Competing allosteric mechanisms modulate substrate binding in a dimeric enzyme

Nature Structural and Molecular Biology

Volumn 18, Issue 3, 2011, Pages 288-294

  Freiburger, Lee A ^a   Baettig, Oliver M ^a   Sprules, Tara ^b   Berghuis, Albert M ^a   Auclair, Karine ^a   Mittermaier, Anthony K ^a  

^a MCGILL UNIVERSITY   (Canada)

^b Quebec/Eastern Canada High Field NMR Facility   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; ACYLTRANSFERASE; AMINOGLYCOSIDE N (6') ACETYLTRANSFERASE II; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; ENZYME BINDING; ENZYME SUBSTRATE COMPLEX; ISOTHERMAL TITRATION CALORIMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; THERMODYNAMICS;

ACETYL COENZYME A; ACETYLTRANSFERASES; ALLOSTERIC REGULATION; CALORIMETRY; CIRCULAR DICHROISM; ENTEROCOCCUS FAECIUM; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 79952361572     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1978     Document Type: Article

References (51)

1. Perutz, M.F. Mechanisms of cooperativity and allosteric regulation in proteins. Q. Rev. Biophys. 22, 139-237 (1989).
2. Monod, J., Wyman, J. & Changeux, J.P. On nature of allosteric transitions-a plausible model. J. Mol. Biol. 12, 88-118 (1965).
3. Fenton, A.W. Allostery: an illustrated defnition for the 'second secret of life'. Trends Biochem. Sci. 33, 420-425 (2008).
4. DeDecker, B.S. Allosteric drugs: thinking outside the active-site box. Chem. Biol. 7, R103-R107 (2000). (Pubitemid 30319698)
5. Koshland, D.E., Nemethy, G. & Filmer, D. Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385 (1966).
6. Perutz, M.F., Wilkinson, A.J., Paoli, M. & Dodson, G.G. The stereochemical mechanism of the cooperative effects in hemoglobin revisited. Annu. Rev. Biophys. Biomol. Struct. 27, 1-34 (1998). (Pubitemid 28286007)
7. Helmstaedt, K., Krappmann, S. & Braus, G.H. Allosteric regulation of catalytic activity: Escherichia coli aspartate transcarbamoylase versus yeast chorismate mutase. Microbiol. Mol. Biol. Rev. 65, 404-421 (2001). (Pubitemid 32881713)
8. Cui, Q. & Karplus, M. Allostery and cooperativity revisited. Protein Sci. 17, 1295-1307 (2008).
9. Kern, D. & Zuiderweg, E.R.P. The role of dynamics in allosteric regulation. Curr. Opin. Struct. Biol. 13, 748-757 (2003). (Pubitemid 37522151)
10. Hilser, V.J. & Thompson, E.B. Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins. Proc. Natl. Acad. Sci. USA 104, 8311-8315 (2007). (Pubitemid 47175484)
11. Reichheld, S.E., Yu, Z. & Davidson, A.R. The induction of folding cooperativity by ligand binding drives the allosteric response of tetracycline repressor. Proc. Natl. Acad. Sci. USA 106, 22263-22268 (2009).
12. Popovych, N., Sun, S.J., Ebright, R.H. & Kalodimos, C.G. Dynamically driven protein allostery. Nat. Struct. Mol. Biol. 13, 831-838 (2006). (Pubitemid 44338778)
13. Cooper, A. & Dryden, D.T.F. Allostery without conformational change-a plausible model. Eur. Biophys. J. 11, 103-109 (1984).
14. Tzeng, S.R. & Kalodimos, C.G. Dynamic activation of an allosteric regulatory protein. Nature 462, 368-372 (2009).
15. Gandhi, P.S., Chen, Z.W., Mathews, F.S. & Di Cera, E. Structural identifcation of the pathway of long-range communication in an allosteric enzyme. Proc. Natl. Acad. Sci. USA 105, 1832-1837 (2008). (Pubitemid 351439425)
16. Lockless, S.W. & Ranganathan, R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286, 295-299 (1999). (Pubitemid 29484693)
17. Tsai, C.J., Kumar, S., Ma, B.Y. & Nussinov, R. Folding funnels, binding funnels, and protein function. Protein Sci. 8, 1181-1190 (1999). (Pubitemid 29264948)
18. Tsai, C.J., Ma, B.Y. & Nussinov, R. Folding and binding cascades: shifts in energy landscapes. Proc. Natl. Acad. Sci. USA 96, 9970-9972 (1999). (Pubitemid 29422488)
19. Kumar, S., Ma, B.Y., Tsai, C.J., Sinha, N. & Nussinov, R. Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci. 9, 10-19 (2000). (Pubitemid 30070934)
20. Pan, H., Lee, J.C. & Hilser, V.J. Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble. Proc. Natl. Acad. Sci. USA 97, 12020-12025 (2000).
21. Volkman, B.F., Lipson, D., Wemmer, D.E. & Kern, D. Two-state allosteric behavior in a single-domain signaling protein. Science 291, 2429-2433 (2001). (Pubitemid 32231808)
22. Gunasekaran, K., Ma, B.Y. & Nussinov, R. Is allostery an intrinsic property of all dynamic proteins? Proteins 57, 433-443 (2004). (Pubitemid 39390799)
23. Clarkson, M.W., Gilmore, S.A., Edgell, M.H. & Lee, A.L. Dynamic coupling and allosteric behavior in a nonallosteric protein. Biochemistry 45, 7693-7699 (2006). (Pubitemid 44185485)
