Structure of nucleophosmin DNA-binding domain and analysis of its complex with a G-quadruplex sequence from the c-MYC promoter

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 26539-26548

  Gallo, Angelo ^a   Lo Sterzo, Carlo ^b   Mori, Mirko ^a   Di Matteo, Adele ^b   Bertini, Ivano ^a   Banci, Lucia ^a   Brunori, Maurizio ^b   Federici, Luca ^c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF CHIETI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE MYELOID LEUKEMIA; C-TERMINAL DOMAINS; CELLULAR FUNCTION; CONTACT SURFACE; DNA-BINDING DOMAIN; G-QUADRUPLEX STRUCTURE; G-QUADRUPLEXES; GENE PROMOTER; HIGH AFFINITY; MOLECULAR DOCKING; NMR ANALYSIS; NUCLEAR EXPORT SIGNALS; NUCLEO-CYTOPLASMIC SHUTTLING; NUCLEOPHOSMIN; PHOSPHATE BACKBONE; SOLUTION STRUCTURES; STRESS STIMULUS;

AMINO ACIDS; CYTOLOGY; NUCLEAR MAGNETIC RESONANCE;

GENES;

GUANINE QUADRUPLEX; MYC PROTEIN; NUCLEOPHOSMIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA HELIX; DNA PROTEIN COMPLEX; HUMAN; MOLECULAR DOCKING; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; RESIDUE ANALYSIS; STATIC ELECTRICITY;

BASE SEQUENCE; BINDING SITES; DNA; G-QUADRUPLEXES; GENES, MYC; HUMANS; MODELS, MOLECULAR; NUCLEAR PROTEINS; OLIGODEOXYRIBONUCLEOTIDES; PROMOTER REGIONS, GENETIC;

EID: 84864565959     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.371013     Document Type: Article

References (53)

