The substrate recognition mechanisms in chaperonins

Journal of Molecular Recognition

Volumn 17, Issue 2, 2004, Pages 85-94

  Gómez Puertas, Paulino ^a   Martín Benito, Jaime ^b   Carrascosa, José L ^b   Willison, Keith R ^c   Valpuesta, José M ^b  

^a CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

^b CSIC   (Spain)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Actin; CCT; Chaperonins; GroEL; Molecular chaperones; Protein folding; Thermosome; Tubulin

Indexed keywords

ACTIN; ARCHAEAL PROTEIN; CHAPERONIN; T COMPLEX POLYPEPTIDE 1; T-COMPLEX POLYPEPTIDE-1; THERMOSOME PROTEIN, ARCHAEAL; TUBULIN;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; ENZYME SPECIFICITY; HUMAN; HYDROPHOBICITY; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN FOLDING; REVIEW;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; ARCHAEAL PROTEINS; CHAPERONINS; HUMANS; HYDROPHOBICITY; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; SUBSTRATE SPECIFICITY; TUBULIN;

EID: 1642320340     PISSN: 09523499     EISSN: None     Source Type: Journal    
DOI: 10.1002/jmr.654     Document Type: Review

References (98)

1. Andreu JM, Oliva MA, Monasterio O. 2002. Reversible unfolding of FtsZ cell division proteins from Archaea and Bacteria. J. Biol. Chem. 277: 43262-43270.
2. Aoki K, Taguchi H, Shindo Y, Yoshida M, Ogasahara K, Yutani K, Tanaka N. 1997. Calorimetric observation of a GroEL-protein binding reaction with little contribution of hydrophobic interaction. J. Biol. Chem. 272: 32158-32162.
3. Archibald JM, Logsdon JM Jr, Doolittle WF. 2000. Origin and evolution of eukaryotic chaperonins: phylogenetic evidence for ancient duplications in CCT genes. Mol. Biol. Evol. 17: 1456-1466.
4. Archibald JM, Blouin C, Doolittle WF. 2001. Gene duplications and the evolution of group II chaperonins: implications for structure and function. J. Struct. Biol. 135: 157-169.
5. Badcoe IG, Smith CJ, Wood S, Halsall DJ, Holbrook JJ, Lund PA, Clarke AR. 1991. Binding of a chaperonin to the folding intermediate of lactate dehydrogenase. Biochemistry 30: 9195-9200.
6. 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.
7. 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.
8. Buckle AM, Zahn R, Fersht AR. 1997. A structural model for GroEL-polypeptide recognition. Proc. Natl Acad. Sci. USA 94: 3571-3575.
9. Bukau B, Horwich AL. 1998. The hsp70, hsp60 chaperone machines. Cell 92: 351-366.
10. Carrascosa JL, Llorca O, Valpuesta JM. 2001. Structural comparison of prokaryotic, eukaryotic chaperonins. Micron 32: 43-50.
11. Chen L, Sigler PB. 1999. The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate recognition. Cell 99: 757-768.
12. 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.
13. Chen X, Sullivan DS, Huffaker TC. 1993. Two yeast genes with similarity to TCP-1 are required for microtubule and actin function in vivo. Proc. Natl Acad. Sci. USA 91: 9111-9115.
14. Cowan NJ, Lewis SA. 2002. Type II chaperonins, prefoldin and the tubulin-specific chaperones. Adv. Prot. Chem. 59: 73-104.
15. Coyle JE, Jaeger J, Gross M, Robinson CV, Radford SE. 1997. Structural and mechanistic consequences of polypeptide binding by GroEL. Fold. Des. 2: R93-R104.
16. 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.
17. Ditzel L, Löwe J, Stock D, Stetter KO, Huber H, Huber R, Steinbacher S. 1997. Crystal structure of the thermosome, the archaeal chaperonin and homologue of CCT. Cell 93: 125-138.
18. Dobrzynski JK, Sternlicht ML, Farr GW, Sternlicht H. 1996. Newly-synthesized β-tubulin demonstrates domain-specific interactions with the cytosolic chaperonin. Biochemistry 35: 15870-15882.
19. Dobrzynski JK, Sternlicht ML, Peng I, Farr GW, Sternlicht H. 2000. Evidence that β-tubulin induces a conformation change in the cytosolic chaperonin which stabilizes binding: implications for the mechanism of action. Biochemistry 39: 3988-4003.
