Neurog2 is a direct downstream target of the Ptf1a-Rbpj transcription complex in dorsal spinal cord

Development

Volumn 136, Issue 17, 2009, Pages 2945-2954

  Henke, R Michael ^a   Savage, Trisha K ^a   Meredith, David M ^a   Glasgow, Stavey M ^a   Hori, Kei ^a   Dumas, Judy ^a   MacDonald, Raymond J ^b   Johnson, Jane E ^a  

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

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

Author keywords

bHLH transcription factor; Cerebellum development; Dorsal neural tube development; Gene regulation; Mouse; Spinal cord development

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; NEUROGENIN 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PTF1 J; TRANSCRIPTION FACTOR PTF1A; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE LOSS; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SPINAL CORD DORSAL HORN;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CELL DIFFERENTIATION; CHICK EMBRYO; EMBRYO, MAMMALIAN; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; SIGNAL TRANSDUCTION; SPINAL CORD; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 69049083510     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.035352     Document Type: Article

References (54)

1. Beres, T., Masui, T., Swift, G. H., Shi, L., Henke, R. M. and MacDonald, R. J. (2006). 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, 117-130.
2. Bolos, V., Grego-Bessa, J. and de la Pompa, J. L. (2007). Notch signaling in development and cancer. Endocr. Rev. 28, 339-363.
3. Brinster, R. L., Chen, H. Y., Trumbauer, M. E., Yagle, M. K. and Palmiter, R. D. (1985). Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs. Proc. Natl. Acad. Sci. USA 82, 4438-4442.
4. Castro, D. S., Skowronska-Krawczyk, D., Armant, O., Donaldson, I. J., Parras, C., Hunt, C., Critchley, J. A., Nguyen, L., Gossler, A., Gottgens, B. et al. (2006). Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev. Cell 11, 831-844.
5. Cheng, L., Arata, A., Mizuguchi, R., Qian, Y., Karunaratne, A., Gray, P. A., Arata, S., Shirasawa, S., Bouchard, M., Luo, P. et al. (2004). Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat. Neurosci. 7, 510-517.
6. Cheng, L., Abdel-Samad, O., Xu, Y., Mizuguchi, R., Luo, P., Shirasawa, S., Goulding, M. and Ma, Q. (2005). Lbx1 and Tlx3 are opposing switches in determining GABAergic versus glutamatergic transmitter phenotypes. Nat. Neurosci. 8, 1510-1515.
7. Del Barrio, M. G., Taveira-Marques, R., Muroyama, Y., Yuk, D. I., Li, S., Wines-Samuelson, M., Shen, J., Smith, H. K., Xiang, M., Rowitch, D. et al. (2007). A regulatory network involving Foxn4, Mash1 and delta-like 4/Notch1 generates V2a and V2b spinal interneurons from a common progenitor pool. Development 134, 3427-3436.
8. Dullin, J. P., Locker, M., Robach, M., Henningfeld, K. A., Parain, K., Afelik, S., Pieler, T. and Perron, M. (2007). Ptf1a triggers GABAergic neuronal cell fates in the retina. BMC Dev. Biol. 7, 110.
9. Fode, C., Gradwohl, G., Morin, X., Dierich, A., LeMeur, M., Goridis, C. and Guillemot, F. (1998). The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 20, 483-494.
10. Fode, C., Ma, Q., Casarosa, S., Ang, S. L., Anderson, D. J. and Guillemot, F. (2000). A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 14, 67-80.
11. Fujitani, Y., Fujitani, S., Luo, H., Qiu, F., Burlison, J., Long, Q., Kawaguchi, Y., Edlund, H., MacDonald, R. J., Furukawa, T. et al. (2006). Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development 133, 4439-4450.
12. Glasgow, S. M., Henke, R. M., Macdonald, R. J., Wright, C. V. and Johnson, J. E. (2005). Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 132, 5461-5469.
13. Gowan, K., Helms, A. W., Hunsaker, T. L., Collisson, T., Ebert, P. J., Odom, R. and Johnson, J. E. (2001). Crossinhibitory activities of Ngn1 and Math1 allow specification of distinct dorsal interneurons. Neuron 31, 219-232.
14. Gradwohl, G., Fode, C. and Guillemot, F. (1996). Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180, 227-241.
