Do all roads lead to Oct4? The emerging concepts of induced pluripotency

Martin, 1981, Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells, Proc. Natl. Acad. Sci. U.S.A., 78, 7634, 10.1073/pnas.78.12.7634 Smith, 2001, Embryo-derived stem cells: of mice and men, Annu. Rev. Cell Dev. Biol., 17, 435, 10.1146/annurev.cellbio.17.1.435 Nichols, 2009, Naive and primed pluripotent states, Cell Stem Cell, 4, 487, 10.1016/j.stem.2009.05.015 Nichols, 2012, Pluripotency in the embryo and in culture, Cold Spring Harb. Perspect. Biol., 4, a008128, 10.1101/cshperspect.a008128 Takahashi, 2006, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors, Cell, 126, 663, 10.1016/j.cell.2006.07.024 Nichols, 1998, Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4, Cell, 95, 379, 10.1016/S0092-8674(00)81769-9 Niwa, 2000, Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells, Nat. Genet., 24, 372, 10.1038/74199 Avilion, 2003, Multipotent cell lineages in early mouse development depend on SOX2 function, Genes Dev., 17, 126, 10.1101/gad.224503 Masui, 2007, Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells, Nat. Cell Biol., 9, 625, 10.1038/ncb1589 Chambers, 2007, Nanog safeguards pluripotency and mediates germline development, Nature, 450, 1230, 10.1038/nature06403 Martello, 2012, Esrrb is a pivotal target of the Gsk3/Tcf3 axis regulating embryonic stem cell self-renewal, Cell Stem Cell, 11, 491, 10.1016/j.stem.2012.06.008 Masui, 2008, Rex1/Zfp42 is dispensable for pluripotency in mouse ES cells, BMC Dev. Biol., 8, 45, 10.1186/1471-213X-8-45 Jiang, 2008, A core Klf circuitry regulates self-renewal of embryonic stem cells, Nat. Cell Biol., 10, 353, 10.1038/ncb1698 Ye, 2013, Embryonic stem cell self-renewal pathways converge on the transcription factor Tfcp2l1, EMBO J., 32, 2548, 10.1038/emboj.2013.175 Martello, 2013, Identification of the missing pluripotency mediator downstream of leukaemia inhibitory factor, EMBO J., 32, 2561, 10.1038/emboj.2013.177 Chambers, 2003, Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells, Cell, 113, 643, 10.1016/S0092-8674(03)00392-1 Festuccia, 2012, Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells, Cell Stem Cell, 11, 477, 10.1016/j.stem.2012.08.002 Hall, 2009, Oct4 and LIF/Stat3 additively induce Kruppel factors to sustain embryonic stem cell self-renewal, Cell Stem Cell, 5, 597, 10.1016/j.stem.2009.11.003 Niwa, 2009, A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells, Nature, 460, 118, 10.1038/nature08113 Kopp, 2008, Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells, Stem Cells, 26, 903, 10.1634/stemcells.2007-0951 Kim, 2009, Oct4-induced pluripotency in adult neural stem cells, Cell, 136, 411, 10.1016/j.cell.2009.01.023 Kim, 2009, Direct reprogramming of human neural stem cells by OCT4, Nature, 461, 649, 10.1038/nature08436 Wu, 2011, Reprogramming of trophoblast stem cells into pluripotent stem cells by Oct4, Stem Cells, 29, 755, 10.1002/stem.617 Tsai, 2011, Single transcription factor reprogramming of hair follicle dermal papilla cells to induced pluripotent stem cells, Stem Cells, 29, 964, 10.1002/stem.649 Yuan, 2011, Brief report: combined chemical treatment enables Oct4-induced reprogramming from mouse embryonic fibroblasts, Stem Cells, 29, 549, 10.1002/stem.594 Li, 2011, Generation of iPSCs from mouse fibroblasts with a single gene, Oct4, and small molecules, Cell Res., 21, 196, 10.1038/cr.2010.142 Zhu, 2010, Reprogramming of human