Dynamic activation of an allosteric regulatory protein

Nature

Volumn 462, Issue 7271, 2009, Pages 368-372

  Tzeng, Shiou Ru ^a,b   Kalodimos, Charalampos G ^a,b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP BINDING PROTEIN; DNA; NITROGEN 15; REGULATOR PROTEIN;

CALORIMETRY; CATALYSIS; DNA; GENETIC ENGINEERING; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN; THERMODYNAMICS;

ALLOSTERISM; ARTICLE; DNA BINDING; ESCHERICHIA COLI; ISOTHERMAL TITRATION CALORIMETRY; ISOTOPE LABELING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLASMID; PRIORITY JOURNAL; PROTEIN CONFORMATION; TEMPERATURE; THERMODYNAMICS; TRANSCRIPTION INITIATION;

CYCLIC AMP; CYCLIC AMP RECEPTOR PROTEIN; DNA; ENERGY METABOLISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 70450191983     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08560     Document Type: Article

References (53)

1. Kuriyan, J. & Eisenberg, D. The origin of protein interactions and allostery in colocalization. Nature 450, 983-990 (2007).
2. Goodey, N. M. & Benkovic, S. J. Allosteric regulation and catalysis emerge via a common route. Nature Chem. Biol. 4, 474-482 (2008).
3. Smock, R. G. & Gierasch, L. M. Sending signals dynamically. Science 324, 198-203 (2009).
4. del Sol, A., Tsai, C. J., Ma, B. & Nussinov, R. The origin of allosteric functional modulation: multiple pre-existing pathways. Structure 17, 1042-1050 (2009).
5. Lee, J. et al. Surface sites for engineering allosteric control in proteins. Science 322, 438-442 (2008).
6. Changeux, J. P. & Edelstein, S. J. Allosteric mechanisms of signal transduction. Science 308, 1424-1428 (2005).
7. Won, H. S., Lee, Y. S., Lee, S. H. & Lee, B. J. Structural overview on the allosteric activation of cyclic AMP receptor protein. Biochim. Biophys. Acta 1794, 1299-1308 (2009).
8. Schultz, S. C., Shields, G. C. & Steitz, T. A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science 253, 1001-1007 (1991).
9. Popovych, N., Tzeng, S. R., Tonelli, M., Ebright, R. H. & Kalodimos, C. G. Structural basis for cAMP-mediated allosteric control of the catabolite activator protein. Proc. Natl Acad. Sci. USA 106, 6927-6932 (2009).
10. Passner, J. M., Schultz, S. C. & Steitz, T. A. Modeling the cAMP-induced allosteric transition using the crystal structure of CAP-cAMP at 2.1 A resolution. J. Mol. Biol. 304, 847-859 (2000).
11. Berg, J. M., Tymoczko, J. L. & Stryer, L. Biochemistry 6th edn (Freeman, 2006).
12. Dai, J., Lin, S. H., Kemmis, C., Chin, A. J. & Lee, J. C. Interplay between site-specific mutations and cyclic nucleotides in modulating DNA recognition by Escherichia coli cyclic AMP receptor protein. Biochemistry 43, 8901-8910 (2004).
13. Baichoo, N. & Heyduk, T. Mapping conformational changes in a protein: application of a protein footprinting technique to cAMP-induced conformational changes in cAMP receptor protein. Biochemistry 36, 10830-10836 (1997).
14. Aiba, H., Nakamura, T., Mitani, H. & Mori, H. Mutations that alter the allosteric nature of cAMP receptor protein of Escherichia coli. EMBO J. 4, 3329-3332 (1985).
15. Mittermaier, A. & Kay, L. E. New tools provide new insights in NMR studies of protein dynamics. Science 312, 224-228 (2006).
16. Palmer, A. G. III. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 104, 3623-3640 (2004).
17. Kern, D. & Zuiderweg, E. R. The role of dynamics in allosteric regulation. Curr. Opin. Struct. Biol. 13, 748-757 (2003).
18. Akke, M., Bruschweiler, R. & Palmer, A. G. III. NMR order parameters and free energy: an analytical approach and its application to cooperative Ca21 binding by calbindin D9k. J. Am. Chem. Soc. 115, 9832-9833 (1993).
19. Yang, D. & Kay, L. E. Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: application to protein folding. J. Mol. Biol. 263, 369-382 (1996).
20. Cavanagh, J. & Akke, M. May the driving force be with you - whatever it is. Nature Struct. Biol. 7, 11-13 (2000).
21. Zhang, F. & Bruschweiler, R. Contact model for the prediction of NMR N-H order parameters in globular proteins. J. Am. Chem. Soc. 124, 12654-12655 (2002).
22. Kay, L. E., Muhandiram, D. R., Wolf, G., Shoelson, S. E. & Forman-Kay, J. D. Correlation between binding and dynamics at SH2 domain interfaces. Nature Struct. Biol. 5, 156-163 (1998).
23. Bracken, C., Carr, P. A., Cavanagh, J. & Palmer, A. G. III. Temperature dependence of intramolecular dynamics of the basic leucine zipper of GCN4: implications for the entropy of association with DNA. J. Mol. Biol. 285, 2133-2146 (1999).
