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Our understanding of molecular chaperone function in membrane protein biogenesis lags far behind that in soluble protein biogenesis. Through a combined approach including isothermal titration calorimetry, UV–Vis spectroscopy, and fluorescence spectroscopy, the behavior of ATP-dependent chaperonin GroEL–GroES, a paradigmatic chaperone of soluble protein folding, was investigated in the refolding of membrane protein bacteriorhodopsin (BR) and its membrane insertion. We found that BR bound asymmetrically to the double-ring GroEL, with a much higher affinity when it was partially denatured. GroEL alone showed a clear influence on BR refolding, but the presence of ATP was necessary to significantly enhance both the rate and yield of the GroEL-mediated folding, in contrast to the adverse effect of GroES on the folding yield. However, synergy between ATP and GroES was shown to be required not only for releasing high-affinity BR species from GroEL, but also for unfolding and rescuing the misfolded conformers complexed to GroEL. This is consistent with the observation that maximum rate enhancement of BR refolding or assembly with the prepared inverted membrane vesicles was achieved when the complete chaperonin system was used. Our results support the iterative unfolding mechanism of GroEL activity previously proposed for soluble proteins, whereby GroEL might perform repeated unfolding and release of BR, thus offering additional opportunities for timely folding or membrane integration. This work provides important information on the convergence of folding of membrane and soluble proteins in light of folding pathways and the role of molecular chaperones.
Almen MS, Nordstrom KJV, Fredriksson R, Schioth HB, (2009) Mapping the human membrane proteome: a majority of the human membrane proteins can be classified according to function and evolutionary origin.BMC Biol 7:50
Behlke J, Ristau O, Schönfeld HJ, (1997) Nucleotide-dependent complex formation between the Escherichia coli chaperonins GroEL and GroES studied under equilibrium conditions.Biochemistry 36:5149-5156
Bochkareva E, Seluanov A, Bibi E, Girshovich A, (1996) Chaperonin-promoted post-translational membrane insertion of a multispanning membrane protein lactose permease.J Biol Chem 271:22256-22261
Bochkareva ES, Solovieva ME, Girshovich AS, (1998) Targeting of GroEL to SecA on the cytoplasmic membrane of Escherichia coli.Proc Natl Acad Sci USA 95:478-483
Booth PJ, (1997) Folding alpha-helical membrane proteins: kinetic studies on bacteriorhodopsin.Fold Des 2:R85-R92
Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler PB, (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 Å.Nature 371:578-586
Calloni G, Chen T, Schermann SM, Chang HC, Genevaux P, Agostini F, Tartaglia GG, Hayer-Hartl M, Hartl FU, (2012) DnaK functions as a central hub in the E. coli chaperone network.Cell Rep 1:251-264
Castanie-Cornet MP, Bruel N, Genevaux P, (2014) Chaperone networking facilitates protein targeting to the bacterial cytoplasmic membrane.BBA-Mol Cell Res 1843:1442-1456
Chen L, Sigler PB, (1999) The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity.Cell 99:757-768
Chi HX, Wang XQ, Li JQ, Ren H, Huang F, (2015) Folding of newly translated membrane protein CCR1 is assisted by the chaperonin GroEL-GroES.Sci Rep 5:17037
Chi HX, Wang XQ, Li JQ, Ren H, Huang F, (2016) Chaperonin-enhanced Escherichia coli cell-free expression of functional CXCR11.J Biotechnol 231:193-200
Coyle JE, Jaeger J, Gross M, Robinson CV, Radford SE, (1997) Structural and mechanistic consequences of polypeptide binding by GroEL.Fold Des 2:R93-104
Dahmane T, Rappaport F, Popot JL, (2013) Amphipol-assisted folding of bacteriorhodopsin in the presence or absence of lipids: functional consequences.Eur Biophys J Biophy 42:85-101
Endow JK, Singhal R, Fernandez DE, Inoue K, (2015) Chaperone-assisted post-translational transport of plastidic type I signal peptidase 1.J Biol Chem 290:28778-28791
Farr GW, Furtak K, Rowland MB, Ranson NA, Saibil HR, Kirchhausen T, Horwich AL, (2000) Multivalent binding of nonnative substrate proteins by the chaperonin GroEL.Cell 100:561-573
Fujiwara K, Ishihama Y, Nakahigashi K, Soga T, Taguchi H, (2010) A systematic survey of in vivo obligate chaperonin-dependent substrates.EMBO J 29:1552-1564
Genier S, Degrandmaison J, Moreau P, Labrecque P, Hebert TE, Parent JL, (2016) Regulation of GPCR expression through an interaction with CCT7, a subunit of the CCT/TRiC complex.Mol Biol Cell 27:3800-3812
Gray TE, Fersht AR, (1993) Refolding of barnase in the presence of GroE.J Mol Biol 232:1197-1207
