Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-05T16:14:44.227Z Has data issue: false hasContentIssue false
  • English
  • Français

Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding

Published online by Cambridge University Press:  29 July 2009

Arthur L. Horwich  and
Wayne A. Fenton
Arthur L. Horwich*
Affiliation:
Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, Connecticut, USA Department of Genetics, Yale University School of Medicine, New Haven, Connecticut, USA
Wayne A. Fenton
Affiliation:
Department of Genetics, Yale University School of Medicine, New Haven, Connecticut, USA
*
*Author for correspondence: Dr. A. L. Horwich, Howard Hughes Medical Institute, Yale University School of Medicine, Boyer Center, 295 Congress Avenue, New Haven, CT 06510, USA. Tel.: 203-737-4431; Fax: 203-737-1761; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The chaperonin ring assembly GroEL provides kinetic assistance to protein folding in the cell by binding non-native protein in the hydrophobic central cavity of an open ring and subsequently, upon binding ATP and the co-chaperonin GroES to the same ring, releasing polypeptide into a now hydrophilic encapsulated cavity where productive folding occurs in isolation. The fate of polypeptide during binding, encapsulation, and folding in the chamber has been the subject of recent experimental studies and is reviewed and considered here. We conclude that GroEL, in general, behaves passively with respect to its substrate proteins during these steps. While binding appears to be able to rescue non-native polypeptides from kinetic traps, such rescue is most likely exerted at the level of maximizing hydrophobic contact, effecting alteration of the topology of weakly structured states. Encapsulation does not appear to involve ‘forced unfolding’, and if anything, polypeptide topology is compacted during this step. Finally, chamber-mediated folding appears to resemble folding in solution, except that major kinetic complications of multimolecular association are prevented.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 42 , Issue 2 , May 2009 , pp. 83 - 116
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

6. References

Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science 181, 223–230.CrossRefGoogle ScholarPubMed
Apetri, A. C. & Horwich, A. L. (2008). Chaperonin chamber accelerates protein folding through passive action of preventing aggregation. Proceedings of the National Academy of Sciences USA 105, 17351–17355.CrossRefGoogle ScholarPubMed
Bhutani, N. & Udgaonkar, J. B. (2000). A thermodynamic coupling mechanism can explain the GroEL-mediated acceleration of the folding of barstar. Journal of Molecular Biology 297, 1037–1044.CrossRefGoogle ScholarPubMed
Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D., 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.CrossRefGoogle Scholar
Braig, K., Simon, M., Furuya, F., Hainfeld, J. F. & Horwich, A. L. (1993). A polypeptide bound to the chaperonin GroEL is localized within a central cavity. Proceedings of the National Academy of Sciences USA 90, 3978–3982.CrossRefGoogle Scholar
Brinker, A., Pfeifer, G., Kerner, M. J., Naylor, D. J., Hartl, F. U. & Hayer-Hartl, M. (2001). Dual function of protein confinement in chaperonin-assisted protein folding. Cell 107, 223–233.CrossRefGoogle ScholarPubMed
