Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2018, Article ID 8642989, 17 pages
https://doi.org/10.1155/2018/8642989
Review Article

Direct Control of Stem Cell Behavior Using Biomaterials and Genetic Factors

1Division of Cardiology, Severance Cardiovascular Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea
2Severance Biomedical Science Institute, College of Medicine, Yonsei University, Seoul, Republic of Korea
3Department of Obstetrics and Gynecology, Yonsei University College of Medicine, Seoul, Republic of Korea
4Department of Orthopaedic Surgery, Yonsei University College of Medicine, Seoul 120-752, Republic of Korea
5Department of Laboratory Medicine, Yonsei University College of Medicine, Seoul, Republic of Korea
6Department of Mechanical Engineering, Georgia Institute of Technology, Atlanta, GA, USA

Correspondence should be addressed to Hak-Joon Sung; ca.shuy@gnus27jh

Received 2 December 2017; Revised 5 February 2018; Accepted 4 April 2018; Published 10 May 2018

Academic Editor: Açelya Yilmazer

Copyright © 2018 Jeong-Kee Yoon 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. O. Ringdén, M. Uzunel, I. Rasmusson et al., “Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease,” Transplantation, vol. 81, no. 10, pp. 1390–1397, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. D. Polchert, J. Sobinsky, G. Douglas et al., “IFN-γ activation of mesenchymal stem cells for treatment and prevention of graft versus host disease,” European Journal of Immunology, vol. 38, no. 6, pp. 1745–1755, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Yanez, M. L. Lamana, J. Garcia-Castro, I. Colmenero, M. Ramirez, and J. A. Bueren, “Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease,” Stem Cells, vol. 24, no. 11, pp. 2582–2591, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. E. J. Koay and K. A. Athanasiou, “Development of serum-free, chemically defined conditions for human embryonic stem cell–derived fibrochondrogenesis,” Tissue Engineering Part A, vol. 15, no. 8, pp. 2249–2257, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. L. A. Solchaga, K. Penick, J. D. Porter, V. M. Goldberg, A. I. Caplan, and J. F. Welter, “FGF-2 enhances the mitotic and chondrogenic potentials of human adult bone marrow-derived mesenchymal stem cells,” Journal of Cellular Physiology, vol. 203, no. 2, pp. 398–409, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Tsutsumi, A. Shimazu, K. Miyazaki et al., “Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF,” Biochemical and Biophysical Research Communications, vol. 288, no. 2, pp. 413–419, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. D. James, A. J. Levine, D. Besser, and A. Hemmati-Brivanlou, “TGFβ/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells,” Development, vol. 132, no. 6, pp. 1273–1282, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Sakaki-Yumoto, Y. Katsuno, and R. Derynck, “TGF-β family signaling in stem cells,” Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1830, no. 2, pp. 2280–2296, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. H. M. van Beuningen, H. L. Glansbeek, P. M. van der Kraan, and W. B. van den Berg, “Differential effects of local application of BMP-2 or TGF-β1 on both articular cartilage composition and osteophyte formation,” Osteoarthritis and Cartilage, vol. 6, no. 5, pp. 306–317, 1998. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Z. Sailor, R. M. Hewick, and E. A. Morris, “Recombinant human bone morphogenetic protein-2 maintains the articular chondrocyte phenotype in long-term culture,” Journal of Orthopaedic Research, vol. 14, no. 6, pp. 937–945, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. C. A. Hellingman, W. Koevoet, N. Kops et al., “Fibroblast growth factor receptors in in vitro and in vivo chondrogenesis: relating tissue engineering using adult mesenchymal stem cells to embryonic development,” Tissue Engineering Part A, vol. 16, no. 2, pp. 545–556, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. A. De Becker and I. Van Riet, “Homing and migration of mesenchymal stromal cells: how to improve the efficacy of cell therapy?” World Journal of Stem Cells, vol. 8, no. 3, pp. 73–87, 2016. View at Publisher · View at Google Scholar
  13. H. M. Lazarus, S. E. Haynesworth, S. L. Gerson, N. S. Rosenthal, and A. I. Caplan, “Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use,” Bone Marrow Transplantation, vol. 16, no. 4, pp. 557–564, 1995. View at Google Scholar
