Chaperonins

Current Opinion in Structural Biology

Volumn 8, Issue 2, 1998, Pages 159-165

  Braig, Kerstin ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN;

CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW;

EID: 0032053508     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(98)80033-X     Document Type: Article

References (56)

1. Anfinsen CB. Principles that govern the folding of protein chains. Science. 181:1973;223-257.
2. Buchner J. Supervising the fold: functional principles of molecular chaperones. FASEB J. 10:1996;10-19.
3. Hartl FU. Molecular chaperones in cellular protein folding. of special interest Nature. 381:1996;571-580 An excellent introduction to the field of molecular chaperones and assisted protein folding, with special emphasis on the hsp70 family and GroEL.
4. Ellis RJ. Proteins as molecular chaperones. Nature. 328:1987;378-379.
5. Frydman J, Hohfeld J. Chaperones get in touch: the Hip-Hop connection. Trends Biochem Sci. 22:1997;87-92.
6. Buchberger A, Schroder H, Hesterkamp T, Schonfeld HJ, Bukau B. Substrate shuttling between the DnaK and GroEL systems indicates a chaperone network promoting protein folding. of outstanding interest J Mol Biol. 261:1996;328-333 Studies with denatured luciferase show that DnaK and GroEL compete for binding to non-native proteins; therefore, in this folding reaction, DnaK and GroEL do not necessarily act in succession by promoting earlier or later folding steps, but rather form a lateral network of proteins.
7. Farr GW, Scharl EC, Schumacher RJ, Sondek S, Horwich AL. Chaperonin-mediated folding in the eukaryotic cytosol proceeds through rounds of release of native and nonnative forms. of outstanding interest Cell. 89:1997;927-937 This study examines the fate of newly synthesized cytosolic proteins bound to CCT in reticulocyte lysate and Xenopus oocytes. In both cases, the production of the native protein is strongly inhibited by the introduction of a chaperonin trap, which is able to bind but not to release substrate protein. The overall mechanism of CCT-assisted protein folding resembles that of GroEL (see annotation [48]).
8. Lewis VA, Heynes GM, Zheng D, Sailbil H, Willison K. T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukaryotic cytosol. Nature. 358:1992;249-252.
9. Phipps BM, Typke D, Hegerl R, Volker S, Hoffmann A, Stetter KO, Baumeister W. Structure of a molecular chaperone from a thermophilic archaebacterium. Nature. 361:1993;475-477.
10. Trent JD, Nimmesgern E, Wall J, Hartl FU, Horwich AL. A molecular chaperone from the thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide-1. Nature. 354:1991;490-493.
11. Kubota H, Hynes G, Willison K. The chaperonin containing t-complex polypeptide 1 (TCP-1) multisubunit machinery assisting in protein folding and assembly in the eukaryotic cytosol. Eur J Biochem. 230:1995;3-16.
12. Knapp S, Schmidt-Krey I, Herbert H, Bergman T, Jornvall H, Ladenstein R. The molecular chaperonin TF55 from the thermophilic archeon Sulfolobus solfataricus. A biochemical and structural characterization. J Mol Biol. 242:1994;397-407.
13. Rommelaere H, van Troys M, Gao Y, Melki R, Cowan NJ, Vandekerckhove J, Ampe C. The eukaryotic cytosolic chaperonin contains t-complex polypeptide and several related subunits. Proc Natl Acad Sci USA. 90:1993;11975-11979.
14. Kubota H, Hynes G, Carne A, Ashworth A, Willison K. Identification of six Tep-1 related genes encoding divergent subunits of the TCP-1-containing chaperonin. Curr Biol. 4:1994;89-99.
15. Gao Y, Thomas JO, Chow RL, Lee GH, Cowan NJ. A cytoplasmic chaperonin that catalyzes β-actin folding. Cell. 69:1992;1043-1050.
16. Lewis SA, Tian G, Vainberg IE, Cowan NJ. Chaperonin-mediated folding of actin and tubulin. J Cell Biol. 132:1996;1-4.
17. Yaffe MB, Farr GW, Miklos D, Horwich AL, Sternlicht ML, Sternlicht H. TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature. 358:1992;245-258.
18. Frydman J, Nimmesgern E, Ohtsuka K, Hartl FU. Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature. 353:1994;111-117.
19. Sternlicht H, Farr GW, Sternlicht ML, Driscoll JK, Willison K, Yaffe M. The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc Natl Acad Sci USA. 90:1993;9422-9426.
20. Roobol A, Holmes FE, Hayes NVL, Baines AJ, Carden AJ. Cytoplasmic chaperonin complexes enter neurites developing in vitro and differ in subunit composition within single cells. J Cell Sci. 108:1995;1477-1488.
21. Braig K, Simon M, Furuya F, Hainfeld JF, Horwich AL. A polypeptide bound by the chaperonin groEL is localized within a central cavity. Proc Natl Acad Sci. 90:1993;3978-3982.
