Microphthalmia-associated transcription factor in melanoma development and MAP-kinase pathway targeted therapy

Pigment Cell and Melanoma Research

Volumn 28, Issue 4, 2015, Pages 390-406

  Wellbrock, Claudia ^a   Arozarena, Imanol ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

BRAF; MAP kinase pathway; MEK; Melanoma; Microphthalmia associated transcription factor

Indexed keywords

B RAF KINASE; B RAF KINASE INHIBITOR; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL INVASION; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; GENE AMPLIFICATION; GENE CONTROL; GENE EXPRESSION; HUMAN; INTRACELLULAR SIGNALING; MELANOGENESIS; MELANOMA; MELANOMA CELL; MELANOMA METASTASIS; MOLECULARLY TARGETED THERAPY; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN ACETYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSCRIPTION INITIATION; TUMOR MICROENVIRONMENT; UBIQUITINATION; ANIMAL; CELL CYCLE; ENZYMOLOGY; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; CARCINOGENESIS; CELL CYCLE; HUMANS; MAP KINASE SIGNALING SYSTEM; MELANOMA; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MOLECULAR TARGETED THERAPY;

EID: 84930925982     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12370     Document Type: Article

References (155)

1. Abel, E.V., Basile, K.J., Kugel, C.H. 3rd et al. (2013). Melanoma adapts to RAF/MEK inhibitors through FOXD3-mediated upregulation of ERBB3. J. Clin. Invest. 123, 2155-2168.
2. Anastas, J.N., Kulikauskas, R.M., Tamir, T. et al. (2014). WNT5A enhances resistance of melanoma cells to targeted BRAF inhibitors. J. Clin. Invest. 124, 2877-2890.
3. Arnheiter, H. (2010). The discovery of the microphthalmia locus and its gene, Mitf. Pigment Cell Melanoma Res. 23, 729-735.
4. Arozarena, I., Bischof, H., Gilby, D., Belloni, B., Dummer, R., and Wellbrock, C. (2011a). In melanoma, beta-catenin is a suppressor of invasion. Oncogene 30, 4531-4543.
5. Arozarena, I., Sanchez-Laorden, B., Packer, L., Hidalgo-Carcedo, C., Hayward, R., Viros, A., Sahai, E., and Marais, R. (2011b). Oncogenic BRAF induces melanoma cell invasion by downregulating the cGMP-specific phosphodiesterase PDE5A. Cancer Cell 19, 45-57.
6. Basile, K.J., Abel, E.V., and Aplin, A.E. (2012). Adaptive upregulation of FOXD3 and resistance to PLX4032/4720-induced cell death in mutant B-RAF melanoma cells. Oncogene 31, 2471-2479.
7. Bauer, G.L., Praetorius, C., Bergsteinsdottir, K. et al. (2009). The role of MITF phosphorylation sites during coat color and eye development in mice analyzed by bacterial artificial chromosome transgene rescue. Genetics 183, 581-594.
8. Bell, R.E., and Levy, C. (2011). The three M's: melanoma, microphthalmia-associated transcription factor and microRNA. Pigment Cell Melanoma Res. 24, 1088-1106.
9. Bemis, L.T., Chen, R., Amato, C.M., Classen, E.H., Robinson, S.E., Coffey, D.G., Erickson, P.F., Shellman, Y.G., and Robinson, W.A. (2008). MicroRNA-137 targets microphthalmia-associated transcription factor in melanoma cell lines. Cancer Res. 68, 1362-1368.
10. 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.
11. Bertolotto, C., Abbe, P., Hemesath, T.J., Bille, K., Fisher, D.E., Ortonne, J.P., and Ballotti, R. (1998a). Microphthalmia gene product as a signal transducer in cAMP-induced differentiation of melanocytes. J. Cell Biol. 142, 827-835.
12. Bertolotto, C., Busca, R., Abbe, P., Bille, K., Aberdam, E., Ortonne, J.P., and Ballotti, R. (1998b). 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.
13. Bertolotto, C., Lesueur, F., Giuliano, S. et al. (2011). A SUMOylation-defective MITF germline mutation predisposes to melanoma and renal carcinoma. Nature 480, 94-98.
14. 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.
15. Beuret, L., Ohanna, M., Strub, T., Allegra, M., Davidson, I., Bertolotto, C., and Ballotti, R. (2011). BRCA1 is a new MITF target gene. Pigment Cell Melanoma Res. 24, 725-727.
16. Bismuth, K., Skuntz, S., Hallsson, J.H., Pak, E., Dutra, A.S., Steingrimsson, E., and Arnheiter, H. (2008). An unstable targeted allele of the mouse Mitf gene with a high somatic and germline reversion rate. Genetics 178, 259-272.
