GroEL-mediated folding of structurally homologous dihydrofolate reductases

Journal of Molecular Biology

Volumn 268, Issue 2, 1997, Pages 512-525

  Clark, A Clay ^a   Frieden, Carl ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chaperonin; DHFR; Kinetics; Protein folding; Stopped flow fluorescence

Indexed keywords

CHAPERONIN; DIHYDROFOLATE REDUCTASE;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ESCHERICHIA COLI; FLUORESCENCE; HUMAN; MASS ACTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY;

ESCHERICHIA COLI; MURINAE;

EID: 0031547963     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.0969     Document Type: Article

References (54)

1. Ahrweiler P. M., Frieden C. Effects of point mutations in a hinge region on the stability, folding, and enzymatic activity of Escherichia coli dihydrofolate reductase. Biochemistry. 30:1991;7801-7909.
2. Ayling A., Baneyx F. Influence of the GroE molecular chaperone machine on the in vitro refolding of Escherichia coli beta-galactosidase. Protein Sci. 5:1996;478-487.
3. Baccanari D., Phillips A., Smith S., Sinski D., Burchall J. Purification and properties of Escherichia coli dihydrofolate reductase. Biochemistry. 24:1975;5267-5273.
4. Badcoe I. G., Smith C. J., Wood S., Halsall D. J., Holbrook J. J., Lund P., Clarke A. R. Binding of a chaperonin to the folding intermediates of lactate dehydrogenase. Biochemistry. 30:1991;9195-9200.
5. Barshop B. A., Wrenn R. F., Frieden C. Analysis of numerical methods for computer simulation of kinetic processes: development of KINSIM - a flexible, portable system. Anal. Biochem. 130:1983;134-145.
6. Boisvert D. C., Wang J. M., Otwinowski Z., Horwich A. L., Sigler P. B. The 2.4 angstrom crystal structure of the bacterial chaperonin GroEL complexed with ATP-gamma-S. Nature Struct. Biol. 3:1996;170-177.
7. Bolin J. T., Filman D. J., Matthews D. A., Hamlin R. C., Kraut J. Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 Å resolution. I. General features and binding of methotrexate. J. Biol. Chem. 257:1982;13650-13662.
8. Braig K., Otwinowski Z., Hegde R., Boisvert D. C., Joachimiak A., Horwich A. L., Sigler P. B. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å Nature. 371:1994;578-586.
9. Braig K., Adams P. D., Brunger A. T. Conformational variability in the refined structure of the chaperonin GroEL at 2.8 angstrom resolution. Nature Struct. Biol. 2:1995;1083-1094.
10. Brunschier R., Danner M., Seckler R. Interactions of phage P22 tailspike protein with GroE molecular chaperones during refolding in vitro. J. Biol. Chem. 268:1993;2767-2772.
11. Cayley P. J., Dunn S. M. J., King R. W. Kinetics of substrate, coenzyme, and inhibitor binding to Escherichia coli dihydrofolate reductase. Biochemistry. 20:1981;874-879.
12. Clark A. C., Hugo E., Frieden C. Determination of regions in the dihydrofolate reductase structure that interact with the molecular chaperonin GroEL. Biochemistry. 35:1996;5893-5901.
13. Corrales F. J., Fersht A. R. The folding of GroEL-bound barnase as a model for chaperonin-mediated protein folding. Proc. Natl Acad. Sci. USA. 92:1995;5326-5330.
14. Davies J. D., Delcamp T. J., Prendergast N. J., Ashford V. A., Freisheim J. H., Kraut J. Crystal structures of recombinant human dihydrofolate reductase complexed with folate and 5-deazafolate. Biochemistry. 29:1990;9467-9479.
