Advertisement

Dental Pulp Stem Cells and Neurogenesis

  • Ibrahim Mortada
  • Rola Mortada
  • Mohamad Al Bazzal
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1083)

Abstract

Recent advances in regenerative medicine and cell-based therapy are bringing promising perspectives for the use of stem cells in clinical trials. Stem cells are undifferentiated cells capable of multilineage differentiation and available in numerous sources in the human body. Dental pulp constitutes an attractive source of these cells since collecting mesenchymal stem cells from this site is a noninvasive procedure which can be done following a common surgical extraction of supernumerary or wisdom teeth. Thus tissue sacrifice is very low and several cytotypes can be obtained owing to these cells’ multipotency, in addition to the fact that they can be cryopreserved and stored for long periods. Mesenchymal stem cells have high proliferation rates making them favorable for clinical application. These multipotent cells present in a biological waste constitute an appropriate support in the management of many neurological disorders. After a brief overview on the different types of dental stem cells, this chapter will focus on the characteristics of dental pulp stem cells, their handling and applications in neural tissue engineering, as well as neural induction protocols leading to their potential therapeutic use in the management of neurological diseases.

Keywords

Biology DPSCs Experimental medicine Regenerative medicine Stem cells 

Abbreviations

a-MEM

Minimum essential medium, alpha modification

ATRA

All-trans retinoic acid

BMMSCs

Bone marrow mesenchymal stem cells

DFPCs

Dental follicle progenitor cells

DFSCs

Dental follicle stem cells

DMEM

Dulbecco’s modified Eagle’s medium

DMSO

Dimethyl sulfoxide

DSCs

Dental stem cells

ECM

Extracellular matrix

EGF

Epidermal growth factor

MAP 2

Microtubule-associated protein 2

MSCs

Mesenchymal stem cells

NSE

Neuron-specific enolase

PDLSCs

Periodontal ligament stem cells

rMSCs

Rat bone marrow mesenchymal stem cells

SCAP

Stem cells from apical papilla

SHED

Stem cells from human exfoliated deciduous teeth

TNC

Tenascin C

Notes

Conflicts of Interest

The authors declare no conflicts of interest in relation to this article.