1. Grisendi, S., Mecucci, C., Falini, B., and Pandolfi, P. P. (2006) Nucleophosmin and cancer. Nat. Rev. Cancer 6, 493-505 (Pubitemid 43980539)
2. Falini, B., Sportoletti, P., and Martelli, M. P. (2009) Acute myeloid leukemia with mutated NPM1: diagnosis, prognosis and therapeutic perspectives. Curr. Opin. Oncol. 21, 573-581
3. Falini, B., Gionfriddo, I., Cecchetti, F., Ballanti, S., Pettirossi, V., and Martelli, M. P. (2011) Acute myeloid leukemia with mutated nucleophosmin (NPM1): any hope for a targeted therapy? Blood Rev. 25, 247-254
4. Falini, B., Mecucci, C., Tiacci, E., Alcalay, M., Rosati, R., Pasqualucci, L., La Starza, R., Diverio, D., Colombo, E., Santucci, A., Bigerna, B., Pacini, R., Pucciarini, A., Liso, A., Vignetti, M., Fazi, P., Meani, N., Pettirossi, V., Saglio, G., Mandelli, F., Lo-Coco, F., Pelicci, P. G., and Martelli, M. F.; GIMEMA Acute Leukemia Working Party (2005) Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N. Engl. J. Med. 352, 254-266 (Pubitemid 40110814)
5. Grummitt, C. G., Townsley, F. M., Johnson, C. M., Warren, A. J., and Bycroft, M. (2008) Structural consequences of nucleophosmin mutations in acute myeloid leukemia. J. Biol. Chem. 283, 23326-23332
6. Scaloni, F., Gianni, S., Federici, L., Falini, B., and Brunori, M. (2009) Folding mechanism of the C-terminal domain of nucleophosmin: residual structure in the denatured state and its pathophysiological significance. FASEB J. 23, 2360-2365
7. Scaloni, F., Federici, L., Brunori, M., and Gianni, S. (2010) Deciphering the folding transition state structure and denatured state properties of nucleophosmin C-terminal domain. Proc. Natl. Acad. Sci. U.S.A. 107, 5447-5452
8. Hingorani, K., Szebeni, A., and Olson, M. O. (2000) Mapping the functional domains of nucleolar protein B23. J. Biol. Chem. 275, 24451-24457 (Pubitemid 30626537)
9. Lindström, M. S. (2011) NPM1/B23: a multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochem. Res. Int. 2011, 195209
10. Xu, Y., Fang, F., Dhar, S. K., St Clair, W. H., Kasarskis, E. J., and St Clair, D. K. (2007) The role of a single-stranded nucleotide loop in transcriptional regulation of the human sod2 gene. J. Biol. Chem. 282, 15981-15994 (Pubitemid 47100336)
11. Federici, L., Arcovito, A., Scaglione, G. L., Scaloni, F., Lo Sterzo, C., Di Matteo, A., Falini, B., Giardina, B., and Brunori, M. (2010) Nucleophosmin C-terminal leukemia-associated domain interacts with G-rich quadruplex forming DNA. J. Biol. Chem. 285, 37138-37149
12. Huppert, J. L., and Balasubramanian, S. (2005) Prevalence of quadruplexes at the human genome. Nucleic Acids Res. 33, 2908-2916
13. Huppert, J. L. (2008) Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes. Chem. Soc. Rev. 37, 1375-1384
14. Qin, Y., and Hurley, L. H. (2008) Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions. Biochimie 90, 1149-1171
15. Siddiqui-Jain, A., Grand, C. L., Bearss, D. J., and Hurley, L. H. (2002) Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc. Natl. Acad. Sci. U.S.A. 99, 11593-11598 (Pubitemid 34994444)
16. Grand, C. L., Han, H., Muñoz, R.M., Weitman, S., Von Hoff, D. D., Hurley, L. H., and Bearss, D. J. (2002) The cationic porphyrin TMPyP4 downregulates c-MYC and human telomerase reverse transcriptase expression and inhibits tumor growth in vivo. Mol. Cancer Ther. 1, 565-573
17. Brown, R. V., Danford, F. L., Gokhale, V., Hurley, L. H., and Brooks, T. A. (2011) Demonstration that drug-targeted downregulation of MYC in non-Hodgkins lymphoma is directly mediated through the promoter G-quadruplex. J. Biol. Chem. 286, 41018-41027
18. González, V., Guo, K., Hurley, L., and Sun, D. (2009) Identification and characterization of nucleolin as a c-myc G-quadruplex-binding protein. J. Biol. Chem. 284, 23622-23635
19. González, V., and Hurley, L. H. (2010) The cMYC NHEIII (1): function and regulation. Annu. Rev. Pharmacol. Toxicol. 50, 111-129
20. Thakur, R. K., Kumar, P., Halder, K., Verma, A., Kar, A., Parent, J. L., Basundra, R., Kumar, A., and Chowdhury, S. (2009) Metastases suppressor NM23-H2 interaction with G-quadruplex DNA within c-MYC promoter nuclease hypersensitive element induces c-MYC expression. Nucleic Acids Res. 37, 172-183
21. Neidle, S. (2009) The structures of quadruplex nucleic acids and their drug complexes. Curr. Opin. Struct. Biol. 19, 239-250
22. Sissi, C., Gatto, B., and Palumbo, M. (2011) The evolving world of protein-G-quadruplex recognition: a medicinal chemist's perspective. Biochimie 93, 1219-1230
23. Padmanabhan, K., Padmanabhan, K. P., Ferrara, J. D., Sadler, J. E., and Tulinsky, A. (1993) The structure of α-thrombin inhibited by a 15-mer single-stranded DNA aptamer. J. Biol. Chem. 268, 17651-17654 (Pubitemid 23260263)
24. Horvath, M. P., and Schultz, S. C. (2001) DNA G-quartets in a 1.86 Åresolution structure of an Oxytricha nova telomeric protein-DNA complex. J. Mol. Biol. 310, 367-377 (Pubitemid 32664874)
