Ascl1 and Neurog2 form novel complexes and regulate Delta-like3 (Dll3) expression in the neural tube

Developmental Biology

Volumn 328, Issue 2, 2009, Pages 529-540

  Henke, R Michael ^a   Meredith, David M ^a   Borromeo, Mark D ^a   Savage, Trisha K ^a   Johnson, Jane E ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

bHLH transcription factors; Delta; Dorsal spinal cord development; Gene regulation; Mash1; Neurogenin; Notch ligands

Indexed keywords

DELTA LIKE 3 PROTEIN; GREEN FLUORESCENT PROTEIN; HELIX LOOP HELIX PROTEIN; NEUROGENIN 2; NOTCH RECEPTOR; TRANSCRIPTION FACTOR MASH1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN MATURATION; CONTROLLED STUDY; DNA BINDING; E BOX ELEMENT; EMBRYO; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENE MUTATION; GENE REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; REPRESSOR GENE;

MUS MUSCULUS;

EID: 63349094403     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.01.007     Document Type: Article

References (44)

1. Anand G., Yin X., Shahidi A.K., Grove L., and Prochownik E.V. Novel regulation of the helix-loop-helix protein Id1 by S5a, a subunit of the 26 S proteasome. J. Biol. Chem. 272 (1997) 19140-19151
2. Begley C.G., Lipkowitz S., Gobel V., Mahon K.A., Bertness V., Green A.R., Gough N.M., and Kirsch I.R. Molecular characterization of NSCL, a gene encoding a helix-loop-helix protein expressed in the developing nervous system. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 38-42
3. Beres T., Masui T., Swift G.H., Shi L., Henke R.M., and MacDonald R.J. PTF1 is an organ-specific and Notch-independent bHLH complex containing the mammalian Suppressor of Hairless (RBP-J) or its paralogue RBP-L. Mol. Cell. Biol. 26 (2006) 117-130
4. Bertrand N., Castro D.S., and Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosc. 3 (2002) 517-530
5. Bettenhausen B., Hrabe de Angelis M., Simon D., Guenet J.-L., and Gossler A. Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development 121 (1995) 2407-2418
6. Brinster R.L., Chen H.Y., Trumbauer M.E., Yagle M.K., and Palmiter R.D. Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs. Proc. Natl. Acad. Sci. U. S. A. 82 (1985) 4438-4442
7. Brown L., Espinosa R., Le Beau M.M., Siciliano M.J., and Baer R. HEN1 and HEN2: a subgroup of basic helix-loop-helix genes that are coexpressed in a human neuroblastoma. Proc. Natl. Acad. Sci. 89 (1992) 8492-8496
8. Casarosa S., Fode C., and Guillemot F. Mash1 regulates neurogenesis in the ventral telencephalon. Development 126 (1999) 525-534
9. Castro D.S., Skowronska-Krawczyk D., Armant O., Donaldson I.J., Parras C., Hunt C., Critchley J.A., Nguyen L., Gossler A., Gottgens B., Matter J.M., and Guillemot F. Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev. Cell 11 (2006) 831-844
10. Dunwoodie S.L., Henrique D., Harrison S.M., and Beddington R.S. 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 (1997) 3065-3076
11. Fode C., Gradwohl G., Morin X., Dierich A., LeMeur M., Goridis C., and Guillemot F. The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 20 (1998) 483-494
12. Geffers I., Serth K., Chapman G., Jaekel R., Schuster-Gossler K., Cordes R., Sparrow D.B., Kremmer E., Dunwoodie S.L., Klein T., and Gossler A. Divergent functions and distinct localization of the Notch ligands DLL1 and DLL3 in vivo. J. Cell Biol. 178 (2007) 465-476
13. Genetta T., Ruezinsky D., and Kadesch T. Displacement of an E-box-binding repressor by basic helix-loop-helix proteins: implications for B-cell specificity of the immunoglobulin heavy-chain enhancer. Mol. Cell. Biol. 14 (1994) 6153-6163
14. Gohlke J.M., Armant O., Parham F.M., Smith M.V., Zimmer C., Castro D.S., Nguyen L., Parker J.S., Gradwohl G., Portier C.J., and Guillemot F. Characterization of the proneural gene regulatory network during mouse telencephalon development. BMC Biol. 6 (2008) 15
15. Gowan K., Helms A.W., Hunsaker T.L., Collisson T., Ebert P.J., Odom R., and Johnson J.E. Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 31 (2001) 219-232
16. Gradwohl G., Fode C., and Guillemot F. Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180 (1996) 227-241
17. Guillemot F., Lo L.C., Johnson J.E., Auerbach A., Anderson D.J., and Joyner A.L. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75 (1993) 463-476
18. Helms A.W., Battiste J., Henke R.M., Nakada Y., Simplicio N., Guillemot F., and Johnson J.E. Sequential roles for Mash1 and Ngn2 in the generation of dorsal spinal cord interneurons. Development 132 (2005) 2709-2719