  14. S. P. Bruder, N. Jaiswal, and S. E. Haynesworth, “Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation,” Journal of Cellular Biochemistry, vol. 64, no. 2, pp. 278–294, 1997. View at Publisher · View at Google Scholar
  15. K. Ksiazek, “A comprehensive review on mesenchymal stem cell growth and senescence,” Rejuvenation Research, vol. 12, no. 2, pp. 105–116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Lam, S. Lu, E. J. Lee et al., “Osteochondral defect repair using bilayered hydrogels encapsulating both chondrogenically and osteogenically pre-differentiated mesenchymal stem cells in a rabbit model,” Osteoarthritis and Cartilage, vol. 22, no. 9, pp. 1291–1300, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. F. Barry, R. E. Boynton, B. Liu, and J. M. Murphy, “Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components,” Experimental Cell Research, vol. 268, no. 2, pp. 189–200, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. H. J. Lee, B. H. Choi, B. H. Min, and S. R. Park, “Low-intensity ultrasound inhibits apoptosis and enhances viability of human mesenchymal stem cells in three-dimensional alginate culture during chondrogenic differentiation,” Tissue Engineering, vol. 13, no. 5, pp. 1049–1057, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Park, K. J. Cho, J. J. Kim, I. H. Kim, and D. K. Han, “Functional PLGA scaffolds for chondrogenesis of bone-marrow-derived mesenchymal stem cells,” Macromolecular Bioscience, vol. 9, no. 3, pp. 221–229, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Padilla, R. Puts, L. Vico, A. Guignandon, and K. Raum, “Stimulation of bone repair with ultrasound,” Advances in Experimental Medicine and Biology, vol. 880, pp. 385–427, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. R. T. Brady, F. J. O'Brien, and D. A. Hoey, “Mechanically stimulated bone cells secrete paracrine factors that regulate osteoprogenitor recruitment, proliferation, and differentiation,” Biochemical and Biophysical Research Communications, vol. 459, no. 1, pp. 118–123, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. M. J. Go, C. Takenaka, and H. Ohgushi, “Forced expression of Sox2 or Nanog in human bone marrow derived mesenchymal stem cells maintains their expansion and differentiation capabilities,” Experimental Cell Research, vol. 314, no. 5, pp. 1147–1154, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. D. S. Yoon, Y. H. Kim, H. S. Jung, S. Paik, and J. W. Lee, “Importance of Sox2 in maintenance of cell proliferation and multipotency of mesenchymal stem cells in low-density culture,” Cell Proliferation, vol. 44, no. 5, pp. 428–440, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. T. M. Liu, Y. N. Wu, X. M. Guo, J. H. P. Hui, E. H. Lee, and B. Lim, “Effects of ectopic Nanog and Oct4 overexpression on mesenchymal stem cells,” Stem Cells and Development, vol. 18, no. 7, pp. 1013–1022, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Ranzani, D. Cesana, C. C. Bartholomae et al., “Lentiviral vector–based insertional mutagenesis identifies genes associated with liver cancer,” Nature Methods, vol. 10, no. 2, pp. 155–161, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Chen, X. Liu, W. Zhu et al., “SIRT1 ameliorates age-related senescence of mesenchymal stem cells via modulating telomere shelterin,” Frontiers in Aging Neuroscience, vol. 6, p. 103, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. D. S. Yoon, Y. Choi, Y. Jang et al., “SIRT1 directly regulates SOX2 to maintain self-renewal and multipotency in bone marrow-derived mesenchymal stem cells,” Stem Cells, vol. 32, no. 12, pp. 3219–3231, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. D. S. Yoon, Y. Choi, S. M. Choi, K. H. Park, and J. W. Lee, “Different effects of resveratrol on early and late passage mesenchymal stem cells through β-catenin regulation,” Biochemical and Biophysical Research Communications, vol. 467, no. 4, pp. 1026–1032, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Harman, “Aging: a theory based on free radical and radiation chemistry,” Journal of Gerontology, vol. 11, no. 3, pp. 298–300, 1956. View at Publisher · View at Google Scholar
