Crowding activates ClpB and enhances its association with DnaK for efficient protein aggregate reactivation

Biophysical Journal

Volumn 106, Issue 9, 2014, Pages 2017-2027

  Martín, Ianire ^a   Celaya, Garbiñe ^a   Alfonso, Carlos ^b   Moro, Fernando ^a   Rivas, Germán ^b   Muga, Arturo ^a  

^a CSIC UPV Unidad de Biofisica UBF   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 70; PROTEIN AGGREGATE;

CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

ADENOSINE TRIPHOSPHATASES; HSP70 HEAT-SHOCK PROTEINS; KINETICS; MODELS, MOLECULAR; PROTEIN AGGREGATES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY;

EID: 84899894047     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.03.042     Document Type: Article

References (59)

1. Y.E. Kim, and M.S. Hipp F.U. Hartl Molecular chaperone functions in protein folding and proteostasis Annu. Rev. Biochem. 82 2013 323 355
2. G.G. Tartaglia, and C.M. Dobson M. Vendruscolo Physicochemical determinants of chaperone requirements J. Mol. Biol. 400 2010 579 588
3. R.J. Ellis, and A.P. Minton Protein aggregation in crowded environments Biol. Chem. 387 2006 485 497
4. G.B. Ralston Effects of crowding in protein solution J. Chem. Educ. 67 1990 857 860
5. S.B. Zimmerman, and S.O. Trach Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli J. Mol. Biol. 222 1991 599 620
6. A.B. Fulton How crowded is the cytoplasm? Cell 30 1982 345 347
7. A.P. Minton Implications of macromolecular crowding for protein assembly Curr. Opin. Struct. Biol. 10 2000 34 39
8. A.P. Minton The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media J. Biol. Chem. 276 2001 10577 10580
9. B. van den Berg, R.J. Ellis, and C.M. Dobson Effects of macromolecular crowding on protein folding and aggregation EMBO J. 18 1999 6927 6933
10. R.J. Ellis Molecular chaperones: avoiding the crowd Curr. Biol. 7 1997 R531 R533
11. R.J. Ellis, and F.U. Hartl Principles of protein folding in the cellular environment Curr. Opin. Struct. Biol. 9 1999 102 110
12. W.E. Balch, and R.I. Morimoto J.W. Kelly Adapting proteostasis for disease intervention Science 319 2008 916 919
13. M.P. Mayer Hsp70 chaperone dynamics and molecular mechanism Trends Biochem. Sci. 38 2013 507 514
14. W. Kress, Z. Maglica, and E. Weber-Ban Clp chaperone-proteases: structure and function Res. Microbiol. 160 2009 618 628
15. S. Lee, and B. Sielaff F.T. Tsai CryoEM structure of Hsp104 and its mechanistic implication for protein disaggregation Proc. Natl. Acad. Sci. USA 107 2010 8135 8140
16. P. Wendler, and J. Shorter H.R. Saibil Motor mechanism for protein threading through Hsp104 Mol. Cell 34 2009 81 92
17. S.P. Acebrón, and I. Martín A. Muga DnaK-mediated association of ClpB to protein aggregates. A bichaperone network at the aggregate surface FEBS Lett. 583 2009 2991 2996
18. R. Rosenzweig, and S. Moradi L.E. Kay Unraveling the mechanism of protein disaggregation through a ClpB-DnaK interaction Science 339 2013 1080 1083
19. C. Schlieker, and I. Tews A. Mogk Solubilization of aggregated proteins by ClpB/DnaK relies on the continuous extraction of unfolded polypeptides FEBS Lett. 578 2004 351 356
20. J. Martin, and F.U. Hartl The effect of macromolecular crowding on chaperonin-mediated protein folding Proc. Natl. Acad. Sci. USA 94 1997 1107 1112
21. J. Martin Requirement for GroEL/GroES-dependent protein folding under nonpermissive conditions of macromolecular crowding Biochemistry 41 2002 5050 5055
22. R. Kityk, and J. Kopp M.P. Mayer Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones Mol. Cell 48 2012 863 874
23. U. del Castillo, and C. Alfonso A. Muga A quantitative analysis of the effect of nucleotides and the M domain on the association equilibrium of ClpB Biochemistry 50 2011 1991 2003
24. K.M. Woo, and K.I. Kim C.H. Chung The heat-shock protein ClpB in Escherichia coli is a protein-activated ATPase J. Biol. Chem. 267 1992 20429 20434
25. F. Moro, V. Fernández, and A. Muga Interdomain interaction through helices A and B of DnaK peptide binding domain FEBS Lett. 533 2003 119 123
26. M. Zylicz, and T. Yamamoto C. Georgopoulos Purification and properties of the dnaJ replication protein of Escherichia coli J. Biol. Chem. 260 1985 7591 7598
27. B. Reija, and B. Monterroso S. Zorrilla Development of a homogeneous fluorescence anisotropy assay to monitor and measure FtsZ assembly in solution Anal. Biochem. 418 2011 89 96
28. P. Schuck, and M.A. Perugini D. Schubert Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems Biophys. J. 82 2002 1096 1111
29. U. del Castillo, and J.A. Fernández-Higuero A. Muga Nucleotide utilization requirements that render ClpB active as a chaperone FEBS Lett. 584 2010 929 934
30. J.R. Hoskins, S.M. Doyle, and S. Wickner Coupling ATP utilization to protein remodeling by ClpB, a hexameric AAA+ protein Proc. Natl. Acad. Sci. USA 106 2009 22233 22238
