006;40:164–72.CrossRefGoogle Scholar
  9. 9.
    Schuurs AH, Gruythuysen RJ, Wesselink PR. Pulp capping with adhesive resin-based composite vs calcium hydroxide: a review. Endod Dent Traumatol. 2000;16:240–50.PubMedCrossRefGoogle Scholar
  10. 10.
    Pang YW, Feng J, Daltoe F, Fatscher R, Gentleman E, Gentleman MM, et al. Perivascular stem cells at the tip of mouse incisors regulate tissue regeneration. J Am Soc Bone Miner Res. 2016;31:514–23.CrossRefGoogle Scholar
  11. 11.
    Arthur A, Koblar S, Shi S, Gronthos S. Eph/ephrinB mediate dental pulp stem cell mobilization and function. J Dent Res. 2009;88:829–34.PubMedCrossRefGoogle Scholar
  12. 12.
    Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A. 2000;97:13625–30.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    El-Denshary ES, Rashed LA, Elhussiny M. Mesenchymal stromal cells versus betamethasone can dampen disease activity in the collagen arthritis mouse model. Clin Exp Med. 2014;14:285–95.PubMedCrossRefGoogle Scholar
  14. 14.
    Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res. 2003;18:696–704.PubMedCrossRefGoogle Scholar
  15. 15.
    Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A. 2003;100:5807–12.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Gronthos S, Zannettino AC, Hay SJ, Shi S, Graves SE, Kortesidis A, et al. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci. 2003;116:1827–35.PubMedCrossRefGoogle Scholar
  17. 17.
    Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, et al. Stem cell properties of human dental pulp stem cells. J Dent Res. 2002;81:531–5.PubMedCrossRefGoogle Scholar
  18. 18.
    Batouli S, Miura M, Brahim J, Tsutsui TW, Fisher LW, Gronthos S, et al. Comparison of stem-cell-mediated osteogenesis and dentinogenesis. J Dent Res. 2003;82:976–81.PubMedCrossRefGoogle Scholar
  19. 19.
    Zhao H, Feng J, Seidel K, Shi S, Klein O, Sharpe P, et al. Secretion of shh by a neurovascular bundle niche supports mesenchymal stem cell homeostasis in the adult mouse incisor. Cell Stem Cell. 2014;14:160–73.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Kaukua N, Shahidi MK, Konstantinidou C, Dyachuk V, Kaucka M, Furlan A, et al. Glial origin of mesenchymal stem cells in a tooth model system. Nature. 2014;513:551–4.PubMedCrossRefGoogle Scholar
  21. 21.
    Abe S, Yamaguchi S, Watanabe A, Hamada K, Amagasa T. Hard tissue regeneration capacity of apical pulp derived cells (APDCs) from human tooth with immature apex. Biochem Biophys Res Commun. 2008;371:90–3.PubMedCrossRefGoogle Scholar
  22. 22.
    Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, et al. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod. 2008;34:166–71.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S. The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res. 2005;8:191–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Menicanin D, Hynes K, Han J, Gronthos S, Bartold PM. Cementum and periodontal ligament regeneration. Adv Exp Med Biol. 2015;881:207–36.PubMedCrossRefGoogle Scholar
  25. 25.
    Yamaza T, Kentaro A, Chen C, Liu Y, Shi Y, Gronthos S, et al. Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell ResTher. 2010;1:5.Google Scholar
  26. 26.
    Tang R, Ding G. Swine dental pulp stem cells inhibit T-cell proliferation. Transplant Proc. 2011;43:3955–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Tomic S, Djokic J, Vasilijic S, Vucevic D, Todorovic V, Supic G, et al. Immunomodulatory properties of mesenchymal stem cells derived from dental pulp and dental follicle are susceptible to activation by toll-like receptor agonists. Stem Cells Dev. 2011;20:695–708.PubMedCrossRefGoogle Scholar
  28. 28.
    Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol. 2009;219:667–76.PubMedCrossRefGoogle Scholar
  29. 29.
    Eubanks EJ, Tarle SA, Kaigler D. Tooth storage, dental pulp stem cell isolation, and clinical scale expansion without animal serum. J Endod. 2014;40:652–7.PubMedCrossRefGoogle Scholar
  30. 30.
