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The Hsp60 chaperonins from prokaryotes and eukaryotes

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Chaperones

Part of the book series: Topics in Current Genetics ((TCG,volume 16))

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Abstract

The Hsp60 molecular chaperones (the chaperonins) are essential proteins throughout biology. They can be separated into two evolutionary classes: the Group I chaperonins from eubacteria and their endosymbiotic counterparts in eukaryotic cells, and the Group II chaperonins from archaea and the eukaryotic cytosol. While the two classes have some similarity to each other in structural and functional characteristics, they also have a number of important distinctions implying that they may have some significant differences in their modes of action. In this review we first examine our current understanding of the Group I class, typified by GroE from Escherichia coli, before looking at the recent developments in the much less well-studied Group II chaperonins, including the archeal thermosome and eukaryotic CCT.

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References

  • 1. Ahmad S, Gupta RS (1990) Cloning of a Chinese hamster protein homologous to the mouse t-complex protein TCP-1: structural similarity to the ubiquitous 'chaperonin' family of heat-shock proteins. Biochim Biophys Acta 1087:253-255

    PubMed  CAS  Google Scholar 

  • 2. Amir A, Horovitz A (2004) Kinetic analysis of ATP-dependent inter-ring communication in GroEL. J Mol Biol 338:979-988

    PubMed  CAS  Google Scholar 

  • 3. Andra S, Frey G, Nitsch M, Baumeister W, Stetter KO (1996) Purification and structural characterization of the thermosome from the hyperthermophilic archaeon Methanopyrus kandleri. FEBS Lett 379:127-131

    PubMed  CAS  Google Scholar 

  • 4. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223-230

    PubMed  CAS  Google Scholar 

  • 5. Archibald JM, Roger AJ (2002) Gene duplication and gene conversion shape the evolution of archaeal chaperonins. J Mol Biol 316:1042-1050

    Google Scholar 

  • 6. Archibald JM, Blouin C, Doolittle WF (2001) Gene duplication and the evolution of Group II chaperonins: implications for structure and function. J Struct Biol 135:157-169

    PubMed  CAS  Google Scholar 

  • 7. Azem A, Diamant S, Kessel M, Weiss C, Goloubinoff P (1995) The protein-folding activity of chaperonins correlates with the symmetrical GroEL14(GroES7)2 heterooligomer. Proc Natl Acad Sci USA 92:12021-12025

    PubMed  CAS  Google Scholar 

  • 8. Badcoe IG, 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

    PubMed  CAS  Google Scholar 

  • 9. Bakkes PJ, Faber BW, van Heerikhuizen H, van der Vies SM (2005) The T4-encoded cochaperonin, gp31, has unique properties that explain its requirement for the folding of the T4 major capsid protein. Proc Natl Acad Sci USA 102:8144-8149

    PubMed  CAS  Google Scholar 

  • 10. Barraclough R, Ellis RJ (1980) Protein synthesis in chloroplasts IX Assembly of newly-synthesized large subunits into ribulose bisphosphate carboxylase in isolated pea chloroplasts. Biochim Biophys Acta 607:19-31

    Google Scholar 

  • 11. Bigotti MG, Clarke AR (2005) Cooperativity in the thermosome. J Mol Biol 348:13-26

    PubMed  CAS  Google Scholar 

  • 12. Boisvert DC, Wang J, Otwinowski Z, Horwich AL, Sigler PB (1996) The 2.4Ã… crystal structure of the bacterial chaperonin GroEL complexed with ATPgS. Nat Struct Biol 3:170-177

    PubMed  CAS  Google Scholar 

  • 13. Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8Ã…. Nature 371:578-586

    PubMed  CAS  Google Scholar 

  • 14. Brinker A, Pfeifer G, Kerner MJ, Naylor DJ, Hartl FU, Hayer-Hartl MK (2001) Dual function of protein confinement in chaperonin-assisted protein folding. Cell 107:223-233

    PubMed  CAS  Google Scholar 

  • 15. Buchner J, Schmidt, M, Fuchs M, Jaenicke R, Rudolph R, Schmid FX, Kiefhaber T (1991) GroE facilitates refolding of citrate synthase by suppressing aggregation. Biochemistry 30:1586-1591

    PubMed  CAS  Google Scholar 

  • 16. Burston SG, Ranson NA, Clarke AR (1995) The origins and consequences of asymmetry in the chaperonin reaction cycle. J Mol Biol 249:138-152