19. Johnson J.E., Birren S.J., and Anderson D.J. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346 (1990) 858-861
20. Johnson J.E., Birren S.J., Saito T., and Anderson D.J. DNA binding and transcriptional regulatory activity of mammalian achaete-scute homologous (MASH) proteins revealed by interaction with a muscle-specific enhancer. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 3596-3600
21. Kageyama R., Ishibashi M., Takebayashi K., and Tomita K. bHLH transcription factors and mammalian neuronal differentiation. Int. J. Biochem. Cell Biol. 29 (1997) 1389-1399
22. Kageyama R., and Ohtsuka T. The Notch-Hes pathway in mammalian neural development. Cell Res. 9 (1999) 179-188
23. Ladi E., Nichols J.T., Ge W., Miyamoto A., Yao C., Yang L.T., Boulter J., Sun Y.E., Kintner C., and Weinmaster G. The divergent DSL ligand Dll3 does not activate Notch signaling but cell autonomously attenuates signaling induced by other DSL ligands. J. Cell Biol. 170 (2005) 983-992
24. Lendahl U. A growing family of Notch ligands. Bioessays 20 (1998) 103-107
25. Lindsell C.E., Boulter J., diSibio G., Gossler A., and Weinmaster G. Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol. Cell. Neurosci. 8 (1996) 14-27
26. Louvi A., and Artavanis-Tsakonas S. Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 7 (2006) 93-102
27. Ma Q., Chen Z., del Barco Barrantes I., de la Pompa J.L., and Anderson D.J. neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 120 (1998) 469-482
28. Ma Q., Sommer L., Cserjesi P., and Anderson D.J. Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J. Neurosci. 17 (1997) 3644-3652
29. Massari M.E., and Murre C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20 (2000) 429-440
30. Matsunaga E., Araki I., and Nakamura H. Role of Pax3/7 in the tectum regionalization. Development 128 (2001) 4069-4077
31. Murre C., Bain G., van Dijk M.A., Engel I., Furnari B.A., Massari M.E., Matthews J.R., Quong M.W., Rivera R.R., and Stuiver M.H. Structure and function of helix-loop-helix proteins. Biochim. Biophys. Acta 1218 (1994) 129-135
32. Odenwald W.F., Rasband W., Kuzin A., and Brody T. EVOPRINTER, a multigenomic comparative tool for rapid identification of functionally important DNA. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 14700-14705
33. Ohtsuka T., Ishibashi M., Gradwohl G., Nakanishi S., Guillemot F., and Kageyama R. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J. 18 (1999) 2196-2207
34. Poitras L., Ghanem N., Hatch G., and Ekker M. The proneural determinant MASH1 regulates forebrain Dlx1/2 expression through the I12b intergenic enhancer. Development 134 (2007) 1755-1765
35. Powell L.M., Zur Lage P.I., Prentice D.R., Senthinathan B., and Jarman A.P. The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites. Mol. Cell. Biol. 24 (2004) 9517-9526
36. Sasai Y., Kageyama R., Tagawa Y., Shigemoto R., and Nakanishi S. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 6 (1992) 2620-2634
37. Shutter J.R., Scully S., Fan W., Richards W.G., Kitajewski J., Deblandre G.A., Kintner C.R., and Stark K.L. Dll4, a novel Notch ligand expressed in arterial endothelium. Genes Dev. 14 (2000) 1313-1318
38. Singson A., Leviten M.W., Bang A.G., Hua X.H., and Posakony J.W. Direct downstream targets of proneural activators in the imaginal disc include genes involved in lateral inhibitory signaling. Genes Dev. 8 (1994) 2058-2071
39. Sommer L., Ma Q., and Anderson D.J. Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell. Neurosci. 8 (1996) 221-241
40. Suemori H., Kadodawa Y., Goto K., Araki I., Kondoh H., and Nakatsuji N. A mouse embryonic stem cell line showing pluripotency of differentiation in early embryos and ubiquitous beta-galactosidase expression. Cell Differ. Dev. 29 (1990) 181-186
41. Timmer J., Johnson J., and Niswander L. The use of in ovo electroporation for the rapid analysis of neural-specific murine enhancers. Genesis 29 (2001) 123-132
42. Weintraub H., Genetta T., and Kadesch T. Tissue-specific gene activation by MyoD: determination of specificity by cis-acting repression elements. Genes Dev. 8 (1994) 2203-2211
43. Yoshida I., Koide S., Hasegawa S.I., Nakagawara A., Tsuji A., and Matsuda Y. Proprotein convertase PACE4 is down-regulated by the basic helix-loop-helix transcription factor hASH-1 and MASH-1. Biochem. J. 360 (2001) 683-689
44. Zhang C., Ng K.L., Li J.D., He F., Anderson D.J., Sun Y.E., and Zhou Q.Y. Prokineticin 2 is a target gene of proneural basic helix-loop-helix factors for olfactory bulb neurogenesis. J. Biol. Chem. 282 (2007) 6917-6921