An iterative genetic and dynamical modelling approach identifies novel features of the gene regulatory network underlying melanocyte development

PLoS Genetics

Volumn 7, Issue 9, 2011, Pages

  Greenhill, Emma R ^a   Rocco, Andrea ^b,c   Vibert, Laura ^a   Nikaido, Masataka ^a,d   Kelsh, Robert N ^a  

^a University of Bath   (United Kingdom)

^b University of Bath   (United Kingdom)

^c UNIVERSITY OF SURREY   (United Kingdom)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MELANIN; PROTEIN SOX9B; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; HDAC1 PROTEIN, ZEBRAFISH; HISTONE DEACETYLASE 1; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITFA PROTEIN, ZEBRAFISH; SOX10 PROTEIN, ZEBRAFISH; SOX9B PROTEIN, ZEBRAFISH; TRANSCRIPTION FACTOR SOX; ZEBRAFISH PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; GENE REPRESSION; GENETIC MODEL; MATHEMATICAL MODEL; MELANOCYTE; MITFA GENE; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; VALIDATION PROCESS; ZEBRA FISH; ANIMAL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NEURAL CREST; STEM CELL; THEORETICAL MODEL; WNT SIGNALING PATHWAY;

DANIO RERIO;

ANIMALS; CELL DIFFERENTIATION; GENE REGULATORY NETWORKS; HISTONE DEACETYLASE 1; MELANOCYTES; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MODELS, THEORETICAL; NEURAL CREST; SOX9 TRANSCRIPTION FACTOR; SOXE TRANSCRIPTION FACTORS; STEM CELLS; WNT SIGNALING PATHWAY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 80053460696     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002265     Document Type: Article

References (76)

1. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, et al. (2002) A genomic regulatory network for development. Science 295: 1669-1678.
2. Ben-Tabou de-Leon S, Davidson EH, (2006) Deciphering the underlying mechanism of specification and differentiation: the sea urchin gene regulatory network. Sci STKE 2006: pe47.
3. Huang S, Guo YP, May G, Enver T, (2007) Bifurcation dynamics in lineage-commitment in bipotent progenitor cells. Dev Biol 305: 695-713.
4. White RJ, Nie Q, Lander AD, Schilling TF, (2007) Complex regulation of cyp26a1 creates a robust retinoic acid gradient in the zebrafish embryo. PLoS Biol 5: e304 doi:10.1371/journal.pbio.0050304.
5. Giudicelli F, Ozbudak EM, Wright GJ, Lewis J, (2007) Setting the tempo in development: an investigation of the zebrafish somite clock mechanism. PLoS Biol 5: e150 doi:10.1371/journal.pbio.0050150.
6. Nordlund JJ, Boissy RE, Hearing VJ, King CY, Oetting WS, et al. (2006) The Pigmentary System: Physiology and Pathophysiology Malden, Oxford, Victoria Blackwell Publishing Ltd.
7. Bennett DC, Lamoreux ML, (2003) The color loci of mice-a genetic century. Pigment Cell Res 16: 333-344.
8. Raible DW, Wood A, Hodsdon W, Henion PD, Weston JA, et al. (1992) Segregation and early dispersal of neural crest cells in the embryonic zebrafish. Dev Dyn 195: 29-42.
9. Rawles ME, (1947) Origin of pigment cells from the neural crest in the mouse embryo. Physiol Zool 20: 248-266.
10. Schilling TF, Kimmel CB, (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120: 483-494.
11. Nishimura EK, Jordan SA, Oshima H, Yoshida H, Osawa M, et al. (2002) Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416: 854-860.
12. Hodgkinson CA, Moore KJ, Nakayama A, Steingrimsson E, Copeland NG, et al. (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.
13. Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW, (1999) nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126: 3757-3767.
14. Bondurand N, Pingault V, Goerich DE, Lemort N, Sock E, et al. (2000) Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum Mol Genet 9: 1907-1917.
15. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, et al. (2001) Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128: 4113-4125.
16. Elworthy S, Lister JA, Carney TJ, Raible DW, Kelsh RN, (2003) Transcriptional regulation of mitfa accounts for the sox10 requirement in zebrafish melanophore development. Development 130: 2809-2818.
17. Lee M, Goodall J, Verastegui C, Ballotti R, Goding CR, (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.
18. Potterf SB, Furumura M, Dunn KJ, Arnheiter H, Pavan WJ, (2000) Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet 107: 1-6.
19. Verastegui C, Bille K, Ortonne JP, 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.
20. Watanabe K, Takeda K, Yasumoto K, Udono T, Saito H, et al. (2002) Identification of a distal enhancer for the melanocyte-specific promoter of the MITF gene. Pigment Cell Res 15: 201-211.
21. Cronin JC, Wunderlich J, Loftus SK, Prickett TD, Wei X, et al. (2009) Frequent mutations in the MITF pathway in melanoma. Pigment Cell Melanoma Res 22: 435-444.
22. Garraway LA, Widlund HR, Rubin MA, Getz G, Berger AJ, et al. (2005) Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436: 117-122.
23. Murisier F, Guichard S, Beermann F, (2007) The tyrosinase enhancer is activated by Sox10 and Mitf in mouse melanocytes. Pigment Cell Res 20: 173-184.
24. Hou L, Arnheiter H, Pavan WJ, (2006) Interspecies difference in the regulation of melanocyte development by SOX10 and MITF. Proc Natl Acad Sci U S A 103: 9081-9085.
25. Ludwig A, Rehberg S, Wegner M, (2004) Melanocyte-specific expression of dopachrome tautomerase is dependent on synergistic gene activation by the Sox10 and Mitf transcription factors. FEBS Lett 556: 236-244.
26. Jiao Z, Mollaaghababa R, Pavan WJ, Antonellis A, Green ED, et al. (2004) Direct interaction of Sox10 with the promoter of murine Dopachrome Tautomerase (Dct) and synergistic activation of Dct expression with Mitf. Pigment Cell Res 17: 352-362.
27. Potterf SB, Mollaaghababa R, Hou L, Southard-Smith EM, Hornyak TJ, et al. (2001) Analysis of SOX10 function in neural crest-derived melanocyte development: SOX10-dependent transcriptional control of dopachrome tautomerase. Dev Biol 237: 245-257.