primary somatic cells by OCT4 and chemical compounds, Cell Stem Cell, 7, 651, 10.1016/j.stem.2010.11.015 Heng, 2010, The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells, Cell Stem Cell, 6, 167, 10.1016/j.stem.2009.12.009 Gu, 2005, Orphan nuclear receptor LRH-1 is required to maintain Oct4 expression at the epiblast stage of embryonic development, Mol. Cell. Biol., 25, 3492, 10.1128/MCB.25.9.3492-3505.2005 Barnea, 2000, Synergy of SF1 and RAR in activation of Oct-3/4 promoter, J. Biol. Chem., 275, 6608, 10.1074/jbc.275.9.6608 Gao, 2013, Replacement of Oct4 by Tet1 during iPSC induction reveals an important role of DNA methylation and hydroxymethylation in reprogramming, Cell Stem Cell, 12, 453, 10.1016/j.stem.2013.02.005 Costa, 2013, NANOG-dependent function of TET1 and TET2 in establishment of pluripotency, Nature, 495, 370, 10.1038/nature11925 Buganim, 2012, Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase, Cell, 150, 1209, 10.1016/j.cell.2012.08.023 Mansour, 2012, The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming, Nature, 488, 409, 10.1038/nature11272 Zhang, 2006, Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1, Nat. Cell Biol., 8, 1114, 10.1038/ncb1481 Yang, 2010, A novel SALL4/OCT4 transcriptional feedback network for pluripotency of embryonic stem cells, PLoS ONE, 5, e10766, 10.1371/journal.pone.0010766 Gao, 2013, Reprogramming to pluripotency using designer TALE transcription factors targeting enhancers, Stem Cell Reports, 1, 183, 10.1016/j.stemcr.2013.06.002 Nakagawa, 2008, Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts, Nat. Biotechnol., 26, 101, 10.1038/nbt1374 Niwa, 2002, Phenotypic complementation establishes requirements for specific POU domain and generic transactivation function of Oct-3/4 in embryonic stem cells, Mol. Cell. Biol., 22, 1526, 10.1128/MCB.22.5.1526-1536.2002 Esch, 2013, A unique Oct4 interface is crucial for reprogramming to pluripotency, Nat. Cell Biol., 15, 295, 10.1038/ncb2680 Frankenberg, 2013, On the origin of POU5F1, BMC Biol., 11, 56, 10.1186/1741-7007-11-56 Frankenberg, 2010, The evolution of class V POU domain transcription factors in vertebrates and their characterisation in a marsupial, Dev. Biol., 337, 162, 10.1016/j.ydbio.2009.10.017 Tapia, 2012, Reprogramming to pluripotency is an ancient trait of vertebrate Oct4 and Pou2 proteins, Nat. Commun., 3, 1279, 10.1038/ncomms2229 Niwa, 2008, Platypus Pou5f1 reveals the first steps in the evolution of trophectoderm differentiation and pluripotency in mammals, Evol. Dev., 10, 671, 10.1111/j.1525-142X.2008.00280.x Morrison, 2006, Conserved roles for Oct4 homologues in maintaining multipotency during early vertebrate development, Development, 133, 2011, 10.1242/dev.02362 Rossello, 2013, Mammalian genes induce partially reprogrammed pluripotent stem cells in non-mammalian vertebrate and invertebrate species, Elife, 2, e00036, 10.7554/eLife.00036 Lu, 2012, Avian-induced pluripotent stem cells derived using human reprogramming factors, Stem Cells Dev., 21, 394, 10.1089/scd.2011.0499 Esteban, 2012, The mesenchymal-to-epithelial transition in somatic cell reprogramming, Curr. Opin. Genet. Dev., 22, 423, 10.1016/j.gde.2012.09.004 Ichida, 2009, A small-molecule inhibitor of tgf-Beta signaling replaces sox2 in reprogramming by inducing nanog, Cell Stem Cell, 5, 491, 10.1016/j.stem.2009.09.012 Maherali, 2009, Tgfbeta signal inhibition cooperates in the induction of iPSCs and