Structural insights of the MLF1/14-3-3 interaction

FEBS Journal

Volumn 279, Issue 4, 2012, Pages 563-571

  Molzan, Manuela ^a   Weyand, Michael ^b   Rose, Rolf ^a   Ottmann, Christian ^a  

^a CHEMICAL GENOMICS CENTRE OF THE MAX PLANCK SOCIETY   (Germany)

^b UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

drug discovery; fragment based ligand discovery; leukaemia; PPI stabilization; protein protein interactions; X ray crystallography

Indexed keywords

MYELOID LEUKEMIA FACTOR 1 PROTEIN; ONCOPROTEIN; PROTEIN 14 3 3; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STRUCTURE ANALYSIS;

14-3-3 PROTEINS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RECOMBINANT PROTEINS; SERINE;

EID: 84856315533     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08445.x     Document Type: Article

References (48)

1. Yoneda-Kato N, Look AT, Kirstein MN, Valentine MB, Raimondi SC, Cohen KJ, Carroll AJ, &, Morris SW, (1996) The t(3;5)(q25.1;q34) of myelodysplastic syndrome and acute myeloid leukemia produces a novel fusion gene, NPM-MLF1. Oncogene 12, 265-275. (Pubitemid 26042564)
2. Olson MO, Wallace MO, Herrera AH, Marshall-Carlson L, &, Hunt RC, (1986) Preribosomal ribonucleoprotein particles are a major component of a nucleolar matrix fraction. Biochemistry 25, 484-491. (Pubitemid 16053814)
3. Falini B, Bigerna B, Pucciarini A, Tiacci E, Mecucci C, Morris SW, Bolli N, Rosati R, Hanissian S, Ma Z, et al. (2006) Aberrant subcellular expression of nucleophosmin and NPM-MLF1 fusion protein in acute myeloid leukaemia carrying t(3;5): a comparison with NPMc+ AML. Leukemia 20, 368-371. (Pubitemid 43148684)
4. Matsumoto N, Yoneda-Kato N, Iguchi T, Kishimoto Y, Kyo T, Sawada H, Tatsumi E, &, Fukuhara S, (2000) Elevated MLF1 expression correlates with malignant progression from myelodysplastic syndrome. Leukemia 14, 1757-1765.
5. Sun W, Zhang K, Zhang X, Lei W, Xiao T, Ma J, Guo S, Shao S, Zhang H, Liu Y, et al. (2004) Identification of differentially expressed genes in human lung squamous cell carcinoma using suppression subtractive hybridization. Cancer Lett 212, 83-93. (Pubitemid 38887723)
6. Chen J, Guo L, Peiffer DA, Zhou L, Chan OTM, Bibikova M, Wickham-Garcia E, Lu S-H, Zhan Q, Wang-Rodriguez J, et al. (2008) Genomic profiling of 766 cancer-related genes in archived esophageal normal and carcinoma tissues. Int J Cancer 122, 2249-2254. (Pubitemid 351542327)
7. Winteringham LN, Kobelke S, Williams JH, Ingley E, &, Klinken SP, (2004) Myeloid leukemia factor 1 inhibits erythropoietin-induced differentiation, cell cycle exit and p27Kip1 accumulation. Oncogene 23, 5105-5109. (Pubitemid 38938746)
8. Yoneda-Kato N, &, Kato J-Y, (2008) Shuttling imbalance of MLF1 results in p53 instability and increases susceptibility to oncogenic transformation. Mol Cell Biol 28, 422-434.
9. Lim R, Winteringham LN, Williams JH, McCulloch RK, Ingley E, Tiao JY-H, Lalonde J-P, Tsai S, Tilbrook PA, Sun Y, et al. (2002) MADM, a novel adaptor protein that mediates phosphorylation of the 14-3-3 binding site of myeloid leukemia factor 1. J Biol Chem 277, 40997-41008. (Pubitemid 35215689)
10. Yoneda-Kato N, Tomoda K, Umehara M, Arata Y, &, Kato J-Y, (2005) Myeloid leukemia factor 1 regulates p53 by suppressing COP1 via COP9 signalosome subunit 3. EMBO J 24, 1739-1749. (Pubitemid 40704984)
11. Hanissian SH, Akbar U, Teng B, Janjetovic Z, Hoffmann A, Hitzler JK, Iscove N, Hamre K, Du X, &, Tong Y, et al. (2004) cDNA cloning and characterization of a novel gene encoding the MLF1-interacting protein MLF1IP. Oncogene 23, 3700-3707. (Pubitemid 38658437)