    PubMed  CAS  Google Scholar 

  • 17. 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

    PubMed  CAS  Google Scholar 

  • 18. Carrascosa JL, Lorca O, Valpuesta JM (2001) Structural comparison of prokaryotic and eukaryotic chaperonins. Micron 32:43-50

    PubMed  CAS  Google Scholar 

  • 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 261:12414-419

    PubMed  CAS  Google Scholar 

  • 20. Chaudhry C, Farr GW, Todd MJ, Rye HS, Brunger AT, Adams PD, Horwich AL, Sigler PB (2003) Role of the g-phosphate of ATP in triggering protein folding by GroEL-GroES: function, structure and energetics. EMBO J 22:4877-4887

    PubMed  CAS  Google Scholar 

  • 21. Chaudhuri TK, Farr GW, Fenton WA, Rospert S, Horwich AL (2001) GroEL/GroES-mediated folding of a protein too large to be encapsulated. Cell 107:235-246

    PubMed  CAS  Google Scholar 

  • 22. Chen L, Sigler PB (1999) The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell 99:757-768

    PubMed  CAS  Google Scholar 

  • 23. Chen J, Walter S, Horwich AL, Smith D (2001) Folding of malate dehydrogenase inside the GroEL-GroES cavity. Nat Struct Biol 8:721-728

    PubMed  CAS  Google Scholar 

  • 24. Cheng MY, Hartl FU, Martin J, Pollock RA, Kalousek F, Neupert W, Hallberg RL, Horwich AL (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337:620-625

    PubMed  CAS  Google Scholar 

  • 25. Cliff MJ, Kad NM, Hay N, Lund PA, Webb MR, Burston SG, Clarke AR (1999) A kinetic analysis of the nucleotide-induced allosteric transitions of GroEL. J Mol Biol 293:667-684

    PubMed  CAS  Google Scholar 

  • 26. Ditzel L, Lowe J, Stock D, Stetter KO, Huber H, Huber R, Steinbacher S (1998) Crystal structure of the thermosome, the archaeal chaperonin and homolog if CCT. Cell 93:125-138

    PubMed  CAS  Google Scholar 

  • 27. Dobrzynski JK, Sternlicht ML, Farr GW, Sternlicht H (1996) Newly synthesized b-tubulin demonstrates domain-specific interactions with the cytosolic chaperonin. Biochemistry 35:15870-15882

    PubMed  CAS  Google Scholar 

  • 28. Dunn AY, Melville MW, Frydman J (2001) Review: cellular substrates of the eukaryotic chaperonin TriC/CCT. J Struct Biol 135:176-184

    PubMed  CAS  Google Scholar 

  • 29. Ellis RJ (1990) The molecular chaperone concept. Semin Cell Biol 1:1-9

    PubMed  CAS  Google Scholar 

  • 30. Falke S, Fisher MT, Gogol EP (2001) Structural changes in GroEL effected by binding of a denatured protein substrate. J Mol Biol 308:569-577

    PubMed  CAS  Google Scholar 

  • 31. Falke S, Tama F, Brooks III CL, Gogol EP, Fisher MT (2005) The 13Ã… structure of a chaperonin GroEL-protein substrate complex by cryo-electron microscopy. J Mol Biol 348:219-230

    PubMed  CAS  Google Scholar 

  • 32. Farr GW, Scharl EC, Schumacher RJ, Sondek S, Horwich AL (1997) Chaperonin-mediated folding in the eukaryotic cytosol proceeds through rounds of release of native and nonnative forms. Cell 89:927-937

    PubMed  CAS  Google Scholar 

  • 33. Farr GW, Furtak K, Rowland MB, Ranson NA, Saibil HR, Kirchausen T, Horwich AL (2000) Multivalent binding of nonnative substrate proteins by the chaperonin GroEL. Cell 100:561-573

    PubMed  CAS  Google Scholar 

  • 34. Farr GW, Fenton WA, Chaudhuri TK, Clare DK, Saibil HR, Horwich AL (2003) Folding with and without encapsulation by cis- and trans-only GroEL-GroES complexes. EMBO J 22:3220-3230

    PubMed  CAS  Google Scholar 

  • 35. Feldman DE, Thulasiraman V, Ferreyra RG, Frydman J (1999) Formation of the VHL-elongin BC tumor soppressor complex is mediated by the chaperonin TriC. Mol Cell 4:1051-1061

    PubMed  CAS  Google Scholar 

  • 36. Feldman DE, Spiess C, Howard DE, Frydman J (2003) Tumorigenic mutations in VHL disrupt folding in vivo by interfering with chaperonin binding. Mol Cell 12:1213-1224