Buchner, J., Schmidt, M., Fuchs, M., Jaenicke, R., Rudolph, R., Schmid, F. X. & Kiefhaber, T. (1991). GroE facilitates refolding of citrate synthase by suppressing aggregation. Biochemistry 30, 1586–1591.CrossRefGoogle ScholarPubMed
Buckle, A. M., Zahn, R. & Fersht, A. R. (1997). A structural model for GroEL-polypeptide recognition. Proceedings of the National Academy of Sciences USA 94, 3571–3575.CrossRefGoogle ScholarPubMed
Burnett, B. P., Horwich, A. L. & Low, K. B. (1994). A carboxy-terminal deletion impairs the assembly of GroEL and confers a pleiotropic phenotype in Escherichia coli K12. Journal of Bacteriology 176, 6980–6985.CrossRefGoogle Scholar
Chapman, E., Farr, G. W., Fenton, W. A. & Horwich, A. L. (2008). Requirement for binding multiple ATP's to convert a GroEL ring to the folding-active state. Proceedings of the National Academy of Sciences USA 105, 19205–19210.CrossRefGoogle Scholar
Chapman, E., Farr, G. W., Usaite, R., Furtak, K., Fenton, W. A., Hondorp, E. R., Matthews, R. G., Wolf, S. G., Yates, J. R., Pypaert, M. & Horwich, A. L. (2006). Global aggregation of newly-translated proteins in an E. coli strain deficient of the chaperonin GroEL. Proceedings of the National Academy of Sciences USA 103, 15445–15450.CrossRefGoogle Scholar
Chaudhry, C., Farr, G. W., Todd, M. J., Rye, H. S., Brunger, A. T., Adams, P. D., Horwich, A. L. & Sigler, P. B. (2003). Role of the γ-phosphate of ATP in triggering protein folding by GroEL–GroES: function, structure, and energetics. EMBO Journal 22, 4877–4887.CrossRefGoogle ScholarPubMed
Chaudhuri, T. K., Farr, G. W., Fenton, W. A., Rospert, S. & Horwich, A. L. (2001). GroEL–GroES-mediated folding of a protein too large to be encapsulated. Cell 107, 235–246.CrossRefGoogle ScholarPubMed
Chen, J., Walter, S., Horwich, A. L. & Smith, D. L. (2001). Folding of malate dehydrogenase inside the GroEL–GroES cavity. Nature Structural Biology 8, 721–728.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Chen, S., Roseman, A. M., Hunter, A. S., Wood, S. P., Burston, S. G., Ranson, N. A., Clarke, A. R. & Saibil, H. R. (1994). Location of a folding protein and shape changes in GroEL–GroES complexes imaged by cryo-electron microscopy. Nature 371, 261–264.CrossRefGoogle ScholarPubMed
Cheng, M. Y., Hartl, F. U., Martin, J., Pollock, R. A., Kalousek, F., Neupert, W., Hallberg, E. M., Hallberg, R. L. & Horwich, A. L. (1989). Mitochondrial heat shock protein HSP60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337, 620–625.CrossRefGoogle ScholarPubMed
Clare, D. K., Bakkes, P. J., van Heerikhuizen, H., van der Vies, S. M. & Saibil, H. R. (2009). Chaperonin complex with a newly folded protein encapsulated in the folding chamber. Nature 457, 107–110.CrossRefGoogle ScholarPubMed
Cliff, M. J., Limpkin, C., Cameron, A., Burston, S. G. & Clarke, A. R. (2006). Elucidation of steps in the capture of a protein substrate for efficient encapsulation by GroE. Journal of Biological Chemistry 281, 21266–21275.CrossRefGoogle ScholarPubMed
Deshaies, R. J., Koch, B. D., Werner-Washburne, M., Craig, E. A. & Schekman, R. (1988). A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332, 800–805.CrossRefGoogle ScholarPubMed
Elad, N., Farr, G. W., Clare, D. K., Orlova, E. V., Horwich, A. L. & Saibil, H. R. (2007). Topologies of a substrate protein bound to the chaperonin GroEL. Molecular Cell 26, 415–426.CrossRefGoogle Scholar