  30. W. Zhu, J. Chen, X. Cong, S. Hu, and X. Chen, “Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells,” Stem Cells, vol. 24, no. 2, pp. 416–425, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Sart, L. Song, and Y. Li, “Controlling redox status for stem cell survival, expansion, and differentiation,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 105135, 14 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. Y.-J. Surh, J. Kundu, and H.-K. Na, “Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals,” Planta Medica, vol. 74, no. 13, pp. 1526–1539, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Zhu, L. Zhang, K. Itoh et al., “Nrf2 controls bone marrow stromal cell susceptibility to oxidative and electrophilic stress,” Free Radical Biology & Medicine, vol. 41, no. 1, pp. 132–143, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Nemoto, M. M. Fergusson, and T. Finkel, “Nutrient availability regulates SIRT1 through a forkhead-dependent pathway,” Science, vol. 306, no. 5704, pp. 2105–2108, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. D. S. Yoon, Y. Choi, and J. W. Lee, “Cellular localization of NRF2 determines the self-renewal and osteogenic differentiation potential of human MSCs via the P53–SIRT1 axis,” Cell Death & Disease, vol. 7, no. 2, article e2093, 2016. View at Publisher · View at Google Scholar · View at Scopus
  36. N. Z. Kuhn and R. S. Tuan, “Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis,” Journal of Cellular Physiology, vol. 222, no. 2, pp. 268–277, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. M. F. Brizzi, G. Tarone, and P. Defilippi, “Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche,” Current Opinion in Cell Biology, vol. 24, no. 5, pp. 645–651, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. S. r. Pattabhi, J. S. Martinez, and T. C. S. Keller III, “Decellularized ECM effects on human mesenchymal stem cell stemness and differentiation,” Differentiation, vol. 88, no. 4-5, pp. 131–143, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Xiong, J. He, W. Zhang, G. Zhou, Y. Cao, and W. Liu, “Retention of the stemness of mouse adipose-derived stem cells by their expansion on human bone marrow stromal cell-derived extracellular matrix,” Tissue Engineering Part A, vol. 21, no. 11-12, pp. 1886–1894, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Rakian, T. J. Block, S. M. Johnson et al., “Native extracellular matrix preserves mesenchymal stem cell “stemness” and differentiation potential under serum-free culture conditions,” Stem Cell Research & Therapy, vol. 6, no. 1, p. 235, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Antebi, Z. Zhang, Y. Wang, Z. Lu, X. D. Chen, and J. Ling, “Stromal-cell-derived extracellular matrix promotes the proliferation and retains the osteogenic differentiation capacity of mesenchymal stem cells on three-dimensional scaffolds,” Tissue Engineering Part C: Methods, vol. 21, no. 2, pp. 171–181, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Zhang, B. Li, and J. H.-C. Wang, “The role of engineered tendon matrix in the stemness of tendon stem cells in vitro and the promotion of tendon-like tissue formation in vivo,” Biomaterials, vol. 32, no. 29, pp. 6972–6981, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Lee, A. A. Abdeen, A. S. Kim, and K. A. Kilian, “Influence of biophysical parameters on maintaining the mesenchymal stem cell phenotype,” ACS Biomaterials Science & Engineering, vol. 1, no. 4, pp. 218–226, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Ansari, P. Sarrion, M. M. Hasani-Sadrabadi, T. Aghaloo, B. M. Wu, and A. Moshaverinia, “Regulation of the fate of dental-derived mesenchymal stem cells using engineered alginate-GelMA hydrogels,” Journal of Biomedical Materials Research Part A, vol. 105, no. 11, pp. 2957–2967, 2017. View at Publisher · View at Google Scholar · View at Scopus
  45. K. C. Rustad, V. W. Wong, M. Sorkin et al., “Enhancement of mesenchymal stem cell angiogenic capacity and stemness by a biomimetic hydrogel scaffold,” Biomaterials, vol. 33, no. 1, pp. 80–90, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. H.-W. Chien, S.-W. Fu, A.-Y. Shih, and W.