17
Views
5
CrossRef citations to date
0
Altmetric
Research Article

Dormant Pluripotent Cells Emerge during Neural Differentiation of Embryonic Stem Cells in a FoxO3-Dependent Manner

&
Article: e00417-16 | Received 16 Jul 2016, Accepted 04 Dec 2016, Published online: 17 Mar 2023

REFERENCES

  • Williams RL, Hilton DJ, Pease S, Willson TA, Stewart CL, Gearing DP, Wagner EF, Metcalf D, Nicola NA, Gough NM. 1988. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336:684–687. https://doi.org/10.1038/336684a0.
  • Smith AG, Heath JK, Donaldson DD, Wong GG, Moreau J, Stahl M, Rogers D. 1988. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336:688–690. https://doi.org/10.1038/336688a0.
  • Ying QL, Nichols J, Chambers I, Smith A. 2003. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115:281–292. https://doi.org/10.1016/S0092-8674(03)00847-X.
  • Kunath T, Saba-El-Leil MK, Almousailleakh M, Wray J, Meloche S, Smith A. 2007. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134:2895–2902. https://doi.org/10.1242/dev.02880.
  • Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, Woodgett J, Cohen P, Smith A. 2008. The ground state of embryonic stem cell self-renewal. Nature 453:519–523. https://doi.org/10.1038/nature06968.
  • Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, Nakanishi S, Nishikawa SI, Sasai Y. 2000. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28:31–40. https://doi.org/10.1016/S0896-6273(00)00083-0.
  • Watanabe K, Kamiya D, Nishiyama A, Katayama T, Nozaki S, Kawasaki H, Watanabe Y, Mizuseki K, Sasai Y. 2005. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8:288–296. https://doi.org/10.1038/nn1402.
  • Smukler SR, Runciman SB, Xu S, van der Kooy D. 2006. Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J Cell Biol 172:79–90. https://doi.org/10.1083/jcb.200508085.
  • Eiraku M, Watanabe K, Matsuo-Takasaki M, Kawada M, Yonemura S, Matsumura M, Wataya T, Nishiyama A, Muguruma K, Sasai Y. 2008. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3:519–532. https://doi.org/10.1016/j.stem.2008.09.002.
  • Ying QL, Stavridis M, Griffiths D, Li M, Smith A. 2003. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21:183–186. https://doi.org/10.1038/nbt780.
  • Fukuda H, Takahashi J, Watanabe K, Hayashi H, Morizane A, Koyanagi M, Sasai Y, Hashimoto N. 2006. Fluorescence-activated cell sorting-based purification of embryonic stem cell-derived neural precursors averts tumor formation after transplantation. Stem Cells 24:763–771. https://doi.org/10.1634/stemcells.2005-0137.
  • Doi D, Morizane A, Kikuchi T, Onoe H, Hayashi T, Kawasaki T, Motono M, Sasai Y, Saiki H, Gomi M, Yoshikawa T, Hayashi H, Shinoyama M, Refaat MM, Suemori H, Miyamoto S, Takahashi J. 2012. Prolonged maturation culture favors a reduction in the tumorigenicity and the dopaminergic function of human ESC-derived neural cells in a primate model of Parkinson's disease. Stem Cells 30:935–945. https://doi.org/10.1002/stem.1060.
  • Darabi R, Gehlbach K, Bachoo RM, Kamath S, Osawa M, Kamm KE, Kyba M, Perlingeiro RC. 2008. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat Med 14:134–143. https://doi.org/10.1038/nm1705.
  • Endo K, Hayashi K, Saito H. 2016. High-resolution identification and separation of living cell types by multiple microRNA-responsive synthetic mRNAs. Sci Rep 6:21991. https://doi.org/10.1038/srep21991.
