Protein structural transitions and their functional role

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 363, Issue 1827, 2005, Pages 331-356

  Karplus, Martin ^a,b   Gao, Yi Qin ^b   Ma, Jianpeng ^c   Van Der Vaart, Arjan ^a,b   Yang, Wei ^b   Zewail, A H ^d  

^a UNIVERSITÉ LOUIS PASTEUR   (France)

^b HARVARD UNIVERSITY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Biomolecular motors; Chaperones; F1 ATPase; Free energy simulations; GroEL; Molecular dynamics simulations

Indexed keywords

EID: 12944292929     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2004.1496     Document Type: Article

References (104)

1. 1-ATPase from bovine heart-mitochondria. Nature 370, 621-628.
2. Alberts, B. 1998 The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92, 291-294.
3. 1-ATPase: a molecular motor that hydrolyzes ATP with sequential opening and closing of catalytic sites coupled to rotation of its γ subunit. Acc. Chem. Res. 31, 819-826.
4. Anfinsen, C. 1973 Principles that govern the folding of protein chains. Science 181, 223-230.
5. 1-ATPase. Biophys. J. 85, 695-706.
6. Austin, R. H., Beeson, K. W., Eisenstein, L., Frauenfelder, H. & Gurisalus, I. C. 1975 Dynamics of ligand binding to myoglobin. Biochemistry 14, 5355-5373.
7. Berg, H. C. 2003 The rotary motor of bacterial flagella. A. Rev. Biochem. 72, 19-54.
8. Betancourt, M. & Thirumalai, D. 1999 Exploring the kinetic requirements for enhancement of protein folding rates in the GroEL cavity. J. Mol. Biol. 287, 627-644.
9. 1-ATPase synthase. Nat. Struct. Biol. 9, 198-202.
10. 1-ATPase β subunit: a molecular dynamics study. Biophys. J. 85, 1482-1491.
11. Boisvert, D. C., Wang, J. M., Otwinowski, A., Horwich, A. L. & Sigler, P. B. 1996 The 2.4 Å crystal structure of the bacterial chaperonin GroEL complexed with ATP γ S. Nat. Struct. Biol. 3, 170-177.
12. Boyer, P. D. 1979 In Membrane bioenergetics (ed. C. P. Lee, C. Schatz & L. Ernster), pp. 461-477. Addison-Wesley.
13. Boyer, P. D. 1993 The binding change mechanism for ATP synthase-some probabilities and possibilities. Biochim. Biophys. Acta 1140, 215-250.
14. Boyer, P. D. 1997 The ATP synthase: a splendid molecular machine. A. Rev. Biochem. 66, 717-749.
15. Boyer, P. D. 2002 A research journey with ATP synthase. J. Biol. Chem. 277, 39045-39061.
16. Braig, K., Otwinowski, Z., Hedge, R., Boisvert, D. C., Joachimiak, A., Horwich, A. L. & Sigler, P. B. 1994 The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371, 578-586.
17. Braig, K., Adams, P. D. & Brünger, A. T. 1995 Conformational variability in the refined structure of the chaperonin GroEL at 2.4 Å resolution. Nat. Struct. Biol. 2, 1083-1094.
18. Brinker, A., Pfeifer, G., Kerner, M., Naylor, D., Hartl, F. & Hayer-Hartl, M. 2001 Dual function of protein confinement in chaperonin-assisted protein folding. Cell 107, 223-233.
19. Brooks, B., Bruccoleri, R., Olafson, B., States, D., Swaninathan, S. & Karplus, M. 1983 CHARMM: a program for macromolecular energy minimization and dynamics calculations. J. Computat. Chem. 4, 187-217.
20. Buckle, A., Zahn, R. & Fersht, A. 1997 A structural model for GroEL-polypeptide recognition. Proc. Natl Acad. Sci. USA 94, 3571-3575.
21. o-type ATP synthase, a biological rotary motor. Trends Biochem. Sci. 27, 154-160.
22. Chan, H. & Dill, K. 1996 A simple model of chaperonin-mediated protein folding. Proteins 24, 345-351.
23. Chaudhuri, T., Farr, G., Fenton, W., Rospert, S. & Horwich, A. 2001 GroEL/GroES-mediated folding of a protein too large to be encapsulated. Cell 107, 235-246.
