Probing the transient dark state of substrate binding to GroEL by relaxation-based solution NMR

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

Volumn 110, Issue 28, 2013, Pages 11361-11366

  Libich, David S ^a   Fawzi, Nicolas L ^a,b   Ying, Jinfa ^a   Clore, G Marius ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

Conformational sampling; Protein protein interactions; Supramolecular machine

Indexed keywords

AMYLOID BETA PROTEIN; CHAPERONIN 60; POLYPEPTIDE;

ARTICLE; CONTROLLED STUDY; DISPERSION; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR PROBE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

CONFORMATIONAL SAMPLING; PROTEIN-PROTEIN INTERACTIONS; SUPRAMOLECULAR MACHINE;

CHAPERONIN 60; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MOLECULAR PROBES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84879947509     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305715110     Document Type: Article

References (39)

1. Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62:349-384. (Pubitemid 23237875)
2. Thirumalai D, Lorimer GH (2001) Chaperonin-mediated protein folding. Annu Rev Biophys Biomol Struct 30:245-269. (Pubitemid 32566164)
3. Horwich AL, Fenton WA (2009) Chaperonin-mediated protein folding: Using a central cavity to kinetically assist polypeptide chain folding. Q Rev Biophys 42(2):83- 116.
4. Saibil HR (2008) Chaperone machines in action. Curr Opin Struct Biol 18(1):35-42.
5. Todd MJ, Lorimer GH, Thirumalai D (1996) Chaperonin-facilitated protein folding: Optimization of rate and yield by an iterative annealing mechanism. Proc Natl Acad Sci USA 93(9):4030-4035. (Pubitemid 26144240)
6. Walter S, Lorimer GH, Schmid FX (1996) A thermodynamic coupling mechanism for GroEL-mediated unfolding. Proc Natl Acad Sci USA 93(18):9425-9430. (Pubitemid 26296624)
7. Frieden C, Clark AC (1997) Protein folding: How the mechanism of GroEL action is defined by kinetics. Proc Natl Acad Sci USA 94(11):5535-5538. (Pubitemid 27241804)
8. Chen L, Sigler PB (1999) The crystal structure of a GroEL/peptide complex: Plasticity as a basis for substrate diversity. Cell 99(7):757-768. (Pubitemid 30017646)
9. Buckle AM, Zahn R, Fersht AR (1997) A structural model for GroEL-polypeptide recognition. Proc Natl Acad Sci USA 94(8):3571-3575. (Pubitemid 27180413)
10. Landry SJ, Jordan R, McMacken R, Gierasch LM (1992) Different conformations for the same polypeptide bound to chaperones DnaK and GroEL. Nature 355(6359):455-457.
11. Wang Z, Feng Hp, Landry SJ, Maxwell J, Gierasch LM (1999) Basis of substrate binding by the chaperonin GroEL. Biochemistry 38(39):12537-12546.
12. Li Y, Gao X, Chen L (2009) GroEL recognizes an amphipathic helix and binds to the hydrophobic side. J Biol Chem 284(7):4324-4331.
13. Bodner CR, Dobson CM, Bax A (2009) Multiple tight phospholipid-binding modes of á-synuclein revealed by solution NMR spectroscopy. J Mol Biol 390(4):775-790.
14. Zahn R, Spitzfaden C, Ottiger M, Wüthrich K, Plückthun A (1994) Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature 368(6468):261-265. (Pubitemid 24108846)
15. Robinson CV, et al. (1994) Conformation of GroEL-bound á-lactalbumin probed by mass spectrometry. Nature 372(6507):646-651.
16. Horst R, et al. (2005) Direct NMR observation of a substrate protein bound to the chaperonin GroEL. Proc Natl Acad Sci USA 102(36):12748-12753. (Pubitemid 41279437)
17. Koculi E, Horst R, Horwich AL, Wüthrich K (2011) Nuclear magnetic resonance spectroscopy with the stringent substrate rhodanese bound to the single-ring variant SR1 of the E. coli chaperonin GroEL. Protein Sci 20(8):1380-1386.
