Restricted leucine zipper dimerization and specificity of DNA recognition of the melanocyte master regulator MITF

Genes and Development

Volumn 26, Issue 23, 2012, Pages 2647-2658

  Pogenberg, Vivian ^a   Ögmundsdóttir, Margrét H ^b   Bergsteinsdóttir, Kristín ^b   Schepsky, Alexander ^b   Phung, Bengt ^b,c   Deineko, Viktor ^a   Milewski, Morlin ^a   Steingrímsson, Eiríkur ^b   Wilmanns, Matthias ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF ICELAND   (Iceland)

^c LUND UNIVERSITY   (Sweden)

Author keywords

Crystal structure; DNA binding; Leucine zipper; Melanocyte regulation; Transcription factor

Indexed keywords

HETERODIMER; LEUCINE ZIPPER PROTEIN; MAX PROTEIN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DNA RESPONSIVE ELEMENT; E BOX ELEMENT; GENE INSERTION; GENE MUTATION; HUMAN; M BOX; MELANOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DNA INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; WAARDENBURG SYNDROME;

AMINO ACID SEQUENCE; ANIMALS; DIMERIZATION; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; HUMANS; LEUCINE ZIPPERS; MICE; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; WAARDENBURG SYNDROME;

MUS;

EID: 84870508533     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.198192.112     Document Type: Article

