Chaperonins: Two rings for folding

Trends in Biochemical Sciences

Volumn 36, Issue 8, 2011, Pages 424-432

  Yébenes, Hugo ^a   Mesa, Pablo ^b   Muñoz, Inés G ^b   Montoya, Guillermo ^b   Valpuesta, José M ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; CHAPERONIN; CHAPERONIN CONTAINING TCP1; MONOMER; THERMOSOME; TUBULIN;

ALLOSTERISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; EUKARYOTE; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

CHAPERONIN CONTAINING TCP-1; GROUP I CHAPERONINS; GROUP II CHAPERONINS; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 79961171567     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2011.05.003     Document Type: Review

References (75)

1. Horwich A.L., et al. Two families of chaperonin: physiology and mechanism. Annu. Rev. Cell Dev. Biol. 2007, 23:115-145.
2. Liou A.K., Willison K.R. Elucidation of the subunit orientation in CCT (chaperonin containing TCP1) from the subunit composition of CCT micro-complexes. EMBO J. 1997, 16:4311-4316.
3. Cong Y., et al. 4.0-Å resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4967-4972.
4. Martin-Benito J., et al. The inter-ring arrangement of the cytosolic chaperonin CCT. EMBO Rep. 2007, 8:252-257.
5. Kalisman N., Levitt M. Insights into the intra-ring subunit order of TRIC/CCT: a structural and evolutionary analysis. Proceedings of the Pacific Symposium on Biocomputing 2010 2010, 252-259. World Scientific. R.B. Altman (Ed.).
6. Braig K., et al. The crystal structure of the bacterial chaperonin GroEL at 2.8Å. Nature 1994, 371:578-586.
7. Ditzel L., et al. Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 1998, 93:125-138.
8. Horovitz A., Willison K.R. Allosteric regulation of chaperonins. Curr. Opin. Struct. Biol. 2005, 15:646-651.
9. 7 chaperonin complex. Nature 1997, 388:741-750.
10. Huo Y., et al. Crystal structure of group II chaperonin in the open state. Structure 2010, 18:1270-1279.
11. Pereira J.H., et al. Crystal structures of a group II chaperonin reveal the open and closed states associated with the protein folding cycle. J. Biol. Chem. 2010, 285:27958-27966.
12. Zhang J., et al. Mechanism of folding chamber closure in a group II chaperonin. Nature 2010, 463:379-383.
13. Munoz I.G., et al. Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin. Nat. Struct. Mol. Biol. 2011, 18:14-19.
14. Douglas N.R., et al. Dual action of ATP hydrolysis couples lid closure to substrate release into the group II chaperonin chamber. Cell 2011, 144:240-252.
15. Ranson N.A., et al. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 2001, 107:869-879.
16. Hunt J.F., et al. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature 1996, 379:37-45.
17. Ranson N.A., et al. Allosteric signaling of ATP hydrolysis in GroEL-GroES complexes. Nat. Struct. Mol. Biol. 2006, 13:147-152.
18. Shomura Y., et al. Crystal structures of the group II chaperonin from Thermococcus strain KS-1: steric hindrance by the substituted amino acid, and inter-subunit rearrangement between two crystal forms. J. Mol. Biol. 2004, 335:1265-1278.
19. Llorca O., et al. Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature 1999, 402:693-696.
20. Llorca O., et al. Eukaryotic chaperonin CCT stabilizes actin and tubulin folding intermediates in open quasi-native conformations. EMBO J. 2000, 19:5971-5979.
21. Schoehn G., et al. Domain rotations between open, closed and bullet-shaped forms of the thermosome, an archaeal chaperonin. J. Mol. Biol. 2000, 301:323-332.
22. Schoehn G., et al. Three conformations of an archaeal chaperonin, TF55 from Sulfolobus shibatae. J. Mol. Biol. 2000, 296:813-819.
23. Yifrach O., Horovitz A. Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 1995, 34:5303-5308.
24. Ma J., et al. A dynamic model for the allosteric mechanism of GroEL. J. Mol. Biol. 2000, 302:303-313.
25. Danziger O., et al. Conversion of the allosteric transition of GroEL from concerted to sequential by the single mutation Asp-155→Ala. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13797-13802.
