Allosteric Mechanisms in Chaperonin Machines

Chemical Reviews

Volumn 116, Issue 11, 2016, Pages 6588-6606

  Gruber, Ranit ^a   Horovitz, Amnon ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

COORDINATION REACTIONS; ESCHERICHIA COLI; PROTEIN FOLDING; SUBSTRATES;

ALLOSTERIC COMMUNICATION; ALLOSTERIC EFFECTORS; ALLOSTERIC MECHANISMS; ALLOSTERIC REGULATION; ALLOSTERIC TRANSITION; POTASSIUM IONS; PROTEIN FOLDING REACTION; PROTEIN SUBSTRATE;

PROTEINS;

ADENOSINE TRIPHOSPHATE; CHAPERONIN; ESCHERICHIA COLI PROTEIN; POTASSIUM;

ALLOSTERISM; CHEMISTRY; ESCHERICHIA COLI; METABOLISM; PROTEIN CONFORMATION; PROTEIN FOLDING;

ADENOSINE TRIPHOSPHATE; ALLOSTERIC REGULATION; CHAPERONINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; POTASSIUM; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 84974555476     PISSN: 00092665     EISSN: 15206890     Source Type: Journal    
DOI: 10.1021/acs.chemrev.5b00556     Document Type: Review

References (195)

1. Monod, J.; Jacob, F. Teleonomic Mechanisms in Cellular Metabolism, Growth, and Differentiation Cold Spring Harbor Symp. Quant. Biol. 1961, 26, 389-401 10.1101/SQB.1961.026.01.048
2. Changeux, J. P. The Feedback Control Mechanism of Biosynthetic L-Threonine Deaminase by L-Isoleucine Cold Spring Harbor Symp. Quant. Biol. 1961, 26, 313-318 10.1101/SQB.1961.026.01.037
3. Hill, A. V. The Possible Effects of the Aggregation of the Molecules of Haemoglobin on Its Dissociation Curves J. Physiol. 1910, 40, IV-VII
4. Monod, J.; Wyman, J.; Changeux, J. P. On the Nature of Allosteric Transitions: A Plausible Model J. Mol. Biol. 1965, 12, 88-118 10.1016/S0022-2836(65)80285-6
5. Koshland, D. E., Jr.; Némethy, G.; Filmer, D. Comparison of Experimental Binding Data and Theoretical Models in Proteins Containing Subunits Biochemistry 1966, 5, 365-385 10.1021/bi00865a047
6. Milo, R.; Hou, J. H.; Springer, M.; Brenner, M. P.; Kirschner, M. W. The Relationship Between Evolutionary and Physiological Variation in Hemoglobin Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 16998-17003 10.1073/pnas.0707673104
7. Changeux, J. P. Allostery and the Monod-Wyman-Changeux Model After 50 Years Annu. Rev. Biophys. 2012, 41, 103-133 10.1146/annurev-biophys-050511-102222
8. Boehr, D. D.; Nussinov, R.; Wright, P. E. The Role of Dynamic Conformational Ensembles in Biomolecular Recognition Nat. Chem. Biol. 2009, 5, 789-796 10.1038/nchembio.232
9. Sharon, M.; Horovitz, A. Probing Allosteric Mechanisms Using Native Mass Spectrometry Curr. Opin. Struct. Biol. 2015, 34, 7-16 10.1016/j.sbi.2015.05.002
10. Eigen, M. Kinetics of Reaction Control and Information Transfer in Enzymes and Nucleic Acids Nobel Symp. 1967, 5, 333-369
11. Cooper, A.; Dryden, D. T. Allostery Without Conformational Change. A Plausible Model Eur. Biophys. J. 1984, 11, 103-109 10.1007/BF00276625
12. Townsend, P. D.; Rodgers, T. L.; Pohl, E.; Wilson, M. R.; McLeish, T. C.; Cann, M. J. Global Low-Frequency Motions in Protein Allostery: CAP as a Model System Biophys. Rev. 2015, 7, 175-182 10.1007/s12551-015-0163-9
13. Hodson, S.; Marshall, J. J.; Burston, S. G. Mapping the Road to Recovery: The ClpB/Hsp104 Molecular Chaperone J. Struct. Biol. 2012, 179, 161-171 10.1016/j.jsb.2012.05.015
14. Kelman, Z.; Finkelstein, J.; O'Donnell, M. Protein Structure: Why Have Six-Fold Symmetry? Curr. Biol. 1995, 5, 1239-1242 10.1016/S0960-9822(95)00247-8
15. Horwich, A. L.; Weber-Ban, E. U.; Finley, D. Chaperone Rings in Protein Folding and Degradation Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 11033-11040 10.1073/pnas.96.20.11033
16. Thirumalai, D.; Klimov, D. K.; Lorimer, G. H. Caging Helps Proteins Fold Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 11195-11197 10.1073/pnas.2035072100
17. Horwich, A. L.; Fenton, W. A. Chaperonin-Mediated Protein Folding: Using a Central Cavity to Kinetically Assist Polypeptide Chain Folding Q. Rev. Biophys. 2009, 42, 83-116 10.1017/S0033583509004764
18. Hayer-Hartl, M.; Bracher, A.; Hartl, F. U. The GroEL-GroES Chaperonin Machine: A Nano-Cage for Protein Folding Trends Biochem. Sci. 2016, 41, 62-76 10.1016/j.tibs.2015.07.009
19. Sauer, R. T.; Baker, T. A. AAA+ Proteases: ATP-Fueled Machines of Protein Destruction Annu. Rev. Biochem. 2011, 80, 587-612 10.1146/annurev-biochem-060408-172623
20. Riedel, C.; Gabizon, R.; Wilson, C. A.; Hamadani, K.; Tsekouras, K.; Marqusee, S.; Pressé, S.; Bustamante, C. The Heat Released During Catalytic Turnover Enhances the Diffusion of an Enzyme Nature 2015, 517, 227-230 10.1038/nature14043
21. Chistol, G.; Liu, S.; Hetherington, C. L.; Moffitt, J. R.; Grimes, S.; Jardine, P. J.; Bustamante, C. High Degree of Coordination and Division of Labor Among Subunits in a Homomeric Ring ATPase Cell 2012, 151, 1017-1028 10.1016/j.cell.2012.10.031
22. Gai, D.; Zhao, R.; Li, D.; Finkielstein, C. V.; Chen, X. S. Mechanisms of Conformational Change for a Replicative Hexameric Helicase of SV40 Large Tumor Antigen Cell 2004, 119, 47-60 10.1016/j.cell.2004.09.017
