Skip to main content

Advertisement

SpringerLink
Log in

Interaction of Notch and gp130 Signaling in the Maintenance of Neural Stem and Progenitor Cells

  • Review Paper
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Notch and gp130 signaling are involved in the regulation of multiple cellular processes across various tissues during animal ontogenesis. In the developing nervous system, both signaling pathways intervene at many stages to determine cell fate—from the first neural lineage commitment and generation of neuronal precursors, to the terminal specification of cells as neurons and glia. In most cases, the effects of Notch and gp130 signaling in these processes are similar. The aim of the current review was to summarize the knowledge regarding the roles of Notch and gp130 signaling in the maintenance of neural stem and progenitor cells during animal ontogenesis, from early embryo to adult. Recent data show a direct crosstalk between these signaling pathways that seems to be specific for a particular type of neural progenitors.

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

Similar content being viewed by others

References

  • Abranches E, Silva M, Pradier L, Schulz H, Hummel O, Henrique D, Bekman E (2009) Neural differentiation of embryonic stem cells in vitro: a road map to neurogenesis in the embryo. PLoS One 4(7):e6286. doi:10.1371/journal.pone.0006286

    PubMed Central  PubMed  Google Scholar 

  • Alexander WS, Hilton DJ (2004) The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response. Annu Rev Immunol 22:503–529

    CAS  PubMed  Google Scholar 

  • Alexson TO, Hitoshi S, Coles BL, Bernstein A, van der Kooy D (2006) Notch signaling is required to maintain all neural stem cell populations—irrespective of spatial or temporal niche. Dev Neurosci 28(1–2):34–48

    CAS  PubMed  Google Scholar 

  • Andersen P, Uosaki H, Shenje LT, Kwon C (2012) Non-canonical notch signaling: emerging role and mechanism. Trends Cell Biol 22(5):257–265

    CAS  PubMed Central  PubMed  Google Scholar 

  • Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442(7104):823–826

    CAS  PubMed  Google Scholar 

  • Bartlett PF, Brooker GJ, Faux CH, Dutton R, Murphy M, Turnley A, Kilpatrick TJ (1998) Regulation of neural stem cell differentiation in the forebrain. Immunol Cell Biol 76(5):414–418

    CAS  PubMed  Google Scholar 

  • Bauer S (2009) Cytokine control of adult neural stem cells. Ann N Y Acad Sci 1153:48–56

    CAS  PubMed  Google Scholar 

  • Bauer S, Patterson PH (2006) Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. J Neurosci 26(46):12089–12099

    CAS  PubMed  Google Scholar 

  • Bettenhausen B, Hrabe de Angelis M, Simon D, Guenet JL, Gossler A (1995) Transient and restricted expression during mouse embryogenesis of DII1, a murine gene closely related to Drosophila Delta. Development 121(8):2407–2418

    CAS  PubMed  Google Scholar 

  • Betz UA, Bloch W, van den Broek M, Yoshida K, Taga T, Kishimoto T, Addicks K, Rajewsky K, Muller W (1998) Postnatally induced inactivation of gp130 in mice results in neurological, cardiac, hematopoietic, immunological, hepatic, and pulmonary defects. J Exp Med 188(10):1955–1965

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bez A, Corsini E, Curti D, Biggiogera M, Colombo A, Nicosia RF, Pagano SF, Parati EA (2003) Neurosphere and neurosphere-forming cells: morphological and ultrastructural characterization. Brain Res 993(1–2):18–29

    CAS  PubMed  Google Scholar 

  • Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278(5337):477–483

    CAS  PubMed  Google Scholar 

  • Borggrefe T, Oswald F (2009) The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 66(10):1631–1646

    CAS  PubMed  Google Scholar 

  • Borghese L, Dolezalova D, Opitz T, Haupt S, Leinhaas A, Steinfarz B, Koch P, Edenhofer F, Hampl A, Brustle O (2010) Inhibition of notch signaling in human embryonic stem cell-derived neural stem cells delays G1/S phase transition and accelerates neuronal differentiation in vitro and in vivo. Stem Cells 28(5):955–964

    CAS  PubMed  Google Scholar 

  • Boyle K, Robb L (2008) The role of SOCS3 in modulating leukaemia inhibitory factor signalling during murine placental development. J Reprod Immunol 77(1):1–6

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bryja V, Cajanek L, Pachernik J, Hall AC, Horvath V, Dvorak P, Hampl A (2005) Abnormal development of mouse embryoid bodies lacking p27Kip1 cell cycle regulator. Stem Cells 23(7):965–974