18. Korzhnev DM, Kay LE (2008) Probing invisible, low-populated states of protein molecules by relaxation dispersion NMR spectroscopy: An application to protein folding. Acc Chem Res 41(3):442-451.
19. Skrynnikov NR, Dahlquist FW, Kay LE (2002) Reconstructing NMR spectra of "invisible" excited protein states using HSQC and HMQC experiments. J Am Chem Soc 124(41):12352-12360. (Pubitemid 35154900)
20. Fawzi NL, Ying J, Torchia DA, Clore GM (2010) Kinetics of amyloid β monomer-to- oligomer exchange by NMR relaxation. J Am Chem Soc 132(29):9948- 9951.
21. 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.
22. Fawzi NL, Ying J, Torchia DA, Clore GM (2012) Probing exchange kinetics and atomic resolution dynamics in high-molecular-weight complexes using dark-state exchange saturation transfer NMR spectroscopy. Nat Protoc 7(8):1523- 1533.
23. Walls KC, et al. (2012) Swedish Alzheimer mutation induces mitochondrial dysfunction mediated by HSP60 mislocalization of amyloid precursor protein (APP) and betaamyloid. J Biol Chem 287(36):30317-30327.
24. Palmer AG, 3rd, Kroenke CD, Loria JP (2001) Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol 339:204- 238.
25. van der Vies SM, Viitanen PV, Gatenby AA, Lorimer GH, Jaenicke R (1992) Conformational states of ribulosebisphosphate carboxylase and their interaction with chaperonin 60. Biochemistry 31(14):3635-3644.
26. McConnell HM (1958) Reaction rates by nuclear magnetic resonance. J Chem Phys 28(3):430-431.
27. Vallurupalli P, Bouvignies G, Kay LE (2011) Increasing the exchange time-scale that can be probed by CPMG relaxation dispersion NMR. J Phys Chem B 115(49): 14891-14900.
28. Stan G, Brooks BR, Lorimer GH, Thirumalai D (2006) Residues in substrate proteins that interact with GroEL in the capture process are buried in the native state. Proc Natl Acad Sci USA 103(12):4433-4438.
29. Kjaergaard M, Brander S, Poulsen FM (2011) Random coil chemical shift for intrinsically disordered proteins: Effects of temperature and pH. J Biomol NMR 49(2):139-149.
30. Camilloni C, De Simone A, Vranken WF, Vendruscolo M (2012) Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts. Biochemistry 51(11):2224-2231.
31. Petkova AT, et al. (2002) A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99(26): 16742-16747. (Pubitemid 36034043)
32. Scheidt HA, Morgado I, Rothemund S, Huster D, Fändrich M (2011) Solid-state NMR spectroscopic investigation of Aβ protofibrils: Implication of a β-sheet remodeling upon maturation into terminal amyloid fibrils. Angew Chem Int Ed Engl 50(12):2837-2840.
33. Carulla N, Zhou M, Giralt E, Robinson CV, Dobson CM (2010) Structure and intermolecular dynamics of aggregates populated during amyloid fibril formation studied by hydrogen/deuterium exchange. Acc Chem Res 43(8):1072-1079.
34. Elad N, et al. (2007) Topologies of a substrate protein bound to the chaperonin GroEL. Mol Cell 26(3):415-426. (Pubitemid 46687100)
35. Shtilerman M, Lorimer GH, Englander SW (1999) Chaperonin function: Folding by forced unfolding. Science 284(5415):822-825. (Pubitemid 29291351)
36. Cantor CR, Schimmel PR (1980) The Behavior of Biological Macromolecules, Part III (Freeman, San Francisco).
37. Todd MJ, Lorimer GH (1998) Criteria for assessing the purity and quality of GroEL. Methods Enzymol 290:135-141. (Pubitemid 28157744)
38. 15N relaxation rates in perdeuterated proteins by TROSY-based methods. J Biomol NMR 53(3):209-221.
39. Yip GN, Zuiderweg ER (2004) A phase cycle scheme that significantly suppresses offset-dependent artifacts in the R2-CPMG 15N relaxation experiment. JMagn Reson 171(1):25-36.