23. Stinson, B. M.; Nager, A. R.; Glynn, S. E.; Schmitz, K. R.; Baker, T. A.; Sauer, R. T. Nucleotide Binding and Conformational Switching in the Hexamaric Ring of a AAA+ Machine Cell 2013, 153, 628-639 10.1016/j.cell.2013.03.029
24. Horovitz, A.; Fridmann, Y.; Kafri, G.; Yifrach, O. Review: Allostery in Chaperonins J. Struct. Biol. 2001, 135, 104-114 10.1006/jsbi.2001.4377
25. Horovitz, A.; Willison, K. R. Allosteric Regulation of Chaperonins Curr. Opin. Struct. Biol. 2005, 15, 646-651 10.1016/j.sbi.2005.10.001
26. Saibil, H. R.; Fenton, W. A.; Clare, D. K.; Horwich, A. L. Structure and Allostery of the Chaperonin GroEL J. Mol. Biol. 2013, 425, 1476-1487 10.1016/j.jmb.2012.11.028
27. Skjærven, L.; Cuellar, J.; Martinez, A.; Valpuesta, J. M. Dynamics, Flexibility, and Allostery in Molecular Chaperonins FEBS Lett. 2015, 589, 2522-2532 10.1016/j.febslet.2015.06.019
28. Thirumalai, D.; Lorimer, G. H. Chaperonin-Mediated Protein Folding Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 245-269 10.1146/annurev.biophys.30.1.245
29. Lin, Z.; Rye, H. S. GroEL-Mediated Protein Folding: Making the Impossible, Possible Crit. Rev. Biochem. Mol. Biol. 2006, 41, 211-239 10.1080/10409230600760382
30. Gutsche, I.; Essen, L. O.; Baumeister, W. Group II Chaperonins: New TRiC(k)s and Turns of a Protein Folding Machine J. Mol. Biol. 1999, 293, 295-312 10.1006/jmbi.1999.3008
31. Horwich, A. L.; Fenton, W. A.; Chapman, E.; Farr, G. W. Two Families of Chaperonin: Physiology and Mechanism Annu. Rev. Cell Dev. Biol. 2007, 23, 115-145 10.1146/annurev.cellbio.23.090506.123555
32. Bigotti, M. G.; Clarke, A. R. Chaperonins: The Hunt for the Group II Mechanism Arch. Biochem. Biophys. 2008, 474, 331-339 10.1016/j.abb.2008.03.015
33. Yébenes, H.; Mesa, P.; Muñoz, I. G.; Montoya, G.; Valpuesta, J. M. Chaperonins: Two Rings for Folding Trends Biochem. Sci. 2011, 36, 424-432 10.1016/j.tibs.2011.05.003
34. Ditzel, L.; Löwe, J.; Stock, D.; Stetter, K. O.; Huber, H.; Huber, R.; Steinbacher, S. Crystal Structure of the Thermosome, the Archaeal Chaperonin and Homolog of CCT Cell 1998, 93, 125-138 10.1016/S0092-8674(00)81152-6
35. Kalisman, N.; Adams, C. M.; Levitt, M. Subunit Order of Eukaryotic TRiC/CCT Chaperonin by Cross-linking, Mass Spectrometry, and Combinatorial Homology Modeling Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 2884-2889 10.1073/pnas.1119472109
36. Leitner, A.; Joachimiak, L. A.; Bracher, A.; Mönkemeyer, L.; Walzthoeni, T.; Chen, B.; Pechmann, S.; Holmes, S.; Cong, Y.; Ma, B. et al. The Molecular Architecture of the Eukaryotic Chaperonin TRiC/CCT Structure 2012, 20, 814-825 10.1016/j.str.2012.03.007
37. Dekker, C.; Roe, S. M.; McCormack, E. A.; Beuron, F.; Pearl, L. H.; Willison, K. R. The Crystal Structure of Yeast CCT Reveals Intrinsic Asymmetry of Eukaryotic Cytosolic Chaperonins EMBO J. 2011, 30, 3078-3090 10.1038/emboj.2011.208
38. Kalisman, N.; Schröder, G. F.; Levitt, M. The Crystal Structures of the Eukaryotic Chaperonin CCT Reveal Its Functional Partitioning Structure 2013, 21, 540-549 10.1016/j.str.2013.01.017
39. Braig, K.; Otwinowski, Z.; Hegde, R.; Boisvert, D. C.; Joachimiak, A.; Horwich, A. L.; Sigler, P. B. The Crystal Structure of the Bacterial Chaperonin GroEL at 2.8 Å Nature 1994, 371, 578-586 10.1038/371578a0
40. Bartolucci, C.; Lamba, D.; Grazulis, S.; Manakova, E.; Heumann, H. Crystal Structure of Wild-Type Chaperonin GroEL J. Mol. Biol. 2005, 354, 940-951 10.1016/j.jmb.2005.09.096
41. Fenton, W. A.; Kashi, Y.; Furtak, K.; Horwich, A. L. Residues in Chaperonin GroEL Required for Polypeptide Binding and Release Nature 1994, 371, 614-619 10.1038/371614a0
42. Hunt, J. F.; Weaver, A. J.; Landry, S. J.; Gierasch, L.; Deisenhofer, J. The Crystal Structure of the GroES Co-Chaperonin at 2.8 Å Resolution Nature 1996, 379, 37-45 10.1038/379037a0
43. Mande, S. C.; Mehra, V.; Bloom, B. R.; Hol, W. G. Structure of the Heat Shock Protein Chaperonin-10 of Mycobacterium leprae Science 1996, 271, 203-207 10.1126/science.271.5246.203
44. Chandrasekhar, G. N.; Tilly, K.; Woolford, C.; Hendrix, R.; Georgopoulos, C. Purification and Properties of the GroES Morphogenetic Protein of Escherichia coli J. Biol. Chem. 1986, 261, 12414-12419
45. 7 Chaperonin Complex Nature 1997, 388, 741-750 10.1038/41944
46. Klumpp, M.; Baumeister, W.; Essen, L. O. Structure of the Substrate Binding Domain of the Thermosome, an Archaeal Group II Chaperonin Cell 1997, 91, 263-270 10.1016/S0092-8674(00)80408-0
47. Iizuka, R.; So, S.; Inobe, T.; Yoshida, T.; Zako, T.; Kuwajima, K.; Yohda, M. Role of the Helical Protrusion in the Conformational Change and Molecular Chaperone Activity of the Archaeal Group II Chaperonin J. Biol. Chem. 2004, 279, 18834-18839 10.1074/jbc.M400839200
48. Viitanen, P. V.; Gatenby, A. A.; Lorimer, G. H. Purified Chaperonin 60 (groEL) Interacts with the Nonnative States of a Multitude of Escherichia coli Proteins Protein Sci. 1992, 1, 363-369 10.1002/pro.5560010308
49. Aoki, K.; Motojima, F.; Taguchi, H.; Yomo, T.; Yoshida, M. GroEL Binds Artificial Proteins with Random Sequences J. Biol. Chem. 2000, 275, 13755-13758 10.1074/jbc.275.18.13755
50. Lorimer, G. H. A Quantitative Assessment of the Role of the Chaperonin Proteins in Protein Folding in Vivo FASEB J. 1996, 10, 5-9