Falke, S., Tama, F., Brooks, C. L. 3rd, Gogol, E. P. & Fisher, M. T. (2005). The 13 angstroms structure of a chaperonin GroEL–protein substrate complex by cryo-electron microscopy. Journal of Molecular Biology 348, 219–230.CrossRefGoogle ScholarPubMed
Farr, G. W., Fenton, W. A. & Horwich, A. L. (2007). Perturbed ATPase activity and not ‘close confinement’ of substrate in the cis cavity affects rates of folding by tail-multipled GroEL. Proceedings of the National Academy of Sciences USA 104, 5342–5347.CrossRefGoogle Scholar
Farr, G. W., Furtak, K., Rowland, M. C., Ranson, N. A., Saibil, H. R., Kirchhausen, T. & Horwich, A. L. (2000). Multivalent binding of non-native substrate proteins by the chaperonin GroEL. Cell 100, 561–573.CrossRefGoogle Scholar
Fayet, O., Ziegelhoffer, T. & Georgopoulos, C. P. (1989). The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. Journal of Bacteriology 171, 1379–1385.CrossRefGoogle ScholarPubMed
Fenton, W. A. & Horwich, A. L. (2003). Chaperonin-mediated protein folding: fate of substrate polypeptide. Quarterly Reviews of Biophysics 36, 229–256.CrossRefGoogle ScholarPubMed
Fenton, W. A., Kashi, Y., Furtak, K. & Horwich, A. L. (1994). Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371, 614–619.CrossRefGoogle ScholarPubMed
Gervasoni, P., Staudenmann, W., James, P., Gehrig, P. & Plückthun, A. (1996). β-lactamase binds to GroEL in a conformation highly protected against hydrogen/deuterium exchange. Proceedings of the National Academy of Sciences USA 93, 12189–12194.CrossRefGoogle Scholar
Gervasoni, P., Staudenmann, W., James, P. & Plückthun, A. (1998). Identification of the binding surface on β-lactamase for GroEL by limited proteolysis and MALDI-mass spectrometry. Biochemistry 37, 11660–11669.CrossRefGoogle ScholarPubMed
Goldberg, M. S., Zhang, J., Sondek, S., Matthews, C. R., Fox, R. O. & Horwich, A. L. (1997). Native-like structure of a protein-folding intermediate bound to the chaperonin GroEL. Proceedings of the National Academy of Sciences USA 94, 1080–1085.CrossRefGoogle Scholar
Goloubinoff, P., Christeller, J. T., Gatenby, A. A. & Lorimer, G. H. (1989). Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and MgATP. Nature 342, 884–889.CrossRefGoogle ScholarPubMed
Groß, M., Robinson, C. V., Mayhew, M., Hartl, F. U. & Radford, S. E. (1996). Significant hydrogen exchange protection in GroEL-bound DHFR is maintained during iterative rounds of substrate cycling. Protein Science 5, 2506–2513.CrossRefGoogle ScholarPubMed
Hayer-Hartl, M., Ewbank, J. J., Creighton, T. E. & Hartl, F. U. (1994). Conformational specificity of the chaperonin GroEL for the compact folding intermediates of α-lactalbumin. EMBO Journal 13, 3192–3202.CrossRefGoogle ScholarPubMed
Herendeen, S. L., van Bogelen, R. A. & Neidhardt, F. C. (1979). Levels of major proteins of Escherichia coli during growth at different temperatures. Journal of Bacteriology 139, 185–194.CrossRefGoogle ScholarPubMed
Hillger, F., Hänni, D., Nettels, D., Geister, S., Grandin, M., Textor, M. & Schuler, B. (2008). Probing protein–chaperone interactions with single-molecule fluorescence spectroscopy. Angewandte Chemie 47, 6184–6188.CrossRefGoogle Scholar
Hinnerwisch, J., Fenton, W. A., Farr, G. W., Furtak, K. & Horwich, A. L. (2005). Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121, 1029–1041.CrossRefGoogle ScholarPubMed
