Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding.

The Escherichia coli chaperonins GroEL and GroES facilitate protein folding in an adenosine triphosphate (ATP)-dependent manner. After a single cycle of ATP hydrolysis by the adenosine triphosphatase (ATPase) activity of GroEL, the bi-toroidal GroEL formed a stable asymmetric ternary complex with GroES and nucleotide (bulletlike structures). With each subsequent turnover, ATP was hydrolyzed by one ring of GroEL in a quantized manner, completely releasing the adenosine diphosphate and GroES that were tightly bound to the other ring as a result of the previous turnover. The catalytic cycle involved formation of a symmetric complex (football-like structures) as an intermediate that accumulated before the rate-determining hydrolytic step. After one to two cycles, most of the substrate protein dissociated still in a nonnative state, which is consistent with intermolecular transfer of the substrate protein between toroids of high and low affinity. A unifying model for chaperonin-facilitated protein folding based on successive rounds of binding and release, and partitioning between committed and kinetically trapped intermediates, is proposed.

[1]  M. Kessel,et al.  Characterization of a functional GroEL14(GroES7)2 chaperonin hetero-oligomer. , 1994, Science.

[2]  R. Jaenicke,et al.  Symmetric complexes of GroE chaperonins as part of the functional cycle. , 1994, Science.

[3]  D A Agard,et al.  Kinetics versus thermodynamics in protein folding. , 1994, Biochemistry.

[4]  T. Atkinson,et al.  Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. , 1994, The Biochemical journal.

[5]  K. Truscott,et al.  Purification and characterization of chaperonin 60 and chaperonin 10 from the anaerobic thermophile Thermoanaerobacter brockii. , 1994, European journal of biochemistry.

[6]  A. Azem,et al.  Effect of divalent cations on the molecular structure of the GroEL oligomer. , 1994, Biochemistry.

[7]  J. Carrascosa,et al.  The formation of symmetrical GroEL‐GroES complexes in the presence of ATP , 1994, FEBS letters.

[8]  D. Eisenberg,et al.  Domain swapping: entangling alliances between proteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Buchner,et al.  On the role of groES in the chaperonin-assisted folding reaction. Three case studies. , 1994, The Journal of biological chemistry.

[10]  K. Wüthrich,et al.  Destabilization of the complete protein secondary structure on binding to the chaperone GroEL , 1994, Nature.

[11]  T. Creighton.  The energetic ups and downs of protein folding , 1994, Nature Structural Biology.

[12]  T. Sosnick,et al.  The barriers in protein folding , 1994, Nature Structural Biology.

[13]  H. Taguchi,et al.  Folding intermediate binds to the bottom of bullet-shaped holo-chaperonin and is readily accessible to antibody. , 1994, Journal of molecular biology.

[14]  Ellis Rj.  Protein folding. Chaperonin duet. , 1993 .

[15]  T. Langer,et al.  The reaction cycle of GroEL and GroES in chaperonin-assisted protein folding , 1993, Nature.

[16]  K. Furtak,et al.  Folding in vivo of bacterial cytoplasmic proteins: Role of GroEL , 1993, Cell.

[17]  G. Lorimer,et al.  Hydrolysis of adenosine 5'-triphosphate by Escherichia coli GroEL: effects of GroES and potassium ion. , 1993, Biochemistry.

[18]  A. Fersht,et al.  Refolding of barnase in the presence of GroE. , 1993, Journal of molecular biology.

[19]  D A Agard,et al.  To fold or not to fold.... , 1993, Science.

[20]  A. Horovitz,et al.  Mutation Ala2-->Ser destabilizes intersubunit interactions in the molecular chaperone GroEL. , 1993, Journal of molecular biology.

[21]  S. Chen,et al.  ATP induces large quaternary rearrangements in a cage-like chaperonin structure , 1993, Current Biology.

