Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2016, Article ID 6240794, 11 pages
http://dx.doi.org/10.1155/2016/6240794
Research Article

Scaffold-Free Fabrication of Osteoinductive Cellular Constructs Using Mouse Gingiva-Derived Induced Pluripotent Stem Cells

1Division of Molecular and Regenerative Prosthodontics, Tohoku University Graduate School of Dentistry, Sendai, Miyagi 980-8575, Japan
2Department of Fixed Prosthodontics, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka 565-0871, Japan
3Department of Biomaterials Science, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka 565-0871, Japan
4Division for Interdisciplinary Dentistry, Osaka University Dental Hospital, 1-8 Yamadaoka, Suita, Osaka 565-0871, Japan
5Department of Biomaterials, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, 2-5-1 Shikada-cho, Kita-ku, Okayama 700-8525, Japan
6Center for Advanced Stem Cell and Regenerative Research, Tohoku University Graduate School of Dentistry, Sendai, Miyagi 980-8575, Japan

Received 21 November 2015; Accepted 18 February 2016

Academic Editor: Boon C. Heng

Copyright © 2016 Hiroko Okawa 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. C. Masaki, T. Nakamoto, T. Mukaibo, Y. Kondo, and R. Hosokawa, “Strategies for alveolar ridge reconstruction and preservation for implant therapy,” Journal of Prosthodontic Research, vol. 59, no. 4, pp. 220–228, 2015. View at Publisher · View at Google Scholar
  2. P. Li, Y. Honda, Y. Arima et al., “Interferon-γ enhances the efficacy of autogenous bone grafts by inhibiting postoperative bone resorption in rat calvarial defects,” Journal of Prosthodontic Research, 2016. View at Publisher · View at Google Scholar
  3. H. Egusa, W. Sonoyama, M. Nishimura, I. Atsuta, and K. Akiyama, “Stem cells in dentistry—part II: clinical applications,” Journal of Prosthodontic Research, vol. 56, no. 4, pp. 229–248, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. C. M. Murphy, F. J. O'Brien, D. G. Little, and A. Schindeler, “Cell-scaffold interactions in the bone tissue engineering triad,” European Cells and Materials, vol. 26, pp. 120–132, 2013. View at Google Scholar · View at Scopus
  5. S. F. Badylak and T. W. Gilbert, “Immune response to biologic scaffold materials,” Seminars in Immunology, vol. 20, no. 2, pp. 109–116, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Egusa, W. Sonoyama, M. Nishimura, I. Atsuta, and K. Akiyama, “Stem cells in dentistry—part I: stem cell sources,” Journal of Prosthodontic Research, vol. 56, no. 3, pp. 151–165, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Kaku, Y. Akiba, K. Akiyama, D. Akita, and M. Nishimura, “Cell-based bone regeneration for alveolar ridge augmentation—cell source, endogenous cell recruitment and immunomodulatory function,” Journal of Prosthodontic Research, vol. 59, no. 2, pp. 96–112, 2015. View at Publisher · View at Google Scholar
  8. J. H. Lee, J.-H. Seo, K. M. Lee, H.-S. Ryu, and H.-R. Baek, “Fabrication and evaluation of osteoblastic differentiation of human mesenchymal stem cells on novel cao-SiO2-P2O5-B2O3 glass-ceramics,” Artificial Organs, vol. 37, no. 7, pp. 637–647, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Zhou, C. Xu, G. Wu et al., “In vitro generation of osteochondral differentiation of human marrow mesenchymal stem cells in novel collagen-hydroxyapatite layered scaffolds,” Acta Biomaterialia, vol. 7, no. 11, pp. 3999–4006, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. J.-I. Sasaki, T. Matsumoto, H. Egusa et al., “In vitro reproduction of endochondral ossification using a 3D mesenchymal stem cell construct,” Integrative Biology, vol. 4, no. 10, pp. 1207–1214, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Kittaka, M. Kajiya, H. Shiba et al., “Clumps of a mesenchymal stromal cell/extracellular matrix complex can be a novel tissue engineering therapy for bone regeneration,” Cytotherapy, vol. 17, no. 7, pp. 860–873, 2015. View at Publisher · View at Google Scholar
  12. Z.-Y. Zhang, S.-H. Teoh, M. S. K. Chong et al., “Superior osteogenic capacity for bone tissue engineering of fetal compared with perinatal and adult mesenchymal stem cells,” STEM CELLS, vol. 27, no. 1, pp. 126–137, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Egusa, K. Okita, H. Kayashima et al., “Gingival fibroblasts as a promising source of induced pluripotent stem cells,” PloS ONE, vol. 5, no. 9, Article ID e12743, 2010. View at Google Scholar · View at Scopus
  15. G. Yu, H. Okawa, K. Okita et al., “Gingival fibroblasts as autologous feeders for induced pluripotent stem cells,” Journal of Dental Research, vol. 95, no. 1, pp. 110–118, 2016. View at Publisher · View at Google Scholar
  16. X. Lou, “Induced pluripotent stem cells as a new strategy for osteogenesis and bone regeneration,” Stem Cell Reviews and Reports, vol. 11, no. 4, pp. 645–651, 2015. View at Publisher · View at Google Scholar
