Structural and functional diversity in the family of small heat shock proteins from the parasite Toxoplasma gondii

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 11, 2009, Pages 1738-1748

  de Miguel, Natalia ^a   Braun, Nathalie ^b   Bepperling, Alexander ^b   Kriehuber, Thomas ^b   Kastenmüller, Andreas ^b   Buchner, Johannes ^b   Angel, Sergio O ^a   Haslbeck, Martin ^b  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

crystallin; Protein aggregation; Protein folding; sHsp; Toxoplasma gondii

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 20; HEAT SHOCK PROTEIN 21; HEAT SHOCK PROTEIN 28; HEAT SHOCK PROTEIN 29; HEAT SHOCK PROTEIN 30; OLIGOMER; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; GEL PERMEATION CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; INTRACELLULAR SPACE; LIFE CYCLE; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMOREGULATION; TOXOPLASMA GONDII;

AMINO ACID MOTIFS; ANIMALS; HEAT-SHOCK PROTEINS, SMALL; PHYLOGENY; PROTEIN STRUCTURE, QUATERNARY; PROTOZOAN PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TOXOPLASMA;

PROTISTA; TOXOPLASMA GONDII;

EID: 71749096555     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.08.005     Document Type: Article

References (69)

1. Haslbeck M., Franzmann T., Weinfurtner D., and Buchner J. Some like it hot: the structure and function of small heat-shock proteins. Nat. Struct. Mol. Biol. 12 (2005) 842-846
2. Haley D.A., Horwitz J., and Stewart P.L. The small heat-shock protein, alphaB-crystallin, has a variable quaternary structure. J. Mol. Biol. 277 (1998) 27-35
3. Haslbeck M., Walke S., Stromer T., Ehrnsperger M., White H.E., Chen S., Saibil H.R., and Buchner J. Hsp26: a temperature-regulated chaperone. EMBO J. 18 (1999) 6744-6751
4. Kim K.K., Kim R., and Kim S.H. Crystal structure of a small heat-shock protein. Nature 394 (1998) 595-599
5. Stromer T., Fischer E., Richter K., Haslbeck M., and 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. 279 (2004) 11222-11228
6. Kennaway C.K., Benesch J.L., Gohlke U., Wang L., Robinson C.V., Orlova E.V., Saibil H.R., and Keep N.H. Dodecameric structure of the small heat shock protein Acr1 from Mycobacterium tuberculosis. J. Biol. Chem. 280 (2005) 33419-33425
7. Haslbeck M., Kastenmuller A., Buchner J., Weinkauf S., and Braun N. Structural dynamics of archaeal small heat shock proteins. J. Mol. Biol. 378 (2008) 362-374
8. Kim K.K., Kim R., and Kim S.H. Crystal structure of a small heat-shock protein. Nature 394 (1998) 595-599
9. Aquilina J.A., Benesch J.L., Ding L.L., Yaron O., Horwitz J., and Robinson C.V. Subunit exchange of polydisperse proteins: mass spectrometry reveals consequences of alphaA-crystallin truncation. J. Biol. Chem. 280 (2005) 14485-14491
10. Franzmann T.M., Wuhr M., Richter K., Walter S., and Buchner J. The activation mechanism of Hsp26 does not require dissociation of the oligomer. J. Mol. Biol. 350 (2005) 1083-1093
11. White H.E., Orlova E.V., Chen S.X., Wang L.C., Ignatiou A., Gowen B., Stromer T., Franzmann T.M., Haslbeck M., Buchner J., and Saibil H.R. Multiple distinct assemblies reveal conformational flexibility in the small heat shock protein Hsp26. Structure 14 (2006) 1197-1204
12. Franzmann T.M., Menhorn P., Walter S., and Buchner J. Activation of the chaperone Hsp26 is controlled by the rearrangement of its thermosensor domain. Mol. Cell 29 (2008) 207-216
