MITF mutations associated with pigment deficiency syndromes and melanoma have different effects on protein function

Human Molecular Genetics

Volumn 22, Issue 21, 2013, Pages 4357-4367

  Grill, Christine ^a   Bergsteinsdó ttir, Kristín ^a   Ögmundsdó ttir, Margrét H ^a   Pogenberg, Vivian ^b   Schepsky, Alexander ^a   Wilmanns, Matthias ^b   Pingault, Veronique ^c   Steingrímsson, Eiríkur ^a  

^a UNIVERSITY OF ICELAND   (Iceland)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOPACHROME TAUTOMERASE; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; TYROSINASE RELATED PROTEIN 1;

ARTICLE; CELL STRAIN HEK293; CLONOGENESIS; CONTROLLED STUDY; DNA BINDING; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; MELANOMA; PIGMENT DEFICIENCY SYNDROME; PIGMENT DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSCRIPTION INITIATION;

ADOLESCENT; ADULT; ALBINISM, OCULOCUTANEOUS; BINDING SITES; CHILD; CHILD, PRESCHOOL; DEAFNESS; FEMALE; GENETIC VARIATION; HEK293 CELLS; HUMANS; MALE; MELANOMA; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MUTATION, MISSENSE; PROMOTER REGIONS, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; WAARDENBURG SYNDROME; YOUNG ADULT;

EID: 84885783345     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt285     Document Type: Article

References (43)

