Structures of unliganded and ATP-bound states of the Escherichia coli chaperonin GroEL by cryoelectron microscopy

Journal of Structural Biology

Volumn 135, Issue 2, 2001, Pages 115-125

  Roseman, Alan M ^a,c   Ranson, Neil A ^a   Gowen, Brent ^b,d   Fuller, Stephen D ^b,d   Saibil, Helen R ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

3D reconstruction; ATP binding; Chaperonin; Cryoelectron microscopy; Molecular chaperone

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN;

ARTICLE; BINDING SITE; CRYOELECTRON MICROSCOPY; ENCAPSULATION; HYDROLYSIS; IMAGE RECONSTRUCTION; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION; PROTEIN STRUCTURE;

ESCHERICHIA COLI;

EID: 0035783162     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.2001.4374     Document Type: Article

References (41)

1. Boisvert, D. C., Wang, J., Otwinowski, Z., Horwich, A. L., and Sigler, P. B. (1996) The 2.4 Å crystal structure of the bacterial chaperonin GroEL complexed with ATPγS. Nat. Struct. Biol. 3, 170-177.
2. Böttcher, B., Wynne, S. A., and Crowther, R. A. (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386, 88-91.
3. Braig, K., Otwinowski, Z., Hegde., R., Boisvert, D. C., Joachimiak, A., Horwich, A. L., and Sigler, P. B. (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371, 578-586.
4. Bukau, B., and Horwich, A. L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
5. Burston, S. G., Ranson, N. A., and Clarke, A. R. (1995) The origins and consequences of asymmetry in the chaperonin reaction cycle. J. Mol. Biol. 249, 138-152.
6. Burston, S. G., Weissman, J. S., Farr, G. W., Fenton, W. A., and Horwich, A. L. (1996) Release of both native and non-native proteins from a cis-only GroEL ternary complex. Nature 383, 96-99.
7. Chandrasekhar, G. N., Tilly, K., Woolford, C., Hendrix, R., and Georgopoulos, C. (1986) Purification and properties of the groES morphogenetic protein of Escherichia coli. J. Biol. Chem. 261, 12414-12419.
8. Chen, S., Roseman, A. M., Hunter, A. S., Wood, S. P., Burston, S. G., Ranson, N. A., Clarke, A. R., and 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.
9. Conway, J. F., Cheng, N., Zlotnick, A., Wingfield, P. T., Stahl, S. J., and Steven, A. C. (1997) Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature 386, 91-94.
10. Crowther, R. A., Henderson, R., and Smith J. (1996) MRC image processing programs. J. Struct. Biol. 116, 9-16.
11. Dubochet, J., Adrian, M., Chang, J. J., Homo, J. C., Lepault, J., McDonnall, A. W., and Schultz, P. (1988) Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21, 129-228.
12. Farr, G. W., Furtak, K., Rowland, M. B., Ranson, N. A., Saibil, H. R., Kirchhausen, T., and Horwich, A. L. (2000) Multivalent binding of non-native substrate proteins by the chaperonin GroEL. Cell 100, 561-573.
13. Fayet, O., Ziegelhoffer, T., and Georgopoulos, C. (1989) The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J. Bacteriol. 171, 1379-1385.
14. Fenton, W. A., Kashi, Y., Furtak, K., and Horwich, A. L. (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371, 614-619.
15. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., and Leith, A. (1996) Spider and Web: Processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199.
16. Gray, T. E., and Fersht, A. R. (1991) Cooperativity in ATP hydrolysis by GroEL is increased by GroES. FEBS Lett. 292, 254-258.
17. Hartl, F. U. (1996) Molecular chaperones in cellular protein folding. Nature 381, 571-579.
18. Jackson, G. S., Staniforth, R. A., Halsall, D. J., Atkinson, T., Holbrook, J. J., Clarke, A. R., and Burston, S. G. (1993) Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle: Implications for the mechanism of assisted protein folding. Biochemistry 32, 2554-2563.
19. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building models in electron density maps and the location of errors in these models. Acta Crystallogr. Sect. A 47, 110-119.