References

  1. About, I. (2013). Dentin–pulp regeneration: The primordial role of the microenvironment and its modification by traumatic injuries and bioactive materials. Endodontic Topics, 28, 61–89.CrossRefGoogle Scholar
  2. Alge, D. L., Zhou, D., Adams, L. L., Wyss, B. K., Shadday, M. D., Woods, E. J., Chu, T. M. G., & Goebel, W. S. (2010). Donor-matched comparison of dental pulp stem cells and bone marrow-derived mesenchymal stem cells in a rat model. Journal of Tissue Engineering and Regenerative Medicine, 4, 73–81.PubMedPubMedCentralGoogle Scholar
  3. Aloe, L., Rocco, M. L., Omar Balzamino, B., & Micera, A. (2015). Nerve growth factor: A focus on Neuroscience and therapy. Current Neuropharmacology, 13, 294–303.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bakopoulou, A., Leyhausen, G., Volk, J., Tsiftsoglou, A., Garefis, P., Koidis, P., & Geurtsen, W. (2011). Assessment of the impact of two different isolation methods on the osteo/odontogenic differentiation potential of human dental stem cells derived from deciduous teeth. Calcified Tissue International, 88, 130–141.CrossRefPubMedGoogle Scholar
  5. Baume, L. J. (1980). The biology of pulp and dentine. A historic, terminologic-taxonomic, histologic-biochemical, embryonic and clinical survey. Monographs in Oral Science, 8, 1–220.PubMedGoogle Scholar
  6. Blau, H. M., & Baltimore, D. (1991). Differentiation requires continuous regulation. The Journal of Cell Biology, 112, 781–783.CrossRefPubMedGoogle Scholar
  7. Brewer, G. J., Torricelli, J. R., Evege, E. K., & Price, P. J. (1993). Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. Journal of Neuroscience Research, 35, 567–576.CrossRefPubMedGoogle Scholar
  8. Chai, Y., Jiang, X., Ito, Y., Bringas, P., Jr., Han, J., Rowitch, D. H., Soriano, P., Mcmahon, A. P., & Sucov, H. M. (2000). Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development, 127, 1671–1679.PubMedGoogle Scholar
  9. Dai, J. W., Yuan, H., Shen, S. Y., Lu, J. T., Zhu, X. F., Yang, T., Zhang, J. F., & Shen, G. F. (2013). p75 neurotrophin receptor positive dental pulp stem cells: New hope for patients with neurodegenerative disease and neural injury. Shanghai Kou Qiang Yi Xue, 22, 469–472.PubMedGoogle Scholar
  10. 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 and Differentiation, 14, 1162–1171.CrossRefPubMedGoogle Scholar
  11. D’aquino, R., De Rosa, A., Laino, G., Caruso, F., Guida, L., Rullo, R., Checchi, V., Laino, L., Tirino, V., & Papaccio, G. (2009). Human dental pulp stem cells: From biology to clinical applications. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 312b, 408–415.CrossRefPubMedGoogle Scholar
  12. Davidson, R. M. (1994). Neural form of voltage-dependent sodium current in human cultured dental pulp cells. Archives of Oral Biology, 39, 613–620.CrossRefPubMedGoogle Scholar
  13. Dezawa, M., Kanno, H., Hoshino, M., Cho, H., Matsumoto, N., Itokazu, Y., Tajima, N., Yamada, H., Sawada, H., Ishikawa, H., Mimura, T., Kitada, M., Suzuki, Y., & Ide, C. (2004). Specific induction of neuronal cells from bone marrow stromal cells and application for autologous transplantation. Journal of Clinical Investigation, 113, 1701–1710.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dimitrova-Nakov, S., Baudry, A., Harichane, Y., Kellermann, O., & Goldberg, M. (2014). Pulp stem cells: Implication in reparative dentin formation. Journal of Endodontia, 40, S13–S18.CrossRefGoogle Scholar
  15. Ding, G., Niu, J., & Wei, F. (2015). Current understanding of orofacial tissue derived mesenchymal stem cells: An immunological perspective. Histology and Histopathology, 30, 255–265.PubMedGoogle Scholar
  16. Doi, M., Nagano, A., & Nakamura, Y. (2004). Molecular cloning and characterization of a novel gene, EMILIN-5, and its possible involvement in skeletal development. Biochemical and Biophysical Research Communications, 313, 888–893.CrossRefPubMedGoogle Scholar