    PubMed  CAS  Google Scholar 

  • 37. Fenton WA, Kashi Y, Furtak K, Horwich AL (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371:614-619

    PubMed  CAS  Google Scholar 

  • 38. Figuereido L, Klunker D, Ang D, Naylor DJ, Kerner MJ, Georgopulos C, Hartl FU, Hayer-Hartl M (2004) Functional characterization of an archaeal GroEL/GroES chaperonin system. J Biol Chem 279:1090-1099

    Google Scholar 

  • 39. Fisher MT (1992) Promotion of the in vitro renaturation of dodecameric glutamine synthetase from Escherichia coli in the presence of GroEL (chaperonin-60) and ATP. Biochemistry 31:3955-3963

    PubMed  CAS  Google Scholar 

  • 40. Franzetti B, Schoehn G, Ebel C, Gagnon J, Ruigrok RW, Zaccai G (2001) Characterization of a novel complex from halophilic archaeabacteria, which displays chaperone-like activities in vitro. J Biol Chem 276:29906-29914

    PubMed  CAS  Google Scholar 

  • 41. Frydman J, Nimmesgern E, Erdjument-Bromage H, Wall JS, Tempst P, Hartl FU (1992) Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. EMBO J 11:4767-4778

    PubMed  CAS  Google Scholar 

  • 42. 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

    PubMed  CAS  Google Scholar 

  • 43. Gao Y, Thomas JO, Chow RL, Lee GH, Cowan NJ (1992) A cytoplasmic chaperonin that catalyzes b-actin folding. Cell 69:1043-1050

    PubMed  CAS  Google Scholar 

  • 44. Georgopoulos C, Hendrix RW, Casjens SR, Kaiser AD (1973) Host participation in bacteriophage lambda head assembly. J Mol Biol 76:45-60

    PubMed  CAS  Google Scholar 

  • 45. Georgopoulos CP, Hohn B (1978) Identification of a host protein necessary for bacteriophage morphogenesis (the GroE gene product). Proc Natl Acad Sci USA 75:131-135

    PubMed  CAS  Google Scholar 

  • 46. Georgopoulos C, Tilly K (1981) Bacteriophage-host interactions in assembly. Prog Clin Biol Res 64:21-34

    PubMed  CAS  Google Scholar 

  • 47. 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 Mg-ATP. Nature 342:884-889

    PubMed  CAS  Google Scholar 

  • 48. Gray TE, Fersht AR (1991) Cooperativity in ATP hydrolysis by GroEL is increased by GroES. FEBS Lett 292:254-258

    PubMed  CAS  Google Scholar 

  • 49. Guagliardi A, Cerchia L, Bartolucci S, Rossi M (1994) The chaperonin from the archaeon Sulfolobus solfataricus promotes correct refolding and promotes thermal denaturation in vitro. Protein Sci 3:1436-1443

    PubMed  CAS  Google Scholar 

  • 50. Gupta RS (1990) Sequence and structural homology between a mouse t-complex proteinTCP-1 and the 'chaperonin' family of bacterial (GroEL, 60-65 kDa heat shock antigen) and eukaryotic proteins. Biochem Int 20:833-841

    PubMed  CAS  Google Scholar 

  • 51. Gupta RS (1995) Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of the eukaryotic cells. Mol Microbiol 15 1-11

    Google Scholar 

  • 52. Gutsche I, Essen L-O, Baumeister W (1999) Group II chaperonins: new TriC(k)s and turns of a protein folding machine. J Mol Biol 293:295-312

    PubMed  CAS  Google Scholar 

  • 53. Gutsche I, Mihalache O, Hegerl R, Typke D, Baumeister W (2000a) ATPase cycle controls the conformation of an archaeal chaperonin as visualized by cryo-electron microscopy. FEBS Lett 477:278-282

    PubMed  CAS  Google Scholar 

  • 54. Gutsche I, Holzinger J, Rossle M, Heumann H, Baumeister W, May RP (2000b) Conformational rearrangements of an archaeal chaperonin upon ATPase cycling. Curr Biol 10:405-408

    PubMed  CAS  Google Scholar 

  • 55. Gutsche I, Mihalache O, Baumeister W (2000c) ATPase cycle of an archaeal chaperonin. J Mol Biol 300:187-196

    PubMed  CAS  Google Scholar 

  • 56. Gutsche I, Holzinger J, Rauh N, Baumeister W, May RP (2001) ATP-induced structural change of the thermosome is temperature-dependent. J Struct Biol 135:139-146