Horst, R., Bertelsen, E. B., Fiaux, J., Wider, G., Horwich, A. L. & Wüthrich, K. (2005). Direct NMR observation of a substrate protein bound to the chaperonin GroEL. Proceedings of the National Academy of Sciences USA 102, 12748–12753.CrossRefGoogle Scholar
Horst, R., Fenton, W. A., Englander, S. W., Wüthrich, K. & Horwich, A. L. (2007). Folding trajectories of human dihydrofolate reductase inside the GroEL–GroES chaperonin cavity and free in solution. Proceedings of the National Academy of Sciences USA 104, 20788–20792.CrossRefGoogle ScholarPubMed
Horwich, A. L., Farr, G. W. & Fenton, W. A. (2006). GroEL–GroES-mediated protein folding. Chemical Reviews 106, 1917–1930.CrossRefGoogle ScholarPubMed
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. Journal of Molecular Biology 327, 183–191.CrossRefGoogle ScholarPubMed
Itzhaki, L. S., Otzen, D. E. & Fersht, A. R. (1995). Nature and consequences of GroEL-protein interactions. Biochemistry 34, 14581–14587.CrossRefGoogle ScholarPubMed
Kawata, Y., Kawagoe, M., Hongo, K., Miyazaki, T., Higurashi, T., Mizobata, T. & Nagai, J. (1999). Functional communications between the apical and equatorial domains of GroEL through the intermediate domain. Biochemistry 38, 15731–15740.CrossRefGoogle ScholarPubMed
Kipnis, Y., Papo, N., Haran, G. & Horovitz, A. (2007). Concerted ATP-induced allosteric transitions in GroEL facilitate release of protein substrate domains in an all-or-none manner. Proceedings of the National Academy of Sciences USA 104, 3119–3124.CrossRefGoogle Scholar
Langer, T., Pfeifer, G., Martin, J., Baumeister, W. & Hartl, F. U. (1992). Chaperonin-mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. EMBO Journal 11, 4757–4765.CrossRefGoogle ScholarPubMed
Li, Y., Gao, X. & Chen, L. (2009). GroEL recognizes an amphipathic helix and binds to the hydrophobic side. Journal of Biological Chemistry 284, 4324–4331.CrossRefGoogle Scholar
Lin, Z. & Rye, H. S. (2004). Expansion and compression of a protein folding intermediate by GroEL. Molecular Cell 16, 23–34.CrossRefGoogle ScholarPubMed
Lin, Z., Schwarz, F. P. & Eisenstein, E. (1995). The hydrophobic nature of GroEL-substrate binding. Journal of Biological Chemistry 270, 1011–1014.CrossRefGoogle ScholarPubMed
Lin, Z., Madan, Z. & Rye, H. S. (2008). GroEL stimulates protein folding through forced unfolding. Nature Structural & Molecular Biology 15, 303–311.CrossRefGoogle ScholarPubMed
Madan, D., Lin, Z. & Rye, H. S. (2008). Triggering protein folding within the GroEL–GroES complex. Journal of Biological Chemistry 283, 32003–32013.CrossRefGoogle ScholarPubMed
Ma, J. & Karplus, M. (1999). The allosteric mechanism of the chaperonin GroEL: a dynamic analysis. Proceedings of the National Academy of Sciences USA 92, 8502–8507.Google Scholar
Mayhew, M., da Silva, A. C. R., Martin, J., Erdjument-Bromage, H., Tempst, P. & Hartl, F. U. (1996). Protein folding in the central cavity of the GroEL–GroES chaperonin complex. Nature 379, 420–426.CrossRefGoogle ScholarPubMed
McLennan, N. F., McAteer, S. & Masters, M. (1994). The tail of a chaperonin: the C-terminal region of Escherichia coli GroEL protein. Molecular Microbiology 14, 309–321.CrossRefGoogle ScholarPubMed
Mendoza, J. A., Rogers, E., Lorimer, G. H. & Horowitz, P. M. (1991). Chaperonin facilitates the in vitro folding of monomeric mitochondrial rhodanese. Journal of Biological Chemistry 266, 13044–13049.CrossRefGoogle ScholarPubMed
