Skip to main content
SpringerLink
Log in

Cell cycle and cell fate in the developing nervous system: the role of CDC25B phosphatase

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Deciphering the core machinery of the cell cycle and cell division has been primarily the focus of cell biologists, while developmental biologists have identified the signaling pathways and transcriptional programs controlling cell fate choices. As a result, until recently, the interplay between these two fundamental aspects of biology have remained largely unexplored. Increasing data show that the cell cycle and regulators of the core cell cycle machinery are important players in cell fate decisions during neurogenesis. Here, we summarize recent data describing how cell cycle dynamics affect the switch between proliferation and differentiation, with an emphasis on the roles played by the cell cycle regulators, the CDC25 phosphatases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agathocleous M, Locker M, Harris WA, Perron M (2007) A general role of hedgehog in the regulation of proliferation. Cell Cycle 6:156–159

    CAS  PubMed  Google Scholar 

  • Ahlstrom JD, Erickson CA (2009) New views on the neural crest epithelial-mesenchymal transition and neuroepithelial interkinetic nuclear migration. Commun Integr Biol 2:489–493

    PubMed Central  PubMed  Google Scholar 

  • Akai J, Halley PA, Storey KG (2005) FGF-dependent Notch signaling maintains the spinal cord stem zone. Genes Dev 19:2877–2887

    CAS  PubMed Central  PubMed  Google Scholar 

  • Alvarez-Medina R, Le Dreau G, Ros M, Marti E (2009) Hedgehog activation is required upstream of Wnt signalling to control neural progenitor proliferation. Development 136:3301–3309

    CAS  PubMed  Google Scholar 

  • Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB (2011) Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2:154

    PubMed Central  PubMed  Google Scholar 

  • Ashcroft NR, Kosinski ME, Wickramasinghe D, Donovan PJ, Golden A (1998) The four cdc25 genes from the nematode Caenorhabditis elegans. Gene 214:59–66

    CAS  PubMed  Google Scholar 

  • Benazeraf B, Chen Q, Peco E, Lobjois V, Medevielle F, Ducommun B, Pituello F (2006) Identification of an unexpected link between the Shh pathway and a G2/M regulator, the phosphatase CDC25B. Dev Biol 294:133–147

    CAS  PubMed  Google Scholar 

  • Bertrand N, Medevielle F, Pituello F (2000) FGF signalling controls the timing of Pax6 activation in the neural tube. Development 127:4837–4843

    CAS  PubMed  Google Scholar 

  • Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517–530

    CAS  PubMed  Google Scholar 

  • Bienvenu F, Jirawatnotai S, Elias JE, Meyer CA, Mizeracka K, Marson A, Frampton GM, Cole MF, Odom DT, Odajima J, Geng Y, Zagozdzon A, Jecrois M, Young RA, Liu XS, Cepko CL, Gygi SP, Sicinski P (2010) Transcriptional role of cyclin D1 in development revealed by a genetic-proteomic screen. Nature 463:374–378

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bouldin CM, Snelson CD, Farr GH 3rd, Kimelman D (2014) Restricted expression of cdc25a in the tailbud is essential for formation of the zebrafish posterior body. Genes Dev 28:384–395

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boutros R, Ducommun B (2008) Asymmetric localization of the CDC25B phosphatase to the mother centrosome during interphase. Cell Cycle 7:401–406

    CAS  PubMed  Google Scholar 

  • Boutros R, Lobjois V, Ducommun B (2007a) CDC25 phosphatases in cancer cells: key players? Good targets? Nat Rev Cancer 7:495–507

    CAS  PubMed  Google Scholar 

  • Boutros R, Lobjois V, Ducommun B (2007b) CDC25B involvement in the centrosome duplication cycle and in microtubule nucleation. Cancer Res 67:11557–11564

    CAS  PubMed  Google Scholar 

  • Boutros R, Lorenzo C, Mondesert O, Jauneau A, Oakes V, Dozier C, Gabrielli B, Ducommun B (2011) CDC25B associates with a centrin 2-containing complex and is involved in maintaining centrosome integrity. Biol Cell 103:55–68

    CAS  PubMed Central  PubMed  Google Scholar 

  • Briscoe J, Therond PP (2013) The mechanisms of Hedgehog signalling and its roles in development and disease. Nat Rev Mol Cell Biol 14:416–429