  17. H. Egusa, H. Kayashima, J. Miura et al., “Comparative analysis of mouse-induced pluripotent stem cells and mesenchymal stem cells during osteogenic differentiation in vitro,” Stem Cells and Development, vol. 23, no. 18, pp. 2156–2169, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. J.-I. Sasaki, T.-A. Asoh, T. Matsumoto et al., “Fabrication of three-dimensional cell constructs using temperature-responsive hydrogel,” Tissue Engineering Part A, vol. 16, no. 8, pp. 2497–2504, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Y. Speer, X. Li, P. G. Hiremath, and C. M. Giachelli, “Runx2/Cbfa1, but not loss of myocardin, is required for smooth muscle cell lineage reprogramming toward osteochondrogenesis,” Journal of Cellular Biochemistry, vol. 110, no. 4, pp. 935–947, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. J. L. Fowlkes, R. C. Bunn, L. Liu et al., “Runt-related transcription factor 2 (RUNX2) and RUNX2-related osteogenic genes are down-regulated throughout osteogenesis in type 1 diabetes mellitus,” Endocrinology, vol. 149, no. 4, pp. 1697–1704, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. L. A. Kaback, D. Y. Soung, A. Naik et al., “Teriparatide (1-34 human PTH) regulation of osterix during fracture repair,” Journal of Cellular Biochemistry, vol. 105, no. 1, pp. 219–226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Jadlowiec, H. Koch, X. Zhang, P. G. Campbell, M. Seyedain, and C. Sfeir, “Phosphophoryn regulates the gene expression and differentiation of NIH3T3, MC3T3-E1, and human mesenchymal stem cells via the integrin/MAPK signaling pathway,” The Journal of Biological Chemistry, vol. 279, no. 51, pp. 53323–53330, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. G. Gautier, M. Humbert, F. Deauvieau et al., “A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells,” The Journal of Experimental Medicine, vol. 201, no. 9, pp. 1435–1446, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Sasaki, M. Hashimoto, S. Yamaguchi et al., “Fabrication of biomimetic bone tissue using mesenchymal stem cell-derived three-dimensional constructs incorporating endothelial cells,” PLoS ONE, vol. 10, no. 6, Article ID e0129266, 2015. View at Google Scholar
  25. T. D. Schmittgen and K. J. Livak, “Analyzing real-time PCR data by the comparative CT method,” Nature Protocols, vol. 3, no. 6, pp. 1101–1108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Egusa, M. Kobayashi, T. Matsumoto, J.-I. Sasaki, S. Uraguchi, and H. Yatani, “Application of cyclic strain for accelerated skeletal myogenic differentiation of mouse bone marrow-derived mesenchymal stromal cells with cell alignment,” Tissue Engineering—Part A, vol. 19, no. 5-6, pp. 770–782, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Tashiro, M. Inamura, K. Kawabata et al., “Efficient adipocyte and osteoblast differentiation from mouse induced pluripotent stem cells by adenoviral transduction,” Stem Cells, vol. 27, no. 8, pp. 1802–1811, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Bilousova, D. H. Jun, K. B. King et al., “Osteoblasts derived from induced pluripotent stem cells form calcified structures in scaffolds both in vitro and in vivo,” Stem Cells, vol. 29, no. 2, pp. 206–216, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Nakashima, X. Zhou, G. Kunkel et al., “The novel zinc finger-containing transcription factor Osterix is required for osteoblast differentiation and bone formation,” Cell, vol. 108, no. 1, pp. 17–29, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. T. M. Liu and E. H. Lee, “Transcriptional regulatory cascades in Runx2-dependent bone development,” Tissue Engineering—Part B: Reviews, vol. 19, no. 3, pp. 254–263, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Kaku and M. Yamauchi, “Mechano-regulation of collagen biosynthesis in periodontal ligament,” Journal of Prosthodontic Research, vol. 58, no. 4, pp. 193–207, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Patti, L. Gennari, D. Merlotti, F. Dotta, and R. Nuti, “Endocrine actions of osteocalcin,” International Journal of Endocrinology, vol. 2013, Article ID 846480, 10 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. T. Matsubara, K. Kida, A. Yamaguchi et al., “BMP2 regulates osterix through Msx2 and Runx2 during osteoblast differentiation,” The Journal of Biological Chemistry, vol. 283, no. 43, pp. 29119–29125, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. D.-S. Lee, H.-W. Choung, H.-J. Kim et al., “NFI-C regulates osteoblast differentiation via control of osterix expression,” Stem Cells, vol. 32, no. 9, pp. 2467–2479, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. M.-H. Lee, T.-G. Kwon, H.-S. Park, J. M. Wozney, and H.-M. Ryoo, “BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2,” Biochemical and Biophysical Research Communications, vol. 309, no. 3, pp. 689–694, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Szabova, S. S. Yamada, H. Wimer et al., “MT1-MMP and type II collagen specify skeletal stem cells and their bone and cartilage progeny,” Journal of Bone and Mineral Research, vol. 24, no. 11, pp. 1905–1916, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Bonucci, “Bone mineralization,” Frontiers in Bioscience, vol. 17, no. 1, pp. 100–128, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Ejtehadifar, K. Shamsasenjan, A. Movassaghpour et al., “The effect of hypoxia on mesenchymal stem cell biology,” Advanced Pharmaceutical Bulletin, vol. 5, no. 2, pp. 141–149, 2015. View at Publisher · View at Google Scholar