    Kim BC, Bae H, Kwon IK, Lee EJ, Park JH, Khademhosseini A, et al. Osteoblastic/cementoblastic and neural differentiation of dental stem cells and their applications to tissue engineering and regenerative medicine. Tissue Eng Part B Rev. 2012;18:235–44.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Tatullo M, Marrelli M, Shakesheff KM, White LJ. Dental pulp stem cells: function, isolation and applications in regenerative medicine. J Tissue Eng Regen Med. 2015;9:1205–16.PubMedCrossRefGoogle Scholar
  32. 32.
    Young CS, Terada S, Vacanti JP, Honda M, Bartlett JD, Yelick PC. Tissue engineering of complex tooth structures on biodegradable polymer scaffolds. J Dent Res. 2002;81:695–700.PubMedCrossRefGoogle Scholar
  33. 33.
    Ikeda E, Morita R, Nakao K, Ishida K, Nakamura T, Takano-Yamamoto T, et al. Fully functional bioengineered tooth replacement as an organ replacement therapy. Proc Natl Acad Sci U S A. 2009;106:13475–80.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Xiao L, Tsutsui T. Three-dimensional epithelial and mesenchymal cell co-cultures form early tooth epithelium invagination-like structures: expression patterns of relevant molecules. J Cell Biochem. 2012;113:1875–85.PubMedCrossRefGoogle Scholar
  35. 35.
    Xiao L, Kumazawa Y, Okamura H. Cell death, cavitation and spontaneous multi-differentiation of dental pulp stem cells-derived spheroids in vitro: a journey to survival and organogenesis. Biol Cell. 2014;106:405–19.PubMedCrossRefGoogle Scholar
  36. 36.
    Ortiz M, Rosales-Ibanez R, Pozos-Guillen A, De Bien C, ToyeD FH, et al. DPSC colonization of functionalized 3D textiles. J Biomed Mater Res B Appl Biomater. 2016; doi: 10.1002/jbm.b.33609.PubMedGoogle Scholar
  37. 37.
    Lobo SE, Glickman R, da Silva WN, Arinzeh TL, Kerkis I. Response of stem cells from different origins to biphasic calcium phosphate bioceramics. Cell Tissue Res. 2015;361:477–95.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Kolind K, Kraft D, Boggild T, Duch M, Lovmand J, Pedersen FS, et al. Control of proliferation and osteogenic differentiation of human dental-pulp-derived stem cells by distinct surface structures. Acta Biomater. 2014;10:641–50.PubMedCrossRefGoogle Scholar
  39. 39.
    Collart-Dutilleul PY, Panayotov I, Secret E, Cunin F, Gergely C, Cuisinier F, et al. Initial stem cell adhesion on porous silicon surface: molecular architecture of actin cytoskeleton and filopodial growth. Nanoscale Res Lett. 2014;9:564.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Collart-Dutilleul PY, Secret E, Panayotov I, Deville de Periere D, Martin-Palma RJ, Torres-Costa V, et al. Adhesion and proliferation of human mesenchymal stem cells from dental pulp on porous silicon scaffolds. ACS Appl Mater Interfaces. 2014;6:1719–28.PubMedCrossRefGoogle Scholar
  41. 41.
    Marrelli M, Falisi G, Apicella A, Apicella D, Amantea M, Cielo A, et al. Behaviour of dental pulp stem cells on different types of innovative mesoporous and nanoporous silicon scaffolds with different functionalizations of the surfaces. J Biol Regul Homeost Agents. 2015;29:991–7.PubMedGoogle Scholar
  42. 42.
    Demarco FF, Casagrande L, Zhang Z, Dong Z, Tarquinio SB, Zeitlin BD, et al. Effects of morphogen and scaffold porogen on the differentiation of dental pulp stem cells. J Endod. 2010;36:1805–11.PubMedCrossRefGoogle Scholar
  43. 43.
    Conde CM, Demarco FF, Casagrande L, Alcazar JC, Nor JE, Tarquinio SB. Influence of poly-l-lactic acid scaffold’s pore size on the proliferation and differentiation of dental pulp stem cells. Braz Dent J. 2015;26:93–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Guan Z, Shi S, Samruajbenjakun B, Kamolmatyakul S. Fabrication, characterization and cell cultures on a novel chitosan scaffold. Biomed Mater Eng. 2015;25:121–35.PubMedGoogle Scholar
  45. 45.