26. Lin P., Sherman F. The unique hetero-oligomeric nature of the subunits in the catalytic cooperativity of the yeast Cct chaperonin complex. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:10780-10785.
27. Kafri G., Horovitz A. Transient kinetic analysis of ATP-induced allosteric transitions in the eukaryotic chaperonin containing TCP-1. J. Mol. Biol. 2003, 326:981-987.
28. Rivenzon-Segal D., et al. Sequential ATP-induced allosteric transitions of the cytoplasmic chaperonin containing TCP-1 revealed by EM analysis. Nat. Struct. Mol. Biol. 2005, 12:233-237.
29. Shimon L., et al. ATP-induced allostery in the eukaryotic chaperonin CCT is abolished by the mutation G345D in CCT4 that renders yeast temperature-sensitive for growth. J. Mol. Biol. 2008, 377:469-477.
30. Valpuesta, J.M. (2005) Structure and Function of the Cytosolic Chaperonin CCT. In Protein folding handbook (Buchner, J. and Kiefhaber, T., eds), Weinheim, Wiley-VCH, pp. 725-755.
31. Kafri G., et al. Nested allosteric interactions in the cytoplasmic chaperonin containing TCP-1. Protein Sci. 2001, 10:445-449.
32. Kusmierczyk A.R., Martin J. Nested cooperativity and salt dependence of the ATPase activity of the archaeal chaperonin Mm-cpn. FEBS Lett. 2003, 547:201-204.
33. Bigotti M.G., Clarke A.R. Cooperativity in the thermosome. J. Mol. Biol. 2005, 348:13-26.
34. Reissmann S., et al. Essential function of the built-in lid in the allosteric regulation of eukaryotic and archaeal chaperonins. Nat. Struct. Mol. Biol. 2007, 14:432-440.
35. Horovitz A., et al. Review: allostery in chaperonins. J. Struct. Biol. 2001, 135:104-114.
36. Kanzaki T., et al. Sequential action of ATP-dependent subunit conformational change and interaction between helical protrusions in the closure of the built-in lid of group II chaperonins. J. Biol. Chem. 2008, 283:34773-34784.
37. Amit M., et al. Equivalent mutations in the eight subunits of the chaperonin CCT produce dramatically different cellular and gene expression phenotypes. J. Mol. Biol. 2010, 401:532-543.
38. Jacob E., et al. Different mechanistic requirements for prokaryotic and eukaryotic chaperonins: a lattice study. Bioinformatics 2007, 23:i240-248.
39. Pappenberger G., et al. Crystal structure of the CCTgamma apical domain: implications for substrate binding to the eukaryotic cytosolic chaperonin. J. Mol. Biol. 2002, 318:1367-1379.
40. Gomez-Puertas P., et al. The substrate recognition mechanisms in chaperonins. J. Mol. Recognit. 2004, 17:85-94.
41. Horwich A.L., Fenton W.A. Chaperonin-mediated protein folding: using a central cavity to kinetically assist polypeptide chain folding. Q. Rev. Biophys. 2009, 42:83-116.
42. Farr G.W., et al. Multivalent binding of nonnative substrate proteins by the chaperonin GroEL. Cell 2000, 100:561-573.
43. Hirtreiter A.M., et al. Differential substrate specificity of group I and group II chaperonins in the archaeon Methanosarcina mazei. Mol. Microbiol. 2009, 74:1152-1168.
44. Iizuka R., et al. Role of the helical protrusion in the conformational change and molecular chaperone activity of the archaeal group II chaperonin. J. Biol. Chem. 2004, 279:18834-18839.
45. Spiess C., et al. Identification of the TRiC/CCT substrate binding sites uncovers the function of subunit diversity in eukaryotic chaperonins. Mol. Cell 2006, 24:25-37.
46. Tang Y.C., et al. Structural features of the GroEL-GroES nano-cage required for rapid folding of encapsulated protein. Cell 2006, 125:903-914.
47. Suzuki M., et al. Effect of the C-terminal truncation on the functional cycle of chaperonin GroEL: implication that the C-terminal region facilitates the transition from the folding-arrested to the folding-competent state. J. Biol. Chem. 2008, 283:23931-23939.
48. Bergeron L.M., et al. Small molecule inhibition of a group II chaperonin: pinpointing a loop region within the equatorial domain as necessary for protein refolding. Arch. Biochem. Biophys. 2009, 481:45-51.
