A dynamic model of long-range conformational adaptations triggered by nucleotide binding in GroEL-GroES

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 10, 2012, Pages 2333-2346

  Skjaerven, Lars ^a,b   Muga, Arturo ^c   Reuter, Nathalie ^a,b   Martinez, Aurora ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b Uni Research AS   (Norway)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Accessible conformational space; Allostery; Chaperonin; Molecular dynamics simulations; Pre existing conformers; Principal component analysis

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN; NUCLEOTIDE; OLIGOMER;

ADAPTATION; ALLOSTERISM; ARTICLE; ESCHERICHIA COLI; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; SIMULATION;

ADENOSINE TRIPHOSPHATE; CHAPERONIN 10; CHAPERONIN 60; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MOLECULAR DYNAMICS SIMULATION; MUTATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84865965918     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24113     Document Type: Article

References (61)

1. Kerner MJ, Naylor DJ, Ishihama Y, Maier T, Chang H-C, Stines AP, Georgopoulos C, Frishman D, Hayer-Hartl M, Mann M, Hartl FU. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 2005; 122: 209-220.
2. Horwich AL, Fenton WA. Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding. Q Rev Biophys 2009; 42: 83-116.
3. Yébenes H, Mesa P, Muñoz IG, Montoya G, Valpuesta JM. Chaperonins: two rings for folding. Trends Biochem Sci 2011; 36: 424-432.
4. Horwich AL, Farr GW, Fenton WA. GroEL-GroES-mediated protein folding. Chem Rev 2006; 106: 1917-1930.
5. Xu Z, Horwich AL, Sigler PB. The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 1997; 388: 741-750.
6. Rye HS, Roseman AM, Chen S, Furtak K, Fenton WA, Saibil HR, Horwich AL. GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell 1999; 97: 325-338.
7. Ranson NA, Farr GW, Roseman AM, Gowen B, Fenton WA, Horwich AL, Saibil HR. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 2001; 107: 869-879.
8. Fridmann Y, Kafri G, Danziger O, Horovitz A. Dissociation of the GroEL-GroES asymmetric complex is accelerated by increased cooperativity in ATP binding to the GroEL ring distal to GroES. Biochemistry 2002; 41: 5938-5944.
9. Rye HS, Burston SG, Fenton WA, Beechem JM, Xu Z, Sigler PB, Horwich AL. Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 1997; 388: 792-798.
10. Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 1994; 371: 578-586.
11. Chaudhry C, Horwich AL, Brunger AT, Adams PD. Exploring the structural dynamics of the E. coli chaperonin GroEL using translation-libration-screw crystallographic refinement of intermediate states. J Mol Biol 2004; 342: 229-245.
12. Ranson NA, Clare DK, Farr GW, Houldershaw D, Horwich AL, Saibil HR. Allosteric signaling of ATP hydrolysis in GroEL-GroES complexes. Nat Struct Mol Biol 2006; 13: 147-152.
13. Yifrach O, Horovitz A. Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 1995; 34: 5303-5308.
14. Boisvert DC, Wang J, Otwinowski Z, Horwich AL, Sigler PB. The 2.4 Å crystal structure of the bacterial chaperonin GroEL complexed with ATP gamma S. Nat Struct Biol 1996; 3: 170-177.
15. Chaudhry C, Farr G, Todd M, Rye H, Brunger A, ADAMS P, Horwich A, Sigler P. Role of the gamma-phosphate of ATP in triggering protein folding by GroEL-GroES: function, structure and energetics. EMBO J 2003; 22: 4877-4887.
16. Wang J, Boisvert DC. Structural basis for GroEL-assisted protein folding from the crystal structure of (GroEL-KMgATP)14 at 2.0A resolution. J Mol Biol 2003; 327: 843-855.
