Regions outside the α-crystallin domain of the small heat shock protein Hsp26 are required for its dimerization

Journal of Molecular Biology

Volumn 398, Issue 1, 2010, Pages 122-131

  Chen, Jin ^a   Feige, Matthias J ^a   Franzmann, Titus M ^a   Bepperling, Alexander ^a   Buchner, Johannes ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Protein association; Protein folding; Protein stability; Small heat shock proteins; crystallin domain

Indexed keywords

CHAPERONE; DIMER; HEAT SHOCK PROTEIN 26; MONOMER; OLIGOMER;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; IONIC STRENGTH; MOLECULAR STABILITY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; THERMODYNAMICS;

SACCHAROMYCES CEREVISIAE;

EID: 77950865810     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.02.022     Document Type: Article

References (37)

1. Lindquist S., Craig E.A. The heat-shock proteins. Annu. Rev. Genet. 1988, 22:631-677.
2. Boston R.S., Viitanen P.V., Vierling E. Molecular chaperones and protein folding in plants. Plant Mol. Biol. 1996, 32:191-222.
3. Horwitz J. Alpha-crystallin. Exp. Eye Res. 2003, 76:145-153.
4. Haslbeck M., Franzmann T.M., Weinfurtner D., Buchner J. Some like it hot: the structure and function of small heat-shock proteins. Nat. Struct. Mol. Biol. 2005, 12:842-846.
5. Walter S., Buchner J. Molecular chaperones-cellular machines for protein folding. Angew. Chem., Int. Ed. Engl. 2002, 41:1098-1113.
6. Mchaourab H.S., Godar J.A., Stewart P.L. Structure and mechanism of protein stability sensors: chaperone small heat shock proteins. Biochemistry 2009, 48:3828-3837.
7. Narberhaus F. α-Crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev. 2002, 66:64-93.
8. Ehrnsperger M., Gräber S., Gaestel M., Buchner J. Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 1997, 16:221-229.
9. Lee G.J., Roseman A.M., Saibil H.R., Vierling E. A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J. 1997, 3:659-671.
10. Veinger L., Diamant S., Buchner J., Goloubinoff P. The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J. Biol. Chem. 1998, 273:11032-11037.
11. van Montfort R.L.M., Slingsby C., Vierling E. Structure and function of the small heat shock protein/α-crystallin family of molecular chaperones. Protein Folding in the Cell: Advances in Protein Structure 2002, vol. 59:105-156. Academic Press, San Diego, CA. A. Horwich (Ed.).
12. Stromer T., Fischer E., Richter K., Haslbeck M., Buchner J. Analysis of the regulation of the molecular chaperone Hsp26 by temperature-induced dissociation: the N-terminal domain is important for oligomer assembly and the binding of unfolding proteins. J. Biol. Chem. 2004, 279:11222-11228.
13. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc. Natl Acad. Sci. USA 1992, 89:10449-10453.
14. Peschek J., Braun N., Franzmann T.M., Georgalis Y., Haslbeck M., Weinkauf S., Buchner J. The eye lens chaperone alpha-crystallin forms defined globular assemblies. Proc. Natl Acad. Sci. USA 2009, 106:13272-13277.
15. Mornon J.P., Halaby D., Malfois M., Durand P., Callebaut I., Tardieu A. α-Crystallin C-terminal domain: on the track of an Ig fold. Int. J. Biol. Macromol. 1998, 22:219-227.
16. Kim K.K., Kim R., Kim S.H. Crystal structure of a small heat-shock protein. Nature 1998, 394:595-599.
17. van Montfort R.L., Basha E., Friedrich K.L., Slingsby C., Vierling E. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct. Biol. 2001, 8:1025-1030.
