Mapping the conformation of a client protein through the Hsp70 functional cycle

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 33, 2015, Pages 10395-10400

  Sekhar, Ashok ^a   Rosenzweig, Rina ^a   Bouvignies, Guillaume ^b   Kay, Lewis E ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIV GRENOBLE ALPES   (France)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

CEST; Hsp70; Molecular chaperones; NMR; Protein folding

Indexed keywords

HEAT SHOCK PROTEIN 70; TELOMERIC REPEAT BINDING FACTOR 1; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CHAPERONE; DNAK PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN;

ARTICLE; BINDING SITE; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING; STRUCTURE ANALYSIS; CHEMISTRY; DIFFUSION; ENZYME SPECIFICITY; HUMAN; HYDROLYSIS; KINETICS; METABOLISM; PROTEIN FOLDING;

ESCHERICHIA COLI;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BINDING SITES; DIFFUSION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CHAPERONES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SUBSTRATE SPECIFICITY; TELOMERIC REPEAT BINDING PROTEIN 1;

EID: 84939838737     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1508504112     Document Type: Article

References (46)

1. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475(7356):324-332.
2. Mayer MP, Bukau B (2005) Hsp70 chaperones: Cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670-684.
3. Rüdiger S, Germeroth L, Schneider-Mergener J, Bukau B (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J 16(7):1501-1507.
4. Kityk R, Kopp J, Sinning I, Mayer MP (2012) Structure and dynamics of the ATP-bound open conformation of Hsp70 chaperones. Mol Cell 48(6):863-874.
5. Qi R, et al. (2013) Allosteric opening of the polypeptide-binding site when an Hsp70 binds ATP. Nat Struct Mol Biol 20(7):900-907.
6. Bertelsen EB, Chang L, Gestwicki JE, Zuiderweg ER (2009) Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc Natl Acad Sci USA 106(21):8471-8476.
7. Mayer MP (2013) Hsp70 chaperone dynamics and molecular mechanism. Trends Biochem Sci 38(10):507-514.
8. Clerico EM, Tilitsky JM, Meng W, Gierasch LM (2015) How Hsp70 molecular machines interact with their substrates to mediate diverse physiological functions. J Mol Biol 427(7):1575-1588.
9. Zhu X, et al. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272(5268):1606-1614.
10. Stevens SY, Cai S, Pellecchia M, Zuiderweg ER (2003) The solution structure of the bacterial HSP70 chaperone protein domain DnaK(393-507) in complex with the peptide NRLLLTG. Protein Sci 12(11):2588-2596.
11. Chen Z, Kurt N, Rajagopalan S, Cavagnero S (2006) Secondary structure mapping of DnaK-bound protein fragments: Chain helicity and local helix unwinding at the binding site. Biochemistry 45(40):12325-12333.
12. Kurt N, Cavagnero S (2008) Nonnative helical motif in a chaperone-bound protein fragment. Biophys J 94(7):L48-L50.
13. Palleros DR, Shi L, Reid KL, Fink AL (1994) hsp70-protein complexes. Complex stability and conformation of bound substrate protein. J Biol Chem 269(18):13107-13114.
14. Sekhar A, Santiago M, Lam HN, Lee JH, Cavagnero S (2012) Transient interactions of a slow-folding protein with the Hsp70 chaperone machinery. Protein Sci 21(7):1042-1055.
15. Kellner R, et al. (2014) Single-molecule spectroscopy reveals chaperone-mediated expansion of substrate protein. Proc Natl Acad Sci USA 111(37):13355-13360.
16. Nishikawa T, Nagadoi A, Yoshimura S, Aimoto S, Nishimura Y (1998) Solution structure of the DNA-binding domain of human telomeric protein, hTRF1. Structure 6(8):1057-1065.
17. Gianni S, et al. (2003) Unifying features in protein-folding mechanisms. Proc Natl Acad Sci USA 100(23):13286-13291.
18. Zhuravleva A, Clerico EM, Gierasch LM (2012) An interdomain energetic tug-of-war creates the allosterically active state in Hsp70 molecular chaperones. Cell 151(6):1296-1307.
19. Pervushin K, Riek R, Wider G, Wüthrich K (1997) Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci USA 94(23):12366-12371.