17. Bohm, M., Moellmann, G., Cheng, E., Alvarez-Franco, M., Wagner, S., Sassone-Corsi, P., and Halaban, R. (1995). Identification of p90RSK as the probable CREB-Ser133 kinase in human melanocytes. Cell Growth Differ. 6, 291-302.
18. Bondurand, N., Pingault, V., Goerich, D.E., Lemort, N., Sock, E., Le Caignec, C., Wegner, M., and Goossens, M. (2000). Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum. Mol. Genet. 9, 1907-1917.
19. Boyle, G.M., Woods, S.L., Bonazzi, V.F., Stark, M.S., Hacker, E., Aoude, L.G., Dutton-Regester, K., Cook, A.L., Sturm, R.A., and Hayward, N.K. (2011). Melanoma cell invasiveness is regulated by miR-211 suppression of the BRN2 transcription factor. Pigment Cell Melanoma Res. 24, 525-537.
20. Bronisz, A., Carey, H.A., Godlewski, J., Sif, S., Ostrowski, M.C., and Sharma, S.M. (2014). The multifunctional protein fused in sarcoma (FUS) is a coactivator of microphthalmia-associated transcription factor (MITF). J. Biol. Chem. 289, 326-334.
21. Busca, R., and Ballotti, R. (2000). Cyclic AMP a key messenger in the regulation of skin pigmentation. Pigment Cell Res. 13, 60-69.
22. Busca, R., Abbe, P., Mantoux, F., Aberdam, E., Peyssonnaux, C., Eychene, A., Ortonne, J.P., and Ballotti, R. (2000). Ras mediates the cAMP-dependent activation of extracellular signal-regulated kinases (ERKs) in melanocytes. EMBO J. 19, 2900-2910.
23. Cantin, G.T., Yi, W., Lu, B., Park, S.K., Xu, T., Lee, J.D., and Yates, J.R. 3rd (2008). Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteomic analysis. J. Proteome Res. 7, 1346-1351.
24. Carreira, S., Goodall, J., Aksan, I., La Rocca, S.A., Galibert, M.D., Denat, L., Larue, L., and Goding, C.R. (2005). Mitf cooperates with Rb1 and activates p21Cip1 expression to regulate cell cycle progression. Nature 433, 764-769.
25. Carreira, S., Goodall, J., Denat, L., Rodriguez, M., Nuciforo, P., Hoek, K.S., Testori, A., Larue, L., and Goding, C.R. (2006). Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev. 20, 3426-3439.
26. Chapman, A., Fernandez Del Ama, L., Ferguson, J., Kamarashev, J., Wellbrock, C., and Hurlstone, A. (2014). Heterogeneous tumor subpopulations cooperate to drive invasion. Cell Rep. 8, 688-695.
27. Cheli, Y., Ohanna, M., Ballotti, R., and Bertolotto, C. (2010). Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res. 23, 27-40.
28. Cheli, Y., Giuliano, S., Botton, T., Rocchi, S., Hofman, V., Hofman, P., Bahadoran, P., Bertolotto, C., and Ballotti, R. (2011). Mitf is the key molecular switch between mouse or human melanoma initiating cells and their differentiated progeny. Oncogene 30, 2307-2318.
29. Cheli, Y., Giuliano, S., Fenouille, N. et al. (2012). Hypoxia and MITF control metastatic behaviour in mouse and human melanoma cells. Oncogene 31, 2461-2470.
30. Chien, A.J., Moore, E.C., Lonsdorf, A.S., Kulikauskas, R.M., Rothberg, B.G., Berger, A.J., Major, M.B., Hwang, S.T., Rimm, D.L., and Moon, R.T. (2009). Activated Wnt/beta-catenin signaling in melanoma is associated with decreased proliferation in patient tumors and a murine melanoma model. Proc. Natl. Acad. Sci. USA 106, 1193-1198.
31. Cook, A.L., Smith, A.G., Smit, D.J., Leonard, J.H., and Sturm, R.A. (2005). Co-expression of SOX9 and SOX10 during melanocytic differentiation in vitro. Exp. Cell Res. 308, 222-235.
32. Damsky, W.E., Curley, D.P., Santhanakrishnan, M. et al. (2011). beta-catenin signaling controls metastasis in Braf-activated Pten-deficient melanomas. Cancer Cell 20, 741-754.