28. Carney TJ, Dutton KA, Greenhill E, Delfino-Machin M, Dufourcq P, et al. (2006) A direct role for Sox10 in specification of neural crest-derived sensory neurons. Development 133: 4619-4630.
29. Kelsh RN, Brand M, Jiang YJ, Heisenberg CP, Lin S, et al. (1996) Zebrafish pigmentation mutations and the processes of neural crest development. Development 123: 369-389.
30. Passeron T, Valencia JC, Bertolotto C, Hoashi T, Le Pape E, et al. (2007) SOX9 is a key player in ultraviolet B-induced melanocyte differentiation and pigmentation. Proc Natl Acad Sci U S A 104: 13984-13989.
31. Cook AL, Smith AG, Smit DJ, Leonard JH, Sturm RA, (2005) Co-expression of SOX9 and SOX10 during melanocytic differentiation in vitro. Exp Cell Res 308: 222-235.
32. Chiang EF, Pai CI, Wyatt M, Yan YL, Postlethwait J, et al. (2001) Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites. Dev Biol 231: 149-163.
33. Li M, Zhao C, Wang Y, Zhao Z, Meng A, (2002) Zebrafish sox9b is an early neural crest marker. Dev Genes Evol 212: 203-206.
34. Yan YL, Willoughby J, Liu D, Crump JG, Wilson C, et al. (2005) A pair of Sox: distinct and overlapping functions of zebrafish sox9 co-orthologs in craniofacial and pectoral fin development. Development 132: 1069-1083.
35. Kim J, Lo L, Dormand E, Anderson DJ, (2003) SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38: 17-31.
36. Kelsh RN, Schmid B, Eisen JS, (2000) Genetic analysis of melanophore development in zebrafish embryos. Dev Biol 225: 277-293.
37. Dutton JR, Antonellis A, Carney TJ, Rodrigues FS, Pavan WJ, et al. (2008) An evolutionarily conserved intronic region controls the spatiotemporal expression of the transcription factor Sox10. BMC Dev Biol 8: 105.
38. Ignatius MS, Moose HE, El-Hodiri HM, Henion PD, (2008) colgate/hdac1 Repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev Biol 313: 568-583.
39. Plaster N, Sonntag C, Schilling TF, Hammerschmidt M, (2007) REREa/Atrophin-2 interacts with histone deacetylase and Fgf8 signaling to regulate multiple processes of zebrafish development. Dev Dyn 236: 1891-1904.
40. Antonellis A, Huynh JL, Lee-Lin SQ, Vinton RM, Renaud G, et al. (2008) Identification of neural crest and glial enhancers at the mouse Sox10 locus through transgenesis in zebrafish. PLoS Genet 4: e1000174 doi:10.1371/journal.pgen.1000174.
41. Werner T, Hammer A, Wahlbuhl M, Bosl MR, Wegner M, (2007) Multiple conserved regulatory elements with overlapping functions determine Sox10 expression in mouse embryogenesis. Nucleic Acids Res 35: 6526-6538.
42. Deal KK, Cantrell VA, Chandler RL, Saunders TL, Mortlock DP, et al. (2006) Distant regulatory elements in a Sox10-beta GEO BAC transgene are required for expression of Sox10 in the enteric nervous system and other neural crest-derived tissues. Dev Dyn 235: 1413-1432.
43. Antonellis A, Bennett WR, Menheniott TR, Prasad AB, Lee-Lin SQ, et al. (2006) Deletion of long-range sequences at Sox10 compromises developmental expression in a mouse model of Waardenburg-Shah (WS4) syndrome. Hum Mol Genet 15: 259-271.
44. Minchin JE, Hughes SM, (2008) Sequential actions of Pax3 and Pax7 drive xanthophore development in zebrafish neural crest. Dev Biol 317: 508-522.
45. Odenthal J, Nusslein-Volhard C, (1998) fork head domain genes in zebrafish. Dev Genes Evol 208: 245-258.
46. Knight RD, Nair S, Nelson SS, Afshar A, Javidan Y, et al. (2003) lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development 130: 5755-5768.
47. Barrallo-Gimeno A, Holzschuh J, Driever W, Knapik EW, (2004) Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 131: 1463-1477.
48. Li W, Cornell RA, (2007) Redundant activities of Tfap2a and Tfap2c are required for neural crest induction and development of other non-neural ectoderm derivatives in zebrafish embryos. Dev Biol 304: 338-354.
49. Lister JA, Close J, Raible DW, (2001) Duplicate mitf genes in zebrafish: complementary expression and conservation of melanogenic potential. Dev Biol 237: 333-344.
50. Saito H, Yasumoto K, Takeda K, Takahashi K, Fukuzaki A, et al. (2002) Melanocyte-specific microphthalmia-associated transcription factor isoform activates its own gene promoter through physical interaction with lymphoid-enhancing factor 1. J Biol Chem 277: 28787-28794.
