Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT

EMBO Journal

Volumn 21, Issue 23, 2002, Pages 6377-6386

  Martín Benito, Jaime ^a   Boskovic, Jasminka ^a   Gómez Puertas, Paulino ^a   Carrascosa, José L ^a   Simons, C Torrey ^a,b   Lewis, Sally A ^a,b   Bartolini, Francesca ^a,b   Cowan, Nicholas J ^a,b   Valpuesta, José M ^a  

^a CSIC   (Spain)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Actin; Chaperonin; Electron microscopy; Prefoldin; Protein folding

Indexed keywords

ACTIN; CELL PROTEIN; CHAPERONIN; CHAPERONIN CCT; OLIGOMER; PREFOLDIN; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; ARTICLE; BIOGENESIS; CRYOELECTRON MICROSCOPY; CYTOSOL; ELECTRON MICROSCOPY; EUKARYOTE; IMAGE RECONSTRUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; THREE DIMENSIONAL IMAGING;

ACTINS; ANIMALS; CATTLE; CHAPERONINS; MALE; METHANOBACTERIUM; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN FOLDING;

ARCHAEA; EUKARYOTA;

EID: 0037011162     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf640     Document Type: Article

References (60)

1. Buckle, A.M., Zahn, R. and Fersht, A.R. (1997) A structural model for GroEL-polypeptide recognition. Proc. Natl. Acad. Sci. USA, 94, 3571-3575.
2. Bukau, B. and Horwich, A.L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell, 92, 351-380.
3. Bukau, B., Deuerling, E., Pfund, C. and Craig, E.A. (2000) Getting newly synthesized proteins into shape. Cell, 101, 119-122.
4. Chen, X., Sullivan, D.S. and Huffaker, T.C. (1994) 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.
5. Cowan, N.J. and Lewis, S.A. (2002) Type II chaperonins, prefoldin and the tubulin-specific chaperones. Adv. Protein Chem., 59, 73-104.
6. Ellis, R.J. (1996) The Chaperonins. Academic Press, San Diego, CA.
7. Fandrich, M., Tito, M.A., Leroux, M.R., Rostom, A.A., Hartl, F.U., Dobson, C.M. and Robinson, C.V. (2000) Observation of the noncovalent assembly and disassembly pathways of the chaperone complex MtGimC by mass spectrometry. Proc. Natl. Acad. Sci. USA, 97, 14151-14155.
8. Farr, G.W., Scharl, E.C., Schumacher, R.J., Sondek, S. and Horwich, A.L. (1997) Chaperonin-mediated folding in the eukaryotic cytosol proceeds through rounds of release of native and nonnative forms. Cell, 89, 927-937.
9. Feldman, D.E. and Frydman, J. (2000) Protein folding in vivo: The importance of molecular chaperones. Curr. Opin. Struct. Biol., 10, 26-33.
10. Feldman, D.E., Thulasiraman, V., Ferreyra, R.G. and Frydman, J. (1999) Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin TRiC. Mol. Cell, 4, 1051-1061.
11. Frank, J. (1996) Three-Dimensional Electron Microscopy of Macromolecular Assemblies. Academic Press, San Diego, CA, pp. 182-246.
12. Frydman, J. (2001) Folding of newly translated proteins in vivo: The role of molecular chaperones. Annu. Rev. Biochem., 70, 603-647.
13. Frydman, J., Nimmesgern, E., Erdjument-Bromage, H., Wall, J.S., Tempst, P. and Hartl, F.U. (1992) Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. EMBO J., 11, 4767-4778.
14. Gao, Y., Thomas, J.O., Chow, R.L., Lee, G.H. and Cowan, N.J. (1992) A cytoplasmic chaperonin that catalyzes β-actin folding. Cell, 69, 1043-1050.
15. Gao, Y., Melki, R., Walden, P.D., Lewis, S.A., Ampe, C., Rommelaere, H., Vandekerckhove, J. and Cowan, N.J. (1994) A novel cochaperonin that modulates the ATPase activity of cytoplasmic chaperonin. J. Cell Biol., 125, 989-996.
16. Geissler, S., Siegers, K. and Schiebel, E. (1998) A novel protein complex promoting formation of functional α- and γ-tubulin. EMBO J., 17, 952-966.
17. Grantcharova, V., Alm, E.J., Baker, D. and Horwich, A.L. (2001) Mechanisms of protein folding. Curr. Opin. Struct. Biol., 11, 70-82.
