Skip to main content

Advertisement

Log in

Adult Craniofacial Stem Cells: Sources and Relation to the Neural Crest

  • Published:
Stem Cell Reviews and Reports Aims and scope Submit manuscript

Abstract

During the process of development, neural crest cells migrate out from their niche between the newly formed ectoderm and the neural tube. Thereafter, they give rise not only to ectodermal cell types, but also to mesodermal cell types. Cell types with neural crest ancestry consequently comprise a number of specialized varieties, such as ectodermal neurons, melanocytes and Schwann cells, as well as mesodermal osteoblasts, adipocytes and smooth muscle cells. Numerous recent studies suggest that stem cells with a neural crest origin persist into adulthood, especially within the mammalian craniofacial compartment. This review discusses the sources of adult neural crest-derived stem cells (NCSCs) derived from the cranium, as well as their differentiation potential and expression of key stem cell markers. Furthermore, the expression of marker genes associated with embryonic stem cells and the issue of multi- versus pluripotency of adult NCSCs is reviewed. Stringent tests are proposed, which, if performed, are anticipated to clarify the issue of adult NCSC potency. Finally, current pre-clinical and clinical data are discussed in light of the clinical impact of adult NCSCs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Crane, J. F., & Trainor, P. A. (2006). Neural crest stem and progenitor cells. Annual Review of Cell and Developmental Biology, 22, 267–286.

    Article  PubMed  CAS  Google Scholar 

  2. Teng, L., & Labosky, P. A. (2006). Neural crest stem cells. Advances in Experimental Medicine and Biology, 589, 206–212.

    Article  PubMed  CAS  Google Scholar 

  3. Dupin, E., Calloni, G., Real, C., Goncalves-Trentin, A., & Le Douarin, N. M. (2007). Neural crest progenitors and stem cells. Comptes Rendus Biologies, 330, 521–529.

    Article  PubMed  CAS  Google Scholar 

  4. Shakhova, O., & Sommer, L. (2010). Neural crest-derived stem cells. In F. H. Gage & F. M. Watt (Eds.), StemBook. Cambridge: Harvard Stem Cell Institute.

    Google Scholar 

  5. Santagati, F., & Rijli, F. M. (2003). Cranial neural crest and the building of the vertebrate head. Nature Reviews Neuroscience, 4, 806–818.

    Article  PubMed  CAS  Google Scholar 

  6. Noden, D. M., & Trainor, P. A. (2005). Relations and interactions between cranial mesoderm and neural crest populations. Journal of Anatomy, 207, 575–601.

    Article  PubMed  Google Scholar 

  7. His, W. (1868). Untersuchungen über die erste Anlage des Wirbeltierleibes. Die erste Entwicklung des Hühnchens im Ei. Leipzig: Vogel.

    Book  Google Scholar 

  8. Vickaryous, M. K., & Hall, B. K. (2006). Human cell type diversity, evolution, development, and classification with special reference to cells derived from the neural crest. Biological Reviews of the Cambridge Philosophical Society, 81, 425–455.

    Article  PubMed  Google Scholar 

  9. Slack, J. M. (2008). Origin of stem cells in organogenesis. Science, 322, 1498–1501.

    Article  PubMed  CAS  Google Scholar 

  10. Tachibana, M., Kobayashi, Y., & Matsushima, Y. (2003). Mouse models for four types of Waardenburg syndrome. Pigment Cell Research, 16, 448–454.

    Article  PubMed  CAS  Google Scholar 

  11. Wilkie, A. O., & Morriss-Kay, G. M. (2001). Genetics of craniofacial development and malformation. Nature Reviews Genetics, 2, 458–468.

    Article  PubMed  CAS  Google Scholar 

  12. Ngan, E. S., Garcia-Barcelo, M. M., Yip, B. H., et al. (2011). Hedgehog/Notch-induced premature gliogenesis represents a new disease mechanism for Hirschsprung disease in mice and humans. The Journal of Clinical Investigation, 121, 3467–3478.

    Article  PubMed  CAS  Google Scholar 

  13. Yoshida, S., Shimmura, S., Nagoshi, N., et al. (2006). Isolation of multipotent neural crest-derived stem cells from the adult mouse cornea. Stem Cells, 24, 2714–2722.

