A direct role for Sox10 in specification of neural crest-derived sensory neurons

Development

Volumn 133, Issue 23, 2006, Pages 4619-4630

  Carney, Thomas J ^a   Dutton, Kirsten A ^a   Greenhill, Emma ^a   Delfino Machín, Mariana ^a   Dufourcq, Pascale ^b   Blader, Patrick ^b   Kelsh, Robert N ^a  

^a University of Bath   (United Kingdom)

^b Centre de Biologie du Developpement Toulouse   (France)

Author keywords

Determination; Dorsal roots ganglion; Fate specification; Neural crest; Neurogenin; Sox10; Transgene; Waardenburg shah syndrome; Zebrafish

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; MUTANT PROTEIN; NEUROGENIN 1; PROTEIN DERIVATIVE; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FATE; CELL INTERACTION; CELL LINEAGE; CELL PROLIFERATION; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; GENE CONTROL; GENE EXPRESSION; GENE ISOLATION; GLIA CELL; NERVE CELL DIFFERENTIATION; NEURAL CREST; NONHUMAN; PIGMENT CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SENSORY NERVE CELL; SPINAL GANGLION; STEM CELL; ZEBRA FISH;

ALLELES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARRIER PROTEINS; CELL SURVIVAL; DNA; GANGLIA, SPINAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HIGH MOBILITY GROUP PROTEINS; MODELS, NEUROLOGICAL; MUTATION; NERVE TISSUE PROTEINS; NEURAL CREST; NEURONS, AFFERENT; PHENOTYPE; PROMOTER REGIONS (GENETICS); RECOMBINANT FUSION PROTEINS; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 33846041093     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02668     Document Type: Article

References (56)

