LSox5 regulates RhoB expression in the neural tube and promotes generation of the neural crest

Development

Volumn 131, Issue 18, 2004, Pages 4455-4465

  Perez Alcala, Siro ^a   Nieto, M Angela ^a   Barbas, Julio A ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

Chick; LSox5; Neural crest; Peripheral glia; RhoB

Indexed keywords

CELL MARKER; HIGH MOBILITY GROUP PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LSOX5; TRANSCRIPTION FACTOR RHOB; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARTILAGE; CELL LINEAGE; CELL MATURATION; CHICKEN; CONTROLLED STUDY; DATA ANALYSIS; EMBRYO DEVELOPMENT; FEEDBACK SYSTEM; GANGLION; GLIA CELL; MOLECULAR CLONING; NEURAL CREST; NEURAL CREST CELL; NEURAL TUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SATELLITE CELL; SCHWANN CELL; SEQUENCE HOMOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CHICK EMBRYO; DNA-BINDING PROTEINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIGH MOBILITY GROUP PROTEINS; MOLECULAR SEQUENCE DATA; NEURAL CREST; NEUROGLIA; NEURONS; NUCLEAR PROTEINS; PERIPHERAL NERVOUS SYSTEM; PROTEIN ISOFORMS; REPRESSOR PROTEINS; RHOB GTP-BINDING PROTEIN; TRANSCRIPTION FACTORS; UP-REGULATION;

ANIMALIA; GALLUS GALLUS; GASTROPODA;

EID: 6944242562     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01329     Document Type: Article

References (58)