    PubMed  CAS  Google Scholar 

  • 57. Hansen WJ, Cowan NJ, Welch WJ (1999) Prefoldin nascent chain complexes in the folding of cytoskeletal proteins. J Cell Biol 145:265-277

    PubMed  CAS  Google Scholar 

  • 58. Hill JE, Penny SL, Crowell KG, Goh SH, Hemmingsen SM (2004) cpnDB: a chaperonin sequence database. Genome Res 14:1669-1675

    PubMed  CAS  Google Scholar 

  • 59. Horovitz A, Amir A, Danziger O, Kafri G (2002) Phi-value analysis of heterogeneity in pathways of allosteric transitions: Evidence for parallel pathways of ATP-induced conformational changes in a GroEL ring. Proc Natl Acad Sci USA 99:14095-14097

    PubMed  CAS  Google Scholar 

  • 60. Horwich AL, Willison KR (1993) Protein folding in the cell: functions of two families of molecular chaperone, hsp 60 and TF55-TCP-1. Philos Trans Roy Soc Lond B Biol Sci 339:313-326

    CAS  Google Scholar 

  • 61. Horwich AL, Low KB, Fenton WA, Hirshfield IN (1993) Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell 74:909-917

    PubMed  CAS  Google Scholar 

  • 62. Houry WA, Frishman D, Eckerskorn C, Lottspeich F, Hartl FU (1999) Identification of in vivo substrates of the chaperonin GroEL. Nature 402:147-154

    PubMed  CAS  Google Scholar 

  • 63. Hunt JF, Weaver AJ, Landry SJ, Gierasch L, Deisenhofer J (1996) The crystal structure of the GroES co-chaperonin at 2.8Ã…. Nature 379:37-45

    PubMed  CAS  Google Scholar 

  • 64. Hunt JF, van der Vies SM, Henry L, Deisenhofer J (1997) Structural adaptations in the specialized bacteriophage T4 co-chaperonin Gp31 expand the size of the Anfinsen cage. Cell 90:361-371

    PubMed  CAS  Google Scholar 

  • 65. Hynes G, Kubota H, Willison KR (1995) Antibody characterisation of two distinct conformations of the chaperonin-containing TCP-1 from mouse testis. FEBS Lett 358:129-132

    PubMed  CAS  Google Scholar 

  • 66. Iizuka R, So S, Inobe T, Yoshida T, Zako T, Kuwajima K, Yohda M (2004) Role of the helical protrusion in the conformational change and molecular chaperone activity of the archaeal Group II chaperonin. J Biol Chem 279:18834-18839

    PubMed  CAS  Google Scholar 

  • 67. Inobe T, Makio T, Takasu-Ishikawa E, Terada TP, Kuwajima K (2001) Nucleotide binding to the chaperonin GroEL: non-cooperative binding of ATP analogs and ADP, and cooperative effect of ATP. Biochim Biophys Acta 1545:160-173

    PubMed  CAS  Google Scholar 

  • 68. Ionobe 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. J Mol Biol 327:183-191

    Google Scholar 

  • 69. 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

    PubMed  CAS  Google Scholar 

  • 70. Kafri G, Willison KR, Horovitz A (2001) Nested allosteric interactions in the cytoplasmic chaperonin containing TCP-1. Protein Sci 10:445-449

    PubMed  CAS  Google Scholar 

  • 71. Kafri G, Horovitz A (2003) Transient kinetic analysis of ATP-induced allosteric transitions in the eukaryotic chaperonin containing TCP-1. J Mol Biol 326:981-987

    PubMed  CAS  Google Scholar 

  • 72. Kim S, Willison KR, Horwich AL (1994) Cytosolic chaperonin subunits have a conserved ATPase domain but diverged polypeptide-binding domains. Trends Biochem Sci 19:543-548

    PubMed  CAS  Google Scholar 

  • 73. Klumpp M, Baumeister W, Essen LO (1997) Structure of the substrate binding domain of the thermosome, an archaeal Group II chaperonin. Cell 91:263-270

    PubMed  CAS  Google Scholar 

  • 74. Klunker D, Haas B, Hirtreiter A, Figueiredo L, Naylor DJ, Pfeifer G, Muller V, Deppenmeier U, Gottschalk G, Hartl FU, Hayer-Hartl M (2003) Coexistence of Group I and Group II chaperonins in the archaeon Methanosarcina mazei. J Biol Chem 278:33256-33267

    PubMed  CAS  Google Scholar 

  • 75. Koshland DE, Nemethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5:365-385

