Structural stability and solution structure of chaperonin GroES heptamer studied by synchrotron small-angle X-ray scattering

Journal of Molecular Biology

Volumn 333, Issue 3, 2003, Pages 605-620

  Higurashi, Takashi ^a,e   Hiragi, Yuzuru ^b,f   Ichimura, Kaoru ^c   Seki, Yasutaka ^d,g   Soda, Kunitsugu ^d   Mizobata, Tomohiro ^a   Kawata, Yasushi ^a  

^a TOTTORI UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c DOKKYO MEDICAL UNIVERSITY   (Japan)

^d NAGAOKA UNIVERSITY OF TECHNOLOGY   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f KANSAI MEDICAL UNIVERSITY   (Japan)

^g NAGOYA UNIVERSITY   (Japan)

Author keywords

Chaperonin GroES; Oligomeric protein folding; Reversible oligomerization; Synchrotron small angle X ray scattering; Three state model

Indexed keywords

CHAPERONIN; MONOMER;

ARTICLE; CONCENTRATION (PARAMETERS); ESCHERICHIA COLI; HEAT STRESS; IN VIVO STUDY; INFORMATION; MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SIMULATION; SYNCHROTRON; X RAY CRYSTALLOGRAPHY;

ESCHERICHIA COLI;

EID: 0141527459     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.08.056     Document Type: Article

References (64)

