An Expanded Conformation of Single-Ring GroEL-GroES Complex Encapsulates an 86 kDa Substrate

Structure

Volumn 14, Issue 11, 2006, Pages 1711-1722

  Chen, Dong Hua ^a   Song, Jiu Li ^b   Chuang, David T ^b   Chiu, Wah ^a   Ludtke, Steven J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOACID DEHYDROGENASE; CHAPERONIN;

ARTICLE; COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; ENCAPSULATION; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; X RAY ANALYSIS;

ADENOSINE TRIPHOSPHATE; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ESCHERICHIA COLI; GROEL PROTEIN; GROES PROTEIN; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; KETONE OXIDOREDUCTASES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTATION; PROTEIN CONFORMATION; TRYPSIN;

EID: 33846202165     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2006.09.010     Document Type: Article

References (46)

1. Böttcher B., Wynne S.A., and Crowther R.A. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386 (1997) 88-91
2. Braig K., Otwinowski Z., Hegde R., Boisvert D.C., Joachimiak A., Horwich A.L., and Sigler P.B. The crystal structure of the bacterial chaperonin GroEL at 2.8 A. Nature 371 (1994) 578-586
3. Brink J., Ludtke S.J., Kong Y., Wakil S.J., Ma J., and Chiu W. Experimental verification of conformational variation of human fatty acid synthase as predicted by normal mode analysis. Structure 12 (2004) 185-191
4. Brinker A., Pfeifer G., Kerner M.J., Naylor D.J., Hartl F.U., and Hayer-Hartl M. Dual function of protein confinement in chaperonin-assisted protein folding. Cell 107 (2001) 223-233
5. Chaudhuri T.K., Farr G.W., Fenton W.A., Rospert S., and Horwich A.L. GroEL/GroES-mediated folding of a protein too large to be encapsulated. Cell 107 (2001) 235-246
6. Chen S., Roseman A.M., Hunter A.S., Wood S.P., Burston S.G., Ranson N.A., Clarke A.R., and Saibil H.R. Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature 371 (1994) 261-264
7. 2 tetramers of human mitochondrial branched-chain α-ketoacid decarboxylase. Obligatory interaction of chaperonins with an αβ dimeric intermediate. J. Biol. Chem. 274 (1999) 10395-10404
8. Clare D.K., Orlova E.V., Finbow M.A., Harrison M.A., Findlay J.B., and Saibil H.R. An expanded and flexible form of the vacuolar ATPase membrane sector. Structure 14 (2006) 1149-1156
9. Ellis R.J., and van der Vies S.M. Molecular chaperones. Annu. Rev. Biochem. 60 (1991) 321-347
10. Ewalt K.L., Hendrick J.P., Houry W.A., and Hartl F.U. In vivo observation of polypeptide flux through the bacterial chaperonin system. Cell 90 (1997) 491-500
11. Falke S., Fisher M.T., and Gogol E.P. Classification and reconstruction of a heterogeneous set of electron microscopic images: a case study of GroEL-substrate complexes. J. Struct. Biol. 133 (2001) 203-213
12. Falke S., Fisher M.T., and Gogol E.P. Structural changes in GroEL effected by binding a denatured protein substrate. J. Mol. Biol. 308 (2001) 569-577
13. Falke S., Tama F., Brooks III C.L., Gogol E.P., and Fisher M.T. The 13 angstroms structure of a chaperonin GroEL-protein substrate complex by cryo-electron microscopy. J. Mol. Biol. 348 (2005) 219-230
14. Fenton W.A., and Horwich A.L. Chaperonin-mediated protein folding: fate of substrate polypeptide. Q. Rev. Biophys. 36 (2003) 229-256
15. Frank J. Chapter 2. Three Dimensional Electron Microscopy. Second edition (2006), Oxford University Press, New York 145-192
16. Goddard T.D., Huang C.C., and Ferrin T.E. Software extensions to UCSF chimera for interactive visualization of large molecular assemblies. Structure 13 (2005) 473-482
17. Hendrix R.W. Purification and properties of groE, a host protein involved in bacteriophage assembly. J. Mol. Biol. 129 (1979) 375-392
18. Hohn T., Hohn B., Engel A., Wurtz M., and Smith P.R. Isolation and characterization of the host protein groE involved in bacteriophage lambda assembly. J. Mol. Biol. 129 (1979) 359-373
19. Horwich A.L., Burston S.G., Rye H.S., Weissman J.S., and Fenton W.A. Construction of single-ring and two-ring hybrid versions of bacterial chaperonin GroEL. Methods Enzymol. 290 (1998) 141-146
20. Horwich A.L., Farr G.W., and Fenton W.A. GroEL-GroES-mediated protein folding. Chem. Rev. 106 (2006) 1917-1930
21. Houry W.A., Frishman D., Eckerskorn C., Lottspeich F., and Hartl F.U. Identification of in vivo substrates of the chaperonin GroEL. Nature 402 (1999) 147-154