Miyazaki, T., Yoshimi, T., Furutsu, Y., Hongo, K., Mizobata, T., Kanemori, M. & Kawata, Y. (2002). GroEL-substrate-GroES ternary complexes are an important transient intermediate of the chaperonin cycle. Journal of Biological Chemistry 277, 50621–50628.CrossRefGoogle ScholarPubMed
Motojima, F., Chaudhry, C., Fenton, W. A., Farr, G. W. & Horwich, A. L. (2004). Substrate polypeptide presents a load on the apical domains of the chaperonin GroEL. Proceedings of the National Academy of Sciences USA 101, 15005–15012.CrossRefGoogle ScholarPubMed
Nojima, T., Murayama, S., Yoshida, M. & Motojima, F. (2008). Determination of the number of active GroES subunits in the fused heptamer GroES required for interactions with GroEL. Journal of Biological Chemistry 283, 18385–18392.CrossRefGoogle ScholarPubMed
Ojha, A., Anand, M., Bhatt, A., Kremer, L., Jacobs, W. R. Jr. & Hatfull, G. F. (2005). GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123, 861–873.CrossRefGoogle ScholarPubMed
Okazaki, A., Ikura, T., Nikaido, K. & Kuwajima, K. (1994). The chaperonin GroEL does not recognize apo-α-lactalbumin in the molten globule state. Nature Structural Biology 1, 439–446.CrossRefGoogle Scholar
Ostermann, J., Horwich, A. L., Neupert, W. & Hartl, F. U. (1989). Protein folding in mitochondria requires complex formation with HSP60 and ATP hydrolysis. Nature 341, 125–130.CrossRefGoogle ScholarPubMed
Papo, N., Kipnis, Y., Haran, G. & Horovitz, A. (2008). Concerted release of substrate domains from GroEL by ATP is demonstrated with FRET. Journal of Molecular Biology 380, 717–725.CrossRefGoogle ScholarPubMed
Park, E. S., Fenton, W. A. & Horwich, A. L. (2005). No evidence for a forced-unfolding mechanism during ATP/GroES binding to substrate-bound GroEL: no observable protection of metastable Rubisco intermediate, or GroEL-bound Rubisco from tritium exchange. FEBS Letters 579, 1183–1186.CrossRefGoogle ScholarPubMed
Pelham, H. R. (1984). Hsp70 accelerates the recovery of nucleolar morphology after heat shock. EMBO Journal 3, 3095–3100.CrossRefGoogle ScholarPubMed
Pelham, H. R. (1986). Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46, 959–961.CrossRefGoogle ScholarPubMed
Peralta, D., Hartman, D. J., Hoogenraad, N. J. & Høj, P. B. (1994). Generation of a stable folding intermediate which can be rescued by the chaperonins GroEL and GroES. FEBS Letters 339, 45–49.CrossRefGoogle ScholarPubMed
Preuss, M., Hutchinson, J. P. & Miller, A. D. (1999). Secondary structure forming propensity coupled with amphiphilicty is an optimal motif in a peptide, or protein for association with chaperonin 60 (GroEL). Biochemistry 38, 10272–10286.CrossRefGoogle ScholarPubMed
Ranson, N. A., Burston, S. G. & Clarke, A. R. (1997). Binding, encapsulation and ejection: substrate dynamics during a chaperonin-assisted folding reaction. Journal of Molecular Biology 266, 656–664.CrossRefGoogle ScholarPubMed
Ranson, N. A., Dunster, N. J., Burston, S. G. & Clarke, A. R. (1995). Chaperonins can catalyse the reversal of early aggregation steps when a protein misfolds. Journal of Molecular Biology 250, 581–586.CrossRefGoogle Scholar
Ranson, N. A., Farr, G. W., Roseman, A. M., Gowen, B., Fenton, W. A., Horwich, A. L. & Saibil, H. R. (2001). ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107, 869–879.CrossRefGoogle ScholarPubMed
Reading, D. S., Hallberg, R. L. & Myers, A. M. (1989). Characterization of the yeast HSP60 gene coding for a mitochondrial assembly factor. Nature 337, 655–659.CrossRefGoogle ScholarPubMed
