Review: Mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones

Journal of Structural Biology

Volumn 135, Issue 2, 2001, Pages 84-93

  Ben Zvi, Anat Peres ^a   Goloubinoff, Pierre ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Aggregate solubilization; ClpB; DnaK; GroEL; Heat shock; Malate dehydrogenase; Stress

Indexed keywords

AMYLOID; CHAPERONE; POLYGLUTAMINE; POLYPEPTIDE; PROTEIN;

BINDING SITE; CATALYSIS; DRUG MECHANISM; ESCHERICHIA COLI; HYDROLYSIS; PRION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN STABILITY; REVIEW; SOLUBILIZATION; STRESS;

ESCHERICHIA COLI;

EID: 0035783169     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.2001.4352     Document Type: Review

References (73)

1. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains. Science 181, 223-230.
2. Blake, M. J., Fargnoli, J., Gershon, D., and Holbrook, N. J. (1991) Concomitant decline in heat-induced hyperthermia and HSP70 mRNA expression in aged rats. Am. J. Physiol. 260, R663-R667.
3. Buchner, J. (1999) Hsp90 & Co. - A holding for folding. Trends Biochem. Sci. 24, 136-141.
4. Buchner, J., Schmidt, M., Fuchs, M., Jaenicke, R., Rudolph, R., Schmid, F. X., and Kiefhaber, T. (1991) GroE facilitates refolding of citrate synthase by suppressing aggregation. Biochemistry 30, 1586-1591.
5. Bukau, B., and Horwich, A. L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
6. Burston, S. G., and Clarke, A. R. (1995) Molecular chaperones: Physical and mechanistic properties. Essays Biochem. 29, 125-136.
7. Chan, H. Y., Warrick, J. M., Gray-Board, G. L., Paulson, H. L., and Bonini, N. M. (2000) Mechanisms of chaperone suppression of polyglutamine disease: Selectivity, synergy and modulation of protein solubility in Drosophila. Hum. Mol. Genet. 9, 2811-2820.
8. Chernoff, Y. O., Lindquist, S. L., Ono, B., Inge-Vechtomov, S. G., and Liebman, S. W. (1995) Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268, 880-884.
9. De Bernardez Clark, E., Schwarz, E., and Rudolph, R. (1999) Inhibition of aggregation side reactions during in vitro protein folding. Methods Enzymol. 309, 217-236.
10. Diamant, S., Ben-Zvi, A. P., Bukau, B., and Goloubinoff, P. (2000) Size-dependent disaggregation of stable protein aggregates by the DnaK chaperone machinery. J. Biol. Chem. 275, 21107-21113.
11. Diamant, S., Azem, A., Weiss, C., and Goloubinoff, P. (1995) Increased efficiency of GroE-assisted protein folding by manganese ions. J. Biol. Chem. 270, 28387-28391.
12. Ehrnsperger, M., Graber, S., Gaestel, M., and Buchner, J. (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16, 221-229.
13. Ellis, R. J. (1997) Molecular chaperones: Avoiding the crowd. Curr. Biol. 7, R531-R533.
14. Fink, A. L. (1998) Protein aggregation: Folding aggregates, inclusion bodies and amyloid. Fold Des 3, R9-R23.
15. Glover, J. R., and Lindquist, S. (1998) Hsp104, Hsp70, and Hsp40: A novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82.
16. Goloubinoff, P., Christeller, J. T., Gatenby, A. A., and Lorimer, G. H. (1989) Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on two chaperonin proteins and Mg-ATP. Nature 342, 884-889.
17. Goloubinoff, P., Mogk, A., Ben Zvi, A. P., Tomoyasu, T., and Bukau, B. (1999) Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc. Natl. Acad. Sci. USA 96, 13732-13737.
18. Grimaud, R., Kessel, M., Beuron, F., Steven, A. C., and Maurizi, M. R. (1998) Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J. Biol. Chem. 273, 12476-12481.
19. Hartman, D. J., Surin, B. P., Dixon, N. E., Hoogenraad, N. J., and Hoj, P. B. (1993) Substoichiometric amounts of the molecular chaperones GroEL and GroES prevent thermal denaturation and aggregation of mammalian mitochondrial malate dehydrogenase in vitro. Proc. Natl. Acad. Sci. USA 90, 2276-2280.
20. Horwitz, J. (1992) Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89, 10449-10453.
21. Hoskins, J. R., Singh, S. K., Maurizi, M. R., and Wickner, S. (2000) Protein binding and unfolding by the chaperone ClpA and degradation by the protease ClpAP. Proc. Natl. Acad. Sci. USA 97, 8892-8897.
22. Jaenicke, R. (1995) Folding and association versus misfolding and aggregation of proteins. Philos. Trans. R. Soc. London B Biol. Sci. 348, 97-105.
23. Kim, Y. I., Burton, R. E., Burton, B. M., Sauer, R. T., and Baker, T. A. (2000) Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol. Cell 5, 639-648.