25. Keller, R. (2004) The Computer Aided Resonance Assignment Tutorial, CANTINA Verlag, Goldau, Switzerland
26. Herrmann, T., Güntert, P., and Wüthrich, K. (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR 24, 171-189 (Pubitemid 36113646)
27. Herrmann, T., Güntert, P., and Wüthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319, 209-227 (Pubitemid 34729497)
28. Güntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378
29. 13C chemical shift index: a simple method for the identification of protein secondary structure using 13C chemical shift data. J. Biomol. NMR 4, 171-180
30. Eghbalnia, H. R., Wang, L., Bahrami, A., Assadi, A., and Markley, J. L. (2005) Protein energetic conformational analysis from NMR chemical shifts (PECAN) and its use in determining secondary structural elements. J. Biomol. NMR 32, 71-81 (Pubitemid 41086469)
31. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR 44, 213-223
32. Bertini, I., Case, D. A., Ferella, L., Giachetti, A., and Rosato, A. (2011) A grid-enabled web portal for NMR structure refinement with AMBER. Bioinformatics 27, 2384-2390
33. Case, D. A., Darden, T. A., Cheatham, T. E., 3rd, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Goetz, A. W., Kolossvai, I., Wong, K. F., Paesani, F., Vanicek, J., Wolf, R. M., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M. J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Salomon-Ferrer, R., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2010) AMBER 11, University of California, San Francisco
34. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)
35. Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52-56, 29
36. Zwahlen, C., Legault, P., Vincent, S. J., Greenblatt, J., Konrat, R., and Kay, L. E. (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage N-peptide/boxB RNA complex. J. Am. Chem. Soc. 119, 6711-6721 (Pubitemid 27343493)
37. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125, 1731-1737 (Pubitemid 36232568)
38. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
39. Linge, J. P., O'Donoghue, S. I., and Nilges, M. (2001) Automated assignment of ambiguous nuclear Overhauser effects with ARIA. Methods Enzymol. 339, 71-90 (Pubitemid 32666557)
40. Linge, J. P., Habeck, M., Rieping, W., and Nilges, M. (2003) ARIA: automated NOE assignment and NMR structure calculation. Bioinformatics 19, 315-316 (Pubitemid 36181930)
41. de Vries, S. J., van Dijk, M., and Bonvin, A. M. (2010) The HADDOCK web server for data-driven biomolecular docking. Nat. Protoc. 5, 883-897
42. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D., and Kay, L. E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33, 5984-6003 (Pubitemid 24184605)
43. 15N NMR spectroscopy. Eur. J. Biochem. 219, 887-896
44. Phan, A. T., Kuryavyi, V., Gaw, H. Y., and Patel, D. J. (2005) Small-molecule interaction with a five-guanine-tract G-quadruplex structure from the human MYC promoter. Nat. Chem. Biol. 1, 167-173
45. Palaniswamy, V., Moraes, K. C., Wilusz, C. J., and Wilusz, J. (2006) Nucleophosmin is selectively deposited on mRNA during polyadenylation. Nat. Struct. Mol. Biol. 13, 429-435 (Pubitemid 43881583)
46. Shandilya, J., Swaminathan, V., Gadad, S. S., Choudhari, R., Kodaganur, G. S., and Kundu, T. K. (2009) Acetylated NPM1 localizes in the nucleoplasm and regulates transcriptional activation of genes implicated in oral cancer manifestation. Mol. Cell. Biol. 29, 5115-5127
47. Wulff, J. E., Siegrist, R., and Myers, A. G. (2007) The natural product avrainvillamide binds to the oncoprotein nucleophosmin. J. Am. Chem. Soc. 129, 14444-14451 (Pubitemid 350171471)
48. Zor, T., Mayr, B. M., Dyson, H. J., Montminy, M. R., and Wright, P. E. (2002) Roles of phosphorylation and helix propensity in the binding of the KIX domain of CREB-binding protein by constitutive (c-Myb) and inducible (CREB) activators. J. Biol. Chem. 277, 42241-42248 (Pubitemid 35257544)
49. Selenko, P., Gregorovic, G., Sprangers, R., Stier, G., Rhani, Z., Krämer, A., and Sattler, M. (2003) Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Mol. Cell 11, 965-976 (Pubitemid 36566318)
50. Tompa, P., and Fuxreiter, M. (2008) Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem. Sci. 33, 2-8
51. Guo, X., Bulyk, M. L., and Hartemink, A. J. (2012) Intrinsic disorder within and flanking the DNA-binding domains of human transcription factors. Pac. Symp. Biocomput. 2012, 104-115
52. Beckmann, R., Buchner, K., Jungblut, P. R., Eckerskorn, C., Weise, C., Hilbert, R., and Hucho, F. (1992) Nuclear substrates of protein kinase C. Eur. J. Biochem. 210, 45-51
53. Okuwaki, M., Tsujimoto, M., and Nagata, K. (2002) The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype. Mol. Biol. Cell 13, 2016-2030 (Pubitemid 34651489)