    CAS  PubMed  Google Scholar 

  • Bryja V, Pachernik J, Vondracek J, Soucek K, Cajanek L, Horvath V, Holubcova Z, Dvorak P, Hampl A (2008) Lineage specific composition of cyclin D-CDK4/CDK6-p27 complexes reveals distinct functions of CDK4, CDK6 and individual D-type cyclins in differentiating cells of embryonic origin. Cell Prolif 41(6):875–893

    CAS  PubMed Central  PubMed  Google Scholar 

  • Burdon T, Smith A, Savatier P (2002) Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 12(9):432–438

    CAS  PubMed  Google Scholar 

  • Cao F, Hata R, Zhu P, Ma YJ, Tanaka J, Hanakawa Y, Hashimoto K, Niinobe M, Yoshikawa K, Sakanaka M (2006) Overexpression of SOCS3 inhibits astrogliogenesis and promotes maintenance of neural stem cells. J Neurochem 98(2):459–470

    CAS  PubMed  Google Scholar 

  • Cao F, Hata R, Zhu P, Nakashiro K, Sakanaka M (2010) Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells. Biochem Biophys Res Commun 394(3):843–847

    CAS  PubMed  Google Scholar 

  • Carter DA, Dick AD, Mayer EJ (2009) CD133+ adult human retinal cells remain undifferentiated in leukaemia inhibitory factor (LIF). BMC Ophthalmol 9:1

    PubMed Central  PubMed  Google Scholar 

  • Chambers CB, Peng Y, Nguyen H, Gaiano N, Fishell G, Nye JS (2001) Spatiotemporal selectivity of response to Notch1 signals in mammalian forebrain precursors. Development 128(5):689–702

    CAS  PubMed  Google Scholar 

  • Chojnacki A, Shimazaki T, Gregg C, Weinmaster G, Weiss S (2003) Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J Neurosci 23(5):1730–1741

    CAS  PubMed  Google Scholar 

  • Conlon RA, Reaume AG, Rossant J (1995) Notch1 is required for the coordinate segmentation of somites. Development 121(5):1533–1545

    CAS  PubMed  Google Scholar 

  • Das D, Lanner F, Main H, Andersson ER, Bergmann O, Sahlgren C, Heldring N, Hermanson O, Hansson EM, Lendahl U (2010) Notch induces cyclin-D1-dependent proliferation during a specific temporal window of neural differentiation in ES cells. Dev Biol 348(2):153–166

    CAS  PubMed  Google Scholar 

  • Del Amo FF, Smith DE, Swiatek PJ, Gendron-Maguire M, Greenspan RJ, McMahon AP, Gridley T (1992) Expression pattern of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 115(3):737–744

    PubMed  Google Scholar 

  • Deverman BE, Patterson PH (2009) Cytokines and CNS development. Neuron 64(1):61–78

    CAS  PubMed  Google Scholar 

  • Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6):703–716

    CAS  PubMed  Google Scholar 

  • Donoviel DB, Hadjantonakis AK, Ikeda M, Zheng H, Hyslop PS, Bernstein A (1999) Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes Dev 13(21):2801–2810

    CAS  PubMed  Google Scholar 

  • D’Souza B, Miyamoto A, Weinmaster G (2008) The many facets of notch ligands. Oncogene 27(38):5148–5167

    PubMed Central  PubMed  Google Scholar 

  • Dunwoodie SL, Henrique D, Harrison SM, Beddington RS (1997) Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo. Development 124(16):3065–3076

    CAS  PubMed  Google Scholar 

  • Elkabetz Y, Panagiotakos G, Al Shamy G, Socci ND, Tabar V, Studer L (2008) Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 22(2):152–165

    CAS  PubMed  Google Scholar 

  • Ellisen LW, Bird J, West DC, Soreng AL, Reynolds TC, Smith SD, Sklar J (1991) TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66(4):649–661

    CAS  PubMed  Google Scholar 

  • Ernst M, Jenkins BJ (2004) Acquiring signalling specificity from the cytokine receptor gp130. Trends Genet 20(1):23–32

    CAS  PubMed  Google Scholar 

  • Escary JL, Perreau J, Dumenil D, Ezine S, Brulet P (1993) Leukaemia inhibitory factor is necessary for maintenance of haematopoietic stem cells and thymocyte stimulation. Nature 363(6427):361–364

    CAS  PubMed  Google Scholar 

  • Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819):154–156

    CAS  PubMed  Google Scholar 

  • Feng GS, Shen R, Heng HH, Tsui LC, Kazlauskas A, Pawson T (1994) Receptor-binding, tyrosine phosphorylation and chromosome localization of the mouse SH2-containing phosphotyrosine phosphatase Syp. Oncogene 9(6):1545–1550

