Exploring the structural dynamics of the E. coli chaperonin GroEL using translation-libration-screw crystallographic refinement of intermediate states

Journal of Molecular Biology

Volumn 342, Issue 1, 2004, Pages 229-245

  Chaudhry, Charu ^a   Horwich, Arthur L ^a   Brunger, Axel T ^b   Adams, Paul D ^c  

^a YALE UNIVERSITY   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

chaperonin; crystallographic refinement; protein folding; structural dynamics; translation libration screw

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CHAPERONIN; NUCLEOTIDE;

ANISOTROPY; ARTICLE; ESCHERICHIA COLI; HYDROLYSIS KINETICS; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 4143061452     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.015     Document Type: Article

References (55)

1. W.A. Fenton, and A.L. Horwich Chaperonin-mediated protein folding: fate of substrate polypeptide Quart. Rev. Biophys. 36 2003 229 256
2. K. Braig, Z. Otwinowski, R. Hegde, D.C. Boisvert, A. Joachimiak, A.L. Horwich, and P.B. Sigler The crystal structure of the bacterial chaperonin GroEL at 2.8 Nature 371 1994 578 586
3. W.A. Fenton, Y. Kashi, K. Furtak, and A.L. Horwich Residues in chaperonin GroEL required for polypeptide binding and release Nature 371 1994 614 619
4. L.S. Itzhaki, D.E. Otzen, and A.R. Fersht Nature and consequences of GroEL-protein interactions Biochemistry 34 1995 14581 14587
5. Z. Lin, F.P. Schwartz, and E. Eisenstein The hydrophobic nature of GroEL-substrate binding J. Biol. Chem. 270 1995 1011 1014
6. A.M. Buckle, R. Zahn, and A.R. Fersht A structural model for GroEL-polypeptide recognition Proc. Natl Acad. Sci. USA 94 1997 3571 3575
7. L. Chen, and P.B. Sigler The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity Cell 99 1999 757 768
8. G.N. Chandrasekhar, K. Tilly, C. Woolford, R. Hendrix, and C. Georgopoulos Purification and properties of the groES morphogenetic protein of Escherichia coli J. Biol. Chem. 261 1986 12414 12419
9. T.E. Gray, and A.R. Fersht Cooperativity in ATP hydrolysis by GroEL is increased by GroES FEBS Letters 292 1991 254 258
10. G.S. Jackson, R.A. Staniforth, D.J. Halsall, T. Atkinson, J.J. Holbrook, A.R. Clarke, and S.G. Burston Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle: implications for the mechanism of assisted protein folding Biochemistry 32 1993 2554 2563
11. M.J. Todd, P.V. Viitanen, and G.H. Lorimer Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding Science 265 1994 659 666
12. J.F. Hunt, A.J. Weaver, S.J. Landry, L. Gierasch, and J. Deisenhofer The crystal structure of the GroES co-chaperonin at 2.8 resolution Nature 379 1996 37 45
13. A.M. Roseman, S. Chen, H. White, K. Braig, and H.R. Saibil The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL Cell 87 1996 241 251
14. Z. Xu, A.L. Horwich, and P.B. Sigler The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex Nature 388 1997 741 750
15. C. Chaudhry, G.W. Farr, M.J. Todd, H.S. Rye, A.T. Brunger, and P.D. Adams Role of the gamma-phosphate of ATP in triggering protein folding by GroEL-GroES: function, structure and energetics EMBO J. 22 2003 4877 4887
16. J.S. Weissman, C.M. Hohl, O. Kovalenko, Y. Kashi, S. Chen, and K. Braig Mechanism of GroEL action: productive release of polypeptide from a sequestered position under GroES Cell 83 1995 577 587
17. J.S. Weissman, H.S. Rye, W.A. Fenton, J.M. Beechem, and A.L. Horwich Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction Cell 84 1996 481 490
18. M. Mayhew, A.C. da Silva, J. Martin, H. Erdjument-Bromage, P. Tempst, and F.U. Hartl Protein folding in the central cavity of the GroEL-GroES chaperonin complex Nature 379 1996 420 426
19. H.S. Rye, S.G. Burston, W.A. Fenton, J.M. Beechem, Z. Xu, P.B. Sigler, and A.L. Horwich Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL Nature 388 1997 792 798
20. H.S. Rye, A.M. Roseman, S. Chen, K. Furtak, W.A. Fenton, H.R. Saibil, and A.L. Horwich GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings Cell 97 1999 325 338
21. O. Yifrach, and A. Horovitz Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL Biochemistry 34 1995 5303 5308
22. S.G. Burston, N.A. Ranson, and A.R. Clarke The origins and consequences of asymmetry in the chaperonin reaction cycle J. Mol. Biol. 249 1995 138 152
23. J. Ma, and M. Karplus The allosteric mechanism of the chaperonin GroEL: a dynamic analysis Proc. Natl Acad. Sci. USA 95 1998 8502 8507
24. J. Ma, P.B. Sigler, Z. Xu, and M. Karplus A dynamic model for the allosteric mechanism of GroEL J. Mol. Biol. 302 2000 303 313
25. V. Schomaker, and K.N. Trueblood On the rigid-body motion of molecules in crystals Acta Crystallog. sect. D 24 1968 63 76