    Article  PubMed  CAS  Google Scholar 

  14. Sieber-Blum, M., & Grim, M. (2004). The adult hair follicle: Cradle for pluripotent neural crest stem cells. Birth Defects Research. Part C, Embryo Today, 72, 162–172.

    Article  CAS  Google Scholar 

  15. Sasaki, R., Aoki, S., Yamato, M., et al. (2008). Neurosphere generation from dental pulp of adult rat incisor. European Journal of Neuroscience, 27, 538–548.

    Article  PubMed  Google Scholar 

  16. Nagoshi, N., Shibata, S., Kubota, Y., et al. (2008). Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell, 2, 392–403.

    Article  PubMed  CAS  Google Scholar 

  17. Techawattanawisal, W., Nakahama, K., Komaki, M., Abe, M., Takagi, Y., & Morita, I. (2007). Isolation of multipotent stem cells from adult rat periodontal ligament by neurosphere-forming culture system. Biochemical and Biophysical Research Communications, 357, 917–923.

    Article  PubMed  CAS  Google Scholar 

  18. Widera, D., Grimm, W. D., Moebius, J. M., et al. (2007). Highly efficient neural differentiation of human somatic stem cells, isolated by minimally invasive periodontal surgery. Stem Cells and Development, 16, 447–460.

    Article  PubMed  Google Scholar 

  19. Widera, D., Zander, C., Heidbreder, M., et al. (2009). Adult palatum as a novel source of neural crest-related stem cells. Stem Cells, 27, 1899–1910.

    Article  PubMed  CAS  Google Scholar 

  20. Nagase, T., Matsumoto, D., Nagase, M., et al. (2007). Neurospheres from human adipose tissue transplanted into cultured mouse embryos can contribute to craniofacial morphogenesis: A preliminary report. The Journal of Craniofacial Surgery, 18, 49–53. discussion 60–1.

    Article  PubMed  Google Scholar 

  21. Hauser, S., Widera, D., Qunneis, F., et al. (2011). Isolation of novel multipotent neural crest-derived stem cells from adult human inferior turbinate. Stem Cells and Developement. doi:10.1089/scd.2011.0419.

  22. Pierret, C., Spears, K., Maruniak, J. A., & Kirk, M. D. (2006). Neural crest as the source of adult stem cells. Stem Cells and Development, 15, 286–291.

    Article  PubMed  CAS  Google Scholar 

  23. Sieber-Blum, M., Grim, M., Hu, Y. F., & Szeder, V. (2004). Pluripotent neural crest stem cells in the adult hair follicle. Developmental Dynamics, 231, 258–269.

    Article  PubMed  CAS  Google Scholar 

  24. Murrell, W., Feron, F., Wetzig, A., et al. (2005). Multipotent stem cells from adult olfactory mucosa. Developmental Dynamics, 233, 496–515.

    Article  PubMed  Google Scholar 

  25. Hunt, D. P., Morris, P. N., Sterling, J., et al. (2008). A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells, 26, 163–172.

    Article  PubMed  CAS  Google Scholar 

  26. Marynka-Kalmani, K., Treves, S., Yafee, M., et al. (2010). The lamina propria of adult human oral mucosa harbors a novel stem cell population. Stem Cells, 28, 984–995.

    PubMed  CAS  Google Scholar 

  27. Delorme, B., Nivet, E., Gaillard, J., et al. (2010). The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells and Development, 19, 853–866.

    Article  PubMed  CAS  Google Scholar 

  28. Jakob, M., Hemeda, H., Janeschik, S., et al. (2010). Human nasal mucosa contains tissue-resident immunologically responsive mesenchymal stromal cells. Stem Cells and Development, 19, 635–644.

    Article  PubMed  CAS  Google Scholar 

  29. Arnold, W. H., Becher, S., Dannan, A., et al. (2010). Morphological characterization of periodontium-derived human stem cells. Annals of Anatomy.

  30. Greiner, J., Hauser, S., Widera, D., et al. (2011). Efficient animal-serum free 3D cultivation method for adult human neural crest-derived stem cell therapeutics. European Cells and Materials, in press.