33. De La Serna, I.L., Ohkawa, Y., Higashi, C., Dutta, C., Osias, J., Kommajosyula, N., Tachibana, T., and Imbalzano, A.N. (2006). The microphthalmia-associated transcription factor requires SWI/SNF enzymes to activate melanocyte-specific genes. J. Biol. Chem. 281, 20233-20241.
34. Delmas, V., Beermann, F., Martinozzi, S. 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.
35. Dissanayake, S.K., Olkhanud, P.B., O'connell, M.P. et al. (2008). Wnt5A regulates expression of tumor-associated antigens in melanoma via changes in signal transducers and activators of transcription 3 phosphorylation. Cancer Res. 68, 10205-10214.
36. Diwakar, G., Zhang, D., Jiang, S., and Hornyak, T.J. (2008). Neurofibromin as a regulator of melanocyte development and differentiation. J. Cell Sci. 121, 167-177.
37. Dorsky, R.I., Raible, D.W., and Moon, R.T. (2000). Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev. 14, 158-162.
38. Du, J., Widlund, H.R., Horstmann, M.A., Ramaswamy, S., Ross, K., Huber, W.E., Nishimura, E.K., Golub, T.R., and Fisher, D.E. (2004). Critical role of CDK2 for melanoma growth linked to its melanocyte-specific transcriptional regulation by MITF. Cancer Cell 6, 565-576.
39. Eichhoff, O.M., Weeraratna, A., Zipser, M.C. et al. (2011). Differential LEF1 and TCF4 expression is involved in melanoma cell phenotype switching. Pigment Cell Melanoma Res. 24, 631-642.
40. Ennen, M., Keime, C., Kobi, D., Mengus, G., Lipsker, D., Thibault-Carpentier, C., and Davidson, I. (2014). Single-cell gene expression signatures reveal melanoma cell heterogeneity. Oncogene doi: 10.1038/onc.2014.262. [Epub ahead of print].
41. Feige, E., Yokoyama, S., Levy, C. et al. (2011). Hypoxia-induced transcriptional repression of the melanoma-associated oncogene MITF. Proc. Natl. Acad. Sci. USA 108, E924-E933.
42. Frederick, D.T., Piris, A., Cogdill, A.P. et al. (2013). BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin. Cancer Res. 19, 1225-1231.
43. Gallagher, S.J., Rambow, F., Kumasaka, M., Champeval, D., Bellacosa, A., Delmas, V., and Larue, L. (2013). Beta-catenin inhibits melanocyte migration but induces melanoma metastasis. Oncogene 32, 2230-2238.
44. Garraway, L.A., Widlund, H.R., Rubin, M.A. et al. (2005). Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436, 117-122.
45. Giuliano, S., Cheli, Y., Ohanna, M. et al. (2010). Microphthalmia-associated transcription factor controls the DNA damage response and a lineage-specific senescence program in melanomas. Cancer Res. 70, 3813-3822.
46. Goodall, J., Martinozzi, S., Dexter, T.J., Champeval, D., Carreira, S., Larue, L., and Goding, C.R. (2004a). Brn-2 expression controls melanoma proliferation and is directly regulated by beta-catenin. Mol. Cell. Biol. 24, 2915-2922.
47. Goodall, J., Wellbrock, C., Dexter, T.J., Roberts, K., Marais, R., and Goding, C.R. (2004b). The Brn-2 transcription factor links activated BRAF to melanoma proliferation. Mol. Cell. Biol. 24, 2923-2931.
48. Goodall, J., Carreira, S., Denat, L., Kobi, D., Davidson, I., Nuciforo, P., Sturm, R.A., Larue, L., and Goding, C.R. (2008). Brn-2 represses microphthalmia-associated transcription factor expression and marks a distinct subpopulation of microphthalmia-associated transcription factor-negative melanoma cells. Cancer Res. 68, 7788-7794.
49. Gopal, Y.N., Rizos, H., Chen, G., et al. (2014). Inhibition of mTORC1/2 overcomes resistance to MAPK pathway inhibitors mediated by PGC1α and oxidative p hosphorylation in melanoma. Cancer Res. 74, 7037-7047.
50. Gray-Schopfer, V., Wellbrock, C., and Marais, R. (2007). Melanoma biology and new targeted therapy. Nature 445, 851-857.
51. Grill, C., Bergsteinsdóttir, K., Ogmundsdóttir, M.H., Pogenberg, V., Schepsky, A., Wilmanns, M., Pingault, V., and Steingrímsson, E. (2013). MITF mutations associated with pigment deficiency syndromes and melanoma have different effects on protein function. Hum Mol Genet. 22, 4357-4367.