    Kanafi MM, Ramesh A, Gupta PK, Bhonde RR. Dental pulp stem cells immobilized in alginate microspheres for applications in bone tissue engineering. Int Endod J. 2014;47:687–97.PubMedCrossRefGoogle Scholar
  46. 46.
    Rosa V, Xie H, Dubey N, Madanagopal TT, Rajan SS, Morin JL, et al. Graphene oxide-based substrate: physical and surface characterization, cytocompatibility and differentiation potential of dental pulp stem cells. Dent Mater. 2016;32(8):1019–25.PubMedCrossRefGoogle Scholar
  47. 47.
    Paduano F, Marrelli M, White LJ, Shakesheff KM, Tatullo M. Odontogenic differentiation of human dental pulp stem cells on hydrogel scaffolds derived from decellularized bone extracellular matrix and collagen type I. PLoS One. 2016;11:e0148225.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Liu G, Xu G, Gao Z, Liu Z, Xu J, Wang J, et al. Demineralized dentin matrix induces odontoblastic differentiation of dental pulp stem cells. Cells Tissues Organs. 2016;201:65–76.PubMedCrossRefGoogle Scholar
  49. 49.
    Qu T, Jing J, Jiang Y, Taylor RJ, Feng JQ, Geiger B, et al. Magnesium-containing nanostructured hybrid scaffolds for enhanced dentin regeneration. Tissue Eng Part A. 2014;20:2422–33.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Bakopoulou A, Papachristou E, Bousnaki M, Hadjichristou C, Kontonasaki E, Theocharidou A, et al. Human treated dentin matrices combined with Zn-doped, Mg-based bioceramic scaffolds and human dental pulp stem cells towards targeted dentin regeneration. Dent Mater. 2016;32(8):e159–75.PubMedCrossRefGoogle Scholar
  51. 51.
    Chou MY, Kao CT, Hung CJ, Huang TH, Huang SC, Shie MY, et al. Role of the P38 pathway in calcium silicate cement-induced cell viability and angiogenesis-related proteins of human dental pulp cell in vitro. J Endod. 2014;40:818–24.PubMedCrossRefGoogle Scholar
  52. 52.
    Chen YW, Ho CC, Huang TH, Hsu TT, Shie MY. The ionic products from mineral trioxide aggregate-induced odontogenic differentiation of dental pulp cells via activation of the Wnt/beta-catenin signaling pathway. J Endod. 2016;42:1062–9.PubMedCrossRefGoogle Scholar
  53. 53.
    Wang S, Hu Q, Gao X, Dong Y. Characteristics and effects on dental pulp cells of a polycaprolactone/submicron bioactive glass composite scaffold. J Endod. 2016;42:1070–5.PubMedCrossRefGoogle Scholar
  54. 54.
    Galler KM, Widbiller M, Buchalla W, Eidt A, Hiller KA, Hoffer PC, et al. EDTA conditioning of dentine promotes adhesion, migration and differentiation of dental pulp stem cells. Int Endod J. 2016;49:581–90.PubMedCrossRefGoogle Scholar
  55. 55.
    Galler KM, D’Souza RN, Federlin M, Cavender AC, Hartgerink JD, Hecker S, et al. Dentin conditioning codetermines cell fate in regenerative endodontics. J Endod. 2011;37:1536–41.PubMedCrossRefGoogle Scholar
  56. 56.
    Cavalcanti BN, Zeitlin BD, Nor JE. A hydrogel scaffold that maintains viability and supports differentiation of dental pulp stem cells. Dent Mater. 2013;29:97–102.PubMedCrossRefGoogle Scholar
  57. 57.
    Diniz IM, Chen C, Xu X, Ansari S, Zadeh HH, Marques MM, et al. Pluronic F-127 hydrogel as a promising scaffold for encapsulation of dental-derived mesenchymal stem cells. J Mater Sci Mater Med. 2015;26:153.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Dissanayaka WL, Hargreaves KM, Jin L, Samaranayake LP, Zhang C. The interplay of dental pulp stem cells and endothelial cells in an injectable peptide hydrogel on angiogenesis and pulp regeneration in vivo. Tissue Eng Part A. 2015;21:550–63.PubMedCrossRefGoogle Scholar
  59. 59.