-B. Tsai, “Modulation of the stemness and osteogenic differentiation of human mesenchymal stem cells by controlling RGD concentrations of poly(carboxybetaine) hydrogel,” Biotechnology Journal, vol. 9, no. 12, pp. 1613–1623, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. R. J. McMurray, N. Gadegaard, P. M. Tsimbouri et al., “Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency,” Nature Materials, vol. 10, no. 8, pp. 637–644, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Zhao, J. J. Veldhuis, Y. Duan et al., “Low oxygen tension and synthetic nanogratings improve the uniformity and stemness of human mesenchymal stem cell layer,” Molecular Therapy, vol. 18, no. 5, pp. 1010–1018, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. K. S. Park, J. Ahn, J. Y. Kim, H. Park, H. O. Kim, and S. H. Lee, “Poly-L-lysine increases the ex vivo expansion and erythroid differentiation of human hematopoietic stem cells, as well as erythroid enucleation efficacy,” Tissue Engineering Part A, vol. 20, no. 5-6, pp. 1072–1080, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. J. S. Heo, H. O. Kim, S. Y. Song, D. H. Lew, Y. Choi, and S. Kim, “Poly-L-lysine prevents senescence and augments growth in culturing mesenchymal stem cells ex vivo,” BioMed Research International, vol. 2016, Article ID 8196078, 13 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  51. L. H. Hofmeister, L. Costa, D. A. Balikov et al., “Patterned polymer matrix promotes stemness and cell-cell interaction of adult stem cells,” Journal of Biological Engineering, vol. 9, no. 1, p. 18, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. D. A. Balikov, S. W. Crowder, T. C. Boire et al., “Tunable surface repellency maintains stemness and redox capacity of human mesenchymal stem cells,” ACS Applied Materials & Interfaces, vol. 9, no. 27, pp. 22994–23006, 2017. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Nejati-Koshki, Y. Pilehvar-Soltanahmadi, E. Alizadeh, A. Ebrahimi-Kalan, Y. Mortazavi, and N. Zarghami, “Development of Emu oil-loaded PCL/collagen bioactive nanofibers for proliferation and stemness preservation of human adipose-derived stem cells: possible application in regenerative medicine,” Drug Development and Industrial Pharmacy, vol. 43, no. 12, pp. 1978–1988, 2017. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Pandolfi, N. T. Furman, X. Wang et al., “A nanofibrous electrospun patch to maintain human mesenchymal cell stemness,” Journal of Materials Science: Materials in Medicine, vol. 28, no. 3, p. 44, 2017. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Pilehvar-Soltanahmadi, M. Nouri, M. M. Martino et al., “Cytoprotection, proliferation and epidermal differentiation of adipose tissue-derived stem cells on emu oil based electrospun nanofibrous mat,” Experimental Cell Research, vol. 357, no. 2, pp. 192–201, 2017. View at Publisher · View at Google Scholar · View at Scopus
  56. 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
  57. T. Taguchi, J. Y. Cho, J. Hao, Y. S. Nout-Lomas, K. S. Kang, and D. J. Griffon, “Influence of hypoxia on the stemness of umbilical cord matrix-derived mesenchymal stem cells cultured on chitosan films,” Journal of Biomedical Materials Research Part B: Applied Biomaterials, vol. 106, no. 2, pp. 501–511, 2018. View at Publisher · View at Google Scholar · View at Scopus
  58. J. L. Robinson, M. A. P. McEnery, H. Pearce et al., “Osteoinductive PolyHIPE foams as injectable bone grafts,” Tissue Engineering Part A, vol. 22, no. 5-6, pp. 403–414, 2016. View at Publisher · View at Google Scholar · View at Scopus
  59. S. W. Crowder, D. Prasai, R. Rath et al., “Three-dimensional graphene foams promote osteogenic differentiation of human mesenchymal stem cells,” Nanoscale, vol. 5, no. 10, pp. 4171–4176, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Lee, A. A. Abdeen, and K. A. Kilian, “Rewiring mesenchymal stem cell lineage specification by switching the biophysical microenvironment,” Scientific Reports, vol. 4, no. 1, p. 5188, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Olivares-Navarrete, E. M. Lee, K. Smith et al., “Substrate stiffness controls osteoblastic and condrocytic differentiation of mesenchymal stem cells without exogenous stimuli,” PLoS One, vol. 12, no. 1, article e0170312, 2017. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Islam, M. Younesi, T. Mbimba, and O. Akkus, “Collagen substrate stiffness anisotropy affects cellular elongation, nuclear shape, and stem cell fate toward anisotropic tissue lineage,” Advanced Healthcare Materials, vol. 5, no. 17, pp. 2237–2247, 2016. View at Publisher · View at Google Scholar · View at Scopus