    PubMed  Google Scholar 

  • Calegari F, Huttner WB (2003) An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 116:4947–4955

    CAS  PubMed  Google Scholar 

  • Cayuso J, Ulloa F, Cox B, Briscoe J, Marti E (2006) The Sonic hedgehog pathway independently controls the patterning, proliferation and survival of neuroepithelial cells by regulating Gli activity. Development 133:517–528

    CAS  PubMed  Google Scholar 

  • Chen MS, Hurov J, White LS, Woodford-Thomas T, Piwnica-Worms H (2001) Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Mol Cell Biol 21:3853–3861

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chenn A, McConnell SK (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82:631–641

    CAS  PubMed  Google Scholar 

  • Clarke AR, Maandag ER, van Roon M, van der Lugt NM, van der Valk M, Hooper ML, Berns A, te Riele H (1992) Requirement for a functional Rb-1 gene in murine development. Nature 359:328–330

    CAS  PubMed  Google Scholar 

  • Cohen M, Briscoe J, Blassberg R (2013) Morphogen interpretation: the transcriptional logic of neural tube patterning. Curr Opin Genet Dev 23:423–428

    CAS  PubMed  Google Scholar 

  • Coqueret O (2002) Linking cyclins to transcriptional control. Gene 299:35–55

    CAS  PubMed  Google Scholar 

  • Coronado D, Godet M, Bourillot PY, Tapponnier Y, Bernat A, Petit M, Afanassieff M, Markossian S, Malashicheva A, Iacone R, Anastassiadis K, Savatier P (2013) A short G1 phase is an intrinsic determinant of naive embryonic stem cell pluripotency. Stem Cell Res 10:118–131

    PubMed  Google Scholar 

  • Cremisi F, Philpott A, Ohnuma S (2003) Cell cycle and cell fate interactions in neural development. Curr Opin Neurobiol 13:26–33

    CAS  PubMed  Google Scholar 

  • Cunningham JJ, Roussel MF (2001) Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ 12:387–396

    CAS  PubMed  Google Scholar 

  • Cunningham JJ, Levine EM, Zindy F, Goloubeva O, Roussel MF, Smeyne RJ (2002) The cyclin-dependent kinase inhibitors p19(Ink4d) and p27(Kip1) are coexpressed in select retinal cells and act cooperatively to control cell cycle exit. Mol Cell Neurosci 19:359–374

    CAS  PubMed  Google Scholar 

  • Das RM, Storey KG (2012) Mitotic spindle orientation can direct cell fate and bias Notch activity in chick neural tube. EMBO Rep 13:448–454

    CAS  PubMed Central  PubMed  Google Scholar 

  • Das RM, Storey KG (2014) Apical abscission alters cell polarity and dismantles the primary cilium during neurogenesis. Science 343:200–204

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davidson G, Niehrs C (2010) Emerging links between CDK cell cycle regulators and Wnt signaling. Trends Cell Biol 20:453–460

    CAS  PubMed  Google Scholar 

  • Davidson G, Shen J, Huang YL, Su Y, Karaulanov E, Bartscherer K, Hassler C, Stannek P, Boutros M, Niehrs C (2009) Cell cycle control of wnt receptor activation. Dev Cell 17:788–799

    CAS  PubMed  Google Scholar 

  • Edgar BA, O’Farrell PH (1989) Genetic control of cell division patterns in the Drosophila embryo. Cell 57:177–187

    CAS  PubMed Central  PubMed  Google Scholar 

  • El Wakil A, Francius C, Wolff A, Pleau-Varet J, Nardelli J (2006) The GATA2 transcription factor negatively regulates the proliferation of neuronal progenitors. Development 133:2155–2165

    PubMed  Google Scholar 

  • Farah MH, Olson JM, Sucic HB, Hume RI, Tapscott SJ, Turner DL (2000) Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127:693–702

    CAS  PubMed  Google Scholar 

  • Ferguson AM, White LS, Donovan PJ, Piwnica-Worms H (2005) Normal cell cycle and checkpoint responses in mice and cells lacking Cdc25B and Cdc25C protein phosphatases. Mol Cell Biol 25:2853–2860

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fish JL, Kosodo Y, Enard W, Paabo S, Huttner WB (2006) Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc Natl Acad Sci U S A 103:10438–10443

