Alternative bacterial two-component small heat shock protein systems

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

Volumn 109, Issue 50, 2012, Pages 20407-20412

  Bepperling, Alexander ^a   Alte, Ferdinand ^a   Kriehuber, Thomas ^a   Braun, Nathalie ^a   Weinkauf, Sevil ^a   Groll, Michael ^a   Haslbeck, Martin ^a   Buchner, Johannes ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Chaperone evolution; Chaperone function; Heat stress; Protein aggregation; Stress response

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHAPERONE; DIMER; HEAT SHOCK PROTEIN; OLIGOMER;

ARTICLE; BACTERIUM; CRYSTAL STRUCTURE; DEINOCOCCUS RADIODURANS; DISSOCIATION CONSTANT; ENZYME SUBSTRATE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN QUATERNARY STRUCTURE; PROTEIN REFOLDING; PROTEIN STABILITY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DEINOCOCCUS; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS, SMALL; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS); DEINOCOCCUS RADIODURANS; ESCHERICHIA COLI;

EID: 84870917750     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1209565109     Document Type: Article

References (53)

1. McHaourab HS, Godar JA, Stewart PL (2009) Structure and mechanism of protein stability sensors: Chaperone activity of small heat shock proteins. Biochemistry 48(18):3828-3837.
2. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: The structure and function of small heat-shock proteins. Nat Struct Mol Biol 12(10):842-846. (Pubitemid 41486706)
3. Liberek K, Lewandowska A, Zietkiewicz S (2008) Chaperones in control of protein disaggregation. EMBO J 27(2):328-335. (Pubitemid 351161659)
4. Basha E, O'Neill H, Vierling E (2012) Small heat shock proteins and alpha-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37(3):106-117.
5. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: Life on the verge of death. Mol Cell 40(2):253-266.
6. Kampinga HH, Brunsting JF, Stege GJ, Konings AW, Landry J (1994) Cells overexpressing Hsp27 show accelerated recovery from heat-induced nuclear protein aggregation. Biochem Biophys Res Commun 204(3):1170-1177.
7. Mogk A, Deuerling E, Vorderwülbecke S, Vierling E, Bukau B (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50(2):585-595. (Pubitemid 37297136)
8. Haslbeck M, Miess A; Stromer T; Walter S; Buchner J (2005) Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104. J Biol Chem 280(25):23861-23868. (Pubitemid 40884873)
9. Cashikar AG, Duennwald ML, Lindquist SL (2005) A chaperone pathway in protein disaggregation. Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J Biol Chem 280(25):23869-23875. (Pubitemid 40884874)
10. Veinger L, Diamant S, Buchner J, Goloubinoff P (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273(18):11032-11037. (Pubitemid 28204946)
11. Kappé G, Leunissen JA, de Jong WW (2002) Evolution and diversity of prokaryotic small heat shock proteins. Prog Mol Subcell Biol 28:1-17.
12. Kriehuber T, et al. (2010) Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J 24(10):3633-3642.
13. Horwitz J (2003) Alpha-crystallin. Exp Eye Res 76(2):145-153.
14. Stamler R, Kappé G, Boelens W, Slingsby C (2005) Wrapping the alpha-crystallin domain fold in a chaperone assembly. J Mol Biol 353(1):68-79. (Pubitemid 41338840)
15. Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heat-shock protein. Nature 394(6693):595-599. (Pubitemid 28366837)
16. Bagnéris C, et al. (2009) Crystal structures of alpha-crystallin domain dimers of alphaBcrystallin and Hsp20. J Mol Biol 392(5):1242-1252.
17. van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8(12):1025-1030. (Pubitemid 33101621)
18. Laganowsky A, et al. (2010) Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci 19(5):1031-1043.
19. Braun N, et al. (2011) Multiple molecular architectures of the eye lens chaperone áBcrystallin elucidated by a triple hybrid approach. Proc Natl Acad Sci USA 108(51):20491-20496.
20. Haslbeck M, Kastenmüller A, Buchner J, Weinkauf S, Braun N (2008) Structural dynamics of archaeal small heat shock proteins. J Mol Biol 378(2):362-374.
21. White HE, et al. (2006) Multiple distinct assemblies reveal conformational fl exibility in the small heat shock protein Hsp26. Structure 14(7):1197-1204. (Pubitemid 44037428)
22. Laskowska E, Wawrzynów A, Taylor A (1996) IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78(2):117-122. (Pubitemid 26260836)
23. Allen SP, Polazzi JO, Gierse JK, Easton AM (1992) Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J Bacteriol 174(21):6938-6947.
24. Matuszewska M, Kuczyńska-Wiśnik D, Laskowska E, Liberek K (2005) 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 280(13):12292-12298.
25. KitagawaM, Miyakawa M, Matsumura Y, Tsuchido T (2002) Escherichia coli small heat shock proteins, IbpA and IbpB, protect enzymes from inactivation by heat and oxidants. Eur J Biochem 269(12):2907-2917. (Pubitemid 34754019)
