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Stem Cells International
Volume 2019, Article ID 8469012, 13 pages
https://doi.org/10.1155/2019/8469012
Research Article

Spontaneously Formed Spheroids from Mouse Compact Bone-Derived Cells Retain Highly Potent Stem Cells with Enhanced Differentiation Capability

1Department of Hard Tissue Research, Graduate School of Oral Medicine, Matsumoto Dental University, Shiojiri 399-0781, Japan
2Department of Oral and Maxillofacial Surgery, School of Dentistry, Matsumoto Dental University, Shiojiri 399-0781, Japan
3Institute for Oral Science, Matsumoto Dental University, Shiojiri 399-0781, Japan
4Department of Stomatology, Shanghai Tenth People’s Hospital, Tongji University School of Medicine, Shanghai 200072, China
5Department of General Medicine, IMSUT Hospital, Institute of Medical Science, University of Tokyo, Tokyo 108-8639, Japan

Correspondence should be addressed to Hideaki Kagami; pj.ca.udm@imagak.ikaedih

Received 19 October 2018; Revised 26 February 2019; Accepted 10 March 2019; Published 5 May 2019

Guest Editor: Tiago Fernandes

Copyright © 2019 Kai Chen 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. Y. Yamada, S. Nakamura, K. Ito et al., “Injectable bone tissue engineering using expanded mesenchymal stem cells,” Stem Cells, vol. 31, no. 3, pp. 572–580, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Kagami, H. Agata, M. Inoue et al., “The use of bone marrow stromal cells (bone marrow-derived multipotent mesenchymal stromal cells) for alveolar bone tissue engineering: basic science to clinical translation,” Tissue Engineering Part B: Reviews, vol. 20, no. 3, pp. 229–232, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Yamaguchi, J. Ohno, A. Sato, H. Kido, and T. Fukushima, “Mesenchymal stem cell spheroids exhibit enhanced in-vitro and in-vivo osteoregenerative potential,” BMC Biotechnology, vol. 14, no. 1, p. 105, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. Z. Cesarz and K. Tamama, “Spheroid culture of mesenchymal stem cells,” Stem Cells International, vol. 2016, Article ID 9176357, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  5. W. J. C. Rombouts and R. E. Ploemacher, “Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture,” Leukemia, vol. 17, no. 1, pp. 160–170, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Stenderup, J. Justesen, C. Clausen, and M. Kassem, “Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells,” Bone, vol. 33, no. 6, pp. 919–926, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Banfi, A. Muraglia, B. Dozin, M. Mastrogiacomo, R. Cancedda, and R. Quarto, “Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy,” Experimental Hematology, vol. 28, no. 6, pp. 707–715, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. F. Sugiura, H. Kitoh, and N. Ishiguro, “Osteogenic potential of rat mesenchymal stem cells after several passages,” Biochemical and Biophysical Research Communications, vol. 316, no. 1, pp. 233–239, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Agata, I. Asahina, N. Watanabe et al., “Characteristic change and loss of in vivo osteogenic abilities of human bone marrow stromal cells during passage,” Tissue Engineering Part A, vol. 16, no. 2, pp. 663–673, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Abbott, “Cell culture: Biology’s new dimension,” Nature, vol. 424, no. 6951, pp. 870–872, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Levenberg, N. F. Huang, E. Lavik, A. B. Rogers, J. Itskovitz-Eldor, and R. Langer, “Differentiation of human embryonic stem cells on three-dimensional polymer scaffolds,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 22, pp. 12741–12746, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. J. E. Frith, B. Thomson, and P. G. Genever, “Dynamic three-dimensional culture methods enhance mesenchymal stem cell properties and increase therapeutic potential,” Tissue Engineering Part C: Methods, vol. 16, no. 4, pp. 735–749, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. J. H. Ylostalo, T. J. Bartosh, A. Tiblow, and D. J. Prockop, “Unique characteristics of human mesenchymal stromal/progenitor cells pre-activated in 3-dimensional cultures under different conditions,” Cytotherapy, vol. 16, no. 11, pp. 1486–1500, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. B. N. Cavalcanti, B. D. Zeitlin, and J. E. Nör, “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