24. Wright, G.D. & Ladak, P. Overexpression and characterization of the chromosomal aminoglycoside 6′-N-acetyltransferase from Enterococcus faecium. Antimicrob. Agents Chemother. 41, 956-960 (1997). (Pubitemid 27194167)
25. Burk, D.L., Xiong, B., Breitbach, C. & Berghuis, A.M. Structures of aminoglycoside acetyltransferase AAC(6′)-Ii in a novel crystal form: structural and normal-mode analyses. Acta Crystallogr. D Biol. Crystallogr. 61, 1273-1279 (2005). (Pubitemid 43961298)
26. Wybenga-Groot, L.E., Draker, K.-A., Wright, G.D. & Berghuis, A.M. Crystal structure of an aminoglycoside 6′-N-acetyltransferase: defning the GCN5-related N-acetyltransferase superfamily fold. Structure 7, 497-507 (1999). (Pubitemid 29230484)
27. Burk, D.L., Ghuman, N., Wybenga-Groot, L.E. & Berghuis, A.M. X-ray structure of the AAC(6′)-Ii antibiotic resistance enzyme at 1.8 angstrom resolution; examination of oligomeric arrangements in GNAT superfamily members. Protein Sci. 12, 426-437 (2003). (Pubitemid 36241102)
28. Gao, F., Yan, X.X., Baettig, O.M., Berghuis, A.M. & Auclair, K. Regio- and chemoselective 6′-N-derivatization of aminoglycosides: bisubstrate inhibitors as probes to study aminoglycoside 6′-N- acetyltransferases. Angew. Chem. Int. Edn Engl. 44, 6859-6862 (2005). (Pubitemid 41546528)
29. Freiburger, L.A., Auclair, K. & Mittermaier, A.K. Elucidating protein binding mechanisms by variable-c ITC. ChemBioChem 10, 2871-2873 (2009).
30. 0 generated by a shift in equilibrium between macrostates of an enzyme. Nature 292, 271-272 (1981). (Pubitemid 11001852)
31. 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). (Pubitemid 40247713)
32. Keramisanou, D. et al. Disorder-order folding transitions underlie catalysis in the helicase motor of SecA. Nat. Struct. Mol. Biol. 13, 594-602 (2006). (Pubitemid 44036469)
33. Adler, A.J., Greenfeld, N.J. & Fasman, G.D. Circular dichroism and optical rotatory dispersion of proteins and polypeptides. Methods Enzymol. 27, 675-735 (1973).
34. Saxena, V.P. & Wetlaufer, D.B. A New Basis for interpreting circular dichroic spectra of proteins. Proc. Natl. Acad. Sci. USA 68, 969-972 (1971).
35. Uversky, V.N. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11, 739-756 (2002). (Pubitemid 34241284)
36. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. J. Biomol. NMR 4, 727-734 (1994).
37. Farmer, B.T. Localizing the NADP(+) binding site on the MurB enzyme by NMR. Nat. Struct. Biol. 3, 995-997 (1996). (Pubitemid 27014626)
38. Koshland, D.E. Application of a theory of enzyme specifcity to protein synthesis. Proc. Natl. Acad. Sci. USA 44, 98-104 (1958).
39. Foote, J. & Milstein, C. Conformational isomerism and the diversity of antibodies. Proc. Natl. Acad. Sci. USA 91, 10370-10374 (1994). (Pubitemid 24328998)
40. Boehr, D.D., Nussinov, R. & Wright, P.E. The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796 (2009).
41. Koshland, D.E. & Hamadani, K. Proteomics and models for enzyme cooperativity. J. Biol. Chem. 277, 46841-46844 (2002). (Pubitemid 36159184)
42. Bosshard, H.R. Molecular recognition by induced ft: how ft is the concept? News Physiol. Sci. 16, 171-173 (2001). (Pubitemid 33713265)
43. Hammes, G.G., Chang, Y.C. & Oas, T.G. Conformational selection or induced ft: a fux description of reaction mechanism. Proc. Natl. Acad. Sci. USA 106, 13737-13741 (2009).
44. Weikl, T.R. & von Deuster, C. Selected-ft versus induced-ft protein binding: kinetic differences and mutational analysis. Proteins 75, 104-110 (2009).
45. Radley, T.L., Markowska, A.I., Bettinger, B.T., Ha, J.H. & Loh, S.N. Allosteric switching by mutually exclusive folding of protein domains. J. Mol. Biol. 332, 529-536 (2003). (Pubitemid 37075979)
46. Laine, O., Streaker, E.D., Nabavi, M., Fenselau, C.C. & Beckett, D. Allosteric signaling in the biotin repressor occurs via local folding coupled to global dampening of protein dynamics. J. Mol. Biol. 381, 89-101 (2008).
47. Ehlert, F.J. Estimation of the affnities of allosteric ligands using radioligand binding and pharmacological null methods. Mol. Pharmacol. 33, 187-194 (1988).
48. Marley, J., Lu, M. & Bracken, C. A method for effcient isotopic labeling of recombinant proteins. J. Biomol. NMR 20, 71-75 (2001). (Pubitemid 32519656)
49. Cavanagh, J., Fairbrother, W., Palmer, A. & Skelton, N. Protein NMR Spectroscopy Principles and Practice (Academic Press, Inc., 1996).
50. Kay, L.E., Keifer, P. & Saarinen, T. Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665 (1992).
51. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).