Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 2582080, 14 pages
https://doi.org/10.1155/2017/2582080
Research Article

The Angiogenic Potential of DPSCs and SCAPs in an In Vivo Model of Dental Pulp Regeneration

Laboratory of Morphology, Biomedical Research Institute (BIOMED), Hasselt University, Diepenbeek, Belgium

Correspondence should be addressed to Petra Hilkens; eb.tlessahu@sneklih.artep

Received 26 April 2017; Revised 4 July 2017; Accepted 13 July 2017; Published 5 September 2017

Academic Editor: Gerald A. Colvin

Copyright © 2017 Petra Hilkens et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Hilkens, N. Meschi, P. Lambrechts, A. Bronckaers, and I. Lambrichts, “Dental stem cells in pulp regeneration: near future or long road ahead?” Stem Cells and Development, vol. 24, no. 14, pp. 1610–1622, 2015. View at Publisher · View at Google Scholar · View at Scopus
  2. K. M. Hargreaves, A. Diogenes, and F. B. Teixeira, “Treatment options: biological basis of regenerative endodontic procedures,” Journal of Endodontia, vol. 39, Supplement 3, pp. S30–S43, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. B. Kahler, G. Rossi-Fedele, N. Chugal, and L. M. Lin, “An evidence-based review of the efficacy of treatment approaches for immature permanent teeth with pulp necrosis,” Journal of Endodontia, vol. 43, no. 7, pp. 1052–1057, 2017. View at Publisher · View at Google Scholar
  4. A. Diogenes, N. B. Ruparel, Y. Shiloah, and K. M. Hargreaves, “Regenerative endodontics: a way forward,” Journal of the American Dental Association (1939), vol. 147, no. 5, pp. 372–380, 2016. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Altaii, L. Richards, and G. Rossi-Fedele, “Histological assessment of regenerative endodontic treatment in animal studies with different scaffolds: a systematic review,” Dental Traumatology, vol. 33, no. 4, pp. 235–244, 2017. View at Publisher · View at Google Scholar
  6. G. T. Huang, M. Al-Habib, and P. Gauthier, “Challenges of stem cell-based pulp and dentin regeneration: a clinical perspective,” Endodontic Topics, vol. 28, no. 1, pp. 51–60, 2013. View at Publisher · View at Google Scholar
  7. J. O. Andreasen, M. K. Borum, H. L. Jacobsen, and F. M. Andreasen, “Replantation of 400 avulsed permanent incisors. 2. Factors related to pulpal healing,” Endodontics & Dental Traumatology, vol. 11, no. 2, pp. 59–68, 1995. View at Google Scholar
  8. M. Kling, M. Cvek, and I. Mejare, “Rate and predictability of pulp revascularization in therapeutically reimplanted permanent incisors,” Endodontics & Dental Traumatology, vol. 2, no. 3, pp. 83–89, 1986. View at Google Scholar
  9. N. Takeuchi, Y. Hayashi, M. Murakami et al., “Similar in vitro effects and pulp regeneration in ectopic tooth transplantation by basic fibroblast growth factor and granulocyte-colony stimulating factor,” Oral Diseases, vol. 21, no. 1, pp. 113–122, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Hilkens, Y. Fanton, W. Martens et al., “Pro-angiogenic impact of dental stem cells in vitro and in vivo,” Stem Cell Research, vol. 12, no. 3, pp. 778–790, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Bakopoulou, A. Kritis, D. Andreadis et al., “Angiogenic potential and secretome of human apical papilla mesenchymal stem cells in various stress microenvironments,” Stem Cells and Development, vol. 24, no. 21, pp. 2496–2512, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Bronckaers, P. Hilkens, Y. Fanton et al., “Angiogenic properties of human dental pulp stem cells,” PLoS One, vol. 8, no. 8, article e71104, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Nakashima, K. Iohara, and M. Sugiyama, “Human dental pulp stem cells with highly angiogenic and neurogenic potential for possible use in pulp regeneration,” Cytokine & Growth Factor Reviews, vol. 20, no. 5-6, pp. 435–440, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Tran-Hung, S. Mathieu, and I. About, “Role of human pulp fibroblasts in angiogenesis,” Journal of Dental Research, vol. 85, no. 9, pp. 819–823, 2006. View at Publisher · View at Google Scholar