51. Kerner, M. J.; Naylor, D. J.; Ishihama, Y.; Maier, T.; Chang, H. C.; Stines, A. P.; Georgopoulos, C.; Frishman, D.; Hayer-Hartl, M.; Mann, M. et al. Proteome-Wide Analysis of Chaperonin-Dependent Protein Folding in Escherichia coli Cell 2005, 122, 209-220 10.1016/j.cell.2005.05.028
52. Fujiwara, K.; Ishihama, Y.; Nakahigashi, K.; Soga, T.; Taguchi, H. A Systematic Survey of in Vivo Obligate Chaperonin-Dependent Substrates EMBO J. 2010, 29, 1552-1564 10.1038/emboj.2010.52
53. Azia, A.; Unger, R.; Horovitz, A. What Distinguishes GroEL Substrates from Other Escherichia coli Proteins? FEBS J. 2012, 279, 543-550 10.1111/j.1742-4658.2011.08458.x
54. Gao, Y.; Thomas, J. O.; Chow, R. L.; Lee, G. H.; Cowan, N. J. A Cytoplasmic Chaperonin that Catalyzes β-Actin Folding Cell 1992, 69, 1043-1050 10.1016/0092-8674(92)90622-J
55. Yaffe, M. B.; Farr, G. W.; Miklos, D.; Horwich, A. L.; Sternlicht, M. L.; Sternlicht, H. TCP1 Complex is a Molecular Chaperone in Tubulin Biogenesis Nature 1992, 358, 245-248 10.1038/358245a0
56. Dekker, C.; Stirling, P. C.; McCormack, E. A.; Filmore, H.; Paul, A.; Brost, R. L.; Costanzo, M.; Boone, C.; Leroux, M. R.; Willison, K. R. The Interaction Network of the Chaperonin CCT EMBO J. 2008, 27, 1827-1839 10.1038/emboj.2008.108
57. Yam, A. Y.; Xia, Y.; Lin, H. T.; Burlingame, A.; Gerstein, M.; Frydman, J. Defining the TRiC/CCT Interactome Links Chaperonin Function to Stabilization of Newly Made Proteins with Complex Topologies Nat. Struct. Mol. Biol. 2008, 15, 1255-1262 10.1038/nsmb.1515
58. Horwich, A. L.; Apetri, A. C.; Fenton, W. A. The GroEL/GroES cis Cavity as a Passive Anti-Aggregation Device FEBS Lett. 2009, 583, 2654-2662 10.1016/j.febslet.2009.06.049
59. Tyagi, N. K.; Fenton, W. A.; Deniz, A. A.; Horwich, A. L. Double Mutant MBP Refolds at Same Rate in Free Solution as Inside the GroEL/GroES Chaperonin Chamber When Aggregation in Free Solution is Prevented FEBS Lett. 2011, 585, 1969-1672 10.1016/j.febslet.2011.05.031
60. Tang, Y. C.; Chang, H. C.; Roeben, A.; Wischnewski, D.; Wischnewski, N.; Kerner, M. J.; Hartl, F. U.; Hayer-Hartl, M. Structural Features of the GroEL-GroES Nano-Cage Required for Rapid Folding of Encapsulated Protein Cell 2006, 125, 903-914 10.1016/j.cell.2006.04.027
61. Georgescauld, F.; Popova, K.; Gupta, A. J.; Bracher, A.; Engen, J. R.; Hayer-Hartl, M.; Hartl, F. U. GroEL/ES Chaperonin Modulates the Mechanism and Accelerates the Rate of TIM-Barrel Domain Folding Cell 2014, 157, 922-934 10.1016/j.cell.2014.03.038
62. Gupta, A. J.; Haldar, S.; Miličić, G.; Hartl, F. U.; Hayer-Hartl, M. Active Cage Mechanism of Chaperonin-Assisted Protein Folding Demonstrated at Single-Molecule Level J. Mol. Biol. 2014, 426, 2739-2754 10.1016/j.jmb.2014.04.018
63. England, J. L.; Lucent, D.; Pande, V. S. A Role for Confined Water in Chaperonin Function J. Am. Chem. Soc. 2008, 130, 11838-11839 10.1021/ja802248m
64. Franck, J. M.; Sokolovski, M.; Kessler, N.; Matalon, E.; Gordon-Grossman, M.; Han, S. I.; Goldfarb, D.; Horovitz, A. Probing Water Density and Dynamics in the Chaperonin GroEL Cavity J. Am. Chem. Soc. 2014, 136, 9396-9403 10.1021/ja503501x
65. Todd, M. J.; Lorimer, G. H.; Thirumalai, D. Chaperonin-Facilitated Protein Folding: Optimization of Rate and Yield by an Iterative Annealing Mechanism Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 4030-4035 10.1073/pnas.93.9.4030
66. Lin, Z.; Madan, D.; Rye, H. S. GroEL Stimulates Protein Folding Through Forced Unfolding Nat. Struct. Mol. Biol. 2008, 15, 303-311 10.1038/nsmb.1394
67. Weaver, J.; Rye, H. S. The C-terminal Tails of the Bacterial Chaperonin GroEL Stimulate Protein Folding by Directly Altering the Conformation of a Substrate Protein J. Biol. Chem. 2014, 289, 23219-23232 10.1074/jbc.M114.577205
68. Priya, S.; Sharma, S. K.; Sood, V.; Mattoo, R. U. H.; Finka, A.; Azem, A.; De Los Rios, P.; Goloubinoff, P. GroEL and CCT are Catalytic Unfoldases Mediating Out-of-Cage Polypeptide Refolding Without ATP Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 7199-7204 10.1073/pnas.1219867110
69. Libich, D. S.; Tugarinov, V.; Clore, G. M. Intrinsic Unfoldase/Foldase Activity of the Chaperonin GroEL Directly Demonstrated Using Multinuclear Relaxation-Based NMR Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 8817-8823 10.1073/pnas.1510083112
70. Chatellier, J.; Hill, F.; Lund, P. A.; Fersht, A. R. In Vivo Activities of GroEL Minichaperones Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 9861-9866 10.1073/pnas.95.17.9861
71. Henderson, B.; Fares, M. A.; Lund, P. A. Chaperonin 60: A Paradoxical, Evolutionary Conserved Protein Family with Multiple Moonlighting Functions Biol. Rev. Camb. Philos. Soc. 2013, 88, 955-987 10.1111/brv.12037
72. Gray, T. E.; Fersht, A. R. Cooperativity in ATP Hydrolysis by GroEL Is Increased by GroES FEBS Lett. 1991, 292, 254-258 10.1016/0014-5793(91)80878-7
73. Bochkareva, E. S.; Lissin, N. M.; Flynn, G. C.; Rothman, J. E.; Girshovich, A. S. Positive Cooperativity in the Functioning of Molecular Chaperone GroEL J. Biol. Chem. 1992, 267, 6796-6800