  • Tohyama S, Hattori F, Sano M, Hishiki T, Nagahata Y, Matsuura T, Hashimoto H, Suzuki T, Yamashita H, Satoh Y, Egashira T, Seki T, Muraoka N, Yamakawa H, Ohgino Y, Tanaka T, Yoichi M, Yuasa S, Murata M, Suematsu M, Fukuda K. 2013. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 12:127–137. https://doi.org/10.1016/j.stem.2012.09.013.
  • Tomizawa M, Shinozaki F, Sugiyama T, Yamamoto S, Sueishi M, Yoshida T. 2013. Survival of primary human hepatocytes and death of induced pluripotent stem cells in media lacking glucose and arginine. PLoS One 8:e71897. https://doi.org/10.1371/journal.pone.0071897.
  • Ben-David U, Gan QF, Golan-Lev T, Arora P, Yanuka O, Oren YS, Leikin-Frenkel A, Graf M, Garippa R, Boehringer M, Gromo G, Benvenisty N. 2013. Selective elimination of human pluripotent stem cells by an oleate synthesis inhibitor discovered in a high-throughput screen. Cell Stem Cell 12:167–179. https://doi.org/10.1016/j.stem.2012.11.015.
  • Toyooka Y, Shimosato D, Murakami K, Takahashi K, Niwa H. 2008. Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 135:909–918. https://doi.org/10.1242/dev.017400.
  • Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A. 2007. Nanog safeguards pluripotency and mediates germline development. Nature 450:1230–1234. https://doi.org/10.1038/nature06403.
  • Niwa H, Ogawa K, Shimosato D, Adachi K. 2009. A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460:118–122. https://doi.org/10.1038/nature08113.
  • Kalmar T, Lim C, Hayward P, Munoz-Descalzo S, Nichols J, Garcia-Ojalvo J, Martinez Arias A. 2009. Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biol 7:e1000149. https://doi.org/10.1371/journal.pbio.1000149.
  • MacArthur BD, Sevilla A, Lenz M, Muller FJ, Schuldt BM, Schuppert AA, Ridden SJ, Stumpf PS, Fidalgo M, Ma'ayan A, Wang J, Lemischka IR. 2012. Nanog-dependent feedback loops regulate murine embryonic stem cell heterogeneity. Nat Cell Biol 14:1139–1147. https://doi.org/10.1038/ncb2603.
  • Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RD. 2007. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448:196–199. https://doi.org/10.1038/nature05972.
  • Rugg-Gunn PJ, Cox BJ, Lanner F, Sharma P, Ignatchenko V, McDonald AC, Garner J, Gramolini AO, Rossant J, Kislinger T. 2012. Cell-surface proteomics identifies lineage-specific markers of embryo-derived stem cells. Dev Cell 22:887–901. https://doi.org/10.1016/j.devcel.2012.01.005.
  • Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L. 2007. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448:191–195. https://doi.org/10.1038/nature05950.
  • Eiraku M, Sasai Y. 2012. Self-formation of layered neural structures in three-dimensional culture of ES cells. Curr Opin Neurobiol 22:768–777. https://doi.org/10.1016/j.conb.2012.02.005.
  • Seoane J, Le HV, Shen L, Anderson SA, Massague J. 2004. Integration of Smad and Forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117:211–223. https://doi.org/10.1016/S0092-8674(04)00298-3.
  • Warr MR, Binnewies M, Flach J, Reynaud D, Garg T, Malhotra R, Debnath J, Passegue E. 2013. FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 494:323–327. https://doi.org/10.1038/nature11895.
  • Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, Burgering BM. 2002. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419:316–321. https://doi.org/10.1038/nature01036.
  • Miyamoto K, Araki KY, Naka K, Arai F, Takubo K, Yamazaki S, Matsuoka S, Miyamoto T, Ito K, Ohmura M, Chen C, Hosokawa K, Nakauchi H, Nakayama K, Nakayama KI, Harada M, Motoyama N, Suda T, Hirao A. 2007. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1:101–112. https://doi.org/10.1016/j.stem.2007.02.001.