20. Dunn AY, Melville MW, Frydman J. 2001. Cellular substrates of the eukaryotic chaperonin TriC/CCT. J. Struct. Biol. 135: 176-184.
21. Ellis RJ. 1994. Opening and closing the Anfinsen cage. Curr. Biol. 4: 633-635.
22. Ellis RJ. 1996. The Chaperonins. Academic Press: San Diego, CA.
23. Ellis RJ, Hartl FU. 1999. Principles of protein folding in the cellular environment. Curr. Opinin. Struct. Biol. 9: 102-110.
24. Farr GW, Furtak K, Rowland MB, Ranson NA, Saibil HR, Kirchhausen T, Horwich AL. 2000. Multivalent binding of nonnative substrate proteins by the chaperonin GroEL. Cell 100: 561-573.
25. Feldman DE, Thulasariman V, Ferreyra RG, Frydman J. 1999. Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TriC. Mol. Cell 4: 1051-1061.
26. Fenton WA, Kashi Y, Furtak K, Horwich AL. 1994. Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371: 614-619.
27. 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.
28. Gao Y, Thomas JO, Chow RL, Lee GH, Cowan NJ. 1992. A cytoplasmic chaperonin that catalyzes beta-actin folding. Cell 69: 1043-50.
29. Gebauer M, Melki R, Gehring U. 1998. The chaperone cofactor Hop/p60 interacts with the cytosolic chaperonin-containing TCP-1 and affects its nucleotide exchange and protein folding activities. J. Biol. Chem. 273: 29475-29480.
30. Geissler S, Siegers K, Schiebel E. 1998. A novel protein complex promoting formation of functional alpha- and gamma-tubulin. EMBO J. 17: 952-966.
31. Grantham J, Llorca O, Valpuesta JM, Willison KR. 2000. Partial occlusion of both cavities of CCT with antibody has no effect upon the rates of β-actin or α-tubulin folding. J. Biol. Chem. 275: 4587-4591.
32. Guagliardi A, Cerchia L, Rossi M. 1995. Prevention of in vitro protein thermal aggregation by the Sulfolobus solfataricus chaperonin. J. Biol. Chem. 270: 28126-28132.
33. Guenther MG, Yu J, Kao GD, Yeu TJ, Lazar MA. 2002. Assembly of the SMRT-histone deactylase 3 repression complex requires the TCP-1 ring complex. Gen. Dev. 16: 3130-3135.
34. Guex N, Peitsch MC. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling. Electrophoresis 18: 2714-2723.
35. Gutsche I, Essen LO, Baumeister W. 1999. Group II chaperonins: new TRIC(k)s and turns of a protein folding machine. J. Mol. Biol. 293: 295-312.
36. Gutsche I, Holzinger J, Röble M, Heumann H, Baumeister W, May RP. 2000. Conformational rearrangements of an archaeal chaperonin upon ATPase cycling. Curr. Biol. 10: 405-408.
37. 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.
38. Hayer-Hartl M, Ewbank JJ, Chreighton TE, Hartl FU. 1994. Conformational specificity of the chaperonin GroEL for the compact folding intermediates of α-lactalbumin. EMBO J. 13: 3192-3202.
39. Hlodan R, Tempst P, Hartl FU. 1995. Binding of defined regions of a polypeptide to GroEL and its implications for chaperonin-mediated protein folding. Nat. Struct. Biol. 2: 587-595.
40. Holm L, Sander C. 1993. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233: 123-138.
41. Horovitz A, Fridmann Y, Kafri G, Yifrach O. 2001. Allostery in chaperonins. J. Struct. Biol. 135: 104-114.
42. Houry WA, Frishman D, Eckerskorn F, Lottspeich F, Hartl FU. 1999. Identification of in vivo substrates of chaperonin GroEL. Nature 402: 147-154.
43. Hutchinson JP, Oldham TC, Elthaler TSH, Miller AD. 1997. Electrostatic as well as hydrophobic interactions are important for the association of cpn60 (GroEL) with peptides. J. Chem. Soc., Perkin Trans. 2: 279-288.
44. Hynes GM, Willison KR. 2000. Individual subunits of the chaperonin containing TCP-1 (CCT) mediate interactions with binding sites located on subdomains of β-actin. J. Biol. Chem. 275: 18985-18994.
45. Itzhaki LS, Otzen DE, Fersht AR. 1995. Nature and consequences of GroEL-protein interactions. Biochemistry 34: 14591-14587.
46. Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC. 1990. Atomic structure of the actin: DNase I complex. Nature 347: 37-44.
47. Katsumata K, Okazaki A, Tsurupa GP, Kwajima K. 1996. Dominant forces in the recognition of a transient folding intermediateof α-lactalbumin by GroEL. J. Mol. Biol. 264: 643-649.
48. 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.
49. Kubota H, Hynes G, Carne A, Asworth A, Willison KR. 1994. Identification of six TCP-1 related genes encoding divergent subunits of the TCP-1 containing chaperonin. Curr. Biol 4: 89-99.
50. Landry SJ, Gierash LM. 1991. The chaperonin GroEL binds a polypeptide in an α-helical conformation. Biochemistry 30: 7359-7362.
51. Landry SJ, Jordan R, McMacken R, Gieras LM. 1992. Different conformations for the same polyeptide bound to chaperones DnaK and GroEL. Nature 355: 455-457.
52. Landry SJ, Zeilstra-Ryalls J, Fayet O, Georgopoulos C, Gierash LM. 1993. Characterization of an im portant mobile domain of GroES. Nature 364: 255-258.
53. Lewis SA, Tian G, Vainberg IE, Cowan NJ. 1996. Chaperonin-mediated folding of actin and tubulin. J. Cell Biol. 132: 1-4.
54. 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. [See comments.] Nature 358: 249-252.
55. 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.
56. Lin S, Schwartz FP, Eisenstein E. 1995. The hydrophobic nature of GroEL-substrate binding. J. Biol. Chem. 270: 1011-1014.
57. 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.
58. 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 cytoplasmic chaperonin (CCT). J. Biol. Chem. 273: 10091-10094.
59. Llorca O, Smyth MG, Carrascosa JL, Willison KR, Radermacher M, Steinbacher S, Valpuesta JM. 1999a. 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.
60. Llorca O, McCormack E, Hynes G, Grantham J, Cordell J, Carrascosa JL, Willison KR, Fernȧndez JJ, Valpuesta JM. 1999b. Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature 402: 693-696.
61. Llorca O, Martin-Benito J, Ritco-Vonsovici M, Grantham J, Hynes G, 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.
62. Llorca O, Martín-Benito J, Gomez-Puertas P, Ritco-Vonsovici M, Willison KR, Carrascosa JL, Valpuesta JM. 2001a. Analysis of the interaction between the eukaryotic chaperonin CCT and its substrates actin and tubulin. J. Struct. Biol. 135: 205-218.
63. Llorca O, Martin-Benito J, Grantham J, Ritco-Vonsovici M, Willison KR, Carrascosa JL, Valpuesta JM. 2001b. The 'sequential allosteric ring' mechanism in the eukaryotic chaperonin-assisted folding of actin and tubulin. EMBO J. 20: 4065-4075.
64. 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.
65. Martin-Benito J, Boskovic J, Gómez-Puertas P, Carrascosa JL, Simons C, Lewis SA, Bartolini F, Cowan NC, Valpuesta JM. 2002. Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT. EMBO J. 21: 6377-6386.
66. McCormack E, Rohman M, Willison KR. 2001a. Mutational screen identifies critical amino acid residues of β-actin mediating interaction between folding intermediates and cytosolic chaperonin TCP-1. J. Struct. Biol. 135: 185-197.
67. McCormack E, Llorca O, Carrascosa JL, Valpuesta JM, Willison KR. 2001b. Point mutations in a hinge linking the small and large domains of β-actin result in trapped folding intermediates bound to cytosolic chaperonin containing TCP-1. J. Struct. Biol. 135: 198-204.
68. Melki R, Cowan NJ. 1994. Facilitated folding of actins and tubulins occurs via a nucleotide-dependent interaction between cytoplasmic chaperonin and distinctive folding intermediates. Mol. Cell. Biol. 14: 2895-2904.
69. Mogk A, Bukau B, Deuerling E. 2001. Cellular functions of cytosolic E. coli chaperones. In Molecular Chaperones in the Cell, Lund P (ed.). Oxford University Press: Oxford; 1-34.
70. Nicholls A, Sharp KA, Honig B. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296.