74. Jackson, G. S.; Staniforth, R. A.; Halsall, D. J.; Atkinson, T.; Holbrook, J. J.; Clarke, A. R.; Burston, S. G. Binding and Hydrolysis of Nucleotides in the Chaperonin Catalytic Cycle: Implications for the Mechanism of Assisted Protein Folding Biochemistry 1993, 32, 2554-2563 10.1021/bi00061a013
75. Inobe, T.; Makio, T.; Takasu-Ishikawa, E.; Terada, T. P.; Kuwajima, K. Nucleotide Binding to the Chaperonin GroEL: Non-Cooperative Binding of ATP Analogs and ADP, and Cooperative Effect of ATP Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 2001, 1545, 160-173 10.1016/S0167-4838(00)00274-0
76. Weissman, J. S.; Hohl, C. M.; Kovalenko, O.; Kashi, Y.; Chen, S.; Braig, K.; Saibil, H. R.; Fenton, W. A.; Horwich, A. L. Mechanism of GroEL Action: Productive Release of Polypeptide from a Sequestered Position Under GroES Cell 1995, 83, 577-587 10.1016/0092-8674(95)90098-5
77. Poso, D.; Clarke, A. R.; Burston, S. G. A Kinetic Analysis of the Nucleotide-Induced Allosteric Transitions in a Single-Ring Mutant of GroEL J. Mol. Biol. 2004, 338, 969-977 10.1016/j.jmb.2004.03.010
78. Amir, A.; Horovitz, A. Kinetic Analysis of ATP-dependent Inter-Ring Communication in GroEL J. Mol. Biol. 2004, 338, 979-988 10.1016/j.jmb.2004.02.076
79. Kafri, G.; Willison, K. R.; Horovitz, A. Nested Allosteric Interactions in the Cytoplasmic Chaperonin Containing TCP-1 Protein Sci. 2001, 10, 445-449 10.1110/ps.44401
80. Kusmierczyk, A. R.; Martin, J. Nested Cooperativity and Salt Dependence of the ATPase Activity of the Archaeal Chaperonin Mm-cpn FEBS Lett. 2003, 547, 201-204 10.1016/S0014-5793(03)00722-1
81. Bigotti, M. G.; Clarke, A. R. Cooperativity in the Thermosome J. Mol. Biol. 2005, 348, 13-26 10.1016/j.jmb.2005.01.066
82. Yifrach, O.; Horovitz, A. Allosteric Control by ATP of Non-Folded Protein Binding to GroEL J. Mol. Biol. 1996, 255, 356-361 10.1006/jmbi.1996.0028
83. Reissmann, S.; Joachimiak, L. A.; Chen, B.; Meyer, A. S.; Nguyen, A.; Frydman, J. A Gradient of ATP Affinities Generates an Asymmetric Power Stroke Driving the Chaperonin TRiC/CCT Folding Cycle Cell Rep. 2012, 2, 866-877 10.1016/j.celrep.2012.08.036
84. Rivenzon-Segal, D.; Wolf, S. G.; Shimon, L.; Willison, K. R.; Horovitz, A. Sequential ATP-Induced Allosteric Transitions of the Cytoplasmic Chaperonin Containing TCP-1 Revealed by EM Analysis Nat. Struct. Mol. Biol. 2005, 12, 233-237 10.1038/nsmb901
85. Muñoz, I. G.; Yébenes, H.; Zhou, M.; Mesa, P.; Serna, M.; Park, A. Y.; Bragado-Nilsson, E.; Beloso, A.; de Cárcer, G.; Malumbres, M. et al. Crystal Structure of the Open Conformation of the Mammalian Chaperonin CCT in Complex with Tubulin Nat. Struct. Mol. Biol. 2011, 18, 14-19 10.1038/nsmb.1971
86. Kafri, G.; Horovitz, A. Transient Kinetic Analysis of ATP-Induced Allosteric Transitions in the Eukaryotic Chaperonin Containing TCP-1 J. Mol. Biol. 2003, 326, 981-987 10.1016/S0022-2836(03)00046-9
87. Inobe, T.; Kikushima, K.; Makio, T.; Arai, M.; Kuwajima, K. The Allosteric Transition of GroEL Induced by Metal Fluoride-ADP Complexes J. Mol. Biol. 2003, 329, 121-134 10.1016/S0022-2836(03)00409-1
88. Melki, R.; Cowan, N. J. Facilitated Folding of Actins and Tubulins Occurs via a Nucleotide-Dependent Interaction Between Cytoplasmic Chaperonin and Distinctive Folding Intermediates Mol. Cell. Biol. 1994, 14, 2895-2904 10.1128/MCB.14.5.2895
89. Chaudhry, C.; Farr, G. W.; Todd, M. J.; Rye, H. S.; Brunger, A. T.; Adams, P. D.; Horwich, A. L.; Sigler, P. B. Role of the Phosphate of ATP in Triggering Protein Folding by GroEL-GroES: Function, Structure and Energetics EMBO J. 2003, 22, 4877-4887 10.1093/emboj/cdg477
90. Rubin, M. M.; Changeux, J. P. On the Nature of Allosteric Transitions: Implications of Non-Exclusive Ligand Binding J. Mol. Biol. 1966, 21, 265-274 10.1016/0022-2836(66)90097-0
91. Viitanen, P. V.; Lubben, T. H.; Reed, J.; Goloubinoff, P.; O'Keefe, D. P.; Lorimer, G. H. Chaperonin-Facilitated Refolding of Ribulose Bisphosphate Carboxylase and ATP Hydrolysis by Chaperonin 60 (groEL) are Potassium Dependent Biochemistry 1990, 29, 5665-5671 10.1021/bi00476a003
92. Todd, M. J.; Viitanen, P. V.; Lorimer, G. H. Hydrolysis of Adenosine 5′-Triphosphate by Escherichia coli GroEL: Effects of GroES and Potassium Ion Biochemistry 1993, 32, 8560-8567 10.1021/bi00084a024
93. + and Substrate Protein on ATP Hydrolysis Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 17334-17338 10.1073/pnas.0807429105
94. 14 at 2.0 Å Resolution J. Mol. Biol. 2003, 327, 843-855 10.1016/S0022-2836(03)00184-0
95. Kiser, P. D.; Lorimer, G. H.; Palczewski, K. Use of Thallium to Identify Monovalent Cation Binding Sites in GroEL Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 2009, 65, 967-971 10.1107/S1744309109032928
96. Yifrach, O.; Horovitz, A. Two Lines of Allosteric Communication in the Oligomeric Chaperonin GroEL are Revealed by the Single Mutation Arg196-Ala J. Mol. Biol. 1994, 243, 397-401 10.1006/jmbi.1994.1667
97. Yifrach, O.; Horovitz, A. Nested Cooperativity in the ATPase Activity of the Oligomeric Chaperonin GroEL Biochemistry 1995, 34, 5303-5308 10.1021/bi00016a001