  • Paik JH, Ding Z, Narurkar R, Ramkissoon S, Muller F, Kamoun WS, Chae SS, Zheng H, Ying H, Mahoney J, Hiller D, Jiang S, Protopopov A, Wong WH, Chin L, Ligon KL, DePinho RA. 2009. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5:540–553. https://doi.org/10.1016/j.stem.2009.09.013.
  • Gopinath SD, Webb AE, Brunet A, Rando TA. 2014. FOXO3 promotes quiescence in adult muscle stem cells during the process of self-renewal. Stem Cell Rep 2:414–426. https://doi.org/10.1016/j.stemcr.2014.02.002.
  • Renault VM, Rafalski VA, Morgan AA, Salih DA, Brett JO, Webb AE, Villeda SA, Thekkat PU, Guillerey C, Denko NC, Palmer TD, Butte AJ, Brunet A. 2009. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5:527–539. https://doi.org/10.1016/j.stem.2009.09.014.
  • Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, McDowell EP, Lazo-Kallanian S, Williams IR, Sears C, Armstrong SA, Passegue E, DePinho RA, Gilliland DG. 2007. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128:325–339. https://doi.org/10.1016/j.cell.2007.01.003.
  • Nagashima T, Shigematsu N, Maruki R, Urano Y, Tanaka H, Shimaya A, Shimokawa T, Shibasaki M. 2010. Discovery of novel Forkhead box O1 inhibitors for treating type 2 diabetes: improvement of fasting glycemia in diabetic db/db mice. Mol Pharmacol 78:961–970. https://doi.org/10.1124/mol.110.065714.
  • Zhang X, Yalcin S, Lee DF, Yeh TY, Lee SM, Su J, Mungamuri SK, Rimmele P, Kennedy M, Sellers R, Landthaler M, Tuschl T, Chi NW, Lemischka I, Keller G, Ghaffari S. 2011. FOXO1 is an essential regulator of pluripotency in human embryonic stem cells. Nat Cell Biol 13:1092–1099. https://doi.org/10.1038/ncb2293.
  • Wang Y, Tian C, Zheng JC. 2013. FoxO3a contributes to the reprogramming process and the differentiation of induced pluripotent stem cells. Stem Cells Dev 22:2954–2963. https://doi.org/10.1089/scd.2013.0044.
  • Lutzner N, Kalbacher H, Krones-Herzig A, Rosl F. 2012. FOXO3 is a glucocorticoid receptor target and regulates LKB1 and its own expression based on cellular AMP levels via a positive autoregulatory loop. PLoS One 7:e42166. https://doi.org/10.1371/journal.pone.0042166.
  • Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G. 1997. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389:994–999. https://doi.org/10.1038/40194.
  • Lin K, Dorman JB, Rodan A, Kenyon C. 1997. daf-16: an HNF-3/Forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278:1319–1322. https://doi.org/10.1126/science.278.5341.1319.
  • Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–868. https://doi.org/10.1016/S0092-8674(00)80595-4.
  • Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG. 2003. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2:28. https://doi.org/10.1186/1475-4924-2-28.
  • Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D. 2003. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13:2004–2008. https://doi.org/10.1016/j.cub.2003.10.031.
  • Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC. 2004. The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci U S A 101:3329–3335. https://doi.org/10.1073/pnas.0308061100.
  • Zheng B, Jeong JH, Asara JM, Yuan YY, Granter SR, Chin L, Cantley LC. 2009. Oncogenic B-RAF negatively regulates the tumor suppressor LKB1 to promote melanoma cell proliferation. Mol Cell 33:237–247. https://doi.org/10.1016/j.molcel.2008.12.026.
  • Chae HD, Lee MR, Broxmeyer HE. 2012. 5-Aminoimidazole-4-carboxyamide ribonucleoside induces G(1)/S arrest and Nanog downregulation via p53 and enhances erythroid differentiation. Stem Cells 30:140–149. https://doi.org/10.1002/stem.778.
