HES5 is a key mediator of wnt-3a-induced neuronal differentiation

Stem Cells and Development

Volumn 23, Issue 12, 2014, Pages 1328-1339

  Mußmann, Carolin ^a   Hübner, Rayk ^a   Trilck, Michaela ^a   Rolfs, Arndt ^a   Frech, Moritz J ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; BETA CATENIN; DICKKOPF 1 PROTEIN; GAMMA SECRETASE INHIBITOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; NOTCH RECEPTOR; WNT3A PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HES5 PROTEIN, HUMAN; INDOLE DERIVATIVE; MALEIMIDE DERIVATIVE; REPRESSOR PROTEIN;

ARTICLE; CELL FATE; CELL THERAPY; CONTROLLED STUDY; DEGENERATIVE DISEASE; GENE; GENE CONTROL; GENE OVEREXPRESSION; GENE REPRESSION; HES 1 GENE; HES 5 GENE; HUMAN; HUMAN CELL; MASH 1 GENE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INDOLES; INDUCED PLURIPOTENT STEM CELLS; MALEIMIDES; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; RECEPTORS, NOTCH; REPRESSOR PROTEINS; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

EID: 84902139005     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0557     Document Type: Article

References (51)

1. Lindvall O and Z Kokaia. (2010). Stem cells in human neurodegenerative disorders-time for clinical translation? J Clin Invest 120:29-40.
2. Aiba K, AA Sharov, MG Carter, C Foroni, AL Vescovi and MS Ko. (2006). Defining a developmental path to neural fate by global expression profiling of mouse embryonic stem cells and adult neural stem/progenitor cells. Stem Cells 24:889-895.
3. Xu Y, Y Shi and S Ding. (2008). A chemical approach to stem-cell biology and regenerative medicine. Nature 453: 338-344.
4. Kageyama R, T Ohtsuka, J Hatakeyama and R Ohsawa. (2005). Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306:343-348.
5. Muroyama Y, H Kondoh and S Takada. (2004). Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem Biophys Res Commun 313:915-921.
6. Hirabayashi Y, Y Itoh, H Tabata, K Nakajima, T Akiyama, N Masuyama and Y Gotoh. (2004). The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131:2791-2801.
7. Kageyama R, T Ohtsuka and T Kobayashi. (2008). Roles of Hes genes in neural development. Dev Growth Differ 50 Suppl 1:S97-S103.
8. Kabos P, A Kabosova and T Neuman. (2002). Blocking HES1 expression initiates GABAergic differentiation and induces the expression of p21(CIP1/WAF1) in human neural stem cells. J Biol Chem 277:8763-8766.
9. Kamakura S, K Oishi, T Yoshimatsu, M Nakafuku, N Masuyama and Y Gotoh. (2004). Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol 6:547-554.
10. Borghese L, D Dolezalova, T Opitz, S Haupt, A Leinhaas, B Steinfarz, P Koch, F Edenhofer, A Hampl and O Brustle. (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 28:955-964.
11. Woo SM, J Kim, HW Han, JI Chae, MY Son, S Cho, HM Chung, YM Han and YK Kang. (2009). Notch signaling is required for maintaining stem-cell features of neuroprogenitor cells derived from human embryonic stem cells. BMC Neurosci 10:10-97.
12. Hojo M, T Ohtsuka, N Hashimoto, G Gradwohl, F Guillemot and R Kageyama. (2000). Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127:2515-2522.
13. Hayward P, T Kalmar and AM Arias. (2008). Wnt/Notch signalling and information processing during development. Development 135:411-424.
14. Komiya Y and R Habas. (2008). Wnt signal transduction pathways. Organogenesis 4:68-75.
15. Nakaya MA, K Biris, T Tsukiyama, S Jaime, JA Rawls and TP Yamaguchi. (2005). Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development 132:5425-5436.
