Overlap between folding and functional energy landscapes for adenylate kinase conformational change

Nature Communications

Volumn 1, Issue 8, 2010, Pages

  Olsson, Ulrika ^a   Wolf Watz, Magnus ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME CONFORMATION; ENZYME STRUCTURE; PROTEIN FOLDING; PROTEIN FUNCTION;

ESCHERICHIA COLI;

EID: 78650049311     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1106     Document Type: Article

References (45)

1. Ogawa, A. et al. Structure of the carboxyl-terminal Src kinase, Csk. J. Biol. Chem. 277, 14351-14354 (2002).
2. Debondt, H. L. et al. Crystal-structure of cyclin-dependent kinase-2. Nature 363, 595-602 (1993).
3. Vonrhein, C., Schlauderer, G. J. & Schulz, G. E. Movie of the structural changes during a catalytic cycle of nucleoside monophosphate kinases. Structure 3, 483-490 (1995).
4. Ikura, M. et al. Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science 256, 632-638 (1992).
5. Leopold, P. E., Montal, M. & Onuchic, J. N. Protein folding funnels: A kinetic approach to the sequence-structure relationship. Proc. Natl Acad. Sci. USA 89, 8721-8725 (1992).
6. Frauenfelder, H., Sligar, S. G. & Wolynes, P. G. The energy landscapes and motions of proteins. Science 254, 1598-1603 (1991).
7. del Sol, A., Tsai, C. J., Ma, B. Y. & Nussinov, R. The origin of allosteric functional modulation: Multiple pre-existing pathways. Structure 17, 1042-1050 (2009).
8. Gerstein, M., Lesk, A. M. & Chothia, C. Structural mechanisms for domain movements in proteins. Biochemistry 33, 6739-6749 (1994).
9. Noda, L. Adenylate kinase. in The Enzymes (ed. Boyer, P. D.) 279-305 (VIII, Academic Press, 1973).
10. Rhoads, D. G. & Lowenstein, J. M. Initial velocity and equilibrium kinetics of myokinase. J. Biol. Chem. 243, 3963-3972 (1968).
11. Sheng, X. R., Li, X. & Pan, X. M. An iso-random Bi Bi mechanism for adenylate kinase. J. Biol. Chem. 274, 22238-22242 (1999).
12. Abele, U. & Schulz, G. E. High-resolution structures of adenylate kinase from yeast ligated with inhibitor Ap5A, showing the pathway of phosphoryl transfer. Protein Sci. 4, 1262-1271 (1995).
13. Müller, C. W., Schlauderer, G. J., Reinstein, J. & Schulz, G. E. Adenylate kinase motions during catalysis: An energetic counterweight balancing substrate binding. Structure 4, 147-156 (1996).
14. Lienhard, G. E. & Secemski, I. I. P 1,P 5-Di(adenosine-5') pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J. Biol. Chem. 248, 1121-1123 (1973).
15. Müller, C. W. & Schulz, G. E. Structure of the complex between adenylate kinase from Escherichia coli and the inhibitor Ap5A refined at 1.9 Å resolution. A model for a catalytic transition state. J. Mol. Biol. 224, 159-177 (1992).
16. Ådén, J. & Wolf-Watz, M. NMR identification of transient complexes critical to adenylate kinase catalysis. J. Am. Chem. Soc. 129, 14003-14012 (2007).
17. Rundqvist, L. et al. Noncooperative folding of subdomains in adenylate kinase. Biochemistry 48, 1911-1927 (2009).
18. Schrank, T. P., Bolen, D. W. & Hilser, V. J. Rational modulation of conformational fluctuations in adenylate kinase reveals a local unfolding mechanism for allostery and functional adaptation in proteins. Proc. Natl Acad. Sci. USA 106, 16984-16989 (2009).
19. Wolf-Watz, M. et al. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nat. Struct. Mol. Biol. 11, 945-949 (2004).
20. Henzler-Wildman, K. A. et al. Intrinsic motions along an enzymatic reaction trajectory. Nature 450, 838-844 (2007).
21. Boehr, D. D., McElheny, D., Dyson, H. J. & Wright, P. E. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313, 1638-1642 (2006).
22. Eisenmesser, E. Z. et al. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438, 117-121 (2005).
23. Beach, H., Cole, R., Gill, M. L. & Loria, J. P. Conservation of mus-ms enzyme motions in the apo- and substrate-mimicked state. J. Am. Chem. Soc. 127, 9167-9176 (2005).