    CAS  PubMed  Google Scholar 

  • Fortini ME (2009) Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 16(5):633–647

    CAS  PubMed  Google Scholar 

  • Foshay KM, Gallicano GI (2008) Regulation of Sox2 by STAT3 initiates commitment to the neural precursor cell fate. Stem Cells Dev 17(2):269–278

    CAS  PubMed  Google Scholar 

  • Gaiano N, Nye JS, Fishell G (2000) Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26(2):395–404

    CAS  PubMed  Google Scholar 

  • Ge W, Martinowich K, Wu X, He F, Miyamoto A, Fan G, Weinmaster G, Sun YE (2002) Notch signaling promotes astrogliogenesis via direct CSL-mediated glial gene activation. J Neurosci Res 69(6):848–860

    CAS  PubMed  Google Scholar 

  • Giachino C, Basak O, Lugert S, Knuckles P, Obernier K, Fiorelli R, Frank S, Raineteau O, Alvarez-Buylla A, Taylor V (2013) Molecular diversity subdivides the adult forebrain neural stem cell population. Stem Cells. doi:10.1002/stem.1520

    Google Scholar 

  • Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8(6):481–488

    CAS  PubMed  Google Scholar 

  • Gouti M, Gavalas A (2008) Hoxb1 controls cell fate specification and proliferative capacity of neural stem and progenitor cells. Stem Cells 26(8):1985–1997

    CAS  PubMed  Google Scholar 

  • Grandbarbe L, Bouissac J, Rand M, Hrabe de Angelis M, Artavanis-Tsakonas S, Mohier E (2003) Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process. Development 130(7):1391–1402

    CAS  PubMed  Google Scholar 

  • Gregg C, Weiss S (2005) CNTF/LIF/gp130 receptor complex signaling maintains a VZ precursor differentiation gradient in the developing ventral forebrain. Development 132(3):565–578

    CAS  PubMed  Google Scholar 

  • Gu F, Hata R, Ma YJ, Tanaka J, Mitsuda N, Kumon Y, Hanakawa Y, Hashimoto K, Nakajima K, Sakanaka M (2005) Suppression of Stat3 promotes neurogenesis in cultured neural stem cells. J Neurosci Res 81(2):163–171

    CAS  PubMed  Google Scholar 

  • Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, Ruas JL, Poellinger L, Lendahl U, Bondesson M (2005) Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 9(5):617–628

    CAS  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(11):e1169. doi:10.1371/journal.pone.0001169

    PubMed Central  PubMed  Google Scholar 

  • Handler M, Yang X, Shen J (2000) Presenilin-1 regulates neuronal differentiation during neurogenesis. Development 127(12):2593–2606

    CAS  PubMed  Google Scholar 

  • Hatakeyama J, Bessho Y, Katoh K, Ookawara S, Fujioka M, Guillemot F, Kageyama R (2004) Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131(22):5539–5550

    CAS  PubMed  Google Scholar 

  • Haydar TF, Ang E Jr, Rakic P (2003) Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc Natl Acad Sci USA 100(5):2890–2895

    CAS  PubMed  Google Scholar 

  • Hayward P, Kalmar T, Arias AM (2008) Wnt/Notch signalling and information processing during development. Development 135(3):411–424

    CAS  PubMed  Google Scholar 

  • Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374(Pt 1):1–20

    CAS  PubMed  Google Scholar 

  • Hicks C, Ladi E, Lindsell C, Hsieh JJ, Hayward SD, Collazo A, Weinmaster G (2002) A secreted Delta1-Fc fusion protein functions both as an activator and inhibitor of Notch1 signaling. J Neurosci Res 68(6):655–667

    CAS  PubMed  Google Scholar 

  • Hirano T, Nakajima K, Hibi M (1997) Signaling mechanisms through gp130: a model of the cytokine system. Cytokine Growth Factor Rev 8(4):241–252

    CAS  PubMed  Google Scholar 

  • Hiratochi M, Nagase H, Kuramochi Y, Koh CS, Ohkawara T, Nakayama K (2007) The Delta intracellular domain mediates TGF-beta/activin signaling through binding to Smads and has an important bi-directional function in the Notch-Delta signaling pathway. Nucleic Acids Res 35(3):912–922

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, Nye JS, Conlon RA, Mak TW, Bernstein A, van der Kooy D (2002) Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16(7):846–858

    CAS  PubMed  Google Scholar 

  • Hitoshi S, Seaberg RM, Koscik C, Alexson T, Kusunoki S, Kanazawa I, Tsuji S, van der Kooy D (2004) Primitive neural stem cells from the mammalian epiblast differentiate to definitive neural stem cells under the control of Notch signaling. Genes Dev 18(15):1806–1811