  63. S. H. Lee, Y. Lee, Y. W. Chun et al., “In situ crosslinkable gelatin hydrogels for vasculogenic induction and delivery of mesenchymal stem cells,” Advanced Functional Materials, vol. 24, no. 43, pp. 6771–6781, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. G. Zhang, C. T. Drinnan, L. R. Geuss, and L. J. Suggs, “Vascular differentiation of bone marrow stem cells is directed by a tunable three-dimensional matrix,” Acta Biomaterialia, vol. 6, no. 9, pp. 3395–3403, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. T. D. Ross, B. G. Coon, S. Yun et al., “Integrins in mechanotransduction,” Current Opinion in Cell Biology, vol. 25, no. 5, pp. 613–618, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Y. Tay, H. Yu, M. Pal et al., “Micropatterned matrix directs differentiation of human mesenchymal stem cells towards myocardial lineage,” Experimental Cell Research, vol. 316, no. 7, pp. 1159–1168, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Lee, A. A. Abdeen, D. Zhang, and K. A. Kilian, “Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition,” Biomaterials, vol. 34, no. 33, pp. 8140–8148, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. M. P. Alfaro, S. Saraswati, and P. P. Young, “Chapter two - molecular mediators of mesenchymal stem cell biology,” Vitamins & Hormones, vol. 87, pp. 39–59, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Wagner, T. Kean, R. Young, J. E. Dennis, and A. I. Caplan, “Optimizing mesenchymal stem cell-based therapeutics,” Current Opinion in Biotechnology, vol. 20, no. 5, pp. 531–536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. D. A. Balikov, B. Fang, Y. W. Chun et al., “Directing lineage specification of human mesenchymal stem cells by decoupling electrical stimulation and physical patterning on unmodified graphene,” Nanoscale, vol. 8, no. 28, pp. 13730–13739, 2016. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Oh, K. S. Brammer, Y. S. J. Li et al., “Stem cell fate dictated solely by altered nanotube dimension,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 7, pp. 2130–2135, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Olivares-Navarrete, S. L. Hyzy, D. L. Hutton et al., “Direct and indirect effects of microstructured titanium substrates on the induction of mesenchymal stem cell differentiation towards the osteoblast lineage,” Biomaterials, vol. 31, no. 10, pp. 2728–2735, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. 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
  74. T. Wakayama and R. Yanagimachi, “Cloning of male mice from adult tail-tip cells,” Nature Genetics, vol. 22, no. 2, pp. 127-128, 1999. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Lister, M. Pelizzola, Y. S. Kida et al., “Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells,” Nature, vol. 471, no. 7336, pp. 68–73, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. D. S. Kim, J. S. Lee, J. W. Leem et al., “Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity,” Stem Cell Reviews, vol. 6, no. 2, pp. 270–281, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Stadtfeld, E. Apostolou, H. Akutsu et al., “Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells,” Nature, vol. 465, no. 7295, pp. 175–181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. K. L. Nazor, G. Altun, C. Lynch et al., “Recurrent variations in DNA methylation in human pluripotent stem cells and their differentiated derivatives,” Cell Stem Cell, vol. 10, no. 5, pp. 620–634, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. K. Kaji, K. Norrby, A. Paca, M. Mileikovsky, P. Mohseni, and K. Woltjen, “Virus-free induction of pluripotency and subsequent excision of reprogramming factors,” Nature, vol. 458, no. 7239, pp. 771–775, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. K. Woltjen, I. P. Michael, P. Mohseni et al., “piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells,” Nature, vol. 458, no. 7239, pp. 766–770, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. K. Okita, T. Ichisaka, and S. Yamanaka, “Generation of germline-competent induced pluripotent stem cells,” Nature, vol. 448, no. 7151, pp. 313–317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Nakagawa, M. Koyanagi, K. Tanabe et al., “Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts,” Nature Biotechnology, vol. 26, no. 1, pp. 101–106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Chakraborty, N. Christoforou, A. Fattahi, R. W. Herzog, and K. W. Leong, “A robust strategy for negative selection of Cre-loxP recombination-based excision of transgenes in induced pluripotent stem cells,” PLoS One, vol. 8, no. 5, article e64342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. M. Stadtfeld and K. Hochedlinger, “Induced pluripotency: history, mechanisms, and applications,” Genes & Development, vol. 24, no. 20, pp. 2239–2263, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. W. Zhou and C. R. Freed, “Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells,” Stem Cells, vol. 27, no. 11, pp. 2667–2674, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Zhang, W. Li, T. Laurent, and S. Ding, “Small molecules, big roles – the chemical manipulation of stem cell fate and somatic cell reprogramming,” Journal of Cell Science, vol. 125, no. 23, pp. 5609–5620, 2012. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Yu, K. Hu, K. Smuga-Otto et al., “Human induced pluripotent stem cells free of vector and transgene sequences,” Science, vol. 324, no. 5928, pp. 797–801, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. H. Ban, N. Nishishita, N. Fusaki et al., “Efficient generation of transgene-free human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 34, pp. 14234–14239, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Nakanishi and M. Otsu, “Development of Sendai virus vectors and their potential applications in gene therapy and regenerative medicine,” Current Gene Therapy, vol. 12, no. 5, pp. 410–416, 2012. View at Publisher · View at Google Scholar · View at Scopus
  90. Y. Shi, C. Desponts, J. T. Do, H. S. Hahm, H. R. Scholer, and S. Ding, “Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds,” Cell Stem Cell, vol. 3, no. 5, pp. 568–574, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. E. J. Kim, G. Shim, K. Kim, I. C. Kwon, Y. K. Oh, and C. K. Shim, “Hyaluronic acid complexed to biodegradable poly L-arginine for targeted delivery of siRNAs,” The Journal of Gene Medicine, vol. 11, no. 9, pp. 791–803, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Huangfu, R. Maehr, W. Guo et al., “Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds,” Nature Biotechnology, vol. 26, no. 7, pp. 795–7, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. D. Huangfu, K. Osafune, R. Maehr et al., “Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2,” Nature Biotechnology, vol. 26, no. 11, pp. 1269–1275, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. Y. Shi, J. Tae Do, C. Desponts, H. S. Hahm, H. R. Schöler, and S. Ding, “A combined chemical and genetic approach for the generation of induced pluripotent stem cells,” Cell Stem Cell, vol. 2, no. 6, pp. 525–528, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. J. K. Ichida, J. Blanchard, K. Lam et al., “A small-molecule inhibitor of tgf-β signaling replaces Sox2 in reprogramming by inducing Nanog,” Cell Stem Cell, vol. 5, no. 5, pp. 491–503, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. N. Maherali and K. Hochedlinger, “Tgfβ signal inhibition cooperates in the induction of iPSCs and replaces Sox2 and cMyc,” Current Biology, vol. 19, no. 20, pp. 1718–1723, 2009. View at Publisher · View at Google Scholar · View at Scopus
  97. W. Li, W. Wei, S. Zhu et al., “Generation of rat and human induced pluripotent stem cells by combining genetic reprogramming and chemical inhibitors,” Cell Stem Cell, vol. 4, no. 1, pp. 16–19, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Trevisan, G. Desole, G. Costanzi, E. Lavezzo, G. Palu, and L. Barzon, “Reprogramming methods do not affect gene expression profile of human induced pluripotent stem cells,” International Journal of Molecular Sciences, vol. 18, no. 1, 2017. View at Publisher · View at Google Scholar · View at Scopus
  99. A. C. Planello, J. Ji, V. Sharma et al., “Aberrant DNA methylation reprogramming during induced pluripotent stem cell generation is dependent on the choice of reprogramming factors,” Cell Regeneration, vol. 3, no. 1, p. 4, 2014. View at Publisher · View at Google Scholar
  100. J. H. Park, L. Daheron, S. Kantarci, B. S. Lee, and J. M. Teixeira, “Human endometrial cells express elevated levels of pluripotent factors and are more amenable to reprogramming into induced pluripotent stem cells,” Endocrinology, vol. 152, no. 3, pp. 1080–1089, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. T. Aasen, A. Raya, M. J. Barrero et al., “Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes,” Nature Biotechnology, vol. 26, no. 11, pp. 1276–1284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  102. J. Hanna, S. Markoulaki, P. Schorderet et al., “Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency,” Cell, vol. 133, no. 2, pp. 250–264, 2008. View at Publisher · View at Google Scholar · View at Scopus