    PubMed  CAS  Google Scholar 

  • 76. Kubota H, Hynes G, Willison K (1995) The chaperonin containing t-complex polypeptide 1 (TCP-1): Multisubunit machinery assisting in protein folding and assembly in the eukaryotic cytosol. Eur J Biochem 230:3-16

    PubMed  CAS  Google Scholar 

  • 77. Kubota H, Hynes G, Carne A, Ashworth A, Willison K (1994) Identification of six Tcp-1-related genes encoding divergent subunits of the TCP-1-containing chaperonin. Curr Biol 4:89-99

    PubMed  CAS  Google Scholar 

  • 78. Kubota H, Hynes GM, Kerr SM, Willison KR (1997) Tissue-specific subunit of the mouse cytosolic chaperonin-containing TCP-1. FEBS Lett 402:53-56

    PubMed  CAS  Google Scholar 

  • 79. Kuo YP, Thompson DK, St Jean A, Charlebois RL, Daniels CJ (1997) Characterization of two heat shock genes from Haloferax volcanii: a model system for transcription regulation in the Archaea. J Bacteriol 179:6318-6324

    PubMed  CAS  Google Scholar 

  • 80. Landry SJ, Gierasch L (1991) The chaperonin GroEL binds a polypeptide in an a-helical conformation. Biochemistry 30:7359-7362

    PubMed  CAS  Google Scholar 

  • 81. Landry SJ, Zeilstra-Ryalls J, Fayet O, Georgopoulos C, Gierasch L (1993) Characterization of a functionally important mobile domain of GroES. Nature 364:255-258

    PubMed  CAS  Google Scholar 

  • 82. Leroux MR, Fandrich M, Klunker D, Siegers K, Lupas AN, Brown JR, Schiebel E, Dobson CM, Hartl FU (1999) MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. EMBO J 18:6730-6743

    PubMed  CAS  Google Scholar 

  • 83. Lewis VA, Hynes GM, Zheng D, Saibil H, Willison K (1992) T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukaryotic cytosol. Nature 358:249-252

    PubMed  CAS  Google Scholar 

  • 84. Lin Z, Schwarz FP, Eisenstein E (1995) The hydrophobic nature of GroEL-substrate binding. J Biol Chem 270:1011-1014

    PubMed  CAS  Google Scholar 

  • 85. Lin P, Sherman F (1997) The unique hetero-oligomeric nature of the subunits in the catalytic cooperativity of the yeast CCT chaperonin complex. Proc Natl Acad Sci USA 94:10780-10785

    PubMed  CAS  Google Scholar 

  • 86. Lin Z, Rye HS (2004) Expansion and compression of a folding intermediate by GroEL. Mol Cell 16:23-34

    PubMed  CAS  Google Scholar 

  • 87. Liou AK, Willison KR (1997) Elucidation of the subunit orientation in CCT (chaperonin containing TCP1) from the subunit composition of CCT micro-complexes. EMBO J 16:4311-4316

    PubMed  CAS  Google Scholar 

  • 88. Llorca O, Smyth MG, Marco S, Carrascosa JL, Willison KR, Valpuesta JM (1998) ATP binding induces large conformational changes in the apical and equatorial domains of the eukaryotic chaperonin containing TCP-1 complex. J Biol Chem 273:10091-10094

    PubMed  CAS  Google Scholar 

  • 89. Llorca O, McCormack EA, Hynes G, Grantham J, Cordell J, Carrascosa JL, Willison KR, Fernandez JJ, Valpuesta JM (1999a) Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature 402:693-696

    PubMed  CAS  Google Scholar 

  • 90. Llorca O, Smyth MG, Carrascosa JL, Willison KR, Radermacher M, Steinbacher S, Valpuesta JM (1999b) 3D reconstruction of the ATP-bound form of CCT reveals the asymmetric folding conformation of a type II chaperonin. Nat Struct Biol 6:639-642

    PubMed  CAS  Google Scholar 

  • 91. Llorca O, Martin-Benito J, Ritco-Vonsovici M, Grantham J, Hynes GM, Willison KR, Carrascosa JL, Valpuesta JM (2000) Eukaryotic chaperonin CCT stabilizes actin and tubulin folding intermediates in open quasi-native conformations. EMBO J 19:5971-5979

    PubMed  CAS  Google Scholar 

  • 92. Llorca O, Martin-Benito J, Grantham J, Ritco-Vonsovici M, Willison KR, Carrascosa JL, Valpuesta JM (2001) The 'sequential allosteric ring' mechanism in the eukaryotic chaperonin-assisted folding of actin and tubulin. EMBO J 20:4065-4075

    PubMed  CAS  Google Scholar 

  • 93. Lopez-Garcia P, Moreira D (1999) Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci 24:88-93