20. Tamiola K, Mulder FA (2012) Using NMR chemical shifts to calculate the propensity for structural order and disorder in proteins. Biochem Soc Trans 40(5):1014-1020.
21. Marsh JA, Singh VK, Jia Z, Forman-Kay JD (2006) Sensitivity of secondary structure propensities to sequence differences between α- and γ-synuclein: Implications for fibrillation. Protein Sci 15(12):2795-2804.
22. Fawzi NL, Ying J, Ghirlando R, Torchia DA, Clore GM (2011) Atomic-resolution dynamics on the surface of amyloid-β protofibrils probed by solution NMR. Nature 480(7376):268-272.
23. Vallurupalli P, Bouvignies G, Kay LE (2012) Studying "invisible" excited protein states in slow exchange with a major state conformation. J Am Chem Soc 134(19):8148-8161.
24. Goloubinoff P, De Los Rios P (2007) The mechanism of Hsp70 chaperones: (Entropic) pulling the models together. Trends Biochem Sci 32(8):372-380.
25. McCarty JS, Walker GC (1991) DnaK as a thermometer: Threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc Natl Acad Sci USA 88(21):9513-9517.
26. Wishart DS (2011) Interpreting protein chemical shift data. Prog Nucl Magn Reson Spectrosc 58(1-2):62-87.
27. Spera S, Bax A (1991) Empirical correlation between protein backbone conformation and C. alpha. and C. beta. 13C nuclear magnetic resonance chemical shifts. J Am Chem Soc 113(14):5490-5492.
28. Saio T, Guan X, Rossi P, Economou A, Kalodimos CG (2014) Structural basis for protein antiaggregation activity of the trigger factor chaperone. Science 344(6184):1250494.
29. Sigler PB, et al. (1998) Structure and function in GroEL-mediated protein folding. Annu Rev Biochem 67(1):581-608.
30. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N (2009) Importing mitochondrial proteins: Machineries and mechanisms. Cell 138(4):628-644.
31. Agashe VR, et al. (2004) Function of trigger factor and DnaK in multidomain protein folding: Increase in yield at the expense of folding speed. Cell 117(2):199-209.
32. Weibezahn J, et al. (2004) Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119(5):653-665.
33. Kirschke E, Goswami D, Southworth D, Griffin PR, Agard DA (2014) Glucocorticoid receptor function regulated by coordinated action of the Hsp90 and Hsp70 chaperone cycles. Cell 157(7):1685-1697.
34. Sharma SK, De los Rios P, Christen P, Lustig A, Goloubinoff P (2010) The kinetic parameters and energy cost of the Hsp70 chaperone as a polypeptide unfoldase. Nat Chem Biol 6(12):914-920.
35. Montgomery DL, Morimoto RI, Gierasch LM (1999) Mutations in the substrate binding domain of the Escherichia coli 70 kDa molecular chaperone, DnaK, which alter substrate affinity or interdomain coupling. J Mol Biol 286(3):915-932.
36. Tugarinov V, Kanelis V, Kay LE (2006) Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy. Nat Protoc 1(2):749-754.
37. Delaglio F, et al. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6(3):277-293.
38. Goddard T, Kneller D (2006) Sparky - NMR assignment and integration software (Univ of California, San Francisco).
39. 13C(β) CEST experiments for studies of ms timescale dynamics in proteins. J Biomol NMR 60(4):203-208.
40. Vallurupalli P, Kay LE (2013) Probing slow chemical exchange at carbonyl sites in proteins by chemical exchange saturation transfer NMR spectroscopy. Angew Chem Int Ed Engl 52(15):4156-4159.
41. Karagöz GE, et al. (2011) N-terminal domain of human Hsp90 triggers binding to the cochaperone p23. Proc Natl Acad Sci USA 108(2):580-585.
42. McConnell HM (1958) Reaction rates by nuclear magnetic resonance. J Chem Phys 28(3):430-431.
43. Cavanagh J, Fairbrother WJ, Palmer AG, Skelton NJ (1995) Protein NMR Spectroscopy: Principles and Practice (Academic, New York).
44. Sattler M, Schleucher J, Griesinger C (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog Nucl Magn Reson Spectrosc 34(2):93-158.
45. Altieri AS, Hinton DP, Byrd RA (1995) Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements. J Am Chem Soc 117(28):7566-7567.
46. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1996) Numerical Recipes in C (Cambridge Univ Press, Cambridge, UK).