Rivenzon-Segal, D., Wolf, S. G., Shimon, L., Willison, K. R. & Horovitz, A. (2005). Sequential ATP-induced allosteric transitions of the cytoplasmic chaperonin containing TCP-1 revealed by EM analysis. Nature Structural & Molecular Biology 12, 233–237.CrossRefGoogle ScholarPubMed
Robinson, C. V., Gross, M., Eyles, S. J., Ewbank, J. J., Mayhew, M., Hartl, F. U., Dobson, C. M. & Radford, S. E. (1994). Conformation of GroEL-bound alpha-lactalbumin probed by mass spectrometry. Nature 372, 646–651.CrossRefGoogle ScholarPubMed
Rye, H. S., Burston, S. G., Fenton, W. A., Beechem, J. M., Xu, Z., Sigler, P. B. & Horwich, A. L. (1997). Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388, 792–798.CrossRefGoogle ScholarPubMed
Rye, H. S., Roseman, A. M., Furtak, K., Fenton, W. A., Saibil, H. R. & Horwich, A. L. (1999). GroEL–GroES cycling: ATP and non-native polypeptide direct alternation of folding-active rings. Cell 97, 325–338.CrossRefGoogle Scholar
Saibil, H. R., Zheng, D., Roseman, A. M., Hunter, A. S., Watson, G. M., Chen, S., Auf der Mauer, A., O'Hara, B. P., Wood, S. P., Mann, N. H., Barnett, L. K. & Ellis, R. J. (1993). ATP induces large quaternary rearrangements in a cage-like chaperonin structure. Current Biology: CB 3, 265–273.Google Scholar
Sauer, R. T., Bolon, D. N., Burton, B. M., Burton, R. E., Flynn, J. M., Grant, R. A., Hersch, G. L., Joshi, S. A., Kenniston, J. A., Levchenko, I., Neher, S. B., Oakes, E. S., Siddiqui, S. M., Wah, D. A. & Baker, T. A. (2004). Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 119, 9–18.CrossRefGoogle ScholarPubMed
Schmidt, M. & Buchner, J. (1992). Interaction of GroE with an All-β-protein. Journal of Biological Chemistry 267, 16829–16833.CrossRefGoogle ScholarPubMed
Sharma, S., Chakraborty, K., Müller, B. K., Astola, N., Tang, Y. C., Lamb, D. C., Hayer-Hartl, M. & Hartl, F. U. (2008). Monitoring protein conformation along the pathway of chaperonin-assisted folding. Cell 133, 142–153.CrossRefGoogle ScholarPubMed
Shewmaker, F., Maskos, K., Simmerling, C. & Landry, S. J. (2001). The disordered mobile loop of GroES folds into a defined β-hairpin upon binding GroEL. Journal of Biological Chemistry 276, 31257–31264.CrossRefGoogle ScholarPubMed
Shtilerman, M., Lorimer, G. H. & Englander, S. W. (1999). Chaperonin function: folding by forced unfolding. Science 284, 822–825.CrossRefGoogle ScholarPubMed
Smith, K. E. & Fisher, M. T. (1995). Interactions between the GroE chaperonins and rhodanese. Multiple intermediates and release and rebinding. Journal of Biological Chemistry 270, 21517–21523.CrossRefGoogle ScholarPubMed
Sprangers, R. & Kay, L. E. (2007). Quantitative dynamics and binding studies of the 20S proteasome by NMR. Nature 445, 618–622.CrossRefGoogle ScholarPubMed
Taguchi, H. & Yoshida, M. (1995). Chaperonin releases the substrate protein in a form with tendency to aggregate and ability to rebind to chaperonin. FEBS Letters 359, 195–198.CrossRefGoogle Scholar
Tang, Y.-C., Chang, H.-C., Roeben, A., Wischnewski, D., Wischnewski, N., Kerner, M. J., Hartl, F. U. & Hayer-Hartl, M. (2006). Structural features of the GroEL–GroES nano-cage required for rapid folding of encapsulated protein. Cell 125, 903–914.CrossRefGoogle ScholarPubMed
Taniguchi, M., Yoshimi, T., Hongo, K., Mizobata, T. & Kawata, Y. (2004). Stopped-flow fluorescent analysis of the conformational changes in the GroEL apical domain. Journal of Biological Chemistry 279, 16368–16376.CrossRefGoogle ScholarPubMed