1. Andermann, P., Ungos, J. and Raible, D. W. (2002). Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Dev. Biol. 251, 45-58.
2. Blader, P., Fischer, N., Gradwohl, G., Guillemot, F. and Strahle, U. (1997). The activity of Neurogenin1 is controlled by local cues in the zebrafish embryo. Development 124, 4557-4569.
3. Blader, P., Plessy, C. and Strahle, U. (2003). Multiple regulatory elements with spatially and temporally distinct activities control neurogenin1 expression in primary neurons of the zebrafish embryo. Mech. Dev. 120, 211-218.
4. Blader, P., Lam, C. S., Rastegar, S., Scardigli, R., Nicod, J. C., Simplicio, N., Plessy, C., Fischer, N., Schuurmans, C., Guillemot, F. et al. (2004). Conserved and acquired features of neurogenin1 regulation. Development 131, 5627-5637.
5. Bondurand, N., Kobetz, A., Pingault, V., Lemort, N., Encha-Razavi, F., Couly, G., Goerich, D. E., Wegner, M., Abitbol, M. and Goossens, M. (1998). Expression of the SOX10 gene during human development. FEBS Lett 432, 168-172.
6. Bondurand, N., Pingault, V., Goerich, D. E., Lemort, N., Sock, E., Le Caignec, C., Wegner, M. and Goossens, M. (2000). Interaction among SOX10 PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum. Mol. Genet. 9, 1907-1917.
7. Britsch, S., Goerich, D. E., Riethmacher, D., Peirano, R. I., Rossner, M., Nave, K. A., Birchmeier, C. and Wegner, M. (2001). The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 15, 66-78.
8. Brosamle, C. and Halpern, M. E. (2002). Characterization of myelination in the developing zebrafish. Glia 39, 47-57.
9. Cheng, Y. C., Cheung, M., Abu-Elmagd, M. M., Orme, A. and Scotting, P. J. (2000). Chick Sox10, a transcription factor expressed in both early neural crest cells and central nervous system. Dev. Brain Res. 121, 233-241.
10. Chiang, E. F., Pai, C. I., Wyatt, M., Yan, Y. L., Postlethwait, J. and Chung, B. (2001). Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites. Dev. Biol. 231, 149-163.
11. Cornell, R. A. and Eisen, J. S. (2002). Delta/Notch signaling promotes formation of zebrafish neural crest by repressing Neurogenin 1 function. Development 129, 2639-2648.
12. Dorsky, R. I., Raible, D. W. and Moon, R. T. (2000). Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev. 14, 158-162.
13. Dutton, K., Dutton, J. R., Pauliny, A. and Kelsh, R. N. (2001a). A morpholino phenocopy of the colourless mutant. Genesis 30, 188-189.
14. Dutton, K. A., Pauliny, A., Lopes, S. S., Elworthy, S., Carney, T. J., Rauch, J., Geisler, R., Haffter, P. and Kelsh, R. N. (2001b). Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128, 4113-4125.
15. Elworthy, S., Lister, J. A., Carney, T. J., Raible, D. W. and Kelsh, R. N. (2003). Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130, 2809-2818.
16. Elworthy, S., Pinto, J. P., Pettifer, A., Cancela, M. L. and Kelsh, R. N. (2005). Phox2b function in the enteric nervous system is conserved in zebrafish and is sox10-dependent. Mech. Dev. 122, 659-669.
17. Fashena, D. and Westerfield, M. (11999). Secondary motoneuron axons localize DM-GRASP on their fasciculated segments. J. Comp. Neurol. 406, 415-424.
18. Greenwood, A. L., Turner, E. E. and Anderson, D. J. (1999), Identification of dividing, determined sensory neuron precursors in the mammalian neural crest. Development 126, 3545-3559.
19. Haffter, P., Granato, M., Brand, M., Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., van Eeden, F. J., Jiang, Y. J., Heisenberg, C. P. et al. (1996). The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio, Development 123, 1-36.
20. Herbarth, B., Pingault, V., Bondurand, N., Kuhlbrodt, K., Hermans-Borgmeyer, I., Puliti, A., Lemort, N., Goossens, M. and Wegner, M. (1998). Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proc. Natl. Acad. Sci. USA 95, 5161-5165.
21. Inoue, K., Tanabe, Y. and Lupski, J. R. (1999). Myelin deficiencies in both the central and the peripheral nervous systems associated with a SOX10 mutation. Ann. Neurol. 46, 313-318.
22. Dom mouse embryos. Pediatr. Dev. Pathol. 2, 559-569.
23. Kelsh, R. N. (2006). Sorting out Sox10 functions in neural crest development. BioEssays 28, 788-798.
24. Kelsh, R. N. and Eisen, J. S. (2000). The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development 127, 515-525.
25. Kelsh, R. N. and Raible, D. W. (2002). Specification of zebrafish neural crest. In Pattern Formation in Zebrafish (ed. L. Solnicka-Kresel), pp. 216-236. Berlin, Heidelberg, New York: Springer-Verlag.
26. Kelsh, R. N., Brand, M., Jiang, Y. J., Heisenberg, C. P., Lin, S., Haffter, P., Odenthal, J., Mullins, M. C., van Eeden, F. J. M., Furutani-Seiki, M. et al. (1996). Zebrafish pigmentation mutations and the processes of neural crest development. Development 123, 369-389.
27. Kelsh, R. N., Dutton, K., Medlin, J. and Eisen, J. S. (2000). Expression of zebrafish fkd6 in neural crest-derived glia. Mech. Dev. 93, 161-164.
28. Kim, J., Lo, L., Dormand, E. and Anderson, D. J. (2003). SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38, 17-31.
29. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T.F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