  103. T. Aoi, K. Yae, M. Nakagawa et al., “Generation of pluripotent stem cells from adult mouse liver and stomach cells,” Science, vol. 321, no. 5889, pp. 699–702, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. H. Loh, S. Agarwal, I. H. Park et al., “Generation of induced pluripotent stem cells from human blood,” Blood, vol. 113, no. 22, pp. 5476–5479, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. C. Li, J. Zhou, G. Shi et al., “Pluripotency can be rapidly and efficiently induced in human amniotic fluid-derived cells,” Human Molecular Genetics, vol. 18, no. 22, pp. 4340–4349, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. N. Tamaoki, K. Takahashi, T. Tanaka et al., “Dental pulp cells for induced pluripotent stem cell banking,” Journal of Dental Research, vol. 89, no. 8, pp. 773–8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. Z. Ghosh, K. D. Wilson, Y. Wu, S. Hu, T. Quertermous, and J. C. Wu, “Persistent donor cell gene expression among human induced pluripotent stem cells contributes to differences with human embryonic stem cells,” PLoS One, vol. 5, no. 2, article e8975, 2010. View at Publisher · View at Google Scholar · View at Scopus
  108. M. C. N. Marchetto, G. W. Yeo, O. Kainohana, M. Marsala, F. H. Gage, and A. R. Muotri, “Transcriptional signature and memory retention of human-induced pluripotent stem cells,” PLoS One, vol. 4, no. 9, article e7076, 2009. View at Publisher · View at Google Scholar · View at Scopus
  109. K. Kim, R. Zhao, A. Doi et al., “Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells,” Nature Biotechnology, vol. 29, no. 12, pp. 1117–1119, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Utikal, J. M. Polo, M. Stadtfeld et al., “Immortalization eliminates a roadblock during cellular reprogramming into iPS cells,” Nature, vol. 460, no. 7259, pp. 1145–1148, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. 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
  112. R. M. Marion, K. Strati, H. Li et al., “A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity,” Nature, vol. 460, no. 7259, pp. 1149–1153, 2009. View at Publisher · View at Google Scholar · View at Scopus
  113. R. M. Marion, K. Strati, H. Li et al., “Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells,” Cell Stem Cell, vol. 4, no. 2, pp. 141–154, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. M. Stadtfeld, M. Nagaya, J. Utikal, G. Weir, and K. Hochedlinger, “Induced pluripotent stem cells generated without viral integration,” Science, vol. 322, no. 5903, pp. 945–949, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. R. Sridharan, J. Tchieu, M. J. Mason et al., “Role of the murine reprogramming factors in the induction of pluripotency,” Cell, vol. 136, no. 2, pp. 364–377, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. A. M. Newman and J. B. Cooper, “Lab-specific gene expression signatures in pluripotent stem cells,” Cell Stem Cell, vol. 7, no. 2, pp. 258–262, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. T. L. Chung, R. M. Brena, G. Kolle et al., “Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells,” Stem Cells, vol. 28, no. 10, pp. 1848–1855, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. T. L. Chung, J. P. Turner, N. Y. Thaker et al., “Ascorbate promotes epigenetic activation of CD30 in human embryonic stem cells,” Stem Cells, vol. 28, no. 10, pp. 1782–1793, 2010. View at Publisher · View at Google Scholar · View at Scopus
  119. Y. Ohi, H. Qin, C. Hong et al., “Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells,” Nature Cell Biology, vol. 13, no. 5, pp. 541–549, 2011. View at Publisher · View at Google Scholar · View at Scopus
  120. N. Singh, S. S. Rahatekar, K. K. K. Koziol et al., “Directing chondrogenesis of stem cells with specific blends of cellulose and silk,” Biomacromolecules, vol. 14, no. 5, pp. 1287–1298, 2013. View at Publisher · View at Google Scholar · View at Scopus
  121. C. Cristallini, E. Cibrario Rocchietti, L. Accomasso et al., “The effect of bioartificial constructs that mimic myocardial structure and biomechanical properties on stem cell commitment towards cardiac lineage,” Biomaterials, vol. 35, no. 1, pp. 92–104, 2014. View at Publisher · View at Google Scholar · View at Scopus
