Allostery Wiring Diagrams in the Transitions that Drive the GroEL Reaction Cycle

Journal of Molecular Biology

Volumn 387, Issue 2, 2009, Pages 390-406

  Tehver, Riina ^a   Chen, Jie ^a   Thirumalai, D ^a  

^a Bldg 142   (United States)

Author keywords

allostery wiring diagram; chaperonin GroEL; evolutionary imprints; functional residues; structural perturbation method

Indexed keywords

CHAPERONIN; PROTEIN GROEL; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

ESCHERICHIA COLI;

EID: 61649124866     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.12.032     Document Type: Article

References (53)

1. Xu Z., Horwich A.L., and Sigler P.B. The crystal structure of the asymmetric GroES(ADP)7 chaperonin complex. Nature 388 (1997) 741-750
2. Boyer P.D. The ATP synthase-a splendid molecular machine. Annu. Rev. Biochem. 66 (1997) 717-749
3. Vale R.D., and Milligan R.A. The way things move: looking under the hood of molecular motors. Science 288 (2000) 88-95
4. Houdusse A., and Sweeney H.L. Myosin motors: missing structures and hidden springs. Curr. Opin. Struct. Biol. 11 (2001) 182-194
5. Zheng W., Brooks B.R., and Thirumalai D. Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proc. Natl Acad. Sci. USA 103 (2006) 7664-7669
6. Zheng W., Brooks B.R., Doniach S., and Thirumalai D. Network of dynamically important residues in the open/closed transition in polymerases is strongly conserved. Structure 13 (2005) 565-577
7. Lockless S.W., and Ranganathan R. Evolutionary conserved pathways of energetic connectivity in protein families. Science 286 (1999) 295-299
8. Dima R., and Thirumalai D. Determination of network of residues that regulate allostery in protein families using sequence analysis. Protein Sci. 15 (2006) 258-268
9. Levitt M., Sander C., and Stern P.S. Normal-mode dynamics of a protein: bovine pancreatic trypsin inhibitor. Int. J. Quant. Chem. 10 (1983) 181-199
10. Go N. Theoretical-studies of protein folding. Annu. Rev. Biophys. Bioeng. 12 (1983) 183-210
11. Ma J. Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Structure 13 (2003) 373-380
12. Bahar I., and Rader A.J. Coarse-grained normal mode analysis in structural biology. Curr. Opin. Struct. Biol. 388 (2005) 586-592
13. Maragakis P., and Karplus M. Large amplitude conformational change in proteins explored with a plastic network model: adenylate kinase. J. Mol. Biol. 352 (2005) 807-822
14. Rader A.J., Chennubhotla C., Yang L.W., and Bahar I. The Gaussian network model: theory and applications. In: Cui Q., and Bahar I. (Eds). Normal Mode Analysis. Theory and Applications to Biological and Chemical Systems (2006), Chapman & Hall CRC Press, Chicago, IL 41-64
15. Sanejouand Y.H. Functional information from slow mode shapes. In: Cui Q., and Bahar I. (Eds). Normal Mode Analysis. Theory and Applications to Biological and Chemical Systems (2006), Chapman & Hall CRC Press, Chicago, IL 91-109
16. Tama F., and Brooks III C.L. Symmetry, form, and shape: Guiding principles for robustness in macromolecular machines. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 115-133
17. Schröder G.F., Brunger A.T., and Levitt M. Combining efficient conformational sampling with a deformable elastic network model facilitates structure refinement at low resolution. Structure 15 (2007) 1630-1641
18. Hyeon C., Lorimer G.H., and Thirumalai D. Dynamics of allosteric transitions in GroEL. Proc. Natl Acad. Sci. USA 103 (2006) 18939-18944
19. Tirion M.M. Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys. Rev. Lett. 77 (1996) 1905-1908
20. Buchete N.V., Straub J.E., and Thirumalai D. Development of novel statistical potentials for protein fold recognition. Curr. Opin. Struct. Biol. 14 (2004) 225-232
21. Cheung M.S., Klimov D., and Thirumalai D. Molecular crowding enhances native state stability and refolding rates. Proc. Natl Acad. Sci. USA 102 (2005) 4753-4758
22. Klimov D.K., and Thirumalai D. Mechanisms and kinetics of β-hairpin formation. Proc. Natl Acad. Sci. USA 97 (2000) 2544-2549
23. Betancourt M.R., and Thirumalai D. Pair potentials for protein folding: choice of reference states and sensitivity of predicted motive states to variations in the interaction schemes. Protein Sci. 8 (1999) 361-389
24. Xu Z., and Sigler P.B. GroEL/GroES: structure and function of a two-stroke folding machine. J. Struct. Biol. 124 (1998) 129-141
25. Thirumalai D., and Lorimer G.H. Chaperonin-mediated protein folding. Annu. Rev. Biophys. Biomol. Struct. 30 (2001) 245-269
