GroEL-mediated protein folding

Protein Science

Volumn 6, Issue 4, 1997, Pages 743-760

  Fenton, Wayne A ^a   Horwich, Arthur L ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

chaperonin; GroES; Hsp60; kinetic partitioning; mechanism of action; X ray structure

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN; HEAT SHOCK PROTEIN 60; POLYPEPTIDE;

AMINO ACID SEQUENCE; BINDING AFFINITY; CIS TRANS ISOMERISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; HYDROLYSIS; HYDROPHOBICITY; KINETICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; THERMODYNAMICS; X RAY ANALYSIS;

EID: 0030910349     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560060401     Document Type: Review

References (122)

1. Anfinsen CB. 1973. Principles that govern the folding of protein chains. Science 181:222-230.
2. 2 heterooligomer. Proc Natl Acad Sci USA 92:12021-12025.
3. 2 chaperonin hetero-oligomer. Science 265:653-656.
4. Badcoe AG, Smith CJ, Wood S, Halsall DJ, Holbrook JJ, Lund P, Clarke AR. 1991. Binding of a chaperonin to the folding intermediates of lactate dehydrogenase. Biochemistry 30:9195-9200.
5. Beckmann RP, Mizzen LA, Welch WJ. 1990. Interaction of Hsp70 with newly synthesized proteins: Implications for protein folding and assembly. Science 248:850-854.
6. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang SR, Sambrook JF, Gething MJ. 1993. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75:717-728.
7. Bochkareva ES, Girshovich AS. 1992. A newly synthesized protein interacts with GroES on the surface of chaperonin GroEL. J Biol Chem 267:25672-25675.
8. Bochkareva ES, Lissin NM, Flynn GC, Rothman JE, Girshovich AS. 1992. Positive cooperativity in the functioning of molecular chaperone GroEL. J Biol Chem 267:6796-6800.
9. Boisvert DC, Wang J, Otwinowski Z, Horwich AL, Sigler PB. 1996. The 2.4 Å crystal structure of the bacterial chaperonin GroEL complexed with ATPγS. Nature Struct Biol 3:170-177.
10. Braig K, Adams PD, Brünger AT. 1995. Conformational variability in the refined structure of the chaperonin GroEL at 2.8 Å resolution. Nature Struct Biol 2:1083-1094.
11. Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB. 1994. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371:578-586.
12. Braig K, Simon M, Furaya F, Hainfeld JF, Horwich AL. 1993. A polypeptide bound by the chaperonin groEL is localized within a central cavity. Proc Natl Acad Sci USA 90:3978-3982.
13. Brunschier R, Danner M, Seckler R. 1993. Interactions of phage P22 tailspike protein with GroE molecular chaperones during refolding in vitro. J Biol Chem 268:2167-2772.
14. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG. 1995. Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins Struct Fund Genet 21:167-195.
15. Buchberger A, Schröder H, Hesterkamp T, Schönfeld HJ, Bukau B. 1996. Substrate shuttling between the DnaK and GroEL systems indicates a chaperone network promoting protein folding. J Mol Biol 261:328-333.
16. Bukau B, Walker GC. 1989. Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J Bacteriol 171:2337-2346.
17. Burston SG, Ranson NA, Clarke AR. 1995. The origins and consequences of asymmetry in the chaperonin reaction cycle. J Mol Biol 249:138-152.
18. Burston SG, Weissman JS, Farr GW, Fenton WA, Horwich AL. 1996. Release of both native and non-native proteins from a cis-only GroEL ternary complex. Nature 383:96-99.
19. Chandrasekhar GN, Tilly K, Woolford C, Hendrix R, Georgopoulos C. 1986. Purification and properties of the GroES morphogenetic protein of Escherichia coli. J Biol Chem 261:12414-12419.
20. Chen S, Roseman AM, Hunter AS, Wood SP, Burston SG, Ranson NA, Clarke AR, Saibil HR. 1994. Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature 371:261-264.
21. Clark AC, Hugo E, Frieden C. 1996. Determination of regions in the dihydrofolate reductase structure that interact with the molecular chaperonin GroEL. Biochemistry 35:5893-5901.