[22]  K. Braig,et al.  A polypeptide bound by the chaperonin groEL is localized within a central cavity. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[23]  T. Atkinson,et al.  Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle: implications for the mechanism of assisted protein folding. , 1993, Biochemistry.

[24]  E. Bochkareva,et al.  A newly synthesized protein interacts with GroES on the surface of chaperonin GroEL. , 1992, The Journal of biological chemistry.

[25]  W. Baumeister,et al.  Chaperonin‐mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity. , 1992, The EMBO journal.

[26]  K. Ito,et al.  Effects of the chaperonin GroE on the refolding of tryptophanase from Escherichia coli. Refolding is enhanced in the presence of ADP. , 1992, The Journal of biological chemistry.

[27]  C. Dobson,et al.  The folding of hen lysozyme involves partially structured intermediates and multiple pathways , 1992, Nature.

[28]  F. Baneyx,et al.  A mutation in GroEL interferes with protein folding by reducing the rate of discharge of sequestered polypeptides. , 1992, The Journal of biological chemistry.

[29]  R. Jaenicke,et al.  Conformational states of ribulosebisphosphate carboxylase and their interaction with chaperonin 60. , 1992, Biochemistry.

[30]  J. Rothman,et al.  Positive cooperativity in the functioning of molecular chaperone GroEL. , 1992, The Journal of biological chemistry.

[31]  G. Lorimer,et al.  Purified chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins , 1992, Protein science : a publication of the Protein Society.

[32]  E. Boekema,et al.  Electron microscopy and image analysis of the GroEL-like protein and its complexes with glutamine synthetase from pea leaves. , 1992, Biochimica et biophysica acta.

[33]  G. Lorimer,et al.  Mammalian mitochondrial chaperonin 60 functions as a single toroidal ring. , 1992, The Journal of biological chemistry.

[34]  A. Fersht,et al.  Cooperativity in ATP hydrolysis by GroEL is increased by GroES , 1991, FEBS letters.

[35]  C Sander,et al.  The role of heat-shock and chaperone proteins in protein folding: possible molecular mechanisms. , 1991, Protein engineering.

[36]  J. Holbrook,et al.  Binding of a chaperonin to the folding intermediates of lactate dehydrogenase. , 1991, Biochemistry.

[37]  R. Jaenicke,et al.  Folding intermediates of hyperthermophilic D‐glyceraldehyde‐3‐phosphate dehydrogenase from Thermotoga maritima are trapped at low temperature , 1991, FEBS letters.

[38]  A. Long,et al.  Sea-level curve , 1991, Nature.

[39]  T. Creighton.  Unfolding protein folding , 1991, Nature.

[40]  R. Jaenicke,et al.  GroE facilitates refolding of citrate synthase by suppressing aggregation. , 1991, Biochemistry.

[41]  C. Georgopoulos,et al.  The universally conserved GroE (Hsp60) chaperonins. , 1991, Annual review of microbiology.

[42]  G. Lorimer,et al.  Chaperonin-facilitated refolding of ribulosebisphosphate carboxylase and ATP hydrolysis by chaperonin 60 (groEL) are K+ dependent. , 1990, Biochemistry.

[43]  G. Lorimer,et al.  Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP , 1989, Nature.

[44]  G. Lorimer,et al.  GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli , 1989, Nature.

[45]  R. Rudolph,et al.  Intermediates on the folding pathway of octopine dehydrogenase from Pecten jacobaeus , 1987 .

[46]  F. C. Hartman,et al.  [83] Ribulosebisphosphate car☐ylase/oxygenase from Rhodospirillum rubrum , 1982 .

[47]  R. Hendrix.  Purification and properties of groE, a host protein involved in bacteriophage assembly. , 1979, Journal of molecular biology.

[48]  A. Engel,et al.  Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. , 1979, Journal of molecular biology.

[49]  C. Anfinsen.  Principles that govern the folding of protein chains. , 1973, Science.