Abstract
Chaperonin GroEL assists protein folding in the presence of ATP and magnesium. Recent studies have shown that several divalent cations other than magnesium induce conformational changes of GroEL, thereby influencing chaperonin-assisted protein folding, but little is known about the detailed mechanism for such actions. Thus, the effects of divalent cations on protein encapsulation by GroEL/ES complexes were investigated. Of the divalent cations, not only magnesium, but also manganese ions enabled the functional refolding and release of 5,10-methylenetetrahydroforate reductase (METF) by GroEL. Neither ATP hydrolysis nor METF refolding was observed in the presence of zinc ion, whereas only ATP hydrolysis was induced by cobalt and nickel ions. SDS-PAGE and gel filtration analyses revealed that cobalt, nickel and zinc ions permit the formation of stable substrate-GroEL-GroES cis-ternary complexes, but prevent the release of METF from GroEL.
References
Azem A, Diamant S, Goloubinoff P (1994) Effect of divalent cations on the molecular structure of the GroEL oligomer. Biochemistry 33:6671–6675
Badcoe IG, Smith CJ, Wood S, Halsall DJ, Holbrook JJ, Lund P, Clarke AR (1991) Binding of a chaperonin to the folding intermediates of lactate dehydrogenase. Biochemistry 30:9195–9200
Blattner FR, Plunkett G III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1474
Braig K (1998) Chaperonins. Curr Opin Struct Biol 8:159–165
Brazil BT, Ybarra J, Horowitz PM (1998) Divalent cations can induce the exposure of GroEL hydrophobic surfaces and strengthen GroEL hydrophobic binding interactions. Novel effects of Zn2+ GroEL interactions. J Biol Chem 273:3257–3263
Chaudhuri TK, Farr GW, Fenton WA, Rospert S, Horwich AL (2001) GroEL/GroES-mediated folding of a protein too large to be encapsulated. Cell 107:235–246
Diamant S, Azem A, Weiss C, Goloubinoff P (1995) Increased efficiency of GroE-assisted protein folding by manganese ions. J Biol Chem 270:28387–28391
Ellis RJ (1996) The chaperonins. Academic Press, San Diego
Farr GW, Fenton WA, Chaudhuri TK, Clare DK, Saibil HR, Horwich AL (2003) Folding with and without encapsulation by cis- and trans-only GroEL-GroES complexes. Embo J 22:3220–3230
Fisher MT (1992) Promotion of the in vitro renaturation of dodecameric glutamine synthetase from Escherichia coli in the presence of GroEL (chaperonin-60) and ATP. Biochemistry 31:3955–3963
Goloubinoff P, Christeller JT, Gatenby AA, Lorimer GH (1989) Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfoleded state depends on two chaperonin proteins and Mg-ATP. Nature 342:884–889
Hartman DJ, Surin BP, Dixon NE, Hoogenraad NJ, Hoj PB (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
Holl-Neugebauer B, Rudolph R, Schmidt M, Buchner J (1991) Reconstitution of a heat shock effect in vitro: influence of GroE on the thermal aggregation of alpha-glucosidase from yeast. Biochemistry 30:11609–11614
Kerner MJ, Naylor DJ, Ishihama Y, Maier T, Chang HC, Stines AP, Georgopoulos C, Frishman D, Hayer-Hartl M, Mann M, Hartl FU (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122:209–220
Lanzetta PA, Alvarez LJ, Reinach PS, Candia OA (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100:95–97
Makino Y, Amada K, Taguchi H, Yoshida M (1997) Chaperonin-mediated folding of green fluorescent protein. J Biol Chem 272:12468–12474
Martin J, Mayhew M, Langer T, Hartl FU (1993) The reaction cycle of GroEL and GroES in chaperonin-assisted protein folding. Nature 366:228–233
Melkani GC, Zardeneta G, Mendoza JA (2003) The ATPase activity of GroEL is supported at high temperatures by divalent cations that stabilize its structure. Biometals 16:479–484
Mizobata T, Akiyama Y, Ito K, Yumoto N, Kawata Y (1992) Effects of the chaperonin GroE on the refolding of tryptophanase from Escherichia coli. Refolding is enhanced in the presence of ADP. J Biol Chem 267:17773–17779
Motojima F, Yoshida M (2003) Discrimination of ATP, ADP, and AMPPNP by chaperonin GroEL: hexokinase treatment revealed the exclusive role of ATP. J Biol Chem 278:26648–26654
Rye HS, Burston SG, Fenton WA, Beechem JM, Xu Z, Sigler PB, Horwich AL (1997) Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388:792–798
Sheppard CA, Trimmer EE, Matthews RG (1999) Purification and properties of NADH-dependent 5, 10-methylenetetrahydrofolate reductase (MetF) from Escherichia coli. J Bacteriol 181:718–725
Taguchi H, Tsukuda K, Motojima F, Koike-Takeshita A, Yoshida M (2004) BeF(x) stops the chaperonin cycle of GroEL-GroES and generates a complex with double folding chambers. J Biol Chem 279:45737–45743
Todd MJ, Viitanen PV, Lorimer GH (1993) Hydrolysis of adenosine 5′-triphosphate by Escherichia coli GroEL: effects of GroES and potassium ion. Biochemistry 32:8560–8567
Xu Z, Horwich AL, Sigler PB (1997) The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature 388:741–750
Acknowledgements
This study was supported in part by the program for Basic Research Activities for Innovative Biosciences (Bio-oriented Technology Research Advancement Institution: BRAIN) of Japan, and by the “Academic Frontier” Project for Private Universities: matching fund subsidy from MEXT of Japan, 2004–2008.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Okuda, H., Sakuhana, C., Yamamoto, R. et al. Effects of divalent cations on encapsulation and release in the GroEL-assisted folding. Biometals 20, 903–910 (2007). https://doi.org/10.1007/s10534-006-9078-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-006-9078-z