Structural and functional roles for β-strand 7 in the α-crystallin domain of p26, a polydisperse small heat shock protein from Artemia franciscana

FEBS Journal

Volumn 273, Issue 5, 2006, Pages 1020-1034

  Sun, Yu ^a   Bojikova Fournier, Svetla ^a   MacRae, Thomas H ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

crystallin domain; Artemia franciscana; Molecular chaperone; p26 structure function; Small heat shock protein

Indexed keywords

ALPHA CRYSTALLIN; AMINO ACID; CHAPERONE; DIMER; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN P26; TETRAMER; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTEMIA; ARTEMIA FRANCISCANA; ARTICLE; BACTERIUM TRANSFORMATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CRYSTALLIZATION; DIAPAUSE; EMBRYO; FLUORESCENCE; HEAT TOLERANCE; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; MEASUREMENT; MOLECULAR MODEL; MOLECULAR PHYSICS; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTECTION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN VARIANT; SITE DIRECTED MUTAGENESIS; STRESS; SURFACE CHARGE; SURFACE PROPERTY; WHEAT; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ARTEMIA; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; COS CELLS; DNA, COMPLEMENTARY; FEMALE; HEAT-SHOCK PROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; ARTEMIA; ARTEMIA FRANCISCANA; BACTERIA (MICROORGANISMS); CRUSTACEA; TRITICUM AESTIVUM;

EID: 33644933681     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05129.x     Document Type: Article

References (77)

