A Mutation in the S-switch Region of the Runt Domain Alters the Dynamics of an Allosteric Network Responsible for CBFβ Regulation

Journal of Molecular Biology

Volumn 364, Issue 5, 2006, Pages 1073-1083

  Li, Zhe ^a   Lukasik, Steven M ^b   Liu, Yizhou ^b   Grembecka, Jolanta ^b   Bielnicka, Izabela ^b   Bushweller, John H ^b   Speck, Nancy A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

allostery; AML1; CBF ; NMR; RUNX

Indexed keywords

CORE BINDING FACTOR; CORE BINDING FACTOR BETA; UNCLASSIFIED DRUG;

ALLOSTERISM; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; DNA BINDING; MOLECULAR DYNAMICS; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; SCREENING; TRANSCRIPTION REGULATION; WILD TYPE;

MAMMALIA;

EID: 33751107244     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.002     Document Type: Article

References (55)

1. Hammes G.G. Multiple conformational changes in enzyme catalysis. Biochemistry 41 (2002) 8221-8228
2. Kern D., and Zuiderweg E.R. The role of dynamics in allosteric regulation. Curr. Opin. Struct. Biol. 13 (2003) 748-757
3. Popovych N., Sun S., Ebright R.H., and Kalodimos C.G. Dynamically driven protein allostery. Nature Struct. Mol. Biol. 13 (2006) 831-838
4. Wang C., Karpowich N., Hunt J.F., Rance M., and Palmer A.G. Dynamics of ATP-binding cassette contribute to allosteric control, nucleotide binding and energy transduction in ABC transporters. J. Mol. Biol. 342 (2004) 525-537
5. Volkman B.F., Lipson D., Wemmer D.E., and Kern D. Two-state allosteric behavior in a single-domain signaling protein. Science 291 (2001) 2429-2433
6. Eisenmesser E.Z., Bosco D.A., Akke M., and Kern D. Enzyme dynamics during catalysis. Science 295 (2002) 1520-1523
7. Hawkins R.J., McLeish T.C., Ebright R.H., and Kalodimos C.G. Coupling of global and local vibrational modes in dynamic allostery of proteins. Biophys. J. 91 (2006) 2055-2062
8. Clarkson M.W., Gilmore S.A., Edgell M.H., and Lee A.L. Dynamic coupling and allosteric behavior in a nonallosteric protein. Biochemistry 45 (2006) 7693-7699
9. Lu J., Cistola D.P., and Li E. Analysis of ligand binding and protein dynamics of human retinoid X receptor alpha ligand-binding domain by nuclear magnetic resonance. Biochemistry 45 (2006) 1629-1639
10. Igumenova T.I., Lee A.L., and Wand A.J. Backbone and side chain dynamics of mutant calmodulin-peptide complexes. Biochemistry 44 (2005) 12627-12639
11. McElroy C., Manfredo A., Wendt A., Gollnick P., and Foster M. TROSY-NMR studies of the 91 kDa TRAP protein reveal allosteric control of a gene regulatory protein by ligand-altered flexibility. J. Mol. Biol. 323 (2002) 463-473
12. Howlett G.J., Blackburn M.N., Compton J.G., and Schachman H.K. Allosteric regulation of aspartate transcarbamoylase. Analysis of the structural and functional behavior in terms of a two-state model. Biochemistry 16 (1977) 5091-5100
13. Hammes G.G., and Wu C.W. Kinetics of allosteric enzymes. Annu. Rev. Biophys. Bioeng. 3 (1974) 1-33
14. Sakash J.B., and Kantrowitz E.R. The contribution of individual interchain interactions to the stabilization of the T and R states of Escherichia coli aspartate transcarbamoylase. J. Biol. Chem. 275 (2000) 28701-28707
15. Chan R.S., Sakash J.B., Macol C.P., West J.M., Tsuruta H., and Kantrowitz E.R. The role of intersubunit interactions for the stabilization of the T state of Escherichia coli aspartate transcarbamoylase. J. Biol. Chem. 277 (2002) 49755-49760