22. Corrales FJ, Fersht AR. 1995. The folding of GroEL-bound barnase as a model for chaperonin-mediated protein folding. Proc Natl Acad Sci USA 92:5326-5330.
23. Corrales FJ, Fersht AR. 1996. Toward a mechanism for GroEL·GroES chaperone activity: An ATPase-gated and -pulsed folding and annealing cage. Proc Natl Acad Sci USA 93:4509-4512.
24. de Crouy-Chanel A, El Yaagoubi A, Kohiyama M, Richarme G. 1995. Reversal by GroES of the GroEL preference from hydrophobic amino acids toward hydrophilic amino acids. J Biol Chem 270:10571-10575.
25. Diamant S, Azem A, Weiss C, Goloubinoff P. 1995. Increased efficiency of GroE-assisted protein folding by manganese ions. J Biol Chem 270:28387-28391.
26. Ellis RJ, Hartl FU. 1996. Protein folding in the cell: Competing models of chaperonin function. FASEB J 10:20-26.
27. Engel A, Hayer-Hartl MK, Goldie KN, Pfeifer G, Hegerl R, Müller S, da Silva ACR, Baumeister W, Hartl FU. 1995. Functional significance of symmetrical versus asymmetrical GroEL-GroES chaperonin complexes. Science 269:832-836.
28. Fayet O, Ziegelhoffer T, 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.
29. Fenton WA, Kashi Y, Furtak K, Horwich AL. 1994. Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371:614-619.
30. Fenton WA, Weissman JS, Horwich AL. 1996. Putting a lid on protein folding: Structure and function of the co-chaperonin, GroES. Chem Biol 3:157-161.
31. Flynn GC, Chappell TG, Rothman JE. 1989. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245:385-390.
32. Flynn GC, Pohl J, Flocco MT, Rothman JE. 1991. Peptide-binding specificity of the molecular chaperone BiP. Nature 353:726-730.
33. Frydman J, Nimmesgern E, Ohtsuka K, Hartl FU. 1994. Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370:111-117.
34. Galisteo ML, Gordon CL, King J. 1995. Stability of wild-type and temperature-sensitive protein subunits of the phage P22 capsid. J Biol Chem 270:16595-16601.
35. 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. Proc Natl Acad Sci USA 93:12189-12194.
36. Goldberg MS, Zhang J, Sondek S, Matthews CR, Fox RO, Horwich AL. 1997. Native-like structure of a protein-folding intermediate bound to the chaperonin GroEL. Proc Natl Acad Sci USA 94:1080-1085.
37. Goloubinoff P, Christeller JT, Gatenby AA, Lorimer GH. 1989. Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and MgATP. Nature 342:884-889.
38. Gordon CL, Sather SK, Casjens S, King J. 1994. Selective in vivo rescue by GroEL/ES of thermolabile folding intermediates to phage P22 structural proteins. J Biol Chem 269:27941-27951.
39. Gragerov A, Gottesman ME. 1994. Different peptide binding specificities of hsp70 family members. J Mol Biol 241:133-135.
40. Gragerov A, Nudler E, Komissarova N, Gaitanaris GA, Gottesman ME, Nikiforov V. 1992. Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc Natl Acad Sci USA 89:10341-10344.
41. Gragerov A, Zeng L, Zhao X, Burkholder W, Gottesman ME. 1994. Specificity of DnaK-peptide binding. J Mol Biol 235:848-854.
42. Gray TE, Fersht AR. 1991. Co-operativity in ATP hydrolysis by GroEL is increased by GroES. FEBS Lett 292:254-258.
43. Gray TE, Fersht AR. 1993. Refolding of barnase in the presence of GroE. J Mol Biol 232:1197-1207.
44. Gulukota K, Wolynes PG. 1994. Statistical mechanics of kinetic proofreading in protein folding in vivo. Proc Natl Acad Sci USA 91:9292-9296.
45. Hartl FU. 1996. Molecular chaperones in cellular protein folding. Nature 381:571-580.
46. Hayer-Hartl MK, Ewbank JJ, Creighton TE, Hartl FU. 1994. Conformational specificity of the chaperonin GroEL for the compact folding intermediates of α-lactalbumin. EMBO J 13:3192-3202.
47. Hayer-Hartl M, Martin J, Hartl FU. 1995. Asymmetrical interaction of GroEL and GroES in the ATPase cycle of assisted protein folding. Science 269:836-841.
48. Hesterkamp T, Hauser S, Lutcke H, Bukau B. 1996. Escherichia coli trigger factor is a prolyl isomerase that associates with nascent polypeptide chains. Proc Natl Acad Sci USA 93:4437-4441.