26. R. Diamond On the use of normal modes in thermal parameter refinement: theory and application to the bovine pancreatic trypsin inhibitor Acta Crystallog. sect. A 46 1990 425 435
27. B. Howlin, D.D. Moss, and G.W. Harris Segmented anisotropic refinement of bovine ribonuclease A by the application of the rigid-body TLS model Acta Crystallog. sect. A 45 1989 851 861
28. T. Schwartz, J. Behlke, K. Lowenhaupt, U. Heinemann, and A. Rich Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins Nature Struct. Biol. 8 2001 761
29. M.Z. Papiz, S.M. Prince, T. Howard, R.J. Cogdell, and N.W. Isaacs The structure and thermal motion of the B800-850 LH2 complex from Rps. Acidophila at 2.0 resolution and 100K: new structural features and functionally relevant motions J. Mol. Biol. 326 2003 1523 1538
30. 2+-bound calmodulin: an analysis of disorder and implications for functionally relevant plasticity J. Mol. Biol. 301 2000 1237 1256
31. Y. Matoba, and M. Sugiyama Atomic resolution structure of prokaryotic phospholipase A2: analysis of internal motion and implication for a catalytic mechanism Proteins: Struct. Funct. Genet. 51 2003 453 469
32. K. Braig, P.D. Adams, and A.T. Brunger Conformational variability in the refined structure of the chaperonin GroEL at 2.8 A resolution Nature Struct. Biol. 2 1995 1083 1094
33. D.C. Boisvert, J. Wang, Z. Otwinowski, A.L. Horwich, and P.B. Sigler The 2.4 crystal structure of the bacterial chaperonin GroEL complexed with ATP gamma S Nature Struct. Biol. 3 1996 170 177
34. J. Wang, and D.C. Boisvert Structural basis of GroEL-assisted protein folding from the crystal structure of (GroEL-KMgATP)14 at 2.0 resolution J. Mol. Biol. 327 2003 843 855
35. N.A. Ranson, G.W. Farr, A.M. Roseman, B. Gowen, W.A. Fenton, A.L. Horwich, and H.R. Saibil ATP-bound states of GroEL captured by cryo-electron microscopy Cell 107 2001 869 879
36. R.E. Rosenfeld, K.N. Trueblood, and J.D. Dunitz A test for rigid-body vibrations based on a generalization of Hirshfeld's "rigid-bond" postulate Acta Crystallog. sect. A 34 1978 828 829
37. M. Levitt, C. Sander, and P.S. Stern Protein normal mode dynamics: trypsin inhibitor, crambin, ribonuclease and lysozyme J. Mol. Biol. 181 1985 423 447
38. J. Fiaux, E.B. Bertelsen, A.L. Horwich, and K. Wuthrich NMR analysis of a 900K GroEL GroES complex Nature 418 2002 207 211
39. H.S. Rye Application of fluorescence resonance energy transfer to the GroEL-GroES chaperonin reaction Methods 24 2001 278 288
40. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, and H. Weissig The Protein Data Bank Nucl. Acids Res. 28 2000 235 242
41. G.J. Kleywegt, and T.A. Jones Software for handling macromolecular envelopes Acta Crystallog. sect. D 55 1999 941 944
42. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
43. J.P. Abrahams, S.K. Buchanan, M.J. Van Raaij, I.M. Fearnley, A.G. Leslie, and J.E. Walker The structure of bovine F1-ATPase complexed with the peptide antibiotic efrapeptin Proc. Natl Acad. Sci. USA 93 1996 9420 9424
44. J.P. Abrahams, and R.A. De Graaff New developments in phase refinement Curr. Opin. Struct. Biol. 5 1998 601 605
45. T.A. Jones, J.Y. Zou, S.W. Cowan, and M. Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallog. sect. A 47 1991 110 119
46. R.A. Laskowski, M.W. Macarthur, D.S. Moss, and J.M. Thornton PROCHECK: a program to check the stereochemical quality of protein structures J. Appl. Crystallog. 26 1993 283 291
47. G.N. Murshudov, A.A. Vagin, A. Lebedev, K.S. Wilson, and E.J. Dodson Efficient anisotropic refinement of macromolecular structures using FFT Acta Crystallog. sect. D 55 1999 247 255
48. M.D. Winn, M.N. Isupov, and G.N. Murshudov Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallog. sect. D 57 2001 122 133
49. B. Howlin, S.A. Butler, D.S. Moss, G.W. Harris, and H.P.C. Driessen TLSANL: TLS parameter-analysis program for segmented anisotropic refinement of macromolecular structures J. Appl. Crystallog. 26 1993 622 624
50. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallog. sect. D 50 1994 760 763
51. Lutz, M. & Ascher, D. (1999). Learning Python. O'Reilly and Associates, San Carlos, CA, USA.
52. DeLano, W. l. (2002). The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.
53. E.A. Merritt, and M.E.P. Murphy Raster3D version 2.0. A program for photorealistic molecular graphics Acta Crystallog. sect. D 50 1994 869 873
54. E.A. Merritt Expanding the model: anisotropic displacement parameters in protein structure refinement Acta Crystallog. sect. D 55 1999 1109 1117
55. D.E. McRee A visual protein crystallographic software system for X11/Xview J. Mol. Graph. 10 1992 44 46