    CAS  PubMed  Google Scholar 

  • Ihrie RA, Alvarez-Buylla A (2008) Cells in the astroglial lineage are neural stem cells. Cell Tissue Res 331(1):179–191

    PubMed  Google Scholar 

  • Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R (2010) Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 30(9):3489–3498

    CAS  PubMed  Google Scholar 

  • Imitola J (2007) Prospects for neural stem cell-based therapies for neurological diseases. Neurotherapeutics 4(4):701–714. doi:S1933-7213(07)00159-6

    CAS  PubMed  Google Scholar 

  • Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R (1994) Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13(8):1799–1805

    CAS  PubMed  Google Scholar 

  • Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F (1995) Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev 9(24):3136–3148

    CAS  PubMed  Google Scholar 

  • Johe KK, Hazel TG, Muller T, Dugich-Djordjevic MM, McKay RD (1996) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev 10(24):3129–3140

    CAS  PubMed  Google Scholar 

  • Jung JE, Kim HS, Lee CS, Shin YJ, Kim YN, Kang GH, Kim TY, Juhnn YS, Kim SJ, Park JW, Ye SK, Chung MH (2008) STAT3 inhibits the degradation of HIF-1alpha by pVHL-mediated ubiquitination. Exp Mol Med 40(5):479–485

    CAS  PubMed  Google Scholar 

  • Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R (2005) Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306(2):343–348

    CAS  PubMed  Google Scholar 

  • Kageyama R, Ohtsuka T, Kobayashi T (2008) Roles of Hes genes in neural development. Dev Growth Differ 50(Suppl 1):S97–103

    CAS  PubMed  Google Scholar 

  • Kageyama R, Ohtsuka T, Shimojo H, Imayoshi I (2009) Dynamic regulation of Notch signaling in neural progenitor cells. Curr Opin Cell Biol 21(6):733–740

    CAS  PubMed  Google Scholar 

  • Kamakura S, Oishi K, Yoshimatsu T, Nakafuku M, Masuyama N, Gotoh Y (2004) Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol 6(6):547–554

    CAS  PubMed  Google Scholar 

  • Katoh M (2009) Transcriptional mechanisms of WNT5A based on NF-kappaB, Hedgehog, TGFbeta, and Notch signaling cascades. Int J Mol Med 23(6):763–769

    CAS  PubMed  Google Scholar 

  • Keller G (2005) Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev 19:1129–1155

    CAS  PubMed  Google Scholar 

  • Kobayashi T, Kageyama R (2010) Hes1 regulates embryonic stem cell differentiation by suppressing Notch signaling. Genes Cells 15(7):689–698

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kobayashi T, Mizuno H, Imayoshi I, Furusawa C, Shirahige K, Kageyama R (2009) The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev 23(16):1870–1875

    CAS  PubMed  Google Scholar 

  • Koblar SA, Turnley AM, Classon BJ, Reid KL, Ware CB, Cheema SS, Murphy M, Bartlett PF (1998) Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor. Proc Natl Acad Sci USA 95(6):3178–3181

    CAS  PubMed  Google Scholar 

  • Komatsu H, Chao MY, Larkins-Ford J, Corkins ME, Somers GA, Tucey T, Dionne HM, White JQ, Wani K, Boxem M, Hart AC (2008) OSM-11 facilitates LIN-12 Notch signaling during Caenorhabditis elegans vulval development. PLoS Biol 6(8):e196. doi:10.1371/journal.pbio.0060196

    PubMed Central  PubMed  Google Scholar 

  • Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kurooka H, Kuroda K, Honjo T (1998) Roles of the ankyrin repeats and C-terminal region of the mouse notch1 intracellular region. Nucleic Acids Res 26(23):5448–5455

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lardelli M, Dahlstrand J, Lendahl U (1994) The novel Notch homologue mouse Notch 3 lacks specific epidermal growth factor-repeats and is expressed in proliferating neuroepithelium. Mech Dev 46(2):123–136

    CAS  PubMed  Google Scholar 

  • Lardelli M, Williams R, Mitsiadis T, Lendahl U (1996) Expression of the Notch 3 intracellular domain in mouse central nervous system progenitor cells is lethal and leads to disturbed neural tube development. Mech Dev 59(2):177–190

    CAS  PubMed  Google Scholar 

  • Lee JH, Suk J, Park J, Kim SB, Kwak SS, Kim JW, Lee CH, Byun B, Ahn JK, Joe CO (2009) Notch signal activates hypoxia pathway through HES1-dependent SRC/signal transducers and activators of transcription 3 pathway. Mol Cancer Res 7(10):1663–1671