52. Haass, N.K., Beaumont, K.A., Hill, D.S., Anfosso, A., Mrass, P., Munoz, M.A., Kinjyo, I., and Weninger, W. (2014). Real-time cell cycle imaging during melanoma growth, invasion, and drug response. Pigment Cell Melanoma Res. 27, 764-776.
53. Haflidadottir, B.S., Bergsteinsdottir, K., Praetorius, C., and Steingrimsson, E. (2010). miR-148 regulates Mitf in melanoma cells. PLoS ONE 5, e11574.
54. Hanna, L.A., Foreman, R.K., Tarasenko, I.A., Kessler, D.S., and Labosky, P.A. (2002). Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev. 16, 2650-2661.
55. Haq, R., Shoag, J., Andreu-Perez, P. et al. (2013a). Oncogenic BRAF regulates oxidative metabolism via PGC1alpha and MITF. Cancer Cell 23, 302-315.
56. Haq, R., Yokoyama, S., Hawryluk, E.B. et al. (2013b). BCL2A1 is a lineage-specific antiapoptotic melanoma oncogene that confers resistance to BRAF inhibition. Proc. Natl. Acad. Sci. USA 110, 4321-4326.
57. Hemesath, T.J., Price, E.R., Takemoto, C., Badalian, T., and Fisher, D.E. (1998). MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes. Nature 391, 298-301.
58. 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.
59. Hoek, K.S., and Goding, C.R. (2010). Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res. 23, 746-759.
60. Hoek, K.S., Schlegel, N.C., Brafford, P. et al. (2006). Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res. 19, 290-302.
61. Hoek, K.S., Eichhoff, O.M., Schlegel, N.C., Dobbeling, U., Kobert, N., Schaerer, L., Hemmi, S., and Dummer, R. (2008). In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res. 68, 650-656.
62. Hou, J.M., Krebs, M., Ward, T., Sloane, R., Priest, L., Hughes, A., Clack, G., Ranson, M., Blackhall, F., and Dive, C. (2011). Circulating tumor cells as a window on metastasis biology in lung cancer. Am. J. Pathol. 178, 989-996.
63. Houben, R., Vetter-Kauczok, C.S., Ortmann, S., Rapp, U.R., Broecker, E.B., and Becker, J.C. (2008). Phospho-ERK staining is a poor indicator of the mutational status of BRAF and NRAS in human melanoma. J. Invest. Dermatol. 128, 2003-2012.
64. Huber, W.E., Price, E.R., Widlund, H.R., Du, J., Davis, I.J., Wegner, M., and Fisher, D.E. (2003). A tissue-restricted cAMP transcriptional response: SOX10 modulates alpha-melanocyte-stimulating hormone-triggered expression of microphthalmia-associated transcription factor in melanocytes. J. Biol. Chem. 278, 45224-45230.
65. Javelaud, D., Alexaki, V.I., Pierrat, M.J. et al. (2011). GLI2 and M-MITF transcription factors control exclusive gene expression programs and inversely regulate invasion in human melanoma cells. Pigment Cell Melanoma Res. 24, 932-943.
66. Johannessen, C.M., Johnson, L.A., Piccioni, F. et al. (2013). A melanocyte lineage program confers resistance to MAP kinase pathway inhibition. Nature 504, 138-142.
67. Khoja, L., Shenjere, P., Hodgson, C., Hodgetts, J., Clack, G., Hughes, A., Lorigan, P., and Dive, C. (2014). Prevalence and heterogeneity of circulating tumour cells in metastatic cutaneous melanoma. Melanoma Res. 24, 40-46.
68. 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.
69. Konieczkowski, D.J., Johannessen, C.M., Abudayyeh, O. et al. (2014). A melanoma cell state distinction influences sensitivity to MAPK pathway inhibitors. Cancer Discov. 4, 816-827.
70. Kono, M., Dunn, I.S., Durda, P.J., Butera, D., Rose, L.B., Haggerty, T.J., Benson, E.M., and Kurnick, J.T. (2006). Role of the mitogen-activated protein kinase signaling pathway in the regulation of human melanocytic antigen expression. Mol. Cancer Res. 4, 779-792.
71. Kubic, J.D., Young, K.P., Plummer, R.S., Ludvik, A.E., and Lang, D. (2008). Pigmentation PAX-ways: the role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res. 21, 627-645.
72. Kubic, J.D., Mascarenhas, J.B., Iizuka, T., Wolfgeher, D., and Lang, D. (2012). GSK-3 promotes cell survival, growth, and PAX3 levels in human melanoma cells. Mol. Cancer Res. 10, 1065-1076.
73. Landsberg, J., Kohlmeyer, J., Renn, M. et al. (2012). Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation. Nature 490, 412-416.