  15. J. De Waele, K. Reekmans, J. Daans, H. Goossens, Z. Berneman, and P. Ponsaerts, “3D culture of murine neural stem cells on decellularized mouse brain sections,” Biomaterials, vol. 41, pp. 122–131, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. B. A. Reynolds and S. Weiss, “Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system,” Science, vol. 255, no. 5052, pp. 1707–1710, 1992. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Lois and A. Alvarez-Buylla, “Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 5, pp. 2074–2077, 1993. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Gritti, E. A. Parati, L. Cova et al., “Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor,” The Journal of Neuroscience, vol. 16, no. 3, pp. 1091–1100, 1996. View at Publisher · View at Google Scholar
  19. L. J. Richards, T. J. Kilpatrick, and P. F. Bartlett, “De novo generation of neuronal cells from the adult mouse brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 18, pp. 8591–8595, 1992. View at Publisher · View at Google Scholar · View at Scopus
  20. T. J. Bartosh and J. H. Ylostalo, “Preparation of anti-inflammatory mesenchymal stem/precursor cells (MSCs) through sphere formation using hanging-drop culture technique,” Current Protocols in Stem Cell Biology, vol. 28, no. 1, pp. 2B.6.1–2B.6.23, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. S. I. Lee, Y. Ko, and J. B. Park, “Evaluation of the osteogenic differentiation of gingiva-derived stem cells grown on culture plates or in stem cell spheroids: comparison of two- and three-dimensional cultures,” Experimental and Therapeutic Medicine, vol. 14, no. 3, pp. 2434–2438, 2017. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Kanao, N. Ogura, K. Takahashi et al., “Capacity of human dental follicle cells to differentiate into neural cells in vitro,” Stem Cells International, vol. 2017, Article ID 8371326, 10 pages, 2017. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Belicchi, F. Pisati, R. Lopa et al., “Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain,” Journal of Neuroscience Research, vol. 77, no. 4, pp. 475–486, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Mueller-Klieser, “Three-dimensional cell cultures: from molecular mechanisms to clinical applications,” American Journal of Physiology-Cell Physiology, vol. 273, no. 4, pp. C1109–C1123, 1997. View at Publisher · View at Google Scholar
  25. T. M. Achilli, J. Meyer, and J. R. Morgan, “Advances in the formation, use and understanding of multi-cellular spheroids,” Expert Opinion on Biological Therapy, vol. 12, no. 10, pp. 1347–1360, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. A. C. Tsai, Y. Liu, X. Yuan, and T. Ma, “Compaction, fusion, and functional activation of three-dimensional human mesenchymal stem cell aggregate,” Tissue Engineering Part A, vol. 21, no. 9-10, pp. 1705–1719, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. X. Li, N. Li, K. Chen, S. Nagasawa, M. Yoshizawa, and H. Kagami, “Around 90° contact angle of dish surface is a key factor in achieving spontaneous spheroid formation,” Tissue Engineering Part C: Methods, vol. 24, no. 10, pp. 578–584, 2018. View at Publisher · View at Google Scholar · View at Scopus
  28. W. Mueller-Klieser, “Multicellular spheroids. A review on cellular aggregates in cancer research,” Journal of Cancer Research and Clinical Oncology, vol. 113, no. 2, pp. 101–122, 1987. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Foty, “A simple hanging drop cell culture protocol for generation of 3D spheroids,” Journal of Visualized Experiments, vol. 6, no. 51, article e2720, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. Kelm and M. Fussenegger, “Microscale tissue engineering using gravity-enforced cell assembly,” Trends in Biotechnology, vol. 22, no. 4, pp. 195–202, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Zhang, X. Li, T. Chihara et al., “Comparing immunocompetent and immunodeficient mice as animal models for bone tissue engineering,” Oral Diseases, vol. 21, no. 5, pp. 583–592, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Zhu, Z. K. Guo, X. X. Jiang et al., “A protocol for isolation and culture of mesenchymal stem cells from mouse compact bone,” Nature Protocols, vol. 5, no. 3, pp. 550–560, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Cai, T. Liu, F. Fang, C. Xiong, and S. Shen, “Comparisons of mouse mesenchymal stem cells in primary adherent culture of compact bone fragments and whole bone marrow,” Stem Cells International, vol. 2015, Article ID 708906, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Corradetti, F. Taraballi, S. Powell et al., “Osteoprogenitor cells from bone marrow and cortical bone: understanding how the environment affects their fate,” Stem Cells and Development, vol. 24, no. 9, pp. 1112–1123, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. J. S. Fernandez-Moure, B. Corradetti, P. Chan et al., “Enhanced osteogenic potential of mesenchymal stem cells from cortical bone: a comparative analysis,” Stem Cell Research & Therapy, vol. 6, no. 1, p. 203, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Blashki, M. B. Murphy, M. Ferrari, P. J. Simmons, and E. Tasciotti, “Mesenchymal stem cells from cortical bone demonstrate increased clonal incidence, potency, and developmental capacity compared to their bone marrow–derived counterparts,” Journal of Tissue Engineering, vol. 7, 2016. View at Publisher · View at Google Scholar
  37. Y. Moritani, M. Usui, K. Sano et al., “Spheroid culture enhances osteogenic potential of periodontal ligament mesenchymal stem cells,” Journal of Periodontal Research, vol. 53, no. 5, pp. 870–882, 2018. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Guo, Y. Zhou, S. Wang, and Y. Wu, “Epigenetic changes of mesenchymal stem cells in three-dimensional (3D) spheroids,” Journal of Cellular and Molecular Medicine, vol. 18, no. 10, pp. 2009–2019, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Guo, R. C. H. Zhao, and Y. Wu, “The role of microRNAs in self-renewal and differentiation of mesenchymal stem cells,” Experimental Hematology, vol. 39, no. 6, pp. 608–616, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. T. H. Cheung, N. L. Quach, G. W. Charville et al., “Maintenance of muscle stem-cell quiescence by microRNA-489,” Nature, vol. 482, no. 7386, pp. 524–528, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Drela, A. Sarnowska, P. Siedlecka et al., “Low oxygen atmosphere facilitates proliferation and maintains undifferentiated state of umbilical cord mesenchymal stem cells in an hypoxia inducible factor-dependent manner,” Cytotherapy, vol. 16, no. 7, pp. 881–892, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Okada, H. Nakauchi, K. Nagayoshi, S. Nishikawa, Y. Miura, and T. Suda, “In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells,” Blood, vol. 80, no. 12, pp. 3044–3050, 1992. View at Google Scholar
  43. G. J. Spangrude, S. Heimfeld, and I. Weissman, “Purification and characterization of mouse hematopoietic stem cells,” Science, vol. 241, no. 4861, pp. 58–62, 1988. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Matsuura, T. Nagai, N. Nishigaki et al., “Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes,” Journal of Biological Chemistry, vol. 279, no. 12, pp. 11384–11391, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. T. J. Bartosh, J. H. Ylostalo, A. Mohammadipoor et al., “Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 31, pp. 13724–13729, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. N. C. Cheng, S. Y. Chen, J. R. Li, and T. H. Young, “Short-term spheroid formation enhances the regenerative capacity of adipose-derived stem cells by promoting stemness, angiogenesis, and chemotaxis,” Stem Cells Translational Medicine, vol. 2, no. 8, pp. 584–594, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. N. C. Cheng, S. Wang, and T. H. Young, “The influence of spheroid formation of human adipose-derived stem cells on chitosan films on stemness and differentiation capabilities,” Biomaterials, vol. 33, no. 6, pp. 1748–1758, 2012. View at Publisher · View at Google Scholar · View at Scopus