24. Chen, L. & Sigler, P. B. 1999 The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell 99, 757-768.
25. Chen, S., Roseman, A., Hunter, A., Wood, S., Burston, S., Ranson, N., Clarke, A. & Saibil, H. 1994 Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature 371, 261-264.
26. Chen, J., Walter, S., Horwich, A. & Smith, D. 2001 Folding of malate dehydrogenase inside the GroEL-GroES cavity. Nat. Struct. Biol. 8, 721-728.
27. 1-ATPase. J. Mol. Biol. 340, 345-372.
28. Diez, M. (and 10 others) 2004 Proton-powered subunit rotation in single membrane-bound F0F1-ATP synthase. Nat. Struct. Biol. 11, 135-141.
29. Dobson, C. 2002 Getting out of shape. Nature 418, 729-730.
30. Elber, R. & Karplus, M. 1987 Multiple conformational states of proteins: a molecular dynamics analysis of myoglobin. Science 235, 318-321.
31. Ellis, R. & Hartl, F. 1999 Principles of protein folding in the cellular environment. Curr. Opin. Struct. Biol. 9, 102-110.
32. Farr, G., Furtak, K., Rowland, M., Ranson, N., Saibil, H., Kirchhausen, T. & Horwich, A. 2000 Multivalent binding of nonnative substrate proteins by the chaperonin GroEL. Cell 100, 561-573.
33. Fenton, W., Kashi, Y., Furtak, K. & Horwich, A. 1994 Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371, 614-619.
34. Fillingame, R. H., Angevine, C. M. & Dmitriev, O. Y. 2003 Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett. 555, 29-34.
35. Frauenfelder, H., Petsko, G. A. & Tsernoglou, D. 1979 Temperature-dependent X-ray-diffraction as a probe of protein structural dynamics. Nature 280, 558-563.
36. 1-ATPase. Proc. Natl Acad. Sci. USA 100, 11339-11344.
37. Garcia-Viloca, M., Gao, J., Karplus, M. & Truhlar, D. G. 2003 How enzymes work: a perspective based on modem reaction rate theory and computer simulations and experiment. Science 303, 186-196.
38. 1-ATPase at 2 4 Å resolution. Nat. Struct. Biol. 7, 1055-1061.
39. o ATP synthase. Biochemistry 37, 8817-8824.
40. Grallert, H. & Buchner, J. 2001 Review: a structural view of the GroE chaperone cycle. J. Struct. Biol. 135, 95-103.
41. 1-ATPase are important for catalytic activity. J. Biol. Chem. 278, 51594-51 598.
42. Groß, M., Robinson, C., Mayhew, M., Hartl, F. & Radford, S. 1996 Significant hydrogen exchange protection in GroEL-bound DHFR is maintained during iterative rounds of substrate cycling. Protein Sci. 5, 2506-2513.
43. Hammarström, P., Persson, M., Owenius, R., Lindgren, M. & Carlsson, U. 2000 Protein substrate binding induces conformational changes in the chaperonin GroEL. J. Biol. Chem. 275, 22832-22838.
44. Hammarström, P., Persson, M. & Carlsson, U. 2001 Protein compactness measured by fluorescence resonance energy transfer. J. Biol. Chem. 276, 21765-21775.
45. Hartl, F. 1996 Molecular chaperones in cellular protein folding. Nature 381, 571-580.
46. Houry, W., Frishman, D., Eckerskorn, C., Lottspeich, F. & Hartl, F. 1999 Identification of in vivo substrates of the chaperonin GroEL. Nature 402, 147-154.
47. Inobe, T., Makio, T., Takasu-Ishikawa, E., Terada, T. &: Kuwajima, K. 2001 Nucleotide binding to the chaperonin GroEL: non-cooperative binding of ATP analogs & ADP, and cooperative effect of ATP. Biochim. Biophys. Acta 1545, 160-173.
48. Inobe, T., Arai, M., Nakao, M., Ito, K., Kamagata, K., Makio, T., Amemiya, Y., Kihara, H. & Kuwajima, K. 2003 Equilibrium and kinetics of the allosteric transition of GroEL studied by solution X-ray scattering and fluorescence spectroscopy. J. Mol. Biol. 327, 183-191.
