Sequential introduction of reprogramming factors reveals a time-sensitive requirement for individual factors and a sequential EMT–MET mechanism for optimal reprogramming (original) (raw)

• Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–676 (2006).
  Article CAS Google Scholar
• Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917–1920 (2007).
  Article CAS Google Scholar
• Zhao, C., Deng, W. & Gage, F. H. Mechanisms and functional implications of adult neurogenesis. Cell 132, 645–660 (2008).
  Article CAS Google Scholar
• Kim, D. et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem. Cell 4, 472–476 (2009).
  Article CAS Google Scholar
• Okita, K., Nakagawa, M., Hyenjong, H., Ichisaka, T. & Yamanaka, S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 322, 949–953 (2008).
  Article CAS Google Scholar
• Warren, L. et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem. Cell 7, 618–630 (2010).
  Article CAS Google Scholar
• Zhou, H. et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem. Cell 4, 381–384 (2009).
  Article CAS Google Scholar
• Liao, J. et al. Generation of induced pluripotent stem cell lines from adult rat cells. Cell Stem. Cell 4, 11–15 (2009).
  Article CAS Google Scholar
• Liu, H. et al. Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. Cell Stem. Cell 3, 587–590 (2008).
  Article CAS Google Scholar
• Nelson, T. J., Martinez-Fernandez, A. & Terzic, A. Induced pluripotent stem cells: developmental biology to regenerative medicine. Nat. Rev. Cardiol. 7, 700–710 (2010).
  Article Google Scholar
• Cheng, L. et al. Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem. Cell 10, 337–344 (2012).
  Article CAS Google Scholar
• Hussein, S. M. et al. Copy number variation and selection during reprogramming to pluripotency. Nature 471, 58–62 (2011).
  Article CAS Google Scholar
• Fairchild, P. J. The challenge of immunogenicity in the quest for induced pluripotency. Nat. Rev. Immunol. 10, 868–875 (2010).
  Article CAS Google Scholar
• Zhao, T., Zhang, Z. N., Rong, Z. & Xu, Y. Immunogenicity of induced pluripotent stem cells. Nature 474, 212–215 (2011).
  Article CAS Google Scholar
• Young, M. A. et al. Background mutations in parental cells account for most of the genetic heterogeneity of induced pluripotent stem cells. Cell Stem. Cell 10, 570–582 (2012).
  Article CAS Google Scholar
• Esteban, M. A. et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem. Cell 6, 71–79 (2010).
  Article CAS Google Scholar
• Wang, T. et al. The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem. Cell 9, 575–587 (2011).
  Article CAS Google Scholar
• Chen, J. et al. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat. Genet. 45, 34–42 (2012).
  Article Google Scholar
• Esteban, M. A. & Pei, D. Vitamin C improves the quality of somatic cell reprogramming. Nat. Genet. 44, 366–367 (2012).
  Article CAS Google Scholar
• Li, R. et al. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 7, 51–63 (2010).
  Article CAS Google Scholar
• Hanna, J. et al. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature 462, 595–601 (2009).
  Article CAS Google Scholar
• Buganim, Y. et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209–1222 (2012).
  Article CAS Google Scholar
• Carey, B. W. et al. Reprogramming of murine and human somatic cells using a single polycistronic vector. Proc. Natl Acad. Sci. USA 106, 157–162 (2009).
  Article CAS Google Scholar
• Pan, G., Li, J., Zhou, Y., Zheng, H. & Pei, D. A negative feedback loop of transcription factors that controls stem cell pluripotency and self-renewal. FASEB J. 20, 1730–1732 (2006).
  Article CAS Google Scholar
• Ruiz, S. et al. A high proliferation rate is required for cell reprogramming and maintenance of human embryonic stem cell identity. Curr. Biol. 21, 45–52 (2010).
  Article Google Scholar
• Samavarchi-Tehrani, P. et al. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem. Cell 7, 64–77 (2010).
  Article CAS Google Scholar
• Conacci-Sorrell, M. et al. Autoregulation of E-cadherin expression by cadherin–cadherin interactions: the roles of β-catenin signaling, Slug, and MAPK. J. Cell Biol. 163, 847–857 (2003).
  Article CAS Google Scholar
• Maeda, M., Johnson, K. R. & Wheelock, M. J. Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J. Cell Sci. 118, 873–887 (2005).
  Article CAS Google Scholar
• Shih, J. Y. & Yang, P. C. The EMT regulator slug and lung carcinogenesis. Carcinogenesis 32, 1299–1304 (2011).
  Article CAS Google Scholar
• Alves, C. C., Carneiro, F., Hoefler, H. & Becker, K.F. Role of the epithelial-mesenchymal transition regulator Slug in primary human cancers. Front Biosci. 14, 3035–3050 (2009).