  31. Yu, H., Fang, D., Kumar, S. M., et al. (2006). Isolation of a novel population of multipotent adult stem cells from human hair follicles. American Journal of Pathology, 168, 1879–1888.

    Article  PubMed  CAS  Google Scholar 

  32. Waddington, R. J., Youde, S. J., Lee, C. P., & Sloan, A. J. (2009). Isolation of distinct progenitor stem cell populations from dental pulp. Cells, Tissues, Organs, 189, 268–274.

    Article  PubMed  Google Scholar 

  33. Park, D., Xiang, A. P., Mao, F. F., et al. (2010). Nestin is required for the proper self-renewal of neural stem cells. Stem Cells, 28, 2162–2171.

    Article  PubMed  CAS  Google Scholar 

  34. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics, 21, 70–71.

    Article  PubMed  CAS  Google Scholar 

  35. Lee, H. Y., Kleber, M., Hari, L., et al. (2004). Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science, 303, 1020–1023.

    Article  PubMed  CAS  Google Scholar 

  36. Kleber, M., Lee, H. Y., Wurdak, H., et al. (2005). Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling. The Journal of Cell Biology, 169, 309–320.

    Article  PubMed  CAS  Google Scholar 

  37. Fernandes, K. J., McKenzie, I. A., Mill, P., et al. (2004). A dermal niche for multipotent adult skin-derived precursor cells. Nature Cell Biology, 6, 1082–1093.

    Article  PubMed  CAS  Google Scholar 

  38. Toma, J. G., Akhavan, M., Fernandes, K. J., et al. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nature Cell Biology, 3, 778–784.

    Article  PubMed  CAS  Google Scholar 

  39. Joannides, A., Gaughwin, P., Schwiening, C., et al. (2004). Efficient generation of neural precursors from adult human skin: Astrocytes promote neurogenesis from skin-derived stem cells. Lancet, 364, 172–178.

    Article  PubMed  CAS  Google Scholar 

  40. Sieber-Blum, M., Schnell, L., Grim, M., Hu, Y. F., Schneider, R., & Schwab, M. E. (2006). Characterization of epidermal neural crest stem cell (EPI-NCSC) grafts in the lesioned spinal cord. Molecular and Cellular Neuroscience, 32, 67–81.

    Article  PubMed  CAS  Google Scholar 

  41. Hu, Y. F., Zhang, Z. J., & Sieber-Blum, M. (2006). An epidermal neural crest stem cell (EPI-NCSC) molecular signature. Stem Cells, 24, 2692–2702.

    Article  PubMed  CAS  Google Scholar 

  42. Sieber-Blum, M. Epidermal neural crest stem cells and their use in mouse models of spinal cord injury. Brain Research Bulletin, 83, 189–93.

  43. Sieber-Blum, M., & Hu, Y. (2008). Epidermal neural crest stem cells (EPI-NCSC) and pluripotency. Stem Cell Reviews, 4, 256–260.

    Article  PubMed  Google Scholar 

  44. Clewes, O., Narytnyk, A., Gillinder, K. R., Loughney, A. D., Murdoch, A. P., Sieber-Blum, M. (2011). Human Epidermal Neural Crest Stem Cells (hEPI-NCSC)-characterization and directed differentiation into osteocytes and melanocytes. Stem Cell Reviews.

  45. Kahnberg, K. E., & Thilander, H. (1982). Healing of experimental excisional wounds in the rat palate. (I) histological study of the interphase in wound healing after sharp dissection. International Journal of Oral Surgery, 11, 44–51.

    Article  PubMed  CAS  Google Scholar 

  46. Kahnberg, K. E., & Thilander, H. (1984). Healing of experimental excisional wounds in the rat palate. II. Histological study of electrosurgical wounds. Swedish Dental Journal, 8, 49–56.

    PubMed  CAS  Google Scholar 

  47. Kahnberg, K. E., & Thilander, H. (1987). Healing of experimental excisional wounds in the rat palate. III. Effects of radiation on wound healing. Swedish Dental Journal, 11, 61–70.