49. Itoh, H., Takahashi, A., Adachi, K., Noji, H., Yasuda, R., Yoshida, M. & Kinoshita, J. R. 2004 Mechanically driven ATP synthesis by F1-ATPase. Nature 427, 465-468.
50. Karplus, M. 2000 Aspects of protein reaction dynamics: deviations from simple behavior. J. Phys. Chem. B104, 11-27.
51. Karplus, M. & Gao, Y. Q. 2004 Biomolecular motors: the F1-ATPase paradigm. Curr. Opin. Struct. Biol. 14, 250-259.
52. Koster, G., VanDuijn, M., Hofs, B. & Dogterom, M. 2003 Membrane tube formation from giant vesicles by dynamic association of motor proteins. Proc. Natl Acad. Sci. USA 100, 15583-15588.
53. 1-ATPase molecular motor. J. Chem. Phys. 118, 9890-9898.
54. Llorca, O., Marco, S., Carrascosa, J. & Valpuesta, J. 1997 Conformational changes in the GroEL oligomer during the functional cycle. J. Struct. Biol. 118, 31-42.
55. Ma, J. & Karplus, M. 1998 The allosteric mechanism of the chaperonin GroEL: a dynamic analysis. Proc. Natl Acad. Sci. USA 95, 8502-8507.
56. Ma, J., Sigler, P. B., Xu, Z. & Karplus, M. 2000 A dynamic model for the allosteric mechanism of GroEL. J. Mol. Biol. 302, 303-313.
57. 1-ATPase. Structure 10, 921-931.
58. McCammon, J. A., Gelin, B. R. & Karplus, M. 1977 Dynamics of folded proteins. Nature 267, 585-590.
59. 1-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106, 331-341.
60. Nishizaka, T., Oiwa, K., Noji, H., Kimura, S., Muneyuki, E., Yoshida, M. & Kinosita, K. 2004 Chemomechanical coupling in F1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation. Nat. Struct. Biol. 11, 142-148.
61. 1-ATPase. Nature 386, 299-302.
62. Oster, G. & Wang, H. Y. 2003 Rotary protein motors. Trends Cell Biol. 13, 114-121.
63. Panke, O. & Rumberg, B. 1999 Kinetic modeling of rotary CF0F1-ATP synthase: storage of elastic energy during energy transduction. Biochim. Biophys. Acta Bioenerg. 1412, 118-128.
64. Panke, O., Cherepanov, D. A., Gumbiowski, K., Engelbrecht, S. & Junge, W. 2001 Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: angular torque profile of the enzyme. Biophys. J. 81, 1220-1233.
65. Patel, P. H. & Loeb, L. A. 2001 Getting a grip on how DNA polymerases function. Nat. Struct. Biol. 8, 656-659.
66. Ranson, N., Farr, G., Roseman, A., Gowen, B., Fenton, W., Horwich, A. & Saibil, H. 2001 ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107, 869-879.
67. Rastogi, V. K. & Girvin, M. E. 1999 Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402, 263-268.
68. Roseman, A., Chen, S., White, H., Braig, K. & Saibil, H. 1996 The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87, 241-251.
69. Rubinstein, J. L., Walker, J. E. & Henderson, R. 2003 Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J. 22, 6182-6192.
70. Rye, H., Burston, S., Fenton, W., Beechem, J., Xu, A., Sigler, P. & Horwich, A. 1997 Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388, 792-798.
71. Rye, H., Roseman, A., Chen, S., Furtak, K., Fenton, W., Saibil, H. & Horwich, A. 1999 GroEL-GroES cycling: aTP and nonnative polypeptide direct alternation of folding-active rings. Cell 97, 325-338.
72. Saibil, H. 2000 Molecular chaperones: containers and surfaces for folding, stabilising or unfolding proteins. Curr. Opin. Struct. Biol. 10, 251-258.
73. Saibil, H., Horwich, A. & Fenton, W. 2002 Allostery and protein substrate conformational change during GroEL/GroES-mediated protein folding. Adv. Prot. Chem. 59, 45-72.
