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Novel MITF targets identified using a two-step DNA microarray strategy

  1. Keith S. Hoek1,
  2. Natalie C. Schlegel1,
  3. Ossia M. Eichhoff1,
  4. Daniel S. Widmer1,
  5. Christian Praetorius2,
  6. Steingrimur O. Einarsson2,3,
  7. Sigridur Valgeirsdottir3,
  8. Kristin Bergsteinsdottir2,
  9. Alexander Schepsky2,4,
  10. Reinhard Dummer1,
  11. Eirikur Steingrimsson2

Article first published online: 11 SEP 2008

DOI: 10.1111/j.1755-148X.2008.00505.x

Issue

Pigment Cell & Melanoma Research

Pigment Cell & Melanoma Research

Volume 21, Issue 6, pages 665–676, December 2008

Additional Information

How to Cite

Hoek, K. S., Schlegel, N. C., Eichhoff, O. M., Widmer, D. S., Praetorius, C., Einarsson, S. O., Valgeirsdottir, S., Bergsteinsdottir, K., Schepsky, A., Dummer, R. and Steingrimsson, E. (2008), Novel MITF targets identified using a two-step DNA microarray strategy. Pigment Cell & Melanoma Research, 21: 665–676. doi: 10.1111/j.1755-148X.2008.00505.x

Author Information

  1. 1

     Department of Dermatology, University Hospital of Zürich, Zürich, Switzerland

  2. 2

     Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Iceland, Reykjavik, Iceland

  3. 3

     NimbleGen Systems of Iceland LLc, Reykjavik, Iceland

  4. 4

     Signalling and Development Lab, Marie Curie Research Institute, Oxted, Surrey, UK

*Keith S. Hoek, e-mail: keith.hoek@usz.ch

Publication History

  1. Issue published online: 11 NOV 2008
  2. Article first published online: 11 SEP 2008
  3. PUBLICATION DATA Received 20 June 2008, revised and accepted for publication 18 August 2008