1. Frydman J 2001 Folding of newly translated proteins in vivo: the role of molecular chaperones Annu Rev Biochem 70 603 647
2. Hartl FU Hayer-Hartl M 2002 Molecular chaperones in the cytosol: from nascent chain to folded protein Science 295 1852 1858
3. Haslbeck M 2002 sHSPS and their role in the chaperone network Cell Mol Life Sci 59 1649 1657
4. Craig EA 2003 Eukaryotic chaperonins: Lubricating the folding of WD-repeat proteins Curr Biol 13 R904 R905
5. Mogk A Bukau B 2004 Molecular chaperones: Structure of a protein disaggregase Curr Biol 14 R78 R80
6. Petrucelli L Dickson D Kehoe K Taylor J Snyder H Grover A De Lucia M McGowan E Lewis J Prihar G et al. 2004 CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation Hum Mol Genet 13 703 714
7. MacRae TH 2000 Structure and function of small heat shock/α- crystallin proteins: established concepts and emerging ideas Cell Mol Life Sci 57 899 913
8. Scharf K-D Siddique M Vierling E 2001 The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins) Cell Stress Chaperones 6 225 237
9. Narberhaus F 2002 α-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network Microbiol Mol Biol Rev 66 64 93
10. Sun W Van Montagu M Verbruggen N 2002 Small heat shock proteins and stress tolerance in plants Biochim Biophys Acta 1577 1 9
11. Horwitz J 2003 Alpha-crystallin Exp Eye Res 76 145 153
12. Laksanalamai P Robb FT 2004 Small heat shock proteins from extremophiles: a review Extremophiles 8 1 11
13. Taylor RP Benjamin IJ 2005 Small heat shock proteins: a new classification scheme in mammals J Mol Cell Cardiol 38 433 444
14. van Montfort RLM Basha E Friedrich KL Slingsby C Vierling E 2001 Crystal structure and assembly of a eukaryotic small heat shock protein Nat Struct Biol 8 1025 1030
15. Koteiche HA Mchaourab HS 2002 The determinants of the oligomeric structure in Hsp16.5 are encoded in the α-crystallin domain FEBS Lett 519 16 22
16. Kim KK Kim R Kim S-H 1998 Crystal structure of a small heat-shock protein Nature 394 595 599
17. Sun Y Mansour M Crack JA Gass GL MacRae TH 2004 Oligomerization, chaperone activity, and nuclear localization of p26, a small heat shock protein from Artemia franciscana J Biol Chem 279 39999 40006
18. 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 N-terminal domain is important for oligomer assembly and the binding of unfolding proteins J Biol Chem 279 11222 11228
19. Wintrode PL Friedrich KL Vierling E Smith JB Smith DL 2003 Solution structure and dynamics of a heat shock protein assembly probed by hydrogen exchange and mass spectrometry Biochemistry 42 10667 10673
20. Salerno JC Eifert CL Salerno KM Koretz JF 2003 Structural diversity in the small heat shock protein superfamily: control of aggregation by the N-terminal region Prot Eng 16 847 851
21. Studer S Obrist M Lentze N Narberhaus F 2002 A critical motif for oligomerization and chaperone activity of bacterial α-heat shock proteins Eur J Biochem 269 3578 3586
22. Fu X Zhang H Zhang X Cao Y Jiao W Liu C Song Y Abulimiti A Chang Z 2005 A dual role for the N-terminal region of Mycobacterium tuberculosis Hsp16.3 in self-oligomerization and binding denaturing substrate proteins J Biol Chem 280 6337 6348
23. Hasan A Yu J Smith DL Smith JB 2004 Thermal stability of human α-crystallins sensed by amide hydrogen exchange Prot Sci 13 332 341
24. Thampi P Abraham EC 2003 Influence of the C-terminal residues on oligomerization of αA-crystallin Biochemistry 42 11857 11863
25. Lindner RA Carver JA Ehrnsperger M Buchner J Esposito G Behlke J Lutsch G Kotlyarov A Gaestel M 2000 Mouse Hsp25, a small shock protein. The role of its C-terminal extension in oligomerization and chaperone action Eur J Biochem 267 1923 1932
26. Haslbeck M Braun N Stromer T Richter B Model N Weinkauf S Buchner J 2004 Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae EMBO J 23 638 649
27. Haley DA Bova MP Huang QL Mchaourab HS Stewart PL 2000 Small heat-shock protein structures reveal a continuum from symmetric to variable assemblies J Mol Biol 298 261 272
28. Regini JW Grossmann JG Burgio MR Malik NS Koretz JF Hodson SA Elliott GF 2004 Structural changes in α-crystallin and whole eye lens during heating, observed by low-angle X-ray diffraction J Mol Biol 336 1185 1194
29. Benesch JL Sobott F Robinson CV 2003 Thermal dissociation of multimeric protein complexes by using nanoelectrospray mass spectrometry Anal Chem 75 2208 2214