15. Dunn S. M. J., Batchelor J. G., King R. W. Kinetics of ligand binding to dihydrofolate reductase: binary complex formation with NADPH and coenzyme analogues. Biochemistry. 17:1978;2356-2364.
16. Ellis R. J. Revisiting the Anfinsen cage. Folding Design. 1:1996;R9-R15.
17. Ellis R. J., Hartl F. U. Protein folding in the cell - competing models of chaperonin function. FASEB J. 10:1996;20-26.
18. Fenton W. A., Kashi Y., Furtak K., Horwich A. L. Residues in chaperonin GroEL required for polypeptide binding and release. Nature. 371:1994;614-619.
19. Fisher M. T. Promotion of the in vitro renaturation of dodecameric glutamine synthetase from Escherichia coli in the presence of GroEL (chaperonin-60) and ATP. Biochemistry. 31:1992;3955-3963.
20. Frieden C. Refolding of Escherichia coli dihydrofolate reductase: sequential formation of substrate binding sites. Proc. Natl Acad. Sci. USA. 87:1990;4413-4416.
21. Gervasoni P., Staudenmann W., James P., Gehrig P., Pluckthun A. Beta-lactamase binds to GroEL in a conformation highly protected against hydrogen/deuterium exchange. Proc. Natl Acad. Sci. USA. 93:1996;12189-12194.
22. Gray T. E., Fersht A. R. Refolding of barnase in the presence of GroE. J. Mol. Biol. 232:1993;1197-1207.
23. Groβ M., Robinson C. V., Mayhew M., Hartl F. U., Radford S. E. Significant hydrogen exchange protection in GroEL-bound DHFR is maintained during iterative rounds of substrate cycling. Protein Sci. 5:1996;2506-2513.
24. Hansen J. E., Gafni A. Thermal switching between enhanced and arrested reactivation of bacterial glucose-6-phosphate dehydrogenase assisted by GroEL in the absence of ATP. J. Biol. Chem. 268:1993;21632-21636.
25. Hayer H. M., Ewbank J. J., Creighton T. E., Hartl F. U. Conformational specificity of the chaperonin GroEL for the compact folding intermediates of alpha-lactalbumin. EMBO J. 13:1994;3192-3202.
26. Hendrix R. W. Purification and properties of GroE, a host protein involved in bacteriophage assembly. J. Mol. Biol. 129:1979;375-392.
27. Hlodan R., Tempst P., Hartl F. U. Binding of defined regions of a polypeptide to GroEL and its implications for chaperonin-mediated protein folding. Nature Struct. Biol. 2:1995;587-595.
28. Hoeltzli S. D., Frieden C. 19F NMR spectroscopy of [6-19F]tryptophan-labeled Escherichia coli dihydrofolate reductase: equilibrium folding and ligand binding studies. Biochemistry. 33:1994;5502-5509.
29. Ishii N., Taguchi H., Sumi M., Yoshida M. Structure of holo-chaperonin studied with electron microscopy. FEBS Letters. 299:1992;169-174.
30. Itzhaki L. S., Otzen D. E., Fersht A. R. Nature and consequences of GroEL-protein interactions. Biochemistry. 34:1995;14581-14587.
31. Katsumata K., Okazaki A., Kuwajima K. Effect of GroEL on the re-folding kinetics of alpha-lactalbumin. J. Mol. Biol. 258:1996;827-838.
32. Lilie H., Buchner J. Interaction of GroEL with a highly structured folding intermediate-iterative binding cycles do not involve unfolding. Proc. Natl Acad. Sci. USA. 92:1995;8100-8104.
33. Lin Z. L., Eisenstein E. Nucleotide binding-promoted conformational changes release a nonnative polypeptide from the Escherichia coli chaperonin GroEL. Proc. Natl Acad. Sci. USA. 93:1996;1977-1981.
34. Lorimer G. H. A quantitative assessment of the role of chaperonin proteins in protein folding in vivo. FASEB J. 10:1996;5-9.
35. Mattingly J. R., Iriarte A., Martinez-Carrion M. Homologous proteins with different affinities for GroEL. J. Biol. Chem. 270:1995;1138-1148.