98. Yifrach, O.; Horovitz, A. Transient Kinetic Analysis of Adenosine 5′-Triphosphate Binding-Induced Conformational Changes in the Allosteric Chaperonin GroEL Biochemistry 1998, 37, 7083-7088 10.1021/bi980370o
99. Cliff, M. J.; Kad, N. M.; Hay, N.; Lund, P. A.; Webb, M. R.; Burston, S. G.; Clarke, A. R. A Kinetic Analysis of the Nucleotide-Induced Allosteric Transitions of GroEL J. Mol. Biol. 1999, 293, 667-684 10.1006/jmbi.1999.3138
100. Taniguchi, M.; Yoshimi, T.; Hongo, K.; Mizobata, T.; Kawata, Y. Stopped-Flow Fluorescence Analysis of the Conformational Changes in the GroEL Apical Domain: Relationships Between Movements in the Apical Domain and the Quaternary Structure of GroEL J. Biol. Chem. 2004, 279, 16368-16376 10.1074/jbc.M311806200
101. LiCata, V. J.; Allewell, N. M. Is Substrate Inhibition a Consequence of Allostery in Aspartate Transcarbamylase? Biophys. Chem. 1997, 64, 225-234 10.1016/S0301-4622(96)02204-1
102. Erbse, A.; Yifrach, O.; Jones, S.; Lund, P. A. Chaperone Activity of a Chimeric GroEL Protein That Can Exist in a Single or Double Ring Form J. Biol. Chem. 1999, 274, 20351-20357 10.1074/jbc.274.29.20351
103. Wyman, J. Allosteric Linkage J. Am. Chem. Soc. 1967, 89, 2202-2218 10.1021/ja00985a037
104. White, H. E.; Chen, S.; Roseman, A. M.; Yifrach, O.; Horovitz, A.; Saibil, H. R. Structural Basis of Allosteric Changes in the GroEL Mutant Arg197-Ala Nat. Struct. Biol. 1997, 4, 690-694 10.1038/nsb0997-690
105. Schoehn, G.; Quaite-Randall, E.; Jiménez, J. L.; Joachimiak, A.; Saibil, H. R. Three Conformations of an Archaeal Chaperonin, TF55 from Sulfolobus shibatae J. Mol. Biol. 2000, 296, 813-819 10.1006/jmbi.2000.3505
106. Llorca, O.; Smyth, M. G.; Carrascosa, J. L.; Willison, K. R.; Radermacher, M.; Steinbacher, S.; Valpuesta, J. M. 3D Reconstruction of the ATP-Bound Form of CCT Reveals the Asymmetric Folding Conformation of a Type II Chaperonin Nat. Struct. Biol. 1999, 6, 639-642 10.1038/10689
107. Inbar, E.; Horovitz, A. GroES Promotes the T to R Transition of the GroEL Ring Distal to GroES in the GroEL-GroES Complex Biochemistry 1997, 36, 12276-12281 10.1021/bi9714870
108. Farr, G. W.; Fenton, W. A.; Chaudhuri, T. K.; Clare, D. K.; Saibil, H. R.; Horwich, A. L. Folding with and Without Encapsulation by cis- and trans-Only GroEL-GroES Complexes EMBO J. 2003, 22, 3220-3230 10.1093/emboj/cdg313
109. 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 10.1021/bi020117v
110. Fei, X.; Yang, D.; LaRonde-LeBlanc, N.; Lorimer, G. H. Crystal Structure of a GroEL-ADP Complex in the Relaxed Allosteric State at 2.7 Å Resolution Proc. Natl. Acad. Sci. U. S. A. 2013, 110, E2958-E2966 10.1073/pnas.1311996110
111. Bochkareva, E. S.; Girshovich, A. S. ATP Induces Non-Identity of Two Rings in Chaperonin GroEL J. Biol. Chem. 1994, 269, 23869-23871
112. Saibil, H.; Dong, Z.; Wood, S.; auf der Mauer, A. Binding of Chaperonins Nature 1991, 353, 25-26 10.1038/353025b0
113. Langer, T.; Pfeifer, G.; Martin, J.; Baumeister, W.; Hartl, F. U. Chaperonin-Mediated Protein Folding: GroES Binds to One End of the GroEL Cylinder, Which Accommodates the Protein Substrate Within Its Central Cavity EMBO J. 1992, 11, 4757-4765
114. Ishii, N.; Taguchi, H.; Sumi, M.; Yoshida, M. Structure of Holo-Chaperonin Studied with Electron Microscopy. Oligomeric Cpn10 on Top of Two Layers of Cpn60 Rings with Two Stripes Each FEBS Lett. 1992, 299, 169-174 10.1016/0014-5793(92)80240-H
115. Haldar, S.; Gupta, A. J.; Yan, X.; Miličić, G.; Hartl, F. U.; Hayer-Hartl, M. Chaperonin-Assisted Protein Folding: Relative Population of Asymmetric and Symmetric GroEL:GroES Complexes J. Mol. Biol. 2015, 427, 2244-2255 10.1016/j.jmb.2015.04.009
116. Schmidt, M.; Rutkat, K.; Rachel, R.; Pfeifer, G.; Jaenicke, R.; Viitanen, P.; Lorimer, G.; Buchner, J. Symmetric Complexes of GroE Chaperonins as Part of the Functional Cycle Science 1994, 265, 656-659 10.1126/science.7913554
117. 2 Chaperonin Hetero-Oligomer Science 1994, 265, 653-656 10.1126/science.7913553
118. Llorca, O.; Marco, S.; Carrascosa, J. L.; Valpuesta, J. M. The Formation of Symmetrical GroEL-GroES Complexes in the Presence of ATP FEBS Lett. 1994, 345, 181-186 10.1016/0014-5793(94)00432-3
119. 14 Complex Determined at 3.8 Å Reveals Rearrangement Between Two GroEL Rings J. Mol. Biol. 2014, 426, 3634-3641 10.1016/j.jmb.2014.08.017
120. 2 Chaperonin Footballs, the Protein-Folding Functional Form Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 12775-12780 10.1073/pnas.1412922111
121. Nisemblat, S.; Yaniv, O.; Parnas, A.; Frolow, F.; Azem, A. Crystal Structure of the Human Mitochondrial Chaperonin Symmetrical Football Complex Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 6044-6049 10.1073/pnas.1411718112
122. Ma, J.; Sigler, P. B.; Xu, Z.; Karplus, M. A Dynamic Model for the Allosteric Mechanism of GroEL J. Mol. Biol. 2000, 302, 303-313 10.1006/jmbi.2000.4014
123. Ma, J.; Karplus, M. The Allosteric Mechanism of the Chaperonin GroEL: A Dynamic Analysis Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 8502-8507 10.1073/pnas.95.15.8502