replaces Sox2 and cMyc, Curr. Biol., 19, 1718, 10.1016/j.cub.2009.08.025 Samavarchi-Tehrani, 2010, Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming, Cell Stem Cell, 7, 64, 10.1016/j.stem.2010.04.015 Li, 2010, A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts, Cell Stem Cell, 7, 51, 10.1016/j.stem.2010.04.014 Wang, 2013, Critical regulation of miR-200/ZEB2 pathway in Oct4/Sox2-induced mesenchymal-to-epithelial transition and induced pluripotent stem cell generation, Proc. Natl. Acad. Sci. U.S.A., 110, 2858, 10.1073/pnas.1212769110 Redmer, 2011, E-cadherin is crucial for embryonic stem cell pluripotency and can replace OCT4 during somatic cell reprogramming, EMBO Rep., 12, 720, 10.1038/embor.2011.88 Ho, 2013, Stage-specific regulation of reprogramming to induced pluripotent stem cells by Wnt signaling and T cell factor proteins, Cell Rep., 3, 2113, 10.1016/j.celrep.2013.05.015 Livigni, 2013, A conserved Oct4/POUV-dependent network links adhesion and migration to progenitor maintenance, Curr. Biol., 23, 2233, 10.1016/j.cub.2013.09.048 Buganim, 2013, Mechanisms and models of somatic cell reprogramming, Nat. Rev. Genet., 14, 427, 10.1038/nrg3473 Soufi, 2012, Facilitators and impediments of the pluripotency reprogramming factors’ initial engagement with the genome, Cell, 151, 994, 10.1016/j.cell.2012.09.045 Zaret, 2011, Pioneer transcription factors: establishing competence for gene expression, Genes Dev., 25, 2227, 10.1101/gad.176826.111 Papp, 2013, Epigenetics of reprogramming to induced pluripotency, Cell, 152, 1324, 10.1016/j.cell.2013.02.043 You, 2011, OCT4 establishes and maintains nucleosome-depleted regions that provide additional layers of epigenetic regulation of its target genes, Proc. Natl. Acad. Sci. U.S.A., 108, 14497, 10.1073/pnas.1111309108 Chen, 2013, H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs, Nat. Genet., 45, 34, 10.1038/ng.2491 Loh, 2007, Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells, Genes Dev., 21, 2545, 10.1101/gad.1588207 Shi, 2008, A combined chemical and genetic approach for the generation of induced pluripotent stem cells, Cell Stem Cell, 2, 525, 10.1016/j.stem.2008.05.011 Feldman, 2006, G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis, Nat. Cell Biol., 8, 188, 10.1038/ncb1353 Athanasiadou, 2010, Targeting of de novo DNA methylation throughout the Oct-4 gene regulatory region in differentiating embryonic stem cells, PLoS ONE, 5, e9937, 10.1371/journal.pone.0009937 Loh, 2011, A precarious balance: pluripotency factors as lineage specifiers, Cell Stem Cell, 8, 363, 10.1016/j.stem.2011.03.013 Shu, 2013, Induction of pluripotency in mouse somatic cells with lineage specifiers, Cell, 153, 963, 10.1016/j.cell.2013.05.001 Montserrat, 2013, Reprogramming of human fibroblasts to pluripotency with lineage specifiers, Cell Stem Cell, 13, 341, 10.1016/j.stem.2013.06.019 Thomson, 2011, Pluripotency factors in embryonic stem cells regulate differentiation into germ layers, Cell, 145, 875, 10.1016/j.cell.2011.05.017 Wang, 2012, Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells, Cell Stem Cell, 10, 440, 10.1016/j.stem.2012.02.016 Takemoto, 2011, Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells, Nature, 470, 394, 10.1038/nature09729 Silva, 2008, Promotion of reprogramming to ground state pluripotency by signal inhibition, PLoS Biol., 6, e253, 10.1371/journal.pbio.0060253 Eminli, 2008, Reprogramming of neural progenitor cells