References (43)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
2. Aksan I, Goding CR. 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.
3. Bendall AJ, Molloy PL. 1994. Base preferences for DNA binding by the bHLH-Zip protein USF: Effects of MgCl2 on specificity and comparison with binding of Myc family members. Nucleic Acids Res 22: 2801-2810.
4. Berka K, Hanak O, Sehnal D, Banas P, Navratilova V, Jaiswal D, Ionescu CM, Svobodova Varekova R, Koca J, Otyepka M. 2004. MOLEonline 2.0: Interactive Web-based analysis of biomacromolecular channels. Nucleic Acids Res 40: W222-W227. doi: 10.1093/nar/gks363.
5. 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.
6. Blackwood EM, Eisenman RN. 1991. Max: A helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science 251: 1211-1217.
7. Brownlie P, Ceska T, Lamers M, Romier C, Stier G, Teo H, Suck D. 1997. The crystal structure of an intact human Max-DNA complex: New insights into mechanisms of transcriptional control. Structure 5: 509-520.
8. Carreira S, Goodall J, Denat L, Rodriguez M, Nuciforo P, Hoek KS, Testori A, Larue L, Goding CR. 2006. Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev 20: 3426-3439.
9. Cheli Y, Ohanna M, Ballotti R, Bertolotto C. 2009. Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res 23: 27-40.
10. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117.
11. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
12. Collaborative Computational Project Number 4. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
13. Corre S, Primot A, Sviderskaya E, Bennett DC, Vaulont S, Goding CR, Galibert MD. 2004. UV-induced expression of key component of the tanning process, the POMC and MC1R genes, is dependent on the p-38-activated upstream stimulating factor-1 (USF-1). J Biol Chem 279: 51226-51233.
14. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
15. Ferre-D'Amare AR, Prendergast GC, Ziff EB, Burley SK. 1993. Recognition by Max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 363: 38-45.
16. Garraway LA, Widlund HR, Rubin MA, Getz G, Berger AJ, Ramaswamy S, Beroukhim R, Milner DA, Granter SR, Du J, et al. 2005. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436: 117-122.
17. Hemesath TJ, Steingrimsson E, McGill G, Hansen MJ, Vaught J, Hodgkinson CA, Arnheiter H, Copeland NG, Jenkins NA, Fisher DE. 1994. Microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev 8: 2770-2780.
18. Jiao Z, Mollaaghababa R, Pavan WJ, Antonellis A, Green ED, Hornyak TJ. 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.
19. Jones S. 2004. An overview of the basic helix-loop-helix proteins. Genome Biol 5: 226. doi: 10.1186/gb-2004-5-6-226.
20. Kim DK, Morii E, Ogihara H, Lee YM, Jippo T, Adachi S, Maeyama K, Kim HM, Kitamura Y. 1999. Different effect of various mutant MITF encoded by mi, Mior, or Miwh allele on phenotype of murine mast cells. Blood 93: 4179-4186.
21. Laskowski RA, Moss DS, Thornton JM. 1993. Main-chain bond lengths and bond angles in protein structures. J Mol Biol 231: 1049-1067.
22. Lavery R, Moakher M, Maddocks JH, Petkeviciute D, Zakrzewska K. 2009. Conformational analysis of nucleic acids revisited: Curves+. Nucleic Acids Res 37: 5917-5929.
23. Leslie AGW, Powell HR. 2007. Processing diffraction data with MOSFLM. In Evolving methods for macromolecular crystallography (ed. R Read and JL Sussman), pp. 41-51. Springer, Dordrecht, The Netherlands.
24. Lupas AN, Gruber M. 2005. The structure of a-helical coiled coils. Adv Protein Chem 70: 37-78.
25. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
26. Nair SK, Burley SK. 2003. X-ray structures of Myc-Max and Mad-Max recognizing DNA. Molecular bases of regulation by proto-oncogenic transcription factors. Cell 112: 193-205.
27. Nishimura EK, Granter SR, Fisher DE. 2005. Mechanisms of hair graying: Incomplete melanocyte stem cell maintenance in the niche. Science 307: 720-724.
28. Pan Y, Tsai CJ, Ma B, Nussinov R. 2010. Mechanisms of transcription factor selectivity. Trends Genet 26: 75-83.
29. Panjikar S, Parthasarathy V, Lamzin VS, Weiss MS, Tucker PA. 2005. Auto-Rickshaw: An automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr D Biol Crystallogr 61: 449-457.
30. Peters JW, Stowell MH, Rees DC. 1996. A leucine-rich repeat variant with a novel repetitive protein structural motif. Nat Struct Biol 3: 991-994.
31. Pingault V, Ente D, Dastot-Le Moal F, Goossens M, Marlin S, Bondurand N. 2010. Review and update of mutations causing Waardenburg syndrome. Hum Mutat 31: 391-406.
32. Sheldrick GM. 2010. Experimental phasing with SHELXC/D/E: Combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66: 479-485.
33. Steingrimsson E. 2010. Interpretation of complex phenotypes: Lessons from the Mitf gene. Pigment Cell Melanoma Res 23: 736-740.
34. Steingrimsson E, Arnheiter H, Hallsson JH, Lamoreux ML, Copeland NG, Jenkins NA. 2003. Interallelic complementation at the mouse Mitf locus. Genetics 163: 267-276.
35. Steingrimsson E, Copeland NG, Jenkins NA. 2004. Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet 38: 365-411.
36. Storoni LC, McCoy AJ, Read RJ. 2004. Likelihood-enhanced fast rotation functions. Acta Crystallogr D Biol Crystallogr 60: 432-438.
37. 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.
38. Tassabehji M, Newton VE, Liu XZ, 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.
39. Terwilliger TC. 2000. Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56: 965-972.
40. Vaguine AA, Richelle J, Wodak SJ. 1999. SFCHECK: A unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallogr D Biol Crystallogr 55: 191-205.
41. Verastegui C, Bertolotto C, Bille K, Abbe P, Ortonne JP, Ballotti R. 2000. TFE3, a transcription factor homologous to microphthalmia, is a potential transcriptional activator of tyrosinase and TyrpI genes. Mol Endocrinol 14: 449-456.
42. Wellbrock C, Rana S, Paterson H, Pickersgill H, Brummelkamp T, Marais R. 2008. Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PLoS ONE 3: e2734. doi: 10.1371/journal.pone.0002734.
43. Yokoyama S, Woods SL, Boyle GM, Aoude LG, Macgregor S, Zismann V, Gartside M, Cust AE, Haq R, Harland M, et al. 2011. A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature 480: 99-103.