1. Akiyama, H., Chaboissier, M. C., Martin, J. F., Schedl, A. and de Crombrugghe, B. (2002). The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 16, 2813-2828.
2. Anderson, C. B. and Meier, S. (1981). The influence of the metameric pattern in the mesoderm on migration of cranial neural crest cells in the chick embryo. Dev. Biol. 85, 385-402.
3. Aoki, Y., Saint-Germain, N., Gyda, M., Magner-Fink, E., Lee, Y. H., Credidio, C. and Saint-jeannet, J. P. (2003). Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Dev. Biol. 259, 19-33.
4. Barembaum, M., Moreno, T. A., LaBonne, C., Sechrist, J. and Bronner-Fraser, M. (2000). Noelin-1 is a secreted glycoprotein involved in generation of the neural crest. Nat. Cell Biol. 2 219-225.
5. Bhattachyaryya, A., Frank, E., Ratner, N. and Brackenbury, R. (1991). P0 is an early marker of the Schwann cell lineage in chickens. Neuron 7, 831-80.
6. Bi, W., Deng, J. M., Zhang, Z., Behringer, R. R. and de Crombrugghe, B. (1999). Sox9 is required for cartilage formation. Nat. Genet. 22, 85-89.
7. Birgbauer, E., Sechrist, J., Bronner-Fraser, M. and Fraser, S. (1995). Rhombomeric origin and rostrocaudal reassortment of neural crest cells revealed by intravital microscopy. Development 121, 935-945.
8. Blom, N., Gammeltoft, S. and Brunak, S. (1999). Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351-1362.
9. Bowles, J., Schepers, G. and Koopman, P. (2000). Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev. Biol. 227, 239-255.
10. Britsch, S. E., Goerich, D., 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.
11. 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. Brain Res. Dev. Brain Res. 121, 233-241.
12. Cheung, M. and Briscoe, J. (2003). Neural crest development is regulated by the transcription factor Sox9. Development 130, 5681-5693.
13. del Barrio, M. G. and Nieto, M. A. (2002). Overexpression of Snail family members highlights their ability to promote chick neural crest formation. Development 129, 1583-1593.
14. del Barrio, M. G. and Nieto, M. A. (2004). Relative expression of Slug, RhoB, and HNK-1 in the cranial neural crest of the early chicken embryo. Dev. Dyn. 229, 136-139.
15. Denny, P., Swift, S., Connor, E. and Ashworth, A. (1992). An SRY-related gene expressed during spermatogenesis in the mouse encodes a sequence-specific DNA-binding protein. EMBO J. 11, 3705-3712.
16. Dottori, M., Gross, M. K., Labosky, P, and Goulding, M. (200 1). The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 128, 4127-4138.
17. Ericson, J., Thor, S., Edlund, T., Jessell, T. M. and Yamada, T. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-1560.
18. Ericson, J., Morton, S., Kawakami, A., Roelink, H. and Jessell, T. M. (1996). Two critical periods of sonic hedgehog signalling required for the specification of motor neuron identity. Cell 87, 661-673.
19. Fedtsova, N., Perris, R. and Turner, E. E. (2003). Sonic hedgehog regulates the position of the trigeminal ganglia. Dev. Biol. 261, 456-469.
20. García-Castro, M. I., Marcelle, C. and Bronner-Fraser, M. (2002). Ectodermal Wnt function as a neural crest inducer. Science 297, 848-851.
21. Graham, A., Heyman, I. and Lumsden, A. (1993). Even-numbered rhombomeres control the apoptotic elimination of neural crest cells from odd-numbered rhombomeres in the chick hindbrain. Development 119, 233-245.
22. Gubbay, J., Collignon, J., Koopman, P., Capel, B., Economou, A., Münsterberg, A., Vivian, N., Goodfellow, P. and Lovell-Badge, R. (1990). A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346, 245-250.
23. Hamburger, V. and Hamilton, H. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
24. Hiraoka, Y., Ogawa, M., Sakai, Y., Kido, S. and Aiso, S. (1998). The mouse Sox5 gene encodes a protein containing the leucine zipper and the Q box. Biochim. Biophys. Acta 1399, 40-46.
25. Huang, W., Zhou, X., Lefebvre, V. and de Crombrugghe, B. (2000). Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocyte-specific enhancer. Mol. Cell. Biol. 20, 4149-4158.
26. Ikeda, T., Zhang, J., Chano, T., Mabuchi, A., Fukuda, A., Kawaguchi, H., Nakamura, K. and Ikegawa, S. (2002). Identification and characterization of the human long form of Sox5 (L-SOX5) gene. Gene 298, 59-68.
27. Ikeya, M., Lee, S. M., Johnson, J. E., McMahon, A. P. and Takada, S. (1997). Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966-970.
28. Itasaki, N., Bel-Vialar, S. and Krumlauf, R. (1999). 'Shocking' developments in chick embryology: electroporation and in ovo gene expression. Nat. Cell Biol. 1, 203-207.
29. Kawakami, A., Kimura-Kawakami, M., Nomura, T. and Fujisawa, H. (1997). Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech. Dev. 66, 119-130.
30. 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.
31. Kos, R., Reedy, M. V., Johnson, R. L. and Erickson, C. A. (2001). The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development 128, 1467-1479.
32. LaBonne, C. and Bronner-Fraser, M. (1998). Neural crest induction in Xenopus: evidence for a two-signal model. Development 125, 2403-2414.
33. Le Douarin, N. M. and Kalcheim, C. (1999). The Neural Crest. Cambridge, UK: Cambridge University Press.
34. Lefebvre, V., Li, P. and de Crombrugghe, B. (1998). A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J. 17, 5718-5733.
35. Liem, K. F. J., Tremml, G., Roelink, H. and Jessell, T. M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969-979.
36. Lioubinski, O., Müller, M., Wegner, M. and Sander, M. (2003). Expression of Sox transcription factors in the developing mouse pancreas. Dev. Dyn. 227, 402-408.
37. Liu, J. and Jessell, T. M. (1998). A role for RhoB in the delamination of neural crest cells from the dorsal neural plate. Development 125, 5055-5057.
38. Lumsden, A., Sprawson, N. and Graham, A. (1991). Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development 113, 1281-1291.
39. Meyer, J., Sudbeck, P., Held, M., Wagner, T., Schmitz, M. L., Bricarelli, F. D., Eggermont, E., Friedrich, U., Haas, O. A., Kobelt, A. et al. (1997). Mutational analysis of the SOX9 gene in campornelic dysplasia and autosomal sex reversal: lack of genotype/phenotype correlations. Hum. Mol. Genet. 6, 91-98.
40. Minichiello, J., Ben-Ya'acov, A., Hearn, C. J., Needham, B. and Newgreen, D. F. (1999). Induction of epithelio-mesenchymal transformation of quail embryonic neural cells by inhibition of atypical protein kinase-C. Cell Tissue Res. 295, 195-206.
41. Mollaaghababa, R. and Pavan, W. J. (2003). The importance of having your SOX on: role of SOX10 in the development of neural crest-derived melanocytes and glia. Oncogene 22, 3024-3034.
42. Mori-Akiyama, Y., Akiyama, H., Rowitch, D. H. and de Crombrugghe, B. (2003). Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc. Natl. Acad. Sci. USA 100, 9360-9365.
43. Nakagawa, S. and Takeichi, M. (1995). Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 121, 1321-1332.
44. Newgreen, D. F. and Minichiello, J. (1995). Control of epitheliomesenchymal transformation. I. Events in the onset of neural crest cell migration are separable and inducible by protein kinase inhibitors. Dev. Biol. 170, 91-101.
45. Nieto, M. A. (2002). The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3 155-166.
46. Nieto, M. A., Sargent, M. G., Wilkinson, D. G. and Cooke, J. (1994). Control of cell behaviour during development by Slug, a zinc finger gene. Science 264, 835-839.
47. Nieto, M. A., Patel, K. and Wilkinson, D. G. (1996). In situ hybridisation analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol. 51, 220-235.
48. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 15, 193-199.
49. 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.
50. Peirano, R. I., Goerich, D. E., Riethmacher, D. and Wegner, M. (2000). Protein zero gene expression is regulated by the glial transcription factor Sox10. Mol. Cell. Biol. 20, 3198-3209.
51. Schepers, G. E., Teasdale, R. D. and Koopman, P. (2002). Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev. Cell 3, 167-170.
52. Selleck, M. A., García-Castro, M. I., Artinger, K. B. and Bronner-Fraser, M. (1998). Effects of Shh and Noggin on neural crest formation demonstrate that BMP is required in the neural tube but not ectoderm. Development 125, 4919-4930.
53. Smits, P., Li, P., Mandel, J., Zhang, Z., Deng, J. M., Behringer, R. R., de Croumbrugghe, B. and Lefebvre, V. (2001). The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell 1, 277-290.
54. Somasiri, A., Howarth, A., Goswami, D., Dedhar, S. and Roskelley, C. D. (2001). Overexpression of the integrin-linked kinase mesenchymally transforms mammary epithelial cells. J. Cell. Sci. 114, 1125-1136.
55. Tosney, K. W. (1982). The segregation and early migration of cranial neural crest cells in the avian embryo. Dev. Biol. 89, 13-24.
56. Tucker, G. C., Aoyama, H., Lipinski, M., Tirsz, T. and Thiery, J. P. (1984). Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Differ. 14, 223-230.
57. Villanueva, S., Glavic, A., Ruiz, P. and Mayor, R. (2002). Posterization by FGF, Wnt, and retinoic acid is required for neural crest induction. Dev. Biol. 241, 289-301.
58. Wunderle, V. M., Critcher, R., Ashworth, A. and Goodfellow, P. N. (1996). Cloning and characterization of SOX5, a new member of the human SOX gene family. Genomics 36, 354-358.