13. Ehrnsperger M., Graber S., Gaestel M., and Buchner J. Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16 (1997) 221-229
14. Lee G.J., and Vierling E. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122 (2000) 189-198
15. Haslbeck M., Miess A., Stromer T., Walter S., and Buchner J. Disassembling protein aggregates in the yeast cytosol: the cooperation of Hsp26 with Ssa1 and Hsp104. J. Biol. Chem. 280 (2005) 23869-23875
16. Cashikar A.G., Duennwald M.L., and Lindquist S.L. A chaperone pathway in protein disaggregation: Hsp26 alters the nature of protein aggregates to facilitate reactivation by Hsp104. J. Biol. Chem. 280 (2005) 23869-23875
17. Liberek K., Lewandowska A., and Zietkiewicz S. Chaperones in control of protein disaggregation. EMBO J. 27 (2008) 328-335
18. de Jong W.W., Caspers G.J., and Leunissen J.A. Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int. J. Biol. Macromol. 22 (1998) 151-162
19. Bellyei S., Szigeti A., Pozsgai E., Boronkai A., Gomori E., Hocsak E., Farkas R., Sumegi B., and Gallyas Jr. F. Preventing apoptotic cell death by a novel small shock protein. Eur. J. Cell Biol. 86 (2007) 161-171
20. Vos M.J., Hageman J., Carra S., and Kampinga H.H. Structural and functional diversities between members of the human HSPB, HSPH, HSPA and DNAJ chaperone families. Biochemistry 47 (2008) 7001-7011
21. Ramelot T.A., Raman E., Kuzin A.P., Xiao R., Ma L., Acton T.B., Hunt J.F., Montelione G.T., Baker D., and Kennedy M.A. Improving NMR protein structure quality by Rosetta refinement: a molecular replacement study. Proteins 45 (2009) 147-167
22. de Miguel N., Echeverria P.C., and Angel S.O. Differential subcellular localization of members of the Toxoplasma gondii small heat shock protein family. Eukaryot. Cell 4 (2005) 1990-1997
23. Tenter A.M., Heckeroth A.R., and Weiss L.M. Toxoplasma gondii: from animals to humans (vol 30, pg 1217, 2000). Int. J. Parasitol. 31 (2001) 217-220
24. Soete M., Fortier B., Camus D., and Dubremetz J.F. Toxoplasma-gondii - kinetics of bradyzoite-tachyzoite interconversion in vitro. Exp. Parasitol. 76 (1993) 259-264
25. Dubey J.P., Miller N.L., and Frenkel J.K. Toxoplasma gondii life cycle in cats. J. Am. Vet. Med. Assoc. 157 (1970) 1767-1770
26. Lyons R.E., McLeod R., and Roberts C.W. Toxoplasma gondii tachyzoite-bradyzoite interconversion. Trends Parasitol. 18 (2002) 198-201
27. Weiss L.M., Laplace D., Takvorian P., Tanowitz H.B., and Wittner M. The association of the stress response and Toxoplasma gondii bradyzoite development. J. Eukaryot. Microbiol. 43 (1996) 120S
28. Echeverria P.C., Matrajt M., Harb O.S., Zappia M.P., Costas M.A., Roos D.S., Dubremetz J.F., and Angel S.O. Toxoplasma gondii Hsp90 is a potential drug target whose expression and subcellular localization are developmentally regulated. J. Mol. Biol. 350 (2005) 723-734
29. Toursel C., Dzierszinski F., Bernigaud A., Mortuaire M., and Tomavo S. Molecular cloning, organellar targeting and developmental expression of mitochondrial chaperone HSP60 in Toxoplasma gondii. Mol. Biochem. Parasitol. 111 (2000) 319-332
30. Weiss L.M., Ma Y.F., Takvorian P.M., Tanowitz H.B., and Wittner M. Bradyzoite development in Toxoplasma gondii and the hsp70 stress response. Infect. Immun. 66 (1998) 3295-3302
31. Bohne W., Gross U., Ferguson D.J., and Heesemann J. Cloning and characterization of a bradyzoite-specifically expressed gene (hsp30/bag1) of Toxoplasma gondii, related to genes encoding small heat-shock proteins of plants. Mol. Microbiol. 16 (1995) 1221-1230
