Dynamic stem cell states: naive to primed pluripotency in rodents and humans (original) (raw)
Hanna, J. H., Saha, K. & Jaenisch, R. Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell143, 508–525 (2010). ArticleCASPubMedPubMed Central Google Scholar
Hackett, J. A. & Surani, M. A. Regulatory principles of pluripotency: from the ground state up. Cell Stem Cell15, 416–430 (2014). ArticleCASPubMed Google Scholar
Manor, Y. S., Massarwa, R. & Hanna, J. H. Establishing the human naive pluripotent state. Curr. Opin. Genet. Dev.34, 35–45 (2015). ArticleCASPubMed Google Scholar
Thomson, J. A. et al. Embryonic stem cell lines derived from human blastocysts. Science282, 1145–1147 (1998). The first study to derive primed ES cells from human blastocysts. ArticleCASPubMed Google Scholar
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
Tesar, P. J. et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature448, 196–199 (2007). ArticleCASPubMed Google Scholar
Brons, I. G. et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature448, 191–195 (2007). References 9 and 10 describe the derivation of primed EpiSC lines from rodent post-implantation epiblasts. ArticleCASPubMed Google Scholar
Leitch, H. G. et al. Embryonic germ cells from mice and rats exhibit properties consistent with a generic pluripotent ground state. Development137, 2279–2287 (2010). ArticleCASPubMedPubMed Central Google Scholar
Matsui, Y., Zsebo, K. & Hogan, B. L. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell70, 841–847 (1992). The first study to describe the generation of pluripotent ES cell-like cells from mouse embryonic PGCs. ArticleCASPubMed Google Scholar
Kanatsu-Shinohara, M. et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell119, 1001–1012 (2004). The first study to describe the generation of pluripotent ES cell-like cells from mouse spermatogonial stem cells. ArticleCASPubMed Google Scholar
Tanaka, T., Kanatsu-Shinohara, M., Hirose, M., Ogura, A. & Shinohara, T. Pluripotent cell derivation from male germline cells by suppression of Dmrt1 and Trp53. J. Reprod. Dev.61, 473–484 (2015). ArticleCASPubMedPubMed Central Google Scholar
Ko, K. et al. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell5, 87–96 (2009). ArticleCASPubMed Google Scholar
Ko, K. et al. Human adult germline stem cells in question. Nature465, E1; discussion E3 (2010). ArticleCASPubMed Google Scholar
Shamblott, M. J. et al. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc. Natl Acad. Sci. USA95, 13726–13731 (1998). ArticleCASPubMedPubMed Central Google Scholar
Yamada, M. et al. Human oocytes reprogram adult somatic nuclei of a type 1 diabetic to diploid pluripotent stem cells. Nature510, 533–536 (2014). ArticleCASPubMed Google Scholar
Tachibana, M. et al. Human embryonic stem cells derived by somatic cell nuclear transfer. Cell153, 1228–1238 (2013). The first study to generate validated human NT-ES cells from somatic fibroblasts. ArticleCASPubMedPubMed Central Google Scholar
Wakayama, T. et al. Differentiation of embryonic stem cell lines generated from adult somatic cells by nuclear transfer. Science292, 740–743 (2001). This study shows the feasibility of somatic cell nuclear transfer in mice. 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). This is the first study to show directin vitroreprogramming of somatic cells into iPSCs using defined transcription factors. 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
Wernig, M. et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature448, 318–324 (2007). ArticleCASPubMed Google Scholar
Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science318, 1917–1920 (2007). ArticleCASPubMed Google Scholar
Deuse, T. et al. SCNT-derived ESCs with mismatched mitochondria trigger an immune response in allogeneic hosts. Cell Stem Cell16, 33–38 (2015). ArticleCASPubMed Google Scholar
Ma, H. et al. Metabolic rescue in pluripotent cells from patients with mtDNA disease. Nature524, 234–238 (2015). ArticleCASPubMed Google Scholar