  17. Feng, X., Xing, J., Feng, G., Sang, A., Shen, B., Xu, Y., Jiang, J., Liu, S., Tan, W., Gu, Z., & Li, L. (2013). Age-dependent impaired neurogenic differentiation capacity of dental stem cell is associated with Wnt/beta-catenin signaling. Cellular and Molecular Neurobiology, 33, 1023–1031.CrossRefPubMedGoogle Scholar
  18. Feng, X., Lu, X., Huang, D., Xing, J., Feng, G., Jin, G., Yi, X., Li, L., Lu, Y., Nie, D., Chen, X., Zhang, L., Gu, Z., & Zhang, X. (2014). 3D porous chitosan scaffolds suit survival and neural differentiation of dental pulp stem cells. Cellular and Molecular Neurobiology, 34, 859–870.CrossRefPubMedGoogle Scholar
  19. Ferro, F., Spelat, R., Beltrami, A. P., Cesselli, D., & Curcio, F. (2012). Isolation and characterization of human dental pulp derived stem cells by using media containing low human serum percentage as clinical grade substitutes for bovine serum. PloS One, 7, e48945.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Foudah, D., Monfrini, M., Donzelli, E., Niada, S., Brini, A. T., Orciani, M., Tredici, G., & Miloso, M. (2014). Expression of neural markers by undifferentiated mesenchymal-like stem cells from different sources. Journal of Immunology Research, 2014, 16.CrossRefGoogle Scholar
  21. Frescaline, G., Bouderlique, T., Mansoor, L., Carpentier, G., Baroukh, B., Sineriz, F., Trouillas, M., Saffar, J.-L., Courty, J., Lataillade, J.-J., Papy-Garcia, D., & Albanese, P. (2013). Glycosaminoglycan mimetic associated to human mesenchymal stem cell-based scaffolds inhibit ectopic bone formation, but induce angiogenesis in vivo. Tissue Engineering. Part A, 19, 1641–1653.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gervois, P., Struys, T., Hilkens, P., Bronckaers, A., Ratajczak, J., Politis, C., Brône, B., Lambrichts, I., & Martens, W. (2015). Neurogenic maturation of human dental pulp stem cells following Neurosphere generation induces morphological and electrophysiological characteristics of functional neurons. Stem Cells and Development, 24, 296–311.CrossRefPubMedGoogle Scholar
  23. Goldberg, M., & Smith, A. J. (2004). Cells and extracellular matrices of dentin and pulp: A biological basis for repair and tissue engineering. Critical Reviews in Oral Biology and Medicine, 15, 13–27.CrossRefPubMedGoogle Scholar
  24. Govindasamy, V., Abdullah, A. N., Ronald, V. S., Musa, S., Ab Aziz, Z. A., Zain, R. B., Totey, S., Bhonde, R. R., & Abu Kasim, N. H. (2010). Inherent differential propensity of dental pulp stem cells derived from human deciduous and permanent teeth. Journal of Endodontia, 36, 1504–1515.CrossRefGoogle Scholar
  25. Govindasamy, V., Ronald, V. S., Abdullah, A. N., Ganesan Nathan, K. R., Aziz, Z. A., Abdullah, M., Zain, R. B., Kasim, N. H., Musa, S., & Bhonde, R. R. (2011). Human platelet lysate permits scale-up of dental pulp stromal cells for clinical applications. Cytotherapy, 13, 1221–1233.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gronthos, S., Brahim, J., Li, W., Fisher, L. W., Cherman, N., Boyde, A., Denbesten, P., Robey, P. G., & Shi, S. (2002). Stem cell properties of human dental pulp stem cells. Journal of Dental Research, 81, 531–535.CrossRefPubMedGoogle Scholar
  28. Guo, L., Li, J., Qiao, X., Yu, M., Tang, W., Wang, H., Guo, W., & Tian, W. (2013). Comparison of odontogenic differentiation of human dental follicle cells and human dental papilla cells. PloS One, 8, e62332.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hata, N., Shinojima, N., Gumin, J., Yong, R., Marini, F., Andreeff, M., & Lang, F. F. (2010). PDGF-BB mediates the tropism of human mesenchymal stem cells for malignant gliomas. Neurosurgery, 66, 144–157.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hemmat, S., Lieberman, D. M., & Most, S. P. (2010). An introduction to stem cell biology. Facial Plastic Surgery, 26, 343–349.CrossRefPubMedGoogle Scholar
  31. Hilkens, P., Gervois, P., Fanton, Y., Vanormelingen, J., Martens, W., Struys, T., Politis, C., Lambrichts, I., & Bronckaers, A. (2013). Effect of isolation methodology on stem cell properties and multilineage differentiation potential of human dental pulp stem cells. Cell and Tissue Research, 353, 65–78.CrossRefPubMedGoogle Scholar