36. Mendoza J. A., Horowitz P. M. Bound substrate polypeptides can generally stabilize the tetradecameric structure of Cpn60 and induce its reassembly from monomers. J. Biol. Chem. 269:1994;25963-25965.
37. Murai N., Taguchi H., Yoshida M. Kinetic analysis of interactions between GroEL and reduced alpha lactalbumin-effect of GroES and nucleotides. J. Biol. Chem. 270:1995;19957-19963.
38. Pace C. N., Shirley B. A., Thomson J. A. Measuring the conformational stability of a protein. Protein Structure and Function, A Practical Approach. 1989;IRL Press, New York.
39. Penner M. H., Frieden C. Kinetic analysis of the mechanism of Escherichia coli dihydrofolate reductase. J. Biol. Chem. 262:1987;15908-15914.
40. Ranson N. A., Dunster N. J., Burston S. G., Clarke A. R. Chaperonins can catalyse the reversal of early aggregation steps when a protein misfolds. J. Mol. Biol. 250:1995;581-586.
41. Rosenberg H. F., Ackerman S. J., Tenen D. G. Characterization of a distinct binding site for the prokaryotic chaperone, GroEL, on a human granulocyte ribonuclease. J. Biol. Chem. 268:1993;4499-4503.
42. Schmidt M., Rutkat K., Rachel R., Pfeifer G., Jaenicke R., Viitanen P., Lorimer G., Buchner J. Symmetric complexes of GroE chaperonins as part of the functional cycle. Science. 265:1994;656-659.
43. Smith K. E., Fisher M. T. Interactions between the GroE chaperonins and rhodanese-multiple intermediates and release and rebinding. J. Biol. Chem. 270:1995;21517-21523.
44. Sparrer H., Lilie H., Buchner J. Dynamics of the GroEL protein complex; effects of nucleotides and folding mutants. J. Mol. Biol. 258:1996;74-87.
45. Staniforth R. A., Burston S. G., Atkinson T., Clarke A. R. Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. Biochem. J. 300:1994a;651-658.
46. Staniforth R. A., Cortes A., Burston S. G., Atkinson T., Holbrook J. J., Clarke A. R. The stability and hydrophobicity of cytosolic and mitochondrial malate dehydrogenases and their relation to chaperonin-assisted folding. FEBS Letters. 344:1994b;129-135.
47. Todd M. J., Viitanen P. V., Lorimer G. H. Dynamics of the chaperonin ATPase cycle: implications for facilitated protein folding. Science. 265:1994;659-666.
48. Viitanen P. V., Donaldson G. K., Lorimer G. H., Lubben T. H., Gatenby A. A. Complex interactions between the chaperonin 60 molecular chaperone and dihydrofolate reductase. Biochemistry. 30:1991;9716-9723.
49. Walter S., Lorimer G. H., Schmid F. X. A thermodynamic coupling mechanism for GroEL-mediated unfolding. Proc. Natl Acad. Sci. USA. 93:1996;9425-9430.
50. Weissman J. S., Kashi Y., Fenton W. A., Horwich A. L. GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative rorms. Cell. 78:1994;693-702.
51. Weissman J. S., Hohl C. M., Kovalenko O., Kashi Y., Chen S. X., Braig K., Saibil H. R., Fenton W. A., Horwich A. L. Mechanism of GroEL action-productive release of polypeptide from a sequestered position under GroES. Cell. 83:1995;577-587.
52. Zahn R., Pluckthun A. GroE prevents the accumulation of early folding intermediates of pre-beta-lactamase without changing the folding pathway. Biochemistry. 31:1992;3249-3255.
53. Zahn R., Spitzfaden C., Ottiger M., Wuthrich K., Pluckthun A. Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature. 368:1994;261-265.
54. Zahn R., Perrett S., Stenberg G., Fersht A. R. Catalysis of amide proton exchange by the molecular chaperones GroEL and SecB. Science. 271:1996;642-645.