15. Gross, M. K., Dottori, M. and Goulding, M. (2002). Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34, 535-549.
16. Guillemot, F., Lo, L. C., Johnson, J. E., Auerbach, A., Anderson, D. J. and Joyner, A. L. (1993). Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476.
17. Hand, R., Bortone, D., Mattar, P., Nguyen, L., Heng, J. I., Guerrier, S., Boutt, E., Peters, E., Barnes, A. P., Parras, C. et al. (2005). Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48, 45-62.
18. Helms, A. W. and Johnson, J. E. (2003). Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 13, 42-49.
19. Helms, A. W., Battiste, J., Henke, R. M., Nakada, Y., Simplicio, N., Guillemot, F. and Johnson, J. E. (2005). Sequential roles for Mash1 and Ngn2 in the generation of dorsal spinal cord interneurons. Development 132, 2709-2719.
20. Henke, R. M., Meredith, D. M., Borromeo, M. D., Savage, T. K. and Johnson, J. E. (2009). Ascl1 and Neurog2 form novel complexes and regulate Delta-like3 (Dll3) expression in the neural tube. Dev. Biol. 328, 529-540.
21. Hori, K., Cholewa-Waclaw, J., Nakada, Y., Glasgow, S. M., Masui, T., Henke, R. M., Wildner, H., Martarelli, B., Beres, T. M., Epstein, J. A. et al. (2008). A nonclassical bHLH Rbpj transcription factor complex is required for specification of GABAergic neurons independent of Notch signaling. Genes Dev. 22, 166-178.
22. Hoshino, M., MNakamura, S., Mori, K., Kawauchi, T., Terao, M., Nishimura, Y., Fukuda, A., Fuse, T., Matsuo, N., Sone, M. et al. (2005). Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47, 201-213.
23. Ille, F., Atanasoski, S., Falk, S., Ittner, L. M., Marki, D., Buchmann-Moller, S., Wurdak, H., Suter, U., Taketo, M. M. and Sommer, L. (2007). Wnt/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord. Dev. Biol. 304, 394-408.
24. Kageyama, R., Ohtsuka, T., Shimojo, H. and Imayoshi, I. (2008). Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci. 11, 1247-1251.
25. Kawaguchi, Y., Cooper, B., Gannon, M., Ray, M., MacDonald, R. J. and Wright, C. V. E. (2002). The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 32, 128-134.
26. Kele, J., Simplicio, N., Ferri, A. L., Mira, H., Guillemot, F., Arenas, E. and Ang, S. L. (2006). Neurogenin 2 is required for the development of ventral midbrain dopaminergic neurons. Development 133, 495-505.
27. Krapp, A., Knofler, M., Ledermann, B., Burki, K., Berney, C., Zoerkler, N., Hagenbuchle, O. and Wellauer, P. K. (1998). The bHLH protein PTF1-p48 is essential for the formation of the exocrine and the correct spatial organization of the endocrine pancreas. Genes Dev. 12, 3752-3763.
28. Kriks, S., Lanuza, G. M., Mizuguchi, R., Nakafuku, M. and Goulding, M. (2005). Gsh2 is required for the repression of Ngn1 and specification of dorsal interneuron fate in the spinal cord. Development 132, 2991-3002.
29. Louvi, A. and Artavanis-Tsakonas, S. (2006). Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 7, 93-102.
30. Ma, Q., Fode, C., Guillemot, F. and Anderson, D. J. (1999). Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Dev. 13, 1717-1728.
31. Masui, T., Long, Q., Beres, T. M., Magnuson, M. A. and MacDonald, R. J. (2007). Early pancreatic development requires the vertebrate Suppressor of Hairless (RBPJ) in the PTF1 bHLH complex. Genes Dev. 21, 2629-2643.
32. Masui, T., Swift, G. H., Hale, M. A., Meredith, D. M., Johnson, J. E. and Macdonald, R. J. (2008). Transcriptional autoregulation controls pancreatic Ptf1a expression during development and adulthood. Mol. Cell. Biol. 28, 5458-5468.
33. Mizuguchi, R., Sugimori, M., Takebayashi, H., Kosako, H., Nagao, M., Yoshida, S., Nabeshima, Y., Shimamura, K. and Nakafuku, M. (2001). Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron 31, 757-771.
34. Mizuguchi, R., Kriks, S., Cordes, R., Gossler, A., Ma, Q. and Goulding, M. (2006). Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat. Neurosci. 9, 770-778.
35. Müller, T., Brohmann, H., Pierani, A., Heppenstall, P. A., Lewin, G. R., Jessell, T. M. and Birchmeier, C. (2002). The homeodomain factor Lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34, 551-562.