1. Anfinsen C.B. Principles that govern the folding of protein chains. Science. 181:1973;223-229.
2. Radford S.E. Protein folding: progress made and promises ahead. Trends Biochem. Sci. 25:2000;611-618.
3. Baker D. A surprising simplicity to protein folding. Nature. 405:2000;39-42.
4. Jaenicke R. Folding and association of proteins. Prog. Biophys. Mol. Biol. 49:1987;117-237.
5. Jaenicke R., Lilie H. Folding and association of oligomeric and multimeric proteins. Advan. Protein Chem. 53:2000;329-401.
6. Higurashi T., Nosaka K., Mizobata T., Nagai J., Kawata Y. Unfolding and refolding of Escherichia coli chaperonin GroES is expressed by a three-state model. J. Mol. Biol. 291:1999;703-713.
7. Seale J.W., Gorovits B.M., Ybarra J., Horowitz P.M. Reversible oligomerization and denaturation of the chaperonin GroES. Biochemistry. 35:1996;4079-4083.
8. Boudker O., Todd M.J., Freire E. The structural stability of the co-chaperonin GroES. J. Mol. Biol. 272:1997;770-779.
9. Panda M., Ybarra J., Horowitz P.M. High hydrostatic pressure can probe the effects of functionally related ligands on the quaternary structures of the chaperonins GroEL and GroES. J. Biol. Chem. 276:2001;6253-6259.
10. Bukau B., Horwich A.L. The Hsp70 and Hsp60 chaperone machines. Cell. 92:1998;351-366.
11. Hartl F.U., Hayer-Hartl M.K. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science. 295:2002;1852-1858.
12. Lorimer G.H. A quantitative assessment of the role of the chaperonin proteins in protein folding in vivo. FASEB J. 10:1996;5-9.
13. Ellis R.J., Hartl F.U. Protein folding in the cell: competing models of chaperonin function. FASEB J. 10:1996;20-26.
14. Herendeen S.L., VanBogelen R.A., Neidhardt F.C. Levels of major protein of Escherichia coli during growth at different temperatures. J. Bacteriol. 139:1979;185-194.
15. Landry S.J., Zeilstra-Ryalls J., Fayet O., Georgopoulos C., Gierasch L.M. Characterization of a functionally important mobile domain of GroES. Nature. 364:1993;255-264.
16. 7 chaperonin complex. Nature. 388:1997;741-750.
17. Hunt J.F., Weaver A.J., Landry S.J., Gierasch L., Deisenhofer J. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature. 379:1996;37-45.
18. Kataoka M., Goto Y. X-ray solution scattering studies of protein folding. Fold. Des. 1:1996;R107-R114.
19. Kajiwara K., Hiragi Y. Structure analysis by small-angle X-ray scattering. Saisho H., Goshi Y. Applications of Synchrotron Radiation to Material Analysis. 1996;353-404 Elsevier, Amsterdam.
20. Damaschun G., Damaschun H., Gast K., Zirwer D. Denatured states of yeast phosphoglycerate kinase. Biochemistry (Moscow). 63:1998;259-275.
21. Doniach S. Changes in biomolecular conformation seen by small angle X-ray scattering. Chem. Rev. 101:2001;1763-1778.
22. Fuseya M., Ichimura K., Yamamura T., Tachi'iri Y., Satake K., Amemiya Y., Kihara H. Dissociation and auto-oxidation of hemerythrin induced by SH-modification: a kinetic study. J. Biochem. 105:1989;293-298.
23. Hiragi Y., Inoue H., Sano Y., Kajiwara K., Ueki T., Nakatani H. Dynamic mechanism of the self-assembly process of tobacco mosaic virus protein studied by rapid temperature-jump small-angle X-ray scattering using synchrotron radiation. J. Mol. Biol. 213:1990;495-502.
24. Kataoka M., Hagihara Y., Mihara K., Goto Y. Molten globule of cytochrome c studied by small angle X-ray scattering. J. Mol. Biol. 229:1993;591-596.
25. Eliezer D., Jennings P.A., Wright P.E., Doniach S., Hodgson K.O., Tsuruta H. The radius of gyration of an apomyoglobin folding intermediate. Science. 270:1995;487-488.
26. Arai M., Ikura T., Semisotnov G.V., Kihara H., Amemiya Y., Kuwajima K. Kinetic refolding of β-lactoglobulin: studies by synchrotron X-ray scattering, circular dichroism, absorption and fluorescence spectroscopy. J. Mol. Biol. 275:1998;149-162.
27. Macol C.P., Tsuruta H., Stec B., Kantrowitz E.R. Direct structural evidence for a concerted allosteric transition in Escherichia coli aspartate transcarbamoylase. Nature Struct. Biol. 8:2001;423-426.
28. Hiragi Y., Inoue H., Sano Y., Kajiwara K., Ueki T., Kataoka M., et al. Temperature dependence of the structure of aggregates of tobacco mosaic virus protein at pH 7.2. Static synchrotron small-angle X-ray scattering. J. Mol. Biol. 204:1988;129-140.
29. Hiragi Y., Seki Y., Ichimura K., Soda K. Direct detection of the protein quaternary structure and denatured entity by small-angle scattering: guanidine hydrochloride denaturation of chaperonin protein GroEL. J. Appl. Crystallog. 35:2002;1-7.
30. Kamatari Y.O., Ohji S., Konno T., Seki Y., Soda K., Kataoka M., Akasaka K. The compact and expanded denatured conformations of apomyoglobin in the methanol-water solvent. Protein Sci. 8:1999;873-882.
31. Henry E.R., Hofrichter J. Singular value decomposition: application to analysis of experimental data. Methods Enzymol. 210:1992;129-192.
32. Hoshino M., Hagihara Y., Hamada D., Kataoka M., Goto Y. Trifluoroethanol-induced conformational transition of hen egg-white lysozyme studied by small-angle X-ray scattering. FEBS Letters. 416:1997;72-76.
33. Gualfetti P.J., Iwakura M., Lee J.C., Kihara H., Bilsel O., Zitzewitz J.A., Matthews C.R. Apparent radii of the native, stable intermediates and unfolded conformers of the α-subunit of tryptophan synthetase from E. coli, a TIM barrel protein. Biochemistry. 38:1999;13367-13378.
34. Glatter O., Kratky O. Small Angle X-ray Scattering. 1982;Academic Press, New York.
