Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 1513281, 15 pages
https://doi.org/10.1155/2017/1513281
Research Article

Preferential Lineage-Specific Differentiation of Osteoblast-Derived Induced Pluripotent Stem Cells into Osteoprogenitors

1Eastern Virginia Medical School, W. Olney Road, Norfolk, VA, USA
2Institute of Regenerative Medicine, LifeNet Health, Concert Drive, Virginia Beach, VA, USA
3School of Medical Diagnostic and Translational Sciences, College of Health Sciences, Old Dominion University, Monarch Way, Norfolk, VA, USA

Correspondence should be addressed to Patrick C. Sachs; ude.udo@shcasp

Received 31 August 2016; Revised 18 November 2016; Accepted 4 December 2016; Published 30 January 2017

Academic Editor: Mitsuo Ochi

Copyright © 2017 Casey L. Roberts 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. A. LoGuidice, A. Houlihan, and R. Deans, “Multipotent adult progenitor cells on an allograft scaffold facilitate the bone repair process,” Journal of Tissue Engineering, vol. 7, 2016. View at Publisher · View at Google Scholar
  2. D. B. Musante, M. E. Firtha, B. L. Atkinson, R. Hahn, J. T. Ryaby, and R. J. Linovitz, “Clinical evaluation of an allogeneic bone matrix containing viable osteogenic cells in patients undergoing one- and two-level posterolateral lumbar arthrodesis with decompressive laminectomy,” Journal of Orthopaedic Surgery and Research, vol. 11, no. 1, article 63, 2016. View at Publisher · View at Google Scholar
  3. J. Vanichkachorn, T. Peppers, D. Bullard, S. K. Stanley, R. J. Linovitz, and J. T. Ryaby, “A prospective clinical and radiographic 12-month outcome study of patients undergoing single-level anterior cervical discectomy and fusion for symptomatic cervical degenerative disc disease utilizing a novel viable allogeneic, cancellous, bone matrix (trinity evolution™) with a comparison to historical controls,” European Spine Journal, vol. 25, no. 7, pp. 2233–2238, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. D. P. Lennon, M. D. Schluchter, and A. I. Caplan, “The effect of extended first passage culture on the proliferation and differentiation of human marrow derived mesenchymal stem cells,” Stem Cells Translational Medicine, vol. 1, no. 4, pp. 279–288, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Mareschi, I. Ferrero, D. Rustichelli et al., “Expansion of mesenchymal stem cells isolated from pediatric and adult donor bone marrow,” Journal of Cellular Biochemistry, vol. 97, no. 4, pp. 744–754, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. M. A. Baxter, R. F. Wynn, S. N. Jowitt, J. E. Wraith, L. J. Fairbairn, and I. Bellantuono, “Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion,” Stem Cells, vol. 22, no. 5, pp. 675–682, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Fakhry, E. Hamade, B. Badran, R. Buchet, and D. Magne, “Molecular mechanisms of mesenchymal stem cell differentiation towards osteoblasts,” World Journal of Stem Cells, vol. 5, no. 4, pp. 136–148, 2013. View at Publisher · View at Google Scholar
  8. N. D. Spencer, J. M. Gimble, and M. J. Lopez, “Mesenchymal stromal cells: past, present, and future,” Veterinary Surgery, vol. 40, no. 2, pp. 129–139, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Hayflick, “The limited in vitro lifetime of human diploid cell strains,” Experimental Cell Research, vol. 37, no. 3, pp. 614–636, 1965. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Wernig, A. Meissner, R. Foreman et al., “In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state,” Nature, vol. 448, no. 7151, pp. 318–324, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. J. Yu, M. A. Vodyanik, K. Smuga-Otto et al., “Induced pluripotent stem cell lines derived from human somatic cells,” Science, vol. 318, no. 5858, pp. 1917–1920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. 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