  39. M. Wagegg, T. Gaber, F. L. Lohanatha et al., “Hypoxia promotes osteogenesis but suppresses adipogenesis of human mesenchymal stromal cells in a hypoxia-inducible factor-1 dependent manner,” PLoS ONE, vol. 7, no. 9, Article ID e46483, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Idelevich, Y. Rais, and E. Monsonego-Ornan, “Bone Gla protein increases HIF-1α-dependent glucose metabolism and induces cartilage and vascular calcification,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 9, pp. e55–e71, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. K. Kim, L.-S. Gu, T. E. Bryan et al., “Mineralisation of reconstituted collagen using polyvinylphosphonic acid/polyacrylic acid templating matrix protein analogues in the presence of calcium, phosphate and hydroxyl ions,” Biomaterials, vol. 31, no. 25, pp. 6618–6627, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. F. Langenbach, C. Naujoks, P. V. Kersten-Thiele et al., “Osteogenic differentiation influences stem cell migration out of scaffold-free microspheres,” Tissue Engineering Part A, vol. 16, no. 2, pp. 759–766, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. M. A. Scott, B. Levi, A. Askarinam et al., “Brief review of models of ectopic bone formation,” Stem Cells and Development, vol. 21, no. 5, pp. 655–667, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. P. A. Janmey, J. P. Winer, and J. W. Weisel, “Fibrin gels and their clinical and bioengineering applications,” Journal of the Royal Society Interface, vol. 6, no. 30, pp. 1–10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Jaquiéry, S. Schaeren, J. Farhadi et al., “In vitro osteogenic differentiation and in vivo bone-forming capacity of human isogenic jaw periosteal cells and bone marrow stromal cells,” Annals of Surgery, vol. 242, no. 6, pp. 859–868, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Sasaki, T. Matsumoto, and S. Imazato, “Oriented bone formation using biomimetic fibrin hydrogels with three-dimensional patterned bone matrices,” Journal of Biomedical Materials Research Part A, vol. 103, no. 2, pp. 622–627, 2015. View at Publisher · View at Google Scholar
  47. F. Long, “Building strong bones: molecular regulation of the osteoblast lineage,” Nature Reviews Molecular Cell Biology, vol. 13, no. 1, pp. 27–38, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Zhong, K. L. Watts, J. L. Gori et al., “Safeguarding nonhuman primate iPS cells with suicide genes,” Molecular Therapy, vol. 19, no. 9, pp. 1667–1675, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. J. W. Weisel, “Fibrinogen and fibrin,” Advances in Protein Chemistry, vol. 70, pp. 247–299, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Kaigler, Z. Wang, K. Horger, D. J. Mooney, and P. H. Krebsbach, “VEGF scaffolds enhance angiogenesis and bone regeneration in irradiated osseous defects,” Journal of Bone and Mineral Research, vol. 21, no. 5, pp. 735–744, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Bentmann, N. Kawelke, D. Moss et al., “Circulating fibronectin affects bone matrix, whereas osteoblast fibronectin modulates osteoblast function,” Journal of Bone and Mineral Research, vol. 25, no. 4, pp. 706–715, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. V. Terraube, I. Marx, and C. V. Denis, “Role of von Willebrand factor in tumor metastasis,” Thrombosis Research, vol. 120, no. 2, pp. S64–S70, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. A. von Au, M. Vasel, S. Kraft et al., “Circulating fibronectin controls tumor growth,” Neoplasia, vol. 15, no. 8, pp. 925–938, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Hayashi, H. Misawa, H. Nakahara et al., “Transplantation of osteogenically differentiated mouse iPS cells for bone repair,” Cell Transplantation, vol. 21, no. 2-3, pp. 591–600, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Cheng, Q. Ke, F. Chen et al., “Protecting against wayward human induced pluripotent stem cells with a suicide gene,” Biomaterials, vol. 33, no. 11, pp. 3195–3204, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. M.-O. Lee, S. H. Moon, H.-C. Jeong et al., “Inhibition of pluripotent stem cell-derived teratoma formation by small molecules,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 35, pp. E3281–E3290, 2013. View at Publisher · View at Google Scholar · View at Scopus