An unusual dimeric small heat shock protein provides insight into the mechanism of this class of chaperones

Journal of Molecular Biology

Volumn 425, Issue 10, 2013, Pages 1683-1696

  Basha, Eman ^a,b   Jones, Christopher ^a   Blackwell, Anne E ^a   Cheng, Guilong ^a   Waters, Elizabeth R ^c   Samsel, Kara A ^a   Siddique, Masood ^d   Pett, Virginia ^e   Wysocki, Vicki ^a   Vierling, Elizabeth ^f  

^a University of Arizona   (United States)

^b TANTA UNIVERSITY   (Egypt)

^c SAN DIEGO STATE UNIVERSITY   (United States)

^d GOETHE UNIVERSITY   (Germany)

^e 931 College Mall   (United States)

^f UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

chaperone; hydrogen deuterium exchange; protein flexibility; subunit exchange; crystallin domain

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90; MESSENGER RNA; MONOMER; OLIGOMER; VEGETABLE PROTEIN;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS THALIANA; ARTICLE; BIOLOGICAL ACTIVITY; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; HYDROPHOBICITY; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE;

ARABIDOPSIS THALIANA;

EID: 84877577000     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.02.011     Document Type: Article

References (59)

1. R. van Montfort, C. Slingsby, and E. Vierling Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones Adv. Protein Chem. 59 2001 105 156
2. H.S. McHaourab, J.A. Godar, and P.L. Stewart Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins Biochemistry 48 2009 3828 3837
3. E. Basha, H. O'Neill, and E. Vierling Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions Trends Biochem. Sci. 37 2012 106 117
4. M.V. Sudnitsyna, E.V. Mymrikov, A.S. Seit-Nebi, and N.B. Gusev The role of intrinsically disordered regions in the structure and functioning of small heat shock proteins Curr. Protein Pept. Sci. 13 2012 76 85
5. J.I. Clark, and P.J. Muchowski Small heat-shock proteins and their potential role in human disease Curr. Opin. Struct. Biol. 10 2000 52 59
6. M.J. Vos, J. Hageman, S. Carra, and H.H. Kampinga Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families Biochemistry 47 2008 7001 7011
7. E.V. Mymrikov, A.S. Seit-Nebi, and N.B. Gusev Large potentials of small heat shock proteins Physiol. Rev. 91 2011 1123 1159
8. T. Kriehuber, T. Rattei, T. Weinmaier, A. Bepperling, M. Haslbeck, and J. Buchner Independent evolution of the core domain and its flanking sequences in small heat shock proteins FASEB J. 24 2010 3633 3642
9. R.L. van Montfort, E. Basha, K.L. Friedrich, C. Slingsby, and E. Vierling Crystal structure and assembly of a eukaryotic small heat shock protein Nat. Struct. Biol. 8 2001 1025 1030
10. K.K. Kim, R. Kim, and S.H. Kim Crystal structure of a small heat-shock protein Nature 394 1998 595 599
11. S. Jehle, P. Rajagopal, B. Bardiaux, S. Markovic, R. Kuhne, and J.R. Stout Solid-state NMR and SAXS studies provide a structural basis for the activation of αB-crystallin oligomers Nat. Struct. Mol. Biol. 17 2010 1037 1042
12. C. Bagneris, O.A. Bateman, C.E. Naylor, N. Cronin, W.C. Boelens, N.H. Keep, and C. Slingsby Crystal structures of α-crystallin domain dimers of αB-crystallin and Hsp20 J. Mol. Biol. 392 2009 1242 1252
13. A. Laganowsky, and D. Eisenberg Non-3D domain swapped crystal structure of truncated zebrafish αA crystallin Protein Sci. 19 2010 1978 1984
14. G.J. Lee, A.M. Roseman, H.R. Saibil, and E. Vierling 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
15. M. Haslbeck, S. Walke, T. Stromer, M. Ehrnsperger, H.E. White, and S. Chen Hsp26: a temperature-regulated chaperone EMBO J. 18 1999 6744 6751
16. R. Shashidharamurthy, H.A. Koteiche, J. Dong, and H.S. McHaourab 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
17. T.M. Franzmann, P. Menhorn, S. Walter, and J. Buchner Activation of the chaperone Hsp26 is controlled by the rearrangement of its thermosensor domain Mol. Cell 29 2008 207 216