17. del Sol A, Tsai C-J, Ma B, Nussinov R. The origin of allosteric functional modulation: multiple pre-existing pathways. Structure 2009; 17: 1042-1050.
18. Kern D, Zuiderweg ERP. The role of dynamics in allosteric regulation. Curr Opin Struct Biol 2003; 13: 748-757.
19. Karplus M, Kuriyan J. Molecular dynamics and protein function. Proc Natl Acad Sci USA 2005; 102: 6679-6685.
20. Karplus M, McCammon JA. Molecular dynamics simulations of biomolecules. Nat Struct Biol 2002; 9: 646-652.
21. Ma J, Sigler PB, Xu Z, Karplus M. A dynamic model for the allosteric mechanism of GroEL. J Mol Biol 2000; 302: 303-313.
22. Sliozberg Y, Abrams CF. Spontaneous conformational changes in the E. coli GroEL subunit from all-atom molecular dynamics simulations. Biophys J 2007; 93: 1906-1916.
23. Skjaerven L, Grant B, Muga A, Teigen K, McCammon JA, Reuter N, Martinez A. Conformational sampling and nucleotide-dependent transitions of the GroEL subunit probed by unbiased molecular dynamics simulations. PLoS Comput Biol 2011; 7: e1002004.
24. Case D, Darden T, Cheatham T, III, Simmerling C, Wang J, Duke R, Luo R, Crowley M, Walker RC, Zhang W, Merz K, B Wang, Hayik S, Roitberg A, Seabra G, Kolossváry I, KF Wong, Paesani F, Vanicek J, Wu X, Brozell S, Steinbrecher T, Gohlke H, Yang L, Tan C, Mongan J, Hornak V, Cui G, Mathews D, Seetin M, Sagui C, Babin V, Kollman P. Amber 10. San Francisco: University of California; 2008.
25. Duan Y, Wu C, Chowdhury S, Lee M, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 2003; 24: 1999-2012.
26. Lee M, Duan Y. Distinguish protein decoys by using a scoring function based on a new AMBER force field, short molecular dynamics simulations, and the generalized born solvent model. Proteins 2004; 55: 620-634.
27. Bartolucci C, Lamba D, Grazulis S, Manakova E, Heumann H. Crystal structure of wild-type chaperonin GroEL. J Mol Biol 2005; 354: 940-951.
28. Cabo-Bilbao A, Mechaly A, Agirre J, Spinelli S, Sot B, Muga A, Guerin DMA. Crystal structure of the allosteric-defective chaperonin GroELE434K mutant. J Biophys Struct Biol 2011; 3: 66-71.
29. Meagher K, Redman L, Carlson H. Development of polyphosphate parameters for use with the AMBER force field. J Comput Chem 2003; 24: 1016-1025.
30. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 1993; 234: 779-815.
31. Berman H, Battistuz T, Bhat T, Bluhm W, Bourne P, Burkhardt K, Iype L, Jain S, Fagan P, Marvin J, Padilla D, Ravichandran V, Schneider B, Thanki N, Weissig H, Westbrook J, Zardecki C. The protein data bank. Acta Crystallogr D 2002; 58: 899-907.
32. Grant BJ, Rodrigues APC, ElSawy KM, McCammon JA, Caves LSD. Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 2006; 22: 2695-2696.
33. Kollman P, Massova I, Reyes C, Kuhn B, Huo S, Chong L, Lee M, Lee T, Duan Y, Wang W, Donini O, Cieplak P, Srinivasan J, Case D, Cheatham T. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 2000; 33: 889-897.
34. Gohlke H, Case DA. Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf. J Comput Chem 2004; 25: 238-250.
35. Onufriev A, Bashford D, Case D. Modification of the generalized Born model suitable for macromolecules. J Phys Chem B 2000; 104: 3712-3720.
36. Onufriev A, Bashford D, Case D. Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins 2004; 55: 383-394.
37. Gohlke H, Kiel C, Case DA. Insights into protein-protein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RalGDS complexes. J Mol Biol 2003; 330: 891-913.
38. DeLano W. The PyMOL molecular graphics system. Schrödinger: LLC; 2010.
39. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996; 14: 27-38.