Paull, D. et al. Nuclear genome transfer in human oocytes eliminates mitochondrial DNA variants. Nature493, 632–637 (2013). ArticleCASPubMed Google Scholar
Hanna, J. et al. Metastable pluripotent states in NOD-mouse-derived ESCs. Cell Stem Cell4, 513–524 (2009). The first study to define distinct requirements in different mouse strains forin vitroandex vivoconversions between naive and primed pluripotent cells. ArticleCASPubMedPubMed Central Google Scholar
Nichols, J. & Smith, A. Naive and primed pluripotent states. Cell Stem Cell4, 487–492 (2009). ArticleCASPubMed Google Scholar
Han, D. W. et al. Direct reprogramming of fibroblasts into epiblast stem cells. Nat. Cell Biol.13, 66–71 (2011). ArticleCASPubMed Google Scholar
Martin, G. R. & Evans, M. J. Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc. Natl Acad. Sci. USA72, 1441–1445 (1975). ArticleCASPubMedPubMed Central Google Scholar
Smith, A. G. et al. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature336, 688–690 (1988). ArticleCASPubMed Google Scholar
Williams, R. L. et al. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature336, 684–687 (1988). ArticleCASPubMed Google Scholar
Ying, Q. L., Nichols, J., Chambers, I. & Smith, A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self renewal in collaboration with STAT3. Cell115, 281–292 (2003). ArticleCASPubMed Google Scholar
Burdon, T., Stracey, C., Chambers, I., Nichols, J. & Smith, A. Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev. Biol.210, 30–43 (1999). ArticleCASPubMed Google Scholar
Ying, Q. L. et al. The ground state of embryonic stem cell self-renewal. Nature453, 519–523 (2008). A study describing defined 3i naive conditions capable of generating LIF- and STAT3-independent mouse ES cells. ArticleCASPubMedPubMed Central Google Scholar
Buehr, M. et al. Capture of authentic embryonic stem cells from rat blastocysts. Cell135, 1287–1298 (2008). ArticleCASPubMed Google Scholar
Nichols, J. et al. Validated germline-competent embryonic stem cell lines from nonobese diabetic mice. Nat. Med.15, 814–818 (2009). ArticleCASPubMed Google Scholar
Chen, H. et al. Erk signaling is indispensable for genomic stability and self-renewal of mouse embryonic stem cells. Proc. Natl Acad. Sci. USA112, E5936–E5943 (2015). ArticleCASPubMedPubMed Central Google Scholar
Shimizu, T. et al. Dual inhibition of Src and GSK3 maintains mouse embryonic stem cells, whose differentiation is mechanically regulated by Src signaling. Stem Cells30, 1394–1404 (2012). ArticleCASPubMed Google Scholar
Dutta, D. et al. Self-renewal versus lineage commitment of embryonic stem cells: protein kinase C signaling shifts the balance. Stem Cells29, 618–628 (2011). The first study using aPKCi to boost the generation of naive murine iPSCs and ES cells. ArticleCASPubMedPubMed Central Google Scholar
Kolodziejczyk, A. A. et al. Single cell RNA-sequencing of pluripotent states unlocks modular transcriptional variation. Cell Stem Cell17, 471–485 (2015). ArticleCASPubMedPubMed Central Google Scholar
Chen, Y., Blair, K. & Smith, A. Robust self-renewal of rat embryonic stem cells requires fine-tuning of glycogen synthase kinase-3 inhibition. Stem Cell Rep.1, 209–217 (2013). ArticleCAS Google Scholar
Meek, S. et al. Tuning of β-catenin activity is required to stabilize self-renewal of rat embryonic stem cells. Stem Cells31, 2104–2115 (2013). ArticleCASPubMed Google Scholar
Rajendran, G. et al. Inhibition of protein kinase C signaling maintains rat embryonic stem cell pluripotency. J. Biol. Chem.288, 24351–24362 (2013). ArticleCASPubMedPubMed Central Google Scholar
Li, X. et al. Calcineurin-NFAT signaling critically regulates early lineage specification in mouse embryonic stem cells and embryos. Cell Stem Cell8, 46–58 (2011). The first study to show that Src inhibition promotes murine naive pluripotency. ArticleCASPubMed Google Scholar
Nishioka, N. et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell16, 398–410 (2009). This study identifies the role of the HIPPO signalling pathway in epiblast versus trophoblast specification in pre-implantation mouse embryos. CASPubMed Google Scholar