16. Hubner R, AC Schmole, A Liedmann, MJ Frech, A Rolfs and J Luo. (2010). Differentiation of human neural progenitor cells regulated by Wnt-3a. Biochem Biophys Res Commun 400:358-362.
17. Mazemondet O, R Hubner, J Frahm, D Koczan, BM Bader, DG Weiss, AM Uhrmacher, MJ Frech, A Rolfs and J Luo. (2011). Quantitative and kinetic profile of Wnt/beta-catenin signaling components during human neural progenitor cell differentiation. Cell Mol Biol Lett 16:515-538.
18. Hirsch C, LM Campano, S Wohrle and A Hecht. (2007). Canonical Wnt signaling transiently stimulates proliferation and enhances neurogenesis in neonatal neural progenitor cultures. Exp Cell Res 313:572-587.
19. Park IH, R Zhao, JA West, A Yabuuchi, H Huo, TA Ince, PH Lerou, MW Lensch and GQ Daley. (2008). Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451:141-146.
20. Trilck M, R Hubner, P Seibler, C Klein, A Rolfs and MJ Frech. (2013). Niemann-Pick type C1 patient-specific induced pluripotent stem cells display disease specific hallmarks. Orphanet J Rare Dis 8:144.
21. Morgan PJ, R Hubner, A Rolfs and MJ Frech. (2013). Spontaneous calcium transients in human neural progenitor cells mediated by transient receptor potential channels. Stem Cells Dev 22:2477-2486.
22. Noggle SA, D Weiler and BG Condie. (2006). Notch signaling is inactive but inducible in human embryonic stem cells. Stem Cells 24:1646-1653.
23. Imura T, I Nakano, HI Kornblum and MV Sofroniew. (2006). Phenotypic and functional heterogeneity of GFAPexpressing cells in vitro: differential expression of LeX/ CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 53:277-293.
24. Ge W, K Martinowich, X Wu, F He, A Miyamoto, G Fan, G Weinmaster and YE Sun. (2002). Notch signaling promotes astrogliogenesis via direct CSL-mediated glial gene activation. J Neurosci Res 69:848-860.
25. Giese AK, J Frahm, R Hubner, JK Luo, A Wree, MJ Frech, A Rolfs and S Ortinau. (2010). Erythropoietin and the effect of oxygen during proliferation and differentiation of human neural progenitor cells. BMC Cell Biol 11:94.
26. Schmole AC, A Brennfuhrer, G Karapetyan, R Jaster, A Pews-Davtyan, R Hubner, S Ortinau, M Beller, A Rolfs and MJ Frech. (2010). Novel indolylmaleimide acts as GSK-3beta inhibitor in human neural progenitor cells. Bioorg Med Chem 18:6785-6795.
27. Kunke D, V Bryja, L Mygland, E Arenas and S Krauss. (2009). Inhibition of canonical Wnt signaling promotes gliogenesis in P0-NSCs. Biochem Biophys Res Commun 386:628-633.
28. Yang J, X Li, Y Li, M Southwood, L Ye, L Long, RS Al-Lamki and NW Morrell. (2013). Id proteins are critical downstream effectors of BMP signaling in human pulmonary arterial smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 305:L312-L321.
29. Semenov MV, K Tamai, BK Brott, M Kuhl, S Sokol and X He. (2001). Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr Biol 11:951-961.
30. Dubreuil V, MR Hirsch, C Jouve, JF Brunet and C Goridis. (2002). The role of Phox2b in synchronizing pan-neuronal and type-specific aspects of neurogenesis. Development 129:5241-5253.
31. Wu Y, Y Liu, EM Levine and MS Rao. (2003). Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors. Dev Dyn 226:675-689.
32. Bai G and SL Pfaff. (2011). Protease regulation: the Yin and Yang of neural development and disease. Neuron 72:9-21.
33. Haupt S, L Borghese, O Brustle and F Edenhofer. (2012). Non-genetic modulation of Notch activity by artificial delivery of Notch intracellular domain into neural stem cells. Stem Cell Rev 8:672-684.
34. Esfandiari F, A Fathi, H Gourabi, S Kiani, S Nemati and H Baharvand. (2012). Glycogen synthase kinase-3 inhibition promotes proliferation and neuronal differentiation of human-induced pluripotent stem cell-derived neural progenitors. Stem Cells Dev 21:3233-3243.