18. E. Basha, K.L. Friedrich, and E. Vierling The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity J. Biol. Chem. 281 2006 39943 39952
19. A. Mogk, C. Schlieker, K.L. Friedrich, H.J. Schonfeld, E. Vierling, and B. Bukau Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK J. Biol. Chem. 278 2003 31033 31042
20. K.L. Friedrich, K.C. Giese, N.R. Buan, and E. Vierling Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes J. Biol. Chem. 279 2004 1080 1089
21. G. Cheng, E. Basha, V.H. Wysocki, and E. Vierling Insights into small heat shock protein and substrate structure during chaperone action derived from hydrogen/deuterium exchange and mass spectrometry J. Biol. Chem. 283 2008 26634 26642
22. F. Stengel, A.J. Baldwin, M.F. Bush, G.R. Hilton, H. Lioe, and E. Basha Dissecting heterogeneous molecular chaperone complexes using a mass spectrum deconvolution approach Chem. Biol. 19 2012 599 607
23. G.J. Lee, and E. Vierling A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein Plant Physiol. 122 2000 189 198
24. A. Mogk, E. Deuerling, S. Vorderwulbecke, E. Vierling, and B. Bukau Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation Mol. Microbiol. 50 2003 585 595
25. M. Haslbeck, A. Miess, T. Stromer, S. Walter, and J. Buchner Disassembling protein aggregates in the yeast cytosol. The cooperation of Hsp26 with Ssa1 and Hsp104 J. Biol. Chem. 280 2005 23861 23868
26. E. Basha, C. Jones, V. Wysocki, and E. Vierling Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol J. Biol. Chem. 285 2010 11489 11497
27. M. Kundu, P.C. Sen, and K.P. Das Structure, stability, and chaperone function of αA-crystallin: role of N-terminal region Biopolymers 86 2007 177 192
28. L. Liu, J.G. Ghosh, J.I. Clark, and S. Jiang Studies of αB crystallin subunit dynamics by surface plasmon resonance Anal. Biochem. 350 2006 186 195
29. K.C. Giese, E. Basha, B.Y. Catague, and E. Vierling Evidence for an essential function of the N terminus of a small heat shock protein in vivo, independent of in vitro chaperone activity Proc. Natl Acad. Sci. USA 102 2005 18896 18901
30. M. Haslbeck, A. Ignatiou, H. Saibil, S. Helmich, E. Frenzl, T. Stromer, and J. Buchner A domain in the N-terminal part of Hsp26 is essential for chaperone function and oligomerization J. Mol. Biol. 343 2004 445 455
31. N. Jaya, V. Garcia, and E. Vierling Substrate binding site flexibility of the small heat shock protein molecular chaperones Proc. Natl Acad. Sci. USA 106 2009 15604 15609
32. P. Poulain, J.C. Gelly, and D. Flatters Detection and architecture of small heat shock protein monomers PLoS One 5 2010 e9990
33. M. Siddique, S. Gernhard, P. von Koskull-Doring, E. Vierling, and K.D. Scharf The plant sHSP superfamily: five new members in Arabidopsis thaliana with unexpected properties Cell Stress Chaperones 13 2008 183 197
34. S. Jehle, B. van Rossum, J.R. Stout, S.M. Noguchi, K. Falber, and K. Rehbein αB-Crystallin: a hybrid solid-state/solution-state NMR investigation reveals structural aspects of the heterogeneous oligomer J. Mol. Biol. 385 2009 1481 1497
35. G.J. Lee, N. Pokala, and E. Vierling Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea J. Biol. Chem. 270 1995 10432 10438
36. A.J. Painter, N. Jaya, E. Basha, E. Vierling, C.V. Robinson, and J.L. Benesch Real-time monitoring of protein complexes reveals their quaternary organization and dynamics Chem. Biol. 15 2008 246 253
37. F. Sobott, J.L. Benesch, E. Vierling, and C.V. Robinson 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
38. A.S. Galhena, S. Dagan, C.M. Jones, R.L. Beardsley, and V.H. Wysocki Surface-induced dissociation of peptides and protein complexes in a quadrupole/time-of-flight mass spectrometer Anal. Chem. 80 2008 1425 1436