    CAS  PubMed Central  PubMed  Google Scholar 

  • Godin JD, Poizat G, Hickey MA, Maschat F, Humbert S (2010) Mutant huntingtin-impaired degradation of beta-catenin causes neurotoxicity in Huntington’s disease. Embo J 29:2433–2445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gonsalvez DG, Cane KN, Landman KA, Enomoto H, Young HM, Anderson CR (2013) Proliferation and cell cycle dynamics in the developing stellate ganglion. J Neurosci 33:5969–5979

    CAS  PubMed  Google Scholar 

  • Gotz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777–788

    PubMed  Google Scholar 

  • Gruber R, Zhou Z, Sukchev M, Joerss T, Frappart PO, Wang ZQ (2011) MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat Cell Biol 13:1325–1334

    CAS  PubMed  Google Scholar 

  • Gui H, Li S, Matise MP (2007) A cell-autonomous requirement for Cip/Kip cyclin-kinase inhibitors in regulating neuronal cell cycle exit but not differentiation in the developing spinal cord. Dev Biol 301:14–26

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hammerle B, Tejedor FJ (2007) A novel function of DELTA-NOTCH signalling mediates the transition from proliferation to neurogenesis in neural progenitor cells. PLoS ONE 2:e1169

    PubMed Central  PubMed  Google Scholar 

  • Harashima H, Dissmeyer N, Schnittger A (2013) Cell cycle control across the eukaryotic kingdom. Trends Cell Biol 23:345–356

    CAS  PubMed  Google Scholar 

  • Herrup K, Yang Y (2007) Cell cycle regulation in the postmitotic neuron: oxymoron or new biology? Nat Rev Neurosci 8:368–378

    CAS  PubMed  Google Scholar 

  • Hu DJ, Baffet AD, Nayak T, Akhmanova A, Doye V, Vallee RB (2013) Dynein recruitment to nuclear pores activates apical nuclear migration and mitotic entry in brain progenitor cells. Cell 154:1300–1313

    CAS  PubMed  Google Scholar 

  • Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA (1992) Effects of an Rb mutation in the mouse. Nature 359:295–300

    CAS  PubMed  Google Scholar 

  • Jimenez J, Alphey L, Nurse P, Glover DM (1990) Complementation of fission yeast cdc2ts and cdc25ts mutants identifies two cell cycle genes from Drosophila: a cdc2 homologue and string. Embo J 9:3565–3571

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jinno S, Suto K, Nagata A, Igarashi M, Kanaoka Y, Nojima H, Okayama H (1994) Cdc25A is a novel phosphatase functioning early in the cell cycle. EMBO J 13:1549–1556

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kakizuka A, Sebastian B, Borgmeyer U, Hermans-Borgmeyer I, Bolado J, Hunter T, Hoekstra MF, Evans RM (1992) A mouse cdc25 homolog is differentially and developmentally expressed. Genes Dev 6:578–590

    CAS  PubMed  Google Scholar 

  • Kawauchi T, Shikanai M, Kosodo Y (2013) Extra-cell cycle regulatory functions of cyclin-dependent kinases (CDK) and CDK inhibitor proteins contribute to brain development and neurological disorders. Genes Cells 18:176–194

    CAS  PubMed Central  PubMed  Google Scholar 

  • Korner K, Jerome V, Schmidt T, Muller R (2001) Cell cycle regulation of the murine cdc25B promoter: essential role for nuclear factor-Y and a proximal repressor element. J Biol Chem 276:9662–9669

    CAS  PubMed  Google Scholar 

  • Kosodo Y (2012) Interkinetic nuclear migration: beyond a hallmark of neurogenesis. Cell Mol Life Sci 69:2727–2738

    CAS  PubMed  Google Scholar 

  • Kosodo Y, Suetsugu T, Suda M, Mimori-Kiyosue Y, Toida K, Baba SA, Kimura A, Matsuzaki F (2011) Regulation of interkinetic nuclear migration by cell cycle-coupled active and passive mechanisms in the developing brain. EMBO J 30:1690–1704

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lacomme M, Liaubet L, Pituello F, Bel-Vialar S (2012) NEUROG2 drives cell cycle exit of neuronal precursors by specifically repressing a subset of cyclins acting at the G1 and S phases of the cell cycle. Mol Cell Biol 32:2596–2607