  15. J. Vanacker, A. Viswanath, P. De Berdt et al., “Hypoxia modulates the differentiation potential of stem cells of the apical papilla,” Journal of Endodontia, vol. 40, no. 9, pp. 1410–1418, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Yu, Y. Zhao, Y. Ma, and L. Ge, “Profiling the secretome of human stem cells from dental apical papilla,” Stem Cells and Development, vol. 25, no. 6, pp. 499–508, 2016. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Ratajczak, A. Bronckaers, Y. Dillen et al., “The neurovascular properties of dental stem cells and their importance in dental tissue engineering,” Stem Cells International, vol. 2016, Article ID 9762871, 17 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  18. A. M. Aranha, Z. Zhang, K. G. Neiva, C. A. Costa, J. Hebling, and J. E. Nör, “Hypoxia enhances the angiogenic potential of human dental pulp cells,” Journal of Endodontia, vol. 36, no. 10, pp. 1633–1637, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. W. L. Dissanayaka, K. M. Hargreaves, L. Jin, L. P. Samaranayake, and C. Zhang, “The interplay of dental pulp stem cells and endothelial cells in an injectable peptide hydrogel on angiogenesis and pulp regeneration in vivo,” Tissue Engineering Part A, vol. 21, no. 3-4, pp. 550–563, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Iohara, L. Zheng, H. Wake et al., “A novel stem cell source for vasculogenesis in ischemia: subfraction of side population cells from dental pulp,” Stem Cells, vol. 26, no. 9, pp. 2408–2418, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Yuan, P. Wang, L. Zhu et al., “Coculture of stem cells from apical papilla and human umbilical vein endothelial cell under hypoxia increases the formation of three-dimensional vessel-like structures in vitro,” Tissue Engineering Part A, vol. 21, no. 5-6, pp. 1163–1172, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Gandia, A. Armiñan, J. M. García-Verdugo et al., “Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction,” Stem Cells, vol. 26, no. 3, pp. 638–645, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. G. T. Huang, T. Yamaza, L. D. Shea et al., “Stem/progenitor cell-mediated de novo regeneration of dental pulp with newly deposited continuous layer of dentin in an in vivo model,” Tissue Engineering Part A, vol. 16, no. 2, pp. 605–615, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Rosa, Z. Zhang, R. H. Grande, and J. E. Nör, “Dental pulp tissue engineering in full-length human root canals,” Journal of Dental Research, vol. 92, no. 11, pp. 970–975, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. J. W. Yang, Y. F. Zhang, C. Y. Wan et al., “Autophagy in SDF-1alpha-mediated DPSC migration and pulp regeneration,” Biomaterials, vol. 44, pp. 11–23, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Bose, S. Tarafder, and A. Bandyopadhyay, “Effect of chemistry on osteogenesis and angiogenesis towards bone tissue engineering using 3D printed scaffolds,” Annals of Biomedical Engineering, vol. 45, no. 1, pp. 261–272, 2017. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Partridge, N. Conlisk, and J. A. Davies, “In-lab three-dimensional printing: an inexpensive tool for experimentation and visualization for the field of organogenesis,” Organogenesis, vol. 8, no. 1, pp. 22–27, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. M. S. Mannoor, Z. Jiang, T. James et al., “3D printed bionic ears,” Nano Letters, vol. 13, no. 6, pp. 2634–2639, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Khalyfa, S. Vogt, J. Weisser et al., “Development of a new calcium phosphate powder-binder system for the 3D printing of patient specific implants,” Journal of Materials Science: Materials in Medicine, vol. 18, no. 5, pp. 909–916, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Rombouts, T. Giraud, C. Jeanneau, and I. About, “Pulp vascularization during tooth development, regeneration, and therapy,” Journal of Dental Research, vol. 96, no. 2, pp. 137–144, 2017. View at Publisher · View at Google Scholar
  31. R. van Noort, “The future of dental devices is digital,” Dental Materials, vol. 28, no. 1, pp. 3–12, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. C. Chiu, H. Y. Fang, T. T. Hsu, C. Y. Lin, and M. Y. Shie, “The characteristics of mineral trioxide aggregate/polycaprolactone 3-dimensional scaffold with osteogenesis properties for tissue regeneration,” Journal of Endodontia, vol. 43, no. 6, pp. 923–929, 2017. View at Publisher · View at Google Scholar
  33. A. Louvrier, E. Euvrard, L. Nicod et al., “Odontoblastic differentiation of dental pulp stem cells from healthy and carious teeth on an original PCL-based 3D scaffold,” International Endodontic Journal, 2017. View at Publisher · View at Google Scholar