30. Lentze N Studer S Narberhaus F 2003 Structural and functional defects caused by point mutations in the α-crystallin domain of a bacterial α-heat shock protein J Mol Biol 328 927 937
31. Franzmann TM Wühr M Richter K Walter S Buchner J 2005 The activation mechanism of Hsp26 does not require dissociation of the oligomer J Mol Biol 350 1083 1093
32. Basha E Lee GJ Breci LA Hausrath AC Buan NR Giese KC Vierling E 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 7566 7575
33. 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 1080 1089
34. Duverger O Paslaru L Morange M 2004 HSP25 is involved in two steps of the differentiation of PAM212 keratinocytes J Biol Chem 279 10252 10260
35. Day RM Gupta JS MacRae TH 2003 A small heat shock/αcrystallin protein from encysted Artemia embryos suppresses tubulin denaturation Cell Stress Chaperones 8 183 193
36. Panasenko OO Kim MV Marston SB Gusev NB 2003 Interaction of the small heat shock protein with molecular mass 25 kDa (hsp25) with actin Eur J Biochem 270 892 901
37. Arrigo A-P Firdaus WJ Mellier G Moulin M Paul C Diaz-Iatoud C Kretz-remy C 2005 Cytotoxic effects induced by oxidative stress in cultured mammalian cells and protection provided by Hsp27 expression Methods 35 126 138
38. Kamradt MC Lu M Werner ME Kwan T Chen F Strohecker A Oshita S Wilkinson JC Yu C Oliver PG et al. 2005 The small heat shock protein αB-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3 J Biol Chem 280 11059 11066
39. Mao Y-W Liu J-P Xiang H Li DW-C 2004 Human αA- and αB-crystallins bind to Bax and Bcl-XS to sequester their translocation during staurosporine-induced apoptosis Cell Death Differ 11 512 526
40. Concannon CG Gorman AM Samali A 2003 On the role of Hsp27 in regulating apoptosis Apoptosis 8 61 70
41. MacRae TH 2003 Molecular chaperones, stress resistance and development in Artemia franciscana Semin Cell Dev Biol 14 251 258
42. Clegg JS Willsie JK Jackson SA 1999 Adaptive significance of a small heat shock/α-crystallin protein (p26) in encysted embryos of the brine shrimp, Artemia franciscana Am Zool 39 836 847
43. Crack JA Mansour M Sun Y MacRae TH 2002 Functional analysis of a small heat shock/α-crystallin protein from Artemia franciscana. Oligomerization and thermotolerance Eur J Biochem 269 933 942
44. Liang P MacRae TH 1999 The synthesis of a small heat shock/α- crystallin protein in Artemia and its relationship to stress tolerance during development Dev Biol 207 445 456
45. Liang P Amons R MacRae TH Clegg JS 1997 Purification, structure and in vitro molecular-chaperone activity of Artemia p26, a small heat-shock/α- crystallin protein Eur J Biochem 243 225 232
46. Liang P Amons R Clegg JS MacRae TH 1997 Molecular characterization of a small heat shock/α-crystallin protein in encysted Artemia embryos J Biol Chem 272 19051 19058
47. Guruprasad K Kumari K 2003 Three-dimensional models corresponding to the C-terminal domain of human αA- and αB-crystallins based on the crystal structure of the small heat-shock protein HSP16.9 from wheat Int J Biol Macromol 33 107 112
48. Bova MP Yaron O Huang Q Ding L Haley DA Stewart PL Horwitz J 1999 Mutation R120G in αB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone-like function Proc Natl Acad Sci USA 96 6137 6142
49. Kumar LVS Ramakrishna T Rao ChM 1999 Structural and functional consequences of the mutation of a conserved arginine residue in αA and αB crystallins J Biol Chem 274 24137 24141
50. Perng MD Muchowski PJ van den IJssel P Wu GJS Hutcheson AM Clark JI Quinlan RA 1999 The cardiomyopathy and lens cataract mutation in αB-crystallin alters its protein structure, chaperone activity, and interaction with intermediate filaments in vitro J Biol Chem 274 33235 33243
51. Shroff NP Cherian-Shaw M Bera S Abraham EC 2000 Mutation of R116C results in highly oligomerized αA-crystallin with modified structure and defective chaperone-like function Biochemistry 39 1420 1426
52. Cobb BA Petrash JM 2000 Structural and functional changes in the αA-crystallin R116C mutant in hereditary cataracts Biochemistry 39 15791 15798
53. Andley UP Patel HC Xi J-H 2002 The R116C mutation in αA-crystallin diminishes its protective ability against stress-induced lens epithelial cell apoptosis J Biol Chem 277 10178 10186