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References

  • Aoki, H., and Moro, O. (2002). Involvement of microphthalmia-associated transcription factor (MITF) in expression of human melanocortin-1 receptor (MC1R). Life Sci. 71, 2171–2179.
  • Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N., and Golani, I. (2001). Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 125, 279–284.
  • Buck, M.J., and Lieb, J.D. (2004). ChIP-chip: considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments. Genomics 83, 349–360.
  • Busca, R., Berra, E., Gaggioli, C. et al. (2005). Hypoxia-inducible factor 1{alpha} is a new target of microphthalmia-associated transcription factor (MITF) in melanoma cells. J. Cell Biol. 170, 49–59.
  • 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.
  • 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.
  • 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.
  • Chang, H., and Schimmer, A.D. (2007). Livin/melanoma inhibitor of apoptosis protein as a potential therapeutic target for the treatment of malignancy. Mol. Cancer Ther. 6, 24–30.
  • Chiaverini, C., Beuret, L., Flori, E., Busca, R., Abbe, P., Bille, K., Bahadoran, P., Ortonne, J.P., Bertolotto, C., and Ballotti, R. (2008). Microphthalmia associated transcription factor (MITF regulates rab27A gene expression and controls melanosomes transport. J. Biol. Chem. 283, 12635–12642.
  • Du, J., and Fisher, D.E. (2002). Identification of Aim-1 as the underwhite mouse mutant and its transcriptional regulation by MITF. J. Biol. Chem. 277, 402–406.
  • Du, J., Miller, A.J., Widlund, H.R., Horstmann, M.A., Ramaswamy, S., and Fisher, D.E. (2003). MLANA/MART1 and SILV/PMEL17/GP100 are transcriptionally regulated by MITF in melanocytes and melanoma. Am. J. Pathol. 163, 333–343.
  • 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.
  • Dummer, R., and Nestle, F.O. (2000). Melanoma vaccines in development: looking to the future. BioDrugs 13, 227–231.
  • Duncan, K.G., Bailey, K.R., Kane, J.P., and Schwartz, D.M. (2002). Human retinal pigment epithelial cells express scavenger receptors BI and BII. Biochem. Biophys. Res. Commun. 292, 1017–1022.
  • Dynek, J.N., Chan, S.M., Liu, J., Zha, J., Fairbrother, W.J., and Vucic, D. (2008). Microphthalmia-associated transcription factor is a critical transcriptional regulator of melanoma inhibitor of apoptosis in melanomas. Cancer Res. 68, 3124–3132.
  • Esumi, N., Kachi, S., Campochiaro, P.A., and Zack, D.J. (2007). VMD2 promoter requires two proximal E-box sites for its activity in vivo and is regulated by the MITF-TFE family. J. Biol. Chem. 282, 1838–1850.
  • Fang, D., Tsuji, Y., and Setaluri, V. (2002). Selective down-regulation of tyrosinase family gene TYRP1 by inhibition of the activity of melanocyte transcription factor, MITF. Nucleic Acids Res. 30, 3096–3106.
  • Gaggioli, C., Busca, R., Abbe, P., Ortonne, J.P., and Ballotti, R. (2003). Microphthalmia-associated transcription factor (MITF) is required but is not sufficient to induce the expression of melanogenic genes. Pigment Cell Res. 16, 374–382.
    Direct Link:
  • 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.
  • Ge, Y., Jippo, T., Lee, Y.M., Adachi, S., and Kitamura, Y. (2001). Independent influence of strain difference and mi transcription factor on the expression of mouse mast cell chymases. Am. J. Pathol. 158, 281–292.
  • Gelineau-van Waes, J., Smith, L., Van Waes, M., Wilberding, J., Eudy, J.D., Bauer, L.K., and Maddox, J. (2008). Altered expression of the iron transporter Nramp1 (Slc11a1) during fetal development of the retinal pigment epithelium in microphthalmia-associated transcription factor Mitf(mi) and Mitf(vitiligo) mouse mutants. Exp. Eye Res. 86, 419–433.
  • Grichnik, J.M., Burch, J.A., Burchette, J., and Shea, C.R. (1998). The SCF/KIT pathway plays a critical role in the control of normal human melanocyte homeostasis. J. Invest. Dermatol. 111, 233–238.
