Nuclear magnetic resonance approaches for characterizing interactions between the bacterial chaperonin GroEL and unstructured proteins

Journal of Bioscience and Bioengineering

Volumn 116, Issue 2, 2013, Pages 160-164

  Nishida, Noritaka ^a,b   Yagi Utsumi, Maho ^b,c   Motojima, Fumihiro ^d   Yoshida, Masasuke ^d   Shimada, Ichio ^a   Kato, Koichi ^b,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b Nagoya City University   (Japan)

^c OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^d KyotoSangyoUniversity ^*  (Japan)

Author keywords

Synuclein; SN; Denaturation; DTT; GdmCl; GroEL; HSQC; Intrinsically disordered protein; Molecular chaperone; Nuclear magnetic resonance; Rho; Rhodanese; SR1

Indexed keywords

DTT; GDMCL; GROEL; HSQC; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR CHAPERONES; RHO; RHODANESE; SR1; SYNUCLEIN;

DENATURATION; ISOTOPES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS;

NUCLEAR MAGNETIC RESONANCE;

ALPHA SYNUCLEIN; BACTERIAL PROTEIN; CHAPERONIN; CHAPERONIN GROEL; UNCLASSIFIED DRUG;

ARTICLE; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATTLE; CHAPERONIN 60; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; THIOSULFATE SULFURTRANSFERASE;

BACTERIA (MICROORGANISMS); BOVINAE;

EID: 84879125630     PISSN: 13891723     EISSN: 13474421     Source Type: Journal    
DOI: 10.1016/j.jbiosc.2013.02.012     Document Type: Article

References (27)

1. Hartl F.U. Molecular chaperones in cellular protein folding. Nature 1996, 381:571-579.
2. Ben-Zvi A.P., Goloubinoff P. Review: mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J.Struct. Biol. 2001, 135:84-93.
3. Kinbara K., Aida T. Toward intelligent molecular machines: directed motions of biological and artificial molecules and assemblies. Chem. Rev. 2005, 105:1377-1400.
4. Braig K., Otwinowski Z., Hegde R., Boisvert D.C., Joachimiak A., Horwich A.L., Sigler P.B. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 1994, 371:578-586.
5. Chatellier J., Buckle A.M., Fersht A.R. GroEL recognises sequential and non-sequential linear structural motifs compatible with extended β-strands and α-helices. J.Mol. Biol. 1999, 292:163-172.
6. Kobayashi N., Freund S.M., Chatellier J., Zahn R., Fersht A.R. NMR analysis of the binding of a rhodanese peptide to a minichaperone in solution. J.Mol. Biol. 1999, 292:181-190.
7. Chen L., Sigler P.B. The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell 1999, 99:757-768.
8. Zahn R., Spitzfaden C., Ottiger M., Wüthrich K., Plückthun A. Destabilization of the complete protein secondary structure on binding to the chaperone GroEL. Nature 1994, 368:261-265.
9. Robinson C.V., Gross M., Eyles S.J., Ewbank J.J., Mayhew M., Hartl F.U., Dobson C.M., Radford S.E. Conformation of GroEL-bound alpha-lactalbumin probed by mass spectrometry. Nature 1994, 372:646-651.
10. Horst R., Bertelsen E.B., Fiaux J., Wider G., Horwich A.L., Wüthrich K. Direct NMR observation of a substrate protein bound to the chaperonin GroEL. Proc. Natl. Acad. Sci. USA 2005, 102:12748-12753.
11. Koculi E., Horst R., Horwich A.L., Wüthrich K. Nuclear magnetic resonance spectroscopy with the stringent substrate rhodanese bound to the single-ring variant SR1 of the E.coli chaperonin GroEL. Protein Sci. 2011, 20:1380-1386.
12. Ishii D., Kinbara K., Ishida Y., Ishii N., Okochi M., Yohda M., Aida T. Chaperonin-mediated stabilization and ATP-triggered release of semiconductor nanoparticles. Nature 2003, 423:628-632.
13. Shults C.W. Lewy bodies. Proc. Natl. Acad. Sci. USA 2006, 103:1661-1668.
14. 13C NMR spectroscopy. J.Biochem. 2006, 140:591-598.
15. Sasakawa H., Sakata E., Yamaguchi Y., Masuda M., Mori T., Kurimoto E., Iguchi T., Hisanaga S., Iwatsubo T., Hasegawa M., Kato K. Ultra-high field NMR studies of antibody binding and site-specific phosphorylation of α-synuclein. Biochem. Biophys. Res. Commun. 2007, 363:795-799.
16. Miller D.M., Kurzban G.P., Mendoza J.A., Chirgwin J.M., Hardies S.C., Horowitz P.M. Recombinant bovine rhodanese: purification and comparison with bovine liver rhodanese. Biochim. Biophys. Acta 1992, 1121:286-292.
17. Mendoza J.A., Rogers E., Lorimer G.H., Horowitz P.M. Chaperonins facilitate the in vitro folding of monomeric mitochondrial rhodanese. J.Biol. Chem. 1991, 266:13044-13049.
18. 13C chemical-shift data. J.Biomol. NMR 1994, 4:171-180.
19. Chen J., Yagi H., Sormanni P., Vendruscolo M., Makabe K., Nakamura T., Goto Y., Kuwajima K. Fibrillogenic propensity of the GroEL apical domain: a Janus-faced minichaperone. FEBS Lett. 2012, 586:1120-1127.
20. Bodner C.R., Maltsev A.S., Dobson C.M., Bax A. Differential phospholipid binding of α-synuclein variants implicated in Parkinson's disease revealed by solution. NMR Spectrosc. Biochem. 2010, 49:862-871.
21. Yamaguchi Y., Masuda M., Sasakawa H., Nonaka T., Hanashima S., Hisanaga S., Kato K., Hasegawa M. Characterization of inhibitor-bound α-synuclein dimer: role of α-synuclein N-terminal region in dimerization and inhibitor binding. J.Mol. Biol. 2010, 395:445-456.
22. Ulmer T.S., Bax A., Cole N.B., Nussbaum R.L. Structure and dynamics of micelle-bound human α-synuclein. J.Biol. Chem. 2005, 280:9595-9603.
23. Bartels T., Ahlstrom L.S., Leftin A., Kamp F., Haass C., Brown M.F., Beyer K. The N-terminus of the intrinsically disordered protein α-synuclein triggers membrane binding and helix folding. Biophys. J. 2010, 99:2116-2124.
24. Yamaguchi T., Uno T., Uekusa Y., Yagi-Utsumi M., Kato K. Ganglioside-embedding small bicelles for probing membrane-landing processes of intrinsically disordered proteins. Chem. Commun. (Camb) 2013, 49:1235-1237.
25. Mittag T., Orlicky S., Choy W.Y., Tang X., Lin H., Sicheri F., Kay L.E., Tyers M., Forman-Kay J.D. Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor. Proc. Natl. Acad. Sci. USA 2008, 105:17772-17777.
26. Fawzi N.L., Ying J., Ghirlando R., Torchia D.A., Clore G.M. Atomic-resolution dynamics on the surface of amyloid-β protofibrils probed by solution NMR. Nature 2011, 480:268-272.
27. Motojima F., Motojima-Miyazaki Y., Yoshida M. Revisiting the contribution of negative charges on the chaperonin cage wall to the acceleration of protein folding. Proc. Natl. Acad. Sci. USA 2012, 109:15740-15745.