31. J. Weibezahn, and C. Schlieker A. Mogk Characterization of a trap mutant of the AAA+ chaperone ClpB J. Biol. Chem. 278 2003 32608 32617
32. S. Diamant, and A.P. Ben-Zvi P. Goloubinoff Size-dependent disaggregation of stable protein aggregates by the DnaK chaperone machinery J. Biol. Chem. 275 2000 21107 21113
33. K. Motohashi, and Y. Watanabe M. Yoshida Heat-inactivated proteins are rescued by the DnaK.J-GrpE set and ClpB chaperones Proc. Natl. Acad. Sci. USA 96 1999 7184 7189
34. S. Zietkiewicz, and M.J. Slusarz S. Rodziewicz-Motowidło Conformational stability of the full-atom hexameric model of the ClpB chaperone from Escherichia coli Biopolymers 93 2010 47 60
35. A.A. Fodeke, and A.P. Minton Quantitative characterization of polymer-polymer, protein-protein, and polymer-protein interaction via tracer sedimentation equilibrium J. Phys. Chem. B 114 2010 10876 10880
36. G. Rivas, and A.P. Minton Non-ideal tracer sedimentation equilibrium: a powerful tool for the characterization of macromolecular interactions in crowded solutions J. Mol. Recognit. 17 2004 362 367
37. I. Pozdnyakova, and P. Wittung-Stafsheda Non-linear effects of macromolecular crowding on enzymatic activity of multi copper oxidase Biochim. Biophys. Acta 1804 2010 1740 1744
38. J.R. Wenner, and V.A. Bloomfield Crowding effects on EcoRV kinetics and binding Biophys. J. 77 1999 3234 3241
39. R.C. Wheast CRC Handbook of Chemistry and Physics 63rd ed. 1982 CRC Press Boca Raton, FL
40. A. Dhar, and A. Samiotakis M.S. Cheung Structure, function, and folding of phosphoglycerate kinase are strongly perturbed by macromolecular crowding Proc. Natl. Acad. Sci. USA 107 2010 17586 17591
41. I. Martin, and J. Underhaug A. Muga Screening and evaluation of small organic molecules as ClpB inhibitors and potential antimicrobials J. Med. Chem. 56 2013 7177 7189
42. A. Christiansen, and P. Wittung-Stafshede Quantification of excluded volume effects on the folding landscape of Pseudomonas aeruginosa apoazurin in vitro Biophys. J. 105 2013 1689 1699
43. X. Aguilar, and C. F Weise P. Wittung-Stafshede Macromolecular crowding extended to a heptameric system: the Co-chaperonin protein 10 Biochemistry 50 2011 3034 3044
44. N.D. Werbeck, S. Schlee, and J. Reinstein Coupling and dynamics of subunits in the hexameric AAA+ chaperone ClpB J. Mol. Biol. 378 2008 178 190
45. A.B. Biter, and S. Lee F.T. Tsai Structural basis for intersubunit signaling in a protein disaggregating machine Proc. Natl. Acad. Sci. USA 109 2012 12515 12520
46. M. Sarkar, A.E. Smith, and G.J. Pielak Impact of reconstituted cytosol on protein stability Proc. Natl. Acad. Sci. USA 110 2013 19342 19347
47. A.P. Minton Quantitative assessment of the relative contributions of steric repulsion and chemical interactions to macromolecular crowding Biopolymers 99 2013 239 244
48. P. Wendler, and J. Shorter H.R. Saibil Atypical AAA+ subunit packing creates an expanded cavity for disaggregation by the protein-remodeling factor Hsp104 Cell 131 2007 1366 1377
49. S.G. Taneva, and F. Moro A. Muga Energetics of nucleotide-induced DnaK conformational states Biochemistry 49 2010 1338 1345
50. H.X. Zhou, G. Rivas, and A.P. Minton Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences Annu. Rev. Biophys 37 2008 375 397
51. J. Weibezahn, and P. Tessarz B. Bukau Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB Cell 119 2004 653 665
52. B. Monterroso, and A.P. Minton Effect of high concentration of inert cosolutes on the refolding of an enzyme: carbonic anhydrase B in sucrose and ficoll 70 J. Biol. Chem. 282 2007 33452 33458
53. R. Bocanegra, C. Alfonso, A. Rodriguez-Huete, M.A. Fuertes, M. Jimenez, G. Rivas, and M.G. Mateu Association equilibrium of the HIV-1 capsid protein in a crowded medium reveals that hexamerization during capsid assembly requires a functional C-domain dimerization interface Biophys. J. 104 2013 884 893
54. J.L. Cole Analysis of heterogeneous interactions Methods Enzymol. 384 2004 212 232
55. S. Zorrilla, and M. Jiménez A.P. Minton General analysis of sedimentation equilibrium in highly nonideal solutions of associating solutes: application to ribonuclease Biophys. Chem. 108 2004 89 100
56. G. Rivas, and A.P. Minton Beyond the second virial coefficient: sedimentation equilibrium in highly non-ideal solutions Methods 54 2011 167 174
57. H.A. Saroff Evaluation of uncertainties for parameters in binding studies: the sum-of-squares profile and Monte Carlo estimation Anal. Biochem. 176 1989 161 169
58. G. Rivas, J.A. Fernández, and A.P. Minton Direct observation of the self-association of dilute proteins in the presence of inert macromolecules at high concentration via tracer sedimentation equilibrium: theory, experiment, and biological significance Biochemistry 38 1999 9379 9388
59. A.P. Minton T.H. Schuster, T.H. Lave, Modern Analytical Ultracentrifugation 1994 Birkhauser Boston, MA 81 93