124. Shiseki, K.; Murai, N.; Motojima, F.; Hisabori, T.; Yoshida, M.; Taguchi, H. Synchronized Domain-Opening Motion of GroEL Is Essential for Communication Between the Two Rings J. Biol. Chem. 2001, 276, 11335-11338 10.1074/jbc.M010348200
125. 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 10.1021/ja983136u
126. Dyachenko, A.; Gruber, R.; Shimon, L.; Horovitz, A.; Sharon, M. Allosteric Mechanisms Can be Distinguished Using Structural Mass Spectrometry Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 7235-7239 10.1073/pnas.1302395110
127. Shimon, L.; Hynes, G. M.; McCormack, E. A.; Willison, K. R.; Horovitz, A. ATP-Induced Allostery in the Eukaryotic Chaperonin CCT Is Abolished by the Mutation G345D in CCT4 that Renders Yeast Temperature-Sensitive for Growth J. Mol. Biol. 2008, 377, 469-477 10.1016/j.jmb.2008.01.011
128. Lin, P.; Sherman, F. The Unique Hetero-Oligomeric Nature of the Subunits in the Catalytic Cooperativity of the Yeast Cct Chaperonin Complex Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 10780-10785 10.1073/pnas.94.20.10780
129. Amit, M.; Weisberg, S. J.; Nadler-Holly, M.; McCormack, E. A.; Feldmesser, E.; Kaganovich, D.; Willison, K. R.; Horovitz, A. Equivalent Mutations in the Eight Subunits of the Chaperonin CCT Produce Dramatically Different Cellular and Gene Expression Phenotypes J. Mol. Biol. 2010, 401, 532-543 10.1016/j.jmb.2010.06.037
130. Kanzaki, T.; Iizuka, R.; Takahashi, K.; Maki, K.; Masuda, R.; Sahlan, M.; Yébenes, H.; Valpuesta, J. M.; Oka, T.; Furutani, M. et al. Sequential Action of ATP-Dependent Subunit Conformational Change and Interaction Between Helical Protrusions in the Closure of the Built-in-Lid of Group II Chaperonins J. Biol. Chem. 2008, 283, 34773-34784 10.1074/jbc.M805303200
131. Douglas, N. R.; Reissmann, S.; Zhang, J.; Chen, B.; Jakana, J.; Kumar, R.; Chiu, W.; Frydman, J. Dual Action of ATP Hydrolysis Couples Lid Closure to Substrate Release into the Group II Chaperonin Chamber Cell 2011, 144, 240-252 10.1016/j.cell.2010.12.017
132. Burston, S. G.; Ranson, N. A.; Clarke, A. R. The Origins and Consequences of Asymmetry in the Chaperonin Reaction Cycle J. Mol. Biol. 1995, 249, 138-152 10.1006/jmbi.1995.0285
133. Kad, N. M.; Ranson, N. A.; Cliff, M. J.; Clarke, A. R. Asymmetry, Commitment and Inhibition in the GroE ATPase Cycle Impose Alternating Functions on the Two GroEL Rings J. Mol. Biol. 1998, 278, 267-278 10.1006/jmbi.1998.1704
134. Danziger, O.; Shimon, L.; Horovitz, A. Glu257 in GroEL Is a Sensor Involved in Coupling Polypeptide Substrate Binding to Stimulation of ATP Hydrolysis Protein Sci. 2006, 15, 1270-1276 10.1110/ps.062100606
135. Martin, J.; Langer, T.; Boteva, R.; Schramel, A.; Horwich, A. L.; Hartl, F. U. Chaperonin-Mediated Protein Folding at the Surface of GroEL Through a Molten Globule'-Like Intermediate Nature 1991, 352, 36-42 10.1038/352036a0
136. Staniforth, R. A.; Burston, S. G.; Atkinson, T.; Clarke, A. R. Affinity of Chaperonin-60 for a Protein Substrate and Its Modulation by Nucleotides and Chaperonin-10 Biochem. J. 1994, 300, 651-658 10.1042/bj3000651
137. Corsepius, N. C.; Lorimer, G. H. Measuring How Much Work the Chaperone GroEL Can Do Proc. Natl. Acad. Sci. U. S. A. 2013, 110, E2451-E2459 10.1073/pnas.1307837110
138. Fersht, A. R.; Matouschek, A.; Serrano, L. The Folding of an Enzyme: I. Theory of Protein Engineering Analysis of Stability and Pathway of Protein Folding J. Mol. Biol. 1992, 224, 771-782 10.1016/0022-2836(92)90561-W
139. Horovitz, A.; Amir, A.; Danziger, O.; Kafri, G. φ Value Analysis of Heterogeneity in Pathways of Allosteric Transitions: Evidence for Parallel Pathways of ATP-Induced Conformational Changes in a GroEL Ring Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 14095-14097 10.1073/pnas.222303299
140. Inobe, T.; Kuwajima, K. φ Value Analysis of an Allosteric Transition of GroEL Based on a Single-Pathway Model J. Mol. Biol. 2004, 339, 199-205 10.1016/j.jmb.2004.03.026
141. Rye, H. S.; Burston, S. G.; Fenton, W. A.; Beechem, J. M.; Xu, Z.; Sigler, P. B.; Horwich, A. L. Distinct Actions of cis and trans ATP Within the Double Ring of the Chaperonin GroEL Nature 1997, 388, 792-798 10.1038/42047
142. Clare, D. K.; Vasishtan, D.; Stagg, S.; Quispe, J.; Farr, G. W.; Topf, M.; Horwich, A. L.; Saibil, H. R. ATP-Triggered Conformational Changes Delineate Substrate-Binding and -Folding Mechanics of the GroEL Chaperonin Cell 2012, 149, 113-123 10.1016/j.cell.2012.02.047
143. Ranson, N. A.; Farr, G. W.; Roseman, A. M.; Gowen, B.; Fenton, W. A.; Horwich, A. L.; Saibil, H. R. ATP-Bound States of GroEL Captured by Cryo-Electron Microscopy Cell 2001, 107, 869-879 10.1016/S0092-8674(01)00617-1
144. Landry, S. J.; Zeilstra-Ryalls, J.; Fayet, O.; Georgopoulos, C.; Gierasch, L. M. Characterization of a Functionally Important Mobile Domain of GroES Nature 1993, 364, 255-258 10.1038/364255a0
145. Sliozberg, Y.; Abrams, C. F. Spontaneous Conformational Changes in the E. coli GroEL Subunit from All-Atom Molecular Dynamics Simulations Biophys. J. 2007, 93, 1906-1916 10.1529/biophysj.107.108043