  • Gutierrez-Gil, B., Wiener, P., and Williams, J.L. (2007). Genetic effects on coat colour in cattle: dilution of eumelanin and phaeomelanin pigments in an F2-Backcross Charolais × Holstein population. BMC Genet. 8, 56.
  • 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.
  • Hoek, K.S. (2007). DNA microarray analyses of melanoma gene expression: a decade in the mines. Pigment Cell Res. 20, 466–484.
    Direct Link:
  • 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.
    Direct Link:
  • Hoek, K.S., Eichhoff, O.M., Schlegel, N.C., Doebbeling, U., 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.
  • Hou, L., Panthier, J.J., and Arnheiter, H. (2000). Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development 127, 5379–5389.
  • Hutton, S.M., and Spritz, R.A. (2008). A comprehensive genetic study of autosomal recessive ocular albinism in caucasian patients. Invest. Ophthalmol. Vis. Sci. 49, 868–872.
  • Ishida, B.Y., Bailey, K.R., Duncan, K.G., Chalkley, R.J., Burlingame, A.L., Kane, J.P., and Schwartz, D.M. (2004). Regulated expression of apolipoprotein E by human retinal pigment epithelial cells. J. Lipid Res. 45, 263–271.
  • Ito, A., Morii, E., Maeyama, K., Jippo, T., Kim, D.K., Lee, Y.M., Ogihara, H., Hashimoto, K., Kitamura, Y., and Nojima, H. (1998). Systematic method to obtain novel genes that are regulated by mi transcription factor: impaired expression of granzyme B and tryptophan hydroxylase in mi/mi cultured mast cells. Blood 91, 3210–3221.
  • Ito, A., Jippo, T., Wakayama, T., Morii, E., Koma, Y., Onda, H., Nojima, H., Iseki, S., and Kitamura, Y. (2003). SgIGSF: a new mast-cell adhesion molecule used for attachment to fibroblasts and transcriptionally regulated by MITF. Blood 101, 2601–2608.
  • Jippo, T., Morii, E., Tsujino, K., Tsujimura, T., Lee, Y.M., Kim, D.K., Matsuda, H., Kim, H.M., and Kitamura, Y. (1997). Involvement of transcription factor encoded by the mouse mi locus (MITF) in expression of p75 receptor of nerve growth factor in cultured mast cells of mice. Blood 90, 2601–2608.
  • Jippo, T., Lee, Y.M., Katsu, Y., Tsujino, K., Morii, E., Kim, D.K., Kim, H.M., and Kitamura, Y. (1999). Deficient transcription of mouse mast cell protease 4 gene in mutant mice of mi/mi genotype. Blood 93, 1942–1950.
  • Johansson, P., Pavey, S., and Hayward, N. (2007). Confirmation of a BRAF mutation-associated gene expression signature in melanoma. Pigment Cell Res. 20, 216–221.
    Direct Link:
  • Kawaguchi, N., and Noda, M. (2000). Mitf is expressed in osteoclast progenitors in vitro. Exp. Cell Res. 260, 284–291.
  • Kenny, J.J., Knobloch, T.J., Augustus, M., Carter, K.C., Rosen, C.A., and Lang, J.C. (1997). GRS, a novel member of the Bcl-2 gene family, is highly expressed in multiple cancer cell lines and in normal leukocytes. Oncogene 14, 997–1001.
  • Kim, D.K., Morii, E., Ogihara, H., Hashimoto, K., Oritani, K., Lee, Y.M., Jippo, T., Adachi, S., Kanakura, Y., and Kitamura, Y. (1998). Impaired expression of integrin alpha-4 subunit in cultured mast cells derived from mutant mice of mi/mi genotype. Blood 92, 1973–1980.
  • 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.
  • Larribere, L., Hilmi, C., Khaled, M., Gaggioli, C., Bille, K., Auberger, P., Ortonne, J.P., Ballotti, R., and Bertolotto, C. (2005). The cleavage of microphthalmia-associated transcription factor, MITF, by caspases plays an essential role in melanocyte and melanoma cell apoptosis. Genes Dev. 19, 1980–1985.
  • 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.
  • 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.
  • Loftus, S.K., Antonellis, A., Matera, I. et al. (2008). Gpnmb is a melanoblast-expressed, MITF-dependent gene. Pigment Cell Melanoma Res. In press.