    CAS  PubMed  Google Scholar 

  • Levine AJ, Brivanlou AH (2007) Proposal of a model of mammalian neural induction. Dev Biol 308(2):247–256

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li W, Nishimura R, Kashishian A, Batzer AG, Kim WJ, Cooper JA, Schlessinger J (1994) A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol Cell Biol 14(1):509–517

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lieber T, Kidd S, Young MW (2002) Kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev 16(2):209–221

    CAS  PubMed  Google Scholar 

  • Lindsell CE, Shawber CJ, Boulter J, Weinmaster G (1995) Jagged: a mammalian ligand that activates Notch1. Cell 80(6):909–917

    CAS  PubMed  Google Scholar 

  • Lowell S, Benchoua A, Heavey B, Smith AG (2006) Notch promotes neural lineage entry by pluripotent embryonic stem cells. PLoS Biol 4(5):e121

    PubMed Central  PubMed  Google Scholar 

  • Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146(1):18–36

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lutticken C, Wegenka UM, Yuan J, Buschmann J, Schindler C, Ziemiecki A, Harpur AG, Wilks AF, Yasukawa K, Taga T et al (1994) Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science 263(5143):89–92

    CAS  PubMed  Google Scholar 

  • Maillard I, Weng AP, Carpenter AC, Rodriguez CG, Sai H, Xu L, Allman D, Aster JC, Pear WS (2004) Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood 104(6):1696–1702

    CAS  PubMed  Google Scholar 

  • Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Gotz M (2003) Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37(5):751–764

    CAS  PubMed  Google Scholar 

  • Malatesta P, Appolloni I, Calzolari F (2008) Radial glia and neural stem cells. Cell Tissue Res 331(1):165–178

    PubMed  Google Scholar 

  • Martens DJ, Tropepe V, van Der Kooy D (2000) Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J Neurosci 20(3):1085–1095

    CAS  PubMed  Google Scholar 

  • Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 78(12):7634–7638

    CAS  PubMed  Google Scholar 

  • Mizutani K, Yoon K, Dang L, Tokunaga A, Gaiano N (2007) Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449(7160):351–355

    CAS  PubMed  Google Scholar 

  • Molne M, Studer L, Tabar V, Ting YT, Eiden MV, McKay RD (2000) Early cortical precursors do not undergo LIF-mediated astrocytic differentiation. J Neurosci Res 59(3):301–311

    CAS  PubMed  Google Scholar 

  • Muller S, Chakrapani BP, Schwegler H, Hofmann HD, Kirsch M (2009) Neurogenesis in the dentate gyrus depends on ciliary neurotrophic factor and signal transducer and activator of transcription 3 signaling. Stem Cells 27(2):431–441

    PubMed  Google Scholar 

  • Nagao M, Sugimori M, Nakafuku M (2007) Cross talk between notch and growth factor/cytokine signaling pathways in neural stem cells. Mol Cell Biol 27(11):3982–3994

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakamura Y, Sakakibara S, Miyata T, Ogawa M, Shimazaki T, Weiss S, Kageyama R, Okano H (2000) The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci 20(1):283–293

    CAS  PubMed  Google Scholar 

  • Nakashima K, Wiese S, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Yoshida K, Kishimoto T, Sendtner M, Taga T (1999) Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J Neurosci 19(13):5429–5434

    CAS  PubMed  Google Scholar 

  • Nemir M, Croquelois A, Pedrazzini T, Radtke F (2006) Induction of cardiogenesis in embryonic stem cells via downregulation of Notch1 signaling. Circ Res 98(12):1471–1478

    CAS  PubMed  Google Scholar 

  • Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409(6821):714–720

    CAS  PubMed  Google Scholar 

  • Nye JS, Kopan R, Axel R (1994) An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 120(9):2421–2430

    CAS  PubMed  Google Scholar 

  • Oda T, Elkahloun AG, Meltzer PS, Chandrasekharappa SC (1997) Identification and cloning of the human homolog (JAG1) of the rat Jagged1 gene from the Alagille syndrome critical region at 20p12. Genomics 43(3):376–379

    CAS  PubMed  Google Scholar 

  • Ohno M, Kohyama J, Namihira M, Sanosaka T, Takahashi JA, Hashimoto N, Nakashima K (2006) Neuropoietin induces neuroepithelial cells to differentiate into astrocytes via activation of STAT3. Cytokine 36(1–2):17–22