26. Ratajczak E, et al. (2010) IbpA the small heat shock protein from Escherichia coli forms fibrils in the absence of its cochaperone IbpB. FEBS Lett 584(11):2253-2257.
27. Shearstone JR, Baneyx F (1999) Biochemical characterization of the small heat shock protein IbpB from Escherichia coli. J Biol Chem 274(15):9937-9945.
28. Richmond CS, Glasner JD, Mau R, Jin H, Blattner FR (1999) Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res 27(19):3821-3835. (Pubitemid 29454430)
29. Ratajczak E, Zietkiewicz S, Liberek K (2009) Distinct activities of Escherichia coli small heat shock proteins IbpA and IbpB promote efficient protein disaggregation. J Mol Biol 386(1):178-189.
30. Heinz K, Marx A (2007) Lesion bypass activity of DNA polymerase A from the extremely radioresistant organism Deinococcus radiodurans. J Biol Chem 282(15):10908-10914. (Pubitemid 47100733)
31. Battista JR (1997) Against all odds: The survival strategies of Deinococcus radiodurans. Annu Rev Microbiol 51:203-224.
32. Airo A, Chan SL, Martinez Z, Platt MO, Trent JD (2004) Heat shock and cold shock in Deinococcus radiodurans. Cell Biochem Biophys 40(3):277-288.
33. Stromer T, Fischer E, Richter K, Haslbeck M, Buchner J (2004) Analysis of the regulation of the molecular chaperone Hsp26 by temperature-induced dissociation: The Nterminal domail is important for oligomer assembly and the binding of unfolding proteins. J Biol Chem 279(12):11222-11228. (Pubitemid 38401617)
34. Friedrich KL, Giese KC, Buan NR, Vierling E (2004) Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes. J Biol Chem 279(2):1080-1089. (Pubitemid 38082629)
35. Haslbeck M, et al. (1999) Hsp26: A temperature-regulated chaperone. EMBO J 18(23):6744-6751.
36. Stromer T, Ehrnsperger M, Gaestel M, Buchner J (2003) Analysis of the interaction of small heat shock proteins with unfolding proteins. J Biol Chem 278(20):18015-18021. (Pubitemid 36799411)
37. Buchner J, Grallert H, Jakob U (1998) Analysis of chaperone function using citrate synthase as nonnative substrate protein. Methods Enzymol 290:323-338. (Pubitemid 28157761)
38. Haslbeck M, et al. (2004) Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J 23(3):638-649. (Pubitemid 38282395)
39. Reddy GB, Das KP, Petrash JM, Surewicz WK (2000) Temperature-dependent chaperone activity and structural properties of human alphaA- and alphaB-crystallins. J Biol Chem 275(7):4565-4570. (Pubitemid 30108838)
40. Lee GJ, Pokala N, Vierling E (1995) Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270(18):10432-10438.
41. Hilario E, Martin FJ, Bertolini MC, Fan L (2011) Crystal structures of Xanthomonas small heat shock protein provide a structural basis for an active molecular chaperone oligomer. J Mol Biol 408(1):74-86.
42. Lin CH, et al. (2010) Characterization of Xanthomonas campestris pv. campestris heat shock protein A (HspA), which possesses an intrinsic ability to reactivate inactivated proteins. Appl Microbiol Biotechnol 88(3):699-709.
43. Padrick SB, et al. (2010) Determination of protein complex stoichiometry through multisignal sedimentation velocity experiments. Anal Biochem 407(1):89-103.
44. Basha E, et al. (2004) 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 279(9):7566-7575. (Pubitemid 38294635)
45. Takeda K, et al. (2011) Dimer structure and conformational variability in the N-terminal region of an archaeal small heat shock protein, StHsp14.0. J Struct Biol 174(1):92-99.
46. Saji H, et al. (2008) 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 71(2):771-782. (Pubitemid 351430015)
47. Bukach OV, Glukhova AE, Seit-Nebi AS, Gusev NB (2009) Heterooligomeric complexes formed by human small heat shock proteins HspB1 (Hsp27) and HspB6 (Hsp20). Biochim Biophys Acta 1794(3):486-495.
48. Bukach OV, Seit-Nebi AS, Marston SB, Gusev NB (2004) Some properties of human small heat shock protein Hsp20 (HspB6). Eur J Biochem 271(2):291-302. (Pubitemid 38130457)
49. Hayes D, Napoli V, Mazurkie A, Stafford WF, Graceffa P (2009) Phosphorylation dependence of hsp27 multimeric size and molecular chaperone function. J Biol Chem 284(28):18801-18807.
50. Haslbeck M, Schuster I, Grallert H (2003) GroE-dependent expression and purification of pig heart mitochondrial citrate synthase in Escherichia coli. J Chromatogr B Analyt Technol Biomed Life Sci 786(1-2):127-136. (Pubitemid 36324568)
51. Mossessova E, Lima CD (2000) Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell 5(5):865-876.
52. Brookes E, Cao W, Demeler B (2010) A two-dimensional spectrum analysis for sedimentation velocity experiments of mixtures with heterogeneity in molecular weight and shape. Eur Biophys J 39(3):405-414.
53. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674. (Pubitemid 47080256)