74. Lauss, M., Haq, R., Cirenajwis, H. et al. (2015). Genome-wide DNA methylation analysis in melanoma reveals the importance of CpG methylation in MITF regulation. J. Invest. Dermatol. doi: 10.1038/jid.2015.61. [Epub ahead of print].
75. Lee, M., Goodall, J., Verastegui, C., Ballotti, R., and Goding, C.R. (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.
76. Levy, C., Sonnenblick, A., and Razin, E. (2003). Role played by microphthalmia transcription factor phosphorylation and its Zip domain in its transcriptional inhibition by PIAS3. Mol. Cell. Biol. 23, 9073-9080.
77. Levy, C., Khaled, M., and Fisher, D.E. (2006). MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med. 12, 406-414.
78. Levy, C., Khaled, M., Iliopoulos, D. et al. (2010). Intronic miR-211 assumes the tumor suppressive function of its host gene in melanoma. Mol. Cell 40, 841-849.
79. Li, X.H., Kishore, A.H., Dao, D., Zheng, W., Roman, C.A., and Word, R.A. (2010). A novel isoform of microphthalmia-associated transcription factor inhibits IL-8 gene expression in human cervical stromal cells. Mol. Endocrinol. 24, 1512-1528.
80. Li, W.Q., Qureshi, A.A., Robinson, K.C., and Han, J. (2014). Sildenafil use and increased risk of incident melanoma in US men: a prospective cohort study. JAMA Intern. Med. 174, 964-970.
81. Lister, J.A., Capper, A., Zeng, Z., Mathers, M.E., Richardson, J., Paranthaman, K., Jackson, I.J., and Patton, E.E. (2014). A conditional zebrafish MITF mutation reveals MITF levels are critical for melanoma promotion vs. regression in vivo. J. Invest. Dermatol. 134, 133-140.
82. Loercher, A.E., Tank, E.M., Delston, R.B., and Harbour, J.W. (2005). MITF links differentiation with cell cycle arrest in melanocytes by transcriptional activation of INK4A. J. Cell Biol. 168, 35-40.
83. Lowings, P., Yavuzer, U., and Goding, C.R. (1992). Positive and negative elements regulate a melanocyte-specific promoter. Mol. Cell. Biol. 12, 3653-3662.
84. Mansky, K.C., Sankar, U., Han, J., and Ostrowski, M.C. (2002). Microphthalmia transcription factor is a target of the p38 MAPK pathway in response to receptor activator of NF-kappa B ligand signaling. J. Biol. Chem. 277, 11077-11083.
85. Marquette, A., Andre, J., Bagot, M., Bensussan, A., and Dumaz, N. (2011). ERK and PDE4 cooperate to induce RAF isoform switching in melanoma. Nat. Struct. Mol. Biol. 18, 584-591.
86. Marshall, C.J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
87. Mazar, J., Deyoung, K., Khaitan, D., Meister, E., Almodovar, A., Goydos, J., Ray, A., and Perera, R.J. (2010). The regulation of miRNA-211 expression and its role in melanoma cell invasiveness. PLoS ONE 5, e13779.
88. Mcgill, G.G., Horstmann, M., Widlund, H.R. et al. (2002). Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109, 707-718.
89. Mcgill, G.G., Haq, R., Nishimura, E.K., and Fisher, D.E. (2006). c-Met expression is regulated by Mitf in the melanocyte lineage. J. Biol. Chem. 281, 10365-10373.
90. Miller, A.J., Levy, C., Davis, I.J., Razin, E., and Fisher, D.E. (2005). Sumoylation of MITF and its related family members TFE3 and TFEB. J. Biol. Chem. 280, 146-155.
91. Molina, D.M., Grewal, S., and Bardwell, L. (2005). Characterization of an ERK-binding domain in microphthalmia-associated transcription factor and differential inhibition of ERK2-mediated substrate phosphorylation. J. Biol. Chem. 280, 42051-42060.
92. Muller, J., Krijgsman, O., Tsoi, J. et al. (2014). Low MITF/AXL ratio predicts early resistance to multiple targeted drugs in melanoma. Nat. Commun. 5, 5712.
93. Murakami, H., and Arnheiter, H. (2005). Sumoylation modulates transcriptional activity of MITF in a promoter-specific manner. Pigment Cell Res. 18, 265-277.
94. Nakai, N., Kishida, T., Shin-Ya, M., Imanishi, J., Ueda, Y., Kishimoto, S., and Mazda, O. (2007). Therapeutic RNA interference of malignant melanoma by electrotransfer of small interfering RNA targeting Mitf. Gene Ther. 14, 357-365.