    PubMed  CAS  Google Scholar 

  • 94. Lorimer GH (2001) A personal account of chaperonin history. Plant Physiol 125:38-41

    PubMed  CAS  Google Scholar 

  • 95. Maeder DL, Macario AJL, Conway de Macario E (2005) Novel chaperonins in a Prokaryote. J Mol Evol 60:409-416

    PubMed  CAS  Google Scholar 

  • 96. Margulis L (1971) Symbiosis and evolution. Sci Am 225:48-57

    Article  PubMed  CAS  Google Scholar 

  • 97. 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

    PubMed  CAS  Google Scholar 

  • 98. Martin-Benito J, Boskovic J, Gomez-Puertas P, Carrascosa JL, Simons CT, Lewis SA, Bartolini F, Cowan NJ, Valpuesta JM (2002) Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT. EMBO J 21:6377-6386

    PubMed  CAS  Google Scholar 

  • 99. Mayhew M, da Silva AC, 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

    PubMed  CAS  Google Scholar 

  • 100. McCallum CD, Do H, Johnson AE, Frydman J (2000) The interaction of the chaperonin tailless complex polypeptide 1 (TCP1) ring complex (TRiC) with ribosome-bound nascent chains examined using photo-cross-linking. J Cell Biol 149:591-601

    PubMed  CAS  Google Scholar 

  • 101. Meyer AS, Gillespie JR, Walther D, Millet IS, Doniach S, Frydman J (2003) Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis. Cell 113:369-381

    PubMed  CAS  Google Scholar 

  • 102. Minuth T, Henn M, Rutkat K, Andra S, Frey G, Rachel R, Stetter KO, Jaenicke R (1999) The recombinant thermosome from the hyperthermophilic archaeon Methanopyrus kandleri: in vitro analysis of its chaperone activity. Biol Chem 380:55-62

    PubMed  CAS  Google Scholar 

  • 103. Monod J, Wyman J, Changeux J-P (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12:88-118

    Article  PubMed  CAS  Google Scholar 

  • 104. Motojima F, Chaudhry C, Fenton WA, Farr GW, Howich AL (2004) Substrate polypeptide presents a load on the apical domains of the chaperonin GroEL. Proc Natl Acad Sci USA 101:15005-15012

    PubMed  CAS  Google Scholar 

  • 105. Netzer WJ, Hartl FU (1997) Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature 388:343-349

    PubMed  CAS  Google Scholar 

  • 106. Nitsch M, Klumpp M, Lupas A, Baumeister W (1997) The thermosome: alternating a and b-subunits within the chaperonin of the archaeon Thermoplasma acidophilum. J Mol Biol 267:142-149

    PubMed  CAS  Google Scholar 

  • 107. Nitsch M, Walz J, Typke D, Klumpp M, Essen LO, Baumeister W (1998) Group II chaperonin in an open conformation examined by electron tomography. Nat Struct Biol 5:855-857

    PubMed  CAS  Google Scholar 

  • 108. Ostermann J, Horwich AL, Neupert W, Hartl FU (1989) Protein folding in the mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature 341:125-130

    PubMed  CAS  Google Scholar 

  • 109. Phipps BM, Hoffmann A, Stetter KO, Baumeister W (1991) A novel ATPase complex selectively accumulated upon heat-shock is a major cellular component of thermophilic archaeabacteria. EMBO J 10:1711-1722

    PubMed  CAS  Google Scholar 

  • 110. Poso D, Clarke AR, Burston SG (2004a) A kinetic analysis of the nucleotide-induced allosteric transitions in a single-ring mutant of GroEL. J Mol Biol 338:969-977

    PubMed  CAS  Google Scholar 

  • 111. Poso D, Clarke AR, Burston SG (2004b) Identification of a major inter-ring coupling step in the GroEL reaction cycle. J Biol Chem 279:38111-38117

    PubMed  CAS  Google Scholar 

  • 112. Ranson NA, Dunster NJ, Burston SG, Clarke AR (1995) Chaperonins can catalyse the reversal of early aggregation steps when a protein misfolds. J Mol Biol 250:581-586

    PubMed  CAS  Google Scholar 

  • 113. Ranson NA, Burston SG, Clarke AR (1997) Binding, encapsulation and ejection: substrate dynamics during a chaperonin-assisted folding reaction. J Mol Biol 266:656-664

    PubMed  CAS  Google Scholar 

  • 114. Ranson NA, Farr GW, Roseman AM, Gowen B, Fenton WA, Horwich AL, Saibil HR (2001) ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107:869-879