    CAS  PubMed  Google Scholar 

  • Ohtani T, Ishihara K, Atsumi T, Nishida K, Kaneko Y, Miyata T, Itoh S, Narimatsu M, Maeda H, Fukada T, Itoh M, Okano H, Hibi M, Hirano T (2000) Dissection of signaling cascades through gp130 in vivo: reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12(1):95–105

    CAS  PubMed  Google Scholar 

  • Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R (1999) Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 18(8):2196–2207

    CAS  PubMed  Google Scholar 

  • Ohtsuka T, Sakamoto M, Guillemot F, Kageyama R (2001) Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. J Biol Chem 276(32):30467–30474

    CAS  PubMed  Google Scholar 

  • Oishi K, Kamakura S, Isazawa Y, Yoshimatsu T, Kuida K, Nakafuku M, Masuyama N, Gotoh Y (2004) Notch promotes survival of neural precursor cells via mechanisms distinct from those regulating neurogenesis. Dev Biol 276(1):172–184

    CAS  PubMed  Google Scholar 

  • Oka C, Nakano T, Wakeham A, de la Pompa JL, Mori C, Sakai T, Okazaki S, Kawaichi M, Shiota K, Mak TW, Honjo T (1995) Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development 121(10):3291–3301

    CAS  PubMed  Google Scholar 

  • Ong J, Plane JM, Parent JM, Silverstein FS (2005) Hypoxic–ischemic injury stimulates subventricular zone proliferation and neurogenesis in the neonatal rat. Pediatr Res 58(3):600–606

    PubMed  Google Scholar 

  • Pacioni S, Rueger MA, Nistico G, Bornstein SR, Park DM, McKay RD, Androutsellis-Theotokis A (2012) Fast, potent pharmacological expansion of endogenous hes3+/sox2+ cells in the adult mouse and rat hippocampus. PLoS One 7(12):e51630. doi:10.1371/journal.pone.0051630

    CAS  PubMed Central  PubMed  Google Scholar 

  • Palmer TD, Takahashi J, Gage FH (1997) The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8(6):389–404

    CAS  PubMed  Google Scholar 

  • Pitman M, Emery B, Binder M, Wang S, Butzkueven H, Kilpatrick TJ (2004) LIF receptor signaling modulates neural stem cell renewal. Mol Cell Neurosci 27(3):255–266

    CAS  PubMed  Google Scholar 

  • Port MD, Gibson RM, Nathanson NM (2007) Differential stimulation-induced receptor localization in lipid rafts for interleukin-6 family cytokines signaling through the gp130/leukemia inhibitory factor receptor complex. J Neurochem 101(3):782–793

    CAS  PubMed  Google Scholar 

  • Raedt R, Boon P (2005) Cell therapy for neurological disorders: a comprehensive review. Acta Neurol Belg 105(3):158–170

    PubMed  Google Scholar 

  • Rajan P, McKay RD (1998) Multiple routes to astrocytic differentiation in the CNS. J Neurosci 18(10):3620–3629

    CAS  PubMed  Google Scholar 

  • Ramasamy SK, Lenka N (2010) Notch exhibits ligand bias and maneuvers stage-specific steering of neural differentiation in embryonic stem cells. Mol Cell Biol 30(8):1946–1957

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rebay I, Fleming RJ, Fehon RG, Cherbas L, Cherbas P, Artavanis-Tsakonas S (1991) Specific EGF repeats of Notch mediate interactions with Delta and Serrate: implications for Notch as a multifunctional receptor. Cell 67(4):687–699

    CAS  PubMed  Google Scholar 

  • Represa A, Shimazaki T, Simmonds M, Weiss S (2001) EGF-responsive neural stem cells are a transient population in the developing mouse spinal cord. Eur J Neurosci 14(3):452–462

    CAS  PubMed  Google Scholar 

  • Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255(5052):1707–1710

    CAS  PubMed  Google Scholar 

  • Rodriguez-Rivera NS, Molina-Hernandez A, Sanchez-Cruz E, Escalante-Alcalde D, Velasco I (2009) Activated Notch1 is a stronger astrocytic stimulus than leukemia inhibitory factor for rat neural stem cells. Int J Dev Biol 53(7):947–953

    CAS  PubMed  Google Scholar 

  • Ronchini C, Capobianco AJ (2001) Induction of cyclin D1 transcription and CDK2 activity by Notch(ic): implication for cell cycle disruption in transformation by Notch(ic). Mol Cell Biol 21(17):5925–5934

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sanalkumar R, Dhanesh SB, James J (2010) Non-canonical activation of Notch signaling/target genes in vertebrates. Cell Mol Life Sci 67(17):2957–2968

    CAS  PubMed  Google Scholar 

  • Schindler C, Darnell JE Jr (1995) Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu Rev Biochem 64:621–651