40. Frauenfelder H, Parak F, Young RD. Conformational substates in proteins. Annu Rev Biophys Biophys Chem 1988; 17: 451-479.
41. Gunasekaran K, Ma B, Nussinov R. Is allostery an intrinsic property of all dynamic proteins? Proteins 2004; 57: 433-443.
42. Wang J, Chen L. Domain motions in GroEL upon binding of an oligopeptide. J Mol Biol 2003; 334: 489-499.
43. Teilum K, Olsen JG, Kragelund BB. Functional aspects of protein flexibility. Cell Mol Life Sci 2009; 66: 2231-2247.
44. Grant BJ, Gorfe AA, McCammon JA. Ras conformational switching: simulating nucleotide-dependent conformational transitions with accelerated molecular dynamics. PLoS Comput Biol 2009; 5: e1000325.
45. Henzler-Wildman KA, Thai V, Lei M, Ott M, Wolf-Watz M, Fenn T, Pozharski E, Wilson MA, Petsko GA, Karplus M, Hübner CG, Kern D. Intrinsic motions along an enzymatic reaction trajectory. Nature 2007; 450: 838-844.
46. Li W, Wolynes PG, Takada S. Frustration, specific sequence dependence, and nonlinearity in large-amplitude fluctuations of allosteric proteins. Proc Natl Acad Sci USA 2011; 108: 3504-3509.
47. Skjærven L, Reuter N, Martinez A. Dynamics, flexibility and ligand-induced conformational changes in biological macromolecules: a computational approach. Future Med Chem 2011; 3: 2079-2100.
48. Henzler-Wildman K, Kern D. Dynamic personalities of proteins. Nature 2007; 450: 964-972.
49. Hub JS, Kubitzki MB, de Groot BL. Spontaneous quaternary and tertiary T-R transitions of human hemoglobin in molecular dynamics simulation. PLoS Computat Biol 2010; 6: e1000774.
50. Frank GA, Goomanovsky M, Davidi A, Ziv G, Horovitz A, Haran G. Out-of-equilibrium conformational cycling of GroEL under saturating ATP concentrations. Proc Natl Acad Sci USA 2010; 107: 6270-6274.
51. Sot B, Banuelos S, Valpuesta J, Muga A. GroEL stability and function-contribution of the ionic interactions at the inter-ring contact sites. J Biol Chem 2003; 278: 32083-32090.
52. Sot B, Galan A, Valpuesta J, Bertrand S, Muga A. Salt bridges at the inter-ring interface regulate the thermostat of GroEL. J Biol Chem 2002; 277: 34024-34029.
53. Cabo-Bilbao A, Spinelli S, Sot B, Agirre J, Mechaly AE, Muga A, Guérin DMA. Crystal structure of the temperature-sensitive and allosteric-defective chaperonin GroELE461K. J Struct Biol 2006; 155: 482-492.
54. Sewell BT, Best RB, Chen S, Roseman AM, Farr GW, Horwich AL, Saibil HR. A mutant chaperonin with rearranged inter-ring electrostatic contacts and temperature-sensitive dissociation. Nat Struct Mol Biol 2004; 11: 1128-1133.
55. Ma J, Karplus M. The allosteric mechanism of the chaperonin GroEL: a dynamic analysis. Proc Natl Acad Sci USA 1998; 95: 8502-8507.
56. Yifrach O, Horovitz A. Mapping the transition state of the allosteric pathway of GroEL by protein engineering. J Am Chem Soc 1998; 120: 13262-13263.
57. Skjaerven L, Martinez A, Reuter N. Principal component and normal mode analysis of proteins: a quantitative comparison using the GroEL subunit. Proteins 2011; 79: 232-243.
58. Buckle AM, Zahn R, Fersht AR. A structural model for GroEL-polypeptide recognition. Proc Natl Acad Sci USA 1997; 94: 3571-3575.
59. Kovalenko O, Yifrach O, Horovitz A. Residue lysine-34 in GroES modulates allosteric transitions in GroEL. Biochemistry 1994; 33: 14974-14978.
60. van der Vaart A, Ma J, Karplus M. The unfolding action of GroEL on a protein substrate. Biophys J 2004; 87: 562-573.
61. Hyeon C, Lorimer GH, Thirumalai D. Dynamics of allosteric transitions in GroEL. Proc Natl Acad Sci USA 2006; 103: 18939-18944.