24. Klunk, W. E., Jacob, R. F., and Mason, R. P. (1999) Quantifying amyloid by congo red spectral shift assay. Methods Enzymol. 309, 285-305.
25. Krobitsch, S., and Lindquist, S. (2000) Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins. Proc. Natl. Acad. Sci. USA 97, 1589-1594.
26. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M. K., and Hartl, F. U. (1992) Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356, 683-689.
27. Laufen, T., Mayer, M. P., Beisel, C., Klostermeier, D., Mogk, A., Reinstein, J., and Bukau, B. (1999) Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc. Natl. Acad. Sci. USA 96, 5452-5457.
28. Levchenko, I., Luo, L., and Baker, T. A. (1995) Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 9, 2399-2408.
29. LeVine, H. (1999) Quantification of beta-sheet amyloid fibril structures with thioflavin T. Methods Enzymol. 309, 274-284.
30. Lomakin, A., Benedek, G. B., and Teplow, D. B. (1999) Monitoring protein assembly using quasielastic light scattering spectroscopy. Methods Enzymol. 309, 429-459.
31. McLaurin, J., Yang, D., Yip, C. M., and Fraser, P. E. (2000) Review: Modulating factors in amyloid-beta fibril formation. J. Struct. Biol. 130, 259-270.
32. Mendoza, J. A., Rogers, E., Lorimer, G. H., and Horowitz, P. M. (1991) Unassisted refolding of urea unfolded rhodanese. J. Biol. Chem. 266, 13587-13591.
33. Minami, Y., and Minami, M. (1999) Hsc70/Hsp40 chaperone system mediates the Hsp90-dependent refolding of firefly luciferase. Genes Cells 4, 721-729.
34. Minton, A. P. (2000) Implications of macromolecular crowding for protein assembly. Curr. Opin. Struct. Biol. 10, 34-39.
35. Mogk, A., Tomoyasu, T., Goloubinoff, P., Rudiger, S., Roder, D., Langen, H., and Bukau, B. (1999) Identification of thermolabile Escherichia coli proteins: Prevention and reversion of aggregation by DnaK and ClpB. EMBO J. 18, 6934-6949.
36. Motohashi, K., Watanabe, Y., Yohda, M., and Yoshida, M. (1999) Heat-inactivated proteins are rescued by the DnaK. J-GrpE set and ClpB chaperones. Proc. Natl. Acad. Sci. USA 96, 7184-7189.
37. Nimmesgern, E., and Hartl, F. U. (1993) ATP-dependent protein refolding activity in reticulocyte lysate. Evidence for the participation of different chaperone components. FEBS Lett. 331, 25-30.
38. Pak, M., and Wickner, S. (1997) Mechanism of protein remodeling by ClpA chaperone. Proc. Natl. Acad. Sci. USA 94, 4901-4906.
39. Panse, V. G., Vogel, P., Trommer, W. E., and Varadarajan, R. (2000) A thermodynamic coupling mechanism for the disaggregation of a model peptide substrate by chaperone secB. J. Biol. Chem. 275, 18698-18703.
40. Parsell, D. A., Kowal, A. S., Singer, M. A., and Lindquist, S. (1994) Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475-478.
41. Patino, M. M., Liu, J. J., Glover, J. R., and Lindquist, S. (1996) Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273, 622-626.
42. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. USA 95, 13363-13383.
43. Radford, S. E. (2000) Protein folding: Progress made and promises ahead. Trends Biochem. Sci. 25, 611-618.
44. Rudiger, S., Germeroth, L., Schneider-Mergener, J., and Bukau, B. (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J. 16, 1501-1507.
45. Sanchez, Y., Parsell, D. A., Taulien, J., Vogel, J. L., Craig, E. A., and Lindquist, S. (1993) Genetic evidence for a functional relationship between Hsp104 and Hsp70. J. Bacteriol. 175, 6484-6491.
46. Satyal, S. H., Schmidt, E., Kitagawa, K., Sondheimer, N., Lindquist, S., Kramer, J. M., and Morimoto, R. I. (2000) Polyglutamine aggregates alter protein folding homeostasis in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 97, 5750-5755.
47. Schmidt, M., Buchner, J., Todd, M. J., Lorimer, G. H., and Viitanen, P. V. (1994) On the role of groES in the chaperonin-assisted folding reaction. Three case studies. J. Biol. Chem. 269, 10304-10311.
48. Schrimer, E. C., Glover, J. R., Singer, M. A., and Lindquist, S. (1996) HSP100/Clp proteins: A common mechanism explains diverse functions. Trends Biochem. Sci. 21, 289-296.
49. Seonga, I. S., Oha, J. Y., Leeab, J. W., Tanakab, K., and Chunga, C. H. (2000) The HslU ATPase acts as a molecular chaperone in prevention of aggregation of SulA, an inhibitor of cell division in Escherichia coli. FEBS Lett. 477, 224-229.
