FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism

Development

Volumn 136, Issue 11, 2009, Pages 1849-1858

  Thomas, Aaron J ^a   Erickson, Carol A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chick; FOXD3; MITF; Neural crest; PAX3; Pigment cell development; Quail; Transcriptional regulation

Indexed keywords

MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXD3; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL LINEAGE; CELL MIGRATION; CHICK; CONTROLLED STUDY; EMBRYO; ENZYME REGULATION; ENZYME REPRESSION; GLIA CELL; MELANOGENESIS; MELANOMA CELL; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPE; PIGMENT CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STEM CELL; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; CELL LINEAGE; CELL MOVEMENT; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; CHICK EMBRYO; EMBRYO, NONMAMMALIAN; FORKHEAD TRANSCRIPTION FACTORS; MELANOCYTES; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MOLECULAR SEQUENCE DATA; NEURAL CREST; NEUROGLIA; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; QUAIL;

AVES; PHASIANIDAE;

EID: 67650992296     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.031989     Document Type: Article

References (64)

1. Bejar, J., Hong, Y. and Schartl, M. (2003). Mitf expression is sufficient to direct differentiation of medaka blastula derived stem cells to melanocytes. Development 130, 6545-6553.
2. 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.
3. Bondurand, N., Pingault, V., Goerich, D. E., Lemort, N., Sock, E., Caignec, C. L., Wegner, M. and Goossens, M. (2000). Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum. Mol. Genet. 9, 1907-1917.
4. Carreira, S., Liu, B. and Goding, C. R. (2000). The gene encoding the T-box factor Tbx2 is a target for the Microphthalmia-associated transcription factor in melanocytes. J. Biol. Chem. 275, 21920-21927.
5. Cheng, Y., 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.
6. Cheung, M. and Briscoe, J. (2003). Neural crest development is regulated by the transcription factor Sox9. Development 130, 5681-5693.
7. Dottori, M., Gross, M. K., Labosky, P. and Goulding, M. (2001). The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 128, 4127-4138.
8. Dupin, E. and Le Douarin, N. M. (2003). Development of melanocyte precursors from the vertebrate neural crest. Oncogene 22, 3016-3023.
9. Dupin, E., Glavieux, C., Vaigot, P. and Le Douarin, N. M. (2000). Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glialmelanocytic progenitor. Proc. Natl. Acad. Sci. USA 97, 7882-7887.
10. Easwaran, H. P., Leonhardt, H. and Cardoso, M. C. (2005). Cell cycle markers for live cell analyses. Cell Cycle 4, 453-455.
11. 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.
12. Erickson, C. A. and Goins, T. L. (1995). Avian neural crest cells can migrate in the dorsolateral path only if they are specified as melanocytes. Development 121, 915-924.
13. Erickson, C. A., Duong, T. D. and Tosney, K. W. (1992). Descriptive and experimental analysis of the dispersion of neural crest cells along the dorsolateral path and their entry into ectoderm in the chick embryo. Dev. Biol. 151, 251-272.
14. Freyaldenhoven, B. S., Freyaldenhoven, M. P., Iacovoni, J. S. and Vogt, P. K. (1997a). Aberrant cell growth induced by avian winged helix proteins. Cancer Res. 57, 123-129.
15. Freyaldenhoven, B. S., Freyaldenhoven, M. P., Iacovoni, J. S. and Vogt, P. K. (1997b). Avian winged helix proteins CWH-1, CWH-2 and CWH-3 repress transcription from Qin binding sites. Oncogene 15, 483-488.
16. Fuse, N., Yasumoto, K., Suzuki, H., Takahashi, K. and Shibahara, S. (1996). Identification of a melanocyte-type promoter of the microphthalmia-associated transcription factor gene. Biochem. Biophys. Res. Commun. 219, 702-707.
17. Guo, Y., Costa, R., Ramsey, H., Starnes, T., Vance, G., Robertson, K., Kelley, M., Reinbold, R., Scholer, H. and Hromas, R. (2002). The embryonic stem cell transcription factors Oct-4 and FoxD3 interact to regulate endodermal-specific promoter expression. Proc. Natl. Acad. Sci. USA 99, 3663-3667.
18. Harris, M. L., Hall, R. and Erickson, C. A. (2008). Directing pathfinding along the dorsolateral path-the role of EDNRB2 and EphB2 in overcoming inhibition. Development 135, 4113-4122.