22. Zahn R, Buckle AM, Perret S, Johnson CM, Corrales FJ, Golbik R, Fersht AR. Chaperonin activity and structure of monomeric polyeptide binding domains of GroEL. of special interest Proc Natl Acad Sci USA. 93:1996;15024-15029 The crystal structure of a monomeric polypeptide that corresponds to the apical domain of GroEL shows a well-ordered structure with the same fold as that of native GroEL. The isolated domain functions as a minichaperone (see annotation [33]).
23. Groß M, Robinson CV, Mayhew M, Hartl FU, Radford SE. Significant hydrogen exchange protection in GroEL-bound DHFR is maintained during iterative rounds of substrate cycling. of special interest Protein Sci. 5:1996;2506-2513 Structural analysis using hydrogen exchange labeling reveals that during several cycles of GroEL-assisted folding of dihydrofolate reductase the protein is partially folded rather than being completely unfolded upon binding to GroEL.
24. Goldberg MS, Zhang J, Sondek S, Matthews CR, Fox RO, Horwich AL. Native-like structure of a protein-folding intermediate bound by the chaperonin GroEL. of outstanding interest Proc Natl Acad Sci USA. 94:1997;1080-1085 The structure of DHFR bound to GroEL was analyzed using hydrogen - deuterium exchange and NMR spectroscopy. The data indicate that central structural elements found in the native protein are also present in the GroEL-bound form of the protein. Since these structural elements are derived from distant parts of the primary structure, the authors conclude that a native-like global topology is present in folding intermediates that are bound to GroEL.
25. Lilie H, Buchner J. Interaction of GroEL with a highly structured folding intermediate: iterative binding cycles do not involve unfolding. Proc Natl Acad Sci USA. 92:1995;8100-8104.
26. Braig K, Otwinowski Z, Hedge R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å resolution. Nature. 371:1994;578-586.
27. Chen S, Roseman AM, Hunter AS, Wood SP, Burston SG, Ranson NA, Clarke AR, Saibil HR. Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryoelectron microscopy. Nature. 371:1994;261-264.
28. Thiyagarajan P, Henderson SJ, Joachimiak A. Solution structures of GroEL and its complex with rhodanase from small-angle neutron scattering. Structure. 4:1996;79-88.
29. Boisvert DC, Wang J, Otwinowski Z, Horwich AL, Sigler PB. The 2.4 Å crystal structure of the bacterial chaperonin GroEL complex with ATPγS. Nat Struct Biol. 3:1996;170-177.
30. Braig K, Adams P, Brunger AT. Conformational variability in the refined structure of the chaperonin GroEL at 2.8 Å resolution. Nat Struct Biol. 2:1995;1083-1093.
31. Ewalt KL, Hendrick JP, Houry WA, Hartl FU. In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell. 90:1997;491-500.
32. Lorimer GH. A quantitative assessment of the role of chaperonin proteins in protein folding in vivo. of special interest FASEB J. 10:1996;5-9 "What proportion of all the proteins of Escherichia coli reach their native states with the assistance of the chaperonins proteins, GroEL and GroES?" The author provides an easy to follow calculation to answer that question for a given E. coli strain under standard conditions.
33. Buckle AM, Zahn R, Fersht AR. A structural model for GroEL-polypeptide recognition. of special interest Proc Natl Acad Sci USA. 94:1997;3571-3575 This paper presents the high resolution structure of an N-terminal-tagged polypeptide corresponding to the isolated apical domain of GroEL. In the structure, the N-terminal tag of one molecule is bound to the active region of a neighbouring molecule. The data presented here are used to reconstruct how a peptide can bind to the GroEL complex.
34. Roseman AM, Chen S, White H, Braig K, Saibil HR. The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell. 87:1996;241-251.
35. 14 complex. The structure shows that there is a massive upward movement of the GroEL apical domains, which is accompanied by a twisting rigid-body movement around a hinge at the junction of the intermediate and apical domains. It further reveals that as a result of these movements, the surface properties of the central cavity in the cis cavity dramatically change from hydrophobic to polar. If one assumes that protein binding is due to hydrophobic interactions. GroEL would lose its binding properties once the cavity becomes polar.
36. Yifrach O, Horovitz A. Two lines af allosteric communication in the oligomeric chaperonin GroEL are revealed by the single mutation Arg196/Ala. J Mol Biol. 234:1994;397-401.