12. Winteringham LN, Endersby R, Kobelke S, McCulloch RK, Williams JH, Stillitano J, Cornwall SM, Ingley E, &, Klinken SP, (2006) Myeloid leukemia factor 1 associates with a novel heterogeneous nuclear ribonucleoprotein U-like molecule. J Biol Chem 281, 38791-38800. (Pubitemid 46042006)
13. Ohno K, Takahashi Y, Hirose F, Inoue YH, Taguchi O, Nishida Y, Matsukage A, &, Yamaguchi M, (2000) Characterization of a Drosophila homologue of the human myelodysplasia/myeloid leukemia factor (MLF). Gene 260, 133-143. (Pubitemid 32008508)
14. Bridges D, &, Moorhead GBG, (2005) 14-3-3 proteins: a number of functions for a numbered protein. Science's STKE 2005, re10.
15. Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ, &, Cantley LC, (1997) The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91, 961-971. (Pubitemid 28027829)
16. Johnson C, Crowther S, Stafford M, Campbell D, Toth R, &, MacKintosh C, (2010) Bioinformatic and experimental survey of 14-3-3-binding sites. Biochem J 427, 69-78.
17. Morrison DK, (2009) The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 19, 16-23.
18. Fantl WJ, Muslin AJ, Kikuchi A, Martin JA, MacNicol AM, Gross RW, &, Williams LT, (1994) Activation of Raf-1 by 14-3-3 proteins. Nature 371, 612-614. (Pubitemid 24315743)
19. Molzan M, Schumacher B, Ottmann C, Baljuls A, Polzien L, Weyand M, Thiel P, Rose R, Rose M, Kuhenne P, et al. (2010) Impaired binding of 14-3-3 to C-RAF in Noonan syndrome suggests new approaches in diseases with increased Ras signaling. Mol Cell Biol 30, 4698-4711.
20. Conklin DS, Galaktionov K, &, Beach D, (1995) 14-3-3 Proteins associate with Cdc25 phosphatases. Proc Natl Acad Sci USA 92, 7892-7896.
21. Peng C-Y, Graves PR, Thoma RS, Wu Z, Shaw AS, &, Piwnica-Worms H, (1997) Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277, 1501-1505. (Pubitemid 27449237)
22. Vassilev A, Kaneko KJ, Shu H, Zhao Y, &, Depamphilis ML, (2001) TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Gene Dev 15, 1229-1241. (Pubitemid 32472752)
23. Schumacher B, Skwarczynska M, Rose R, &, Ottmann C, (2010) Structure of a 14-3-3σ-YAP phosphopeptide complex at 1.15 A resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun 66, 978-984.
24. Rajagopalan S, Sade RS, Townsley FM, &, Fersht AR, (2010) Mechanistic differences in the transcriptional activation of p53 by 14-3-3 isoforms. Nucleic Acids Res 38, 893-906.
25. Schumacher B, Mondry J, Thiel P, Weyand M, &, Ottmann C, (2010) Structure of the p53 C-terminus bound to 14-3-3: implications for stabilization of the p53 tetramer. FEBS Lett 584, 1443-1448.
26. Hermeking H, (2003) The 14-3-3 cancer connection. Nature Rev Cancer 3, 931-943. (Pubitemid 37500178)
27. Berg D, Holzmann C, &, Riess O, (2003) 14-3-3 proteins in the nervous system. Nat Rev Neurosci 4, 752-762. (Pubitemid 37280154)
28. Fu H, Coburn J, &, Collier RJ, (1993) The eukaryotic host factor that activates exoenzyme S of Pseudomonas aeruginosa is a member of the 14-3-3 protein family. Proc Natl Acad Sci USA 90, 2320-2324. (Pubitemid 23078618)
29. Ottmann C, Yasmin L, Weyand M, Veesenmeyer JL, Diaz MH, Palmer RH, Francis MS, Hauser AR, Wittinghofer A, &, Hallberg B, (2007) Phosphorylation-independent interaction between 14-3-3 and exoenzyme S: from structure to pathogenesis. EMBO J 26, 902-913.
30. Hitzler JK, Witte DP, Jenkins NA, Copeland NG, Gilbert DJ, Naeve CW, Look AT, &, Morris SW, (1999) cDNA cloning, expression pattern, and chromosomal localization of Mlf1, murine homologue of a gene involved in myelodysplasia and acute myeloid leukemia. Am J Pathol 155, 53-59. (Pubitemid 29318702)