26. Horwich A.L., Farr G.W., and Fenton W.A. GroEL-GroES-mediated protein folding. Chem. Rev. 106 (2006) 1917-1930
27. Lin Z., Madan D., and Rye H.S. GroEL stimulates protein folding through forced unfolding. Nat. Struct. Mol. Biol. 15 (2008) 303-311
28. Zheng W., Brooks B.R., and Thirumalai D. Allosteric transitions in the chaperonin GroEL are captured by a dominant normal mode that is most robust to sequence variations. Biophys. J. 93 (2007) 2289-2299
29. Keskin O., Bahar I., Flatow D., Covell D.G., and Jernigan R.L. Molecular mechanisms of chaperonin GroEL-GroES function. Biochemistry 42 (2002) 491-501
30. Ma J., and Karplus M. The allosteric mechanism of the chaperonin GroEL: a dynamic analysis. Proc. Natl Acad. Sci. USA 95 (1998) 8502-8507
31. Grason J., Gresham J., and Lorimer G. Setting the chaperonin timer: a two-stroke, two-speed, protein machine. Proc. Natl Acad. Sci. USA 105 (2008) 17339-17344
32. Braig K., Otwinowski Z., Hegde R., Boisvert D.C., Joachimiak A., Horwich A.L., and Sigler P.B. The crystal structure of the bacterial chaperonin GroEL at 2.8 Ǻ. Nature 371 (1994) 578-586
33. Ranson N.A., Farr G.W., Roseman A.M., Gowen B., Fenton W.A., Horwich A.L., and Saibil H.R. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107 (2001) 869-879
34. Betancourt M.R., and Thirumalai D. Exploring the kinetic requirements for enhancement of protein folding rates in the GroEL cavity. J. Mol. Biol. 287 (1999) 627-644
35. Yang, Y. (2006). Site-directed mutagenesis of GroEL: developing a system for monitoring allosteric movements by flourescence resonance energy transfer. Master's thesis, University of Maryland, College Park, MD.
36. Murai N., Makino Y., and Yoshida M. GroEL locked in a closed conformation by an interdomain cross-link can bind ATP and polypeptide but cannot process further reaction steps. J. Biol. Chem. 271 (1996) 28229-28234
37. Kass I., and Horovitz A.L. Mapping pathways of allosteric communication in GroEL by analysis of correlated mutations. Proteins 48 (2002) 611-617
38. Brocchieri L., and Karlin S. Conservation among HSP60 sequences in relation to structure, function, and evolution. Protein Sci. 9 (2000) 476-486
39. Stan G., Thirumalai D., Lorimer G.H., and Brooks B.R. Annealing function of GroEL: structural and bioinformatic analysis. Biophys. Chem. 100 (2003) 453-467
40. Klein G., and Georgopoulos C. Identification of important amino acid residues that modulate binding of Escherichia coli GroEL to its various cochaperones. Genetics 158 (2001) 507-517
41. Fenton W.A., Kashi Y., Furtak K., and Horwich A.L. Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371 (1994) 614-619
42. Stan G., Brooks B.R., Lorimer G.H., and Thirumalai D. Identifying natural substrates for chaperonins using a sequence-based approach. Protein Sci. 14 (2005) 193-201
43. Aharoni A., and Horovitz A. Inter-ring communication is disrupted in the GroEL mutant Arg13 Gly:Ala126 Val with known crystal structure. J. Mol. Biol. 258 (1996) 732-735
44. Danziger O., Shimon L., and Horovitz A. Glu257 in GroEL is a sensor involved in coupling polypeptide substrate binding to stimulation of ATP hydrolysis. Protein Sci. 15 (2006) 1270-1276
45. Yifrach O., and Horovitz A. Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34 (1994) 5303-5308
46. Chennubhotla C., Yang Z., and Bahar I. Coupling between global dynamics and signal transduction pathways: a mechanism of allostery for chaperonin GroEL. Mol. BioSyst. 4 (2008) 287-292
47. Chennubhotla C., and Bahar I. Markov propagation of allosteric effects in biomolecular systems: application to GroEL-GroES. Mol. Syst. Biol. 2 (2006) 36
48. Suel G.M., Lockless S.W., Wall M.A., and Ranganathan R.I. Evolutionary conserved networks of residues mediate allosteric communication in proteins. Nat. Struct. Biol. 10 (2003) 59-68
49. Buckle A.M., Zahn R., and Fersht A.R. A structural model for GroEL-polypeptide recognition. Proc. Natl Acad. Sci. USA 94 (1997) 3571-3575
50. Chen L.L., and Sigler P.B. The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell 99 (1999) 757-768
51. Bochkareva E.S., Horovitz A., and Girshovich A.S. Direct demonstration that ATP is in contact with Cys-137 in chaperonin GroEL. J. Biol. Chem. 269 (1994) 44-46
52. Zheng W., and Doniach S. A comparative study of motor-protein motions by using a simple elastic-network model. Proc. Natl Acad. Sci. USA 100 (2003) 13253-13258
53. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680