19. Henion, P. D. and Weston, J. A. (1997). Timing and pattern of cell fate restrictions in the neural crest lineage. Development 124, 4351-4359.
20. Henion, P. D., Blyss, G. K., Luo, R., An, M., Maynard, T. M., Cole, G. J. and Weston, J. A. (2000). Avian transitin expression mirrors glial cell fate restrictions during neural crest development. Dev. Dyn. 218, 150-159.
21. Hodgkinson, C. A., Moore, K. J., Nakayama, A., Steingrimsson, E., Copeland, N. G., Jenkins, N. A. and Arnheiter, H. (1993). Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell 74, 395-404.
22. Hodgkinson, C. A., Nakayama, A., Li, H., Swenson, L. B., Opdecamp, K., Asher, J. H., Jr, Arnheiter, H. and Glaser, T. (1998). Mutation at the anophthalmic white locus in Syrian hamsters: haploinsufficiency in the Mitf gene mimics human Waardenburg syndrome type 2. Hum. Mol. Genet. 7, 703-708.
23. Hollenbach, A. D., Sublett, J. E., McPherson, C. J. and Grosveld, G. (1999). The Pax3-FKHR oncoprotein is unresponsive to the Pax3-associated repressor hDaxx. EMBO J. 18, 3702-3711.
24. Hollenbach, A. D., McPherson, C. J., Lagutina, I. and Grosveld, G. (2002). The EF-hand calcium-binding protein calmyrin inhibits the transcriptional and DNA-binding activity of Pax3. Biochim. Biophys. Acta 1574, 321-328.
25. Hou, L., Arnheiter, H. and Pavan, W. J. (2006). Interspecies difference in the regulation of melanocyte development by SOX10 and MITF. Proc. Natl. Acad. Sci. USA 103, 9081-9085.
26. Ignatius, M. S., Moose, H. E., El-Hodiri, H. M. and Henion, P. D. (2008). colgate/hdac1 Repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev. Biol. 313, 568-583.
27. Jin, E. J., Erickson, C. A., Takada, S. and Burrus, L. W. (2001). Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev. Biol. 233, 22-37.
28. Kamaraju, A. K., Bertolotto, C., Chebath, J. and Revel, M. (2002). Pax3 downregulation and shut-off of melanogenesis in melanoma B16/F10.9 by interleukin-6 receptor signaling. J. Biol. Chem. 277, 15132-15141.
29. Kel, A. E., Gossling, E., Reuter, I., Cheremushkin, E., Kel-Margoulis, O. V. and Wingender, E. (2003). MATCH: a tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res. 31, 3576-3579.
30. 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.
31. Kuhlbrodt, K., Herbarth, B., Sock, E., Hermans-Borgmeyer, I. and Wegner, M. (1998). Sox10, a novel transcriptional modulator in glial cells. J. Neurosci. 18, 237-250.
32. Lang, D. and Epstein, J. A. (2003). Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum. Mol. Genet. 12, 937-945.
33. Le Douarin, N. M. and Dupin, E. (2003). Multipotentiality of the neural crest. Curr. Opin. Genet. Dev. 13, 529-536.
34. Levy, C., Khaled, M. and Fisher, D. E. (2006). MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med. 12, 406-414.
35. Lister, J. A., Robertson, C. P., Lepage, T., Johnson, S. L. and Raible, D. W. (1999). nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126, 3757-3767.
36. Loring, J., Glimelius, B., Erickson, C. and Weston, J. A. (1981). Analysis of developmentally homogeneous neural crest cell populations in vitro. I. Formation, morphology and differentiative behavior. Dev. Biol. 82, 86-94.
37. Magnaghi, P., Roberts, C., Lorain, S., Lipinski, M. and Scambler, P. J. (1998). HIRA, a mammalian homologue of Saccharomyces cerevisiae transcriptional co-repressors, interacts with Pax3. Nat. Genet. 20, 74-77.
38. McGill, G. G., Horstmann, M., Widlund, H. R., Du, J., Motyckova, G., Nishimura, E. K., Lin, Y. L., Ramaswamy, S., Avery, W., Ding, H. F. et al. (2002). Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109, 707-718.
39. McKeown, S. J., Lee, V. M., Bronner-Fraser, M., Newgreen, D. F. and Farlie, P. G. (2005). Sox10 overexpression induces neural crest-like cells from all dorsoventral levels of the neural tube but inhibits differentiation. Dev. Dyn. 233, 430-444.
40. Mochii, M., Ono, T., Matsubara, Y. and Eguchi, G. (1998). Spontaneous transdifferentiation of quail pigmented epithelial cell is accompanied by a mutation in the Mitf gene. Dev. Biol. 196, 145-159.
41. Monsoro-Burq, A. H., Wang, E. and Harland, R. (2005). Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev. Cell 8, 167-178.
42. Otto, A., Schmidt, C. and Patel, K. (2006). Pax3 and Pax7 expression and regulation in the avian embryo. Anat. Embryol. (Berl) 211, 293-310.