    PubMed  CAS  Google Scholar 

  48. Dong, R., Liu, X., Fan, M., Yang, L., Peng, L., & Zhang, L. (2010). Isolation and differentiation of nestin positive cells from rat oral mucosal lamina propria. Differentiation, 79, 9–14.

    Article  PubMed  CAS  Google Scholar 

  49. Davies, L. C., Locke, M., Webb, R. D., et al. (2010). A multipotent neural crest-derived progenitor cell population is resident within the oral mucosa lamina propria. Stem Cells and Development, 19, 819–830.

    Article  PubMed  CAS  Google Scholar 

  50. Seo, B. M., Miura, M., Gronthos, S., et al. (2004). Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet, 364, 149–155.

    Article  PubMed  CAS  Google Scholar 

  51. Coura, G. S., Garcez, R. C., de Aguiar, C. B., Alvarez-Silva, M., Magini, R. S., & Trentin, A. G. (2008). Human periodontal ligament: A niche of neural crest stem cells. Journal of Periodontal Research, 43, 531–536.

    Article  PubMed  CAS  Google Scholar 

  52. Huang, C. Y., Pelaez, D., Dominguez-Bendala, J., Garcia-Godoy, F., & Cheung, H. S. (2009). Plasticity of stem cells derived from adult periodontal ligament. Regenerative Medicine, 4, 809–821.

    Article  PubMed  Google Scholar 

  53. Kawanabe, N., Murata, S., Murakami, K., et al. (2010). Isolation of multipotent stem cells in human periodontal ligament using stage-specific embryonic antigen-4. Differentiation, 79, 74–83.

    Article  PubMed  CAS  Google Scholar 

  54. Gronthos, S., Mankani, M., Brahim, J., Robey, P. G., & Shi, S. (2000). Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proceedings of the National Academy of Sciences of the United States of America, 97, 13625–13630.

    Article  PubMed  CAS  Google Scholar 

  55. Shi, S., Robey, P. G., & Gronthos, S. (2001). Comparison of human dental pulp and bone marrow stromal stem cells by cDNA microarray analysis. Bone, 29, 532–539.

    Article  PubMed  CAS  Google Scholar 

  56. Miura, M., Gronthos, S., Zhao, M., et al. (2003). SHED: Stem cells from human exfoliated deciduous teeth. Proceedings of the National Academy of Sciences of the United States of America, 100, 5807–5812.

    Article  PubMed  CAS  Google Scholar 

  57. Sloan, A. J., & Waddington, R. J. (2009). Dental pulp stem cells: What, where, how? International Journal of Paediatric Dentistry, 19, 61–70.

    Article  PubMed  Google Scholar 

  58. Lumsden, A. (1988). Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development, 103, 155–170.

    PubMed  Google Scholar 

  59. Chai, Y., Jiang, X., Ito, Y., et al. (2000). Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development, 127, 1671–1679.

    PubMed  CAS  Google Scholar 

  60. Stevens, A., Zuliani, T., Olejnik, C., et al. (2008). Human dental pulp stem cells differentiate into neural crest-derived melanocytes and have label-retaining and sphere-forming abilities. Stem Cells and Development, 17, 1175–1184.

    Article  PubMed  Google Scholar 

  61. Arthur, A., Rychkov, G., Shi, S., Koblar, S. A., & Gronthos, S. (2008). Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells, 26, 1787–1795.

    Article  PubMed  CAS  Google Scholar 

  62. Govindasamy, V., Abdullah, A. N., Ronald, V. S., et al. (2010). Inherent differential propensity of dental pulp stem cells derived from human deciduous and permanent teeth. Journal of Endodontics, 36, 1504–1515.

    Article  PubMed  Google Scholar 

  63. Yalvac, M. E., Ramazanoglu, M., Rizvanov, A. A., et al. (2010). Isolation and characterization of stem cells derived from human third molar tooth germs of young adults: Implications in neo-vascularization, osteo-, adipo- and neurogenesis. The Pharmacogenomics Journal, 10, 105–113.

    Article  PubMed  CAS  Google Scholar 

  64. Franssen, E. H., de Bree, F. M., & Verhaagen, J. (2007). Olfactory ensheathing glia: Their contribution to primary olfactory nervous system regeneration and their regenerative potential following transplantation into the injured spinal cord. Brain Research Reviews, 56, 236–258.