146. Danziger, O.; Rivenzon-Segal, D.; Wolf, S. G.; Horovitz, A. Conversion of the Allosteric Transition of GroEL from Concerted to Sequential by the Single Mutation Asp-155-Ala Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 13797-13802 10.1073/pnas.2333925100
147. Yang, Z.; Májek, P.; Bahar, I. Allosteric Transitions of Supramolecular Systems Explored by Network Models: Application to Chaperonin GroEL PLoS Comput. Biol. 2009, 5, e1000360 10.1371/journal.pcbi.1000360
148. Hyeon, C.; Lorimer, G. H.; Thirumalai, D. Dynamics of Allosteric Transitions in GroEL Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 18939-18944 10.1073/pnas.0608759103
149. Tehver, R.; Chen, J.; Thirumalai, D. Allostery Wiring Diagrams in the Transitions that Drive the GroEL Reaction Cycle J. Mol. Biol. 2009, 387, 390-406 10.1016/j.jmb.2008.12.032
150. Kass, I.; Horovitz, A. Mapping Pathways of Allosteric Communication in GroEL by Analysis of Correlated Mutations Proteins: Struct., Funct., Genet. 2002, 48, 611-617 10.1002/prot.10180
151. Skjaerven, L.; Grant, B.; Muga, A.; Teigen, K.; McCammon, J. A.; 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 10.1371/journal.pcbi.1002004
152. Klein, G.; Georgopoulos, C. Identification of Important Amino Acid Residues that Modulate Binding of Escherichia coli GroEL to Its Various Cochaperones Genetics 2001, 158, 507-517
153. Huo, Y.; Hu, Z.; Zhang, K.; Wang, L.; Zhai, Y.; Zhou, Q.; Lander, G.; Zhu, J.; He, Y.; Pang, X. et al. Crystal Structure of Group II Chaperonin in the Open State Structure 2010, 18, 1270-1279 10.1016/j.str.2010.07.009
154. Jayasinghe, M.; Shrestha, P.; Wu, X.; Tehver, R.; Stan, G. Weak Intra-Ring Allosteric Communications of the Archaeal Chaperonin Thermosome Revealed by Normal Mode Analysis Biophys. J. 2012, 103, 1285-1295 10.1016/j.bpj.2012.07.049
155. Zheng, W.; Brooks, B. R.; Thirumalai, D. Allosteric Transitions in the Chaperonin GroEL are Captured by a Dominant Normal Mode That Is Most Robust to Sequence Variations Biophys. J. 2007, 93, 2289-2299 10.1529/biophysj.107.105270
156. Sewell, B. T.; Best, R. B.; Chen, S.; Roseman, A. M.; Farr, G. W.; Horwich, A. L.; Saibil, H. R. A Mutant Chaperonin with Rearranged Inter-Ring Electrostatic Contacts and Temperature-Sensitive Dissociation Nat. Struct. Mol. Biol. 2004, 11, 1128-1133 10.1038/nsmb844
157. E461K J. Struct. Biol. 2006, 155, 482-492 10.1016/j.jsb.2006.06.008
158. Sot, B.; Galán, A.; Valpuesta, J. M.; Bertrand, S.; Muga, A. Salt Bridges at the Inter-Ring Interface Regulate the Thermostat of GroEL J. Biol. Chem. 2002, 277, 34024-34029 10.1074/jbc.M205733200
159. Aharoni, A.; Horovitz, A. Inter-Ring Communication Is Disrupted in the GroEL Mutant Arg13-Gly; Ala126-Val with Known Crystal Structure J. Mol. Biol. 1996, 258, 732-735 10.1006/jmbi.1996.0282
160. Ranson, N. A.; Clare, D. K.; Farr, G. W.; Houldershaw, D.; Horwich, A. L.; Saibil, H. R. Allosteric Signaling of ATP Hydrolysis in GroEL-GroES Complexes Nat. Struct. Mol. Biol. 2006, 13, 147-152 10.1038/nsmb1046
161. Horovitz, A.; Bochkareva, E. S.; Yifrach, O.; Girshovich, A. S. Prediction of an Inter-Residue Interaction in the Chaperonin GroEL from Multiple Sequence Alignment is Confirmed by Double-Mutant Cycle Analysis J. Mol. Biol. 1994, 238, 133-138 10.1006/jmbi.1994.1275
162. Chennubhotla, C.; Bahar, I. Markov Propagation of Allosteric Effects in Biomolecular Systems: Application to GroEL-GroES Mol. Syst. Biol. 2006, 2, 36 10.1038/msb4100075
163. Keskin, O.; Bahar, I.; Flatow, D.; Covell, D. G.; Jernigan, R. L. Molecular Mechanisms of Chaperonin GroEL-GroES Function Biochemistry 2002, 41, 491-501 10.1021/bi011393x
164. Falke, S.; Tama, F.; Brooks, C. L., 3rd.; Gogol, E. P.; Fisher, M. T. The 13 Å Structure of a Chaperonin GroEL-Protein Substrate Complex by Cryo-Electron Microscopy J. Mol. Biol. 2005, 348, 219-230 10.1016/j.jmb.2005.02.027
165. Edelstein, S. J. Extensions of the Allosteric Model for Haemoglobin Nature 1971, 230, 224-227 10.1038/230224a0
166. Kirschner, K.; Gallego, E.; Schuster, I.; Goodall, D. Co-operative Binding of Nicotinamide-Adenine Dinucleotide to Yeast Glyceraldehyde-3-Phosphate Dehydrogenase. I. Equilibrium and Temperature-Jump Studies at pH 8.5 and 40 °C J. Mol. Biol. 1971, 58, 29-50 10.1016/0022-2836(71)90230-0
167. Yifrach, O.; Horovitz, A. Coupling Between Protein Folding and Allostery in the GroE Chaperonin System Proc. Natl. Acad. Sci. U. S. A. 2000, 97, 1521-1524 10.1073/pnas.040449997
168. Betancourt, M. R.; Thirumalai, D. Exploring the Kinetic Requirements for Enhancement of Protein Folding Rates in the GroEL Cavity J. Mol. Biol. 1999, 287, 627-644 10.1006/jmbi.1999.2591
169. Tehver, R.; Thirumalai, D. Kinetic Model for the Coupling Between Allosteric Transitions in GroEL and Substrate Protein Folding and Aggregation J. Mol. Biol. 2008, 377, 1279-1295 10.1016/j.jmb.2008.01.059
170. Netzer, W. J.; Hartl, F. U. Recombination of Protein Domains Facilitated by Co-Translational Folding in Eukaryotes Nature 1997, 388, 343-349 10.1038/41024
171. Jacob, E.; Horovitz, A.; Unger, R. Different Mechanistic Requirements for Prokaryotic and Eukaryotic Chaperonins: A Lattice Study Bioinformatics 2007, 23, i240-i248 10.1093/bioinformatics/btm180