35. Nelson BR, BH Hartman, SA Georgi, MS Lan and TA Reh. (2007). Transient inactivation of Notch signaling synchronizes differentiation of neural progenitor cells. Dev Biol 304:479-498.
36. Wall DS, AJ Mears, B McNeill, C Mazerolle, S Thurig, Y Wang, R Kageyama and VA Wallace. (2009). Progenitor cell proliferation in the retina is dependent on Notchindependent Sonic hedgehog/Hes1 activity. J Cell Biol 184:101-112.
37. Takebayashi K, Y Sasai, Y Sakai, T Watanabe, S Nakanishi and R Kageyama. (1994). Structure, chromosomal locus and promoter analysis of the gene encoding the mouse helixloop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J Biol Chem 269:5150-5156.
38. Kageyama R, T Ohtsuka, H Shimojo and I Imayoshi. (2009). Dynamic regulation of Notch signaling in neural progenitor cells. Curr Opin Cell Biol 21:733-740.
39. Basak O and V Taylor. (2007). Identification of selfreplicating multipotent progenitors in the embryonic nervous system by high Notch activity and Hes5 expression. Eur J Neurosci 25:1006-1022.
40. Ohtsuka T, M Ishibashi, G Gradwohl, S Nakanishi, F Guillemot and R Kageyama. (1999). Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 18:2196-2207.
41. Gomes FC, D Paulin and N Moura, V. (1999). Glial fibrillary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Braz J Med Biol Res 32:619-631.
42. Garcia AD, NB Doan, T Imura, TG Bush and MV Sofroniew. (2004). GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233-1241.
43. Ijuin K, K Nakanishi and K Ito. (2008). Different downstream pathways for Notch signaling are required for gliogenic and chondrogenic specification of mouse mesencephalic neural crest cells. Mech Dev 125:462-474.
44. Shimizu T, M Nakazawa, S Kani, YK Bae, T Shimizu, R Kageyama and M Hibi. (2010). Zinc finger genes Fezf1 and Fezf2 control neuronal differentiation by repressing Hes5 expression in the forebrain. Development 137:1875-1885.
45. Hartl D, M Irmler, I Romer, MT Mader, L Mao, C Zabel, MH de Angelis, J Beckers and J Klose. (2008). Transcriptome and proteome analysis of early embryonic mouse brain development. Proteomics 8:1257-1265.
46. Tiberi L, AJ van den, J Dimidschstein, J Piccirilli, D Gall, A Herpoel, A Bilheu, J Bonnefont, M Iacovino, et al. (2012). BCL6 controls neurogenesis through Sirt1-dependent epigenetic repression of selective Notch targets. Nat Neurosci 15:1627-1635.
47. Espinosa L, J Ingles-Esteve, C Aguilera and A Bigas. (2003). Phosphorylation by glycogen synthase kinase-3 beta down-regulates Notch activity, a link for Notch and Wnt pathways. J Biol Chem 278:32227-32235.
48. Duncan AW, FM Rattis, LN DiMascio, KL Congdon, G Pazianos, C Zhao, K Yoon, JM Cook, K Willert, N Gaiano and T Reya. (2005). Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 6:314-322.
49. Aoyama K, C Delaney, B Varnum-Finney, AD Kohn, RT Moon and ID Bernstein. (2007). The interaction of the Wnt and Notch pathways modulates natural killer versus T cell differentiation. Stem Cells 25:2488-2497.
50. Shimizu T, T Kagawa, T Inoue, A Nonaka, S Takada, H Aburatani and T Taga. (2008). Stabilized beta-catenin functions through TCF/LEF proteins and the Notch/RBPJkappa complex to promote proliferation and suppress differentiation of neural precursor cells. Mol Cell Biol 28:7427-7441.
51. Lie DC, SA Colamario, HJ Song, L Desire, H Mira, A Consiglio, ES Lein, S Jessberger, H Lansford, AR Dearie and FH Gage. (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375.