32. Parmley S.F., Weiss L.M., and Yang S. Cloning of a bradyzoite-specific gene of Toxoplasma gondii encoding a cytoplasmic antigen. Mol. Biochem. Parasitol. 73 (1995) 253-257
33. de Miguel N., Lebrun M., Heaslip A., Hu K., Beckers C.J., Matrajt M., Dubremetz J.F., and Angel S.O. Toxoplasma gondii Hsp20 is a stripe-arranged chaperone-like protein associated with the outer leaflet of the inner membrane complex. Biol. Cell 100 (2008) 479-489
34. Haslbeck M., Schuster I., and Grallert H. GroE-dependent expression and purification of pig heart mitochondrial citrate synthase in Escherichia coli. J. Chromatogr., B, Anal. Technol. Biomed. Life Sci. 786 (2003) 127-136
35. Thompson J.D., Higgins D.G., and Gibson T.J. Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
36. Wernersson R., and Pedersen A.G. RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31 (2003) 3537-3539
37. Goloboff P.A. Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15 (1999) 415-428
38. Buchner J., Grallert H., and Jakob U. Analysis of chaperone function using citrate synthase as nonnative substrate protein. Methods Enzymol. 290 (1998) 323-338
39. Srere P.A. Citrate-condensing enzyme-oxalacetate binary complex. Studies on its physical and chemical properties. J. Biol. Chem. 241 (1966) 2157-2165
40. Bova M.P., Huang Q., Ding L., and Horwitz J. Subunit exchange, conformational stability, and chaperone-like function of the small heat shock protein 16.5 from Methanococcus jannaschii. J. Biol. Chem. 277 (2002) 38468-38475
41. Kappe G., Leunissen J.A., and De Jong W.W. Evolution and diversity of prokaryotic small heat shock proteins. Prog. Mol. Subcell. Biol. 28 (2002) 1-17
42. Waters E.R., Lee G.J., and Vierling E. Evolution, structure and function of the small heat shock proteins in plants. J. Exp. Bot. 47 (1996) 325-338
43. van Montfort R.L., Basha E., Friedrich K.L., Slingsby C., and Vierling E. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct. Biol. 8 (2001) 1025-1030
44. Haslbeck M. Recombinant expression and in vitro refolding of the yeast small heat shock protein Hsp42. Int. J. Biol. Macromol. 38 (2006) 107-114
45. Haslbeck M., Braun N., Stromer T., Richter B., Model N., Weinkauf S., and Buchner J. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J. 23 (2004) 638-649
46. Haslbeck M., Ignatiou A., Saibil H., Helmich S., Frenzl E., Stromer T., and Buchner J. A domain in the N-terminal part of Hsp26 is essential for chaperone function and oligomerization. J. Mol. Biol. 343 (2004) 445-455
47. Dudich I.V., Zav'yalov V.P., Pfeil W., Gaestel M., Zav'yalova G.A., Denesyuk A.I., and Korpela T. Dimer structure as a minimum cooperative subunit of small heat-shock proteins. Biochim. Biophys. Acta 1253 (1995) 163-168
48. Peschek J., Braun N., Franzmann T.M., Georgalis Y., Haslbeck M., Weinkauf S., and Buchner J. The eye lens chaperone a-crystallin forms defined globular assemblies. Proc. Natl. Acad. Sci. USA (2009) (Electronic publication ahead of print)
49. Shashidharamurthy R., Koteiche H.A., Dong J., and Mchaourab H.S. Mechanism of chaperone function in small heat shock proteins: dissociation of the HSP27 oligomer is required for recognition and binding of destabilized T4 lysozyme. J. Biol. Chem. 280 (2005) 5281-5289
50. Basha E., Lee G.J., Demeler B., and Vierling E. Chaperone activity of cytosolic small heat shock proteins from wheat. Eur. J. Biol. 271 (2004) 1426-1436