    Article  PubMed  Google Scholar 

  65. Kocsis, J. D., Lankford, K. L., Sasaki, M., & Radtke, C. (2009). Unique in vivo properties of olfactory ensheathing cells that may contribute to neural repair and protection following spinal cord injury. Neuroscience Letters, 456, 137–142.

    Article  PubMed  CAS  Google Scholar 

  66. Lindsay, S. L., Riddell, J. S., Barnett, S. C. Olfactory mucosa for transplant-mediated repair: A complex tissue for a complex injury? Glia, 58, 125–34.

  67. Barraud, P., Seferiadis, A. A., Tyson, L. D., et al. Neural crest origin of olfactory ensheathing glia. Proceedings of the National Academy of Sciences of the United States of America, 107, 21040–5.

  68. Tome, M., Lindsay, S. L., Riddell, J. S., & Barnett, S. C. (2009). Identification of nonepithelial multipotent cells in the embryonic olfactory mucosa. Stem Cells, 27, 2196–2208.

    Article  PubMed  CAS  Google Scholar 

  69. Savchenko, E. A., Andreeva, N. A., Dmitrieva, T. B., Viktorov, I. V., & Chekhonin, V. P. (2005). Culturing of specialized glial cells (olfactory ensheathing cells) of human olfactory epithelium. Bulletin of Experimental Biology and Medicine, 139, 510–513.

    Article  PubMed  CAS  Google Scholar 

  70. Pellitteri, R., Spatuzza, M., Stanzani, S., & Zaccheo, D. (2010). Biomarkers expression in rat olfactory ensheathing cells. Frontiers in Bioscience (Scholar Edition), 2, 289–298.

    Article  Google Scholar 

  71. Viktorov, I. V., Savchenko, E. A., & Chekhonin, V. P. (2007). Spontaneous neural differentiation of stem cells in culture of human olfactory epithelium. Bulletin of Experimental Biology and Medicine, 144, 596–601.

    Article  PubMed  CAS  Google Scholar 

  72. Sorokin, S. (1988). The respiratory system. In L. Weiss (Ed.), A textbook of histology (pp. 751–814). Baltimore: Urban & Schwarzenberg.

    Google Scholar 

  73. Nakashima, T., Kimmelman, C. P., & Snow, J. B., Jr. (1984). Structure of human fetal and adult olfactory neuroepithelium. Archives of Otolaryngology, 110, 641–646.

    Article  PubMed  CAS  Google Scholar 

  74. Paik, S. I., Lehman, M. N., Seiden, A. M., Duncan, H. J., & Smith, D. V. (1992). Human olfactory biopsy. The influence of age and receptor distribution. Archives of Otolaryngology – Head & Neck Surgery, 118, 731–738.

    Article  CAS  Google Scholar 

  75. Feron, F., Perry, C., McGrath, J. J., & Mackay-Sim, A. (1998). New techniques for biopsy and culture of human olfactory epithelial neurons. Archives of Otolaryngology – Head & Neck Surgery, 124, 861–866.

    CAS  Google Scholar 

  76. Mansour, H. A. (2011). Repair of nasal septal perforation using inferior turbinate graft. Journal of Laryngology & Otology, 1–5.

  77. Gage, P. J., Rhoades, W., Prucka, S. K., & Hjalt, T. (2005). Fate maps of neural crest and mesoderm in the mammalian eye. Investigative Ophthalmology & Visual Science, 46, 4200–4208.

    Article  Google Scholar 

  78. Brandl, C., Florian, C., Driemel, O., Weber, B. H., & Morsczeck, C. (2009). Identification of neural crest-derived stem cell-like cells from the corneal limbus of juvenile mice. Experimental Eye Research, 89, 209–217.

    Article  PubMed  CAS  Google Scholar 

  79. Harun, M. H., Sepian, S. N., Chua, K. H., et al. (2011). Human forniceal region is the stem cell-rich zone of the conjunctival epithelium. Human Cell.

