The Effect of Molecular Chaperones on in Vivo and in Vitro Folding Processes

Biological Chemistry Hoppe-Seyler

Volumn 377, Issue 7-8, 1996, Pages 411-488

  Schwarz, Elisabeth ^a   Lilie, Hauke ^a   Rudolph, Rainer ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; BIOTECHNOLOGY; CELL INCLUSION; CONTROLLED STUDY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; SHORT SURVEY; STRESS;

HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; PROTEIN FOLDING;

EID: 0029842904     PISSN: 01773593     EISSN: None     Source Type: Journal    
DOI: 10.1515/bchm3.1996.377.7-8.411     Document Type: Article

References (76)

1. Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science 787,223–230.
2. Amrein, K. E., Takacs, B., Stieger, M., Molnos, J., Flint, N. A., and Burn, P. (1995). Purification and characterization of recombinant human p50csk protein-tyrosine kinase from an Escherichia coli expression system overproducing the bacterial chaperones GroES and GroEL. Proc. Natl. Acad. Sci. USA 92, 1048–1052.
3. Ang, D., Liberek, K., Skowyra, D., Zylicz, M., and Georgopoulos, C. (1991). Biological role and regulation of the universally conserved heat shock proteins. J. Biol. Chem. 266,24233–24236.
4. Allen, S. P., Polazzi, J. O., Gierse, J. K., Easton, A. M. (1992). Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J. Bacteriol. 174, 6938–6947.
5. Bansal, G. S., Norton, P. M., Latchman, D. S. (1991). The 90-kDa heat shock protein protects mammalian cells from thermal stress but not from viral infection. Exp. Cell Res. 195,303–306.
6. Blond-Elguindi, S., Cwirla, S. E., Dower, W. J., Lipshutz, R. J., Sprang, S. R., Sambrook, J. F., and Gething, M. J. H. (1993). Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75, 717–728.
7. Buchner, J. (1996). Supervising the fold: functional principles of molecular chaperones. FASEB J. 10,10–19.
8. 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.
9. Bukau, B., and Walker, G. C. (1990). Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone. EMBO J. 9, 4027–4036.
10. Cheng, M. Y., Hartl, F. U., Martin, J., Pollock, R. A., Kalousek, F., Neupert, W., Hallberg, E. M., Hallberg, R. L., and Horwich, A. L. (1989). Mitochondrial heat shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337,620–625.
11. Cheng, M. Y., Hartl, F. U., and Horwich, A. L. (1990). The mitochondrial chaperonin hsp60 is required for its own assembly. Nature 348,455–458.
12. Corrales, F. J., and Fersht, A. R. (1995). The folding of GroEL-bound barnase as a model for chaperonin-mediated protein folding. Proc. Natl. Acad. Sci. USA 92, 5326–5330.
13. Ellis, R. J. (1993). The general concept of molecular chaperones. In: Molecular Chaperones. Biological Sciences, Vol. 339, R. J. Ellis, R. A. Laskey and G. H. Lorimer, eds. (Phil. Trans. R. Soc. London B), pp. 257–261.
14. Ellis, R. J. (1994). Molecular chaperones - opening and closing the Anfinsen cage. Curr. Biol. 4, 633–635.
15. Escher, A., and Szalay, A. A. (1993). GroE-mediated folding of bacterial luciferase in vivo. Mol. Gen. Genet. 238, 65–73.
16. Fayet, O., Ziegelhoffer, T., and Georgopoulos, C. (1986). The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J. Bacteriol. 171,1379–1385.
17. Friedman, D. I., Olson, E. R., Georgopoulos, C., Tilly, K., Herskowitz, I., and Banuett, F. (1984). Interactions of bacteriophage and host molecules in the growth of bacteriophage lambda. Microbiol. Rev. 48, 299–325.
18. 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.
19. Gao, Y., Thomas, J. O., Chow, R. L., Lee, G. H., and Cowan, N. J. (1992). A cytoplasmic chaperonin that catalyzes ß-actin folding. Cell 69,1043–1050.
20. Gao, Y., Vainberg, I. E., Chow, R. L., and Cowan, N. J. (1993). Two cofactors and cytoplasmic chaperonin are required for the folding of a-and ß-tubulin. Mol. Cell. Biol. 13, 2478–2485.
21. Georgopoulos, C. P., and Herskowitz, I. (1971). Escherichia coli mutants blocked in lambda DNA synthesis. In: The Bacteriophage Lambda. A. D. Hershey, ed. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 553–564.
22. Georgopoulos, C., Ang, D., Liberek, K., and Zylicz, M. (1990). In: Stress Proteins in Biology and Medicine. R. Morimoto, A. Tissieres, and C. Georgopoulos, eds. (Cold Spring Harbor, New York: CSH Press), pp. 191–221.
23. Goloubinoff, P., Gatenby, A. A., and Lorimer, G. H. (1989). GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature 337, 44–47.