Gruber R, Horovitz A, (2016) Allosteric mechanisms in chaperonin machines.Chem Rev 116:6588-6606
Hartl FU, Bracher A, Hayer-Hartl M, (2011) Molecular chaperones in protein folding and proteostasis.Nature 475:324-332
Hayer-Hartl M, Bracher A, Hartl FU, (2016) The GroEL-GroES chaperonin machine: a nano-cage for protein folding.Trends Biochem Sci 41:62-76
Horwich AL, Farr GW, Fenton WA, (2006) GroEL-GroES-mediated protein folding.Chem Rev 106:1917-1930
Itzhaki LS, Otzen DE, Fersht AR, (1995) Nature and consequences of GroEL-protein interactions.Biochemistry 34:14581-14587
Jewett AI, Shea JE, (2010) Reconciling theories of chaperonin accelerated folding with experimental evidence.Cell Mol Life Sci 67:255-276
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
Kim SY, Semyonov AN, Twieg RJ, Horwich AL, Frydman J, Moerner WE, (2005) Probing the sequence of conformationally induced polarity changes in the molecular chaperonin GroEL with fluorescence spectroscopy.J Phys Chem B 109:24517-24525
Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU, (2013) Molecular chaperone functions in protein folding and proteostasis.Annu Rev Biochem 82:323-355
Kriegenburg F, Ellgaard L, Hartmann-Petersen R, (2012) Molecular chaperones in targeting misfolded proteins for ubiquitin-dependent degradation.FEBS J 279:532-542
Krishnamani V, Hegde BG, Langen R, Lanyi JK, (2012) Secondary and tertiary structure of bacteriorhodopsin in the SDS denatured state.Biochemistry 51:1051-1060
Libich DS, Tugarinov V, Clore GM, (2015) Intrinsic unfoldase/foldase activity of the chaperonin GroEL directly demonstrated using multinuclear relaxation-based NMR.Proc Natl Acad Sci USA 112:8817-8823
Lin Z, Rye HS, (2006) GroEL-mediated protein folding: making the impossible, possible.Crit Rev Biochem Mol 41:211-239
Lin Z, Madan D, Rye HS, (2008) GroEL stimulates protein folding through forced unfolding.Nat Struct Mol Biol 15:303-311
Molugu SK, Li JH, Bernal RA, (2015) Separation of E. coli chaperonin groEL from beta-galactosidase without denaturation.J Chromatogr B 1007:93-99
Moparthi SB, Sjölander D, Villebeck L, Jonsson BH, Hammarström P, Carlsson U, (2013) Transient conformational remodeling of folding proteins by GroES-individually and in concert with GroEL.J Chem Biol 7:1-15
Morein S, Henricson D, Rilfors L, (1994) Separation of inner and outer membrane vesicles from Escherichia coli in self-generating Percoll gradients.Anal Biochem 216:47-51
Motojima F, Yoshida M, (2010) Polypeptide in the chaperonin cage partly protrudes out and then folds inside or escapes outside.EMBO J 29:4008-4019
Motojima F, Makio T, Aoki K, Makino Y, Kuwajima K, Yoshida M, (2000) Hydrophilic residues at the apical domain of GroEL contribute to GroES binding but attenuate polypeptide binding.Biochem Biophys Res Commun 267:842-849
Priya S, Sharma SK, Sood V, Mattoo RUH, Finka A, Azem A, De Los Rios P, Goloubinoff P, (2013) GroEL and CCT are catalytic unfoldases mediating out-of-cage polypeptide refolding without ATP.Proc Natl Acad Sci USA 110:7199-7204
Rapoport TA, Goder V, Heinrich SU, Matlack KES, (2004) Membrane-protein integration and the role of the translocation channel.Trends Cell Biol 14:568-575
Saibil H, (2013) Chaperone machines for protein folding, unfolding and disaggregation.Nat Rev Mol Cell Bio 14:630-642
Schnell DJ, Hebert DN, (2003) Protein translocons: multifunctional mediators of protein translocation across membranes.Cell 112:491-505
Sharma S, Chakraborty K, Mueller BK, Astola N, Tang YC, Lamb DC, Hayer-Hartl M, Hartl FU, (2008) Monitoring protein conformation along the pathway of chaperonin-assisted folding.Cell 133:142-153
Sharpe HJ, Stevens TJ, Munro S, (2010) A Comprehensive comparison of transmembrane domains reveals organelle-specific properties.Cell 142:158-169
Skjaerven L, Cuellar J, Martinez A, Valpuesta JM, (2015) Dynamics, flexibility, and allostery in molecular chaperonins.FEBS Lett 589:2522-2532
Stevens TJ, Mizuguchi K, Arkin IT, (2004) Distinct protein interfaces in transmembrane domains suggest an in vivo folding model.Protein Sci 13:3028-3037
Sun JC, Savva CG, Deaton J, Kaback HR, Svrakic M, Young R, Holzenburg A, (2005) Asymmetric binding of membrane proteins to GroEL.Arch Biochem Biophys 434:352-357
Thirumalai D, Lorimer GH, (2001) Chaperonin-mediated protein folding.Annu Rev Bioph Biom 30:245-269
Weissman JS, Hohl CM, Kovalenko O, Kashi Y, Chen S, Braig K, Saibil HR, Fenton WA, Horwich AL, (1995) Mechanism of GroEL action: productive release of polypeptide from a sequestered position under GroES.Cell 83:577-587
White SH, von Heijne G, (2004) The machinery of membrane protein assembly.Curr Opin Struct Biol 14:397-404
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