54. Chávez Zobel AT Lambert H Thériault JR Landry J 2005 Structural instability caused by a mutation at a conserved arginine in the α-crystallin domain of Chinese hamster heat shock protein 27 Cell Stress Chaperones 10 157 166
55. Studer S Narberhaus F 2000 Chaperone activity and homo- and hetero-oligomer formation of bacterial small heat shock proteins J Biol Chem 275 37212 37218
56. Leroux MR Melki R Gordon B Batelier G Candido EPM 1997 Structure-function studies on small heat shock protein oligomeric assembly and interaction with unfolded polypeptides J Biol Chem 272 24646 24656
57. Valdez MM Clark JI Wu GJS Muchowski PJ 2002 Functional similarities between the small heat shock proteins Mycobacterium tuberculosis HSP 16.3 and human αB-crystallin Eur J Biochem 269 1806 1813
58. Lindner RA Kapur A Mariani M Titmuss SJ Carver JA 1998 Structural alterations of α-crystallin during its chaperone action Eur J Biochem 258 170 183
59. Berengian AR Bova MP Mchaourab HS 1997 Structure and function of the conserved domain in αA-crystallin. Site-directed spin labeling identifies a α-strand located near a subunit interface Biochemistry 36 9951 9957
60. Reddy GB Das KP Petrash JM Surewicz WK 2000 Temperature-dependent chaperone activity and structural properties of human αA- and αB-crystallins J Biol Chem 275 4565 4570
61. Zobel ATC Loranger A Marceau N Thériault JR Lambert H Landry J 2003 Distinct chaperone mechanisms can delay the formation of aggresomes by the myopathy-causing R120G αB-crystallin mutant Hum Mol Genet 12 1609 1620
62. Litt M Kramer P LaMorticella DM Murphey W Lovrien EW Weleber RG 1998 Autosomal dominant congenital cataract associated with a missense mutation in the human alpha crystallin gene CRYAA Hum Mol Genet 7 471 474
63. Vicart P Caron A Guicheney P Li Z Prevost M-C Faure A Chateau D Chapon F Tomé F Dupret J-M et al. 1998 A missense mutation in the αB-crystallin chaperone gene causes a desmin-related myopathy Nat Genet 20 92 95
64. Sanbe A Osinska H Saffitz JE Glabe CG Kayed R Maloyan A Robbins J 2004 Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis Proc Natl Acad Sci USA 101 10132 10136
65. Willsie JK Clegg JS 2001 Nuclear p26, a small heat shock/α- crystallin protein, and its relationship to stress resistance in Artemia franciscana embryos J Exp Biol 204 2339 2350
66. van de Klundert FAJM de Jong WW 1999 The small heat shock proteins Hsp20 and αB-crystallin in cultured cardiac myocytes: differences in cellular localization and solubilization after heat stress Eur J Cell Biol 78 567 572
67. van den IJssel P Wheelock R Prescott A Russell P Quinlan RA 2003 Nuclear speckle localisation of the small heat shock protein αB-crystallin and its inhibition by the R120G cardiomyopathy-linked mutation Exp Cell Res 287 249 261
68. Ito H Kamei K Iwamoto I Inaguma Y Tsuzuki M Kishikawa M Shimada A Hosokawa M Kato K 2003 Hsp27 suppresses the formation of inclusion bodies induced by expression of R120G αB-crystallin, a cause of desmin-related myopathy Cell Mol Life Sci 60 1217 1223
69. Siddique M Port M Tripp J Weber C Zielinski D Calligaris R Winkelhaus S Scharf K-D 2003 Tomato heat stress protein Hsp16.1-CIII represents a member of a new class of nucleocytoplasmic small heat stress proteins in plants Cell Stress Chaperones 8 381 394
70. Rajaraman K Raman B Ramakrishna T Rao CM 2001 Interaction of human recombinant αA- and αB-crystallins with early and late unfolding intermediates of citrate synthase on its thermal denaturation FEBS Lett 497 118 123
71. Jones DT 1999 Protein secondary structure prediction based on position-specific scoring matrices J Mol Biol 292 195 202
72. Sali A Blundell TL 1993 Comparative modeling by satisfaction of spatial restraints J Mol Biol 234 779 815
73. Eisenberg D Lüthy R Bowie JU 1997 VERIFY3D: assessment of protein models with three-dimensional profiles Methods Enzymol 277 396 404
74. Luthy R Bowie JU Eisenberg D 1992 Assessment of protein models with three-dimensional profiles Nature 356 83 85
75. Zhu J Weng Z 2005 FAST: a novel protein structure alignment algorithm Proteins 58 618 617
76. Laskowski RA MacArthur MW Moss DS Thornton JM 1993 PROCHECK: a program to check the stereochemical quality of protein structures J Appl Cryst 26 283 291
77. Humphrey W Dalke A Schulten K 1996 VMD - Visual Molecular Dynamics J Mol Graph Model 14 33 38