  14. L. D. K. Buttery, S. Bourne, J. D. Xynos et al., “Differentiation of osteoblasts and in Vitro bone formation from murine embryonic stem cells,” Tissue Engineering, vol. 7, no. 1, pp. 89–99, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. L. A. Hidalgo-Bastida and S. H. Cartmell, “Mesenchymal stem cells, osteoblasts and extracellular matrix proteins: enhancing cell adhesion and differentiation for bone tissue engineering,” Tissue Engineering—Part B: Reviews, vol. 16, no. 4, pp. 405–412, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. J. Lengner, “IPS cell technology in regenerative medicine,” Annals of the New York Academy of Sciences, vol. 1192, pp. 38–44, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. C. J. Taylor, S. Peacock, A. N. Chaudhry, J. A. Bradley, and E. M. Bolton, “Generating an iPSC bank for HLA-matched tissue transplantation based on known donor and recipient HLA types,” Cell Stem Cell, vol. 11, no. 2, pp. 147–152, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Solomon, F. Pitossi, and M. S. Rao, “Banking on iPSC- is it doable and is it worthwhile,” Stem Cell Reviews and Reports, vol. 11, no. 1, pp. 1–10, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. P.-A. Gourraud, L. Gilson, M. Girard, and M. Peschanski, “The role of human leukocyte antigen matching in the development of multiethnic ‘haplobank’ of induced pluripotent stem cell lines,” Stem Cells, vol. 30, no. 2, pp. 180–186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Okita, Y. Matsumura, Y. Sato et al., “A more efficient method to generate integration-free human iPS cells,” Nature Methods, vol. 8, no. 5, pp. 409–412, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Kim, C.-H. Kim, J.-I. Moon et al., “Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins,” Cell Stem Cell, vol. 4, no. 6, pp. 472–476, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. P. A. Goh, S. Caxaria, C. Casper et al., “A systematic evaluation of integration free reprogramming methods for deriving clinically relevant patient specific induced pluripotent stem (iPS) cells,” PLoS ONE, vol. 8, no. 11, Article ID e81622, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. N. Fusaki, H. Ban, A. Nishiyama, K. Saeki, and M. Hasegawa, “Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome,” Proceedings of the Japan Academy Series B: Physical and Biological Sciences, vol. 85, no. 8, pp. 348–362, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Fergus, R. Quintanilla, and U. Lakshmipathy, “Characterizing pluripotent stem cells using the TaqMan® hPSC scorecard™ panel,” Methods in Molecular Biology, vol. 1307, pp. 25–37, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. S. B. Lee, D. Seo, D. Choi et al., “Contribution of hepatic lineage stage-specific donor memory to the differential potential of induced mouse pluripotent stem cells,” Stem Cells, vol. 30, no. 5, pp. 997–1007, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. S. P. Medvedev, E. A. Pokushalov, and S. M. Zakian, “Epigenetics of pluripotent cells,” Acta Naturae, vol. 4, no. 4, pp. 28–46, 2012. View at Google Scholar
  27. S. Yamanaka, “Induced pluripotent stem cells: past, present, and future,” Cell Stem Cell, vol. 10, no. 6, pp. 678–684, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Nishizawa, K. Chonabayashi, M. Nomura et al., “Epigenetic variation between human induced pluripotent stem cell lines is an indicator of differentiation capacity,” Cell Stem Cell, vol. 19, no. 3, pp. 341–354, 2016. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Kim, A. Doi, B. Wen et al., “Epigenetic memory in induced pluripotent stem cells,” Nature, vol. 467, no. 7313, pp. 285–290, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. O. Bar-Nur, H. A. Russ, S. Efrat, and N. Benvenisty, “Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells,” Cell Stem Cell, vol. 9, no. 1, pp. 17–23, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. R. Rizzi, E. Di Pasquale, P. Portararo et al., “Post-natal cardiomyocytes can generate iPS cells with an enhanced capacity toward cardiomyogenic re-differentation,” Cell Death and Differentiation, vol. 19, no. 7, pp. 1162–1174, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. G. J. Sullivan, Y. Bai, J. Fletcher, and I. Wilmut, “Induced pluripotent stem cells: epigenetic memories and practical implications,” Molecular Human Reproduction, vol. 16, no. 12, pp. 880–885, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Szpalski, M. Barbaro, F. Sagebin, and S. M. Warren, “Bone tissue engineering: current strategies and techniques—part II: cell types,” Tissue Engineering Part B: Reviews, vol. 18, no. 4, pp. 258–269, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Spencer, M. Keramari, and