49. Hlodan R, Tempst P, Hartl FU. 1995. Binding of defined regions of a polypeptide to GroEL and its implications for chaperonin-mediated protein folding. Nature Struct Biol 2:587-595.
50. Höll-Neugebauer B, Rudolph R. 1991. Reconstitution of a heat shock effect in vitro: Influence of GroE on the thermal aggregation of α-glucosidase from yeast. Biochemistry 30:11609-11614.
51. Horwich AL, Low KB, Fenton WA, Hirshfield IN, Furtak K. 1993. Folding in vivo of bacterial cytoplasmic proteins: Role of GroEL. Cell 74:909-917.
52. Hunt JF, Weaver AJ, Landry SJ, Gierasch L, Deisenhofer J. 1996. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature 379:37-45.
53. Ishii N, Taguchi H, Sasabe H, Yoshida M. 1994. Folding intermediate binds to the bottom of bullet-shaped holo-chaperonin and is readily accessible to antibody. J Mol Biol 236:691-696.
54. Itzhaki LS, Otzen DE, Fersht AR. 1995. Nature and consequences of GroEL-protein interactions. Biochemistry 34:14581-14587.
55. Jackson GS, Staniforth RA, Halsall DJ, Atkinson T, Holbrook JJ, Clarke AR, Burston SG. 1993. Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle: Implications for the mechanism of assisted protein folding. Biochemistry 32:2554-2563.
56. Kandror O, Busconi L, Sherman M, Goldberg AL. 1994. Rapid degradation of an abnormal protein in Escherichia coli involves the chaperones GroEL and GroES. J Biol Chem 269:23575-23582.
57. Katsumata K, Okazaki A, Kuwajima K. 1996. Effect of GroEL on the re-folding kinetics of α-lactalbumin. J Mol Biol 258:827-838.
58. Knarr G, Gething MJ, Modrow S, Buchner J. 1995. BiP binding sequences in antibodies. J Biol Chem 270:27589-27594.
59. Laminet AA, Ziegelhoffer T, Georgopoulos C, Pluckthun A. 1990. The Escherichia coli heat shock proteins GroEL and GroES modulate the folding of the β-lactamase precursor. EMBO J 9:2315-2319.
60. Landry SJ, Gierasch LM. 1991. The chaperonin GroEL binds a polypeptide in an α-helical conformation. Biochemistry 30:7359-7362.
61. Landry S, Jordan R, McMacken R, Gierasch L. 1992. Different conformations for the same polypeptide bound to chaperones DnaK and GroEL. Nature 355:455-457.
62. Landry SJ, Zeilstra-Ryalls J, Fayet O, Georgopoulos C, Gierasch LM. 1993. Characterization of a functionally important mobile domain of GroES. Nature 364:255-258.
63. Langer T, Pfeifer G, Martin J, Baumeister W, Hartl FU. 1992. Chaperonin-mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. EMBO J 11:4757-4765.
64. Lilie H, Buchner J. 1995. Interaction of GroEL with a highly structured folding intermediate: Iterative binding cycles do not involve unfolding. Proc Natl Acad Sci USA 92:8100-8104.
65. Lin S, Schwarz FP, Eisenstein E. 1995. The hydrophobic nature of GroEL-substrate binding. J Biol Chem 270:1011-1014.
66. Llorca O, Carrascosa JL, Valpuesta JM. 1996. Biochemical characterization of symmetric GroEL-GroES complexes: Evidence for a role in protein folding. J Biol Chem 271:68-76.
67. Lorimer GH. 1996. A quantitative assessment of the role of the chaperonin proteins in protein folding in vivo. FASEB J 10:5-9.
68. Mande SC, Mehra V, Bloom BR, Hol WGJ. 1996. Structure of the heat shock protein chaperonin-10 of Mycobacterium leprae. Science 271:203-207.
69. Martin J, Horwich AL, Hartl FU. 1992. Role of hsp60 in preventing denaturation under heat stress. Science 258:995-998.
70. Martin J, Langer T, Boteva R, Schramel A, Horwich AL, Hartl FU. 1991. Chaperonin-mediated protein folding at the surface of groEL through a "molten globule"-like intermediate. Nature 352:36-42.
71. Martin J, Mayhew M, Langer T, Hartl FU. 1993. The reaction cycle of GroEL and GroES in chaperonin-assisted protein folding. Nature 366:228-233.
72. Mattingly JR Jr, Iriarte A, Martinez-Carrion M. 1995. Homologous proteins with different affinities for groEL. The refolding of the aspartate amino-transferase isozymes at varying temperatures. J Biol Chem 270:1138-1148.
73. Mayhew M, da Silva ACR, Martin J, Erdjument-Bromage H, Tempst P, Hartl FU. 1996. Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 379:420-426.