into induced pluripotent stem cells in the absence of exogenous Sox2 expression, Stem Cells, 26, 2467, 10.1634/stemcells.2008-0317 Yamaguchi, 2011, Sox2 expression effects on direct reprogramming efficiency as determined by alternative somatic cell fate, Stem Cell Res., 6, 177, 10.1016/j.scr.2010.09.004 Carey, 2011, Reprogramming factor stoichiometry influences the epigenetic state and biological properties of induced pluripotent stem cells, Cell Stem Cell, 9, 588, 10.1016/j.stem.2011.11.003 Papapetrou, 2009, Stoichiometric and temporal requirements of Oct4, Sox2, Klf4, and c-Myc expression for efficient human iPSC induction and differentiation, Proc. Natl. Acad. Sci. U.S.A., 106, 12759, 10.1073/pnas.0904825106 Tiemann, 2011, Optimal reprogramming factor stoichiometry increases colony numbers and affects molecular characteristics of murine induced pluripotent stem cells, Cytometry A, 79, 426, 10.1002/cyto.a.21072 Nagamatsu, 2012, Optimal ratio of transcription factors for somatic cell reprogramming, J. Biol. Chem., 287, 36273, 10.1074/jbc.M112.380683 Radzisheuskaya, 2013, A defined Oct4 level governs cell state transitions of pluripotency entry and differentiation into all embryonic lineages, Nat. Cell Biol., 15, 579, 10.1038/ncb2742 Karwacki-Neisius, 2013, Reduced Oct4 expression directs a robust pluripotent state with distinct signaling activity and increased enhancer occupancy by Oct4 and Nanog, Cell Stem Cell, 12, 531, 10.1016/j.stem.2013.04.023 Finley, 1999, BMP-4 inhibits neural differentiation of murine embryonic stem cells, J. Neurobiol., 40, 271, 10.1002/(SICI)1097-4695(19990905)40:3<271::AID-NEU1>3.0.CO;2-C Ying, 2003, BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3, Cell, 115, 281, 10.1016/S0092-8674(03)00847-X Shimozaki, 2003, Involvement of Oct3/4 in the enhancement of neuronal differentiation of ES cells in neurogenesis-inducing cultures, Development, 130, 2505, 10.1242/dev.00476 Hammachi, 2012, Transcriptional activation by Oct4 is sufficient for the maintenance and induction of pluripotency, Cell Rep., 1, 99, 10.1016/j.celrep.2011.12.002 Cirillo, 2002, Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4, Mol. Cell, 9, 279, 10.1016/S1097-2765(02)00459-8 Yang, 2011, Geminin escapes degradation in G1 of mouse pluripotent cells and mediates the expression of Oct4, Sox2, and Nanog, Curr. Biol., 21, 692, 10.1016/j.cub.2011.03.026 Theunissen, 2011, Nanog overcomes reprogramming barriers and induces pluripotency in minimal conditions, Curr. Biol., 21, 65, 10.1016/j.cub.2010.11.074 Polo, 2012, A molecular roadmap of reprogramming somatic cells into iPS cells, Cell, 151, 1617, 10.1016/j.cell.2012.11.039 O’Malley, 2013, High-resolution analysis with novel cell-surface markers identifies routes to iPS cells, Nature, 499, 88, 10.1038/nature12243 Oka, 2013, Differential role for transcription factor Oct4 nucleocytoplasmic dynamics in somatic cell reprogramming and self-renewal of embryonic stem cells, J. Biol. Chem., 288, 15085, 10.1074/jbc.M112.448837 Plachta, 2011, Oct4 kinetics predict cell lineage patterning in the early mammalian embryo, Nat. Cell Biol., 13, 117, 10.1038/ncb2154 Faunes, 2013, A membrane-associated beta-catenin/Oct4 complex correlates with ground-state pluripotency in mouse embryonic stem cells, Development, 140, 1171, 10.1242/dev.085654 Frum, 2013, Oct4 cell-autonomously promotes primitive endoderm development in the mouse blastocyst, Dev. Cell, 25, 610, 