51. Dutton K, Abbas L, Spencer J, Brannon C, Mowbray C, et al. (2009) A zebrafish model for Waardenburg syndrome type IV reveals diverse roles for Sox10 in the otic vesicle. Dis Model Mech 2: 68-83.
52. Loftus SK, Baxter LL, Buac K, Watkins-Chow DE, Larson DM, et al. (2009) Comparison of melanoblast expression patterns identifies distinct classes of genes. Pigment Cell Melanoma Res 22: 611-622.
53. Hinman VF, Yankura KA, McCauley BS, (2009) Evolution of gene regulatory network architectures: examples of subcircuit conservation and plasticity between classes of echinoderms. Biochim Biophys Acta 1789: 326-332.
54. Motohashi T, Yamanaka K, Chiba K, Aoki H, Kunisada T, (2009) Unexpected Multipotency of Melanoblasts Isolated from Murine Skin. Stem Cells 27: 888-897.
55. Lang D, Lu MM, Huang L, Engleka KA, Zhang M, et al. (2005) Pax3 functions at a nodal point in melanocyte stem cell differentiation. Nature 433: 884-887.
56. Greenhill ER, (2008) Genetic regulation of neural crest cell differentiation Bath University of Bath.
57. Cunliffe VT, (2004) Histone deacetylase 1 is required to repress Notch target gene expression during zebrafish neurogenesis and to maintain the production of motoneurones in response to hedgehog signalling. Development 131: 2983-2995.
58. Cunliffe VT, (2008) Eloquent silence: developmental functions of Class I histone deacetylases. Curr Opin Genet Dev 18: 404-410.
59. Vance KW, Goding CR, (2004) The transcription network regulating melanocyte development and melanoma. Pigment Cell Res 17: 318-325.
60. Price ER, Horstmann MA, Wells AG, Weilbaecher KN, Takemoto CM, et al. (1998) alpha-Melanocyte-stimulating hormone signaling regulates expression of microphthalmia, a gene deficient in Waardenburg syndrome. J Biol Chem 273: 33042-33047.
61. Logan DW, Bryson-Richardson RJ, Pagan KE, Taylor MS, Currie PD, et al. (2003) The structure and evolution of the melanocortin and MCH receptors in fish and mammals. Genomics 81: 184-191.
62. Logan DW, Burn SF, Jackson IJ, (2006) Regulation of pigmentation in zebrafish melanophores. Pigment Cell Res 19: 206-213.
63. Gross JB, Borowsky R, Tabin CJ, (2009) A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet 5: e1000326 doi:10.1371/journal.pgen.1000326.
64. Richardson J, Lundegaard PR, Reynolds NL, Dorin JR, Porteous DJ, et al. (2008) mc1r Pathway regulation of zebrafish melanosome dispersion. Zebrafish 5: 289-295.
65. Carreira S, Goodall J, Denat L, Rodriguez M, Nuciforo P, et al. (2006) Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev 20: 3426-3439.
66. Widlund HR, Horstmann MA, Price ER, Cui J, Lessnick SL, et al. (2002) Beta-catenin-induced melanoma growth requires the downstream target Microphthalmia-associated transcription factor. J Cell Biol 158: 1079-1087.
67. Delmas V, Beermann F, Martinozzi S, Carreira S, Ackermann J, et al. (2007) Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with N-Ras in melanoma development. Genes Dev 21: 2923-2935.
68. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of Embryonic Development of the Zebrafish. Dev Dynamics 203: 253-310.
69. Thisse C, Thisse B, Schilling TF, Postlethwait JH, (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119: 1203-1215.
70. Thisse B, Pfumio S, Fürthauer M, B L, Heyer V, et al. (2001) Expression of the zebrafish genome during embryogenesis. ZFIN online publication.
71. Camp E, Lardelli M, (2001) Tyrosinase gene expression in zebrafish embryos. Dev Genes Evol 211: 150-153.
72. Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL, (2000) An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development 127: 3031-3044.
73. Park HC, Boyce J, Shin J, Appel B, (2005) Oligodendrocyte specification in zebrafish requires notch-regulated cyclin-dependent kinase inhibitor function. J Neurosci 25: 6836-6844.
74. Ungos JM, Karlstrom RO, Raible DW, (2003) Hedgehog signaling is directly required for the development of zebrafish dorsal root ganglia neurons. Development 130: 5351-5362.
75. Matys V, Fricke E, Geffers R, Gossling E, Haubrock M, et al. (2003) TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31: 374-378.
76. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.