Azzolin, L. et al. YAP/TAZ incorporation in the β-catenin destruction complex orchestrates the Wnt response. Cell158, 157–170 (2014). ArticleCASPubMed Google Scholar
Lian, I. et al. The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev.24, 1106–1118 (2010). ArticleCASPubMedPubMed Central Google Scholar
Wray, J. et al. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat. Cell Biol.13, 838–845 (2011). ArticleCASPubMedPubMed Central Google Scholar
Faunes, F. et al. A membrane-associated β-catenin/Oct4 complex correlates with ground-state pluripotency in mouse embryonic stem cells. Development140, 1171–1183 (2013). ArticleCASPubMedPubMed Central Google Scholar
Morgani, S. M. & Brickman, J. M. LIF supports primitive endoderm expansion during pre-implantation development. Development142, 3488–3499 (2015). ArticleCASPubMed Google Scholar
Maza, I. et al. Transient acquisition of pluripotency during somatic cell transdifferentiation with iPSC reprogramming factors. Nat. Biotechnol.33, 769–774 (2015). ArticleCASPubMedPubMed Central Google Scholar
Carter, A. C., Davis-Dusenbery, B. N., Koszka, K., Ichida, J. K. & Eggan, K. Nanog-independent reprogramming to iPSCs with canonical factors. Stem Cell Rep.2, 119–126 (2014). ArticleCAS Google Scholar
Schwartz, B. A. et al. Nanog is dispensable for the generation of induced pluripotent stem cells. Curr. Biol.24, 347–350 (2014). ArticleCAS Google Scholar
Festuccia, N. et al. Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells. Cell Stem Cell11, 477–490 (2012). ArticleCASPubMedPubMed Central Google Scholar
Yeo, J. C. et al. Klf2 is an essential factor that sustains ground state pluripotency. Cell Stem Cell14, 864–872 (2014). ArticleCASPubMed Google Scholar
Reynolds, N. et al. NuRD suppresses pluripotency gene expression to promote transcriptional heterogeneity and lineage commitment. Cell Stem Cell10, 583–594 (2012). This study establishes MBD3–NuRD as a repressor of naive pluripotency-promoting genes in mouse ES cells. ArticleCASPubMedPubMed Central Google Scholar
Rais, Y. et al. Deterministic direct reprogramming of somatic cells to pluripotency. Nature502, 65–70 (2013). ArticleCASPubMed Google Scholar
Loh, K. M. & Lim, B. A precarious balance: pluripotency factors as lineage specifiers. Cell Stem Cell8, 363–369 (2011). ArticleCASPubMed Google Scholar
Geula, S. et al. m6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation. Science347, 1002–1006 (2015). The first study to show an opposing dependence on epigenetic repressors between mouse naive and primed PSCs. ArticleCASPubMed Google Scholar
Huang, Y. et al. In vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation. Cell Rep.2, 1571–1578 (2012). ArticleCASPubMed Google Scholar
Buecker, C. et al. Reorganization of enhancer patterns in transition from naive to primed pluripotency. Cell Stem Cell14, 838–853 (2014). ArticleCASPubMedPubMed Central Google Scholar
Gafni, O. et al. Derivation of novel human ground state naive pluripotent stem cells. Nature504, 282–286 (2013). The first study to generate genetically unmodified and indefinitely stable human MEK-independent naive PSCs, which were also capable of generating advanced mouse–human chimeric embryos. ArticleCASPubMed Google Scholar
Factor, D. C. et al. Epigenomic comparison reveals activation of “seed” enhancers during transition from naive to primed pluripotency. Cell Stem Cell14, 854–863 (2014). ArticleCASPubMedPubMed Central Google Scholar
Kim, H. et al. Modulation of β-catenin function maintains mouse epiblast stem cell and human embryonic stem cell self-renewal. Nat. Commun.4, 2403 (2013). ArticlePubMed Google Scholar
Kojima, Y. et al. The transcriptional and functional properties of mouse epiblast stem cells resemble the anterior primitive streak. Cell Stem Cell14, 107–120 (2014). ArticleCASPubMed Google Scholar
