Hes6 inhibits astrocyte differentiation and promotes neurogenesis through different mechanisms

Journal of Neuroscience

Volumn 26, Issue 43, 2006, Pages 11061-11071

  Jhas, Sumit ^a   Ciura, Sorana ^a   Belanger Jasmin, Stephanie ^a   Dong, Zhifeng ^a   Llamosas, Estelle ^a   Theriault, Francesca M ^a   Joachim, Kerline ^a   Tang, Yeman ^a   Liu, Lauren ^a   Liu, Jisheng ^a   Stifani, Stefano ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Astrocyte; Cortical development; Groucho; Hes6; LXXLL motif; Neurogenesis

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES6; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN CELL; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL STRUCTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STEM CELL;

ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; GROWTH INHIBITORS; HUMANS; MICE; NEURAL INHIBITION; REPRESSOR PROTEINS;

EID: 33751084319     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1358-06.2006     Document Type: Article

References (45)

1. Bae SK, Bessho Y, Hojo M, Kageyama R (2000) The bHLH gene Hes6, an inhibitor of Hes1, promotes neuronal differentiation. Development 127:2933-2943.
2. Barnabe-Heider F, Wasylnka JA, Fernandes KJ, Porsche C, Sendtner M, Kaplan DR, Miller FD (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48:253-265.
3. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517-530.
4. Chen HA, Thiagalingam A, Chopra H, Borges MW, Feder JN, Nelkin BD, Baylin SB, Ball DW (1997) Conservation of the Drosophila lateral inhibition pathway in human lung cancer: a hairy-related protein (HES-1) directly represses achaete-scute homolog-1 expression. Proc Natl Acad Sci USA 94:5355-5360.
5. Cossins J, Vernon AE, Zhang Y, Philpott A, Jones PH (2002) Hes6 regulates myogenic differentiation. Development 129:2195-2207.
6. Fishell G, Kriegstein AR (2003) Neurons from radial glia: the consequences of asymmetric inheritance. Curr Opin Neurobiol 13:34-41.
7. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL (2000) rax, Hes1, and Notch1 promote the formation of Mueller glia by postnatal retinal progenitor cells. Neuron 26:383-394.
8. Gaiano N, Fishell G (2002) The role of Notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 25:471-490.
9. Gao X, Chandra T, Gratton MO, Quelo I, Prud'homme J, Stifani S, St-Arnaud R (2001) Hes6 acts as a transcriptional repressor in myoblasts and can induce the myogenic differentiation program. J Cell Biol 154:1161-1171.
10. Ghosh A, Greenberg ME (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15:89-103.
11. Giagtzoglou N, Alifragis P, Koumbanakis KA, Delidakis C (2003) Two modes of recruitment of E(spl) repressors onto target genes. Development 130:259-270.
12. Gratton ME, Torban E, Belanger-Jasmin S, Theriault FM, German MS, Stifani S (2003) Hes6 promotes cortical neurogenesis and inhibits Hes1 transcription repression activity by multiple mechanisms. Mol Cell Biol 23:6922-6935.
13. 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 13:1799-1805.
14. 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 9:3136-3148.
15. Jennings BH, Tyler DM, Bray SJ (1999) Target specificities of Drosophila enhancer of split basic helix-loop-helix proteins. Mol Cell Biol 19:4600-4610.
16. Job C, Tan SS (2003) Constructing the mammalian cortex: the role of intrinsic factors. Dev Biol 257:221-232.
17. Ju BG, Solum D, Song EJ, Lee KJ, Rose DW, Glass CK, Rosenfeld MG (2004) Activating the PARP-1 sensor component of the Groucho/TLE1 corepressor complex mediates a CaMKinase IIδ-dependent neurogenic gene activation pathway. Cell 119:815-829.
18. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R (2005) Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306:343-348.
19. 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 6:547-554.
20. Kang SA, Seol JH, Kim J (2005) The conserved WRPW motif of Hes6 mediates proteasomal degradation. Biochem Biophys Res Comm 332:33-36.