31. Williams JH, Daly LN, Ingley E, Beaumont JG, Tilbrook PA, Lalonde JP, Stillitano JP, &, Klinken SP, (1999) HLS7, a hemopoietic lineage switch gene homologous to the leukemia-inducing gene MLF1. EMBO J 18, 5559-5566. (Pubitemid 29486375)
32. Tzivion G, Gupta VS, Kaplun L, &, Balan V, (2006) 14-3-3 proteins as potential oncogenes. Semin Cancer Biol 16, 203-213. (Pubitemid 43810260)
33. Andrews RK, Du X, &, Berndt MC, (2007) The 14-3-3zeta-GPIb-IX-V complex as an antiplatelet target. Drug News Perspect 20, 285-292.
34. Wu H, Ge J, &, Yao SQ, (2010) Microarray-assisted high-throughput identification of a cell-permeable small-molecule binder of 14-3-3 proteins. Angew Chem Int Ed Engl 49, 6528-6532.
35. Corradi V, Mancini M, Manetti F, Petta S, Santucci MA, &, Botta M, (2010) Identification of the first non-peptidic small molecule inhibitor of the c-Abl/14-3-3 protein-protein interactions able to drive sensitive and imatinib-resistant leukemia cells to apoptosis. Bioorg Med Chem Lett 20, 6133-6137.
36. Mancini M, Corradi V, Petta S, Barbieri E, Manetti F, Botta M, &, Santucci MA, (2011) A new nonpeptidic inhibitor of 14-3-3 induces apoptotic cell death in chronic myeloid leukemia sensitive or resistant to imatinib. J Pharmacol Exp Ther 336, 596-604.
37. Zhao J, Du Y, Horton JR, Upadhyay AK, Lou B, Bai Y, Zhang X, Du L, Li M, Wang B, et al. (2011) Discovery and structural characterization of a small molecule 14-3-3 protein-protein interaction inhibitor. Proc Natl Acad Sci USA 108, 16212-16216.
38. Rose R, Erdmann S, Bovens S, Wolf A, Rose M, Hennig S, Waldmann H, &, Ottmann C, (2010) Identification and structure of small-molecule stabilizers of 14-3-3 protein-protein interactions. Angew Chem Int Ed Engl 49, 4129-4132.
39. Ballio A, Chain EB, DeLeo P, Erlanger BF, Mauri M, &, Tonolo A, (1964) Fusicoccin: a new wilting toxin produced by Fusicoccum amygdali Del. Nature 203, 297-297.
40. Sassa T, Tojyo T, &, Munakata K, (1970) Isolation of a new plant growth substance with cytokinin-like activity. Nature 227, 379.
41. Würtele M, Jelich-Ottmann C, Wittinghofer A, &, Oecking C, (2003) Structural view of a fungal toxin acting on a 14-3-3 regulatory complex. EMBO J 22, 987-994. (Pubitemid 36313583)
42. Ottmann C, Marco S, Jaspert N, Marcon C, Schauer N, Weyand M, Vandermeeren C, Duby G, Boutry M, Wittinghofer A, et al. (2007) Structure of a 14-3-3 coordinated hexamer of the plant plasma membrane H+ -ATPase by combining X-ray crystallography and electron cryomicroscopy. Mol Cell 25, 427-440. (Pubitemid 46199284)
43. Ottmann C, Weyand M, Sassa T, Inoue T, Kato N, Wittinghofer A, &, Oecking C, (2009) A structural rationale for selective stabilization of anti-tumor interactions of 14-3-3 proteins by cotylenin A. J Mol Biol 386, 913-919.
44. Yang X, Lee WH, Sobott F, Papagrigoriou E, Robinson CV, Grossmann JG, Sundström M, Doyle DA, &, Elkins JM, (2006) Structural basis for protein-protein interactions in the 14-3-3 protein family. Proc Natl Acad Sci USA 103, 17237-17242. (Pubitemid 44788953)
45. Kabsch W, (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26, 795-800.
46. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, &, Read RJ, (2007) Phaser crystallographic software. J Appl Crystallogr 40, 658-674. (Pubitemid 47080256)
47. Emsley P, &, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132. (Pubitemid 41742764)
48. Murshudov GN, Vagin AA, &, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240-255. (Pubitemid 27235885)