50. Serio, T. R., and Lindquist, S. L. (2000) Protein-only inheritance in yeast: Something to get [PSI+]-ched about. Trends Cell Biol. 10, 98-105.
51. Singh, S. K., Grimaud, R., Hoskins, J. R., Wickner, S., and Maurizi, M. R. (2000) Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP. Proc. Natl. Acad. Sci. USA 97, 8898-8903.
52. Skowyra, D., Georgopoulos, C., and Zylicz, M. (1990) The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell 62, 939-944.
53. Spiess, C., Beil, A., and Ehrmann, M. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97, 339-347.
54. Stenberg, G., and Fersht, A. R. (1997) Folding of barnase in the presence of the molecular chaperone SecB. J. Mol. Biol. 274, 268-275.
55. Suzuki, C. K., Rep, M., van Dijl, J. M., Suda, K., Grivell, L. A., and Schatz, G. (1997) ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem. Sci. 22, 118-123.
56. Thomas, J. G., and Baneyx, F. (1998) Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: Comparison with ClpA, ClpB, and HtpG in vivo. J. Bacteriol. 180, 5165-5172.
57. Thomas, J. G., and Baneyx, F. (2000) ClpB and HtpG facilitate de novo protein folding in stressed Escherichia coli cells. Mol. Microbiol. 36, 1360-1370.
58. Todd, M. J., and Lorimer, G. H. (1995) Stability of the asymmetric Escherichia coli chaperonin complex. Guanidine chloride causes rapid dissociation. J. Biol. Chem. 270, 5388-5394.
59. Tomoyasu, T., Mogk, A., Langen, H., Goloubinoff, P., and Bukau, B. (2001). Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the E. coli cytosol. Mol. Biol. 40, 397-413. in press.
60. Török, Z., Goloubinoff, P., Horváth, I., Tsvetkova, Glaz, Balogh, Varvasovszki, Vierling, E., Crowe, and Vígh, L. (2001) HSP17 from Synechocystis 6803 is an amphitropic protein with chaperone activity for membranes and proteins under heat-stress. Proc. Natl. Acad. Sci. USA 98, 3098-3103.
61. VanBogelen, R. A., Kelley, P. M., and Neidhardt, F. C. (1987) Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J. Bacteriol. 169, 26-32.
62. van den Berg, B., Ellis, R. J., and Dobson, C. M. (1999) Effects of macromolecular crowding on protein folding and aggregation. EMBO J. 18, 6927-6933.
63. Veinger, L., Diamant, S., Buchner, J., and Goloubinoff, P. (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 273, 11032-11037.
64. Vogel, J. L., Parsell, D. A., and Lindquist, S. (1995) Heat-shock proteins Hsp104 and Hsp70 reactivate mRNA splicing after heat inactivation. Curr. Biol. 5, 306-317.
65. Warrick, J. M., Chan, H. Y., Gray-Board, G. L., Chai, Y., Paulson, H. L., and Bonini, N. M. (1999) Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat. Genet. 23, 425-428.
66. Wawrzynow, A., Wojtkowiak, D., Marszalek, J., Banecki, B., Jonsen, M., Graves, B., Georgopoulos, C., and Zylicz, M. (1995) The ClpX heat-shock protein of Escherichia coli, the ATP-dependent substrate specificity component of the ClpP-ClpX protease, is a novel molecular chaperone. EMBO J. 14, 1867-1877.
67. Weber-Ban, E. U., Reid, B. G., Miranker, A. D., and Horwich, A. L. (1999) Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 401, 90-93.
68. Wickner, S., Gottesman, S., Skowyra, D., Hoskins, J., McKenney, K., and Maurizi, M. R. (1994) A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc. Natl. Acad. Sci. USA 91, 12218-12222.
69. Yamamoto, A., Lucas, J. J., and Hen, R. (2000) Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell 101, 57-66.
70. Zahn, R., Buckle, A. M., Perrett, S., Johnson, C. M., Corrales, F. J., Golbik, R., and Fersht, A. R. (1996a) Chaperone activity and structure of monomeric polypeptide binding domains of GroEL. Proc. Natl. Acad. Sci. USA 93, 15024-15029.
71. Zahn, R., Perrett, S., and Fersht, A. R. (1996b) Conformational states bound by the molecular chaperones GroEL and secB: A hidden unfolding (annealing) activity. J. Mol. Biol. 261, 43-61.
72. Ziemienowicz, A., Skowyra, D., Zeilstra-Ryalls, J., Fayet, O., Georgopoulos, C., and Zylicz, M. (1993) Both the Escherichia coli chaperone systems, GroEL/GroES and DnaK/DnaJ/GrpE, can reactivate heat-treated RNA polymerase. Different mechanisms for the same activity. J. Biol. Chem. 268, 25425-25431.
73. Zolkiewski, M. (1999) ClpB cooperates with DnaK, DnaJ, and GrpE in suppressing protein aggregation. A novel multi-chaperone system from Escherichia coli. J. Biol. Chem. 274, 28083-28086.