    PubMed  CAS  Google Scholar 

  • 115. Rivenzon-Segal N, Wolf SG, Shimon L, Willison KR, Horovitz A (2005) Sequential ATP-induced allosteric transitions of the cytoplasmic chaperonin containing TCP-1 revealed by EM analysis. Nat Struct Mol Biol 12:233-237

    PubMed  CAS  Google Scholar 

  • 116. Rommelaere H, De Neve M, Melki R, Vandekerckhove J, Ampe C (1999) The cytosolic class II chaperonin CCT recognizes delineated hydrophobic sequences in its target proteins. Biochemistry 38:3246-3257

    PubMed  CAS  Google Scholar 

  • 117. Roseman AM, Chen S, White HE, Braig K, Saibil HR (1996) The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87:241-251

    PubMed  CAS  Google Scholar 

  • 118. Rye HS, Burston SG, Fenton WA, Beechem JM, Xu Z, Sigler PB, Horwich AL (1997) Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388:792-797

    PubMed  CAS  Google Scholar 

  • 119. Rye HS, Roseman AM, Chen S, Furtak K, Fenton WA, Saibil HR, Horwich AL (1999) GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell 97:325-338

    PubMed  CAS  Google Scholar 

  • 120. Saibil H, Dong Z, Wood S, auf der Mauer A (1991) Binding of chaperonins. Nature 353:25-26

    PubMed  CAS  Google Scholar 

  • 121. Saibil, HR, Zheng D, Roseman AM, Hunter AS, Watson GM, Chen S, auf der Mauer A, O'Hara BP, Wood SP, Mann NH, Barnett LK, Ellis RJ (1993) ATP induces large quaternary rearrangements in a cage-like chaperonin structure. Curr Biol 3:265-273

    PubMed  CAS  Google Scholar 

  • 122. Schmidt M, Buchner J (1992) Interaction of GroE with an all b-protein. J Biol Chem 267:16829-16833

    PubMed  CAS  Google Scholar 

  • 123. Schoehn G, Quaite-Randall E, Jimenez JL, Joachimiak A, Saibil HR (2000a) Three conformations of an archaeal chaperonin, TF55 from Sulfolobus shibatae. J Mol Biol 296:813-819

    PubMed  CAS  Google Scholar 

  • 124. Schoehn G, Hayes M, Cliff M, Clarke AR, Saibil HR (2000b) Domain rotations between open, closed and bullet-shaped forms of the thermosome, an archaeal chaperonin. J Mol Biol 301:323-332

    PubMed  CAS  Google Scholar 

  • 125. Shtilerman M, Lorimer GH, Englander SW (1999) Chaperonin function: folding by forced unfolding. Science 284:822-825

    PubMed  CAS  Google Scholar 

  • 126. Siegers K, Bolter B, Schwarz JP, Bottcher UM, Guha S, Hartl FU (2003) TRiC/CCT cooperates with different upstream chaperones in the folding of distinct protein classes. EMBO J 22:5230-5240

    PubMed  CAS  Google Scholar 

  • 127. Siegert R, Leroux MR, Scheufler C, Hartl FU, Moarefi I (2000) Structure of the molecular chaperone prefoldin: unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell 103:621-632

    PubMed  CAS  Google Scholar 

  • 128. Silver LM, Artzt K, Bennet D (1979) A major testicular cell protein specified by a mouse T/t complex gene. Cell 17:275-284

    PubMed  CAS  Google Scholar 

  • 129. Silver LM, Kleene KC, Distel RJ, Hecht NB (1987) Synthesis of mouse t complex proteins during haploid stages of spermatogenesis. Dev Biol 119:605-608

    PubMed  CAS  Google Scholar 

  • 130. Staniforth RA, Burston SG, Atkinson T, Clarke AR (1994) Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. Biochem J 300:651-658

    PubMed  CAS  Google Scholar 

  • 131. Szpikowska BK, Swiderek KM, Sherman MA, Mas MT (1998) MgATP binding to the nucleotide-binding domains of the eukaryotic cytoplasmic chaperonin induces conformational changes in the putative substrate-binding domains. Protein Sci 7:1524-1530

    Article  PubMed  CAS  Google Scholar 

  • 132. Thulasiraman V, Yang CF, Frydman J (1999) In vivo newly translated polypeptides are sequestered in a protective folding environment. EMBO J 18:85-95

    PubMed  CAS  Google Scholar 

  • 133. Tilly K, McKittrick N, Georgopoulos C, Murialdo H (1981) Studies on Escherichia coli mutants which block bacteriophage morphogenesis. Prog Clin Biol Res 64:35-45