24. Gerstein, M., Schulz, G. & Chothia, C. Domain closure in adenylate kinase. Joints on either side of two helices close like neighboring fingers. J. Mol. Biol. 229, 494-501 (1993).
25. Miyashita, O., Onuchic, J. N. & Wolynes, P. G. Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc. Natl Acad. Sci. USA 100, 12570-12575 (2003).
26. Whitford, P. C., Miyashita, O., Levy, Y. & Onuchic, J. N. Conformational transitions of adenylate kinase: Switching by cracking. J. Mol. Biol. 366, 1661-1671 (2007).
27. Henzler-Wildman, K. A. et al. A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450, 913-916 (2007).
28. Monnot, M. et al. Circular dichroism investigation of Escherichia coli adenylate kinase. J. Biol. Chem. 262, 2502-2506 (1987).
29. Sanders, C. R. II, Tian, G. C. & Tsai, M. D. Mechanism of adenylate kinase. Is there a relationship between local substrate dynamics, local binding energy, and the catalytic mechanism? Biochemistry 28, 9028-9043 (1989).
30. Reinstein, J. et al. Fluorescence and NMR investigations on the ligand binding properties of adenylate kinases. Biochemistry 29, 7440-7450 (1990).
31. McElroy, C. A., Manfredo, A., Gollnick, P. & Foster, M. P. Thermodynamics of tryptophan-mediated activation of the trp RNA-binding attenuation protein. Biochemistry 45, 7844-7853 (2006).
32. Krishnamurthy, H., Munro, K., Yan, H. & Vieille, C. Dynamics in Thermotoga neapolitana adenylate kinase: 15N relaxation and hydrogen-deuterium exchange studies of a hyperthermophilic enzyme highly active at 30 degrees C. Biochemistry 48, 2723-2739 (2009).
33. Bryngelson, J. D. & Wolynes, P. G. Spin glasses and the statistical mechanics of protein folding. Proc. Natl Acad. Sci. USA 84, 7524-7528 (1987).
34. Berger, C., Jelesarov, I. & Bosshard, H. R. Coupled folding and site-specific binding of the GCN4-bZIP transcription factor to the AP-1 and ATF/CREB DNA sites studied by microcalorimetry. Biochemistry 35, 14984-14991 (1996).
35. Keramisanou, D. et al. Disorder-order folding transitions underlie catalysis in the helicase motor of SecA. Nat. Struct. Mol. Biol. 13, 594-602 (2006).
36. Cliff, M. J., Williams, M. A., Brooke-Smith, J., Barford, D. & Ladbury, J. E. Molecular recognition via coupled folding and binding in a TPR domain. J. Mol. Biol. 346, 717-732 (2005).
37. Radhakrishnan, I. et al. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: A model for activator:coactivator interactions. Cell 91, 741-752 (1997).
38. Jackson, S. E. & Fersht, A. R. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30, 10428-10435 (1991).
39. Watters, A. L. et al. The highly cooperative folding of small naturally occurring proteins is likely the result of natural selection. Cell 128, 613-624 (2007).
40. Vuister, G. W. & Bax, A. Quantitative J correlation: A new approach for measuring homonuclear 3-bond J(H(N)H(alpha) coupling-constants in N-15-enriched proteins. J. Am. Chem. Soc. 115, 7772-7777 (1993).
41. Delaglio, F. et al. NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
42. Helgstrand, M., Kraulis, P., Allard, P. & Härd, T. Ansig for Windows: An interactive computer program for semiautomatic assignment of protein NMR spectra. J. Biomol. NMR 18, 329-336 (2000).
43. Shapiro, Y. E., Sinev, M. A., Sineva, E. V., Tugarinov, V. & Meirovitch, E. Backbone dynamics of Escherichia coli adenylate kinase at the extreme stages of the catalytic cycle studied by (15)N NMR relaxation. Biochemistry 39, 6634-6644 (2000).
44. Koradi, R., Billeter, M. & Wüthrich, K. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55, 29-32 (1996).
45. Schlauderer, G. J., Proba, K. & Schulz, G. E. Structure of a mutant adenylate kinase ligated with an ATP-analogue showing domain closure over ATP. J. Mol. Biol. 256, 223-227 (1996).(3)(3)