  • Luchin, A., Purdom, G., Murphy, K., Clark, M.Y., Angel, N., Cassady, A.I., Hume, D.A., and Ostrowski, M.C. (2000). The microphthalmia transcription factor regulates expression of the tartrate-resistant acid phosphatase gene during terminal differentiation of osteoclasts. J. Bone Miner. Res. 15, 451–460.
    Direct Link:
  • Magnoni, C., Tenedini, E., Ferrari, F. et al. (2007). Transcriptional profiles in melanocytes from clinically unaffected skin distinguish the neoplastic growth pattern in patients with melanoma. Br. J. Dermatol. 156, 62–71.
    Direct Link:
  • 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.
  • 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.
  • Meadows, N.A., Sharma, S.M., Faulkner, G.J., Ostrowski, M.C., Hume, D.A., and Cassady, A.I. (2007). The expression of Clcn7 and Ostm1 in osteoclasts is coregulated by microphthalmia transcription factor. J. Biol. Chem. 282, 1891–1904.
  • Miller, A.J., Du, J., Rowan, S., Hershey, C.L., Widlund, H.R., and Fisher, D.E. (2004). Transcriptional regulation of the melanoma prognostic marker melastatin (TRPM1) by MITF in melanocytes and melanoma. Cancer Res. 64, 509–516.
  • Morii, E., Tsujimura, T., Jippo, T., Hashimoto, K., Takebayashi, K., Tsujino, K., Nomura, S., Yamamoto, M., and Kitamura, Y. (1996). Regulation of mouse mast cell protease 6 gene expression by transcription factor encoded by the mi locus. Blood 88, 2488–2494.
  • Morii, E., Jippo, T., Tsujimura, T., Hashimoto, K., Kim, D.K., Lee, Y.M., Ogihara, H., Tsujino, K., Kim, H.M., and Kitamura, Y. (1997). Abnormal expression of mouse mast cell protease 5 gene in cultured mast cells derived from mutant mi/mi mice. Blood 90, 3057–3066.
  • Morii, E., Ogihara, H., Oboki, K., Sawa, C., Sakuma, T., Nomura, S., Esko, J.D., Handa, H., and Kitamura, Y. (2001). Inhibitory effect of the mi transcription factor encoded by the mutant mi allele on GA binding protein-mediated transcript expression in mouse mast cells. Blood 97, 3032–3039.
  • Motyckova, G., Weilbaecher, K.N., Horstmann, M., Rieman, D.J., Fisher, D.Z., and Fisher, D.E. (2001). Linking osteopetrosis and pycnodysostosis: regulation of cathepsin K expression by the microphthalmia transcription factor family. Proc. Natl. Acad. Sci. U.S.A. 98, 5798–5803.
  • Murakami, H., and Arnheiter, H. (2005). Sumoylation modulates transcriptional activity of MITF in a promoter-specific manner. Pigment Cell Res. 18, 265–277.
    Direct Link:
  • Murakami, M., Ikeda, T., Saito, T., Ogawa, K., Nishino, Y., Nakaya, K., and Funaba, M. (2006). Transcriptional regulation of plasminogen activator inhibitor-1 by transforming growth factor-beta, activin A and microphthalmia-associated transcription factor. Cell Signal 18, 256–265.
  • Nechushtan, H., Zhang, Z., and Razin, E. (1997). Microphthalmia (mi) in murine mast cells: regulation of its stimuli-mediated expression on the translational level. Blood 89, 2999–3008.
  • Ochrietor, J.D., Clamp, M.F., Moroz, T.P., Grubb, J.H., Shah, G.N., Waheed, A., Sly, W.S., and Linser, P.J. (2005). Carbonic anhydrase XIV identified as the membrane CA in mouse retina: strong expression in Muller cells and the RPE. Exp. Eye Res. 81, 492–500.
  • Park, H.Y., Wu, C., Yonemoto, L., Murphy-Smith, M., Wu, H., Stachur, C.M., and Gilchrest, B.A. (2006). MITF mediates cAMP-induced protein kinase C-beta expression in human melanocytes. Biochem. J. 395, 571–578.
  • Piva, R., Pellegrino, E., Mattioli, M. et al. (2006). Functional validation of the anaplastic lymphoma kinase signature identifies CEBPB and BCL2A1 as critical target genes. J. Clin. Invest. 116, 3171–3182.
  • 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.
  • Prieto, V.G., Mourad-Zeidan, A.A., Melnikova, V. et al. (2006). Galectin-3 expression is associated with tumor progression and pattern of sun exposure in melanoma. Clin. Cancer Res. 12, 6709–6715.