30. Le Douarin, N. M. and Kalcheim, C. (11999). The Neural Crest. Cambridge: Cambridge University Press.
31. Lee, H. Y., Kleber, M., Hari, L., Brault, V., Suter, U., Taketo, M. M., Kemler, R. and Sommer, L. (2004). Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 303, 1020-1023.
32. Lee, M., Goodall, J., Verastegui, C., Ballotti, R. and Goding, C. R. (2000). Direct regulation of the Microphthalmia promoter by Sox10 links Waardenburg-Shah syndrome (WS4)-associated hypopigmentation and deafness to WS2. J. Biol. Chem. 275, 37978-37983.
33. Li, M., Zhao, C. T, Wang, Y., Zhao, Z. X. and Meng, A. M. (2002). Zebrafish sox9b is an early neural crest marker. Dev. Genes Evol. 212, 203-206.
34. Ma, Q. F., 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.
35. Malicki, J., Schier, A. F., SolnicaKrezel, L., Stemple, D. L., Neuhauss, S. C. F., Stainier, D. Y. R., Abdelilah, S., Rangini, Z., Zwartkruls, F. and Driever, W. (1996). Mutations affecting development of the zebrafish ear. Development 123, 275-283.
36. Marusich, M. F., Furneaux, H. M., Henion, P. D. and Weston, J. A. (1994). Hu neuronal proteins are expressed in proliferating neurogenic cells. J. Neurobiol. 25, 143-155.
37. Morrison, S. J., Perez, S. E., Qiao, Z., Verdi, J. M., Hicks, C., Weinmaster, G. and Anderson, D. J. (2000). Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499-510.
38. Paratore, C., Goerich, D. E., Suter, U., Wegner, M. and Sommer, L. (2001). Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128, 3949-3961.
39. Park, H. C., Boyce, J., Shin, J. and Appel, B. (2005). Oligodendrocyte specification in zebrafish requires notch-regulated cyclin-dependent kinase inhibitor function. J. Neurosci. 25, 6836-6844.
40. Perez, S. E., Rebelo, S. and Anderson, D. J. (1999). Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126, 1715-1728.
41. Pingault, V., Bondurand, N., Kuhlbrodt, K., Goerich, D. E., Prehu, M. O. Puliti, A., Herbarth, B., Hermans-Borgmeyer, I., Legius, E., Matthijs, G. et al. (1998). SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet. 18, 171-173.
42. Pingault, V., Guiochon-Mantel, A., Bondurand, N., Faure, C., Lacroix, C., Lyonnet, S., Goossens, M. and Landrieu, P. (2000). Peripheral neuropathy with hypomyelination, chronic intestinal pseudo-obstruction and deafness: a developmental "neural crest syndrome" related to a SOX10 mutation. Ann. Neurol. 48, 671-676.
43. Potterf, S. B., Furumura, M., Dunn, K. J., Arnheiter, H. and Pavan, W. J. (2000). Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum. Genet. 107, 1-6.
44. Riethmacher, D., Sonnenberg-Riethmacher, E., Brinkmann, V., Yamaai, T., Lewin, G. R. and Birchmeier, C. (1997). Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389, 725-730.
45. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
46. Sonnenberg-Riethmacher, E., Miehe, M., Stolt, C. C., Goerich, D. E., Wegner, M. and Riethmacher, D. (2001). Development and degeneration of dorsal root ganglia in the absence of the HMG-domain transcription factor Sox10. Mech. Dev. 109, 253-265.
47. Southard-Smith, E. M., Kos, L. and Pavan, W. J. (1998). Sox10 mutation disrupts neural crest development in DOM Hirschsprung mouse model. Nat. Genet 18, 60-64.
48. Takeda, K., Yasumoto, K., Takada, R., Takada, S., Watanabe, K., Udono, T., Saito, H., Takahashi, K. and Shibahara, S. (2000). Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a. J. Biol. Chem. 275, 14013-14016.
49. Touraine, R. L., Attie-Bitach, T., Manceau, E., Korsch, E., Sarda, P., Pingault, V., Encha-Razavi, F., Pelet, A., Auge, J., Nivelon-Chevallier, A. et al. (2000). Neurological phenotype in Waardenburg syndrome type 4 correlates with novel SOX10 truncating mutations and expression in developing brain. Am. J. Hum. Genet. 66, 1496-1503.
50. Ungos, J. M., Karlstrom, R. O. and Raible, D. W. (2003). Hedgehog signaling is directly required for the development of zebrafish dorsal root ganglia neurons. Development 130, 5351-5362.
51. Verastegui, C., Bille, K., Ortonne, J. P. and Ballotti, R. (2000). Regulation of the microphthalmia-associated transcription factor gene by the Waardenburg syndrome type 4 gene, SOX10. J. Biol. Chem. 275, 30757-30760.
52. Wada, N., Javidan, Y., Nelson, S., Carney, T. J., Kelsh, R. N. and Schilling, T. F. (2005). Hedgehog signaling is required for cranial neural crest morphogenesis and chondrogenesis at the midline in the zebrafish skull. Development 132, 3977-3988.
53. Wakamatsu, Y., Maynard, T. M. and Weston, J. A. (2000). Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development 127, 2811-2821.
54. Wegner, M. and Stolt, C. C. (2005). From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci. 28, 583-588.
55. Yan, Y. L., Willoughby, J., Liu, D., Crump, J. G., Wilson, C., Miller, C. T., Singer, A., Kimmel, C., Westerfield, M. and Postlethwait, J. H. (2005). A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development 132, 1069-1083.
56. Yasumoto, K., Takeda, K., Saito, H., Watanabe, K., Takahashi, K. and Shibahara, S. (2002). Microphthalmia-associated transcription factor interacts with LEF-1, a mediator of Wnt signaling. EMBO J. 21, 2703-2714.