Identification of a melanocyte-specific, microphthalmia-associated transcription factor-dependent regulatory element in the intronic duplication causing hair greying and melanoma in horses

Pigment Cell and Melanoma Research

Volumn 25, Issue 1, 2012, Pages 28-36

  Sundström, Elisabeth ^a   Komisarczuk, Anna Z ^b   Jiang, Lin ^c   Golovko, Anna ^c   Navratilova, Pavla ^d   Rinkwitz, Silke ^b   Becker, Thomas S ^b,d   Andersson, Leif ^a,c  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UPPSALA UNIVERSITY   (Sweden)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

Hair greying; Horses; Melanoma; Microphthalmia associated transcription factor; NR4A3; STX17; Zebrafish

Indexed keywords

MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; SYNTAXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CONTROLLED STUDY; EMBRYO; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; HORSE; INTRON; MELANOCYTE; MELANOMA; MELANOPHORE; NEURAL CREST CELL; NONHUMAN; SITE DIRECTED MUTAGENESIS; VITILIGO; ZEBRA FISH;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; ENHANCER ELEMENTS, GENETIC; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DOMINANT; GENES, REPORTER; HAIR COLOR; HORSE DISEASES; HORSES; HUMANS; INTRONS; MAMMALS; MELANOCYTES; MELANOMA; MELANOPHORES; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; NEURAL CREST; PHENOTYPE; QA-SNARE PROTEINS; SKIN NEOPLASMS; SPECIES SPECIFICITY; ZEBRAFISH;

DANIO RERIO; EQUIDAE;

EID: 83955164241     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/j.1755-148X.2011.00902.x     Document Type: Article

References (33)