74. McCarty JS, Rudiger S, Schonfeld HJ, Schneidermergener J, Nakahigashi K, Yura T, Bukau B. 1996. Regulatory region C of the E. coli heat shock transcription factor, σ(32), constitutes a DnaK binding site and is conserved among eubacteria. J Mol Biol 256:829-837.
75. Mendoza JA, Butler MC, Horowitz PM. 1992a. Characterization of a stable, reactivatable complex between chaperonin 60 and mitochondrial rhodanese. J Biol Chem 267:24648-24654.
76. Mendoza JA, Lorimer GH, Horowitz PM. 1992b. Chaperonin cpn60 from Escherichia coli protects the mitochondrial enzyme rhodanese against heat inactivation and supports folding at elevated temperatures. J Biol Chem 267:17631-17634.
77. Mendoza JA, Rogers E, Lorimer GH, Horowitz PM. 1991. Chaperonins facilitate the in vitro folding of monomeric mitochondrial rhodanese. J Biol Chem 266:13044-13049.
78. Murai N, Taguchi H, Yoshida M. 1995. Kinetic analysis of interactions between GroEL and reduced α-lactalbumin. Effect of GroES and nucleotides. J Biol Chem 270:19957-19963.
79. Nelson RJ, Ziegelhoffer T, Nicolet C, Werner-Washburne M, Craig EA. 1992. The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71:97-105.
80. Okazaki A, Ikura T, Nikaido K, Kuwajima K. 1994. The chaperonin GroEL does not recognize apo-α-lactalbumin in the molten globule state. Nature Struct Biol 1:439-446.
81. Paek KH, Walker GC. 1987. Escherichia coli dnaK null mutants are inviable at high temperature. J Bacteriol 169:283-290.
82. Peralta F, Hartman DJ, Hoogenraad NJ, Høj PB. 1994. Generation of a stable folding intermediate which can be rescued by the chaperonins GroEL and GroES. FEBS Lett 339:45-49.
83. Ranson NA, Dunster NJ, Burston SG, Clarke AR. 1995. Chaperonins can catalyze the reversal of early aggregation steps when a protein misfolds. J Mol Biol 250:581-586.
84. Reid BG, Flynn GC. 1996. GroEL binds to and unfolds rhodanese posttranslationally. J Biol Chem 271:7212-7217.
85. Richarme G, Kohiyama M. 1994. Amino acid specificity of the Escherichia coli chaperone GroEL (heat shock protein 60). J Biol Chem 269:7095-7098.
86. Robinson CV, Gross N, Eyles SJ, Ewbank JJ, Mayhew M, Hartl FU, Dobson CM, Radford SE. 1994. Conformation of GroEL-bound α-lactalbumin probed by mass spectrometry. Nature 372:646-651.
87. 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.
88. Roy H, Kupferschmid M, Bell AJ. 1992. Theory of chaperonin action: Inertial model for enhancement of prokariotic Rubisco assembly. Protein Sci 1:925-934.
89. Saibil H, Dong Z, Wood S, auf der Mauer A. 1991. Binding of chaperonins. Nature 353:25-26.
90. Schmidt M, Buchner J. 1992. Interaction of GroE with an all-β-protein. J Biol Chem 267:16829-16833.
91. Schmidt M, Buchner J, Todd MJ, Lorimer GH, Viitanen PV. 1994a. On the role of GroES in the chaperonin-assisted folding reaction. Three case studies. J Biol Chem 269:10304-10311.
92. Schmidt M, Rutkat K, Rachel R, Pfeifer G, Jaenicke R, Viitanen P, Lorimer G, Buchner J. 1994b. Symmetric complexes of GroE chaperonins as part of the functional cycle. Science 265:656-659.
93. Schroder J, Langer T, Hartl FU, Bukau B. 1993. DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J 12:4137-4144.
94. Smith KE, Fisher MT. 1995. Interactions between the GroE chaperonins and rhodanese. Multiple intermediates and release and rebinding. J Biol Chem 270:21517-21523.
95. Sparrer H, Lilie H, Buchner J. 1996. Dynamics of the GroEL-protein complex: Effects of nucleotides and folding mutants. J Mol Biol 258:74-87.
96. Staniforth RA, Burston SG, Atkinson T, Clarke AR. 1994a. Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. Biochem J 300:651-658.
97. Staniforth RA, Cortés A, Burston SG, Atkinson T, Holbrook JJ, Clarke AR. 1994b. The stability and hydrophobicity of cytosolic and mitochondrial malate dehydrogenases and their relation to chaperonin-assisted folding. FEBS Lett 344:129-135.
98. Stoller G, Rucknagel KP, Nierhaus KH, Schmid FX, Fischer G, Rahfeld JU. 1995. A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J 14:4939-4948.
