Methods for making induced pluripotent stem cells: reprogramming à la carte (original) (raw)
Evans, M. J. & Kaufman, M. H. Establishment in culture of pluripotential cells from mouse embryos. Nature292, 154–156 (1981). ArticleCASPubMed Google Scholar
Martin, G. R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl Acad. Sci. USA78, 7634–7638 (1981). ArticleCASPubMedPubMed Central Google Scholar
Thomson, J. A. et al. Embryonic stem cell lines derived from human blastocysts. Science282, 1145–1147 (1998). Princepspaper describing the generation of a human blastocyst-derived, pluripotent cell lines relevant for human transplantation medicine. ArticleCASPubMed Google Scholar
Hochedlinger, K. & Jaenisch, R. Nuclear reprogramming and pluripotency. Nature441, 1061–1067 (2006). ArticleCASPubMed Google Scholar
Hochedlinger, K. & Jaenisch, R. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature415, 1035–1038 (2002). ArticleCASPubMed Google Scholar
Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell126, 663–676 (2006). The first paper describing the generation of iPSC lines from MEFs by overexpressing theOct4, Sox2, Klf4andMyctranscription factors. ArticleCASPubMed Google Scholar
Maherali, N. et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell1, 55–70 (2007). ArticleCASPubMed Google Scholar
Okita, K., Ichisaka, T. & Yamanaka, S. Generation of germline-competent induced pluripotent stem cells. Nature448, 313–317 (2007). ArticleCASPubMed Google Scholar
Wernig, M. et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature448, 318–324 (2007). ArticleCASPubMed Google Scholar
Aoi, T. et al. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science321, 699–702 (2008). ArticleCASPubMed Google Scholar
Stadtfeld, M., Brennand, K. & Hochedlinger, K. Reprogramming of pancreatic β cells into induced pluripotent stem cells. Curr. Biol.18, 890–894 (2008). ArticleCASPubMedPubMed Central Google Scholar
Eminli, S., Utikal, J., Arnold, K., Jaenisch, R. & Hochedlinger, K. Reprogramming of neural progenitor cells into induced pluripotent stem cells in the absence of exogenous Sox2 expression. Stem Cells26, 2467–2474 (2008). ArticleCASPubMed Google Scholar
Kim, J. B. et al. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature454, 646–650 (2008). ArticleCASPubMed Google Scholar
Aasen, T. et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nature Biotech.26, 1276–1284 (2008). ArticleCAS Google Scholar
Giorgetti, A. et al. Generation of induced pluripotent stem cells from human cord blood using OCT4 and SOX2. Cell Stem Cell5, 353–357 (2009). This paper describes the generation of iPSCs from cord blood CD133+ cells, which could facilitate the constitution of iPSC banks that represent a wide panel of relevant haplotypes that are useful for transplantation. ArticleCASPubMedPubMed Central Google Scholar
Nakagawa, M. et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nature Biotech.26, 101–106 (2008). ArticleCAS Google Scholar
Wernig, M., Meissner, A., Cassady, J. P. & Jaenisch, R. c-Myc is dispensable for direct reprogramming of mouse fibroblasts. Cell Stem Cell2, 10–12 (2008). ArticleCASPubMed Google Scholar
Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science318, 1917–1920 (2007). ArticleCASPubMed Google Scholar
Daley, G. Q. et al. Broader implications of defining standards for the pluripotency of iPSCs. Cell Stem Cell4, 200–201; author reply 202 (2009). ArticleCASPubMed Google Scholar
Ellis, J. et al. Alternative induced pluripotent stem cell characterization criteria for in vitro applications. Cell Stem Cell4, 198–199; author reply 202 (2009). ArticleCASPubMed Google Scholar
Maherali, N. & Hochedlinger, K. Guidelines and techniques for the generation of induced pluripotent stem cells. Cell Stem Cell3, 595–605 (2008). ArticleCASPubMed Google Scholar
Kim, J. B. et al. Oct4-induced pluripotency in adult neural stem cells. Cell136, 411–419 (2009). ArticleCASPubMed Google Scholar
Eminli, S. et al. Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nature Genet.41, 968–976 (2009). It is assumed that the level of differentiation of the donor cell population may represent a barrier to reprogramming. This article directly addresses this question by testing the reprogramming potential of mouse haematopoietic cells at different stages of differentiation. ArticleCASPubMed Google Scholar