18. Guex, N. and Peitsch, M.C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling. Electrophoresis, 18, 2714-2723.
19. Hansen, W.J., Cowan, N.J. and Welch, W.J. (1999) Prefoldin-nascent chain complexes in the folding of cytoskeletal proteins. J. Cell Biol., 145, 265-277.
20. Hartl, F.U. (1996) Molecular chaperones in cellular protein folding. Nature, 381, 571-579.
21. Heymann, J.B. (2001) Bsoft: Image and molecular processing in electron microscopy. J. Struct. Biol., 133, 156-169.
22. Horwich, A.L., Fenton, W.A. and Rapoport, T.A. (2001) Protein folding taking shape: Workshop on molecular chaperones. EMBO Rep., 2, 1068-1073.
23. Humphrey, W., Dalke, A. and Schulten, K. (1996) VMD: Visual molecular dynamics. J. Mol. Graphics, 14, 33-38.
24. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjeldgaard. (1991) Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A, 47, 110-119.
25. Kabsch, W., Mannherz, H.G., Suck, D., Pai, E.F. and Holmes, K.C. (1990) Atomic structure of the actin:DNase I complex. Nature, 347, 37-44.
26. Klumpp, M., Baumeister, W. and Essen, L.O. (1997) Structure of the substrate binding domain of the thermosome, an archaeal group II chaperonin. Cell, 91, 263-270.
27. Leroux, M.R., Fandrich, M., Klunker, D., Siegers, K., Lupas, A.N., Brown, J.R., Schiebel, E., Dobson, C.M. and Hartl, F.U. (1999) MtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin. EMBO J., 18, 6730-6743.
28. Lewis, V.A., Hynes, G.M., Zheng, D., Saibil, H. and Willison, K. (1992) T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukaryotic cytosol. Nature, 358, 249-252.
29. Liou, A.K. and Willison, K.R. (1997) Elucidation of the subunit orientation in CCT (chaperonin containing TCP1) from the subunit composition of CCT micro-complexes. EMBO J., 16, 4311-4316.
30. Llorca, O., McCormack, E.A., Hynes, G., Grantham, J., Cordell, J., Carrascosa, J.L., Willison, K.R., Fernandez, J.J. and Valpuesta, J.M. (1999) Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature, 402, 693-696.
31. Llorca, O., Martin-Benito, J., Ritco-Vonsovici, M., Grantham, J., Hynes, G.M., Willison, K.R., Carrascosa, J.L. and Valpuesta, J.M. (2000) Eukaryotic chaperonin CCT stabilizes actin and tubulin folding intermediates in open quasi-native conformations. EMBO J., 19, 5971-5979.
32. Llorca, O., Martin-Benito, J., Gomez-Puertas, P., Ritco-Vonsovici, M., Willison, K.R., Carrascosa, J.L. and Valpuesta, J.M. (2001a) Analysis of the interaction between the eukaryotic chaperonin CCT and its substrates actin and tubulin. J. Struct. Biol., 135, 205-218.
33. Llorca, O., Martin-Benito, J., Grantham, J., Ritco-Vonsovici, M., Willison, K.R., Carrascosa, J.L. and Valpuesta, J.M. and (2001b) The 'sequential allosteric ring' mechanism in the eukaryotic chaperonin-assisted folding of actin and tubulin. EMBO J., 20, 4065-4075.
34. Lorimer, G. (1997) Protein folding. Folding with a two-stroke motor. Nature, 388, 720-721, 723.
35. Marabini, R. and Carazo, J.M. (1994) Pattern recognition and classification of images of biological macromolecules using artificial neural networks. Biophys. J., 66, 1804-1814.
36. Marabini, R., Herman, G.T. and Carazo, J.M. (1998) 3D reconstruction in electron microscopy using ART with smooth spherically symmetric volume elements (blobs). Ultramicroscopy, 72, 53-65.
37. McCallum, C.D., Do, H., Johnson, A.E. and 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, 591-602.
38. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
39. Nielsen, K.L. and Cowan, N.J. (1998) A single ring is sufficient for productive chaperonin-mediated folding in vivo. Mol. Cell, 2, 93-99.
40. Nogales, E., Wolf, S.G. and Downing, K.H. (1998) Structure of the αβ tubulin dimer by electron crystallography [published erratum appears in Nature, 1998, 393, 191]. Nature, 391, 199-203.