16. Lipscomb W.N. Aspartate transcarbamylase from Escherichia coli: activity and regulation. Advan. Enzymol. Relat. Areas Mol. Biol. 68 (1994) 67-151
17. Ito Y. Oncogenic potential of the RUNX gene family: 'overview'. Oncogene 23 (2004) 4198-4208
18. Sasaki K., Yagi H., Bronson R.T., Tominaga K., Matsunashi T., Deguchi K., et al. Absence of fetal liver hematopoiesis in mice deficient in transcriptional coactivator core binding factor beta. Proc. Natl Acad. Sci. USA 93 (1996) 12359-12363
19. Wang Q., Stacy T., Miller J.D., Lewis A.F., Huang X., Bories J.-C., et al. The CBFβ subunit is essential for CBFα2 (AML1) function in vivo. Cell 87 (1996) 697-708
20. Miller J., Horner A., Stacy T., Lowrey C., Lian J.B., Stein G., et al. The core-binding factor β subunit is required for bone formation and hematopoietic maturation. Nature Genet. 32 (2002) 645-649
21. Yoshida C.A., Furuichi T., Fujita T., Fukuyama R., Kanatani N., Kobayashi S., et al. Core-binding factor β interacts with Runx2 and is required for skeletal development. Nature Genet. 32 (2002) 633-638
22. Kundu M., Javed A., Jeon J.-P., Horner A., Shum L., Eckhaus M., et al. The hematopoietic transcription factor, Cbfβ, interacts with Cbfa1 and plays a critical role in bone developent. Nature Genet. 32 (2002) 639-644
23. Nagata T., Gupta V., Sorce D., Kim W.-Y., Sali A., Chait B.T., et al. Immunoglobulin motif DNA-binding and heterodimerization for the PEBP2/CBF Runt-domain. Nature Struct. Biol. 6 (1999) 615-619
24. Berardi M., Sun C., Zehr M., Abildgaard F., Peng J., Speck N.A., and Bushweller J.H. The Ig fold of the core binding factor α Runt domain is a member of a family of structurally and functionally related Ig fold DNA binding domains. Struct. Fold. Des. 7 (1999) 1247-1256
25. Tahirov T.H., Inoue-Bungo T., Morii H., Fujikawa A., Sasaki M., Kimura K., et al. Structural analyses of DNA recognition by the AML1/Runx-1 Runt domain and its allosteric control by CBFβ. Cell 104 (2001) 755-767
26. Bravo J., Li Z., Speck N.A., and Warren A.J. The leukaemia-associated AML1 (Runx1)-CBFβ complex functions as a DNA-induced molecular clamp. Nature Struct. Biol. 8 (2001) 371-377
27. Kamachi Y., Ogawa E., Asano M., Ishida S., Murakami Y., Satake M., et al. Purification of a mouse nuclear factor that binds to both the A and B cores of the polyomavirus enhancer. J. Virol. 64 (1990) 4808-4819
28. Wang S., Wang Q., Crute B.E., Melnikova I.N., Keller S.R., and Speck N.A. Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol. Cell. Biol. 13 (1993) 3324-3339
29. Tang Y.-Y., Shi J., Zhang L., Davis A., Bravo J., Warren A.J., et al. Energetic and functional contribution of residues in the core binding factor β (CBFβ) subunit to heterodimerization with CBFα. J. Biol. Chem. 275 (2000) 39579-39588
30. Tang Y.-Y., Crute B.E., Kelley III J.J., Huang X., Yan J., Shi J., et al. Biophysical characterization of interactions between the core-binding factor α and β subunits and DNA. FEBS Letters 470 (2000) 167-172
31. Gu T.-L., Goetz T.L., Graves B.J., and Speck N.A. Autoinhibition and partner proteins, CBFβ and Ets-1, modulate DNA binding by CBFα2(AML1). Mol. Cell. Biol. 20 (2000) 91-103
32. Kanno T., Kanno Y., Chen L.-F., Ogawa E., Kim W.-Y., and Ito Y. Intrinsic transcriptional activation-inhibition domains of the polyomavirus enhancer binding protein 2/core binding factor α subunit revealed in the presence of the β subunit. Mol. Cell. Biol. 18 (1998) 2444-2454