    CAS  PubMed  Google Scholar 

  • Schroeder T, Fraser ST, Ogawa M, Nishikawa S, Oka C, Bornkamm GW, Honjo T, Just U (2003) Recombination signal sequence-binding protein Jkappa alters mesodermal cell fate decisions by suppressing cardiomyogenesis. Proc Natl Acad Sci USA 100(7):4018–4023

    CAS  PubMed  Google Scholar 

  • Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478(4):359–378

    PubMed  Google Scholar 

  • Shawber C, Boulter J, Lindsell CE, Weinmaster G (1996) Jagged2: a serrate-like gene expressed during rat embryogenesis. Dev Biol 180(1):370–376

    CAS  PubMed  Google Scholar 

  • Shen Y, Inoue N, Heese K (2010) Neurotrophin-4 (ntf4) mediates neurogenesis in mouse embryonic neural stem cells through the inhibition of the signal transducer and activator of transcription-3 (stat3) and the modulation of the activity of protein kinase B. Cell Mol Neurobiol 30(6):909–916

    CAS  PubMed  Google Scholar 

  • Shimazaki T, Shingo T, Weiss S (2001) The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci 21(19):7642–7653

    CAS  PubMed  Google Scholar 

  • Shimizu K, Chiba S, Saito T, Kumano K, Hamada Y, Hirai H (2002) Functional diversity among Notch1, Notch2, and Notch3 receptors. Biochem Biophys Res Commun 291(4):775–779

    CAS  PubMed  Google Scholar 

  • Shimojo H, Ohtsuka T, Kageyama R (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58(1):52–64

    CAS  PubMed  Google Scholar 

  • Shimojo H, Ohtsuka T, Kageyama R (2011) Dynamic expression of notch signaling genes in neural stem/progenitor cells. Front Neurosci 5:78

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shuai K (2006) Regulation of cytokine signaling pathways by PIAS proteins. Cell Res 16(2):196–202

    CAS  PubMed  Google Scholar 

  • 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(1):79–90

    CAS  PubMed  Google Scholar 

  • Stahl N, Boulton TG, Farruggella T, Ip NY, Davis S, Witthuhn BA, Quelle FW, Silvennoinen O, Barbieri G, Pellegrini S et al (1994) Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6 beta receptor components. Science 263(5143):92–95

    CAS  PubMed  Google Scholar 

  • Struhl G, Adachi A (1998) Nuclear access and action of notch in vivo. Cell 93(4):649–660

    CAS  PubMed  Google Scholar 

  • Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, Fan G, Greenberg ME (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104(3):365–376

    CAS  PubMed  Google Scholar 

  • Taga T (1997) The signal transducer gp130 is shared by interleukin-6 family of haematopoietic and neurotrophic cytokines. Ann Med 29(1):63–72

    CAS  PubMed  Google Scholar 

  • Takahashi-Tezuka M, Yoshida Y, Fukada T, Ohtani T, Yamanaka Y, Nishida K, Nakajima K, Hibi M, Hirano T (1998) Gab1 acts as an adapter molecule linking the cytokine receptor gp130 to ERK mitogen-activated protein kinase. Mol Cell Biol 18(7):4109–4117

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takeda K, Noguchi K, Shi W, Tanaka T, Matsumoto M, Yoshida N, Kishimoto T, Akira S (1997) Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci USA 94(8):3801–3804

    CAS  PubMed  Google Scholar 

  • Takizawa T, Yanagisawa M, Ochiai W, Yasukawa K, Ishiguro T, Nakashima K, Taga T (2001) Directly linked soluble IL-6 receptor-IL-6 fusion protein induces astrocyte differentiation from neuroepithelial cells via activation of STAT3. Cytokine 13(5):272–279

    CAS  PubMed  Google Scholar 

  • Tanigaki K, Nogaki F, Takahashi J, Tashiro K, Kurooka H, Honjo T (2001) Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29(1):45–55

    CAS  PubMed  Google Scholar 

  • Temple S, Alvarez-Buylla A (1999) Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 9(1):135–141

    CAS  PubMed  Google Scholar 

  • Tokunaga A, Kohyama J, Yoshida T, Nakao K, Sawamoto K, Okano H (2004) Mapping spatio-temporal activation of Notch signaling during neurogenesis and gliogenesis in the developing mouse brain. J Neurochem 90(1):142–154

    CAS  PubMed  Google Scholar 

  • Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D (1999) Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev Biol 208(1):166–188

    CAS  PubMed  Google Scholar 

  • Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, van der Kooy D (2001) Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30(1):65–78