35. Zhou J.-M., Fan Y.-X., Kihara H., Kimura K., Amemiya Y. Unfolding of dimeric creatine kinase in urea and guanidine hydrochloride as measured using small angle X-ray scattering with synchrotron radiation. FEBS Letters. 415:1997;183-185.
36. Kojima K., Tanokura M., Maeda M., Kimura K., Amemiya Y., Kihara H., Takahashi K. pH-dependent unfolding of Aspergillopepsin II studied by small-angle X-ray scattering. Biochemistry. 39:2000;1364-1372.
37. Fujisawa T., Kato M., Inoko Y. Structural characterization of lactate dehydrogenase dissociation under high pressure studied by synchrotron high-pressure small-angle X-ray scattering. Biochemistry. 38:1999;6411-6418.
38. Timchenko A.A., Melnik B.S., Kihara H., Kimura K., Semisotnov G.V. GroES co-chaperonin small-angle X-ray scattering study shows ring orifice increase in solution. FEBS Letters. 471:2000;211-214.
39. Stegmann R., Manakova E., Rossle M., Heumann H., Nieba-Axmann N., Plückthum A., et al. Structural changes of the Escherichia coli GroEL-GroES chaperonins upon complex formation in solution: a neutron small angle scattering study. J. Struct. Biol. 121:1998;30-40.
40. Hubbard S.R., Hodgson K.O., Doniach S. Small-angle X-ray scattering investigation of the solution structure of troponin C. J. Biol. Chem. 263:1988;4151-4158.
41. Kataoka M., Head J.F., Persechini A., Kretsinger R.H., Engelman D.M. Small-angle X-ray scattering studies of calmodulin mutants with deletions in the linker region of the central helix indicate that the linker region retains a predominantly α-helical conformation. Biochemistry. 30:1991;1188-1192.
42. Yuzawa S., Yokochi M., Hatanaka H., Ogura K., Kataoka M., Miura K., et al. Solution structure of Grb2 reveals extensive flexibility necessary for target recognition. J. Mol. Biol. 306:2001;527-537.
43. Sousa M.C., Trame C.B., Tsuruta H., Wilbanks S.M., Reddy V.S., McKay D.B. Crystal and solution of an HslUV protease-chaperone complex. Cell. 103:2000;633-643.
44. Semisotnov G.V., Kihara H., Kotova N.V., Kimura K., Amemiya Y., Wakabayashi K., et al. Protein globularization during folding; a study by synchrotron small-angle X-ray scattering. J. Mol. Biol. 262:1996;559-574.
45. Arai M., Ito K., Inobe T., Nakao M., Maki K., Kamagata K., et al. Fast compaction of α-lactalbumin during folding studied by stopped-flow X-ray scattering. J. Mol. Biol. 321:2002;121-132.
46. Chen L., Hodgson K.O., Doniach S. A lysozyme folding intermediate revealed by solution X-ray scattering. J. Mol. Biol. 261:1996;658-671.
47. Landry S.J., Steede N.K., Maskos K. Temperature dependence of backbone dynamics in loops of human mitochondrial heat shock protein 10. Biochemistry. 36:1997;10975-10986.
48. Landry S.J., Taher A., Georgopoulos C., van der Vies S.M. Interplay of structure and disorder in cochaperonin mobile loops. Proc. Natl Acad. Sci. USA. 93:1996;11622-11627.
49. Fiaux J., Bertelsen E.B., Horwich A.L., Wüthrich K. NMR analysis of a 900K GroEL-GroES complex. Nature. 418:2002;207-211.
50. Hemmingsen S.M., Woolford C., van der Vies S.M., Tilly K., Dennis D.T., Georgopoulos C.P., et al. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature. 333:1988;330-334.
51. Millett I.S., Doniach S., Plaxco K.W. Toward a taxonomy of the denatured state: small angle scattering studies of unfolded proteins. Advan. Protein Chem. 62:2002;241-262.
52. Mizobata T., Akiyama Y., Ito K., Yumoto N., Kawata Y. Effects of the chaperonin GroE on the refolding of tryptophanase from Escherichia coli. J. Biol. Chem. 267:1992;17773-17779.
53. Kawata Y., Kawagoe M., Hongo K., Miyazaki T., Higurashi T., Mizobata T., Nagai J. Functional communications between the apical and equatorial domains of GroEL through the intermediate domain. Biochemistry. 38:1999;15731-15740.
54. Kamireddi M., Eisenstein E., Reddy P. Stable expression and rapid purification of Escherichia coli GroEL and GroES chaperonins. Protein Expr. Purif. 11:1997;47-52.
55. Makio T., Arai M., Kuwajima K. Chaperonin-affected refolding of α-lactalbumin: effects of nucleotides and the co-chaperonin GroES. J. Mol. Biol. 293:1999;125-137.
56. Ueki T., Hiragi Y., Izumi Y., Tagawa H., Kataoka M., Muroga Y., et al. Dynamic behavior of biopolymers by small-angle X-ray scattering (I). Photon Factory Activity Rep. 1982/83:1983;VI70-VI71.
57. Ueki T., Hiragi Y., Kataoka M., Inoko Y., Amemiya Y., Izumi Y., et al. Aggregation of bovine serum albumin upon cleavage of its disulfide bonds, studied by the time-resolved small-angle X-ray scattering technique with synchrotron radiation. Biophys. Chem. 23:1985;115-124.
58. Hiragi Y., Sano Y., Matsumoto T. SAXSANA: an interactive programme for the analysis and monitoring of static and time-resolved small-angle X-ray solution scattering measurements. J. Synchrotoron Rad. 10:2003;193-196.
59. Guinier A., Fournet G. Small-angle Scattering of X-rays. 1955;Chapman & Hall, New York.
60. Kratky O., Porod G., Kahovec L. Einige Neuerungen in der Technik und Auswertung von Röntgen-kleinwinkelmessungen. Zeit. Electrochem. 55:1951;53-59.
61. Soda K., Miki Y., Nishizawa T., Seki Y. New method for incorporating solvent influence into the evaluation of X-ray scattering intensity of proteins in solution. Biophys. Chem. 65:1997;45-53.
62. Seki Y., Tomizawa T., Khechinashvili N.N., Soda K. Contribution of solvent water to the solution X-ray scattering profile of proteins. Biophys. Chem. 95:2002;235-252.
63. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
64. Zondlo J., Fisher K.E., Lin Z., Ducote K.R., Eisenstein E. Monomer-heptamer equilibrium of the Escherichia coli chaperonin GroES. Biochemistry. 34:1995;10334-10339.