95. Nishimura, E.K., Suzuki, M., Igras, V., Du, J., Lonning, S., Miyachi, Y., Roes, J., Beermann, F., and Fisher, D.E. (2010). Key roles for transforming growth factor beta in melanocyte stem cell maintenance. Cell Stem Cell 6, 130-140.
96. O'connell, M.P., Marchbank, K., Webster, M.R. et al. (2013). Hypoxia induces phenotypic plasticity and therapy resistance in melanoma via the tyrosine kinase receptors ROR1 and ROR2. Cancer Discov. 3, 1378-1393.
97. Olsen, J.V., Vermeulen, M., Santamaria, A. et al. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3.
98. 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.
99. Passeron, T., Valencia, J.C., Namiki, T., Vieira, W.D., Passeron, H., Miyamura, Y., and Hearing, V.J. (2009). Upregulation of SOX9 inhibits the growth of human and mouse melanomas and restores their sensitivity to retinoic acid. J. Clin. Invest. 119, 954-963.
100. Patton, E.E., Widlund, H.R., Kutok, J.L. et al. (2005). BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr. Biol. 15, 249-254.
101. Pierrat, M.J., Marsaud, V., Mauviel, A., and Javelaud, D. (2012). Expression of microphthalmia-associated transcription factor (MITF), which is critical for melanoma progression, is inhibited by both transcription factor GLI2 and transforming growth factor-beta. J. Biol. Chem. 287, 17996-18004.
102. Pinner, S., Jordan, P., Sharrock, K., Bazley, L., Collinson, L., Marais, R., Bonvin, E., Goding, C., and Sahai, E. (2009). Intravital imaging reveals transient changes in pigment production and Brn2 expression during metastatic melanoma dissemination. Cancer Res. 69, 7969-7977.
103. Ploper, D., Taelman, V.F., Robert, L., Perez, B.S., Titz, B., Chen, H.W., Graeber, T.G., Von Euw, E., Ribas, A., and De Robertis, E.M. (2015). MITF drives endolysosomal biogenesis and potentiates Wnt signaling in melanoma cells. Proc. Natl. Acad. Sci. USA 112, E420-E429.
104. 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.
105. 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.
106. Price, E.R., Ding, H.F., Badalian, T., Bhattacharya, S., Takemoto, C., Yao, T.P., Hemesath, T.J., and Fisher, D.E. (1998a). Lineage-specific signaling in melanocytes. C-kit stimulation recruits p300/CBP to microphthalmia. J. Biol. Chem. 273, 17983-17986.
107. Price, E.R., Horstmann, M.A., Wells, A.G., Weilbaecher, K.N., Takemoto, C.M., Landis, M.W., and Fisher, D.E. (1998b). alpha-Melanocyte-stimulating hormone signaling regulates expression of microphthalmia, a gene deficient in Waardenburg syndrome. J. Biol. Chem. 273, 33042-33047.
108. Salama, A.K., and Flaherty, K.T. (2013). BRAF in melanoma: current strategies and future directions. Clin. Cancer Res. 19, 4326-4334.
109. Salti, G.I., Manougian, T., Farolan, M., Shilkaitis, A., Majumdar, D., and Das Gupta, T.K. (2000). Micropthalmia transcription factor: a new prognostic marker in intermediate-thickness cutaneous malignant melanoma. Cancer Res. 60, 5012-5016.
110. 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.
111. Sato-Jin, K., Nishimura, E.K., Akasaka, E. et al. (2008). Epistatic connections between microphthalmia-associated transcription factor and endothelin signaling in Waardenburg syndrome and other pigmentary disorders. FASEB J. 22, 1155-1168.
112. Schepsky, A., Bruser, K., Gunnarsson, G.J., Goodall, J., Hallsson, J.H., Goding, C.R., Steingrimsson, E., and Hecht, A. (2006). The microphthalmia-associated transcription factor Mitf interacts with beta-catenin to determine target gene expression. Mol. Cell. Biol. 26, 8914-8927.
113. Scholl, F.A., Kamarashev, J., Murmann, O.V., Geertsen, R., Dummer, R., and Schafer, B.W. (2001). PAX3 is expressed in human melanomas and contributes to tumor cell survival. Cancer Res. 61, 823-826.
114. Segura, M.F., Hanniford, D., Menendez, S. et al. (2009). Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc. Natl. Acad. Sci. USA 106, 1814-1819.
115. Sensi, M., Catani, M., Castellano, G. et al. (2011). Human cutaneous melanomas lacking MITF and melanocyte differentiation antigens express a functional Axl receptor kinase. J. Invest. Dermatol. 131, 2448-2457.