49. Melki R., et al. Cytoplasmic chaperonin containing TCP-1: structural and functional characterization. Biochemistry 1997, 36:5817-5826.
50. Clare D.K., et al. Chaperonin complex with a newly folded protein encapsulated in the folding chamber. Nature 2009, 457:107-110.
51. Brinker A., et al. Dual function of protein confinement in chaperonin-assisted protein folding. Cell 2001, 107:223-233.
52. Chakraborty K., et al. Chaperonin-catalyzed rescue of kinetically trapped states in protein folding. Cell 2010, 142:112-122.
53. Ellis R.J. Molecular chaperones. Opening and closing the Anfinsen cage. Curr. Biol. 1994, 4:633-635.
54. Kanno R., et al. Cryo-EM structure of the native GroEL-GroES complex from Thermus thermophilus encapsulating substrate inside the cavity. Structure 2009, 17:287-293.
55. Llorca O., et al. Analysis of the interaction between the eukaryotic chaperonin CCT and its substrates actin and tubulin. J. Struct. Biol. 2001, 135:205-218.
56. Stuart S.F., et al. A two-step mechanism for the folding of actin by the yeast cytosolic chaperonin. J. Biol. Chem. 2011, 286:178-184.
57. Villebeck L., et al. Domain-specific chaperone-induced expansion is required for beta-actin folding: a comparison of beta-actin conformations upon interactions with GroEL and tail-less complex polypeptide 1 ring complex (TRiC). Biochemistry 2007, 46:12639-12647.
58. Villebeck L., et al. Conformational rearrangements of tail-less complex polypeptide 1 (TCP-1) ring complex (TRiC)-bound actin. Biochemistry 2007, 46:5083-5093.
59. Kiser P.D., et al. Use of thallium to identify monovalent cation binding sites in GroEL. Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 2009, 65:967-971.
60. Chaudhry C., et al. Role of the gamma-phosphate of ATP in triggering protein folding by GroEL-GroES: function, structure and energetics. EMBO J. 2003, 22:4877-4887.
61. Braig K., et al. Conformational variability in the refined structure of the chaperonin GroEL at 2.8 Å resolution. Nat. Struct. Biol. 1995, 2:1083-1094.
62. Cuellar J., et al. The structure of CCT-Hsc70 NBD suggests a mechanism for Hsp70 delivery of substrates to the chaperonin. Nat. Struct. Mol. Biol. 2008, 15:858-864.
63. Martin-Benito J., et al. Structure of the complex between the cytosolic chaperonin CCT and phosducin-like protein. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:17410-17415.
64. Stirling P.C., et al. PhLP3 modulates CCT-mediated actin and tubulin folding via ternary complexes with substrates. J. Biol. Chem. 2006, 281:7012-7021.
65. Gebauer M., et al. Interference between proteins Hap46 and Hop/p60, which bind to different domains of the molecular chaperone hsp70/hsc70. Mol. Cell. Biol. 1998, 18:6238-6244.
66. Lopez-Fanarraga M., et al. Review: postchaperonin tubulin folding cofactors and their role in microtubule dynamics. J. Struct. Biol. 2001, 135:219-229.
67. Thulasiraman V., et al. In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J. 1999, 18:85-95.
68. Kerner M.J., et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 2005, 122:209-220.
69. Dekker C., et al. The interaction network of the chaperonin CCT. EMBO J. 2008, 27:1827-1839.
70. Yam A.Y., et al. Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat. Struct. Mol. Biol. 2008, 15:1255-1262.
71. Kubota H., et al. Identification of six Tcp-1-related genes encoding divergent subunits of the TCP-1-containing chaperonin. Curr. Biol. 1994, 4:89-99.
72. Valpuesta J.M., et al. Structure and function of a protein folding machine: the eukaryotic cytosolic chaperonin CCT. FEBS Lett. 2002, 529:11-16.
73. Kubota S., et al. Cytosolic chaperonin protects folding intermediates of Gbeta from aggregation by recognizing hydrophobic beta-strands. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8360-8365.
74. Camasses A., et al. The CCT chaperonin promotes activation of the anaphase-promoting complex through the generation of functional Cdc20. Mol. Cell 2003, 12:87-100.
75. Feldman D.E., et al. Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TRiC. Mol. Cell 1999, 4:1051-1061.