36. Nakazaki, H., Reddy, A. C., Mania-Farnell, B. L., Shen, Y. W., Ichi, S., McCabe, C., George, D., McLone, D. G., Tomita, T. and Mayanil, C. S. (2008). Key basic helix-loop-helix transcription factor genes Hes1 and Ngn2 are regulated by Pax3 during mouse embryonic development. Dev. Biol. 316, 510-523.
37. Nakhai, H., Sel, S., Favor, J., Mendoza-Torres, L., Paulsen, F., Duncker, G. I. and Schmid, R. M. (2007). Ptf1a is essential for the differentiation of GABAergic and glycinergic amacrine cells and horizontal cells in the mouse retina. Development 134, 1151-1160.
38. Novitch, B. G., Chen, A. I. and Jessell, T. M. (2001). Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31, 773-789.
39. Obata, J., Yano, M., Mimura, H., Goto, T., Nakayama, R., Mibu, Y., Oka, C. and Kawaichi, M. (2001). p48 subunit of mouse PTF1 binds to RBP-Jk/CBF-1, the intracellular mediator of Notch signalling, and is expressed in the neural tube of early stage embryos. Genes Cells 6, 345-360.
40. Parras, C. M., Schuurmans, C., Scardigli, R., Kim, J., Anderson, D. J. and Guillemot, F. (2002). Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev. 16, 324-338.
41. Pascual, M., Abasolo, I., Mingorance-Le Meur, A., Martinez, A., Del Rio, J. A., Wright, C. V., Real, F. X. and Soriano, E. (2007). Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc. Natl. Acad. Sci. USA 104, 5193-5198.
42. Scardigli, R., Schuurmans, C., Gradwohl, G. and Guillemot, F. (2001). Crossregulation between neurogenin2 and pathways specifying neuronal identity in the spinal cord. Neuron 31, 203-217.
43. Scardigli, R., Bäumer, N., Gruss, P., Guillemot, F. and Le Roux, I. (2003). Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development 130, 3269-3281.
44. Schuurmans, C., Armant, O., Nieto, M., Stenman, J. M., Britz, O., Klenin, N., Brown, C., Langevin, L. M., Seibt, J., Tang, H. et al. (2004). Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J. 23, 2892-2902.
45. Seibt, J., Schuurmans, C., Gradwhol, G., Dehay, C., Vanderhaeghen, P., Guillemot, F. and Polleux, F. (2003). Neurogenin2 specifies the connectivity of thalamic neurons by controlling axon responsiveness to intermediate target cues. Neuron 39, 439-452.
46. Sellick, G. S., Barker, K. T., Stolte-Dijkstra, I., Fleischmann, C., Coleman, R. J., Garrett, C., Gloyn, A. L., Edghill, E. L., Hattersley, A. T., Wellauer, P. K. et al. (2004). Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat. Genet. 36, 1301-1305.
47. Simmons, A. D., Horton, S., Abney, A. L. and Johnson, J. E. (2001). Neurogenin2 expression in ventral and dorsal spinal neural tube progenitor cells is regulated by distinct enhancers. Dev. Biol. 229, 327-339.
48. Sommer, L., Ma, Q. and Anderson, D. J. (1996). Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogenity in the developing CNS and PNS. Mol. Cell. Neurosci. 8, 221-241.
49. Timmer, J., Johnson, J. and Niswander, L. (2001). The use of in ovo electroporation for the rapid analysis of neural-specific murine enhancers. Genesis 29, 123-132.
50. Wildner, H., Muller, T., Cho, S. H., Brohl, D., Cepko, C. L., Guillemot, F. and Birchmeier, C. (2006). dILA neurons in the dorsal spinal cord are the product of terminal and non-terminal asymmetric progenitor cell divisions, and require Mash1 for their development. Development 133, 2105-2113.
51. Yamada, M., Terao, M., Terashima, T., Fujiyama, T., Kawaguchi, Y., Nabeshima, Y. and Hoshino, M. (2007). Origin of climbing fiber neurons and their developmental dependence on Ptf1a. J. Neurosci. 27, 10924-10934.
52. Yang, X., Tomita, T., Wines-Samuelson, M., Beglopoulos, V., Tansey, M. G., Kopan, R. and Shen, J. (2006). Notch1 signaling influences v2 interneuron and motor neuron development in the spinal cord. Dev. Neurosci. 28, 102-117.
53. Yee, S. and Rigby, P. W. J. (1993). The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7, 1277-1289.
54. Zordan, P., Croci, L., Hawkes, R. and Consalez, G. G. (2008). Comparative analysis of proneural gene expression in the embryonic cerebellum. Dev. Dyn. 237, 1726-1735.