  • Ryu, B., Kim, D.S., Deluca, A.M., and Alani, R.M. (2007). Comprehensive expression profiling of tumor cell lines identifies molecular signatures of melanoma progression. PLoS ONE 2, e594.
  • Sato-Jin, K., Nishimura, E.K., Akasaka, E. et al. (2007). Epistatic connections between microphthalmia-associated transcription factor and endothelin signaling in Waardenburg syndrome and other pigmentary disorders. FASEB J. 22, 1155–1168.
  • Schwabe, M., Zhao, J., and Kung, H.F. (1994). Differential expression and ligand-induced modulation of the human interleukin-6 receptor on interleukin-6-responsive cells. J. Biol. Chem. 269, 7201–7209.
  • 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.
  • So, H., Rho, J., Jeong, D., Park, R., Fisher, D.E., Ostrowski, M.C., Choi, Y., and Kim, N. (2003). Microphthalmia transcription factor and PU.1 synergistically induce the leukocyte receptor osteoclast-associated receptor gene expression. J. Biol. Chem. 278, 24209–24216.
  • Steingrimsson, E., Copeland, N.G., and Jenkins, N.A. (2004). Melanocytes and the Microphthalmia Transcription Factor Network. Annu. Rev. Genet. 38, 365–411.
  • Stolt, C.C., Rehberg, S., Ader, M., Lommes, P., Riethmacher, D., Schachner, M., Bartsch, U., and Wegner, M. (2002). Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev. 16, 165–170.
  • Sundram, U., Harvell, J.D., Rouse, R.V., and Natkunam, Y. (2003). Expression of the B-cell proliferation marker MUM1 by melanocytic lesions and comparison with S100, gp100 (HMB45), and MelanA. Mod. Pathol. 16, 802–810.
  • Tachibana, M. (1997). Evidence to suggest that expression of MITF induces melanocyte differentiation and haploinsufficiency of MITF causes Waardenburg syndrome type 2A. Pigment Cell Res. 10, 25–33.
    Direct Link:
  • Truzzi, F., Marconi, A., Lotti, R., Dallaglio, K., French, L.E., Hempstead, B.L., and Pincelli, C. (2008). Neurotrophins and Their Receptors Stimulate Melanoma Cell Proliferation and Migration. J. Invest. Dermatol. 128, 2031–2040.
  • Tsujimura, T., Morii, E., Nozaki, M., Hashimoto, K., Moriyama, Y., Takebayashi, K., Kondo, T., Kanakura, Y., and Kitamura, Y. (1996). Involvement of transcription factor encoded by the mi locus in the expression of c-kit receptor tyrosine kinase in cultured mast cells of mice. Blood 88, 1225–1233.
  • 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.
  • Vetrini, F., Auricchio, A., Du, J., Angeletti, B., Fisher, D.E., Ballabio, A., and Marigo, V. (2004). The microphthalmia transcription factor (Mitf) controls expression of the ocular albinism type 1 gene: link between melanin synthesis and melanosome biogenesis. Mol. Cell. Biol. 24, 6550–6559.
  • Wagner, K.W., Punnoose, E.A., Januario, T. et al. (2007). Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat. Med. 13, 1070–1077.
  • Wang, R., Tang, P., Wang, P., Boissy, R.E., and Zheng, H. (2006). Regulation of tyrosinase trafficking and processing by presenilins: partial loss of function by familial Alzheimer’s disease mutation. Proc. Natl. Acad. Sci. U.S.A. 103, 353–358.
  • Weeraratna, A.T., Becker, D., Carr, K.M. et al. (2004). Generation and analysis of melanoma SAGE libraries: SAGE advice on the melanoma transcriptome. Oncogene 23, 2264–2274.
  • De Wit, N.J., Rijntjes, J., Diepstra, J.H., Van Kuppevelt, T.H., Weidle, U.H., Ruiter, D.J., and Van Muijen, G.N. (2005). Analysis of differential gene expression in human melanocytic tumour lesions by custom made oligonucleotide arrays. Br. J. Cancer 92, 2249–2261.
  • 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.
  • 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.
  • Yasumoto, K., Takeda, K., Saito, H., Watanabe, K., Takahashi, K., and Shibahara, S. (2002). Microphthalmia-associated transcription factor interacts with LEF-1, a mediator of Wnt signaling. EMBO J. 21, 2703–2714.
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