    CAS  PubMed  Google Scholar 

  • Uemura A, Takizawa T, Ochiai W, Yanagisawa M, Nakashima K, Taga T (2002) Cardiotrophin-like cytokine induces astrocyte differentiation of fetal neuroepithelial cells via activation of STAT3. Cytokine 18(1):1–7

    CAS  PubMed  Google Scholar 

  • Uyttendaele H, Marazzi G, Wu G, Yan Q, Sassoon D, Kitajewski J (1996) Notch4/int-3, a mammary proto-oncogene, is an endothelial cell-specific mammalian Notch gene. Development 122(7):2251–2259

    CAS  PubMed  Google Scholar 

  • Viti J, Feathers A, Phillips J, Lillien L (2003) Epidermal growth factor receptors control competence to interpret leukemia inhibitory factor as an astrocyte inducer in developing cortex. J Neurosci 23(8):3385–3393

    CAS  PubMed  Google Scholar 

  • Weinmaster G, Roberts VJ, Lemke G (1992) Notch2: a second mammalian Notch gene. Development 116(4):931–941

    CAS  PubMed  Google Scholar 

  • Wong PC, Zheng H, Chen H, Becher MW, Sirinathsinghji DJ, Trumbauer ME, Chen HY, Price DL, Van der Ploeg LH, Sisodia SS (1997) Presenilin 1 is required for Notch1 and DII1 expression in the paraxial mesoderm. Nature 387(6630):288–292

    CAS  PubMed  Google Scholar 

  • Yanagisawa M, Nakashima K, Taga T (1999) STAT3-mediated astrocyte differentiation from mouse fetal neuroepithelial cells by mouse oncostatin M. Neurosci Lett 269(3):169–172

    CAS  PubMed  Google Scholar 

  • Yanagisawa M, Nakashima K, Arakawa H, Ikenaka K, Yoshida K, Kishimoto T, Hisatsune T, Taga T (2000) Astrocyte differentiation of fetal neuroepithelial cells by interleukin-11 via activation of a common cytokine signal transducer, gp130, and a transcription factor, STAT3. J Neurochem 74(4):1498–1504

    CAS  PubMed  Google Scholar 

  • Yang X, Klein R, Tian X, Cheng HT, Kopan R, Shen J (2004) Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. Dev Biol 269(1):81–94

    CAS  PubMed  Google Scholar 

  • Yang X, Tomita T, Wines-Samuelson M, Beglopoulos V, Tansey MG, Kopan R, Shen J (2006) Notch1 signaling influences v2 interneuron and motor neuron development in the spinal cord. Dev Neurosci 28(1–2):102–117

    CAS  PubMed  Google Scholar 

  • Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, Fujiwara H, Hirata M, Yamagami T, Nakahata T, Hirabayashi T, Yoneda Y, Tanaka K, Wang WZ, Mori C, Shiota K, Yoshida N, Kishimoto T (1996) Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci USA 93(1):407–411

    CAS  PubMed  Google Scholar 

  • Yoshimatsu T, Kawaguchi D, Oishi K, Takeda K, Akira S, Masuyama N, Gotoh Y (2006) Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133(13):2553–2563

    CAS  PubMed  Google Scholar 

  • Yoshiura S, Ohtsuka T, Takenaka Y, Nagahara H, Yoshikawa K, Kageyama R (2007) Ultradian oscillations of Stat, Smad, and Hes1 expression in response to serum. Proc Natl Acad Sci USA 104(27):11292–11297

    CAS  PubMed  Google Scholar 

  • Zhu P, Hata R, Cao F, Gu F, Hanakawa Y, Hashimoto K, Sakanaka M (2008) Ramified microglial cells promote astrogliogenesis and maintenance of neural stem cells through activation of Stat3 function. FASEB J 22(11):3866–3877

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from MEYS CR Cost CZ LD11015 and the Ministry of Education, Youth and Sport of the Czech Republic MSM0021622430.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Faculty of Science, Institute of Experimental Biology, Masaryk University, Brno, Czech Republic

    Hana Kotasová, Jiřina Procházková & Jiří Pacherník

  2. Center of Biomolecular and Cellular Engineering, International Clinical Research Center, St. Anne’s University Hospital Brno, Brno, Czech Republic

    Jiří Pacherník

Authors
  1. Hana Kotasová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiřina Procházková
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiří Pacherník
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiří Pacherník.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kotasová, H., Procházková, J. & Pacherník, J. Interaction of Notch and gp130 Signaling in the Maintenance of Neural Stem and Progenitor Cells. Cell Mol Neurobiol 34, 1–15 (2014). https://doi.org/10.1007/s10571-013-9996-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-013-9996-6

Keywords

Search

Navigation