71. 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.
72. Nogales E, Wolf SG, Downing KH. 1998a. Structure of the αβtubulin dimer by electron crystallography. Nature 391: 199-203.
73. Nogales E, Downing KH, Amos LA, Löwe J. 1998b. Tubulin and FtsZ form a distinct family of GTPases. Nat. Struct. Biol. 5: 451-458.
74. Pappenberger G, Wilsher JA, Roe SM, Counsell DJ, Willison KR, Pearl LH. 2002. Crystal structure of the CCTγ apical domain: implications for substrate binding to the eukaryotic cytosolic chaperonin. J. Mol. Biol. 318: 1367-1379.
75. 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 archaebacteria. EMBO J. 10: 1711-1722.
76. Richarme G, Kohiyama M. 1994. Amino acid specificity of the Escherichia coli chaperone GroEL (heat shock protein 60). J. Biol. Chem. 269: 7095-7098.
77. Ritco-Vonsovici M, Willison KR. 2000. Defining the eukaryotic chaperonin-binding sites in human tubulins. J. Mol. Biol. 304: 81-98.
78. Robinson CV, Gross M, 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
79. Rommelaere H, van Troys M, Gao Y, Melki R, Cowan NJ, Vandekerckhove J, Ampe C. 1993. Eukaryotic cyrosolic chaperonin contains t-complex polypeptide 1 and seven related subunits. Proc. Natl Acad. Sci. USA 90: 11975-11979.
80. 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.
81. 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.
82. Schoehn G, Hayes M, Cliff M, Clarke AR, Saibil HR. 2000b. Domain rotations between open, closed and bullet-shaped forms of the thermosome, an archael chaperonin. J. Mol. Biol. 301: 323-332.
83. Schüler H, Lindberg U, Schutt CE, Karlsson R. 2000. Thermal unfolding of G-actin monitored with the Dnase I-inhibition assay. Eur. J. Biochem. 267: 476-486.
84. Shtilerman M, Lorimer GH, Englander SW. 1999. Chaperonin function: folding by forced unfolding. Science 284: 822-825.
85. Tian G, Vainberg IE, Tap WD, Lewis SA, Cowan NJ. 1995a. Specificity in chaperonin-mediated protein folding. Nature 375: 250-253.
86. Tian G, Vainberg IE, Tap WD, Lewis SA, Cowan NJ. 1995b. Quasi-native chaperonin-bound intermediates in facilitated protein folding. J. Biol. Chem. 270: 23910-23913.
87. Vainberg IE, Lewis SA, Rommelaere H, Ampe C, Vandekerckhove J, Klein HL, Cowan NJ. 1998. Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93: 863-873.
88. Valpuesta JM, Martín-Benito J, Gómez-Puertas P, Carrascosa JL, Willison KR. 2002. Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS lett. 529: 11-16.
89. van den Ent F, Amos LA, Löwe J. 2001. Prokaryotic origin of the actin cytoskeleton. Nature 413: 39-44.
90. 14 at 2.0 Å resolution. J. Mol. Biol. 327: 843-855.
91. Walther S, Lorimer GH, Schmid FX. 1996. A thermodynamic coupling mechanism for GroEL-mediating unfolding. Proc. Natl Acad. Sci. USA 93: 9425-9430.
92. Willison KR. 1999. Composition and function of the eukaryotic cytosolic chaperonin-containing TCP1. In Molecular Chaperones and Folding Catalysts, Bukau B (ed.). Harwood Academic: Amsterdam; 555-571.
93. Willison KR, Grantham J. 2001. Molecular Chaperones: Frontiers in Molecular Biology, Lund P (ed.). Oxford University Press: Oxford; 90-118.
94. Willison KR, Horwich AL. 1996. Structure and function of chaperonins. In The Chaperonins, Ellis RJ (ed.). Academic Press: San Diego, CA; 107-135.
95. 7 chaperonin complex. Nature 388: 741-750.
96. Yaffe MB, Farr GW, Miklos D, Norwich AL, Sternlicht ML, Sternlicht J. 1992. TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature 358: 245-248.
97. Zahn R, Spitzfaden C, Ottiger M, Wüthrich K, Plückthun A. 1994. Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature 368: 261-265.
98. Zahn R, Perrett S, Fersht AR. 1996. Conformational states bound by the molecular chaperones GroEL and SecB - a hidden unfolding (annealing) activity. J. Mol. Biol. 261: 43-61.