Sumoylation modulates transcriptional activity of MITF in a promoter-specific manner

Pigment Cell Research

Volumn 18, Issue 4, 2005, Pages 265-277

  Murakami, Hideki ^a   Arnheiter, Heinz ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Cooperation; Melanocyte; Posttranslational regulation; Sox10; Transcription regulation

Indexed keywords

ARGININE; LYSINE; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; PROTEIN SAE I; PROTEIN SAE II; PROTEIN UBC9; SUMO PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; HUMAN; HUMAN CELL; IN VITRO STUDY; MELANOMA CELL; MOLECULAR MECHANICS; MOUSE; MUTATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PROMOTER REGION; PROTEIN MODIFICATION; PROTEIN STABILITY; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CELL LINE, TUMOR; HUMANS; MELANOMA; MICE; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); SEQUENCE HOMOLOGY, AMINO ACID; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TRANSCRIPTION, GENETIC; UBIQUITIN-CONJUGATING ENZYMES;

EID: 22744450397     PISSN: 08935785     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0749.2005.00234.x     Document Type: Article

References (54)

1. Aksan, I., and Goding, C.R. (1998). Targeting the microphthalmia basic helix-loop-helix-leucine zipper transcription factor to a subset of E-box elements in vitro and in vivo. Mol. Cell. Biol. 18, 6930-6938.
2. Arnheiter, H., Hou, L., Nguyen, M.-T.T., Bismuth, K., Csermely, T., Murakami, H., Skuntz, S., Liu, W., and Bharti, K. (in press). Mitf - a matter of life and death for the developing melanocyte. Melanocytes to Melanoma: The Progression to Malignancy (Totowa, NJ: Humana Press) (in press).
3. 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.
4. Desterro, J.M., Thomson, J., and Hay, R.T. (1997). Ubch9 conjugates SUMO but not ubiquitin. FEBS Lett. 417, 297-300.
5. Desterro, J.M., Rodriguez, M.S., and Hay, R.T. (1998). SUMO-1 modification of IκBα inhibits NF-κB activation. Mol. Cell. 2, 233-239.
6. Desterro, J.M., Rodriguez, M.S., Kemp, G.D., and Hay, R.T. (1999). Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J. Biol. Chem. 274, 10618-10624.
7. Gong, L., Kamitani, T., Fujise, K., Caskey, L.S., and Yen, E.T. (1997). Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J. Biol. Chem. 272, 28198-28201.
8. Gross, M., Yang, R., Top, I., Gasper, C., and Shuai, K. (2004). PIASy-mediated repression of the androgen receptor is independent of sumoylation. Oncogene 23, 3059-3066.
9. Hallsson, J.H., Haflidadottir, B.S., Stivers, C., Odenwald, W., Arnheiter, H., Pignoni, F., and Steingrimsson, E. (2004). The basic helix-loop-helix leucine zipper transcription factor Mitf is conserved in Drosophila and functions in eye development. Genetics 167, 233-241.
10. Hemesath, TJ., 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.
11. 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.
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. Holmstrom, S., VanAntwerp, M.E., and Iniguez-Lluhi, J.A. (2003). Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy. Proc. Natl Acad. Sci. U. S. A. 100, 15758-15763.
14. Iniguez-Lluhi, J.A., and Pearce, D. (2000). A common motif within the negative regulatory regions of multiple factors inhibits their transcriptional synergy. Mol. Cell. Biol. 20, 6040-6050.
15. Jiao, Z., Mollaaghababa, R., Pavan, W.J., Antonellis, A., Green, E.D., and Hornyak, T.J. (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.
16. Kagey, M.H., Melhuish, T.A., and Wotton, D. (2003). The polycomb protein Pc2 is a SUMO E3. Cell 113, 127-137.
17. Kahyo, T., Nishida, T., and Yasuda, H. (2001). Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell. 8, 713-718.
18. Kamitani, T., Kito, K., Nguyen, H.P., and Yeh, E.T. (1997). Characterization of NEDD8, a developmentally down-regulated ubiquitin-like protein. J. Biol. Chem. 272, 28557-28562.
19. Kotaja, N., Karvonen, U., Janne, O.A., and Palvimo, J.J. (2002). PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 22, 5222-5234.
20. Lapenta, V., Chiurazzi, P., VanDerSpek, P., Pizzuti, A., Hanaoka, F., and Brahe, C. (1997). SMT3A, a human homologue of the S. cerevisiae SMT3 gene, maps to chromosome 21qter and defines a novel gene family. Genomics 40, 362-366.
21. Levy, C., Nechushtan, H., and Razin, E. (2002). A new role for the STATS inhibitor, PIAS3: a repressor of microphthalmia transcription factor. J. Biol. Chem. 277, 1962-1966.
22. 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.
23. Ludwig, A., Rehberg, S., and 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.
24. Mahajan, R., Delphin, C., Guan, T., Gerace, L., and Melchior, F. (1997). A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88, 97-107.