10.1016/j.devcel.2013.05.004 Aksoy, 2013, Oct4 switches partnering from Sox2 to Sox17 to reinterpret the enhancer code and specify endoderm, EMBO J., 32, 938, 10.1038/emboj.2013.31 Zeineddine, 2006, Oct-3/4 dose dependently regulates specification of embryonic stem cells toward a cardiac lineage and early heart development, Dev. Cell, 11, 535, 10.1016/j.devcel.2006.07.013 Teo, 2011, Pluripotency factors regulate definitive endoderm specification through eomesodermin, Genes Dev., 25, 238, 10.1101/gad.607311 Palmieri, 1994, Oct-4 transcription factor is differentially expressed in the mouse embryo during establishment of the first two extraembryonic cell lineages involved in implantation, Dev. Biol., 166, 259, 10.1006/dbio.1994.1312 Guo, 2010, Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst, Dev. Cell, 18, 675, 10.1016/j.devcel.2010.02.012 Downs, 2008, Systematic localization of Oct-3/4 to the gastrulating mouse conceptus suggests manifold roles in mammalian development, Dev. Dyn., 237, 464, 10.1002/dvdy.21438 Yeom, 1996, Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells, Development, 122, 881, 10.1242/dev.122.3.881 Deveale, 2013, Oct4 is required ∼e7.5 for proliferation in the primitive streak, PLoS Genet., 9, e1003957, 10.1371/journal.pgen.1003957 Young, 2011, Control of the embryonic stem cell state, Cell, 144, 940, 10.1016/j.cell.2011.01.032 Whyte, 2013, Master transcription factors and mediator establish super-enhancers at key cell identity genes, Cell, 153, 307, 10.1016/j.cell.2013.03.035 Whyte, 2012, Enhancer decommissioning by LSD1 during embryonic stem cell differentiation, Nature, 482, 221, 10.1038/nature10805 Pardo, 2010, An expanded Oct4 interaction network: implications for stem cell biology, development, and disease, Cell Stem Cell, 6, 382, 10.1016/j.stem.2010.03.004 van den Berg, 2010, An Oct4-centered protein interaction network in embryonic stem cells, Cell Stem Cell, 6, 369, 10.1016/j.stem.2010.02.014 Ding, 2012, Oct4 links multiple epigenetic pathways to the pluripotency network, Cell Res., 22, 155, 10.1038/cr.2011.179 Palmqvist, 2005, Correlation of murine embryonic stem cell gene expression profiles with functional measures of pluripotency, Stem Cells, 23, 663, 10.1634/stemcells.2004-0157 Glover, 2006, Meta-analysis of differentiating mouse embryonic stem cell gene expression kinetics reveals early change of a small gene set, PLoS Comput. Biol., 2, e158, 10.1371/journal.pcbi.0020158 Kaji, 2006, The NuRD component Mbd3 is required for pluripotency of embryonic stem cells, Nat. Cell Biol., 8, 285, 10.1038/ncb1372 Wang, 2009, The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation, Nat. Genet., 41, 125, 10.1038/ng.268 Reynolds, 2012, NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment, Cell Stem Cell, 10, 583, 10.1016/j.stem.2012.02.020 Szabo, 2010, Direct conversion of human fibroblasts to multilineage blood progenitors, Nature, 468, 521, 10.1038/nature09591 Efe, 2011, Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy, Nat. Cell Biol., 13, 215, 10.1038/ncb2164 Kim, 2011, Direct reprogramming of mouse fibroblasts to neural progenitors, Proc. Natl. Acad. Sci. U.S.A., 108, 7838, 10.1073/pnas.1103113108 Thier, 2012, Direct conversion of fibroblasts into stably expandable neural stem cells, Cell Stem Cell, 10, 473, 10.1016/j.stem.2012.03.003 Hou, 2013, Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds, Science, 341, 651, 10.1126/science.1239278