    PubMed  CAS  Google Scholar 

  • 134. Todd MJ, Viitanen PV, Lorimer GH (1993) Hydrolysis of adenosine 5'-triphosphate by Escherichia coli GroEL: effects of GroES and potassium ion. Biochemistry 32:8560-8567

    PubMed  CAS  Google Scholar 

  • 135. Todd MJ, Viitanen PV, Lorimer GH (1994) Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265:659-666

    PubMed  CAS  Google Scholar 

  • 136. Trent JD, Nimmesgern E, Wall JS, Hartl FU, Horwich AL (1991) A molecular chaperone from a thermophilic archaeabacterium is related to the eukaryotic protein t-complex polypeptide-1. Nature 354:490-493

    PubMed  CAS  Google Scholar 

  • 137. Ursic D, Culbertson MR (1992) Is yeast TCP1 a chaperonin? Nature 356:392

    PubMed  CAS  Google Scholar 

  • 138. Ursic D, Culbertson MR (1991) The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol Cell Biol 11:2629-2640

    PubMed  CAS  Google Scholar 

  • 139. Ursic D, Ganetzky B (1988) A Drosophila melanogaster gene encodes a protein homologous to the mouse t-complex polypeptide 1. Gene 68:267-274

    PubMed  CAS  Google Scholar 

  • 140. Waldmann T, Nimmesgern E, Nitsch M, Peters J, Pfeifer G, Muller S, Kellermann J, Engel A, Hartl FU, Baumeister W (1995a) The thermosome of Thermoplasma acidophilum and its relationship to the eukaryotic chaperonin TRiC. Eur J Biochem 227:848-856

    PubMed  CAS  Google Scholar 

  • 141. Waldmann T, Lupas A, Kellermann J, Peters J, Baumeister W (1995b) Primary structure of the thermosome from Thermoplasma acidophilum. Biol Chem Hoppe-Seyler 376:119-126

    Google Scholar 

  • 142. Wang J, Boisvert DC (2003) Structural basis for GroEL-assisted protein folding from the crystal structure of (GroEL-KMgATP)14 at 2.0Ã… resolution. J Mol Biol 327:843-855

    PubMed  CAS  Google Scholar 

  • 143. Wang J, Chen L (2003) Domain motions in GroEL upon binding of an oligopeptide. J Mol Biol 334:489-499

    PubMed  CAS  Google Scholar 

  • 144. Wang JD, Herman C, Tipton KA, Gross CA, Weissman JS (2002) Directed evolution of substrate-optimized GroEL/S chaperonins. Cell 111:1027-1039

    PubMed  CAS  Google Scholar 

  • 145. 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

    PubMed  CAS  Google Scholar 

  • 146. 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 83:577-587

    PubMed  CAS  Google Scholar 

  • 147. 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

    PubMed  CAS  Google Scholar 

  • 148. Willison K, Kelly A, Dudley K, Goodfellow P, Spurr N, Groves V, Gorman P, Sheer D, Trowsdale J (1987) The human homologue of the mouse t-complex gene, TCP1, is located on chromosome 6 but is not near the HLA region. EMBO J 6:1967-1974

    PubMed  CAS  Google Scholar 

  • 149. Willison KR, Grantham J (2001) In: Lund P (Ed), Molecular Chaperones: Frontiers in Molecular Biology. Oxford University Press, Oxford, pp 90-118

    Google Scholar 

  • 150. Won KA, Schumacher RJ, Farr GW, Horwich AL, Reed SI (1998) Maturation of human cyclin E requires the function of eukaryotic chaperonin CCT. Mol Cell Biol 18:7584-7589

    PubMed  CAS  Google Scholar 

  • 151. Yaffe MB, Farr GW, Miklos D, Horwich AL, Sternlicht ML, Sternlicht H (1992) TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature 358:245-248

    PubMed  CAS  Google Scholar 

  • 152. Zako T, Iizuka R, Okochi M, Nomura T, Ueno T, Tadakuma H, Yohda M, Funatsu T (2005) Facilitated release of substrate protein from prefoldin by chaperonin. FEBS Lett 579:3718-3724

    PubMed  CAS  Google Scholar 

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Bigotti, M.G., Clarke, A.R., Burston, S.G. The Hsp60 chaperonins from prokaryotes and eukaryotes. In: Braakman, I. (eds) Chaperones. Topics in Current Genetics, vol 16. Springer, Berlin, Heidelberg. https://doi.org/10.1007/4735_116

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