18. Bagnéris C., Bateman O.A., Naylor C.E., Cronin N., Boelens W.C., Keep N.H., Slingsby C. Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20. J. Mol. Biol. 2009, 392:1242-1252.
19. Haslbeck M., Walke S., Stromer T., Ehrnsperger M., White H.E., Chen S. Hsp26: a temperature-regulated chaperone. EMBO J. 1999, 18:6744-6751.
20. Koteiche H.A., Mchaourab H.S. The determinants of the oligomeric structure in Hsp16.5 are encoded in the α-crystallin domain. FEBS Lett. 2002, 519:16-22.
21. Wintrode P.L., Friedrich K.L., Vierling E., Smith J.B., Smith D.L. Solution structure and dynamics of a heat shock protein assembly probed by hydrogen exchange and mass spectrometry. Biochemistry 2003, 42:10667-10673.
22. Haslbeck M., Braun N., Stromer T., Richter B., Model N., Weinkauf S., Buchner J. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J. 2004, 23:638-649.
23. Franzmann T.M., Wühr M., Richter K., Walter S., Buchner J. The activation mechanism of Hsp26 does not require dissociation of the oligomer. J. Mol. Biol. 2005, 350:1083-1093.
24. Susek R.E., Lindquist S.L. Hsp26 of Saccharomyces cerevisiae is related to the superfamily of small heat shock proteins but is without a demonstrable function. Mol. Cell. Biol. 1989, 9:5265-5271.
25. Haslbeck M., Ignatiou A., Saibil H., Helmich S., Frenzl E., Stromer T., Buchner J. A domain in the N-terminal part of Hsp26 is essential for chaperone function and oligomerization. J. Mol. Biol. 2004, 343:445-455.
26. White H.E., Orlova E.V., Chen S., Wang L., Ignatiou A., Gowen B. Multiple distinct assemblies reveal conformational flexibility in the small heat shock protein Hsp26. Structure 2006, 14:1197-1204.
27. Franzmann T., Menhorn P., Walter S., Buchner J. Activation of the chaperone Hsp26 is controlled by the rearrangement of its thermo sensor domain. Mol. Cell 2008, 29:207-216.
28. Stromer T., Ehrnsperger M., Gaestel M., Buchner J. Analysis of the interaction of small heat shock proteins with unfolding proteins. J. Biol. Chem. 2003, 278:18015-18021.
29. 1H NMR spectroscopy reveals that mouse Hsp25 has a flexible C-terminal extension of 18 amino acids. FEBS Lett. 1995, 369:305-310.
30. Fernando P., Abdulle R., Mohindra A., Guillemette J.G., Heikkila J.J. Mutation or deletion of the C-terminal tail affects the function and structure of Xenopus laevis small heat shock protein, Hsp30. Comput. Biochem. Physiol. B: Biochem. Mol. Biol. 2002, 133:95-103.
31. Lindner R.A., Carver J.A., Ehrnsperger M., Buchner J., Esposito G., Behlke J. Mouse Hsp25, a small shock protein. The role of its C-terminal extension in oligomerization and chaperone action. Eur. J. Biochem. 2000, 267:1923-1932.
32. de Jong W.W., Caspers G.J., Leunissen J.A.M. Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int. J. Biol. Macromol. 1998, 22:151-162.
33. de Miguel N., Braun N., Bepperling A., Kriehuber T., Kastenmuller A., Buchner J. Structural and functional diversity in the family of small heat shock proteins from the parasite Toxoplasma gondii. Biochim. Biophys. Acta 2009, 1793:1738-1748.
34. Haley D.A., Horwitz J., Stewart P.L. The small heat-shock protein, alpha B-crystallin, has a variable quaternary structure. J. Mol. Biol. 1998, 277:27-35.
35. Haslbeck M., Kastenmüller A., Buchner J., Weinkauf S., Braun N. Structural dynamics of archaeal small heat shock proteins. J. Mol. Biol. 2008, 378:362-374.
36. 3DHSP27). J. Biol. Chem. 2001, 276:26753-26761.
37. Santoro M.M., Bolen D.W. Unfolding free energy changes determined by the linear extrapolation. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 1988, 27:8063-8068.