Chaperonin-mediated folding in the eukaryotic cytosol proceeds through rounds of release of native and nonnative forms

Cell

Volumn 89, Issue 6, 1997, Pages 927-937

  Farr, George W ^a   Scharl, Elizabeth C ^b   Schumacher, Robert J ^a   Sondek, Stacey ^a   Horwich, Arthur L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN; TRANSDUCIN; TUBULIN;

ARTICLE; CYTOSOL; EUKARYOTE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PURIFICATION; RETICULOCYTE LYSATE; XENOPUS LAEVIS;

BACTERIA (MICROORGANISMS); EUKARYOTA; XENOPUS LAEVIS;

EID: 0030730821     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80278-0     Document Type: Article

References (38)

1. Buchberger, A., Schröder, H., Hesterkamp, T., Schönfeld, H.J., and Bukau, B. (1996). Substrate shuttling between the DnaK and GroEL systems indicates a chaperone network promoting protein folding. J. Mol. Biol. 261, 328-333.
2. Ellis, R.J., and Hartl, F.U. (1996). Protein folding in the cell: competing models of chaperonin function. FASEB J. 10, 20-26.
3. Faurobert, E., Otto-Bruc, A., Chardin, P., and Chabre, M. (1993). Tryptophan W207 in transducin Tα is the fluorescence sensor of the G protein activation switch and is involved in the effector binding. EMBO J. 12, 4191-4198.
4. Fenton, W.A., and Horwich, A.L. (1997). GroEL-mediated protein folding. Prot. Sci. 6, 743-760.
5. Frydman, J., Nimmesgern, E., Ohtsuka, K., and Hartl, F.U. (1994). Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370, 111-117.
6. Frydman, J., and Hartl, F.U. (1996). Principles of chaperone-assisted protein folding: differences between in vitro and in vivo mechanisms. Science 272, 1497-1502.
7. Gao, Y., Thomas, J.O., Chow, R.L., Lee, G.-H., and Cowan, N.J. (1992). Acytoplasmic chaperonin that catalyzes β-actin folding. Cell 69, 1043-1050.
8. Gao, Y., Vainberg, I.E., Chow, R.L., and Cowan, N.J. (1993). Two cofactors and cytoplasmic chaperonin are required for the folding of α-and β-tubulin. Mol. Cell. Biol. 13, 2478-2485.
9. Gao, Y., Melki, R.,Waiden, 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.
10. Gragerov, A., Nudler, E., Komissarova, N., Gaitanaris, G.A., Gottesman, M.E., and Nikiforov, V. (1992). Cooperation of GroEL/GroES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc. Natl. Acad. Sci. USA 89, 10341-10344.
11. Gunning, P., Ponte, P., Okayama, H., Engel, J., Blau, H., and Kedes, L. (1983). Isolation and characterization of full-length cDNA clones for human α, β, and γ-actin mRNAs. Mol. Cell. Biol. 3, 787-795.
12. Hartl, F.U. (1996). Molecular chaperones in cellular protein folding. Nature 381, 571-580.
13. Kubota, H., Hynes, G., and 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.
14. Lazarides, E., and Lindberg, U. (1974). Actin is the naturally occurring inhibitor of deoxyribonuclease I. Proc. Natl. Acad. Sci. USA 71, 4742-4746.
15. Levilliers, N., Peron-Renner, M., Coffe, G., and Pudles, J. (1984). Actin purification from a gel of rat brain extracts. Biochimie 66, 531-537.
16. Lewis, S.A., Tian, G., Vainberg, I.E., and Cowan, N.J. (1996). Chaperonin-mediated folding of actin and tubulin. J. Cell Biol. 132, 1-4.
17. Marco, S., Carrascosa, J.L., and Valpuesta, J.M. (1994). Reversible interaction of beta-actin along the channel of the TCP-1 cytoplasmic chaperonin. Biophys. J. 67, 364-368.