Miura, K. et al. Variation in the safety of induced pluripotent stem cell lines. Nature Biotech.27, 743–745 (2009). The first large-scale study evaluating the safety of iPSCs fora therapeutic context, by evaluating the teratoma-forming capacity of injected iPSC-derived secondary neurospheres generated from 36 mouse iPSC lines derived in 11 different ways. ArticleCAS Google Scholar
Hanna, J. et al. Direct cell reprogramming is a stochastic process amenable to acceleration. Nature462, 595–601 (2009). An in-depth analysis of reprogramming in mouse cells, revealing the stochastic nature of this process and showing that almost all donor cells can give rise to iPSCs after continued culture and transcription-factor expression. ArticleCASPubMedPubMed Central Google Scholar
Zhao, Y. et al. Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell3, 475–479 (2008). ArticleCASPubMed Google Scholar
Tsubooka, N. et al. Roles of Sall4 in the generation of pluripotent stem cells from blastocysts and fibroblasts. Genes Cells14, 683–694 (2009). ArticleCASPubMed Google Scholar
Park, I. H. et al. Reprogramming of human somatic cells to pluripotency with defined factors. Nature451, 141–146 (2008). ArticleCASPubMed Google Scholar
Mallanna, S. K. & Rizzino, A. Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev. Biol.344, 16–25 (2010). ArticleCASPubMedPubMed Central Google Scholar
Wang, Y. et al. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nature Genet.40, 1478–1483 (2008). ArticleCASPubMed Google Scholar
Judson, R. L., Babiarz, J. E., Venere, M. & Blelloch, R. Embryonic stem cell-specific microRNAs promote induced pluripotency. Nature Biotech.27, 459–461 (2009). ArticleCAS Google Scholar
Kawamura, T. et al. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature460, 1140–1144 (2009). The inhibition of tumour suppressor genes such as p53 greatly improves reprogramming efficiency. This observation suggests that reprogramming per secan exert selective pressure on the pool of donor cells in which this pathway is impaired. ArticleCASPubMedPubMed Central Google Scholar
Huangfu, D. et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nature Biotech.26, 795–797 (2008). The first of many of articles that show the ability of chemical compounds to increase reprogramming efficiency or completely replace defined factors used in reprogramming. This work opens the door to eventually generating iPSCs using only chemicals. ArticleCAS Google Scholar
Huangfu, D. et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nature Biotech.26, 1269–1275 (2008). ArticleCAS Google Scholar
Feldman, N. et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nature Cell Biol.8, 188–194 (2006). ArticleCASPubMed Google Scholar
Shi, Y. et al. Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell3, 568–574 (2008). ArticleCASPubMed Google Scholar
Mali, P. et al. Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-associated genes. Stem Cells28, 713–720 (2010). ArticleCASPubMedPubMed Central Google Scholar
Esteban, M. A. et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell6, 71–79 (2010). ArticleCASPubMed Google Scholar
Chung, T. L. et al. Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells. Stem Cells28, 1848–1855 (2010). ArticleCASPubMed Google Scholar
Yoshida, Y., Takahashi, K., Okita, K., Ichisaka, T. & Yamanaka, S. Hypoxia enhances the generation of induced pluripotent stem cells. Cell Stem Cell5, 237–241 (2009). ArticleCASPubMed Google Scholar
Dravid, G. et al. Defining the role of Wnt/β-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells23, 1489–1501 (2005). ArticleCASPubMed Google Scholar
Okada, M., Oka, M. & Yoneda, Y. Effective culture conditions for the induction of pluripotent stem cells. Biochim. Biophys. Acta1800, 956–963 (2010). ArticleCASPubMed Google Scholar
Kitamura, T. et al. Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp. Hematol.31, 1007–1014 (2003). ArticleCASPubMed Google Scholar
Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell131, 861–872 (2007). ArticleCASPubMed Google Scholar
Takahashi, K., Okita, K., Nakagawa, M. & Yamanaka, S. Induction of pluripotent stem cells from fibroblast cultures. Nature Protoc.2, 3081–3089 (2007). ArticleCAS Google Scholar
Hawley, R. G., Lieu, F. H., Fong, A. Z. & Hawley, T. S. Versatile retroviral vectors for potential use in gene therapy. Gene Ther.1, 136–138 (1994). CASPubMed Google Scholar
Jahner, D. et al. De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature298, 623–628 (1982). ArticleCASPubMed Google Scholar
