Leukemia fusion target AF9 is an intrinsically disordered transcriptional regulator that recruits multiple partners via coupled folding and binding

Structure

Volumn 21, Issue 1, 2013, Pages 176-183

  Leach, Benjamin I ^a   Kuntimaddi, Aravinda ^a   Schmidt, Charles R ^a   Cierpicki, Tomasz ^a   Johnson, Stephanie A ^b   Bushweller, John H ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN; PROTEIN AF9; UNCLASSIFIED DRUG;

ACUTE LEUKEMIA; ARTICLE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; DNA-BINDING PROTEINS; FLUORESCENCE POLARIZATION; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY;

EID: 84872157616     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.11.011     Document Type: Article

References (38)

1. M.A. Andrade, P. Chacón, J.J. Merelo, and F. Morán Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network Protein Eng. 6 1993 383 390 (Pubitemid 23197398)
2. R.L. Baldwin, C. Frieden, and G.D. Rose Dry molten globule intermediates and the mechanism of protein unfolding Proteins 78 2010 2725 2737
3. J.I. Bárdos, A.J. Saurin, C. Tissot, E. Duprez, and P.S. Freemont HPC3 is a new human polycomb orthologue that interacts and associates with RING1 and Bmi1 and has transcriptional repression properties J. Biol. Chem. 275 2000 28785 28792
4. E. Bitoun, P.L. Oliver, and K.E. Davies The mixed-lineage leukemia fusion partner AF4 stimulates RNA polymerase II transcriptional elongation and mediates coordinated chromatin remodeling Hum. Mol. Genet. 16 2007 92 106 (Pubitemid 46152547)
5. A.N. Boettiger, and M. Levine Synchronous and stochastic patterns of gene activation in the Drosophila embryo Science 325 2009 471 473
6. V.S. Chopra, J.W. Hong, and M. Levine Regulation of Hox gene activity by transcriptional elongation in Drosophila Curr. Biol. 19 2009 688 693
7. R.N. De Guzman, M.A. Martinez-Yamout, H.J. Dyson, and P.E. Wright Interaction of the TAZ1 domain of the CREB-binding protein with the activation domain of CITED2: regulation by competition between intrinsically unstructured ligands for non-identical binding sites J. Biol. Chem. 279 2004 3042 3049 (Pubitemid 38114297)
8. S.J. Demarest, M. Martinez-Yamout, J. Chung, H. Chen, W. Xu, H.J. Dyson, R.M. Evans, and P.E. Wright Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators Nature 415 2002 549 553 (Pubitemid 34130612)
9. J.F. Dimartino, and M.L. Cleary Mll rearrangements in haematological malignancies: lessons from clinical and biological studies Br. J. Haematol. 106 1999 614 626 (Pubitemid 29434198)
10. Z. Dosztányi, V. Csizmok, P. Tompa, and I. Simon IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content Bioinformatics 21 2005 3433 3434 (Pubitemid 41222453)
11. F. Erfurth, C.S. Hemenway, A.C. de Erkenez, and P.H. Domer MLL fusion partners AF4 and AF9 interact at subnuclear foci Leukemia 18 2004 92 102 (Pubitemid 38159444)
12. S.M. Gagné, S. Tsuda, L. Spyracopoulos, L.E. Kay, and B.D. Sykes Backbone and methyl dynamics of the regulatory domain of troponin C: anisotropic rotational diffusion and contribution of conformational entropy to calcium affinity J. Mol. Biol. 278 1998 667 686 (Pubitemid 28224863)
13. M.G. Guenther, R.G. Jenner, B. Chevalier, T. Nakamura, C.M. Croce, E. Canaani, and R.A. Young Global and Hox-specific roles for the MLL1 methyltransferase Proc. Natl. Acad. Sci. USA 102 2005 8603 8608 (Pubitemid 40862782)
14. N. He, C.K. Chan, B. Sobhian, S. Chou, Y. Xue, M. Liu, T. Alber, M. Benkirane, and Q. Zhou Human Polymerase-Associated Factor complex (PAFc) connects the Super Elongation Complex (SEC) to RNA polymerase II on chromatin Proc. Natl. Acad. Sci. USA 108 2011 E636 E645
15. C.S. Hemenway, A.C. de Erkenez, and G.C. Gould The polycomb protein MPc3 interacts with AF9, an MLL fusion partner in t(9;11)(p22;q23) acute leukemias Oncogene 20 2001 3798 3805 (Pubitemid 32646190)
16. K.D. Huynh, W. Fischle, E. Verdin, and V.J. Bardwell BCoR, a novel corepressor involved in BCL-6 repression Genes Dev. 14 2000 1810 1823 (Pubitemid 30602999)
17. J.M. Kneller, M. Lu, and C. Bracken An effective method for the discrimination of motional anisotropy and chemical exchange J. Am. Chem. Soc. 124 2002 1852 1853 (Pubitemid 34215292)
18. C. Lin, E.R. Smith, H. Takahashi, K.C. Lai, S. Martin-Brown, L. Florens, M.P. Washburn, J.W. Conaway, R.C. Conaway, and A. Shilatifard AFF4, a component of the ELL/P-TEFb elongation complex and a shared subunit of MLL chimeras, can link transcription elongation to leukemia Mol. Cell 37 2010 429 437