24. Mauldin, R. V., Carroll, M. J. & Lee, A. L. Dynamic dysfunction in dihydrofolate reductase results from antifolate drug binding: modulation of dynamics within a structural state. Structure 17, 386-394 (2009).
25. Frederick, K. K., Marlow, M. S., Valentine, K. G. & Wand, A. J. Conformational entropy in molecular recognition by proteins. Nature 448, 325-329 (2007).
26. Popovych, N., Sun, S., Ebright, R. H. & Kalodimos, C. G. Dynamically driven protein allostery. Nature Struct. Mol. Biol. 13, 831-838 (2006).
27. MacRaild, C. A., Daranas, A. H., Bronowska, A. & Homans, S. W. Global changes in local protein dynamics reduce the entropic cost of carbohydrate binding in the arabinose-binding protein. J. Mol. Biol. 368, 822-832 (2007).
28. Kim, J., Adhya, S. & Garges, S. Allosteric changes in the cAMP receptor protein of Escherichia coli: hinge reorientation. Proc. Natl Acad. Sci. USA 89, 9700-9704 (1992).
29. Wand, A. J. Dynamic activation of protein function: a view emerging from NMR spectroscopy. Nature Struct. Biol. 8, 926-931 (2001).
30. Henzler-Wildman, K. & Kern, D. Dynamic personalities of proteins. Nature 450, 964-972 (2007).
31. Parkinson, G. et al. Structure of the CAP-DNA complex at 2.5 A resolution: a complete picture of the protein-DNA interface. J. Mol. Biol. 260, 395-408 (1996).
32. Takeuchi, K., Ng, E., Malia, T. J. & Wagner, G. 1-13C amino acid selective labeling in a 2H15N background for NMR studies of large proteins. J. Biomol. NMR 38, 89-98 (2007).
33. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
34. Johnson, B. A. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352 (2004).
35. Evenäs, J. et al. Ligand-induced structural changes to maltodextrin-binding protein as studied by solution NMR spectroscopy. J. Mol. Biol. 309, 961-974 (2001).
36. Palmer, A. G. III. ModelFree. Æhttp://www.palmer.hs.columbia.edu/ software/ modelfree.htmlæ.).
37. Cole, R. & Loria, J. P. FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data. J. Biomol. NMR 26, 203-213 (2003)
38. d'Auvergne, E. J. & Gooley, P. R. Optimisation of NMR dynamic models I. Minimisation algorithms and their performance within the model-free and Brownian rotational diffusion spaces. J. Biomol. NMR 40, 107-119 (2008).
39. Lipari, G. & 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, 4546-4559 (1982).
40. Tjandra, N., Feller, S. E., Pastor, R. W. & Bax, A. Rotational diffusion anisotropy of human ubiquitin from 15N NMR relaxation. J. Am. Chem. Soc. 117, 12562-12566 (1995).
41. Hwang, P. M., Skrynnikov, N. R. & Kay, L. E. Domain orientation in beta-cyclodextrin-loaded maltose binding protein: diffusion anisotropy measurements confirm the results of a dipolar coupling study. J. Biomol. NMR 20, 83-88 (2001).
42. Palmer, A. G. III. quadric-diffusion. Æhttp://www.palmer.hs. columbia.edu/ software/quadric.htmlæ.).
43. Dosset, P., Hus, J. C., Blackledge, M. & Marion, D. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR 16, 23-28 (2000).
44. Mandel, A. M., Akke, M. & Palmer, A. G. III. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246, 144-163 (1995).
45. Loria, J. P., Rance, M. & Palmer, A. G. III. A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J. Biomol. NMR 15, 151-155 (1999).
46. Mulder, F. A., Mittermaier, A., Hon, B., Dahlquist, F. W. & Kay, L. E. Studying excited states of proteins by NMR spectroscopy. Nature Struct. Biol. 8, 932-935 (2001).
47. Carver, J. P. & Richards, R. E. A general two-site solution for the chemical exchange produced dependence of T2 upon the Carr-Purcell pulse separation. J. Magn. Reson. 6, 89-105 (1972).
48. Watt, E. D., Shimada, H., Kovrigin, E. L. & Loria, J. P. The mechanism of rate-limiting motions in enzyme function. Proc. Natl Acad. Sci. USA 104, 11981-11986 (2007).
49. Henzler-Wildman, K. A. et al. Intrinsic motions along an enzymatic reaction trajectory. Nature 450, 838-844 (2007).
50. Boehr, D. D., McElheny, D., Dyson, H. J. & Wright, P. E. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313, 1638-1642 (2006).
51. Korzhnev, D. M. et al. Low-populated folding intermediates of Fyn SH3 characterized by relaxation dispersion NMR. Nature 430, 586-590 (2004).
52. Palmer, A. G. III. CPMGFit. Æhttp://www.cumc.columbia.edu/dept/ gsas/ biochem/labs/palmer/software/cpmgfit.htmlæ.).
53. Millet, O., Loria, J. P., Kroenke, C. D., Pons, M. & Palmer, A. G. The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122, 2867-2877 (2000).