    Dissanayaka WL, Zhu L, Hargreaves KM, Jin L, Zhang C. Scaffold-free prevascularized microtissue spheroids for pulp regeneration. J Dent Res. 2014;93:1296–303.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Dissanayaka WL, Zhu L, Hargreaves KM, Jin L, Zhang C. In vitro analysis of scaffold-free prevascularized microtissue spheroids containing human dental pulp cells and endothelial cells. J Endod. 2015;41:663–70.PubMedCrossRefGoogle Scholar
  61. 61.
    Ferroni L, Gardin C, Sivolella S, Brunello G, Berengo M, Piattelli A, et al. A hyaluronan-based scaffold for the in vitro construction of dental pulp-like tissue. Int J Mol Sci. 2015;16:4666–81.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Rosa V, Zhang Z, Grande RH, Nor JE. Dental pulp tissue engineering in full-length human root canals. J Dent Res. 2013;92:970–5.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Jones TD, Kefi A, Sun S, Cho M, Alapati SB. An optimized injectable hydrogel scaffold supports human dental pulp stem cell viability and spreading. Adv Med. 2016;2016:7363579.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Kuang R, Zhang Z, Jin X, Hu J, Shi S, Ni L, et al. Nanofibrous spongy microspheres for the delivery of hypoxia-primed human dental pulp stem cells to regenerate vascularized dental pulp. Acta Biomater. 2016;33:225–34.PubMedCrossRefGoogle Scholar
  65. 65.
    Jia W, Zhao Y, Yang J, Wang W, Wang X, Ling L, et al. Simvastatin promotes dental pulp stem cell-induced coronal pulp regeneration in pulpotomized teeth. J Endod. 2016;42:1049–54.PubMedCrossRefGoogle Scholar
  66. 66.
    Ruparel NB, Teixeira FB, Ferraz CC, Diogenes A. Direct effect of intracanal medicaments on survival of stem cells of the apical papilla. J Endod. 2012;38:1372–5.PubMedCrossRefGoogle Scholar
  67. 67.
    Chuensombat S, Khemaleelakul S, Chattipakorn S, Srisuwan T. Cytotoxic effects and antibacterial efficacy of a 3-antibiotic combination: an in vitro study. J Endod. 2013;39:813–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Yadlapati M, Souza LC, Dorn S, Garlet GP, Letra A, Silva RM. Deleterious effect of triple antibiotic paste on human periodontal ligament fibroblasts. Int Endod J. 2014;47:769–75.PubMedCrossRefGoogle Scholar
  69. 69.
    Alghilan MA, Windsor LJ, Palasuk J, Yassen GH. Attachment and proliferation of dental pulp stem cells on dentine treated with different regenerative endodontic protocols. Int Endod J. 2016; doi: 10.1111/iej.12669.PubMedGoogle Scholar
  70. 70.
    Martin DE, De Almeida JF, Henry MA, Khaing ZZ, Schmidt CE, Teixeira FB, et al. Concentration-dependent effect of sodium hypochlorite on stem cells of apical papilla survival and differentiation. J Endod. 2014;40:51–5.PubMedCrossRefGoogle Scholar
  71. 71.
    Trevino EG, Patwardhan AN, Henry MA, Perry G, Dybdal-Hargreaves N, Hargreaves KM, et al. Effect of irrigants on the survival of human stem cells of the apical papilla in a platelet-rich plasma scaffold in human root tips. J Endod. 2011;37:1109–15.PubMedCrossRefGoogle Scholar
  72. 72.
    Kamocki K, Nor JE, Bottino MC. Dental pulp stem cell responses to novel antibiotic-containing scaffolds for regenerative endodontics. Int Endod J. 2015;48:1147–56.PubMedCrossRefGoogle Scholar
  73. 73.
    Dissanayaka WL, Zhan X, Zhang C, Hargreaves KM, Jin L, Tong EH. Coculture of dental pulp stem cells with endothelial cells enhances osteo−/odontogenic and angiogenic potential in vitro. J Endod. 2012;38:454–63.PubMedCrossRefGoogle Scholar
  74. 74.
    Chen YJ, Zhao YH, Zhao YJ, Liu NX, Lv X, Li Q, et al. Potential dental pulp revascularization and odonto-/osteogenic capacity of a novel transplant combined with dental pulp stem cells and platelet-rich fibrin. Cell Tissue Res. 2015;361:439–55.PubMedCrossRefGoogle Scholar
  75. 75.