  32. Hu, Y., Zhang, Y. A. N., Tian, K., Xun, C., Wang, S., & Lv, D. (2016). Effects of nerve growth factor and basic fibroblast growth factor dual gene modification on rat bone marrow mesenchymal stem cell differentiation into neuron-like cells in vitro. Molecular Medicine Reports, 13, 49–58.CrossRefPubMedGoogle Scholar
  33. Huang, A. H., Chen, Y. K., Lin, L. M., Shieh, T. Y., & Chan, A. W. (2008). Isolation and characterization of dental pulp stem cells from a supernumerary tooth. Journal of Oral Pathology & Medicine, 37, 571–574.CrossRefGoogle Scholar
  34. Iwasaki, K., Komaki, M., Yokoyama, N., Tanaka, Y., Taki, A., Kimura, Y., Takeda, M., Oda, S., Izumi, Y., & Morita, I. (2013). Periodontal ligament stem cells possess the characteristics of pericytes. Journal of Periodontology, 84, 1425–1433.CrossRefPubMedGoogle Scholar
  35. Jalali, A., Bassuk, A. G., Kan, L., Israsena, N., Mukhopadhyay, A., Mcguire, T., & Kessler, J. A. (2011). HeyL promotes neuronal differentiation of neural progenitor cells. Journal of Neuroscience Research, 89, 299–309.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jung, S., Panchalingam, K. M., Rosenberg, L., & Behie, L. A. (2012). Ex vivo expansion of human mesenchymal stem cells in defined serum-free media. Stem Cells International, 2012, 21.CrossRefGoogle Scholar
  37. Kadar, K., Kiraly, M., Porcsalmy, B., Molnar, B., Racz, G. Z., Blazsek, J., Kallo, K., Szabo, E. L., Gera, I., Gerber, G., & Varga, G. (2009). Differentiation potential of stem cells from human dental origin - promise for tissue engineering. Journal of Physiology and Pharmacology, 60(Suppl 7), 167–175.PubMedGoogle Scholar
  38. Karaoz, E., Dogan, B. N., Aksoy, A., Gacar, G., Akyuz, S., Ayhan, S., Genc, Z. S., Yuruker, S., Duruksu, G., Demircan, P. C., & Sariboyaci, A. E. (2010). Isolation and in vitro characterisation of dental pulp stem cells from natal teeth. Histochemistry and Cell Biology, 133, 95–112.CrossRefPubMedGoogle Scholar
  39. Kawashima, N. (2012). Characterisation of dental pulp stem cells: A new horizon for tissue regeneration? Archives of Oral Biology, 57, 1439–1458.CrossRefPubMedGoogle Scholar
  40. Kerkis, I., & Caplan, A. I. (2012). Stem cells in dental pulp of deciduous teeth. Tissue Engineering. Part B, Reviews, 18, 129–138.CrossRefPubMedGoogle Scholar
  41. Kim, H., Zahir, T., Tator, C. H., & Shoichet, M. S. (2011). Effects of dibutyryl cyclic-AMP on survival and neuronal differentiation of neural stem/progenitor cells transplanted into spinal cord injured rats. PloS One, 6, e21744.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kiraly, M., Kadar, K., Horvathy, D. B., Nardai, P., Racz, G. Z., Lacza, Z., Varga, G., & Gerber, G. (2011). Integration of neuronally predifferentiated human dental pulp stem cells into rat brain in vivo. Neurochemistry International, 59, 371–381.CrossRefPubMedGoogle Scholar
  43. La Noce, M., Mele, L., Tirino, V., Paino, F., De Rosa, A., Naddeo, P., Papagerakis, P., Papaccio, G., & Desiderio, V. (2014). Neural crest stem cell population in craniomaxillofacial development and tissue repair. European Cells & Materials, 28, 348–357.CrossRefGoogle Scholar
  44. 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). Journal of Bone and Mineral Research, 20, 1394–1402.CrossRefPubMedGoogle Scholar
  45. Ledesma-Martínez, E., Mendoza-Núñez, V. M., & Santiago-Osorio, E. (2016). Mesenchymal stem cells derived from dental pulp: A review. Stem Cells International, 2016, 12.CrossRefGoogle Scholar
  46. Lee, J. H., Lee, D. S., Choung, H. W., Shon, W. J., Seo, B. M., Lee, E. H., Cho, J. Y., & Park, J. C. (2011). Odontogenic differentiation of human dental pulp stem cells induced by preameloblast-derived factors. Biomaterials, 32, 9696–9706.CrossRefPubMedGoogle Scholar
  47. Liu, H., Gronthos, S., & Shi, S. (2006). Dental pulp stem cells. Methods in Enzymology, 419, 99–113.CrossRefPubMedGoogle Scholar