99. Taguchi H, Yoshida M. 1995. Chaperonin releases the substrate protein in a form with tendency to aggregate and ability to rebind to chaperonin. FEBS Lett 359:195-198.
100. Thiyagarajan P, Henderson SJ, Joachimiak A. 1996. Solution structures of GroEL and its complex with rhodanese from small-angle neutron scattering. Structure 4:79-88.
101. Tian G, Vainberg IE, Tap WD, Lewis SA, Cowan NJ. 1995. Specificity in chaperonin-mediated protein folding. Nature 375:250-253.
102. Todd MJ, Viitanen PV, Lorimer GH. 1994. Dynamics of the chaperonin ATPase cycle: Implications for facilitated protein folding. Science 265:659-666.
103. Todd MJ, Lorimer GH, 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.
104. Valent QA, Kendall DA, High S, Kusters R, Oudega B, Luirink J. 1995. Early events in preprotein recognition in E. coli: Interaction of SRP and trigger factor with nascent polypeptides. EMBO J 14:5494-5505.
105. Van Dyk TK, Gatenby AA, LaRossa RA. 1989. Demonstration by genetic suppression of interaction of GroE products with many proteins. Nature 342:451-453.
106. Viitanen PV, Donaldson GK, Lorimer GH, Lubben TH, Gatenby AA. 1991. Complex interactions between the chaperonin 60 molecular chaperone and dihydrofolate reductase. Biochemistry 30:9116-9723.
107. Viitanen PV, Gatenby AA, Lorimer GH. 1992. Purified chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins. Protein Sci 1:363-369.
108. Walter S, Lorimer GH, Schmid FX. 1996. A thermodynamic coupling mechanism for GroEL-mediated unfolding. Proc Natl Acad Sci USA 93:9425-9430.
109. Weissman JS, Hohl CM, Kovalenko O, Kashi Y, Chen S, Braig K, Saibil HR, Fenton WA, Horwich AL. 1995. Mechanism of GroEL action: Productive release of polypeptide from a sequestered position under GroES. Cell 83:577-588.
110. Weissman JS, Kashi Y, Fenton WA, Horwich AL. 1994. GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78:693-702.
111. Weissman JS, Rye HS, Fenton WA, Beechem JM, Horwich AL. 1996. Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 84:481-490.
112. Yee DP, Chan HS, Havel TF, Dill KA. 1994. Does compactness induce secondary structure in proteins? A study of poly-alanine chains computed by distance geometry. J Mol Biol 241:557-573.
113. Yifrach O, Horovitz A. 1994. Two lines of allosteric communication in the oligomeric chaperonin GroEL are revealed by the single mutation Arg 196 → Ala. J Mol Biol 243:397-401.
114. Yifrach O, Horovitz A. 1995. Nested cooperativity in the ATPase activity in the oligomeric chaperonin GroEL. Biochemistry 34:9716-9723.
115. Yifrach O, Horovitz A. 1996. Allosteric control by ATP of non-folded protein binding to GroEL. J Mol Biol 255:356-361.
116. Zahn R, Axmann SE, Rucknagel KP, Jaeger E, Laminet AA, Pluckthun A. 1994a. Thermodynamic partitioning model for hydrophobic binding of polypeptides by GroEL. I. GroEL recognizes the signal sequences of β-lactamase precursor. J Mol Biol 242:150-164.
117. Zahn R, Lindner P, Axmann SE, Pluckthun A. 1996a. Effect of single point mutations in citrate synthase on binding to GroEL. FEBS Lett 380:152-156.
118. Zahn R, Perrett S, Fersht AR. 1996b. Conformational states bound by the molecular chaperones GroEL and SecB - A hidden folding (annealing) activity. J Mol Biol 261:43-61.
119. Zahn R, Perrett S, Stenberg G, Fersht AT. 1996c. Catalysis of amide proton exchange by the molecular chaperones GroEL and SecB. Science 271:642-645.
120. Zahn R, Pluckthun A. 1992. GroE prevents the accumulation of early folding intermediates of pre-β-lactamase without changing the folding pathway. Biochemistry 31:3249-3255.
121. Zahn R, Pluckthun A. 1994. Thermodynamic partitioning model for hydrophobic binding of polypeptides by GroEL. II. GroEL recognizes thermally unfolded mature β-lactamase. J Mol Biol 242:165-174.
122. Zahn R, Spitzfaden C, Ottiger M, Wüthrich K, Plückthun A. 1994b. Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature 368:261-265.