Key basic helix-loop-helix transcription factor genes Hes1 and Ngn2 are regulated by Pax3 during mouse embryonic development

Developmental Biology

Volumn 316, Issue 2, 2008, Pages 510-523

  Nakazaki, Hiromichi ^a   Reddy, Anvesh C ^a   Mania Farnell, Barbara L ^a   Shen, Yueh Wei ^a   Ichi, Shunsuke ^a   McCabe, Christopher ^a   George, David ^a   McLone, David G ^a   Tomita, Tadanori ^a   Mayanil, C S K ^a  

^a CHILDREN S MEMORIAL RESEARCH CENTER   (United States)

Author keywords

Chromatin immunoprecipitation; Explant cultures; Hes1; Neural tube; Neurogenin2; Pax3; Premature neurogenesis; Promoter; Splotch; Stem cells

Indexed keywords

HELIX LOOP HELIX PROTEIN; LUCIFERASE; NEUROGENIN 2; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR PAX3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EXPLANT; FEMALE; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY SEQUENCE; TRANSCRIPTION REGULATION;

EID: 41349083523     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.01.008     Document Type: Article

References (52)

1. Anderson D.J. Genes, lineages and the neural crest: a speculative review. Philos. Trans. R. Soc. Lond., B Biol. Sci. 355 (2000) 953-964
2. Barsi J.C., Rajendra R., Wu J.I., and Artzt K. Mind bomb1 is a ubiquitin ligase essential for mouse embryonic development and Notch signaling. Mech. Dev. 122 (2005) 1106-1117
3. Bel-Vialar S., Medevielle F., and Pituello F. The on/off of Pax6 controls the tempo of neuronal differentiation in the developing spinal cord. Dev. Biol. 305 (2007) 659-673
4. Buckingham M., and Relaix F. The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu. Rev. Cell Dev. Biol. 23 (2007) 645-673
5. Campuzano S., and Modolell J. Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 8 (1992) 202-208
6. Castella P., Sawai S., Nakao K., Wagner J.A., and Caudy M. HES-1 repression of differentiation and proliferation in PC12 cells: role for the helix 3-helix 4 domain in transcription repression. Mol. Cell. Biol. 20 (2000) 6170-6183
7. Cau E., Gradwohl G., Casarosa S., Kageyama R., and Guillemot F. Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development 127 (2000) 2323-2332
8. Daston G., Lamar E., Olivier M., and Goulding M. Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development 122 (1996) 1017-1027
9. Epstein D.J., Vekemans M., and Gros P. Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 67 (1991) 767-774
10. Epstein D.J., Vogan K.J., Trasler D.G., and Gros P. A mutation within intron 3 of the Pax-3 gene produces aberrantly spliced mRNA transcripts in the splotch (Sp) mouse mutant. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 532-536
11. Epstein J.A., Shapiro D.N., Cheng J., Lam P.Y.P., and Maas R.L. Pax3 modulates expression of the c-Met receptor during limb muscle development. J. Biol. Chem. 93 (1996) 4213-4218
12. Epstein J.A., Li J., Lang D., Chen F., Brown C.B., Jin F., Lu M.M., Thomas M., Liu E., Wessels A., and Lo C.W. Migration of cardiac neural crest cells in Splotch embryos. Development 127 (2000) 1869-1878
13. 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
14. Fode C., Ma Q., Casarosa S., Ang S.L., Anderson D.J., and Guillemot F. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 14 (2000) 67-80
15. Ge W., He F., Kim K.J., Blanchi B., Coskun V., Nguyen L., Wu X., Zhao J., Heng J.I., Martinowich K., Tao J., Wu H., Castro D., Sobeih M.M., Corfas G., Gleeson J.G., Greenberg M.E., Guillemot F., and Sun Y.E. Coupling of cell migration with neurogenesis by proneural bHLH factors. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1319-1324
16. Guillemot F. Vertebrate bHLH genes and the determination of neuronal fates. Exp. Cell Res. 253 (1999) 357-364
17. Hatfield S.D., Shcherbata H.R., Fischer K.A., Nakahara K., Carthew R.W., and Ruohola-Baker H. Stem cell division is regulated by the microRNA pathway. Nature 435 (2005) 974-978
18. Hirata H., Tomita K., Bessho Y., and Kageyama R. Hes1 and Hes3 regulate maintenance of the isthmic organizer and development of the mid/hindbrain. EMBO J. 20 (2001) 4454-4466
19. Ishibashi M., Moriyoshi K., Sasai Y., Shiota K., Nakanishi S., and Kageyama R. Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J. 13 (1994) 1799-1805
20. Ishibashi M., Ang S.-L., Shiota K., Kageyama S., and Guillemont R. 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 (1995) 3136-3148
21. Kageyama R., Ohtsuka T., Hatakeyama J., and Ohsawa R. Roles of bHLH genes in neural stem cell differentiation. Exp. Cell Res. 306 (2005) 343-348
22. Kioussi C., Gross M.K., and Gruss P. Pax3: a paired domain gene as a regulator in PNS myelination. Neuron 15 (1995) 553-562
23. Kippin T.E., Martens D.J., and van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 19 (2005) 756-767
24. Koblar S.A., Murphy M., Barrett G.L., Underhill A., Gros P., and Bartlett P.F. Pax-3 regulates neurogenesis in neural crest-derived precursor cells. J. Neurosci. Res. 56 (1999) 518-530