  48. Lizier, N. F., Kerkis, A., Gomes, C. M., Hebling, J., Oliveira, C. F., Caplan, A. I., & Kerkis, I. (2012). Scaling-up of dental pulp stem cells isolated from multiple niches. PloS One, 7, e39885.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Lu, Y., Yuan, X., Ou, Y., Cai, Y., Wang, S., Sun, Q., & Zhang, W. (2012). Autophagy and apoptosis during adult adipose-derived stromal cells differentiation into neuron-like cells in vitro. Neural Regeneration Research, 7, 1205–1212.PubMedPubMedCentralGoogle Scholar
  50. Martens, W., Wolfs, E., Struys, T., Politis, C., Bronckaers, A., & Lambrichts, I. (2012). Expression pattern of basal markers in human dental pulp stem cells and tissue. Cells, Tissues, Organs, 196, 490–500.CrossRefPubMedGoogle Scholar
  51. Mukhopadhyay, A., Jarrett, J., Chlon, T., & Kessler, J. A. (2009). HeyL regulates the number of TrkC neurons in dorsal root ganglia. Developmental Biology, 334, 142–151.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Nanci, A. (2007). Ten Cate’s oral histology - Pageburst on VitalSource: Development, structure, and function. Elsevier Health Sciences.Google Scholar
  53. Ni, L., Wen, Y., Peng, X., & Jonakait, G. M. (2001). Antioxidants N-acetylcysteine (NAC) and 2-mercaptoethanol (2-ME) affect the survival and differentiative potential of cholinergic precursors from the embryonic septal nuclei and basal forebrain: Involvement of ras signaling. Brain Research. Developmental Brain Research, 130, 207–216.CrossRefPubMedGoogle Scholar
  54. Osathanon, T., Manokawinchoke, J., Nowwarote, N., Aguilar, P., Palaga, T., & Pavasant, P. (2013). Notch signaling is involved in neurogenic commitment of human periodontal ligament-derived mesenchymal stem cells. Stem Cells and Development, 22, 1220–1231.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Osathanon, T., Sawangmake, C., Nowwarote, N., & Pavasant, P. (2014). Neurogenic differentiation of human dental pulp stem cells using different induction protocols. Oral Diseases, 20, 352–358.CrossRefPubMedGoogle Scholar
  56. Park, H. Y., Kim, J. H., Sun Kim, H., & Park, C. K. (2012). Stem cell-based delivery of brain-derived neurotrophic factor gene in the rat retina. Brain Research, 1469, 10–23.CrossRefPubMedGoogle Scholar
  57. Paschalidis, T., Bakopoulou, A., Papa, P., Leyhausen, G., Geurtsen, W., & Koidis, P. (2014). Dental pulp stem cells’ secretome enhances pulp repair processes and compensates TEGDMA-induced cytotoxicity. Dental Materials, 30, e405–e418.CrossRefPubMedGoogle Scholar
  58. Racz, G. Z., Kadar, K., Foldes, A., Kallo, K., Perczel-Kovach, K., Keremi, B., Nagy, A., & Varga, G. (2014). Immunomodulatory and potential therapeutic role of mesenchymal stem cells in periodontitis. Journal of Physiology and Pharmacology, 65, 327–339.PubMedGoogle Scholar
  59. Ranganathan, K., & Lakshminarayanan, V. (2012). Stem cells of the dental pulp. Indian Journal of Dental Research, 23, 558.CrossRefPubMedGoogle Scholar
  60. Raoof, M., Yaghoobi, M. M., Derakhshani, A., Kamal-Abadi, A. M., Ebrahimi, B., Abbasnejad, M., & Shokouhinejad, N. (2014). A modified efficient method for dental pulp stem cell isolation. Dent Res J (Isfahan), 11, 244–250.Google Scholar
  61. Roozafzoon, R., Lashay, A., Vasei, M., AI, J., Khoshzaban, A., Keshel, S. H., Barabadi, Z., & Bahrami, H. (2015). Dental pulp stem cells differentiation into retinal ganglion-like cells in a three dimensional network. Biochemical and Biophysical Research Communications, 457, 154–160.CrossRefPubMedGoogle Scholar
  62. Saito, M. T., Silvério, K. G., Casati, M. Z., Sallum, E. A., & Nociti, F. H., Jr. (2015). Tooth-derived stem cells: Update and perspectives. World Journal of Stem Cells, 7, 399–407.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Sakai, K., Yamamoto, A., Matsubara, K., Nakamura, S., Naruse, M., Yamagata, M., Sakamoto, K., tauchi, R., wakao, N., Imagama, S., Hibi, H., Kadomatsu, K., Ishiguro, N., & Ueda, M. (2012). Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. The Journal of Clinical Investigation, 122, 80–90.PubMedGoogle Scholar