116. Shakhova, O., Zingg, D., Schaefer, S.M. et al. (2012). Sox10 promotes the formation and maintenance of giant congenital naevi and melanoma. Nat. Cell Biol. 14, 882-890.
117. Smith, M.P., Ferguson, J., Arozarena, I., Hayward, R., Marais, R., Chapman, A., Hurlstone, A., and Wellbrock, C. (2013). Effect of SMURF2 targeting on susceptibility to MEK inhibitors in melanoma. J. Natl Cancer Inst. 105, 33-46.
118. Smith, M.P., Sanchez-Laorden, B., O'brien, K. et al. (2014). The immune microenvironment confers resistance to MAPK pathway inhibitors through macrophage-derived TNFalpha. Cancer Discov. 4, 1214-1229.
119. Steingrimsson, E., Copeland, N.G., and Jenkins, N.A. (2004). Melanocytes and the microphthalmia transcription factor network. Annu. Rev. Genet. 38, 365-411.
120. Strub, T., Giuliano, S., Ye, T. et al. (2011). Essential role of microphthalmia transcription factor for DNA replication, mitosis and genomic stability in melanoma. Oncogene 30, 2319-2332.
121. Sturm, R.A., Fox, C., Mcclenahan, P. et al. (2014). Phenotypic characterization of nevus and tumor patterns in MITF E318K mutation carrier melanoma patients. J. Invest. Dermatol. 134, 141-149.
122. Sun, C., Wang, L., Huang, S. et al. (2014). Reversible and adaptive resistance to BRAF(V600E) inhibition in melanoma. Nature 508, 118-122.
123. Tachibana, M. (2000). MITF: a stream flowing for pigment cells. Pigment Cell Res. 13, 230-240.
124. Tachibana, M., Perez-Jurado, L.A., Nakayama, A., Hodgkinson, C.A., Li, X., Schneider, M., Miki, T., Fex, J., Francke, U., and Arnheiter, H. (1994). Cloning of MITF, the human homolog of the mouse microphthalmia gene and assignment to chromosome 3p14.1-p12.3. Hum. Mol. Genet. 3, 553-557.
125. Takeda, K., Takemoto, C., Kobayashi, I., Watanabe, A., Nobukuni, Y., Fisher, D.E., and Tachibana, M. (2000a). Ser298 of MITF, a mutation site in Waardenburg syndrome type 2, is a phosphorylation site with functional significance. Hum. Mol. Genet. 9, 125-132.
126. Takeda, K., Yasumoto, K., Takada, R., Takada, S., Watanabe, K., Udono, T., Saito, H., Takahashi, K., and Shibahara, S. (2000b). Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a. J. Biol. Chem. 275, 14013-14016.
127. Tap, W.D., Gong, K.W., Dering, J. et al. (2010). Pharmacodynamic characterization of the efficacy signals due to selective BRAF inhibition with PLX4032 in malignant melanoma. Neoplasia 12, 637-649.
128. Tassabehji, M., Newton, V.E., Liu, X.Z. et al. (1995). The mutational spectrum in Waardenburg syndrome. Hum. Mol. Genet. 4, 2131-2137.
129. Taylor, K.L., Lister, J.A., Zeng, Z., Ishizaki, H., Anderson, C., Kelsh, R.N., Jackson, I.J., and Patton, E.E. (2011). Differentiated melanocyte cell division occurs in vivo and is promoted by mutations in Mitf. Development 138, 3579-3589.
130. Thomas, A.J., and Erickson, C.A. (2008). The making of a melanocyte: the specification of melanoblasts from the neural crest. Pigment Cell Melanoma Res. 21, 598-610.
131. Thomas, A.J., and Erickson, C.A. (2009). FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136, 1849-1858.
132. Thomson, J.A., Murphy, K., Baker, E., Sutherland, G.R., Parsons, P.G., Sturm, R.A., and Thomson, F. (1995). The brn-2 gene regulates the melanocytic phenotype and tumorigenic potential of human melanoma cells. Oncogene 11, 691-700.
133. Thurber, A.E., Douglas, G., Sturm, E.C., Zabierowski, S.E., Smit, D.J., Ramakrishnan, S.N., Hacker, E., Leonard, J.H., Herlyn, M., and Sturm, R.A. (2011). Inverse expression states of the BRN2 and MITF transcription factors in melanoma spheres and tumour xenografts regulate the NOTCH pathway. Oncogene 30, 3036-3048.