25. Lee S.K., and Pfaff S.L. Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38 (2003) 731-745
26. Lo L., Dormand E., Greenwood A., and Anderson D.J. Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 29 (2002) 1553-1567
27. Ma Q., Fode C., Guillemot F., and Anderson D.J. Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Dev. 13 (1999) 1717-1728
28. Maroto M., Reshef R., Munsterberg A.E., Koester S., Goulding M., and Lassar A.B. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89 (1997) 139-148
29. Maschhoff K.L., and Baldwin H.S. Molecular determinants of neural crest migration. Am. J. Med. Genet. 97 (2000) 280-288
30. Mayanil C.S.K., George D., Mania-Farnell B., Bremer C.L., McLone D.G., and Bremer E.G. Over expression of murine Pax3 increases NCAM polysialylation in a human medulloblastoma cell line. J. Biol. Chem. 275 (2000) 23259-23266
31. Mayanil C.S.K., George D., Freilich L., Miljan E.J., Mania-Farnell B., McLone D.G., and Bremer E.G. Microarray analysis detects novel Pax3 downstream target genes. J. Biol. Chem. 276 (2001) 49299-49309
32. Mayanil C.S.K., Pool A., Nakazaki H., Reddy A.C., Mania-Farnell B., Yun B., George D., McLone D.G., and Bremer E.G. Regulation of murine TGFβ2 by Pax3 during early embryonic development. J. Biol. Chem. 281 (2006) 24544-24552
33. Mizuguchi R., Sugimori M., Takebayashi H., Kosako H., Nagao M., Yoshida S., Nabeshima Y., Shimamura K., and Nakafuku M. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31 (2001) 757-771
34. Nakamura Y., Sakakibara S., Miyata T., Ogawa M., Shimazaki T., Weiss S., Kageyama R., and Okano H. The bHLH gene Hes1 as a repressor of the neuronal commitment of CNS stem cells. J. Neurosci. 20 (2000) 283-293
35. Nieto M., Schuurmans C., Britz O., and Guillemot F. Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron 29 (2001) 401-413
36. 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
37. Parras C.M., Schuurmans C., Scardigli R., Kim J., Anderson D.J., and Guillemot F. Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev. 16 (2002) 324-338
38. Péault B., Rudnicki M., Torrente Y., Cossu G., Tremblay J.P., Partridge T., Gussoni E., Kunkel L.M., and Huard J. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol. Ther. 15 (2007) 867-877
39. Perez S.E., Rebelo S., and Anderson D.J. Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126 (1999) 1715-1728
40. Ross S.E., Greenberg M.E., and Stiles C.D. Basic helix-loop-helix factors in cortical development. Neuron 39 (2003) 13-25
41. Scardigli R., Schuurmans C., Gradwohl G., and Guillemot F. Cross-regulation between Neurogenin2 and pathways specifying neuronal identity in the spinal cord. Neuron 31 (2001) 203-217
42. Schuurmans C., Armant O., Nieto M., Stenman J.M., Britz O., Klenin N., Brown C., Langevin L.M., Seibt J., Tang H., Cunningham J.M., Dyck R., Walsh C., Campbell K., Polleux F., and Guillemot F. Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J. 23 (2004) 2892-2902
43. Seibt J., Schuurmans C., Gradwhol G., Dehay C., Vanderhaeghen P., Guillemot F., and Polleux F. Neurogenin2 specifies the connectivity of thalamic neurons by controlling axon responsiveness to intermediate target cues. Neuron 39 (2003) 439-452
44. Shen Q., Goderie S.K., Jin L., Karanth N., Sun Y., Abramova N., Vincent P., Pumiglia K., and Temple S. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304 (2004) 1338-1340
45. Simmons A.D., Horton S., Abney A.L., and Johnson J.E. Neurogenin2 expression in ventral and dorsal spinal neural tube progenitor cells is regulated by distinct enhancers. Dev. Biol. 229 (2001) 327-339
46. Sugimori M., Nagao M., Bertrand N., Parras C.M., Guillemot F., and Nakafuku M. Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 134 (2007) 1617-1629
47. Sun Y.E., Nadal-Vicens M., Misono S., Lin M.Z., Zubiaga A., Hua X., Fan G., and Greenberg M.E. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104 (2001) 365-376
48. Takebayashi K., Sasai Y., Sakai Y., Watanabe T., Nakanishi S., and Kageyama R. Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1. Negative autoregulation through the multiple N box elements. J. Biol. Chem. 269 (1994) 5150-5156
49. Tajbakhsh S., Rocancourt D., Cossu G., and Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89 (1997) 127-138
50. Theriault F.M., Nuthall H.N., Dong Z., Lo R., Barnabe-Heider F., Miller F.D., and Stifani S. Role for Runx1 in the proliferation and neuronal differentiation of selected progenitor cells in the mammalian nervous system. J. Neurosci. 25 (2005) 2050-2061
51. Tomita K., Ishibashi M., Nakahara K., Ang S.L., Nakanishi S., Guillemot F., and Kageyama R. Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. Neuron 16 (1996) 723-734
52. Wilkinson D.G. In Situ Hybridization: A Practical Approach (1992), IRL Press, Oxford