74. Schlitter, J., Engels, M., Krüger, P., Jacoby, E. & Wollmer, A. 1993 Targeted molecular dynamics simulation of conformational change - application to the T → R transition in insulin. Mol. Simulat. 10, 291-308.
75. Schliwa, M. (ed.) 2003 Molecular motors. Weinheim: Wiley-VCH.
76. Seelert, H., Dencher, N. A. & Möller, D. J. 2003 Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J. Mol. Biol. 333, 337-344.
77. 1-ATPase. J. Bioenerg. Biomembr. 24, 479-484.
78. 1-ATP synase. Biochim. Biophys. Acta 1553, 188-211.
79. Sfatos, C., Gutin, A., Abkevich, V. & Shakhnovich, E. 1996 Simulations of chaperone-assisted folding. Biochemistry 35, 334-339.
80. 1 motor: cleavage of ATP at the catalytic site occurs in 1 ms before 40 degrees substep rotation. Proc. Natl Acad. Sci. USA 100, 14731-14736.
81. Shtilerman, M., Lorimer, G. & Englander, S. 1999 Chaperonin function: folding by forced unfolding. Science 284, 822-825.
82. Stan, G., Thirumalai, D., Lorimer, G. & Brooks, B. 2003 Annealing function of GroEL: structural and bioinformatic analysis. Biophys. Chem. 100, 453-467.
83. 1-ATPase. Eur. Biophys. J. 32, 676-683.
84. 1-ATPase and its implications for the rotation cycle. Biophys. J. 86, 1373-1384.
85. Thirumalai, D. & Lorimer, G. 2001 Chaperonin-mediated protein folding. A. Rev. Biophys. Biomol. Struct. 30, 245-269.
86. Todd, M., Viitanen, P. & Lorimer, G. 1994 Dynamics of the chaperonin ATPase cycle: implcations for facilitated protein folding. Science 265, 659-666.
87. Todd, M., Lorimer, G. & Thirumalai, D. 1996 Chaperonin-facilitated protein folding: optimization of rate and yield by an iterative annealing mechanism. Proc. Natl Acad. Sci. USA 93, 4030-4035.
88. van der Vaart, A., Ma, J. & Karplus, M. 2004 The unfolding action of GroEL on a protein substrate. Biophys. J. 87, 562-573.
89. Vendruscolo, M. & Dobson, C. M. 2005 Towards complete descriptions of the free-energy land-scapes of proteins. Phil. Trans. R. Soc. A 363, 433-452.
90. Wales, D. J. 2005 The energy landscape as a unifying theme in molecular science. Phil. Trans. R. Soc. A 363, 357-377.
91. Walter, S., Lorimer, G. & Schmid, F. 1996 A thermodynamic coupling mechanism for GroEL-mediated unfolding. Proc. Natl Acad. Sci. USA 93, 9425-9430.
92. 14 at 2. 0 Å resolution. J. Mol. Biol. 327, 843-855.
93. 1 motor of ATP synthase. Nature 396, 279-282.
94. Wang, H. & Oster, G. 2002 The Stokes efficiency for molecular motors and its applications. Europhys. Lett. 57, 134-140.
95. 1-ATPase. Biochim. Biophys. Acta 1319, 19-58.
96. Weissman, J., Kashi, Y., Fenton, W. & Horwich, A. 1994 GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78, 693-702.
97. Weissman, J., Rye, H., Fenton, W., Beechem, J. & Horwich, A. 1996 Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 84, 481-490.
98. Wolynes, P. G. 2005 Energy landscapes and solved protein-folding problems. Phil. Trans. R. Soc. A 363, 453-467.
99. 7 chaperonin complex. Nature 388, 741-750.
100. 1-ATPase. Proc. Natl Acad. Sci. USA 100, 874-879.
101. 1-ATPase is a highly efficient molecular motor that rotates with discrete 120° steps. Cell 93, 1117-1124.
102. 1-ATPase. Nature 410, 898-904.
103. Zahn, R., Perrett, S. & Fersht, A. 1996a Conformational states bound by the molecular chaperones GroEL and SecB: a hidden unfolding (annealing) activity. J. Mol. Biol. 261, 43-61.
104. Zahn, R., Perrett, S., Stenberg, G. & Fersht, A. 1996b Catalysis of amide proton exchange by the molecular chaperones GroEL and SecB. Science 271, 642-644.