51. Haslbeck M., Walke S., Stromer T., Ehrnsperger M., White H.E., Chen S.X., Saibil H.R., and Buchner J. Hsp26: a temperature-regulated chaperone. EMBO J. 18 (1999) 6744-6751
52. Franzmann T.M., Wühr M., Richter K., Walter S., and Buchner J. The activation mechanism of Hsp26 involves structural changes within the oligomer. Dissociation is not required. J. Mol. Biol. 350 (2005) 1083-1093
53. Haslbeck M., and Buchner J. Chaperone function of sHsps. Prog. Mol. Subcell. Biol. 28 (2002) 37-59
54. Van Montfort R., Slingsby C., and Vierling E. Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. Adv. Protein Chem. 59 (2002) 105-156
55. Narberhaus F. Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev. 66 (2002) 64-93
56. Horwitz J. Alpha-crystallin. Exp. Eye Res. 76 (2003) 145-153
57. Ehrnsperger M., Lilie H., Gaestel M., and Buchner J. The dynamics of Hsp25 quaternary structure. Structure and function of different oligomeric species. J. Biol. Chem. 274 (1999) 14867-14874
58. Lee G.J., Roseman A.M., Saibil H.R., and 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. 16 (1997) 659-671
59. Studer S., and Narberhaus F. Chaperone activity and homo- and hetero-oligomer formation of bacterial small heat shock proteins. J. Biol. Chem. 275 (2000) 37212-37218
60. Morrow G., Heikkila J.J., and Tanguay R.M. Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster. Cell Stress Chaperones 11 (2006) 51-60
61. Stromer T., Ehrnsperger M., Gaestel M., and Buchner J. Analysis of the interaction of small heat shock proteins with unfolding proteins. J. Biol. Chem. 278 (2003) 18015-18021
62. Sobott F., Benesch J.L., Vierling E., and Robinson C.V. Subunit exchange of multimeric protein complexes. Real-time monitoring of subunit exchange between small heat shock proteins by using electrospray mass spectrometry. J. Biol. Chem. 277 (2002) 38921-38929
63. Lentze N., Aquilina J.A., Lindbauer M., Robinson C.V., and Narberhaus F. Temperature and concentration-controlled dynamics of rhizobial small heat shock proteins. Eur. J. Biochem. 271 (2004) 2494-2503
64. Bova M.P., Mchaourab H.S., Han Y., and Fung B.K.K. Subunit exchange of small heat shock proteins - analysis of oligomer formation of alpha A-crystallin and Hsp27 by fluorescence resonance energy transfer and site-directed truncations. J. Biol. Chem. 275 (2000) 1035-1042
65. Zhang Y.W., Kim K., Ma Y.F., Wittner M., Tanowitz H.B., and Weiss L.M. Disruption of the Toxoplasma gondii bradyzoite-specific gene BAG1 decreases in vivo cyst formation. Mol. Microbiol. 31 (1999) 691-701
66. Bohne W., Hunter C.A., White M.W., Ferguson D.J., Gross U., and Roos D.S. Targeted disruption of the bradyzoite-specific gene BAG1 does not prevent tissue cyst formation in Toxoplasma gondii. Mol. Biochem. Parasitol. 92 (1998) 291-301
67. Sugino C., Hirose M., Tohda H., Yoshinari Y., Abe T., Giga-Hama Y., Iizuka R., Shimizu M., Kidokoro S.I., Ishii N., and Yohda M. Characterization of a sHsp of Schizosaccharomyces pombe, SpHsp15.8, and the implication of its functional mechanism by comparison with another sHsp, SpHsp16.0. Proteins 74 (2008) 6-17
68. Rinehart J.P., Li A., Yocum G.D., Robich R.M., Hayward S.A., and Denlinger D.L. Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc. Natl. Acad. Sci. USA 104 (2007) 11130-11137
69. Roobol A., Carden M.J., Newsam R.J., and Smales C.M. Biochemical insights into the mechanisms central to the response of mammalian cells to cold stress and subsequent rewarming. FEBS J. 276 (2008) 286-302