18. Martin, J., and Hartl, F.-U. (1997). The effect of macromolecular crowding on chaperonin-mediated protein folding. Proc. Natl. Acad. Sci. USA 94, 1107-1112.
19. t. Biochemistry 28, 9873-9880.
20. t. J. Biol. Chem. 266, 14072-14081.
21. Medynski, D.C., Sullivan, K., Smith, D., van Dop, C., Chang, F.-H., Fung, B.K.-K., Seeburg, P.H., and Bourne, H.R. (1985). Amino acid sequence of the a subunit of transducin deduced from the cDNA sequence. Proc. Natl. Acad. Sci. USA 82, 4311-4315.
22. Melki, R., and Cowan, N.J. (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.
23. Melki, R., Rommelaere, H., Leguy, R., Vandekerckhove, J., and Ampe, C. (1996). Cofactor A is a molecular chaperone required for β-tubulin folding: functional and structural characterization. Biochemistry 35, 10422-10435.
24. Ranson, N.A., Dunster, N.J., Burston, S.G., and Clarke, A.R. (1995). Chaperonins can catalyze the reversal of early aggregation steps when a protein misfolds. J. Mol. Biol. 250, 581-586.
25. Rosenblatt, J., Peluso, P., and Mitchison, T. (1995). The bulk of unpolymerized actin in Xenopus egg extracts is ATP-bound. Mol. Biol. Cell 6, 227-236.
26. Shoemaker, M.T., and Haley, B.E. (1993). Identification of a guanine binding domain peptide of the GTP binding site of glutamate dehydrogenase: isolation with metal-chelate affinity chromatography. Biochemistry 32, 1883-1890.
27. αi1 chimeras. J. Biol. Chem. 271, 413-424.
28. Sternlicht, H., and Ringel, I. (1979). Colchicine inhibition of microtu-bule assembly via copolymer formation. J. Biol. Chem. 254, 10540-10550.
29. Sternlicht, H., Farr, G., Sternlicht, M., Driscoll, J., Willison, K., and Yaffe, M. (1993). The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc. Natl. Acad. Sci. USA 90, 9422-9426.
30. Tian, G., Vainberg, I.E., Tap, W.D., Lewis, S.A., and Cowan, N.J. (1995a). Specificity in chaperonin-mediated protein folding. Nature 375, 250-253.
31. Tian, G., Vainberg, I.E., Tap, W.D., Lewis, S.A., and Cowan, N.J. (1995b). Quasi-native chaperonin-bound intermediates in facilitated protein folding. J. Biol. Chem. 270, 23910-23913.
32. Tian, G., Huang, Y., Rommelaere, H., Vandekerckhove, J., Ampe, C., and Cowan, N.J. (1996). Pathway leading to correctly folded β-tubulin. Cell 86, 287-296.
33. Todd, M.J., Lorimer, G.H., and Thirumalai, D. (1996). Chaperoninfacilitated protein folding: optimization of rate and yield by an iterative annealing mechanism. Proc. Natl. Acad. Sci. USA 93, 4030-4035.
34. Ursic, D., and Culbertson, M.R. (1991). The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol. Cell. Biol. 11, 2629-2640.
35. Vinh, D.B.-N., and Drubin, D.G. (1994). A yeast TCP-1-llke protein is required for actin function in vivo. Proc. Natl. Acad. Sci. USA 91, 9116-9120.
36. Weissman, J.S., Kashi, Y., Fenton, W.A., and Horwich, A.L. (1994). GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78, 693-702.
37. Yaffe, M.B., Farr, G.W., and Sternlicht, H. (1988). Translation of β-tubulin mRNA in vitro generates multiple molecular forms. J. Biol. Chem. 263, 16023-16031.
38. Yaffe, M.B., Farr, G.W., Miklos, D., Horwich, A.L., Sternlicht, M., and Sternlicht, H. (1992). TCP-1 complex is a molecular chaperone in tubulin biogenesis. Nature 355, 245-248.