  80. Zhou, S. Y., Zhang, C., Baradaran, E., & Chuck, R. S. (2010). Human corneal basal epithelial cells express an embryonic stem cell marker OCT4. Current Eye Research, 35, 978–985.

    Article  PubMed  CAS  Google Scholar 

  81. Chang, C. Y., McGhee, J. J., Green, C. R., Sherwin, T. (2011). Comparison of stem cell properties in cell populations isolated from human central and limbal corneal epithelium. Cornea.

  82. Vroemen, M., & Weidner, N. (2003). Purification of Schwann cells by selection of p75 low affinity nerve growth factor receptor expressing cells from adult peripheral nerve. Journal of Neuroscience Methods, 124, 135–143.

    Article  PubMed  CAS  Google Scholar 

  83. Morrison, S. J., White, P. M., Zock, C., & Anderson, D. J. (1999). Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell, 96, 737–749.

    Article  PubMed  CAS  Google Scholar 

  84. Li, H. Y., Say, E. H., & Zhou, X. F. (2007). Isolation and characterization of neural crest progenitors from adult dorsal root ganglia. Stem Cells, 25, 2053–2065.

    Article  PubMed  CAS  Google Scholar 

  85. Jiang, X., Gwye, Y., McKeown, S. J., Bronner-Fraser, M., Lutzko, C., & Lawlor, E. R. (2009). Isolation and characterization of neural crest stem cells derived from in vitro-differentiated human embryonic stem cells. Stem Cells and Development, 18, 1059–1070.

    Article  PubMed  CAS  Google Scholar 

  86. Stemple, D. L., & Anderson, D. J. (1992). Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell, 71, 973–985.

    Article  PubMed  CAS  Google Scholar 

  87. Dupin, E., Real, C., Glavieux-Pardanaud, C., Vaigot, P., & Le Douarin, N. M. (2003). Reversal of developmental restrictions in neural crest lineages: Transition from Schwann cells to glial-melanocytic precursors in vitro. Proceedings of the National Academy of Sciences of the United States of America, 100, 5229–5233.

    Article  PubMed  CAS  Google Scholar 

  88. Real, C., Glavieux-Pardanaud, C., Vaigot, P., Le-Douarin, N., & Dupin, E. (2005). The instability of the neural crest phenotypes: Schwann cells can differentiate into myofibroblasts. International Journal of Developmental Biology, 49, 151–159.

    Article  PubMed  CAS  Google Scholar 

  89. Adameyko, I., Lallemend, F., Aquino, J. B., et al. (2009). Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell, 139, 366–379.

    Article  PubMed  CAS  Google Scholar 

  90. Rizvi, T. A., Huang, Y., Sidani, A., et al. (2002). A novel cytokine pathway suppresses glial cell melanogenesis after injury to adult nerve. Journal of Neuroscience, 22, 9831–9840.

    PubMed  CAS  Google Scholar 

  91. Woodhoo, A., Alonso, M. B., Droggiti, A., et al. (2009). Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nature Neuroscience, 12, 839–847.

    Article  PubMed  CAS  Google Scholar 

  92. Nonaka, D., Chiriboga, L., & Rubin, B. P. (2008). Sox10: A pan-schwannian and melanocytic marker. The American Journal of Surgical Pathology, 32, 1291–1298.

    Article  PubMed  Google Scholar 

  93. Britsch, S., Goerich, D. E., Riethmacher, D., et al. (2001). The transcription factor Sox10 is a key regulator of peripheral glial development. Genes & Development, 15, 66–78.

    Article  CAS  Google Scholar 

  94. Yamamoto, N., Akamatsu, H., Hasegawa, S., et al. (2007). Isolation of multipotent stem cells from mouse adipose tissue. Journal of Dermatological Science, 48, 43–52.

    Article  PubMed  CAS  Google Scholar 

  95. Garratt, A. N., Britsch, S., & Birchmeier, C. (2000). Neuregulin, a factor with many functions in the life of a Schwann cell. Bioessays, 22, 987–996.

    Article  PubMed  CAS  Google Scholar 

  96. Stewart, H. J., Morgan, L., Jessen, K. R., & Mirsky, R. (1993). Changes in DNA synthesis rate in the Schwann cell lineage in vivo are correlated with the precursor–Schwann cell transition and myelination. European Journal of Neuroscience, 5, 1136–1144.