  64. Santa-Olalla, J., & Covarrubias, L. (1995). Epidermal growth factor (EGF), transforming growth factor-alpha (TGF-alpha), and basic fibroblast growth factor (bFGF) differentially influence neural precursor cells of mouse embryonic mesencephalon. Journal of Neuroscience Research, 42, 172–183.CrossRefPubMedGoogle Scholar
  65. Santos, N. C., Figueira-Coelho, J., Martins-Silva, J., & Saldanha, C. (2003). Multidisciplinary utilization of dimethyl sulfoxide: Pharmacological, cellular, and molecular aspects. Biochemical Pharmacology, 65, 1035–1041.CrossRefPubMedGoogle Scholar
  66. Silvério, K. G., Davidson, K. C., James, R. G., Adams, A. M., Foster, B. L., Nociti, F. H., Somermam, M. J., & Moon, R. T. (2012). Wnt/β-catenin pathway regulates Bmp2-mediated differentiation of dental follicle cells. Journal of Periodontal Research, 47. doi: 10.1111/j.1600-0765.2011.01433.x.CrossRefPubMedGoogle Scholar
  67. Sonoyama, W., Yamaza, T., Gronthos, S., & Shi, S. (2007). Multipotent stem cells in dental pulp. In Culture of human stem cells. Hoboken: Wiley.Google Scholar
  68. Suchanek, J., Visek, B., Soukup, T., El-Din Mohamed, S. K., Ivancaková, R., Mokrỳ, J., Aboul-Ezz, E. H., & Omran, A. (2010). Stem cells from human exfoliated deciduous teeth--isolation, long term cultivation and phenotypical analysis. Acta Medica (Hradec Králové), 53, 93–99.CrossRefGoogle Scholar
  69. Sun, H.-H., Chen, B., Zhu, Q.-L., Kong, H., Li, Q.-H., Gao, L.-N., Xiao, M., Chen, F.-M., & Yu, Q. (2014). Investigation of dental pulp stem cells isolated from discarded human teeth extracted due to aggressive periodontitis. Biomaterials, 35, 9459–9472.CrossRefPubMedGoogle Scholar
  70. Tamaki, Y., Nakahara, T., Ishikawa, H., & Sato, S. (2013). In vitro analysis of mesenchymal stem cells derived from human teeth and bone marrow. Odontology, 101, 121–132.CrossRefGoogle Scholar
  71. Tatullo, M., Marrelli, M., Shakesheff, K. M., & White, L. J. (2015). Dental pulp stem cells: Function, isolation and applications in regenerative medicine. Journal of Tissue Engineering and Regenerative Medicine, 9, 1205–1216.CrossRefPubMedGoogle Scholar
  72. Tsiperson, V., Huang, Y., Bagayogo, I., Song, Y., Vondran, M. W., Dicicco-Bloom, E. & Dreyfus, C. F. 2015. Brain-derived neurotrophic factor deficiency restricts proliferation of oligodendrocyte progenitors following Cuprizone-induced demyelination. ASN Neuro, 7, 1759091414566878.CrossRefGoogle Scholar
  73. Van Kooten, T. G., Spijker, H. T., & Busscher, H. J. (2004). Plasma-treated polystyrene surfaces: Model surfaces for studying cell-biomaterial interactions. Biomaterials, 25, 1735–1747.CrossRefPubMedGoogle Scholar
  74. Wada, N., Menicanin, D., Shi, S., Bartold, P. M., & Gronthos, S. (2009). Immunomodulatory properties of human periodontal ligament stem cells. Journal of Cellular Physiology, 219, 667–676.CrossRefPubMedGoogle Scholar
  75. Xiao, L., & Nasu, M. (2014). From regenerative dentistry to regenerative medicine: Progress, challenges, and potential applications of oral stem cells. Stem Cells and Cloning: Advances and Applications, 7, 89–99.Google Scholar
  76. Xiao, L., & Tsutsui, T. (2013). Characterization of human dental pulp cells-derived spheroids in serum-free medium: Stem cells in the core. Journal of Cellular Biochemistry, 114, 2624–2636.CrossRefPubMedGoogle Scholar
  77. Yalvac, M. E., Ramazanoglu, M., Rizvanov, A. A., Sahin, F., Bayrak, O. F., Salli, U., Palotas, A., & Kose, G. T. (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.CrossRefPubMedGoogle Scholar
  78. Zhao, H., & Chai, Y. (2015). Stem cells in teeth and craniofacial bones. Journal of Dental Research, 94, 1495–1501.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Ibrahim Mortada
    • 1
  • Rola Mortada
    • 2
  • Mohamad Al Bazzal
    • 2
  1. 1.Faculty of MedicineAmerican University of BeirutBeirutLebanon
  2. 2.Lebanese University School of DentistryBeirutLebanon

Personalised recommendations