Flexibility of GroES mobile loop is required for efficient chaperonin function

Journal of Molecular Biology

Volumn 422, Issue 2, 2012, Pages 291-299

  Nojima, Tatsuya ^a   Ikegami, Takahisa ^b   Taguchi, Hideki ^c   Yoshida, Masasuke ^a  

^a KYOTO SANGYO UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

chaperonin; disulfide bond; GroEL; GroES; mobile loop

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONIN; CYSTEINE; POLYPEPTIDE;

ARTICLE; BINDING AFFINITY; CROSS LINKING; DISULFIDE BOND; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION;

EID: 84864852123     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.05.026     Document Type: Article

References (38)

1. P.B. Sigler, Z. Xu, H.S. Rye, S.G. Burston, W.A. Fenton, and A.L. Horwich Structure and function in GroEL-mediated protein folding Annu. Rev. Biochem. 67 1998 581 608 (Pubitemid 28411139)
2. D. Thirumalai, and G.H. Lorimer Chaperonin-mediated protein folding Annu. Rev. Biophys. Biomol. Struct. 30 2001 245 269 (Pubitemid 32566164)
3. B. Bukau, and A.L. Horwich The Hsp70 and Hsp60 chaperone machines Cell 92 1998 351 366 (Pubitemid 28093013)
4. A.I. Jewett, and J.E. Shea Reconciling theories of chaperonin accelerated folding with experimental evidence Cell. Mol. Life Sci. 67 2010 255 276
5. O. Fayet, T. Ziegelhoffer, and C. Georgopoulos The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures J. Bacteriol. 171 1989 1379 1385 (Pubitemid 19080775)
6. K. Braig, Z. Otwinowski, R. Hegde, D.C. Boisvert, A. Joachimiak, A.L. Horwich, and P.B. Sigler The crystal structure of the bacterial chaperonin GroEL at 2.8 Å Nature 371 1994 578 586
7. P.V. Viitanen, A.A. Gatenby, and G.H. Lorimer Purified chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins Protein Sci. 1 1992 363 369 (Pubitemid 23007303)
8. A.L. Horwich, K.B. Low, W.A. Fenton, I.N. Hirshfield, and K. Furtak Folding in vivo of bacterial cytoplasmic proteins: role of GroEL Cell 74 1993 909 917 (Pubitemid 23270610)
9. W.A. Fenton, Y. Kashi, K. Furtak, and A.L. Horwich Residues in chaperonin GroEL required for polypeptide binding and release Nature 371 1994 614 619 (Pubitemid 24315744)
10. K.L. Ewalt, J.P. Hendrick, W.A. Houry, and F.U. Hartl In vivo observation of polypeptide flux through the bacterial chaperonin system Cell 90 1997 491 500 (Pubitemid 27347239)
11. W.A. Houry, D. Frishman, C. Eckerskorn, F. Lottspeich, and F.U. Hartl Identification of in vivo substrates of the chaperonin GroEL Nature 402 1999 147 154
12. T. Nojima, and M. Yoshida Probing open conformation of GroEL rings by cross-linking reveals single and double open ring structures of GroEL in ADP and ATP J. Biol. Chem. 284 2009 22834 22839
13. J.F. Hunt, A.J. Weaver, S.J. Landry, L. Gierasch, and J. Deisenhofer The crystal structure of the GroES co-chaperonin at 2.8 Å resolution Nature 379 1996 37 45
14. J.S. Weissman, C.M. Hohl, O. Kovalenko, Y. Kashi, S. Chen, and K. Braig Mechanism of GroEL action: productive release of polypeptide from a sequestered position under GroES Cell 83 1995 577 587
15. M. Mayhew, A.C. da Silva, J. Martin, H. Erdjument-Bromage, P. Tempst, and F.U. Hartl Protein folding in the central cavity of the GroEL-GroES chaperonin complex Nature 379 1996 420 426
16. F. Motojima, and M. Yoshida Polypeptide in the chaperonin cage partly protrudes out and then folds inside or escapes outside EMBO J. 29 2010 4008 4019
17. S.J. Landry, J. Zeilstra-Ryalls, O. Fayet, C. Georgopoulos, and L.M. Gierasch Characterization of a functionally important mobile domain of GroES Nature 364 1993 255 258 (Pubitemid 23257087)
18. F. Shewmaker, K. Maskos, C. Simmerling, and S.J. Landry The disordered mobile loop of GroES folds into a defined beta-hairpin upon binding GroEL J. Biol. Chem. 276 2001 31257 31264 (Pubitemid 37384995)