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lancaster MA, Knoblich JA (2012) Spindle orientation in mammalian cerebral cortical development. Curr Opin Neurobiol 22:737–746

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lange C, Calegari F (2010) Cdks and cyclins link G(1) length and differentiation of embryonic, neural and hematopoietic stem cells. Cell Cycle 9:1893–1900

    CAS  PubMed  Google Scholar 

  • Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5:320–331

    CAS  PubMed  Google Scholar 

  • Le Dreau G, Marti E (2013) The multiple activities of BMPs during spinal cord development. Cell Mol Life Sci 70:4293–4305

    PubMed  Google Scholar 

  • Le Dreau G, Saade M, Gutierrez-Vallejo I, Marti E (2014) The strength of SMAD1/5 activity determines the mode of stem cell division in the developing spinal cord. J Cell Biol 204:591–605

    PubMed Central  PubMed  Google Scholar 

  • Lee EY, Chang CY, Hu N, Wang YC, Lai CC, Herrup K, Lee WH, Bradley A (1992) Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288–294

    CAS  PubMed  Google Scholar 

  • Lee EY, Hu N, Yuan SS, Cox LA, Bradley A, Lee WH, Herrup K (1994) Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes Dev 8:2008–2021

    CAS  PubMed  Google Scholar 

  • Lee G, White LS, Hurov KE, Stappenbeck TS, Piwnica-Worms H (2009) Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion. Proc Natl Acad Sci U S A 106:4701–4706

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leung L, Klopper AV, Grill SW, Harris WA, Norden C (2011) Apical migration of nuclei during G2 is a prerequisite for all nuclear motion in zebrafish neuroepithelia. Development 138:5003–5013

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lincoln AJ, Wickramasinghe D, Stein P, Schultz RM, Palko ME, De Miguel MP, Tessarollo L, Donovan PJ (2002) Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet 30:446–449

    CAS  PubMed  Google Scholar 

  • Lobjois V, Benazeraf B, Bertrand N, Medevielle F, Pituello F (2004) Specific regulation of cyclins D1 and D2 by FGF and Shh signaling coordinates cell cycle progression, patterning, and differentiation during early steps of spinal cord development. Dev Biol 273:195–209

    CAS  PubMed  Google Scholar 

  • Lobjois V, Bel-Vialar S, Trousse F, Pituello F (2008) Forcing neural progenitor cells to cycle is insufficient to alter cell-fate decision and timing of neuronal differentiation in the spinal cord. Neural Dev 3:4

    PubMed Central  PubMed  Google Scholar 

  • Locker M, Agathocleous M, Amato MA, Parain K, Harris WA, Perron M (2006) Hedgehog signaling and the retina: insights into the mechanisms controlling the proliferative properties of neural precursors. Genes Dev 20:3036–3048

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lukaszewicz AI, Anderson DJ (2011) Cyclin D1 promotes neurogenesis in the developing spinal cord in a cell cycle-independent manner. Proc Natl Acad Sci U S A 108:11632–11637

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lukaszewicz A, Savatier P, Cortay V, Kennedy H, Dehay C (2002) Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J Neurosci 22:6610–6622

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martinez-Morales PL, Quiroga AC, Barbas JA, Morales AV (2010) SOX5 controls cell cycle progression in neural progenitors by interfering with the WNT-beta-catenin pathway. EMBO Rep 11:466–472

  • Megason SG, McMahon AP (2002) A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129:2087–2098

    CAS  PubMed  Google Scholar 

  • Mizuguchi R, Sugimori M, Takebayashi H, Kosako H, Nagao M, Yoshida S, Nabeshima Y, Shimamura K, Nakafuku M (2001) Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31:757–771

    CAS  PubMed  Google Scholar 

  • Morin X, Jaouen F, Durbec P (2007) Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat Neurosci 10:1440–1448

    CAS  PubMed  Google Scholar 

  • Nakajo N, Deno YK, Ueno H, Kenmochi C, Shimuta K, Sagata N (2011) Temporal and spatial expression patterns of Cdc25 phosphatase isoforms during early Xenopus development. Int J Dev Biol 55:627–632

    CAS  PubMed  Google Scholar 

  • Nogare DE, Arguello A, Sazer S, Lane ME (2007) Zebrafish cdc25a is expressed during early development and limiting for post-blastoderm cell cycle progression. Dev Dyn 236:3427–3435