39. F. Stengel, A.J. Baldwin, A.J. Painter, N. Jaya, E. Basha, and L.E. Kay Quaternary dynamics and plasticity underlie small heat shock protein chaperone function Proc. Natl Acad. Sci. USA 107 2010 2007 2012
40. P.L. Wintrode, K.L. Friedrich, E. Vierling, J.B. Smith, and D.L. Smith Solution structure and dynamics of a heat shock protein assembly probed by hydrogen exchange and mass spectrometry Biochemistry 42 2003 10667 10673
41. O.V. Bukach, A.S. Seit-Nebi, S.B. Marston, and N.B. Gusev Some properties of human small heat shock protein Hsp20 (HspB6) Eur. J. Biochem. 271 2004 291 302
42. F.A. van de Klundert, R.H. Smulders, M.L. Gijsen, R.A. Lindner, R. Jaenicke, J.A. Carver, and W.W. de Jong The mammalian small heat-shock protein Hsp20 forms dimers and is a poor chaperone Eur. J. Biochem. 258 1998 1014 1021
43. M.R. Leroux, B.J. Ma, G. Batelier, R. Melki, and E.P. Candido Unique structural features of a novel class of small heat shock proteins J. Biol. Chem. 272 1997 12847 12853
44. B.P. Kokke, M.R. Leroux, E.P. Candido, W.C. Boelens, and W.W. de Jong Caenorhabditis elegans small heat-shock proteins Hsp12.2 and Hsp12.3 form tetramers and have no chaperone-like activity FEBS Lett. 433 1998 228 232
45. B.P. Kokke, W.C. Boelens, and W.W. de Jong The lack of chaperonelike activity of Caenorhabditis elegans Hsp12.2 cannot be restored by domain swapping with human αB-crystallin Cell Stress Chaperones 6 2001 360 367
46. R. Stamler, G. Kappe, W. Boelens, and C. Slingsby Wrapping the α-crystallin domain fold in a chaperone assembly J. Mol. Biol. 353 2005 68 79
47. A. Laganowsky, J.L. Benesch, M. Landau, L. Ding, M.R. Sawaya, and D. Cascio Crystal structures of truncated αA and αB crystallins reveal structural mechanisms of polydispersity important for eye lens function Protein Sci. 19 2010 1031 1043
48. I.K. Feil, M. Malfois, J. Hendle, H. van Der Zandt, and D.I. Svergun A novel quaternary structure of the dimeric α-crystallin domain with chaperone-like activity J. Biol. Chem. 276 2001 12024 12029
49. X. Fu, H. Zhang, X. Zhang, Y. Cao, W. Jiao, and C. Liu 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 2005 6337 6348
50. W. Jiao, M. Qian, P. Li, L. Zhao, and Z. Chang The essential role of the flexible termini in the temperature-responsiveness of the oligomeric state and chaperone-like activity for the polydisperse small heat shock protein IbpB from Escherichia coli J. Mol. Biol. 347 2005 871 884
51. T. Stromer, E. Fischer, K. Richter, M. Haslbeck, and J. Buchner 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
52. A.R. Clark, C.E. Naylor, C. Bagneris, N.H. Keep, and C. Slingsby Crystal structure of R120G disease mutant of human αB-crystallin domain dimer shows closure of a groove J. Mol. Biol. 408 2011 118 134
53. A.J. Weaver, W.P. Sullivan, S.J. Felts, B.A. Owen, and D.O. Toft Crystal structure and activity of human p23, a heat shock protein 90 co-chaperone J. Biol. Chem. 275 2000 23045 23052
54. T.A. Hall BioEdit: a user-friendly biological sequence alignment editor and analysis program for WIndows 95/98/NT Nucleic Acids Symp. Ser. 41 1999 95 98
55. J.D. Thompson, T.J. Gibson, F. Plewniak, F. Jeanmougin, and D.G. Higgins The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res. 25 1997 4876 4882
56. M. Swamy, G.M. Siegers, S. Minguet, B. Wollscheid, and W.W.A. Schamel Blue native polyacrylamide gel electrophoresis (BN-PAGE) for the identification and analysis of multiprotein complexes Sci. STKE 2006 2006 pl4
57. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78 2000 1606 1619
58. J.C. Jurchen, and E.R. Williams Origin of asymmetric charge partitioning in the dissociation of gas-phase protein homodimers J. Am. Chem. Soc. 125 2003 2817 2826
59. H. Hernandez, and C.V. Robinson Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry Nat. Protoc. 2 2007 715 726