43. Ovcharenko, I., Nobrega, M. A., Loots, G. G. and Stubbs, L. (2004). ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res. 32, W280-W286.
44. Planque, N., Turque, N., Opdecamp, K., Bailly, M., Martin, P. and Saule, S. (1999). Expression of the microphthalmia-associated basic helix-loop-helix leucine zipper transcription factor Mi in avian neuroretina cells induces a pigmented phenotype. Cell Growth Differ. 10, 525-536.
45. Planque, N., Raposo, G., Leconte, L., Anezo, O., Martin, P. and Saule, S. (2004). Microphthalmia transcription factor induces both retinal pigmented epithelium and neural crest melanocytes from neuroretina cells. J. Biol. Chem. 279, 41911-41917.
46. Pohl, B. S. and Knochel, W. (2001). Overexpression of the transcriptional repressor FoxD3 prevents neural crest formation in Xenopus embryos. Mech. Dev. 103, 93-106.
47. 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.
48. Reed, J. A., Finnerty, B. and Albino, A. P. (1999). Divergent cellular differentiation pathways during the invasive stage of cutaneous malignant melanoma progression. Am. J. Pathol. 155, 549-555.
49. Reedy, M. V., Faraco, C. D. and Erickson, C. A. (1998). The delayed entry of thoracic neural crest cells into the dorsolateral path is a consequence of the late emigration of melanogenic neural crest cells from the neural tube. Dev. Biol. 200, 234-246.
50. Sasai, N., Mizuseki, K. and Sasai, Y. (2001). Requirement of FoxD3-class signaling for neural crest determination in Xenopus. Development 128, 2525-2536.
51. Steingrimsson, E., Copeland, N. G. and Jenkins, N. A. (2004). Melanocytes and the Microphthalmia transcription factor network. Annu. Rev. Genet. 38, 365-411.
52. Sutton, J., Costa, R., Klug, M., Field, L., Xu, D., Largaespada, D. A., Fletcher, C. F., Jenkins, N. A., Copeland, N. G., Klemsz, M. et al. (1996). Genesis, a winged helix transcriptional repressor with expression restricted to embryonic stem cells. J. Biol. Chem. 271, 23126-23133.
53. Swartz, M. E., Eberhart, J., Pasquale, E. B. and Krull, C. E. (2001). EphA4/ephrin-A5 interactions in muscle precursor cell migration in the avian forelimb. Development 128, 4669-4680.
54. Tachibana, M., Takeda, K., Nobukuni, Y., Urabe, K., Long, J. E., Meyers, K. A., Aaronson, S. A. and Miki, T. (1996). Ectopic expression of MITF, a gene for Waardenburg syndrome type 2, converts fibroblasts to cells with melanocyte characteristics. Nat. Genet. 14, 50-54.
55. Tachibana, M., Kobayashi, Y. and Matsushima, Y. (2003). Mouse models for four types of Waardenburg syndrome. Pigment Cell Res. 16, 448-454.
56. Takeda, K., Yasumoto, K., Takada, R., Takada, S., Watanabe, K., Udono, T., Saito, H., Takahashi, K. and Shibahara, S. (2000). Induction of melanocytespecific microphthalmia-associated transcription factor by Wnt-3a. J. Biol. Chem. 275, 14013-14016.
57. Taneyhill, L. A. and Bronner-Fraser, M. (2005). Dynamic alterations in gene expression after Wnt-mediated induction of avian neural crest. Mol. Biol. Cell 16, 5283-5293.
58. Tribulo, C., Aybar, M. J., Nguyen, V. H., Mullins, M. C. and Mayor, R. (2003). Regulation of Msx genes by a Bmp gradient is essential for neural crest specification. Development 130, 6441-6452.
59. Vance, K. W. and Goding, C. R. (2004). The transcription network regulating melanocyte development and melanoma. Pigment Cell Res. 17, 318-325.
60. Watanabe, A., Takeda, K., Ploplis, B. and Tachibana, M. (1998). Epistatic relationship between Waardenburg syndrome genes MITF and PAX3. Nat. Genet. 18, 283-286.
61. Watanabe, K., Takeda, K., Yasumoto, K., Udono, T., Saito, H., Ikeda, K., Takasaka, T., Takahashi, K., Kobayashi, T., Tachibana, M. et al. (2002). Identification of a distal enhancer for the melanocyte-specific promoter of the MITF gene. Pigment Cell Res. 15, 201-211.
62. Weston, J. A. (1991). Sequential segregation and fate of developmentally restricted intermediate cell populations in the neural crest lineage. Curr. Top. Dev. Biol. 25, 133-153.
63. Wiggan, O., Taniguchi-Sidle, A. and Hamel, P. A. (1998). Interaction of the pRB-family proteins with factors containing paired-like homeodomains. Oncogene 16, 227-236.
64. Yaklichkin, S., Steiner, A. B., Lu, Q. and Kessler, D. S. (2007). FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. J. Biol. Chem. 282, 2548-2557.