  122. C. M. Murphy, A. Matsiko, M. G. Haugh, J. P. Gleeson, and F. J. O’Brien, “Mesenchymal stem cell fate is regulated by the composition and mechanical properties of collagen–glycosaminoglycan scaffolds,” Journal of the Mechanical Behavior of Biomedical Materials, vol. 11, pp. 53–62, 2012. View at Publisher · View at Google Scholar · View at Scopus
  123. E. Mooney, J. N. Mackle, D. J. P. Blond et al., “The electrical stimulation of carbon nanotubes to provide a cardiomimetic cue to MSCs,” Biomaterials, vol. 33, no. 26, pp. 6132–6139, 2012. View at Publisher · View at Google Scholar · View at Scopus
  124. L. Glennon-Alty, R. Williams, S. Dixon, and P. Murray, “Induction of mesenchymal stem cell chondrogenesis by polyacrylate substrates,” Acta Biomaterialia, vol. 9, no. 4, pp. 6041–6051, 2013. View at Publisher · View at Google Scholar · View at Scopus
  125. I. H. Park, R. Zhao, J. A. West et al., “Reprogramming of human somatic cells to pluripotency with defined factors,” Nature, vol. 451, no. 7175, pp. 141–146, 2008. View at Publisher · View at Google Scholar · View at Scopus
  126. B. K. Chou, P. Mali, X. Huang et al., “Efficient human iPS cell derivation by a non-integrating plasmid from blood cells with unique epigenetic and gene expression signatures,” Cell Research, vol. 21, no. 3, pp. 518–529, 2011. View at Publisher · View at Google Scholar · View at Scopus
  127. F. Jia, K. D. Wilson, N. Sun et al., “A nonviral minicircle vector for deriving human iPS cells,” Nature Methods, vol. 7, no. 3, pp. 197–199, 2010. View at Publisher · View at Google Scholar · View at Scopus
  128. L. Warren, P. D. Manos, T. Ahfeldt et al., “Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA,” Cell Stem Cell, vol. 7, no. 5, pp. 618–630, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. M. Silva, L. Daheron, H. Hurley et al., “Generating iPSCs: translating cell reprogramming science into scalable and robust biomanufacturing strategies,” Cell Stem Cell, vol. 16, no. 1, pp. 13–17, 2015. View at Publisher · View at Google Scholar · View at Scopus
  130. 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. 472–6, 2009. View at Publisher · View at Google Scholar · View at Scopus
  131. Q. Zhou, J. Brown, A. Kanarek, J. Rajagopal, and D. A. Melton, “In vivo reprogramming of adult pancreatic exocrine cells to β-cells,” Nature, vol. 455, no. 7213, pp. 627–632, 2008. View at Publisher · View at Google Scholar · View at Scopus
  132. K. Wolfrum, Y. Wang, A. Prigione, K. Sperling, H. Lehrach, and J. Adjaye, “The LARGE principle of cellular reprogramming: lost, acquired and retained gene expression in foreskin and amniotic fluid-derived human iPS cells,” PLoS One, vol. 5, no. 10, article e13703, 2010. View at Publisher · View at Google Scholar · View at Scopus
  133. S. N. Dowey, X. Huang, B. K. Chou, Z. Ye, and L. Cheng, “Generation of integration-free human induced pluripotent stem cells from postnatal blood mononuclear cells by plasmid vector expression,” Nature Protocols, vol. 7, no. 11, pp. 2013–2021, 2012. View at Publisher · View at Google Scholar · View at Scopus
  134. K. Streckfuss-Bomeke, 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
  135. M. Ieda, J. D. Fu, P. Delgado-Olguin et al., “Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors,” Cell, vol. 142, no. 3, pp. 375–386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  136. Y. Oda, Y. Yoshimura, H. Ohnishi et al., “Induction of pluripotent stem cells from human third molar mesenchymal stromal cells,” The Journal of Biological Chemistry, vol. 285, no. 38, pp. 29270–29278, 2010. View at Publisher · View at Google Scholar · View at Scopus
  137. T. Vierbuchen, A. Ostermeier, Z. P. Pang, Y. Kokubu, T. C. Sudhof, and M. Wernig, “Direct conversion of fibroblasts to functional neurons by defined factors,” Nature, vol. 463, no. 7284, pp. 1035–1041, 2010. View at Publisher · View at Google Scholar · View at Scopus
  138. E. Szabo, S. Rampalli, R. M. Risueno et al., “Direct conversion of human fibroblasts to multilineage blood progenitors,” Nature, vol. 468, no. 7323, pp. 521–526, 2010. View at Publisher · View at Google Scholar · View at Scopus
  139. P. Huang, Z. He, S. Ji et al., “Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors,” Nature, vol. 475, no. 7356, pp. 386–389, 2011. View at Publisher · View at Google Scholar · View at Scopus
  140. M. Stadtfeld, K. Brennand, and K. Hochedlinger, “Reprogramming of pancreatic β cells into induced pluripotent stem cells,” Current Biology, vol. 18, no. 12, pp. 890–894, 2008. View at Publisher · View at Google Scholar · View at Scopus