33. Huang G., Shigesada K., Ito K., Wee H.J., Yokomizo T., and Ito Y. Dimerization with PEBP2β protects RUNX1/AML1 from ubiquitin-proteosome-mediated degradation. EMBO J. 15 (2001) 723-733
34. Bartfeld D., Shimon L., Couture G.C., Rabinovich D., Frolow F., Levanon D., et al. DNA recognition by the RUNX1 transcription factor is mediated by an allosteric transition in the RUNT domain and by DNA bending. Structure 10 (2002) 1395-1407
35. Bäckström S., Wolf-Watz M., Grundström C., Härd T., Grundström T., and Sauer U.H. The RUNX1 Runt domain at 1.25 Å resolution: a structural switch and specifically bound chloride ions modulate DNA binding. J. Mol. Biol. 322 (2002) 259-272
36. Warren A.J., Bravo J., Williams R.L., and Rabbitts T.H. Structural basis for the heterodimeric interaction between the acute leukaemia-associated transcription factors AML1 and CBFβ. EMBO J. 19 (2000) 3004-3115
37. Yan J., Liu Y., Lukasik S.M., Speck N.A., and Bushweller J.H. CBFbeta allosterically regulates the Runx1 Runt domain via a dynamic conformational equilibrium. Nature Struct. Mol. Biol. 11 (2004) 901-906
38. Lewis A.F., Stacy T., Green W., Taddesse-Heath L., Hartley J.W., and Speck N.A. Core-binding factor influences the disease specificity of Moloney murine leukemia virus. J. Virol. 73 (1999) 5535-5547
39. Kneller J.M., Lu M., and Bracken C. An effective method for the discrimination of motional anisotropy and chemical exchange. J. Am. Chem. Soc. 124 (2002) 1852-1853
40. Rennert J., Coffman J.A., Mushegian A.R., and Robertson A.J. The evolution of Runx genes I. A comparative study of sequences from phylogenetically diverse model organisms. BMC Evol. Biol. 3 (2003) 4
41. Freire E. Can allosteric regulation be predicted from structure?. Proc. Natl Acad. Sci. USA 97 (2000) 11680-11682
42. Pan H., Lee J.C., and Hilser V.J. Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble. Proc. Natl Acad. Sci. USA 97 (2000) 12020-12025
43. Li Z., Yan J., Matheny C.J., Corpora T., Bravo J., Warren A.J., et al. Energetic contribution of residues in the Runx1 Runt domain to DNA binding. J. Biol. Chem. 278 (2003) 33088-33096
44. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
45. Navaza J. Amore-An automated package for molecular replacement. Acta Crystallog. sect. A 50 (1994) 157-163
46. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
47. Bailey S. The Cdp4 suite-Programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
48. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
49. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., et al. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
50. 15N spin relaxation studies of protein mobility. Biochemistry 36 (1997) 7305-7312
51. Kamath U., and Shriver J.W. Characterization of thermotropic state changes in myosin subfragment-1 and heavy meromyosin by UV difference spectroscopy. J. Biol. Chem. 264 (1989) 5586-5592
52. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 104 (1982) 4546-4559
53. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 104 (1982) 4559-4570
54. Clore G.M., Szabo A., Bax A., Kay L.E., Driscoll P.C., and Gronenborn A.M. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-5 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 112 (1990) 144-163
55. Mandel A.M., Akke M., and Palmer III A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246 (1995) 144-163