    PubMed  Google Scholar 

  • Novitch BG, Chen AI, Jessell TM (2001) Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31:773–789

    CAS  PubMed  Google Scholar 

  • Olivera-Martinez I, Schurch N, Li RA, Song J, Halley PA, Das RM, Burt DW, Barton GJ, Storey KG (2014) Major transcriptome re-organisation and abrupt changes in signalling, cell cycle and chromatin regulation at neural differentiation in vivo. Development 141:3266–3276

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pauklin S, Vallier L (2013) The cell-cycle state of stem cells determines cell fate propensity. Cell 155:135–147

    CAS  PubMed Central  PubMed  Google Scholar 

  • Peco E, Escude T, Agius E, Sabado V, Medevielle F, Ducommun B, Pituello F (2012) The CDC25B phosphatase shortens the G2 phase of neural progenitors and promotes efficient neuron production. Development 139:1095–1104

    CAS  PubMed  Google Scholar 

  • Peyre E, Morin X (2012) An oblique view on the role of spindle orientation in vertebrate neurogenesis. Dev Growth Differ 54:287–305

    CAS  PubMed  Google Scholar 

  • Pilaz LJ, Patti D, Marcy G, Ollier E, Pfister S, Douglas RJ, Betizeau M, Gautier E, Cortay V, Doerflinger N, Kennedy H, Dehay C (2009) Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci U S A 106:21924–21929

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ratineau C, Petry MW, Mutoh H, Leiter AB (2002) Cyclin D1 represses the basic helix-loop-helix transcription factor, BETA2/NeuroD. J Biol Chem 277:8847–8853

    CAS  PubMed  Google Scholar 

  • Rodriguez-Aznar E, Barrallo-Gimeno A, Nieto MA (2013) Scratch2 prevents cell cycle re-entry by repressing miR-25 in postmitotic primary neurons. J Neurosci 33:5095–5105

    CAS  PubMed  Google Scholar 

  • Rohrer H, Thoenen H (1987) Relationship between differentiation and terminal mitosis: chick sensory and ciliary neurons differentiate after terminal mitosis of precursor cells, whereas sympathetic neurons continue to divide after differentiation. J Neurosci 7:3739–3748

    CAS  PubMed  Google Scholar 

  • Saade M, Gutierrez-Vallejo I, Le Dreau G, Rabadan MA, Miguez DG, Buceta J, Marti E (2013) Sonic hedgehog signaling switches the mode of division in the developing nervous system. Cell Rep 4:492–503

    CAS  PubMed  Google Scholar 

  • Sakai D, Dixon J, Dixon MJ, Trainor PA (2012) Mammalian neurogenesis requires Treacle-Plk1 for precise control of spindle orientation, mitotic progression, and maintenance of neural progenitor cells. PLoS Genet 8:e1002566

    PubMed Central  PubMed  Google Scholar 

  • Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H, Osawa H, Kashiwagi S, Fukami K, Miyata T, Miyoshi H, Imamura T, Ogawa M, Masai H, Miyawaki A (2008) Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132:487–498

    CAS  PubMed  Google Scholar 

  • Schuller U, Zhao Q, Godinho SA, Heine VM, Medema RH, Pellman D, Rowitch DH (2007) Forkhead transcription factor FoxM1 regulates mitotic entry and prevents spindle defects in cerebellar granule neuron precursors. Mol Cell Biol 27:8259–8270

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sela Y, Molotski N, Golan S, Itskovitz-Eldor J, Soen Y (2012) Human embryonic stem cells exhibit increased propensity to differentiate during the G1 phase prior to phosphorylation of retinoblastoma protein. Stem Cells 30:1097–1108

    CAS  PubMed  Google Scholar 

  • Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13:1501–1512

    CAS  PubMed  Google Scholar 

  • Skapek SX, Rhee J, Spicer DB, Lassar AB (1995) Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science 267:1022–1024

    CAS  PubMed  Google Scholar 

  • Skapek SX, Rhee J, Kim PS, Novitch BG, Lassar AB (1996) Cyclin-mediated inhibition of muscle gene expression via a mechanism that is independent of pRB hyperphosphorylation. Mol Cell Biol 16:7043–7053