24. Gragerov, A., Nudler, E., Komissarowa, N., Gaitanaris, G. A., Gottesman, M. E., and Nikiforov, V. (1992). Cooperation of GroEL/ES and DnaK/DnaJ heat shock proteins in preventing protein misfolding in Escherichia coli. Proc. Natl. Acad. Sci. USA 89,10341–10344.
25. Gragerov, A., and Gottesmann, M. E. (1994). Different peptide specificities of hsp70 family members. J. Mol. Biol. 241, 133–135.
26. Gray, T. E., Eder, J., Bycroft, M., Day, A. G., and Fersht, A. R. (1993). Refolding of barnase mutants and pro-barnase in the presence and absence of GroEL. EMBO J. 12, 4145–4150.
27. Hammond, C., and Helenius, A. (1995). Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7, 523–529.
28. Hayer-Hartl, M. K., Ewbank, J. E., Creighton, T. E., and Hartl, F. U. (1994). Conformational specificity of the chaperonin GroEL for the compact folding intermediates of a-lactalbumin. EMBO J. 13, 3192–3202.
29. Hemmingsen, S. M., Woolford, C., van der Vies, S. M., Tilly, K., Dennis, D. T., Georgopoulos, C., Hendrix, R. W., and Ellis, R. J. (1988). Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333, 330–334.
30. Höll-Neugebauer, B., Rudolph, R., Schmidt, M., and Buchner, J. (1991). Reconstitution of a heat shock effect in vitro: Influence of GroE on the thermal aggregation of a-glucosidase from yeast. Biochemistry 30,11609–11614.
31. Horwich, A. L., Low, K. B., Fenton, W. A., Hirshfield, I. N., and Furtak, K. (1993). Folding in vivo of bacterial cytoplasmic proteins: Role of GroEL. Cell 74, 909–917.
32. Jackson, G. S., Staniforth, R. A., Halsall, D. J., Atkinson, T., Holbrook, J. J., Clarke, R. A., and Burston, S. G. (1993). Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle: Implications for the mechansim of assisted protein folding. Biochemistry 32, 2554–2563.
33. Jämsä, E., Vakula, N., Arffman, A., Kilpeläinen, I., and Makarow, M. (1995). In vivo reactivation of heat-denatured protein in the endoplasmic reticulum of yeast. EMBO J. 14, 6028–6033.
34. Jakob, U., Gaestel, M., Engel, K., and Buchner, J. (1993). Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268, 1517–1520.
35. Jakob, U., and Buchner, J. (1994). Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones. Trends Biochem. Sci. 19, 205–211.
36. Jakob, U., Scheibel, T., Bose, S., Reinstein, J., and Buchner, J. (1996). Assessment of the ATP binding properties of Hsp90. J. Biol. Chem. 271,10035–10041.
37. Knauf, U., Jakob, U., Engel, K., Buchner, J., and Gaestel, M. (1994). Stress-and mitogen-induced phosphorylation of the small heat shock protein Hsp25 by MAPKAP kinase 2 is not essential for chaperone properties and cellular thermoresistance. EMBOJ. 13, 54–60.
38. Landry S. J., Jordan, R., McMacken, R. and Gierasch, L. M. (1992). Different conformations for the same polypeptide bound to chaperones DnaK and GroEL. Nature 355,455–457.
39. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M. K., and Hartl, F. U. (1992). Successive action of DnaK, DnaJ and GroELalong the pathway of chaperone-mediated protein folding. Nature 356, 683–689.
40. Laskey, R. A., Honda, B. M., Mills, A. D., and Finch, J. T. (1978). Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275, 416–420.
41. Laskey, R. A., Mills, A. D., Philpott, A., Leno, G. H., Dilworth, S. M., and Dingwall, C. (1993). The role of nucleoplasmin in chromatin assembly and disassembly. In: Molecular Chaperones. Biological Sciences, Vol. 339, R. J. Ellis, R. A. Laskey and G. H. Lorimer, eds. (Phil. Trans. R. Soc. London B), pp. 263–269.
42. Lee, S. C., and Olins, P. O. (1992). Effect of overproduction of heat shock chaperones GroESL and DnaK on human procollagenase production in Escherichia coli. J. Biol. Chem. 267, 2849–2852.
43. Li, G. C., Li, L. G., Liu, Y. K., Mak, J. Y., Chen, L., and Lee, W. M. (1991). Thermal response of rat fibroblasts stably transfected with the human 70 kDa heat shock protein encoding gene. Proc. Natl. Acad. Sci. USA 88,1681–1685.
44. Maeda, Y., Ueda, T., and Imoto, T. (1996). Effective renaturation of denatured and reduced immunoglobulin G in vitro without assistance of chaperone. Protein Engin. 9, 95–100.
45. Martin, J., Horwich, A. L., and Hartl, F. U. (1992). Prevention of protein dénaturation under heat stress by the chaperonin hsp60. Science 258, 995–998.
46. Martin, J., Mayhew, M., Langer, T., and Hartl, F. U. (1993). The reaction cycle of GroEL and GroES in chaperonin-assisted protein folding. Nature 366, 228–233.
47. Mayhew, M., da Silva, A. C. R., Martin, J., Erdjument-Bromage, H., Tempst, P., and Hartl, F. U. (1996). Protein folding in the central cavity of the GroEL-GroES chaperonin complex. Nature 379, 420–426.