    Janebodin K, Zeng Y, Buranaphatthana W, Ieronimakis N, Reyes M. VEGFR2-dependent angiogenic capacity of pericyte-like dental pulp stem cells. J Dent Res. 2013;92:524–31.PubMedCrossRefGoogle Scholar
  76. 76.
    Zhang Z, Nor F, Oh M, Cucco C, Shi S, Nor JE. Wnt/beta-catenin signaling determines the vasculogenic fate of postnatal mesenchymal stem cells. Stem Cells. 2016;34:1576–87.PubMedCrossRefGoogle Scholar
  77. 77.
    Yang JW, Zhang YF, Wan CY, Sun ZY, Nie S, Jian SJ, et al. Autophagy in SDF-1alpha-mediated DPSC migration and pulp regeneration. Biomaterials. 2015;44:11–23.PubMedCrossRefGoogle Scholar
  78. 78.
    Arthur A, Shi S, Zannettino AC, Fujii N, Gronthos S, Koblar SA. Implanted adult human dental pulp stem cells induce endogenous axon guidance. Stem Cells. 2009;27:2229–37.PubMedCrossRefGoogle Scholar
  79. 79.
    Psaltis PJ, Paton S, See F, Arthur A, Martin S, Itescu S, et al. Enrichment for STRO-1 expression enhances the cardiovascular paracrine activity of human bone marrow-derived mesenchymal cell populations. J Cell Physiol. 2010;223:530–40.PubMedGoogle Scholar
  80. 80.
    Zhang W, Zhang Z, Chen S, Macri L, Kohn J, Yelick PC. Mandibular jaw bone regeneration using human dental cell-seeded tyrosine-derived polycarbonate scaffolds. Tissue Eng Part A. 2016;22(13-14):985–93.PubMedCrossRefGoogle Scholar
  81. 81.
    Lei M, Li K, Li B, Gao LN, Chen FM, Jin Y. Mesenchymal stem cell characteristics of dental pulp and periodontal ligament stem cells after in vivo transplantation. Biomaterials. 2014;35:6332–43.PubMedCrossRefGoogle Scholar
  82. 82.
    Iohara K, Murakami M, Nakata K, Nakashima M. Age-dependent decline in dental pulp regeneration after pulpectomy in dogs. Exp Gerontol. 2014;52:39–45.PubMedCrossRefGoogle Scholar
  83. 83.
    Murakami M, Horibe H, Iohara K, Hayashi Y, Osako Y, Takei Y, et al. The use of granulocyte-colony stimulating factor induced mobilization for isolation of dental pulp stem cells with high regenerative potential. Biomaterials. 2013;34:9036–47.PubMedCrossRefGoogle Scholar
  84. 84.
    Iohara K, Murakami M, Takeuchi N, Osako Y, Ito M, Ishizaka R, et al. A novel combinatorial therapy with pulp stem cells and granulocyte colony-stimulating factor for total pulp regeneration. Stem Cells Transl Med. 2013;2:521–33.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Volponi AA, Gentleman E, Fatscher R, Pang YW, Gentleman MM, Sharpe PT. Composition of mineral produced by dental mesenchymal stem cells. J Dent Res. 2015;94:1568–74.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Chun SY, Lee HJ, Choi YA, Kim KM, Baek SH, Park HS, et al. Analysis of the soluble human tooth proteome and its ability to induce dentin/tooth regeneration. Tissue Eng Part A. 2011;17:181–91.PubMedCrossRefGoogle Scholar
  87. 87.
    Lee CH, Hajibandeh J, Suzuki T, Fan A, Shang P, Mao JJ. Three-dimensional printed multiphase scaffolds for regeneration of periodontium complex. Tissue Eng Part A. 2014;20:1342–51.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Qu T, Jing J, Ren Y, Ma C, Feng JQ, Yu Q, et al. Complete pulpodentin complex regeneration by modulating the stiffness of biomimetic matrix. Acta Biomater. 2015;16:60–70.PubMedCrossRefGoogle Scholar
  89. 89.
    Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C, et al. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One. 2006;1:e79.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Wang S, Liu Y, Fang D, Shi S. The miniature pig: a useful large animal model for dental and orofacial research. Oral Dis. 2007;13:530–7.PubMedCrossRefGoogle Scholar
  91. 91.