37. White HE, Chen S, Roseman AM, Yifrach O, Horovitz A, Saibil HR. Structural basis of the allosteric changes in the GroEL mutant Arg 197 → Ala. of outstanding interest Nat Struct Biol. 4:1997;690-694 Cryo-electron microscopy has been used to generate three-dimensional reconstructions of a GroEL mutant with weaker intersubunit contacts, in different nucleotide-bound states. In this mutant, the domains are more free to move about the intermediate domain at all ATP concentrations. The study provides new insights into the nucleotide-dependent allosteric switching of GroEL.
38. Aharoni A, Horovitz A. Detection of changes in pairwise interactions during allosteric transitions: Coupling between local and global conformational changes in GroEL. Proc Natl Acad Sci USA. 94:1997;1698-1702.
39. Fenton WA, Kashi Y, Furtak K, Horwich AL. Residues in chapronin GroEL required for polypeptide binding and release. Nature. 371:1994;614-619.
40. Hunt JF, Weaver AJ, Landry SJ, Gierasch L, Deisenhofer J. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature. 379:1996;37-45.
41. Manda SC, Mehra V, Bloom BR, Hol WGJ. Structure of the heat shock protein chaperonin-10 of Mycobacterium leprae. Science. 271:1996;203-207.
42. Rye HS, Burston SG, Fenton WA, Beechem JM, Xu Z, Sigler P, Horwich AL. Distinct action of cis and trans ATP within the double ring of the chaperonin GroEL. Nature. 388:1997;792-798.
43. Ellis RJ. Opening and closing the Anfinsen cage. Curr Biol. 4:1994;633-635.
44. Jackson GS, Staniforth RA, Halsall DJ, Atkinson T, Holbrook JJ, Clarke AR, Burston SG. Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle: Implications for the mechanism of assisted protein folding. Biochemistry. 32:1993;2554-2563.
45. Weissman JS, Kashi Y, Fenton WA, Horwich AL. GroEL mediated protein folding proceeds by multiple rounds of binding and release of non-native forms. Cell. 78:1994;693-702.
46. Ranson NA, Dunster NJ, Burston SG, Clarke AR. Chaperonins can catalyse the reversal of early aggregation steps when a protein misfolds. J Mol Biol. 250:1995;581-586.
47. Burston SG, Weissman JS, Farr GW, Fenton WA, Horwich AL. Release of both native and non-native proteins from cis-only GroEL ternary complex. Nature. 383:1996;96-99.
48. Martin J, Hartl FU. The effect of macromolecular crowding in chaperonin-mediated protein folding. of outstanding interest Proc Natl Acad Sci USA. 94:1997;1107-1112 The point of this study was to investigate the fate of newly synthesized proteins in a dense cytosolic solution or in the presence of macromolecular crowding agents. Under these conditions, the transfer to a chaperonin trap, which is able to bind but not to release substrate protein, is prevented. At a twofold dilution, a significant increase in the rate of transfer is observed. The authors come to the conclusion that the release of non-native polypeptide is not an essential feature of the productive chaperonin mechanism. See annotation [7].
49. Nelson RJ, Ziegelhoffer T, Nicolet C, Werner-Washburne M, Craig EA. The translation machinery and 70 kDa heat shock protein cooperate in protein synthesis. Cell. 71:1992;97-105.
50. Reid BG, Flynn GC. GroEL binds to and unfolds rhodanase posttranslationally. J Biol Chem. 271:1996;7212-7217.
51. Hesterkamp T, Hauser S, Lutcke H, Bukau B. Escherichia coli trigger factor is a propyl isomerase that associates with nascent polypeptide chains. Proc Natl Acad Sci USA. 93:1996;4437-4441.
52. Valent QA, Kendall DA, High S, Kusters R, Oudega B, Luirink J. Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 14:1995;5494-5505.
53. Langer T, Lu C, Echols H, Flanagan J, Hayer MK, Hartl FU. Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature. 356:1992;683-689.
54. Gragerov A, Nudler E, Komissarova N, Gaitanaris GA, Gottesman ME, Nikiforov V. Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc Natl Acad Sci USA. 89:1992;10341-10344.
55. Bukau B, Walker GC. Cellular defects caused by deletion of the Escherichia coli DnaK gene indicate roles for heat shock protein in normal metabolism. J Bacteriol. 171:1989;2337-2346.
56. Sparrer H, Buchner J. How GroES regulates binding of nonnative protein to GroEL. of special interest J Biol Chem. 272:1997;14080-14086 This kinetic study suggests that the slow release of substrate protein from the unproductive trans position in the asymmetric GroEL - GroES complex favours the binding of a second GroES. The formation of a symmetric complex ensures that the substrate protein is sequestered in a position underneath GroES. According to this model, the intrinsic binding characteristics of the asymmetric trans complex determine the sequence of events during the reaction cycle.