1. Cheli, Y., Ohanna, M., Ballotti, R. and Bertolotto, C. (2009) Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res., 23, 27-40.
2. Strub, T., Giuliano, S., Ye, T., Bonet, C., Keime, C., Kobi, D., Le Gras, S., Cormont, M., Ballotti, R., Bertolotto, C. et al. (2011) Essential role of microphthalmia transcription factor for DNA replication, mitosis and genomic stability in melanoma. Oncogene, 30, 2319-2332.
3. Steingrimsson, E., Copeland, N.G., and Jenkins, N.A. (2004) Melanocytes and the microphthalmia transcription factor network. Annu. Rev. Genet., 38, 365-411.
4. Hughes, A.E., Newton, V.E., Liu, X.Z., and Read, A.P. (1994) A gene for Waardenburg syndrome type 2 maps close to the human homologue of the microphthalmia gene at chromosome 3p12-p14.1. Nat. Genet., 7, 509-512.
5. Tassabehji, M., Newton, V.E., Liu, X.Z., Brady, A., Donnai, D., Krajewska-Walasek, M., Murday, V., Norman, A., Obersztyn, E., Reardon, W. et al. (1995) The mutational spectrum in Waardenburg syndrome. Hum. Mol. Genet., 4, 2131-2137.
6. Waardenburg, P.J. (1951) A new syndrome combining developmental anomalies of the eyelids, eyebrows and nose root with pigmentary defects of the iris and head hair and with congenital deafness. Am. J. Hum. Genet., 3, 195-253.
7. Tietz, W. (1963) A syndrome of deaf-mutism associated with albinism showing dominant autosomal inheritance. Am. J. Hum. Genet., 15, 259-264.
8. Read, A.P., and Newton, V.E. (1997) Waardenburg syndrome. J. Med. Genet., 34, 656-665.
9. Pingault, V., Ente, D., Dastot-Le Moal, F., Goossens, M., Marlin, S., and Bondurand, N. (2010) Review and update of mutations causing Waardenburg syndrome. Hum. Mutat., 31, 391-406.
10. Smith, S.D., Kelley, P.M., Kenyon, J.B., and Hoover, D. (2000) Tietz syndrome (hypopigmentation/deafness) caused by mutation of MITF. J. Med. Genet., 37, 446-448.
11. Shigemura, T., Shiohara, M., Tanaka, M., Takeuchi, K., and Koike, K. (2010) Effect of the mutant microphthalmia-associated transcription factor found in Tietz syndrome on the in vitro development of mast cells. J. Pediatr. Hematol. Oncol., 32, 442-447.
12. Leger, S., Balguerie, X., Goldenberg, A., Drouin-Garraud, V., Cabot, A., Amstutz-Montadert, I., Young, P., Joly, P., Bodereau, V., Holder-Espinasse, M. et al. (2012) Novel and recurrent non-truncating mutations of the MITF basic domain: genotypic and phenotypic variations in Waardenburg and Tietz syndromes. Eur. J. Hum. Genet., 20, 584-587.
13. King, R., Weilbaecher, K.N., McGill, G., Cooley, E., Mihm, M., and Fisher, D.E. (1999) Microphthalmia transcription factor. A sensitive and specific melanocyte marker for MelanomaDiagnosis. Am. J. Pathol., 155, 731-738.
14. King, R., Googe, P.B., Weilbaecher, K.N., Mihm, M.C. Jr and Fisher, D.E. (2001) Microphthalmia transcription factor expression in cutaneous benign, malignant melanocytic, and nonmelanocytic tumors. Am. J. Surg. Pathol., 25, 51-57.
15. Garraway, L.A., Widlund, H.R., Rubin, M.A., Getz, G., Berger, A.J., Ramaswamy, S., Beroukhim, R., Milner, D.A., Granter, S.R., Du, J. et al. (2005) Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature, 436, 117-122.
16. Cronin, J.C., Wunderlich, J., Loftus, S.K., Prickett, T.D., Wei, X., Ridd, K., Vemula, S., Burrell, A.S., Agrawal, N.S., Lin, J.C. et al. (2009) Frequent mutations in the MITF pathway in melanoma. Pigment Cell Melanoma Res., 22, 435-444.
17. Bertolotto, C., Lesueur, F., Giuliano, S., Strub, T., de Lichy, M., Bille, K., Dessen, P., d'Hayer, B., Mohamdi, H., Remenieras, A. et al. (2011) A SUMOylation-defective MITF germline mutation predisposes to melanoma and renal carcinoma. Nature, 480, 94-98.
18. Yokoyama, S., Woods, S.L., Boyle, G.M., Aoude, L.G., Macgregor, S., Zismann, V., Gartside, M., Cust, A.E., Haq, R., Harland, M. et al. (2011) A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature, 480, 99-103.
19. Garraway, L.A., and Sellers, W.R. (2006) Lineage dependency and lineage-survival oncogenes in human cancer. Nat. Rev. Cancer, 6, 593-602.
20. Pogenberg, V., Ogmundsdottir, M.H., Bergsteinsdottir, K., Schepsky, A., Phung, B., Deineko, V., Milewski, M., Steingrimsson, E., and Wilmanns, M. (2012) Restricted leucine zipper dimerization and specificity of DNA recognition of the melanocyte master regulator MITF. Genes Dev., 26, 2647-2658.
21. Leger, S., Balguerie, X., Goldenberg, A., Drouin-Garraud, V., Cabot, A., Amstutz-Montadert, I., Young, P., Joly, P., Bodereau, V., Holder-Espinasse, M. et al. (2012) Novel and recurrent non-truncating mutations of the MITF basic domain: genotypic and phenotypic variations in Waardenburg and Tietz syndromes. Eur. J. Hum. Genet, 20, 584-587.
22. 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.
23. Murakami, H., and Arnheiter, H. (2005) Sumoylation modulates transcriptional activity ofMITFin a promoter-specific manner. Pigment Cell Res., 18, 265-277.