21. Koyano-Nakagawa N, Kim J, Anderson D, Kintner C (2000) Hes6 acts in a positive feedback loop with the neurogenins to promote neuronal differentiation. Development 127:4203-4216.
22. Lee JC, Smith SB, Watada H, Lin J, Scheel D, Wang J, Mirmira RG, German MS (2001) Regulation of the pancreatic pro-endocrine gene Neurogenin3. Diabetes 50:928-936.
23. Lee SK, Pfaff SL (2003) Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38:731-745.
24. Litterst CM, Pfitzner E (2002) An LXXLL motif in the transactivation domain of STAT6 mediates recruitment of NcoA-1/SRC-1. J Biol Chem 277:36052-36060.
25. Mahajan MA, Samuels HH (2005) Nuclear hormone receptor coregulator: role in hormone action, metabolism, growth, and development. Endocr Rev 26:583-597.
26. 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 37:751-764.
27. Marcal N, Patel H, Dong Z, Belanger-Jasmin S, Hoffman B, Helgason CD, Dang J, Stifani S (2005) Antagonistic effects of Grg6 and Groucho/TLE on the transcription repression activity of brain factor 1/FoxG1 and cortical neuron differentiation. Mol Cell Biol 25:10916-10929.
28. McLarren KW, Lo R, Grbavec D, Thirunavukkarasu K, Karsenty G, Stifani S (2000) The mammalian basic helix loop helix protein HES-1 binds to and modulates the transactivating function of the Runt-related factor Cbfa1. J Biol Chem 275:530-538.
29. McLarren KW, Theriault FM, Stifani S (2001) Association with the nuclear matrix and interaction with Groucho and RUNX proteins regulate the transcription repression activity of the basic helix loop helix factor Hes1. J Biol Chem 276:1578-1584.
30. Morrow T, Song MR, Ghosh A (2001) Sequential specification of neurons and glia by developmentally regulated extracellular factors. Development 128:3585-3594.
31. Nakashima K, Takizawa T, Occhiai W, Yanagisawa M, Hisatune T, Nakafuku M, Miyazono K, Kishimoto T, Kageyama R, Taga T (2001) BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci USA 98:5868-5873.
32. Nieto M, Schuurmans C, Britz O, Guillemot F (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29:401-413.
33. Nuthall HN, Husain J, McLarren KW, Stifani S (2002) Role for Hes1-induced phosphorylation in Groucho-mediated transcriptional repression. Mol Cell Biol 22:389-399.
34. Nuthall HN, Joachim K, Stifani S (2004) Phosphorylation of serine 239 of Groucho/TLE1 by protein kinase CK2 is important for inhibition of neuronal differentiation. Mol Cell Biol 24:8395-8407.
35. Park JK, Williams BP, Alberta JA, Stiles CD (1999) Bipotent cortical progenitor cells process conflicting cues for neurons and glia in a hierarchical manner. J Neurosci 19:10383-10389.
36. Pissarra L, Henrique D, Duarte A (2000) Expression of hes6, a new member of the Hairy/Enhancer of split family, in mouse development. Mech Dev 95:275-278.
37. Ross SE, Greenberg ME, Stiles CD (2003) Basic helix-loop-helix factors in cortical development. Neuron 39:13-25.
38. Sasai Y, Kageyama R, Tagawa Y, Shigemoto R, Nakanishi S (1992) Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev 6:2620-2634.
39. Savkur RS, Burris TP (2004) The coactivator LXXLL nuclear receptor recognition motif. J Pept Res 63:207-212.
40. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9:743-751.
41. 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 104:365-376.
42. Theriault FM, Nuthall HN, Dong Z, Lo R, Barnabe-Heider F, Miller FD, Stifani S (2005) Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. J Neurosci 25:2050-2061.
43. Vasiliauskas D, Stern C (2000) Expression of mouse HES-6, a new member of the Hairy/Enhancer of split family of bHLH transcription factors. Mech Dev 98:133-137.
44. Wu Y, Liu Y, Levine EM, Rao MS (2003) Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors. Dev Dyn 226:675-689.
45. Yao J, Lai E, Stifani S (2001) The winged helix protein brain factor 1 interacts with Groucho and Hes proteins to repress transcription. Mol Cell Biol 21:1962-1972.