19. N.F. Marshall, J. Peng, Z. Xie, and D.H. Price Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase J. Biol. Chem. 271 1996 27176 27183 (Pubitemid 26359140)
20. C. Meyer, E. Kowarz, J. Hofmann, A. Renneville, J. Zuna, J. Trka, R. Ben Abdelali, E. Macintyre, E. De Braekeleer, and M. De Braekeleer New insights to the MLL recombinome of acute leukemias Leukemia 23 2009 1490 1499
21. T.A. Milne, J. Kim, G.G. Wang, S.C. Stadler, V. Basrur, S.J. Whitcomb, Z. Wang, A.J. Ruthenburg, K.S. Elenitoba-Johnson, R.G. Roeder, and C.D. Allis Multiple interactions recruit MLL1 and MLL1 fusion proteins to the HOXA9 locus in leukemogenesis Mol. Cell 38 2010 853 863
22. G. Mitterbauer, C. Zimmer, C. Fonatsch, O. Haas, R. Thalhammer-Scherrer, I. Schwarzinger, P. Kalhs, U. Jaeger, K. Lechner, and C. Mannhalter Monitoring of minimal residual leukemia in patients with MLL-AF9 positive acute myeloid leukemia by RT-PCR Leukemia 13 1999 1519 1524 (Pubitemid 29465613)
23. M. Mohan, H.M. Herz, Y.H. Takahashi, C. Lin, K.C. Lai, Y. Zhang, M.P. Washburn, L. Florens, and A. Shilatifard Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom) Genes Dev. 24 2010 574 589
24. A.G. Muntean, J. Tan, K. Sitwala, Y. Huang, J. Bronstein, J.A. Connelly, V. Basrur, K.S. Elenitoba-Johnson, and J.L. Hess The PAF complex synergizes with MLL fusion proteins at HOX loci to promote leukemogenesis Cancer Cell 17 2010 609 621
25. T. O'Brien, S. Hardin, A. Greenleaf, and J.T. Lis Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation Nature 370 1994 75 77 (Pubitemid 24216957)
26. C.M. Palermo, C.A. Bennett, A.C. Winters, and C.S. Hemenway The AF4-mimetic peptide, PFWT, induces necrotic cell death in MV4-11 leukemia cells Leuk. Res. 32 2008 633 642 (Pubitemid 351248957)
27. B.W. Pontius Close encounters: why unstructured, polymeric domains can increase rates of specific macromolecular association Trends Biochem. Sci. 18 1993 181 186 (Pubitemid 23142574)
28. R. Prasad, T. Yano, C. Sorio, T. Nakamura, R. Rallapalli, Y. Gu, D. Leshkowitz, C.M. Croce, and E. Canaani Domains with transcriptional regulatory activity within the ALL1 and AF4 proteins involved in acute leukemia Proc. Natl. Acad. Sci. USA 92 1995 12160 12164 (Pubitemid 26014030)
29. B.A. Shoemaker, J.J. Portman, and P.G. Wolynes Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl. Acad. Sci. USA 97 2000 8868 8873 (Pubitemid 30626639)
30. R.S. Spolar, and M.T. Record Jr. Coupling of local folding to site-specific binding of proteins to DNA Science 263 1994 777 784 (Pubitemid 24093205)
31. R.S. Srinivasan, A.C. de Erkenez, and C.S. Hemenway The mixed lineage leukemia fusion partner AF9 binds specific isoforms of the BCL-6 corepressor Oncogene 22 2003 3395 3406 (Pubitemid 36713736)
32. R.S. Srinivasan, J.B. Nesbit, L. Marrero, F. Erfurth, V.F. LaRussa, and C.S. Hemenway The synthetic peptide PFWT disrupts AF4-AF9 protein complexes and induces apoptosis in t(4;11) leukemia cells Leukemia 18 2004 1364 1372 (Pubitemid 39136746)
33. D.J. Steger, M.I. Lefterova, L. Ying, A.J. Stonestrom, M. Schupp, D. Zhuo, A.L. Vakoc, J.E. Kim, J. Chen, and M.A. Lazar DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells Mol. Cell. Biol. 28 2008 2825 2839 (Pubitemid 351542379)
34. P. Tompa, and M. Fuxreiter Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions Trends Biochem. Sci. 33 2008 2 8
35. S. Veiksina, S. Kopanchuk, and A. Rinken Fluorescence anisotropy assay for pharmacological characterization of ligand binding dynamics to melanocortin 4 receptors Anal. Biochem. 402 2010 32 39
36. A. Yokoyama, M. Lin, A. Naresh, I. Kitabayashi, and M.L. Cleary A higher-order complex containing AF4 and ENL family proteins with P-TEFb facilitates oncogenic and physiologic MLL-dependent transcription Cancer Cell 17 2010 198 212
37. W. Zhang, X. Xia, M.R. Reisenauer, C.S. Hemenway, and B.C. Kone Dot1a-AF9 complex mediates histone H3 Lys-79 hypermethylation and repression of ENaCα in an aldosterone-sensitive manner J. Biol. Chem. 281 2006 18059 18068 (Pubitemid 44035606)
38. K.L. Zobeck, M.S. Buckley, W.R. Zipfel, and J.T. Lis Recruitment timing and dynamics of transcription factors at the Hsp70 loci in living cells Mol. Cell 40 2010 965 975