Stewart, C. L., Stuhlmann, H., Jahner, D. & Jaenisch, R. De novo methylation, expression, and infectivity of retroviral genomes introduced into embryonal carcinoma cells. Proc. Natl Acad. Sci. USA79, 4098–4102 (1982). ArticleCASPubMedPubMed Central Google Scholar
Hotta, A. & Ellis, J. Retroviral vector silencing during iPS cell induction: an epigenetic beacon that signals distinct pluripotent states. J. Cell. Biochem.105, 940–948 (2008). ArticleCASPubMed Google Scholar
Blelloch, R., Venere, M., Yen, J. & Ramalho-Santos, M. Generation of induced pluripotent stem cells in the absence of drug selection. Cell Stem Cell1, 245–247 (2007). ArticleCASPubMedPubMed Central Google Scholar
Yao, S. et al. Retrovirus silencing, variegation, extinction, and memory are controlled by a dynamic interplay of multiple epigenetic modifications. Mol. Ther.10, 27–36 (2004). ArticleCASPubMed Google Scholar
Varas, F. et al. Fibroblast-derived induced pluripotent stem cells show no common retroviral vector insertions. Stem Cells27, 300–306 (2009). ArticleCASPubMedPubMed Central Google Scholar
Hanna, J. et al. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science318, 1920–1923 (2007). The first demonstration of the therapeutical potential of iPSCs in a humanized sickle-cell anaemia mouse model, highlighting the need to resolve the problems relating to the use of retroviruses and oncogenes in reprogramming for human therapy. ArticleCASPubMed Google Scholar
Brambrink, T. et al. Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell2, 151–159 (2008). ArticleCASPubMedPubMed Central Google Scholar
Ryan, M. D. & Drew, J. Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein. EMBO J.13, 928–933 (1994). ArticleCASPubMedPubMed Central Google Scholar
Ryan, M. D. & Flint, M. Virus-encoded proteinases of the picornavirus super-group. J. Gen. Virol.78, 699–723 (1997). ArticleCASPubMed Google Scholar
Hasegawa, K., Cowan, A. B., Nakatsuji, N. & Suemori, H. Efficient multicistronic expression of a transgene in human embryonic stem cells. Stem Cells25, 1707–1712 (2007). ArticleCASPubMed Google Scholar
Rodriguez-Piza, I. et al. Reprogramming of human fibroblasts to induced pluripotent stem cells under xeno-free conditions. Stem Cells28, 36–44 (2010). ArticleCASPubMed Google Scholar
Carey, B. W. et al. Reprogramming of murine and human somatic cells using a single polycistronic vector. Proc. Natl Acad. Sci. USA106, 157–162 (2009). ArticleCASPubMed Google Scholar
Sommer, C. A. et al. Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells27, 543–549 (2009). ArticleCASPubMedPubMed Central Google Scholar
Sommer, C. A. et al. Excision of reprogramming transgenes improves the differentiation potential of iPS cells generated with a single excisable vector. Stem Cells28, 64–74 (2010). ArticleCASPubMedPubMed Central Google Scholar
Cary, L. C. et al. Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology172, 156–169 (1989). ArticleCASPubMed Google Scholar
Lacoste, A., Berenshteyn, F. & Brivanlou, A. H. An efficient and reversible transposable system for gene delivery and lineage-specific differentiation in human embryonic stem cells. Cell Stem Cell5, 332–342 (2009). ArticleCASPubMed Google Scholar
Fraser, M. J., Cary, L., Boonvisudhi, K. & Wang, H. G. Assay for movement of Lepidopteran transposon IFP2 in insect cells using a baculovirus genome as a target DNA. Virology211, 397–407 (1995). ArticleCASPubMed Google Scholar
Fraser, M. J., Ciszczon, T., Elick, T. & Bauser, C. Precise excision of TTAA-specific lepidopteran transposons piggyBac (IFP2) and tagalong (TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera. Insect Mol. Biol.5, 141–151 (1996). ArticleCASPubMed Google Scholar
Wilson, M. H., Coates, C. J. & George, A. L. PiggyBac transposon-mediated gene transfer in human cells. Mol. Ther.15, 139–145 (2007). ArticleCASPubMed Google Scholar
Yusa, K., Rad, R., Takeda, J. & Bradley, A. Generation of transgene-free induced pluripotent mouse stem cells by the piggyBac transposon. Nature Methods6, 363–369 (2009). ArticleCASPubMedPubMed Central Google Scholar
Stadtfeld, M., Nagaya, M., Utikal, J., Weir, G. & Hochedlinger, K. Induced pluripotent stem cells generated without viral integration. Science322, 945–949 (2008). ArticleCASPubMedPubMed Central Google Scholar
Sigal, S. H. et al. Evidence for a terminal differentiation process in the rat liver. Differentiation59, 35–42 (1995). ArticleCASPubMed Google Scholar
Gupta, S. Hepatic polyploidy and liver growth control. Semin. Cancer Biol.10, 161–171 (2000). ArticleCASPubMed Google Scholar