    Wei F, Song T, Ding G, Xu J, Liu Y, Liu D, et al. Functional tooth restoration by allogeneic mesenchymal stem cell-based bio-root regeneration in swine. Stem Cells Dev. 2013;22:1752–62.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Gao ZH, Hu L, Liu GL, Wei FL, Liu Y, Liu ZH, et al. Bio-root and implant-based restoration as a tooth replacement alternative. J Dent Res. 2016;95:642–9.PubMedCrossRefGoogle Scholar
  93. 93.
    Luo X, Yang B, Sheng L, Chen J, Li H, Xie L, et al. CAD based design sensitivity analysis and shape optimization of scaffolds for bio-root regeneration in swine. Biomaterials. 2015;57:59–72.PubMedCrossRefGoogle Scholar
  94. 94.
    Tassin M, Bonte E, Loison-Robert LS, Nassif A, Berbar T, Le Goff S, et al. Effects of high-temperature-pressure polymerized resin-infiltrated ceramic networks on oral stem cells. PLoS One. 2016;11:e0155450.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Chen Y, Zheng YL, Qiu DB, Sun YP, Kuang SJ, Xu Y, et al. An extracellular matrix culture system for induced pluripotent stem cells derived from human dental pulp cells. Eur Rev Med Pharmacol Sci. 2015;19:4035–46.PubMedGoogle Scholar
  96. 96.
    Ishiy FA, Fanganiello RD, Griesi-Oliveira K, Suzuki AM, Kobayashi GS, Morales AG, et al. Improvement of in vitro osteogenic potential through differentiation of induced pluripotent stem cells from human exfoliated dental tissue towards mesenchymal-like stem cells. Stem Cells Int. 2015;2015:249098.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Takeda-Kawaguchi T, Sugiyama K, Chikusa S, Iida K, Aoki H, Tamaoki N, et al. Derivation of iPSCs after culture of human dental pulp cells under defined conditions. PLoS One. 2014;9:e115392.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Tomokiyo A, Hynes K, Ng J, Menicanin D, Camp E, Arthur A, et al. Generation of neural crest-like cells from human periodontal ligament cell-derived induced pluripotent stem cells. J Cell Physiol. 2016;232(2):402–16.PubMedCrossRefGoogle Scholar
  99. 99.
    Okawa H, Kayashima H, Sasaki J, Miura J, Kamano Y, Kosaka Y, et al. Scaffold-free fabrication of osteoinductive cellular constructs using mouse gingiva-derived induced pluripotent stem cells. Stem Cells Int. 2016;2016:6240794.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Wu Q, Yang B, Hu K, Cao C, Man Y, Wang P. Deriving osteogenic cells from induced pluripotent stem cells for bone tissue engineering. Tissue Eng Part B Rev. 2017;23(1):1–8.PubMedCrossRefGoogle Scholar
  101. 101.
    Hynes K, Menicanin D, Gronthos S, Bartold MP. Differentiation of iPSC to mesenchymal stem-like cells and their characterization. Methods Mol Biol. 2016;1357:353–74.PubMedCrossRefGoogle Scholar
  102. 102.
    Ng J, Hynes K, White G, Sivanathan KN, Vandyke K, Bartold PM, et al. Immunomodulatory properties of induced pluripotent stem cell-derived mesenchymal cells. J Cell Biochem. 2016;117(12):2844.PubMedCrossRefGoogle Scholar
  103. 103.
    Hynes K, Menichanin D, Bright R, Ivanovski S, Hutmacher DW, Gronthos S, et al. Induced pluripotent stem cells: a new frontier for stem cells in dentistry. J Dent Res. 2015;94:1508–15.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Agnieszka Arthur
    • 1
    • 2
  • Songtao Shi
    • 3
  • Stan Gronthos
    • 1
    • 2
    Email author
  1. 1.Mesenchymal Stem Cell Laboratory, Adelaide Medical School, Faculty of Health and Medical SciencesUniversity of AdelaideAdelaideAustralia
  2. 2.South Australian Health and Medical Research InstituteAdelaideAustralia
  3. 3.Department of Anatomy and Cell BiologyUniversity of Pennsylvania School of Dental MedicinePhiladelphiaUSA

Personalised recommendations