Wu, J. et al. An alternative pluripotent state confers interspecies chimaeric competency. Nature521, 316–321 (2015). References 74 and 75 are the first two studies describing region-specific features of mouse EpiSCs expandedin vitro. ArticleCASPubMedPubMed Central Google Scholar
Han, D. W. et al. Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell143, 617–627 (2010). ArticleCASPubMed Google Scholar
Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S. & Saitou, M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell146, 519–532 (2011). ArticleCASPubMed Google Scholar
Guo, G. et al. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development136, 1063–1069 (2009). Together with reference 30, one of two studies that are the first to show conversion between murine naive and primed pluripotent cells. ArticleCASPubMedPubMed Central Google Scholar
Bao, S. et al. Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature461, 1292–1295 (2009). ArticleCASPubMed Google Scholar
Gillich, A. et al. Epiblast stem cell-based system reveals reprogramming synergy of germline factors. Cell Stem Cell10, 425–439 (2012). ArticleCASPubMedPubMed Central Google Scholar
Greber, B. et al. Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell6, 215–226 (2010). ArticleCASPubMed Google Scholar
Ficz, G. et al. FGF signaling inhibition in ESCs drives rapid genome-wide demethylation to the epigenetic ground state of pluripotency. Cell Stem Cell13, 351–359 (2013). ArticleCASPubMedPubMed Central Google Scholar
Hackett, J. A. et al. Synergistic mechanisms of DNA demethylation during transition to ground-state pluripotency. Stem Cell Rep.1, 518–531 (2013). ArticleCAS Google Scholar
Galonska, C., Ziller, M. J., Karnik, R. & Meissner, A. Ground state conditions induce rapid reorganization of core pluripotency factor binding before global epigenetic reprogramming. Cell Stem Cell17, 462–470 (2015). ArticleCASPubMedPubMed Central Google Scholar
Tee, W. W., Shen, S. S., Oksuz, O., Narendra, V. & Reinberg, D. Erk1/2 activity promotes chromatin features and RNAPII phosphorylation at developmental promoters in mouse ESCs. Cell156, 678–690 (2014). ArticleCASPubMedPubMed Central Google Scholar
Bertero, A. et al. Activin/Nodal signaling and NANOG orchestrate human embryonic stem cell fate decisions by controlling the H3K4me3 chromatin mark. Genes Dev.29, 702–717 (2015). ArticleCASPubMedPubMed Central Google Scholar
Chia, N. Y. et al. A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature468, 316–320 (2010). ArticleCASPubMed Google Scholar
Shipony, Z. et al. Dynamic and static maintenance of epigenetic memory in pluripotent and somatic cells. Nature513, 115–119 (2014). ArticleCASPubMed Google Scholar
Betschinger, J. et al. Exit from pluripotency is gated by intracellular redistribution of the bHLH transcription factor Tfe3. Cell153, 335–347 (2013). ArticleCASPubMedPubMed Central Google Scholar
Hanna, J. et al. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc. Natl Acad. Sci. USA107, 9222–9227 (2010). This study provides the first evidence for alternative transgene-dependent human PSCs that can be expanded in conditions containing 2i and LIF. ArticleCASPubMedPubMed Central Google Scholar
Theunissen, T. W. et al. Systematic identification of culture conditions for induction and maintenance of naive human pluripotency. Cell Stem Cell15, 471–487 (2014). ArticleCASPubMedPubMed Central Google Scholar
Takashima, Y. et al. Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell158, 1254–1269 (2014). ArticleCASPubMedPubMed Central Google Scholar
Blakeley, P. et al. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development142, 3151–3165 (2015). ArticleCASPubMedPubMed Central Google Scholar
Shakiba, N. et al. CD24 tracks divergent pluripotent states in mouse and human cells. Nat. Commun.6, 7329 (2015). ArticleCASPubMed Google Scholar
Barakat, T. S. et al. Stable X chromosome reactivation in female human induced pluripotent stem cells. Stem Cell Rep.4, 199–208 (2015). ArticleCAS Google Scholar
Chan, Y. S. et al. Induction of a human pluripotent state with distinct regulatory circuitry that resembles preimplantation epiblast. Cell Stem Cell13, 663–675 (2013). ArticleCASPubMed Google Scholar