1. Akalin, A., Fredman, D., Arner, E., Dong, X., Bryne, J.C., Suzuki, H., Daub, C.O., Hayashizaki, Y., and Lenhard, B. (2009). Transcriptional features of genomic regulatory blocks. Genome Biol. 10, R38.
2. Barsh, G., Gunn, T., He, L., Schlossman, S., and Duke-Cohan, J. (2000). Biochemical and genetic studies of pigment-type switching. Pigment Cell Res. 13(Suppl 8), 48-53.
3. Bennett, D.C., Cooper, P.J., and Hart, I.R. (1987). A line of non-tumorigenic mouse melanocytes, syngeneic with the B16 melanoma and requiring a tumour promoter for growth. Int. J. Cancer 39, 414-418.
4. Bentley, N.J., Eisen, T., and Goding, C.R. (1994). Melanocyte-specific expression of the human tyrosinase promoter: activation by the microphthalmia gene product and role of the initiator. Mol. Cell. Biol. 14, 7996-8006.
5. Bertolotto, C., Bille, K., Ortonne, J.P., and Ballotti, R. (1996). Regulation of tyrosinase gene expression by cAMP in B16 melanoma cells involves two CATGTG motifs surrounding the TATA box: implication of the microphthalmia gene product. J. Cell Biol. 134, 747-755.
6. Bertolotto, C., Busca, R., Abbe, P., Bille, K., Aberdam, E., Ortonne, J.P., and Ballotti, R. (1998). Different cis-acting elements are involved in the regulation of TRP1 and TRP2 promoter activities by cyclic AMP: pivotal role of M boxes (GTCATGTGCT) and of microphthalmia. Mol. Cell. Biol. 18, 694-702.
7. D'orazio, J.A., Nobuhisa, T., Cui, R. et al. (2006). Topical drug rescue strategy and skin protection based on the role of Mc1r in UV-induced tanning. Nature 443, 340-344.
8. Engström, P.G., Fredman, D., and Lenhard, B. (2008). Ancora: a web resource for exploring highly conserved noncoding elements and their association with developmental regulatory genes. Genome Biol. 9, R34.
9. Fleury, C., Berard, F., Leblond, A., Faure, C., Ganem, N., and Thomas, L. (2000). The study of cutaneous melanomas in Camargue-type gray-skinned horses (2): epidemiological survey. Pigment Cell Res. 13, 47-51.
10. 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.
11. Hemesath, T.J., Steingrimsson, E., Mcgill, G., Hansen, M.J., Vaught, J., Hodgkinson, C.A., Arnheiter, H., Copeland, N.G., Jenkins, N.A., and Fisher, D.E. (1994). microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev. 8, 2770-2780.
12. 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.
13. Karlsson, E.K., Baranowska, I., Wade, C.M. et al. (2007). Efficient mapping of mendelian traits in dogs through genome-wide association. Nat. Genet. 39, 1321-1328.
14. Kikuta, H., Laplante, M., Navratilova, P. et al. (2007). Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res. 17, 545-555.
15. 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.
16. Komisarczuk, A.Z., Kawakami, K., and Becker, T.S. (2009). Cis-regulation and chromosomal rearrangement of the fgf8 locus after the teleost/tetrapod split. Dev. Biol. 336, 301-312.
17. Lenhard, B., Sandelin, A., Mendoza, L., Engstrom, P., Jareborg, N., and Wasserman, W.W. (2003). Identification of conserved regulatory elements by comparative genome analysis. J. Biol. 2, 13.
18. 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.
19. Maxwell, M.A., and Muscat, G.E. (2006). The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl. Recept. Signal. 4, e002.
20. Murre, C., Mccaw, P.S., and Baltimore, D. (1989a). A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56, 777-783.
21. Murre, C., Mccaw, P.S., Vaessin, H. et al. (1989b). Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537-544.
22. Nasevicius, A., and Ekker, S.C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
23. Navratilova, P., Fredman, D., Hawkins, T.A., Turner, K., Lenhard, B., and Becker, T.S. (2009). Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes. Dev. Biol. 327, 526-540.
24. Nomiyama, T., Nakamachi, T., Gizard, F., Heywood, E.B., Jones, K.L., Ohkura, N., Kawamori, R., Conneely, O.M., and Bruemmer, D. (2006). The NR4A orphan nuclear receptor NOR1 is induced by platelet-derived growth factor and mediates vascular smooth muscle cell proliferation. J. Biol. Chem. 281, 33467-33476.
25. Opdecamp, K., Nakayama, A., Nguyen, M.T., Hodgkinson, C.A., Pavan, W.J., and Arnheiter, H. (1997). Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 124, 2377-2386.
26. Paulsen, R.F., Granas, K., Johnsen, H., Rolseth, V., and Sterri, S. (1995). Three related brain nuclear receptors, NGFI-B, Nurr1, and NOR-1, as transcriptional activators. J. Mol. Neurosci. 6, 249-255.
27. Rosengren Pielberg, G., Golovko, A., Sundstrom, E. et al. (2008). A cis-acting regulatory mutation causes premature hair graying and susceptibility to melanoma in the horse. Nat. Genet. 40, 1004-1009.
28. Smith, A.G., Luk, N., Newton, R.A., Roberts, D.W., Sturm, R.A., and Muscat, G.E. (2008). Melanocortin-1 receptor signaling markedly induces the expression of the NR4A nuclear receptor subgroup in melanocytic cells. J. Biol. Chem. 283, 12564-12570.
29. Sutton, R.H., and Coleman, G.T. (1997). Melanoma and the Graying Horse. In RIRDC Research Paper Series, (Barton, Australia).
30. Tassabehji, M., Newton, V.E., and Read, A.P. (1994). Waardenburg syndrome type 2 caused by mutations in the human microphthalmia (MITF) gene. Nat. Genet. 8, 251-255.
31. Westerfield, M. (2000). The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). (Eugene: University of Oregon Press).
32. Wilson, T.E., Paulsen, R.E., Padgett, K.A., and Milbrandt, J. (1992). Participation of non-zinc finger residues in DNA binding by two nuclear orphan receptors. Science 256, 107-110.
33. Yasumoto, K., Yokoyama, K., Shibata, K., Tomita, Y., and Shibahara, S. (1994). Microphthalmia-associated transcription factor as a regulator for melanocyte-specific transcription of the human tyrosinase gene. Mol. Cell. Biol. 14, 8058-8070.