C. M. Ward, “Using cadherin expression to assess spontaneous differentiation of embryonic stem cells,” Methods in Molecular Biology, vol. 690, pp. 81–94, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. C. E. P. Aronin and R. S. Tuan, “Therapeutic potential of the immunomodulatory activities of adult mesenchymal stem cells,” Birth Defects Research Part C - Embryo Today: Reviews, vol. 90, no. 1, pp. 67–74, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Hynes, D. Menicanin, K. Mrozik, S. Gronthos, and P. M. Bartold, “Generation of functional mesenchymal stem cells from different induced pluripotent stem cell lines,” Stem Cells and Development, vol. 23, no. 10, pp. 1084–1096, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Teng, C. Liu, C. Krettek, and M. Jagodzinski, “The application of induced pluripotent stem cells for bone regeneration: current progress and prospects,” Tissue Engineering - Part B: Reviews, vol. 20, no. 4, pp. 328–339, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Kang, Y. Zhou, S. Tan et al., “Mesenchymal stem cells derived from human induced pluripotent stem cells retain adequate osteogenicity and chondrogenicity but less adipogenicity,” Stem Cell Research and Therapy, vol. 6, no. 1, article no. 144, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. M. P. Francis, P. C. Sachs, L. W. Elmore, and S. E. Holt, “Isolating adipose-derived mesenchymal stem cells from lipoaspirate blood and saline fraction,” Organogenesis, vol. 6, no. 1, pp. 11–14, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. A. J. Katz, A. Tholpady, S. S. Tholpady, H. Shang, and R. C. Ogle, “Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells,” Stem Cells, vol. 23, no. 3, pp. 412–423, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. P. C. Sachs, M. P. Francis, M. Zhao et al., “Defining essential stem cell characteristics in adipose-derived stromal cells extracted from distinct anatomical sites,” Cell and Tissue Research, vol. 349, no. 2, pp. 505–515, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. H. K. Salem and C. Thiemermann, “Mesenchymal stromal cells: current understanding and clinical status,” Stem Cells, vol. 28, no. 3, pp. 585–596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Zanotti and E. Canalis, “Notch1 and Notch2 expression in osteoblast precursors regulates femoral microarchitecture,” Bone, vol. 62, pp. 22–28, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Yorgan, N. Vollersen, C. Riedel et al., “Osteoblast-specific Notch2 inactivation causes increased trabecular bone mass at specific sites of the appendicular skeleton,” Bone, vol. 87, pp. 136–146, 2016. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Siersbæk, R. Nielsen, and S. Mandrup, “PPARγ in adipocyte differentiation and metabolism—novel insights from genome-wide studies,” FEBS Letters, vol. 584, no. 15, pp. 3242–3249, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Chen, X. Chen, M. Li et al., “Hierarchical Oct4 binding in concert with primed epigenetic rearrangements during somatic cell reprogramming,” Cell Reports, vol. 14, no. 6, pp. 1540–1554, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Raab, M. Klingenstein, S. Liebau, and L. Linta, “A comparative view on human somatic cell sources for iPSC generation,” Stem Cells International, vol. 2014, Article ID 768391, 12 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Streckfuss-Bömeke, F. Wolf, A. Azizian et al., “Comparative study of human-induced pluripotent stem cells derived from bone marrow cells, hair keratinocytes, and skin fibroblasts,” European Heart Journal, vol. 34, no. 33, pp. 2618–2629, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. A. M. Soto and C. Sonnenschein, “The tissue organization field theory of cancer: a testable replacement for the somatic mutation theory,” BioEssays, vol. 33, no. 5, pp. 332–340, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. A. M. Soto and C. Sonnenschein, “The somatic mutation theory of cancer: growing problems with the paradigm?” BioEssays, vol. 26, no. 10, pp. 1097–1107, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Hayflick and P. S. Moorhead, “The serial cultivation of human diploid cell strains,” Experimental Cell Research, vol. 25, no. 3, pp. 585–621, 1961. View at Publisher · View at Google Scholar · View at Scopus