25. 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.
26. Mao, Y., Sun, M., Desai, S.D., and Liu, L.F. (2000). SUMO-1 conjugation to topoisomerase I: a possible repair response to topoisomerase-mediated DNA damage. Proc. Natl Acad. Sci. U. S. A. 97, 4046-4051.
27. Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y., Ishii, T., George, M.D., Klionsky, D.J., Ohsumi, M., and Ohsumi, Y. (1998). A protein conjugation system essential for autophagy. Nature 395, 395-398.
28. 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.
29. 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.
30. Muller, S., Matunis, M.J., and Dejean, A. (1998). Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. Embo. J. 17, 61-70.
31. Murakami, H., Yamamura, Y., Shimono, Y., Kawai, K., Kurokawa, K., and Takahashi, M. (2002). Role of Dok1 in cell signaling mediated by RET tyrosine kinase. J. Biol. Chem. 277, 32781-32790.
32. Nakayama, A., Nguyen, M.T., Chen, C.C., Opdecamp, K., Hodgkinson, C.A., and Arnheiter, H. (1998). Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently. Mech. Dev. 70, 155-166.
33. Poukka, H., Karvonen, U., Janne, O.A., and Palvimo, J.J. (2000). Covalent modification of the androgen receptor by small ubiquitin-like modifier 1 (SUMO-1). Proc. Natl Acad. Sci. U. S. A. 97, 14145-14150.
34. Price, E.R., Ding, H.F., Badalian, T., Bhattacharya, S., Takemoto, C., Yao, T.P., Hemesath, T.J., and Fisher, D.E. (1998). Lineage-specific signaling in melanocytes. C-kit stimulation recruits p300/CBP to microphthalmia. J. Biol. Chem. 273, 17983-17986.
35. Qi, F., Ridpath, J.F., and Berry, E.S. (1998). Insertion of a bovine SMT3B gene in NS4B and duplication of NS3 in a bovine viral diarrhea virus genome correlate with the cytopathogenicity of the virus. Virus Res. 57, 1-9.
36. Rehli, M., DenElzen, N., Cassady, A.I., Ostrowski, M.C., and Hume, D.A. (1999). Cloning and characterization of the murine genes for bHLH-ZIP transcription factors TFEC and TFEB reveal a common gene organization for all MiT subfamily members. Genomics 56, 111-120.
37. Rodriguez, M.S., Dargemont, C., and Hay, R.T. (2001). SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659.
38. Sachdev, S., Bruhn, L., Sieber, H., Pichler, A., Melchior, F., and Grosschedl, R. (2001). PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15, 3088-3103.
39. 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.
40. Shiio, Y., and Eisenman, R.N. (2003). Histone sumoylation is associated with transcriptional repression. Proc. Natl Acad. Sci. U. S. A. 100, 13225-13230.
41. Shimono, Y., Murakami, H., Hasegawa, Y., and Takahashi, M. (2000). RET finger protein is a transcriptional repressor and interacts with enhancer of polycomb that has dual transcriptional functions. J. Biol. Chem. 275, 39411-39419.
42. Steingrimsson, E., Moore, K.J., Lamoreux, M.L. et al. (1994). Molecular basis of mouse microphthalmia (mi) mutations helps explain their developmental and phenotypic consequences. Nat. Genet. 8, 256-263.
43. Steingrimsson, E., Copeland, N.G., and Jenkins, N.A. (2004). Melanocytes and the microphthalmia transcription factor network. Annu. Rev. Genet. 38, 365-411.
44. Suzuki, T., Ichiyama, A., Saitoh, H., Kawakami, T., Omata, M., Chung, C.H., Kimura, M., Shimbara, N., and Tanaka, K. (1999). A new 30-kDa ubiquitin-related SUMO-1 hydrolase from bovine brain. J. Biol. Chem. 274, 31131-31134.
45. 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.
46. 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.
47. Tian, S., Poukka, H., Palvimo, J.J., and Janne, O.A. (2002). Small ubiquitin-related modifier-1 (SUMO-1) modification of the glucocorticoid receptor. Biochem. J. 367, 907-911.
48. Vance, K.W., and Goding, C.R. (2004). The transcription network regulating melanocyte development and melanoma. Pigment Cell Res. 17, 318-325.
49. Weilbaecher, K.N., Motyckova, G., Huber, W.E., Takemoto, C.M., Hemesath, T.J., Xu, Y., Hershey, C.L., Dowland, N.R., Wells, A.G., and Fisher, D.E. (2001). Linkage of M-CSF signaling to Mitf, TFE3, and the osteoclast defect in Mitf(mi/mi) mice. Mol. Cell. 8, 749-758.
50. 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.
51. 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 enzymeh UBC9. Exp. Cell. Res. 255, 135-143.
52. Yang, S.H., and Sharrocks, A.D. (2004). SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell. 13, 611-617.
53. Yasumoto, K., Yokoyama, K., Takahashi, K., Tomita, Y., and Shibahara, S. (1997). Functional analysis of microphthalmia-associated transcription factor in pigment cell-specific transcription of the human tyrosinase family genes. J. Biol. Chem. 272, 503-509.
54. 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.