  34. F. Wei, T. Song, G. Ding et al., “Functional tooth restoration by allogeneic mesenchymal stem cell-based bio-root regeneration in swine,” Stem Cells and Development, vol. 22, no. 12, pp. 1752–1762, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. L. E. Bertassoni, M. Cecconi, V. Manoharan et al., “Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs,” Lab on a Chip, vol. 14, no. 13, pp. 2202–2211, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. J. S. Miller, K. R. Stevens, M. T. Yang et al., “Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues,” Nature Materials, vol. 11, no. 9, pp. 768–774, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Gronthos, M. Mankani, J. Brahim, P. G. Robey, and S. Shi, “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, vol. 97, no. 25, pp. 13625–13630, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. W. Zhang, X. F. Walboomers, G. J. van Osch, J. van den Dolder, and J. A. Jansen, “Hard tissue formation in a porous HA/TCP ceramic scaffold loaded with stromal cells derived from dental pulp and bone marrow,” Tissue Engineering Part A, vol. 14, no. 2, pp. 285–294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. Z. H. Gao, L. Hu, G. L. Liu et al., “Bio-root and implant-based restoration as a tooth replacement alternative,” Journal of Dental Research, vol. 95, no. 6, pp. 642–649, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. B. N. Cavalcanti, B. D. Zeitlin, and J. E. Nor, “A hydrogel scaffold that maintains viability and supports differentiation of dental pulp stem cells,” Dental Materials, vol. 29, no. 1, pp. 97–102, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Hilkens, P. Gervois, Y. Fanton et al., “Effect of isolation methodology on stem cell properties and multilineage differentiation potential of human dental pulp stem cells,” Cell and Tissue Research, vol. 353, no. 1, pp. 65–78, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Lin, K. L. Chow, and Y. Leng, “Study of hydroxyapatite osteoinductivity with an osteogenic differentiation of mesenchymal stem cells,” Journal of Biomedical Materials Research. Part A, vol. 89, no. 2, pp. 326–335, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. S. E. Lobo, R. Glickman, W. N. da Silva, T. L. Arinzeh, and I. Kerkis, “Response of stem cells from different origins to biphasic calcium phosphate bioceramics,” Cell and Tissue Research, vol. 361, no. 2, pp. 477–495, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Zhang, P. R. Cooper, G. Smith, J. E. Nör, and A. J. Smith, “Angiogenic activity of dentin matrix components,” Journal of Endodontia, vol. 37, no. 1, pp. 26–30, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. Y. Bai, P. Li, G. Yin et al., “BMP-2, VEGF and bFGF synergistically promote the osteogenic differentiation of rat bone marrow-derived mesenchymal stem cells,” Biotechnology Letters, vol. 35, no. 3, pp. 301–308, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. A. D. Berendsen and B. R. Olsen, “How vascular endothelial growth factor-A (VEGF) regulates differentiation of mesenchymal stem cells,” The Journal of Histochemistry and Cytochemistry, vol. 62, no. 2, pp. 103–108, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. I. D' Alimonte, E. Nargi, F. Mastrangelo et al., “Vascular endothelial growth factor enhances in vitro proliferation and osteogenic differentiation of human dental pulp stem cells,” Journal of Biological Regulators and Homeostatic Agents, vol. 25, no. 1, pp. 57–69, 2011. View at Google Scholar
  48. W. Zhang, W. Liu, J. Ling et al., “Odontogenic differentiation of vascular endothelial growth factor-transfected human dental pulp stem cells in vitro,” Molecular Medicine Reports, vol. 10, no. 4, pp. 1899–1906, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. A. I. Hoch, B. Y. Binder, D. C. Genetos, and J. K. Leach, “Differentiation-dependent secretion of proangiogenic factors by mesenchymal stem cells,” PLoS One, vol. 7, no. 4, article e35579, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. H. Wu, N. Kang, Q. Wang et al., “The dose-effect relationship between the seeding quantity of human marrow mesenchymal stem cells and in vivo tissue-engineered bone yield,” Cell Transplantation, vol. 24, no. 10, pp. 1957–1968, 2015. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Xue, J. Y. Li, Y. Yeh, L. Yang, and S. Chien, “Effects of matrix elasticity and cell density on human mesenchymal stem cells differentiation,” Journal of Orthopaedic Research, vol. 31, no. 9, pp. 1360–1365, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Iohara, K. Imabayashi, R. Ishizaka et al., “Complete pulp regeneration after pulpectomy by transplantation of CD105+ stem cells with stromal cell-derived factor-1,” Tissue Engineering Part A, vol. 17, no. 15-16, pp. 1911–1920, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Iohara, M. Murakami, K. Nakata, and M. Nakashima, “Age-dependent decline in dental pulp regeneration after pulpectomy in dogs,” Experimental Gerontology, vol. 52, pp. 39–45, 2014. View at Publisher · View at Google Scholar · View at Scopus