22. Huang Y.S., and Chuang D.T. Mechanisms for GroEL/GroES-mediated folding of a large 86-kDa fusion polypeptide in vitro. J. Biol. Chem. 274 (1999) 10405-10412
23. Jiang W., Baker M.L., Ludtke S.J., and Chiu W. Bridging the information gap: computational tools for intermediate resolution structure interpretation. J. Mol. Biol. 308 (2001) 1033-1044
24. Kong Y., Ming D., Wu Y., Stoops J.K., Zhou Z.H., and Ma J. Conformational flexibility of pyruvate dehydrogenase complexes: a computational analysis by quantized elastic deformational model. J. Mol. Biol. 330 (2003) 129-135
25. Ludtke S.J., Baldwin P.R., and Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128 (1999) 82-97
26. Ludtke S.J., Jakana J., Song J.L., Chuang D.T., and Chiu W. A 11.5 Å single particle reconstruction of GroEL using EMAN. J. Mol. Biol. 314 (2001) 253-262
27. Ludtke S.J., Chen D.H., Song J.L., Chuang D.T., and Chiu W. Seeing GroEL at 6 Å resolution by single particle electron cryomicroscopy. Structure 12 (2004) 1129-1136
28. Martin J., and Hartl F.U. Chaperone-assisted protein folding. Curr. Opin. Struct. Biol. 7 (1997) 41-52
29. Motojima F., Chaudhry C., Fenton W.A., Farr G.W., and Horwich A.L. Substrate polypeptide presents a load on the apical domains of the chaperonin GroEL. Proc. Natl. Acad. Sci. USA 101 (2004) 15005-15012
30. Nielsen K.L., and Cowan N.J. A single ring is sufficient for productive chaperonin-mediated folding in vivo. Mol. Cell 2 (1998) 93-99
31. Nielsen K.L., McLennan N., Masters M., and Cowan N.J. A single-ring mitochondrial chaperonin (Hsp60-Hsp10) can substitute for GroEL-GroES in vivo. J. Bacteriol. 181 (1999) 5871-5875
32. Ranson N.A., Farr G.W., Roseman A.M., Gowen B., Fenton W.A., Horwich A.L., and Saibil H.R. ATP-bound states of GroEL captured by cryo-electron microscopy. Cell 107 (2001) 869-879
33. Roseman A.M., Chen S., White H., Braig K., and Saibil H.R. The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87 (1996) 241-251
34. Rye H.S., Burston S.G., Fenton W.A., Beechem J.M., Xu Z., Sigler P.B., and Horwich A.L. Distinct actions of cis and trans ATP within the double ring of the chaperonin GroEL. Nature 388 (1997) 792-798
35. Rye H.S., Roseman A.M., Chen S., Furtak K., Fenton W.A., Saibil H.R., and Horwich A.L. GroEL-GroES cycling: ATP and nonnative polypeptide direct alternation of folding-active rings. Cell 97 (1999) 325-338
36. Sakikawa C., Taguchi H., Makino Y., and Yoshida M. On the maximum size of proteins to stay and fold in the cavity of GroEL underneath GroES. J. Biol. Chem. 274 (1999) 21251-21256
37. Sigler P.B., Xu Z., Rye H.S., Burston S.G., Fenton W.A., and Horwich A.L. Structure and function in GroEL-mediated protein folding. Annu. Rev. Biochem. 67 (1998) 581-608
38. 2 assembly of mitochondrial branched-chain α-ketoacid dehydrogenase. cis capping of the native-like 86-kDa intermediate by GroES. J. Biol. Chem. 275 (2000) 22305-22312
39. Song J.L., Li J., Huang Y.S., and Chuang D.T. Encapsulation of an 86-kDa assembly intermediate inside the cavities of GroEL and its single-ring variant SR1 by GroES. J. Biol. Chem. 278 (2003) 2515-2521
40. Tang Y.C., Chang H.C., Roeben A., Wischnewski D., Wischnewski N., Kerner M.J., Hartl F.U., and Hayer-Hartl M. Structural features of the GroEL-GroES nano-cage required for rapid folding of encapsulated protein. Cell 125 (2006) 903-914
41. van Heel M. Similarity measures between images. Ultramicroscopy 21 (1987) 95-100
42. Viitanen P.V., Lorimer G.H., Seetharam R., Gupta R.S., Oppenheim J., Thomas J.O., and Cowan N.J. Mammalian mitochondrial chaperonin 60 functions as a single toroidal ring. J. Biol. Chem. 267 (1992) 695-698
43. Weissman J.S., Hohl C.M., Kovalenko O., Kashi Y., Chen S., Braig K., Saibil H.R., Fenton W.A., and Horwich A.L. Mechanism of GroEL action: productive release of polypeptide from a sequestered position under GroES. Cell 83 (1995) 577-587
44. Wynn R.M., Song J.L., and Chuang D.T. GroEL/GroES promote dissociation/reassociation cycles of a heterodimeric intermediate during alpha(2)beta(2) protein assembly. Iterative annealing at the quaternary structure level. J. Biol. Chem. 275 (2000) 2786-2794
45. 7 chaperonin complex. Nature 388 (1997) 741-750
46. Zhou Z.H., Liao W., Cheng R.H., Lawson J.E., McCarthy D.B., Reed L.J., and Stoops J.K. Direct evidence for the size and conformational variability of the pyruvate dehydrogenase complex revealed by three-dimensional electron microscopy. The "breathing" core and its functional relationship to protein dynamics. J. Biol. Chem. 276 (2001) 21704-21713