    Article  PubMed  CAS  Google Scholar 

  97. Widera, D., Heimann, P., Zander, C., et al. (2011). Schwann cells can be reprogrammed to multipotency by culture. Stem Cells and Development.

  98. Nagoshi, N., Shibata, S., Hamanoue, M., et al. (2011). Schwann cell plasticity after spinal cord injury shown by neural crest lineage tracing. Glia, 59, 771–784.

    Article  PubMed  Google Scholar 

  99. Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663–676.

    Article  PubMed  CAS  Google Scholar 

  100. Takahashi, K., Tanabe, K., Ohnuki, M., et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131, 861–872.

    Article  PubMed  CAS  Google Scholar 

  101. Smith, K. P., Luong, M. X., & Stein, G. S. (2009). Pluripotency: Toward a gold standard for human ES and iPS cells. Journal of Cellular Physiology, 220, 21–29.

    Article  PubMed  CAS  Google Scholar 

  102. Sieber-Blum, M. (2010). Epidermal neural crest stem cells and their use in mouse models of spinal cord injury. Brain Research Bulletin, 83, 189–193.

    Article  PubMed  CAS  Google Scholar 

  103. Hu, Y. F., Gourab, K., Wells, C., Clewes, O., Schmit, B. D., & Sieber-Blum, M. (2010). Epidermal neural crest stem cell (EPI-NCSC)–mediated recovery of sensory function in a mouse model of spinal cord injury. Stem Cell Reviews, 6, 186–198.

    Article  PubMed  Google Scholar 

  104. Li, Y., Field, P. M., & Raisman, G. (1997). Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science, 277, 2000–2002.

    Article  PubMed  CAS  Google Scholar 

  105. Mackay-Sim, A., Feron, F., Cochrane, J., et al. (2008). Autologous olfactory ensheathing cell transplantation in human paraplegia: A 3-year clinical trial. Brain, 131, 2376–2386.

    Article  PubMed  CAS  Google Scholar 

  106. King-Robson, J. (2010). Encouraging regeneration in the central nervous system: Is there a role for olfactory ensheathing cells? Neuroscience Research, 69, 263–275.

    Article  PubMed  Google Scholar 

  107. Murrell, W., Wetzig, A., Donnellan, M., et al. (2008). Olfactory mucosa is a potential source for autologous stem cell therapy for Parkinson’s disease. Stem Cells, 26, 2183–2192.

    Article  PubMed  CAS  Google Scholar 

  108. Nivet, E., Vignes, M., Girard, S. D., et al. (2011). Engraftment of human nasal olfactory stem cells restores neuroplasticity in mice with hippocampal lesions. The Journal of Clinical Investigation, 121, 2808–2820.

    Article  PubMed  CAS  Google Scholar 

  109. Lavoie, J. F., Biernaskie, J. A., Chen, Y., et al. (2009). Skin-derived precursors differentiate into skeletogenic cell types and contribute to bone repair. Stem Cells and Development, 18, 893–906.

    Article  PubMed  CAS  Google Scholar 

  110. d'Aquino, R., De Rosa, A., Lanza, V., et al. (2009). Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. European Cells & Materials, 18, 75–83.

    Google Scholar 

Download references

Acknowledgments

Work described herein that was performed in our laboratory was supported by a University of Bielefeld FiF (Förderung Innovativer Forschung) grant to DW, grants of the German Research Council (DFG) to CK, and a grant of the German Ministry of Research and Education (BMBF) to BK (grant number 01GN1006A). We thank Johannes Greiner, Stefan Hauser and Jana Mallah for their critical reading of the manuscript, and Janine Müller for the immucytochemical staining of human inferior turbinate tissue.

Conflict of interest disclosure

The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Darius Widera.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaltschmidt, B., Kaltschmidt, C. & Widera, D. Adult Craniofacial Stem Cells: Sources and Relation to the Neural Crest. Stem Cell Rev and Rep 8, 658–671 (2012). https://doi.org/10.1007/s12015-011-9340-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12015-011-9340-9

Keywords

Navigation