20. Kad, N. M., Ranson, N. A., Cliff, M. J., and Clarke, A. R. (1998) Asymmetry, commitment and inhibition in the GroE ATPase cycle impose alternating functions on the two GroEL rings. J. Mol. Biol. 278, 267-278.
21. Malhotra, A., Penczek, P., Agrawal, R. K., Gabashvili, I. S., Grassucci, R. A., Junemann, R., Burkhardt, N., Nierhaus, K. H., and Frank, J. (1998) Escherichia coli 70 S ribosome at 15 Å resolution by cryo-electron microscopy: Localization of fMet-tRNAfMet and fitting of L1 protein. J. Mol. Biol. 280, 103-116.
22. Mayhew, M., da Silva, A. C., Martin, J., Erdjument-Bromage, H., Tempst, P., and Hartl, F. U. (1996) Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 379, 420-426.
23. Ranson, N. A., Burston, S. G., and Clarke, A. R. (1997) Binding, encapsulation and ejection: Substrate dynamics during a chaperonin-assisted folding reaction. J. Mol. Biol. 266, 656-664.
24. Ranson, N. A., White, H. E., and Saibil, H. R. (1998) Chaperonins. Biochem. J. 333, 233-242.
25. Roseman, A. M. (2000) Docking structures of domains into maps from cryo-electron microscopy using local correlation. Acta Crystallogr. Sect. D 56, 1332-1340.
26. Roseman, A., Chen, S., White, H., Braig, K., and Saibil, H. (1996) The chaperonin ATPase cycle: Mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87, 241-251.
27. Rye, H. S., Burston, S. G., Fenton, W. A., Beechem, J. M., Xu, Z., Sigler, P. B., and Horwich, A. L. (1997) Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388, 792-798.
28. Rye, H. S., Roseman, A. M., Chen, S., Furtak, K., Fenton, W. A., Saibil, H. R., and Horwich, A. L. (1999) GroEL-GroES cycling: ATP and non-native polypeptide direct alternation of folding active rings. Cell 97, 325-338.
29. Shtilerman, M., Lorimer, G. H., and Englander, S. W. (1999) Chaperonin function: Folding by forced unfolding. Science 284, 822-825.
30. Sigler, P. B., Xu, Z., Rye, H. S., Burston, S. G., Fenton, W. A., and Horwich, A. L. (1998) Structure and function in GroEL-mediated protein folding. Annu. Rev. Biochem. 67, 581-608.
31. Staniforth, R. A., Burston, S. G., Atkinson, T., and Clarke, A. R. (1994) Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. Biochem. J. 300, 651-658.
32. Stewart, P. L., Fuller, S. D., and Burnett, R. M. (1993) Difference imaging of adenovirus: Bridging the resolution gap between X-ray crystallography and electron microscopy. EMBO J. 12, 2589-2599.
33. Todd, M. J., Viitanen, P. V., and Lorimer, G. H. (1994) Dynamics of the chaperonin ATPase cycle: Implications for facilitated protein folding. Science 265, 659-666.
34. van Heel, M., Harauz, G., Orlova, E., Schmidt, R., and Schatz, M. (1996) A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24.
35. Weissman, J. S., Hohl, C. M., Kovalenko, O., Kashi, Y., Chen, S., Braig, K., Saibil, H. R., Fenton, W. A., and Horwich, A. L. (1995) Mechanism of GroEL action: Productive release of polypeptide from a sequestered position under GroES. Cell 83, 577-587.
36. Weissman, J. S., Kashi, Y., Fenton, W. A., and Horwich A. L. (1994) GroEL-mediated protein folding proceeds by multiple rounds of binding and release of non-native forms. Cell 78, 693-702.
37. Weissman, J. S., Rye, H. S., Fenton, W. A., Beechem, J. M., and Horwich, A. L. (1996) Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 84, 481-490.
38. White, H., Chen, S., Roseman, A., Yifrach, O., Horovitz, A., and Saibil, H. (1997) Structural basis of allosteric changes in the GroEL mutant Arg197 → Ala. Nat. Struct. Biol. 4, 690-694.
39. 7 chaperonin complex. Nature 388, 741-750.
40. Yifrach, O., and Horovitz, A. (1994) Two lines of allosteric communication in the oligomeric chaperonin GroEL are revealed by the single mutation Arg196 → Ala. J. Mol. Biol. 243, 397-401.
41. Yifrach, O., and Horovitz, A. (1995) Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34, 5303-5308.