172. Papo, N.; Kipnis, Y.; Haran, G.; Horovitz, A. Concerted Release of Substrate Domains from GroEL by ATP Is Demonstrated with FRET J. Mol. Biol. 2008, 380, 717-725 10.1016/j.jmb.2008.05.021
173. Kipnis, Y.; Papo, N.; Haran, G.; Horovitz, A. Concerted ATP-Induced Allosteric Transitions in GroEL Facilitate Release of Protein Substrate Domains in an All-or-None Manner Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 3119-3124 10.1073/pnas.0700070104
174. Farr, G. W.; Furtak, K.; Rowland, M. B.; Ranson, N. A.; Saibil, H. R.; Kirchhausen, T.; Horwich, A. L. Multivalent Binding of Nonnative Substrate Proteins by the Chaperonin GroEL Cell 2000, 100, 561-573 10.1016/S0092-8674(00)80692-3
175. Sharma, S.; Chakraborty, K.; Müller, B. K.; Astola, N.; Tang, Y. C.; Lamb, D. C.; Hayer-Hartl, M.; Hartl, F. U. Monitoring Protein Conformation Along the Pathway of Chaperonin-Assisted Folding Cell 2008, 133, 142-153 10.1016/j.cell.2008.01.048
176. Fersht, A. R.; Serrano, L. Principles of Protein Stability Derived from Protein Engineering Experiments Curr. Opin. Struct. Biol. 1993, 3, 75-83 10.1016/0959-440X(93)90205-Y
177. Horovitz, A. Putting Handcuffs on the Chaperonin GroEL Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 10884-10885 10.1073/pnas.1309581110
178. Vinckier, A.; Gervasoni, P.; Zaugg, F.; Ziegler, U.; Lindner, P.; Groscurth, P.; Plückthun, A.; Semenza, G. Atomic Force Microscopy Detects Changes in the Interaction Forces Between GroEL and Substrate Proteins Biophys. J. 1998, 74, 3256-3263 10.1016/S0006-3495(98)78032-4
179. Villebeck, L.; Persson, M.; Luan, S. L.; Hammarström, P.; Lindgren, M.; Jonsson, B. H. Conformational Rearrangements of Tail-Less Complex Polypeptide 1 (TCP-1) Ring Complex (TRiC)-Bound Actin Biochemistry 2007, 46, 5083-5093 10.1021/bi062093o
180. Frank, G. A.; 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. U. S. A. 2010, 107, 6270-6274 10.1073/pnas.0910246107
181. Haraguchi, T.; Tominaga, M.; Matsumoto, R.; Sato, K.; Nakano, A.; Yamamoto, K.; Ito, K. Molecular Characterization and Subcellular Localization of Arabidopsis Class VIII Myosin, ATM1 J. Biol. Chem. 2014, 289, 12343-12355 10.1074/jbc.M113.521716
182. Rye, H. S.; Roseman, A. M.; Chen, S.; Furtak, K.; Fenton, W. A.; Saibil, H. R.; Horwich, A. L. GroEL-GroES Cycling: ATP and Nonnative Polypeptide Direct Alternation of Folding-Active Rings Cell 1999, 97, 325-338 10.1016/S0092-8674(00)80742-4
183. Kawe, M.; Plückthun, A. GroEL Walks the Fine Line: The Subtle Balance of Substrate and Co-Chaperonin Binding by GroEL. A Combinatorial Investigation by Design, Selection and Screening J. Mol. Biol. 2006, 357, 411-426 10.1016/j.jmb.2005.12.005
184. Fridmann, Y.; Ulitzur, S.; Horovitz, A. In Vivo and in Vitro Function of GroEL Mutants with Impaired Allosteric Properties J. Biol. Chem. 2000, 275, 37951-37956 10.1074/jbc.M007594200
185. Viitanen, P. V.; Lorimer, G. H.; Seetharam, R.; Gupta, R. S.; Oppenheim, J.; Thomas, J. O.; Cowan, N. J. Mammalian Mitochondrial Chaperonin 60 Functions as a Single Toroidal Ring J. Biol. Chem. 1992, 267, 695-698
186. Nielsen, K. L.; Cowan, N. J. A Single Ring Is Sufficient for Productive Chaperonin-Mediated Folding in Vivo Mol. Cell 1998, 2, 93-99 10.1016/S1097-2765(00)80117-3
187. 2 Complexes are the Protein-Folding Functional Form of the Chaperonin Nanomachine Proc. Natl. Acad. Sci. U. S. A. 2013, 110, E4298-E4305 10.1073/pnas.1318862110
188. 2 Complex Biochem. J. 2010, 427, 247-254 10.1042/BJ20091845
189. Ye, X.; Lorimer, G. H. Substrate Protein Switches GroE Chaperonins from Asymmetric to Symmetric Cycling by Catalyzing Nucleotide Exchange Proc. Natl. Acad. Sci. U. S. A. 2013, 110, E4289-E4297 10.1073/pnas.1317702110
190. Albe, K. R.; Butler, M. H.; Wright, B. E. Cellular Concentrations of Enzymes and Their Substrates J. Theor. Biol. 1990, 143, 163-195 10.1016/S0022-5193(05)80266-8
191. Tran, Q. H.; Unden, G. Changes in the Proton Potential and the Cellular Energetics of Escherichia coli During Growth by Aerobic and Anaerobic Respiration or by Fermentation Eur. J. Biochem. 1998, 251, 538-543 10.1046/j.1432-1327.1998.2510538.x
192. Yamamoto, Y. Y.; Abe, Y.; Moriya, K.; Arita, M.; Noguchi, K.; Ishii, N.; Sekiguchi, H.; Sasaki, Y. C.; Yohda, M. Inter-Ring Communication is Dispensable in the Reaction Cycle of Group II Chaperonins J. Mol. Biol. 2014, 426, 2667-2678 10.1016/j.jmb.2014.05.013
193. Viappiani, C.; Abbruzzetti, S.; Ronda, L.; Bettati, S.; Henry, E. R.; Mozzarelli, A.; Eaton, W. A. Experimental Basis for a New Allosteric Model for Multisubunit Proteins Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 12758-12763 10.1073/pnas.1413566111
194. Hammes, G. G.; Wu, C. W. Regulation of Enzyme Activity. The Activity of Enzymes Can Be Controlled by a Multiplicity of Conformational Equilibria Science 1971, 172, 1205-1211 10.1126/science.172.3989.1205
195. Braig, K.; Adams, P. D.; Brünger, A. T. Conformational Variability in the Refined Structure of the Chaperonin GroEL at 2.8 Å Resolution Nat. Struct. Biol. 1995, 2, 1083-1094 10.1038/nsb1295-1083