Duggal, G. et al. Alternative routes to induce naive pluripotency in human embryonic stem cells. Stem Cells33, 2686–2698 (2015). ArticleCASPubMed Google Scholar
Chen, H. et al. Reinforcement of STAT3 activity reprogrammes human embryonic stem cells to naive-like pluripotency. Nat. Commun.6, 7095 (2015). ArticleCASPubMed Google Scholar
Ohgushi, M., Minaguchi, M. & Sasai, Y. Rho-signaling-directed YAP/TAZ activity underlies the long-term survival and expansion of human embryonic stem cells. Cell Stem Cell17, 448–461 (2015). A study connecting RHO and HIPPO signalling pathways in the maintenance of human primed pluripotency. ArticleCASPubMed Google Scholar
Kameda, T. & Thomson, J. A. Human ERas gene has an upstream premature polyadenylation signal that results in a truncated, noncoding transcript. Stem Cells23, 1535–1540 (2005). ArticleCASPubMed Google Scholar
Boroviak, T. et al. Lineage-specific profiling delineates the emergence and progression of naive pluripotency in mammalian embryogenesis. Dev. Cell35, 366–382 (2015). ArticleCASPubMedPubMed Central Google Scholar
Buecker, C. & Wysocka, J. Enhancers as information integration hubs in development: lessons from genomics. Trends Genet.28, 276–284 (2012). ArticleCASPubMedPubMed Central Google Scholar
Karwacki-Neisius, V. et al. Reduced Oct4 expression directs a robust pluripotent state with distinct signaling activity and increased enhancer occupancy by Oct4 and Nanog. Cell Stem Cell12, 531–545 (2013). ArticleCASPubMedPubMed Central Google Scholar
Boroviak, T., Loos, R., Bertone, P., Smith, A. & Nichols, J. The ability of inner-cell-mass cells to self-renew as embryonic stem cells is acquired following epiblast specification. Nat. Cell Biol.16, 516–528 (2014). ArticleCASPubMedPubMed Central Google Scholar
Osafune, K. et al. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat. Biotechnol.26, 313–315 (2008). ArticleCASPubMed Google Scholar
Irie, N. et al. SOX17 is a critical specifier of human primordial germ cell fate. Cell160, 253–268 (2015). The first study to generate human PGC-like cellsin vitroand demonstrate altered function of human MEK-independent naive PSCs. ArticleCASPubMedPubMed Central Google Scholar
Bock, C. et al. Reference maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell144, 439–452 (2011). ArticleCASPubMedPubMed Central Google Scholar
Kobayashi, T. et al. Generation of rat pancreas in mouse by interspecific blastocyst injection of pluripotent stem cells. Cell142, 787–799 (2010). The first study to generate cross-species chimerism between mice and rats by microinjecting naive PSCs from one species into host blastocysts from the other. ArticleCASPubMed Google Scholar
Chen, Y. et al. Generation of cynomolgus monkey chimeric fetuses using embryonic stem cells. Cell Stem Cell17, 116–124 (2015). A study demonstrating the first chimeric monkey fetuses to be generated, using naive monkey ES cells established in NHSM conditions supplemented with vitamin C. ArticleCASPubMed Google Scholar
Fang, R. et al. Generation of naive induced pluripotent stem cells from rhesus monkey fibroblasts. Cell Stem Cell15, 488–496 (2014). ArticleCASPubMed Google Scholar
Bock, A. S., Leigh, N. D. & Bryda, E. C. Effect of Gsk3 inhibitor CHIR99021 on aneuploidy levels in rat embryonic stem cells. In Vitro Cell Dev. Biol. Anim.50, 572–579 (2014). ArticleCASPubMedPubMed Central Google Scholar
Kim, K. et al. Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat. Biotechnol.29, 1117–1119 (2011). ArticleCASPubMedPubMed Central Google Scholar
Choi, J. et al. A comparison of genetically matched cell lines reveals the equivalence of human iPSCs and ESCs. Nat. Biotechnol.33, 1173–1181 (2015). ArticleCASPubMedPubMed Central Google Scholar
Pastor, W. A. et al. Naive human pluripotent cells feature a methylation landscape devoid of blastocyst or germline memory. Cell Stem Cellhttp://dx.doi.org/10.1016/j.stem.2016.01.019 (2016).