41. Norcum, M.T. (1996) Novel isolation method and structural stability of a eukaryotic chaperonin: The TCP-1 ring complex from rabbit reticulocytes. Protein Sci., 5, 1366-1375.
42. Penczek, P., Radermacher, M. and Frank, J. (1992) Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy, 40, 33-53.
43. Ranson, N.A., White, H.E. and Saibil, H.R. (1998) Chaperonins. Biochem. J., 333, 233-242.
44. Rommelaere, H., De Neve, M., Neirynck, K., Peelaers, D., Waterschoot, D., Goethals, M., Fraeyman, N., Vandekerckhove, J. and Ampe, C. (2001) Prefoldin recognition motifs in the nonhomologous proteins of the actin and tubulin families. J. Biol. Chem., 276, 41023-41028.
45. Rye, H.S., Burston, S.G., Fenton, W.A., Beechem, J.M., Xu, Z., Sigler, P.B. and Horwich, A.L. (1997) Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature, 388, 792-798.
46. Saibil, H. (2000) Molecular chaperones: Containers and surfaces for folding, stabilising or unfolding proteins. Curr. Opin. Struct. Biol., 10, 251-258.
47. Schüler, H., Lindberg, U., Schutt, C.E. and Karlsson, R. (2000) Thermal unfolding of G-actin monitored with the DNase I-inhibition assay. Eur. J. Biochem., 267, 476-486.
48. Schwede, T., Diemand, A., Guex, N. and Peitsch, M.C. (2000) Protein structure computing in the genomic era. Res. Microbiol., 151, 107-112.
49. Siegers, K., Waldmann, T., Leroux, M.R., Grein, K., Shevchenko, A., Schiebel, E. and Hartl, F.U. (1999) Compartmentation of protein folding in vivo: Sequestration of non-native polypeptide by the chaperonin-GimC system. EMBO J., 18, 75-84.
50. Siegert, R., Leroux, M.R., Scheufler, C., Hartl, F.U. and Moarefi, I. (2000) Structure of the molecular chaperone prefoldin. Unique interaction of multiple coiled coil tentacles with unfolded proteins. Cell, 103, 621-632.
51. Sternlicht, H., Farr, G.W., Sternlicht, M.L., Driscoll, J.K., Willison, K. and Yaffe, M.B. (1993) The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc. Natl. Acad. Sci. USA, 90, 9422-9426.
52. Thulasiraman, V., Yang, C.F. and Frydman, J. (1999) In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J., 18, 85-95.
53. Tian, G., Vainberg, I.E., Tap, W.D., Lewis, S.A. and Cowan, N.J. (1995) Specificity in chaperonin-mediated protein folding. Nature, 375, 250-253.
54. Unser, M., Trus, B.L. and Steven, A.C. (1987) A new resolution criterion based on spectral signal-to-noise ratios. Ultramicroscopy, 23, 39-51.
55. Vainberg, I.E., Lewis, S.A., Rommelaere, H., Ampe, C., Vandekerckhove, J., Klein, H.L. and Cowan, N.J. (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell, 93, 863-873.
56. Vinh, D.B. and Drubin, D.G. (1994) A yeast TCP-1-like protein is required for actin function in vivo. Proc. Natl. Acad. Sci. USA, 91, 9116-9120.
57. Weissman, J.S., Hohl, C.M., Kovalenko, O., Kashi, Y., Chen, S., Braig, K., Saibil, H.R., Fenton, W.A. and Horwich, A.L. (1995) Mechanism of GroEL action: Productive release of polypeptide from a sequestered position under GroES. Cell, 83, 577-587.
58. Willison, K.R. (1999) Composition and function of the eukaryotic cytosolic chaperonin containing TCP1. In Bukau, B. (ed.), Molecular Chaperones and Folding Catalysts. Harwood Academic Publishers, Amsterdam, The Netherlands, pp. 555-571.
59. Willison, K.R. (2001) The roles of cytosolic chaperonin, CCT, in normal eukaryotic cell growth. In Lund, P. (ed.), Molecular Chaperones: Frontiers in Molecular Biology. Oxford University Press, Oxford, England, pp. 90-118.
60. Won, K.A., Schumacher, R.J., Farr, G.W., Horwich, A.L. and Reed, S.I. (1998) Maturation of human cyclin E requires the function of eukaryotic chaperonin CCT. Mol. Cell. Biol., 18, 7584-7589.