48. Nelson, R. J., Ziegelhoffer. T., Nicolet, C., Werner-Washburne, M., and Craig, E. A. (1992). The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71,97–105.
49. Neupert, W., and Hartl, F. U. (1992). Verfahren zur biokatalytischen korrekten Kettenfaltung denaturierter rekombinanter Fusionsproteine. German Patent No. DE 39 26103 C2.
50. Nguyen, V. T., and Bensaude, O. (1994). Increased thermal aggregation of proteins in ATP-depleted mammalian cells. Eur. J. Biochem. 220, 239–246.
51. Nover, L., and Scharf, K. D. (1984). Synthesis, modification and structural binding of heat-shock proteins in tomato cell cultures. Eur. J. Biochem. 139, 303–308.
52. Parseli, D. A., Kowal, A. S., Singer, M. A., and Lindquist, S. (1994). Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372, 475–478.
53. Pelham, H. R. B. (1986). Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46, 959–961.
54. Petko, L., and Lindquist, S. (1986). Hsp26 is not required for growth at high temperatures, nor for thermotolerance, spore development, or germination. Cell 45, 885–894.
55. Prip-Buus, C., Westermann, B., Schmitt, M., Langer, T., Neupert, W., and Schwarz, E. (1996). Role of the mitochondrial DnaJ homologue, Mdj1 p, in the prevention of heat-induced protein aggregation. FEBS Lett. 380,142–146.
56. Ranson, N. A., Dunster, N. J., Burston, S. G., and Clarke, A. R. (1995). Chaperoninscan catalyse the reversal of early aggregation steps when a protein misfolds. J. Mol. Biol. 250, 581–586.
57. Rudolph, R. (1996). Successful protein folding on an industrial scale. In: Protein Engineering: Principles and Practice. J. L. Cleland, and C. S. Craik, eds. (London, New York: Wiley-Liss, Inc.).
58. Rudolph, R., and Lilie, H. (1996). In vitro folding of inclusion body proteins. FASEB J. 10,49–56.
59. Saibil, H. (1996). The lid that shapes the pot: structure and function of the chaperonin GroES. Nature Structure 4,1–4.
60. Schmidt, M., and Buchner, J. (1992). Interaction of GroE with an all-ß-protein. J. Biol. Chem. 267,16829–16833.
61. Schröder, H., Langer, T., Hartl, F. U., and Bukau. B. (1993). DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J. 12, 4137–4144.
62. 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.
63. Smith, K. E., and Fisher, M. T. (1995). Interactions between the GroE chaperonins and rhodanese. J. Biol. Chem. 270, 21517–21523.
64. 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.
65. Todd, M. J., Viitanen, P. V., and Lorimer, G. H. (1994). Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science 265, 659–666.
66. Ursic, D., and Culbertson, M. R. (1991). The yeast homolog to mouse TCP-1 affects microtubule-mediated processes. Mol. Cell. Biol. 11, 2629–2640.
67. van den IJssel, P. R. L. A., Overkamp, P., Knauf, U., Gaestel, M., de Jong, W. W. (1994). aA-crystallin confers cellular thermoresistance. FEBS Lett. 355, 54–56.
68. Viitanen, P. V., Gatenby, A. A., and Lorimer, G. H. (1992). Purified chaperonin 60 (groEL) interacts with nonnative states of a multitude of Escherichia coli proteins. Protein Sci. 1,363–369.
69. 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.
70. 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.
71. Weissman, J. S., Rye, H. S., Fenton, W. A., Beechem, J. M., Horwich, A. L. (1996). Characterization of the active intermediate of a GroEL-GroES-mediated protein folding reaction. Cell 84, 481–490.
72. Wiech, H., Buchner, J., Zimmermann, R., and Jakob, U. (1992). Hsp90 chaperones protein folding in vitro. Nature 358, 169–170.
73. Yaffe, M. B., Farr, G. W., Miklos, D., Horwich, A. L., Sternlicht, M. L., and Sternlicht, H. (1992). TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature 358, 245–248.
74. Zettlmeissl, G., Rudolph, R., and Jaenicke, R. (1979). Reconstitution of lactic dehydrogenase. Noncovalent aggregation vs. reactivation. 1. Physical properties and kinetics of aggregation. Biochemistry 18, 5567–5571.
75. Ziemienowicz, A., Skowyra, D., Zeilstra-Ryalls, J., Fayet, O., Georgopoulos. C., and Zylicz, M. (1993). Both the Escherichia coli chaperone systems, GroELVGroES and DnaK/DnaJ/GrpE, can reactivate heat-treated RNA-polymerase. Different mechanism for the activity. J. Biol. Chem. 268,25425–25431.
76. Ziemienowicz, A., Zylicz, M., Floth, C., and Hübscher, U. (1995). Calf thymus Hsc70 protein protects and reactivates prokaryotic and eukaryotic enzymes. J. Biol. Chem. 270, 15479–15484.