    CAS  PubMed Central  PubMed  Google Scholar 

  • Taverna E, Huttner WB (2010) Neural progenitor nuclei IN motion. Neuron 67:906–914

    CAS  PubMed  Google Scholar 

  • Timofeev O, Cizmecioglu O, Settele F, Kempf T, Hoffmann I (2010) Cdc25 phosphatases are required for timely assembly of CDK1-cyclin B at the G2/M transition. J Biol Chem 285:16978–16990

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ueno M, Katayama K, Yamauchi H, Nakayama H, Doi K (2006) Cell cycle progression is required for nuclear migration of neural progenitor cells. Brain Res 1088:57–67

    CAS  PubMed  Google Scholar 

  • Ueno H, Nakajo N, Watanabe M, Isoda M, Sagata N (2008) FoxM1-driven cell division is required for neuronal differentiation in early Xenopus embryos. Development 135:2023–2030

    CAS  PubMed  Google Scholar 

  • Ulloa F, Itasaki N, Briscoe J (2007) Inhibitory Gli3 activity negatively regulates Wnt/beta-catenin signaling. Curr Biol 17:545–550

    CAS  PubMed  Google Scholar 

  • van der Laan S, Tsanov N, Crozet C, Maiorano D (2013) High Dub3 expression in mouse ESCs couples the G1/S checkpoint to pluripotency. Mol Cell 52:366–379

    PubMed  Google Scholar 

  • Vijayakumar S, Liu G, Rus IA, Yao S, Chen Y, Akiri G, Grumolato L, Aaronson SA (2011) High-frequency canonical Wnt activation in multiple sarcoma subtypes drives proliferation through a TCF/beta-catenin target gene, CDC25A. Cancer Cell 19:601–612

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461:947–955

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wilcock AC, Swedlow JR, Storey KG (2007) Mitotic spindle orientation distinguishes stem cell and terminal modes of neuron production in the early spinal cord. Development 134:1943–1954

    CAS  PubMed  Google Scholar 

  • Willardsen MI, Link BA (2011) Cell biological regulation of division fate in vertebrate neuroepithelial cells. Dev Dyn 240:1865–1879

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wilson V, Olivera-Martinez I, Storey KG (2009) Stem cells, signals and vertebrate body axis extension. Development 136:1591–1604

    CAS  PubMed  Google Scholar 

  • Wu X, Gu X, Han X, Du A, Jiang Y, Zhang X, Wang Y, Cao G, Zhao C (2014) A novel function for Foxm1 in interkinetic nuclear migration in the developing telencephalon and anxiety-related behavior. J Neurosci 34:1510–1522

    CAS  PubMed  Google Scholar 

  • Zindy F, Cunningham JJ, Sherr CJ, Jogal S, Smeyne RJ, Roussel MF (1999) Postnatal neuronal proliferation in mice lacking Ink4d and Kip1 inhibitors of cyclin-dependent kinases. Proc Natl Acad Sci U S A 96:13462–13467

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Pr. B. Ducommun and Dr. X.Morin for critical reading of the manuscript and C. Monod-Wissler for improving the English writing. Work in F.P.’s laboratory is funded by the Centre National de la Recherche Scientifique, L’Université P. Sabatier, le Ministère de l’Education Nationale et de la recherche, the Fondation pour la Recherche sur le Cancer (ARC) and the Fédération pour la Recherche sur le Cerveau (FRC).

Author information

Authors and Affiliations

  1. Université Toulouse 3; Centre de Biologie du Développement (CBD), 118 route de Narbonne, 31062, Toulouse, France

    Eric Agius, Sophie Bel-Vialar, Frédéric Bonnet & Fabienne Pituello

  2. CNRS-UMR5547, 31062, Toulouse, France

    Eric Agius, Sophie Bel-Vialar, Frédéric Bonnet & Fabienne Pituello

Authors
  1. Eric Agius
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sophie Bel-Vialar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frédéric Bonnet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabienne Pituello
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabienne Pituello.

Additional information

Eric Agius and Sophie Bel-Vialar equally contributed to this review.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Agius, E., Bel-Vialar, S., Bonnet, F. et al. Cell cycle and cell fate in the developing nervous system: the role of CDC25B phosphatase. Cell Tissue Res 359, 201–213 (2015). https://doi.org/10.1007/s00441-014-1998-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-014-1998-2

Keywords

Search

Navigation