Fibrillogenic propensity of the GroEL apical domain: A Janus-faced minichaperone

FEBS Letters

Volumn 586, Issue 8, 2012, Pages 1120-1127

  Chen, Jin ^a   Yagi, Hisashi ^b   Sormanni, Pietro ^c   Vendruscolo, Michele ^c   Makabe, Koki ^a,d   Nakamura, Takashi ^a,d   Goto, Yuji ^b   Kuwajima, Kunihiro ^a,d  

^a OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

2 Microglobulin; Amyloid; Fibril; GroEL apical domain; Molecular chaperone

Indexed keywords

AMYLOID; BETA 2 MICROGLOBULIN; CHAPERONE; CHAPERONIN; PROTEIN GROEL; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ELECTRON MICROSCOPY; FIBER; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE;

AMYLOID; BETA 2-MICROGLOBULIN; BINDING SITES; CHAPERONIN 60; CIRCULAR DICHROISM; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 84859909161     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.03.019     Document Type: Article

References (45)

1. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366 (Pubitemid 44118036)
2. T.A. Pertinhez, M.L. Bouchard, E.J. Tomlinson, R. Wain, S.J. Ferguson, C.M. Dobson, and L.J. Smith Amyloid fibril formation by a helical cytochrome FEBS Lett. 495 2001 184 186 (Pubitemid 32397701)
3. M. Fandrich, M.A. Fletcher, and C.M. Dobson Amyloid fibrils from muscle myoglobin-even an ordinary globular protein can assume a rogue guise if conditions are right Nature 410 2001 165 166 (Pubitemid 32216577)
4. G.G. Tartaglia, S. Pechmann, C.M. Dobson, and M. Vendruscolo Life on the edge: a link between gene expression levels and aggregation rates of human proteins Trends Biochem. Sci. 32 2007 204 206 (Pubitemid 46694330)
5. L. Goldschmidt, P.K. Teng, R. Riek, and D. Eisenberg Identifying the amylome, proteins capable of forming amyloid-like fibrils Proc. Natl. Acad. Sci. U S A 107 2010 3487 3492
6. S. Meehan Characterisation of amyloid fibril formation by small heat-shock chaperone proteins human alpha A-, alpha beta- and R120G alpha B-Crystallins J. Mol. Biol. 372 2007 470 484 (Pubitemid 47277407)
7. K. Usui, N. Ishii, Y. Kawarabayasi, and M. Yohda Expression and biochemical characterization of two small heat shock proteins from the thermoacidophilic crenarchaeon Sulfolobus tokodaii strain 7 Protein Sci. 13 2004 134 144 (Pubitemid 38021148)
8. X.D. Shi Small heat shock protein AgsA forms dynamic fibrils FEBS Lett. 585 2011 3396 3402
9. D.C. Thorn Amyloid fibril formation by bovine milk kappa-casein and its inhibition by the molecular chaperones alpha(s-) and beta-casein Biochemistry 44 2005 17027 17036 (Pubitemid 43007231)
10. S. Meehan, Y. Berry, B. Luisi, C.M. Dobson, J.A. Carver, and C.E. MacPhee Amyloid fibril formation by lens crystallin proteins and its implications for cataract formation J. Biol. Chem. 279 2004 3413 3419 (Pubitemid 38140578)
11. M.S. Kosinski-Collins, and J. King In vitro unfolding, refolding, and polymerization of human gamma D crystallin, a protein involved in cataract formation Protein Sci. 12 2003 480 490 (Pubitemid 36241106)
12. A.L. Horwich, G.W. Farr, and W.A. Fenton GroEL-GroES-mediated protein folding Chem. Rev. 106 2006 1917 1930 (Pubitemid 43792786)
13. S. Walter, and J. Buchner Molecular chaperones-cellular machines for protein folding Angew. Chem. Int. Ed. 41 2002 1098 1113
14. Z. Lin, and H.S. Rye GroEL-mediated protein folding: making the impossible, possible Crit. Rev. Biochem. Mol. Biol. 41 2006 211 239 (Pubitemid 44100582)
15. J.P. Grason, J.S. Gresham, and G.H. Lorimer Setting the chaperonin timer: a two-stroke, two-speed, protein machine Proc. Natl. Acad. Sci. U S A 105 2008 17339 17344
16. M. Illingworth, A. Ramsey, Z.D. Zheng, and L.L. Chen Stimulating the substrate folding activity of a single ring GroEL variant by modulating the cochaperonin GroES J. Biol. Chem. 286 2011 30401 30408
17. A. Horovitz, and K.R. Willison Allosteric regulation of chaperonins Curr. Opin. Struct. Biol. 15 2005 646 651 (Pubitemid 41668520)
18. T. Higurashi, H. Yagi, T. Mizobata, and Y. Kawata Amyloid-like fibril formation of co-chaperonin GroES: Nucleation and extension prefer different degrees of molecular compactness J. Mol. Biol. 351 2005 1057 1069 (Pubitemid 41133452)
19. H. Iwasa, S. Meshitsuka, K. Hongo, T. Mizobata, and Y. Kawata Covalent structural changes in unfolded GroES that lead to amyloid fibril formation detected by NMR: Insight into intrinsically disordered proteins J. Biol. Chem. 286 2011 21796 21805