24. Lowings, P., Yavuzer, U., and Goding, C.R. (1992) Positive and negative elements regulate a melanocyte-specific promoter. Mol. Cell Biol., 12, 3653-3662.
25. Bottaro, D.P., Rubin, J.S., Faletto, D.L., Chan, A.M., Kmiecik, T.E., Vande Woude, G.F., and Aaronson, S.A. (1991) Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science, 251, 802-804.
26. Schmidt, L., Duh, F.M., Chen, F., Kishida, T., Glenn, G., Choyke, P., Scherer, S.W., Zhuang, Z., Lubensky, I., Dean, M.et al. (1997) Germline and somatic mutations in the tyrosine kinase domain of theMETproto-oncogene in papillary renal carcinomas. Nat. Genet., 16, 68-73.
27. Natali, P.G., Nicotra, M.R., Di Renzo, M.F., Prat, M., Bigotti, A., Cavaliere, R., and Comoglio, P.M. (1993) Expression of the c-Met/HGF receptor in human melanocytic neoplasms: demonstration of the relationship to malignant melanoma tumour progression. Br. J. Cancer, 68, 746-750.
28. Strub, T., Giuliano, S., Ye, T., Bonet, C., Keime, C., Kobi, D., Le Gras, S., Cormont, M., Ballotti, R., Bertolotto, C. et al. (2011) Essential role of microphthalmia transcription factor for DNA replication, mitosis and genomic stability in melanoma. Oncogene, 30, 2319-2332.
29. Bharti, K., Liu, W., Csermely, T., Bertuzzi, S., and Arnheiter, H. (2008) Alternative promoter use in eye development: the complex role and regulation of the transcription factor MITF. Development, 135, 1169-1178.
30. Takebayashi, K., Chida, K., Tsukamoto, I., Morii, E., Munakata, H., Arnheiter, H., Kuroki, T., Kitamura, Y., and Nomura, S. (1996) The recessive phenotype displayed by a dominant negative microphthalmia-associated transcription factor mutant is a result of impaired nucleation potential. Mol. Cell Biol., 16, 1203-1211.
31. Zhang, H., Luo, H., Chen, H., Mei, L., He, C., Jiang, L., Li, J.D., and Feng, Y. (2012) Functional analysis of MITF gene mutations associated with Waardenburg syndrome type 2. FEBS Lett, 586, 4126-4131.
32. Hauswirth, R., Haase, B., Blatter, M., Brooks, S.A., Burger, D., Drogemuller, C., Gerber, V., Henke, D., Janda, J., Jude, R. et al. (2012) Mutations in MITF and PAX3 cause 'splashed white' and other white spotting phenotypes in horses. PLoS Genet., 8, e1002653.
33. Takeda, K., Takemoto, C., Kobayashi, I., Watanabe, A., Nobukuni, Y., Fisher, D.E., and Tachibana, M. (2000) Ser298 of MITF, a mutation site in Waardenburg syndrome type 2, is a phosphorylation site with functional significance. Hum. Mol. Genet., 9, 125-132.
34. Fiol, C.J., Wang, A., Roeske, R.W., and Roach, P.J. (1990) Ordered multisite protein phosphorylation. Analysis of glycogen synthase kinase 3 action using model peptide substrates. J. Biol. Chem., 265, 6061-6065.
35. Wang, Q.M., Park, I.K., Fiol, C.J., Roach, P.J., and DePaoli-Roach, A.A. (1994) Isoform differences in substrate recognition by glycogen synthase kinases 3 alpha and 3 beta in the phosphorylation of phosphatase inhibitor 2. Biochemistry, 33, 143-147.
36. Frame, S., and Cohen, P. (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem. J., 359, 1-16.
37. Sato, S., Roberts, K., Gambino, G., Cook, A., Kouzarides, T., and Goding, C.R. (1997) CBP/p300 as a co-factor for the microphthalmia transcription factor. Oncogene, 14, 3083-3092.
38. Vachtenheim, J., and Drdova, B. (2004) A dominant negative mutant of microphthalmia transcription factor (MITF) lacking two transactivation domains suppresses transcription mediated by wild type MITF and a hyperactive MITF derivative. Pigment Cell Res., 17, 43-50.
39. Beuret, L., Flori, E., Denoyelle, C., Bille, K., Busca, R., Picardo, M., Bertolotto, C., and Ballotti, R. (2007) Up-regulation of MET expression by alpha-melanocyte-stimulating hormone and MITF allows hepatocyte growth factor to protect melanocytes and melanoma cells from apoptosis. J. Biol. Chem., 282, 14140-14147.
40. Nobukuni, Y., Watanabe, A., Takeda, K., Skarka, H., and Tachibana, M. (1996) Analyses of loss-of-function mutations of the MITF gene suggest that haploinsufficiency is a cause of Waardenburg syndrome type 2A. Am. J. Hum. Genet., 59, 76-83.
41. Chen, H., Jiang, L., Xie, Z., Mei, L., He, C., Hu, Z., Xia, K., and Feng, Y. (2010) Novel mutations of PAX3, MITF, and SOX10 genes in Chinese patients with type I or type II Waardenburg syndrome. Biochem. Biophys. Res. Commun., 397, 70-74.
42. Lalwani, A.K., Attaie, A., Randolph, F.T., Deshmukh, D., Wang, C., Mhatre, A., and Wilcox, E. (1998) Point mutation in the MITF gene causing Waardenburg syndrome type II in a three-generation Indian family. Am. J. Med. Genet., 80, 406-409.
43. Welch, K.O., Smith, S.D., Hoover, D., Arnos, K.S., Kelley, P.M., and Pandya, A. (2002) A variant of Tietz syndrome caused by a mutation in the basic domain of the MITF gene. 2002 ASHG Annual Meeting, Baltimore, MD, USA.