134. Ugurel, S., Houben, R., Schrama, D., Voigt, H., Zapatka, M., Schadendorf, D., Brocker, E.B., and Becker, J.C. (2007). Microphthalmia-associated transcription factor gene amplification in metastatic melanoma is a prognostic marker for patient survival, but not a predictive marker for chemosensitivity and chemotherapy response. Clin. Cancer Res. 13, 6344-6350.
135. Van Allen, E.M., Wagle, N., Sucker, A. et al. (2014). The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov. 4, 94-109.
136. Verastegui, C., Bille, K., Ortonne, J.P., and 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.
137. Von Kriegsheim, A., Baiocchi, D., Birtwistle, M. et al. (2009). Cell fate decisions are specified by the dynamic ERK interactome. Nat. Cell Biol. 11, 1458-1464.
138. Watanabe, A., Takeda, K., Ploplis, B., and Tachibana, M. (1998). Epistatic relationship between Waardenburg syndrome genes MITF and PAX3. Nat. Genet. 18, 283-286.
139. Weeraratna, A.T., Jiang, Y., Hostetter, G., Rosenblatt, K., Duray, P., Bittner, M., and Trent, J.M. (2002). Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1, 279-288.
140. Wellbrock, C. (2014). MAPK pathway inhibition in melanoma: resistance three ways. Biochem. Soc. Trans. 42, 727-732.
141. Wellbrock, C., and Marais, R. (2005). Elevated expression of MITF counteracts B-RAF-stimulated melanocyte and melanoma cell proliferation. J. Cell Biol. 170, 703-708.
142. Wellbrock, C., Weisser, C., Geissinger, E., Troppmair, J., and Schartl, M. (2002). Activation of p59(Fyn) leads to melanocyte dedifferentiation by influencing MKP-1-regulated mitogen-activated protein kinase signaling. J. Biol. Chem. 277, 6443-6454.
143. Wellbrock, C., Karasarides, M., and Marais, R. (2004a). The RAF proteins take centre stage. Nat. Rev. Mol. Cell Biol. 5, 875-885.
144. Wellbrock, C., Ogilvie, L., Hedley, D., Karasarides, M., Martin, J., Niculescu-Duvaz, D., Springer, C.J., and Marais, R. (2004b). V599EB-RAF is an oncogene in melanocytes. Cancer Res. 64, 2338-2342.
145. Wellbrock, C., Rana, S., Paterson, H., Pickersgill, H., Brummelkamp, T., and Marais, R. (2008). Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PLoS ONE 3, e2734.
146. Widlund, H.R., Horstmann, M.A., Price, E.R., Cui, J., Lessnick, S.L., Wu, M., He, X., and Fisher, D.E. (2002). Beta-catenin-induced melanoma growth requires the downstream target Microphthalmia-associated transcription factor. J. Cell Biol. 158, 1079-1087.
147. Widmer, D.S., Hoek, K.S., Cheng, P.F., Eichhoff, O.M., Biedermann, T., Raaijmakers, M.I., Hemmi, S., Dummer, R., and Levesque, M.P. (2013). Hypoxia contributes to melanoma heterogeneity by triggering HIF1alpha-dependent phenotype switching. J. Invest. Dermatol. 133, 2436-2443.
148. Wu, M., Hemesath, T.J., Takemoto, C.M., Horstmann, M.A., Wells, A.G., Price, E.R., Fisher, D.Z., and Fisher, D.E. (2000). c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev. 14, 301-312.
149. Xu, W., Gong, L., Haddad, M.M., Bischof, O., Campisi, J., Yeh, E.T., and Medrano, E.E. (2000). Regulation of microphthalmia-associated transcription factor MITF protein levels by association with the ubiquitin-conjugating enzyme hUBC9. Exp. Cell Res. 255, 135-143.
150. Yang, G., Li, Y., Nishimura, E.K., Xin, H., Zhou, A., Guo, Y., Dong, L., Denning, M.F., Nickoloff, B.J., and Cui, R. (2008). Inhibition of PAX3 by TGF-beta modulates melanocyte viability. Mol. Cell 32, 554-563.
151. 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.
152. Yokoyama, S., Woods, S.L., Boyle, G.M. et al. (2011). A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature 480, 99-103.
153. Yu, M., Bardia, A., Wittner, B.S. et al. (2013). Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580-584.
154. Zeng, Z., Johnson, S.L., Lister, J.A., and Patton, E.E. (2015). Temperature-sensitive splicing of mitfa by an intron mutation in zebrafish. Pigment Cell Melanoma Res. 28, 229-232.
155. Zhao, X., Fiske, B., Kawakami, A., Li, J., and Fisher, D.E. (2011). Regulation of MITF stability by the USP13 deubiquitinase. Nat. Commun. 2, 414.