20. 2-microglobulin amyloid fibril by H/D exchange Nat. Struct. Biol. 9 2002 332 336 (Pubitemid 34462549)
21. R. Zahn, A.M. Buckle, S. Perrett, C.M. Johnson, F.J. Corrales, R. Golbik, and A.R. Fersht Chaperone activity and structure of monomeric polypeptide binding domains of GroEL Proc. Natl. Acad. Sci. U S A 93 1996 15024 15029 (Pubitemid 27009545)
22. 2- binding to the chaperonin GroEL J. Mol. Biol. 410 2011 343 356
23. A. Laganowsky Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function Protein Sci. 19 2010 1031 1043
24. W.F. Xue, S.W. Homans, and S.E. Radford Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly Proc. Natl. Acad. Sci. U S A 105 2008 8926 8931
25. V. Sluzky, J.A. Tamada, A.M. Klibanov, and R. Langer Kinetics of insulin aggregation in aqueous-solutions upon agitation in the presence of hydrophobic surfaces Proc. Natl. Acad. Sci. U S A 88 1991 9377 9381 (Pubitemid 21915634)
26. H. Naiki, K. Higuchi, M. Hosokawa, and T. Takeda Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavine T Anal. Biochem. 177 1989 244 249 (Pubitemid 19088253)
27. A. Trovato, F. Chiti, A. Maritan, and F. Seno Insight into the structure of amyloid fibrils from the analysis of globular proteins PLoS Comput. Biol. 2 2006 1608 1618 (Pubitemid 46045173)
28. G.G. Tartaglia, A.P. Pawar, S. Campioni, C.M. Dobson, F. Chiti, and M. Vendruscolo Prediction of aggregation-prone regions in structured proteins J. Mol. Biol. 380 2008 425 436
29. R. Linding, J. Schymkowitz, F. Rousseau, F. Diella, and L. Serrano A comparative study of the relationship between protein structure and β-aggregation in globular and intrinsically disordered proteins J. Mol. Biol. 342 2004 345 353 (Pubitemid 39094525)
30. A.M. Fernandez-Escamilla, F. Rousseau, J. Schymkowitz, and L. Serrano Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins Nat. Biotech. 22 2004 1302 1306 (Pubitemid 39336784)
31. 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)
32. A.E. Ashcroft Structural plasticity and noncovalent substrate binding in the GroEL apical Domain J. Biol. Chem. 277 2002 33115 33126
33. R. Golbik, R. Zahn, S.E. Harding, and A.R. Fersht Thermodynamic stability and folding of GroEL minichaperones J. Mol. Biol. 276 1998 505 515 (Pubitemid 28085336)
34. A.L. Smoot, M. Panda, B.T. Brazil, A.M. Buckle, A.R. Fersht, and P.M. Horowitz The binding of bis-ANS to the isolated GroEL apical domain fragment induces the formation of a folding intermediate with increased hydrophobic surface not observed in tetradecameric GroEL Biochemistry 40 2001 4484 4492 (Pubitemid 32319594)
35. J. Pettersson-Kastberg Alpha-Lactalbumin, engineered to be nonnative and inactive, kills tumor cells when in complex with oleic acid: a new biological function resulting from partial unfolding J. Mol. Biol. 394 2009 994 1010
36. N. Tanaka, and A.R. Fersht Identification of substrate binding site of GroEL minichaperone in solution J. Mol. Biol. 292 1999 173 180 (Pubitemid 29425662)
37. J. Chatellier, F. Hill, P.A. Lund, and A.R. Fersht In vivo activities of GroEL minichaperones Proc. Natl. Acad. Sci. U S A 95 1998 9861 9866 (Pubitemid 28415260)
38. J. Chen, M.J. Feige, T.M. Franzmann, A. Bepperling, and J. Buchner Regions outside the α-crystallin domain of the small heat shock protein Hsp26 are required for its dimerization J. Mol. Biol. 398 2010 122 131
39. +] prion in yeast and aggregation of Sup35 in vitro Proc. Natl. Acad. Sci. U S A 101 2004 12934 12939 (Pubitemid 39167561)
40. S. Pechmann, E.D. Levy, G.G. Tartaglia, and M. Vendruscolo Physicochemical principles that regulate the competition between functional and dysfunctional association of proteins Proc. Natl. Acad. Sci. U S A 106 2009 10159 10164
41. C. Dekker, K.R. Willison, and W.R. Taylor On the evolutionary origin of the chaperonins Proteins 79 2010 1172 1192
42. H. Olzscha Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions Cell 144 2011 67 78
43. J.D. Trent, H.K. Kagawa, T. Yaoi, E. Olle, and N.J. Zaluzec Chaperonin filaments: the archaeal cytoskeleton? Proc. Natl. Acad. Sci. U S A 94 1997 5383 5388 (Pubitemid 27214792)
44. S.L. Shammas Binding of the molecular chaperone alphaB-crystallin to a beta amyloid fibrils inhibits fibril elongation Biophys. J. 101 2011 1681 1689
45. T.P.J. Knowles, W.M. Shu, G.L. Devlin, S. Meehan, S. Auer, C.M. Dobson, and M.E. Welland Kinetics and thermodynamics of amyloid formation from direct measurements of fluctuations in fibril mass Proc. Natl. Acad. Sci. U S A 104 2007 10016 10021 (Pubitemid 47175255)