Zhou, W. & Freed, C. R. Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells27, 2667–2674 (2009). ArticleCASPubMed Google Scholar
Fusaki, N., Ban, H., Nishiyama, A., Saeki, K. & Hasegawa, M. 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. Proc. Jpn Acad. Ser. B Phys. Biol. Sci.85, 348–362 (2009). ArticleCASPubMedPubMed Central Google Scholar
Seki, T. et al. Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell7, 11–14 (2010). ArticleCASPubMed Google Scholar
Tokusumi, T. et al. Recombinant Sendai viruses expressing different levels of a foreign reporter gene. Virus Res.86, 33–38 (2002). ArticleCASPubMed Google Scholar
Li, H. O. et al. A cytoplasmic RNA vector derived from nontransmissible Sendai virus with efficient gene transfer and expression. J. Virol.74, 6564–6569 (2000). ArticleCASPubMedPubMed Central Google Scholar
Inoue, M. et al. Nontransmissible virus-like particle formation by F-deficient Sendai virus is temperature sensitive and reduced by mutations in M and HN proteins. J. Virol.77, 3238–3246 (2003). ArticleCASPubMedPubMed Central Google Scholar
Okita, K., Nakagawa, M., Hyenjong, H., Ichisaka, T. & Yamanaka, S. Generation of mouse induced pluripotent stem cells without viral vectors. Science322, 949–953 (2008). ArticleCASPubMed Google Scholar
González, F. et al. Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc. Natl Acad. Sci.USA106, 8918–8922 (2009). Article Google Scholar
Okita, K., Hong, H., Takahashi, K. & Yamanaka, S. Generation of mouse-induced pluripotent stem cells with plasmid vectors. Nature Protoc.5, 418–428 (2010). ArticleCAS Google Scholar
Pollack, Y., Stein, R., Razin, A. & Cedar, H. Methylation of foreign DNA sequences in eukaryotic cells. Proc . Natl Acad . Sci .USA77, 6463–6467 (1980). ArticleCAS Google Scholar
Yates, J., Warren, N., Reisman, D. & Sugden, B. A _cis_-acting element from the Epstein-Barr viral genome that permits stable replication of recombinant plasmids in latently infected cells. Proc. Natl Acad. Sci. USA81, 3806–3810 (1984). ArticleCASPubMedPubMed Central Google Scholar
Yates, J. L., Warren, N. & Sugden, B. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells. Nature313, 812–815 (1985). ArticleCASPubMed Google Scholar
Chen, Z. Y., He, C. Y., Ehrhardt, A. & Kay, M. A. Minicircle DNA vectors devoid of bacterial DNA result in persistent and high-level transgene expression in vivo. Mol. Ther.8, 495–500 (2003). ArticleCASPubMed Google Scholar
Chen, Z. Y., He, C. Y. & Kay, M. A. Improved production and purification of minicircle DNA vector free of plasmid bacterial sequences and capable of persistent transgene expression in vivo. Hum. Gene Ther.16, 126–131 (2005). ArticleCASPubMed Google Scholar
Warren, L. et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell7, 618–630 (2010). ArticleCASPubMedPubMed Central Google Scholar
Inoue, M. et al. p53 protein transduction therapy: successful targeting and inhibition of the growth of the bladder cancer cells. Eur. Urol.49, 161–168 (2006). ArticleCASPubMed Google Scholar
Michiue, H. et al. The NH2 terminus of influenza virus hemagglutinin-2 subunit peptides enhances the antitumor potency of polyarginine-mediated p53 protein transduction. J. Biol. Chem.280, 8285–8289 (2005). ArticleCASPubMed Google Scholar
Wadia, J. S. & Dowdy, S. F. Protein transduction technology. Curr. Opin. Biotechnol.13, 52–56 (2002). ArticleCASPubMed Google Scholar
Zhou, H. et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell4, 381–384 (2009). ArticleCASPubMed Google Scholar
Kim, D. et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell4, 472–476 (2009). ArticleCASPubMedPubMed Central Google Scholar
Stadtfeld, M., Maherali, N., Borkent, M. & Hochedlinger, K. A reprogrammable mouse strain from gene-targeted embryonic stem cells. Nature Methods7, 53–55 (2009). ArticlePubMedPubMed CentralCAS Google Scholar
Feng, B., Ng, J. H., Heng, J. C. & Ng, H. H. Molecules that promote or enhance reprogramming of somatic cells to induced pluripotent stem cells. Cell Stem Cell4, 301–312 (2009). ArticleCASPubMed Google Scholar
Stadtfeld, M. et al. Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature465, 175–181 (2010). ArticleCASPubMedPubMed Central Google Scholar
Boué, S., Paramonov, I., Barrero, M. J. & Izpisúa Belmonte, J. C. Analysis of human and mouse reprogramming of somatic cells to induced pluripotent stem cells. What is in the plate? PLoS ONE5, e12664 (2010). ArticlePubMedPubMed CentralCAS Google Scholar