19. Z. Xu, A.L. Horwich, and P.B. Sigler The crystal structure of the asymmetric GroEL-GroES-(ADP)7 chaperonin complex Nature 388 1997 741 750 (Pubitemid 27375147)
20. L. Chen, and P.B. Sigler The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity Cell 99 1999 757 768 (Pubitemid 30017646)
21. K. Motohashi, and T. Hisabori HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen J. Biol. Chem. 281 2006 35039 35047 (Pubitemid 46036543)
22. J.H. Ploegman, G. Drent, K.H. Kalk, W.G. Hol, R.L. Heinrikson, and P. Keim The covalent and tertiary structure of bovine liver rhodanese Nature 273 1978 124 129 (Pubitemid 8322606)
23. D.M. Miller-Martini, J.M. Chirgwin, and P.M. Horowitz Mutations of noncatalytic sulfhydryl groups influence the stability, folding, and oxidative susceptibility of rhodanese J. Biol. Chem. 269 1994 3423 3428 (Pubitemid 24237660)
24. S. Tanaka, Y. Kawata, G. Otting, N.E. Dixon, K. Matsuzaki, and M. Hoshino Chaperonin-encapsulation of proteins for NMR Biochim. Biophys. Acta 1804 2010 866 871
25. N. Murai, Y. Makino, and M. Yoshida GroEL locked in a closed conformation by an interdomain cross-link can bind ATP and polypeptide but cannot process further reaction steps J. Biol. Chem. 271 1996 28229 28234 (Pubitemid 26374634)
26. Y. Makino, K. Amada, H. Taguchi, and M. Yoshida Chaperonin-mediated folding of green fluorescent protein J. Biol. Chem. 272 1997 12468 12474 (Pubitemid 27203336)
27. H.S. Rye, S.G. Burston, W.A. Fenton, J.M. Beechem, Z. Xu, P.B. Sigler, and A.L. Horwich Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL Nature 388 1997 792 798 (Pubitemid 27375160)
28. J.S. Weissman, Y. Kashi, W.A. Fenton, and A.L. Horwich GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms Cell 78 1994 693 702 (Pubitemid 24268591)
29. N. Elad, G.W. Farr, D.K. Clare, E.V. Orlova, A.L. Horwich, and H.R. Saibil Topologies of a substrate protein bound to the chaperonin GroEL Mol. Cell 26 2007 415 426 (Pubitemid 46687100)
30. F. Motojima, T. Makio, K. Aoki, Y. Makino, K. Kuwajima, and M. Yoshida Hydrophilic residues at the apical domain of GroEL contribute to GroES binding but attenuate polypeptide binding Biochem. Biophys. Res. Commun. 267 2000 842 849 (Pubitemid 30099411)
31. D.M. Miller, G.P. Kurzban, J.A. Mendoza, J.M. Chirgwin, S.C. Hardies, and P.M. Horowitz Recombinant bovine rhodanese: purification and comparison with bovine liver rhodanese Biochim. Biophys. Acta 1121 1992 286 292
32. T. Nojima, S. Murayama, M. Yoshida, and F. Motojima Determination of the number of active GroES subunits in the fused heptamer GroES required for interactions with GroEL J. Biol. Chem. 283 2008 18385 18392
33. Y.H. Watanabe, and M. Yoshida Trigonal DnaK-DnaJ complex versus free DnaK and DnaJ: heat stress converts the former to the latter, and only the latter can do disaggregation in cooperation with ClpB J. Biol. Chem. 279 2004 15723 15727 (Pubitemid 38509256)
34. H. Taguchi, T. Ueno, H. Tadakuma, M. Yoshida, and T. Funatsu Single-molecule observation of protein-protein interactions in the chaperonin system Nat. Biotechnol. 19 2001 861 865 (Pubitemid 32816757)
35. T. Ueno, H. Taguchi, H. Tadakuma, M. Yoshida, and T. Funatsu GroEL mediates protein folding with a two successive timer mechanism Mol. Cell 14 2004 423 434 (Pubitemid 38648796)
36. A. Koike-Takeshita, T. Shimamura, K. Yokoyama, M. Yoshida, and H. Taguchi Leu309 plays a critical role in the encapsulation of substrate protein into the internal cavity of GroEL J. Biol. Chem. 281 2006 962 967
37. T. Yamada, N. Akutsu, K. Miyazaki, K. Kakinuma, M. Yoshida, and T. Oshima Purification, catalytic properties, and thermal stability of threo-Ds-3-isopropylmalate dehydrogenase coded by leuB gene from an extreme thermophile, Thermus thermophilus strain HB8 J. Biochem. 108 1990 449 456 (Pubitemid 20301367)
38. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293