Alternative Bacterial Two-component Small Heat Shock Protein Systems

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2012 Nov 28

PMID 23184973

Citations 54

Authors

Alexander Bepperling

Ferdinand Alte

Thomas Kriehuber

Nathalie Braun

Sevil Weinkauf

Michael Groll

Martin Haslbeck

Johannes Buchner

Affiliations

Soon will be listed here.

Abstract

Small heat shock proteins (sHsps) are molecular chaperones that prevent the aggregation of nonnative proteins. The sHsps investigated to date mostly form large, oligomeric complexes. The typical bacterial scenario seemed to be a two-component sHsps system of two homologous sHsps, such as the Escherichia coli sHsps IbpA and IbpB. With a view to expand our knowledge on bacterial sHsps, we analyzed the sHsp system of the bacterium Deinococcus radiodurans, which is resistant against various stress conditions. D. radiodurans encodes two sHsps, termed Hsp17.7 and Hsp20.2. Surprisingly, Hsp17.7 forms only chaperone active dimers, although its crystal structure reveals the typical α-crystallin fold. In contrast, Hsp20.2 is predominantly a 36mer that dissociates into smaller oligomeric assemblies that bind substrate proteins stably. Whereas Hsp20.2 cooperates with the ATP-dependent bacterial chaperones in their refolding, Hsp17.7 keeps substrates in a refolding-competent state by transient interactions. In summary, we show that these two sHsps are strikingly different in their quaternary structures and chaperone properties, defining a second type of bacterial two-component sHsp system.

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References

Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J . Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J. 2010; 24(10):3633-42. DOI: 10.1096/fj.10-156992. View

Friedrich K, Giese K, Buan N, Vierling E . Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes. J Biol Chem. 2003; 279(2):1080-9. DOI: 10.1074/jbc.M311104200. View

Saji H, Iizuka R, Yoshida T, Abe T, Kidokoro S, Ishii N . Role of the IXI/V motif in oligomer assembly and function of StHsp14.0, a small heat shock protein from the acidothermophilic archaeon, Sulfolobus tokodaii strain 7. Proteins. 2007; 71(2):771-82. DOI: 10.1002/prot.21762. View

Lin C, Lee C, Lin J, Tsai W, Wang S, Weng S . Characterization of Xanthomonas campestris pv. campestris heat shock protein A (HspA), which possesses an intrinsic ability to reactivate inactivated proteins. Appl Microbiol Biotechnol. 2010; 88(3):699-709. DOI: 10.1007/s00253-010-2776-z. View

van Montfort R, Basha E, Friedrich K, Slingsby C, Vierling E . Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol. 2001; 8(12):1025-30. DOI: 10.1038/nsb722. View

Bukach O, Seit-Nebi A, Marston S, Gusev N . Some properties of human small heat shock protein Hsp20 (HspB6). Eur J Biochem. 2004; 271(2):291-302. DOI: 10.1046/j.1432-1033.2003.03928.x. View

Battista J . Against all odds: the survival strategies of Deinococcus radiodurans. Annu Rev Microbiol. 1997; 51:203-24. DOI: 10.1146/annurev.micro.51.1.203. View

Ratajczak E, Zietkiewicz S, Liberek K . Distinct activities of Escherichia coli small heat shock proteins IbpA and IbpB promote efficient protein disaggregation. J Mol Biol. 2008; 386(1):178-89. DOI: 10.1016/j.jmb.2008.12.009. View

Kampinga H, Brunsting J, Stege G, Konings A, Landry J . Cells overexpressing Hsp27 show accelerated recovery from heat-induced nuclear protein aggregation. Biochem Biophys Res Commun. 1994; 204(3):1170-7. DOI: 10.1006/bbrc.1994.2586. View

10.

Kim K, Kim R, Kim S . Crystal structure of a small heat-shock protein. Nature. 1998; 394(6693):595-9. DOI: 10.1038/29106. View

11.

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 domail is important for oligomer assembly and the binding of unfolding proteins. J Biol Chem. 2004; 279(12):11222-8. DOI: 10.1074/jbc.M310149200. View

12.

Bukach O, Glukhova A, Seit-Nebi A, Gusev N . Heterooligomeric complexes formed by human small heat shock proteins HspB1 (Hsp27) and HspB6 (Hsp20). Biochim Biophys Acta. 2008; 1794(3):486-95. DOI: 10.1016/j.bbapap.2008.11.010. View

13.

Matuszewska M, Kuczynska-Wisnik D, Laskowska E, Liberek K . The small heat shock protein IbpA of Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J Biol Chem. 2005; 280(13):12292-8. DOI: 10.1074/jbc.M412706200. View

14.

Basha E, Lee G, Breci L, Hausrath A, Buan N, Giese K . The identity of proteins associated with a small heat shock protein during heat stress in vivo indicates that these chaperones protect a wide range of cellular functions. J Biol Chem. 2003; 279(9):7566-75. DOI: 10.1074/jbc.M310684200. View

15.

Ratajczak E, Strozecka J, Matuszewska M, Zietkiewicz S, Kuczynska-Wisnik D, Laskowska E . IbpA the small heat shock protein from Escherichia coli forms fibrils in the absence of its cochaperone IbpB. FEBS Lett. 2010; 584(11):2253-7. DOI: 10.1016/j.febslet.2010.04.060. View

16.

Hilario E, Martin F, Bertolini M, Fan L . Crystal structures of Xanthomonas small heat shock protein provide a structural basis for an active molecular chaperone oligomer. J Mol Biol. 2011; 408(1):74-86. DOI: 10.1016/j.jmb.2011.02.004. View

17.

Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White H, Chen S . Hsp26: a temperature-regulated chaperone. EMBO J. 1999; 18(23):6744-51. PMC: 1171736. DOI: 10.1093/emboj/18.23.6744. View

18.

Heinz K, Marx A . Lesion bypass activity of DNA polymerase A from the extremely radioresistant organism Deinococcus radiodurans. J Biol Chem. 2007; 282(15):10908-14. DOI: 10.1074/jbc.M611404200. View

19.

Airo A, Chan S, Martinez Z, Platt M, Trent J . Heat shock and cold shock in Deinococcus radiodurans. Cell Biochem Biophys. 2004; 40(3):277-88. DOI: 10.1385/CBB:40:3:277. View

20.

Mogk A, Deuerling E, Vorderwulbecke S, Vierling E, Bukau B . Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol. 2003; 50(2):585-95. DOI: 10.1046/j.1365-2958.2003.03710.x. View