  • Shi X, Wu Y, Ai Z, Liu X, Yang L, Du J, Shao J, Guo Z, Zhang Y. 2013. AICAR sustains J1 mouse embryonic stem cell self-renewal and pluripotency by regulating transcription factor and epigenetic modulator expression. Cell Physiol Biochem 32:459–475. https://doi.org/10.1159/000354451.
  • Scognamiglio R, Cabezas-Wallscheid N, Thier MC, Altamura S, Reyes A, Prendergast AM, Baumgartner D, Carnevalli LS, Atzberger A, Haas S, von Paleske L, Boroviak T, Worsdorfer P, Essers MA, Kloz U, Eisenman RN, Edenhofer F, Bertone P, Huber W, van der Hoeven F, Smith A, Trumpp A. 2016. Myc depletion induces a pluripotent dormant state mimicking diapause. Cell 164:668–680. https://doi.org/10.1016/j.cell.2015.12.033.
  • Delpuech O, Griffiths B, East P, Essafi A, Lam EW, Burgering B, Downward J, Schulze A. 2007. Induction of Mxi1-SR alpha by FOXO3a contributes to repression of Myc-dependent gene expression. Mol Cell Biol 27:4917–4930. https://doi.org/10.1128/MCB.01789-06.
  • Gan B, Lim C, Chu G, Hua S, Ding Z, Collins M, Hu J, Jiang S, Fletcher-Sananikone E, Zhuang L, Chang M, Zheng H, Wang YA, Kwiatkowski DJ, Kaelin WG, Jr, Signoretti S, DePinho RA. 2010. FoxOs enforce a progression checkpoint to constrain mTORC1-activated renal tumorigenesis. Cancer Cell 18:472–484. https://doi.org/10.1016/j.ccr.2010.10.019.
  • Kress TR, Cannell IG, Brenkman AB, Samans B, Gaestel M, Roepman P, Burgering BM, Bushell M, Rosenwald A, Eilers M. 2011. The MK5/PRAK kinase and Myc form a negative feedback loop that is disrupted during colorectal tumorigenesis. Mol Cell 41:445–457. https://doi.org/10.1016/j.molcel.2011.01.023.
  • Seoane J, Le HV, Massague J. 2002. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419:729–734. https://doi.org/10.1038/nature01119.
  • Giancotti FG. 2013. Mechanisms governing metastatic dormancy and reactivation. Cell 155:750–764. https://doi.org/10.1016/j.cell.2013.10.029.
  • Naka K, Hoshii T, Muraguchi T, Tadokoro Y, Ooshio T, Kondo Y, Nakao S, Motoyama N, Hirao A. 2010. TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 463:676–680. https://doi.org/10.1038/nature08734.
  • Sunayama J, Sato A, Matsuda K, Tachibana K, Watanabe E, Seino S, Suzuki K, Narita Y, Shibui S, Sakurada K, Kayama T, Tomiyama A, Kitanaka C. 2011. FoxO3a functions as a key integrator of cellular signals that control glioblastoma stem-like cell differentiation and tumorigenicity. Stem Cells 29:1327–1337. https://doi.org/10.1002/stem.696.
  • Niwa H, Masui S, Chambers I, Smith AG, Miyazaki J. 2002. Phenotypic complementation establishes requirements for specific POU domain and generic transactivation function of Oct-3/4 in embryonic stem cells. Mol Cell Biol 22:1526–1536. https://doi.org/10.1128/MCB.22.5.1526-1536.2002.
  • Ogawa K, Matsui H, Ohtsuka S, Niwa H. 2004. A novel mechanism for regulating clonal propagation of mouse ES cells. Genes Cells 9:471–477. https://doi.org/10.1111/j.1356-9597.2004.00736.x.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.