Chaperonin GroEL Uses Asymmetric and Symmetric Reaction Cycles in Response to the Concentration of Non-native Substrate Proteins

Overview

Journal Biophys Physicobiol

Specialty Biophysics

Date 2016 Dec 8

PMID 27924258

Citations 4

Authors

Ryo Iizuka

Takashi Funatsu

Affiliations

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Abstract

The chaperonin GroEL is an essential molecular chaperone that mediates protein folding in association with its cofactor, GroES. It is widely accepted that GroEL alternates the GroES-sealed folding-active rings during the reaction cycle. In other words, an asymmetric GroEL-GroES complex is formed during the cycle, whereas a symmetric GroEL-(GroES) complex is not formed. However, this conventional view has been challenged by the recent reports indicating that such symmetric complexes can be formed in the GroEL-GroES reaction cycle. In this review, we discuss the studies of the symmetric GroEL-(GroES) complex, focusing on the molecular mechanism underlying its formation. We also suggest that GroEL can be involved in two types of reaction cycles (asymmetric or symmetric) and the type of cycle used depends on the concentration of non-native substrate proteins.

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References

Fayet O, Ziegelhoffer T, Georgopoulos C . The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol. 1989; 171(3):1379-85. PMC: 209756. DOI: 10.1128/jb.171.3.1379-1385.1989. View

Sameshima T, Iizuka R, Ueno T, Funatsu T . Denatured proteins facilitate the formation of the football-shaped GroEL-(GroES)2 complex. Biochem J. 2010; 427(2):247-54. DOI: 10.1042/BJ20091845. View

Ye X, Lorimer G . Substrate protein switches GroE chaperonins from asymmetric to symmetric cycling by catalyzing nucleotide exchange. Proc Natl Acad Sci U S A. 2013; 110(46):E4289-97. PMC: 3831975. DOI: 10.1073/pnas.1317702110. View

Azem A, Diamant S, Kessel M, Weiss C, Goloubinoff P . The protein-folding activity of chaperonins correlates with the symmetric GroEL14(GroES7)2 heterooligomer. Proc Natl Acad Sci U S A. 1995; 92(26):12021-5. PMC: 40288. DOI: 10.1073/pnas.92.26.12021. View

Behlke J, Ristau O, Schonfeld H . Nucleotide-dependent complex formation between the Escherichia coli chaperonins GroEL and GroES studied under equilibrium conditions. Biochemistry. 1997; 36(17):5149-56. DOI: 10.1021/bi962755h. View

Sameshima T, Iizuka R, Ueno T, Wada J, Aoki M, Shimamoto N . Single-molecule study on the decay process of the football-shaped GroEL-GroES complex using zero-mode waveguides. J Biol Chem. 2010; 285(30):23159-64. PMC: 2906309. DOI: 10.1074/jbc.M110.122101. View

Koike-Takeshita A, Arakawa T, Taguchi H, Shimamura T . Crystal structure of a symmetric football-shaped GroEL:GroES2-ATP14 complex determined at 3.8Å reveals rearrangement between two GroEL rings. J Mol Biol. 2014; 426(21):3634-41. DOI: 10.1016/j.jmb.2014.08.017. View

Hayer-Hartl M, Bracher A, Hartl F . The GroEL-GroES Chaperonin Machine: A Nano-Cage for Protein Folding. Trends Biochem Sci. 2015; 41(1):62-76. DOI: 10.1016/j.tibs.2015.07.009. View

Aharoni A, Horovitz A . Inter-ring communication is disrupted in the GroEL mutant Arg13 --> Gly; Ala126 --> Val with known crystal structure. J Mol Biol. 1996; 258(5):732-5. DOI: 10.1006/jmbi.1996.0282. View

10.

Sakikawa C, Taguchi H, Makino Y, Yoshida M . On the maximum size of proteins to stay and fold in the cavity of GroEL underneath GroES. J Biol Chem. 1999; 274(30):21251-6. DOI: 10.1074/jbc.274.30.21251. View

11.

Taguchi H . Reaction Cycle of Chaperonin GroEL via Symmetric "Football" Intermediate. J Mol Biol. 2015; 427(18):2912-8. DOI: 10.1016/j.jmb.2015.04.007. View

12.

Skjaerven L, Cuellar J, Martinez A, Valpuesta J . Dynamics, flexibility, and allostery in molecular chaperonins. FEBS Lett. 2015; 589(19 Pt A):2522-32. DOI: 10.1016/j.febslet.2015.06.019. View

13.

Schmidt M, Rutkat K, Rachel R, Pfeifer G, Jaenicke R, Viitanen P . Symmetric complexes of GroE chaperonins as part of the functional cycle. Science. 1994; 265(5172):656-9. DOI: 10.1126/science.7913554. View

14.

Ewalt K, Hartl F . On the role of symmetrical and asymmetrical chaperonin complexes in assisted protein folding. Biol Chem. 1999; 380(5):531-40. DOI: 10.1515/BC.1999.068. View

15.

SPARRER H, Rutkat K, Buchner J . Catalysis of protein folding by symmetric chaperone complexes. Proc Natl Acad Sci U S A. 1997; 94(4):1096-100. PMC: 19750. DOI: 10.1073/pnas.94.4.1096. View

16.

Llorca O, Marco S, Carrascosa J, Valpuesta J . Conformational changes in the GroEL oligomer during the functional cycle. J Struct Biol. 1997; 118(1):31-42. DOI: 10.1006/jsbi.1996.3832. View

17.

Houry W, Frishman D, Eckerskorn C, Lottspeich F, Hartl F . Identification of in vivo substrates of the chaperonin GroEL. Nature. 2000; 402(6758):147-54. DOI: 10.1038/45977. View

18.

Taguchi H, Ueno T, Tadakuma H, Yoshida M, Funatsu T . Single-molecule observation of protein-protein interactions in the chaperonin system. Nat Biotechnol. 2001; 19(9):861-5. DOI: 10.1038/nbt0901-861. View

19.

Taguchi H, Tsukuda K, Motojima F, Koike-Takeshita A, Yoshida M . BeF(x) stops the chaperonin cycle of GroEL-GroES and generates a complex with double folding chambers. J Biol Chem. 2004; 279(44):45737-43. DOI: 10.1074/jbc.M406795200. View

20.

Xu Z, Horwich A, SIGLER P . The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex. Nature. 1997; 388(6644):741-50. DOI: 10.1038/41944. View