Thiyagarajan, P., Henderson, S. J. & Joachimiak, A. (1996). Solution structures of GroEL and its complex with rhodanese from small-angle neutron scattering. Structure 4, 79–88.CrossRefGoogle ScholarPubMed
Tian, G., Vainberg, I. E., Tap, W. D., Lewis, S. A. & Cowan, N. J. (1995). Specificity in chaperonin-mediated protein folding. Nature 375, 250–253.CrossRefGoogle ScholarPubMed
Todd, M. J., Lorimer, G. H. & Thirumalai, D. (1996). Chaperonin-facilitated protein folding: optimization of rate and yield by an iterative annealing mechanism. Proceedings of the National Academy of Sciences USA 93, 4030–4035.CrossRefGoogle ScholarPubMed
Todd, M. J., Viitanen, P. V. & Lorimer, G. H. (1994). Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265, 659–666.CrossRefGoogle ScholarPubMed
Viitanen, P. V., Gatenby, A. A. & Lorimer, G. H. (1992). Purified chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins. Protein Science 1, 363–369.CrossRefGoogle ScholarPubMed
Viitanen, P. V., Lubben, T. H., Reed, J., Goloubinoff, P., O'Keefe, D. P. & Lorimer, G. H. (1990). Chaperonin-facilitated refolding of ribulosebisphosphate carboxylase and ATP hydrolysis by chaperonin 60 (groEL) are K+ dependent. Biochemistry 29, 5665–5671.CrossRefGoogle ScholarPubMed
Walter, S., Lorimer, G. H. & Schmid, F. X. (1996). A thermodynamic coupling mechanism for GroEL-mediated unfolding. Proceedings of the National Academy of Sciences USA 93, 9425–9430.CrossRefGoogle ScholarPubMed
Wang, W., Hwa-Ping, F., Landry, S. J., Maxwell, J. & Gierasch, L. M. (1999). Basis of substrate binding by the chaperonin GroEL. Biochemistry 38, 12537–12546.CrossRefGoogle ScholarPubMed
Weissman, J. S., Hohl, C. M., Kovalenko, O., Chen, S., Braig, K., Saibil, H. R., Fenton, W. A. & Horwich, A. L. (1995). Mechanism of GroEL action: productive release of polypeptide from a sequestered position under GroES. Cell 83, 577–587.CrossRefGoogle ScholarPubMed
Weissman, J. S., Kashi, Y., Fenton, W. A. & Horwich, A. L. (1994). GroEL-mediated protein folding proceeds by multiple rounds of release and rebinding of non-native forms. Cell 78, 693–702.CrossRefGoogle Scholar
Weissman, J. S., Rye, H. S., Fenton, W. A., Beechem, J. M. & Horwich, A. L. (1996). Characterization of the active intermediate of a GroEL–GroES-mediated folding reaction. Cell 84, 481–490.CrossRefGoogle ScholarPubMed
Xu, Z., Horwich, A. L. & Sigler, P. B. (1997). The crystal structure of the asymmetric GroEL–GroES-(ADP)7 chaperonin complex. Nature 388, 741–751.CrossRefGoogle ScholarPubMed
Yifrach, O. & Horovitz, A. (1995). Nested cooperativity in the ATPase activity in the oligomeric chaperonin GroEL. Biochemistry 34, 9716–9723.CrossRefGoogle ScholarPubMed
Yifrach, O. & Horovitz, A. (1998). Transient kinetic analysis of adenosine 5′ triphosphate binding-induced conformational changes in the allosteric chaperonin GroEL. Biochemistry 37, 7083–7088.CrossRefGoogle ScholarPubMed
Zahn, R. & Plückthun, A. (1994). Thermodynamic partitioning model for hydrophobic binding of polypeptides by GroEL: II. GroEL recognizes thermally unfolded mature β-lactamase. Journal of Molecular Biology 242, 165–174.CrossRefGoogle ScholarPubMed
Zahn, R., Spitzfaden, C., Ottiger, M., Wüthrich, K. & Plückthun, A. (1994). Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature 368, 261–265.CrossRefGoogle Scholar