  Article Google Scholar
• Schulte, J. et al. Expression of the E-cadherin repressors Snail, Slug and Zeb1 in urothelial carcinoma of the urinary bladder: relation to stromal fibroblast activation and invasive behaviour of carcinoma cells. Histochem. Cell Biol. 138, 847–860 (2012).
  Article CAS Google Scholar
• Wels, C., Joshi, S., Koefinger, P., Bergler, H. & Schaider, H. Transcriptional activation of ZEB1 by Slug leads to cooperative regulation of the epithelial-mesenchymal transition-like phenotype in melanoma. J. Invest. Dermatol. 131, 1877–1885 (2011).
  Article CAS Google Scholar
• Chiou, S. H. et al. Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res. 70, 10433–10444 (2010).
  Article CAS Google Scholar
• Liu, Y. N. et al. Critical and reciprocal regulation of KLF4 and SLUG in transforming growth factor β-initiated prostate cancer epithelial-mesenchymal transition. Mol. Cell. Biol. 32, 941–953 (2012).
  Article Google Scholar
• Ichida, J. K. et al. A small-molecule inhibitor of tgf- β signaling replaces sox2 in reprogramming by inducing nanog. Cell Stem. Cell 5, 491–503 (2009).
  Article CAS Google Scholar
• Soufi, A., Donahue, G. & Zaret, K. S. Facilitators and impediments of the pluripotency reprogramming factors’ initial engagement with the genome. Cell 151, 994–1004 (2012).
  Article CAS Google Scholar
• Friedl, P. & Alexander, S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147, 992–1009 (2011).
  Article CAS Google Scholar
• Thiery, J. P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442–454 (2002).
  Article CAS Google Scholar
• Palma-Nicolas, J. P. & Lopez-Colome, A. M. Thrombin induces slug-mediated E-cadherin transcriptional repression and the parallel Up-regulation of N-cadherin by a transcription-independent mechanism in RPE cells. J. Cell. Physiol. 228, 581–589 (2013).
  Article CAS Google Scholar
• Gravdal, K., Halvorsen, O. J., Haukaas, S. A. & Akslen, L. A. A switch from E-cadherin to N-cadherin expression indicates epithelial to mesenchymal transition and is of strong and independent importance for the progress of prostate cancer. Clin. Cancer Res. 13, 7003–7011 (2007).
  Article CAS Google Scholar
• Baum, B., Settleman, J. & Quinlan, M. P. Transitions between epithelial and mesenchymal states in development and disease. Sem. Cell Dev. Biol. 19, 294–308 (2008).
  Article CAS Google Scholar
• Lim, J. & Thiery, J. P. Epithelial-mesenchymal transitions: insights from development. Development 139, 3471–3486 (2012).
  Article CAS Google Scholar
• Davies, J. A. Mesenchyme to epithelium transition during development of the mammalian kidney tubule. Acta Anatom. 156, 187–201 (1996).
  Article CAS Google Scholar
• Nakaya, Y., Kuroda, S., Katagiri, Y. T., Kaibuchi, K. & Takahashi, Y. Mesenchymal-epithelial transition during somitic segmentation is regulated by differential roles of Cdc42 and Rac1. Dev. Cell 7, 425–438 (2004).
  Article CAS Google Scholar
• Nakajima, Y., Yamagishi, T., Hokari, S. & Nakamura, H. Mechanisms involved in valvuloseptal endocardial cushion formation in early cardiogenesis: roles of transforming growth factor (TGF)- β and bone morphogenetic protein (BMP). Anatom. Rec. 258, 119–127 (2000).
  Article CAS Google Scholar
• Li, B., Zheng, Y. W., Sano, Y. & Taniguchi, H. Evidence for mesenchymal-epithelial transition associated with mouse hepatic stem cell differentiation. PloS One 6, e17092 (2011).
  Article CAS Google Scholar
• Trusolino, L., Bertotti, A. & Comoglio, P. M. MET signalling: principles and functions in development, organ regeneration and cancer. Nat. Rev. Mol. Cell Biol. 11, 834–848 (2010).
  Article CAS Google Scholar
• Silva, J. et al. Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol. 6, e253 (2008).
  Article Google Scholar
• Qin, D. et al. Mouse meningiocytes express Sox2 and yield high efficiency of chimeras after nuclear reprogramming with exogenous factors. J. Biol. Chem. 283, 33730–33735 (2008).
  Article CAS Google Scholar
• Chen, J. et al. Rational optimization of reprogramming culture conditions for the generation of induced pluripotent stem cells with ultra-high efficiency and fast kinetics. Cell Res. 21, 884–894 (2011).
  Article CAS Google Scholar