Insights into the domains required for dimerization and assembly of human αB crystallin

Protein Science

Volumn 14, Issue 3, 2005, Pages 684-695

  Ghosh, Joy G ^a   Clark, John I ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

B crystallin; Assembly; Chaperone; Lens; Molecular modeling; Small heat shock protein

Indexed keywords

ALPHA CRYSTALLIN; PROTEIN ALPHAA CRYSTALLIN; PROTEIN ALPHAB CRYSTALLIN; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ABSORPTION SPECTROPHOTOMETRY; ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME LINKED IMMUNOSORBENT ASSAY; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

ALPHA-CRYSTALLIN B CHAIN; AMINO ACID SEQUENCE; BRADYRHIZOBIUM; DIMERIZATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN ARRAY ANALYSIS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 14144255401     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041152805     Document Type: Article

References (70)

1. Aiyar, A. 2000. The use of CLUSTAL W and CLUSTAL X for multiple sequence alignment. Methods Mol. Biol. 132: 221-241.
2. Alizadeh, A., Clark, J., Seeberger, T., Hess, J., Blankenship, T., and FitzGerald, P.G. 2003. Targeted deletion of the lens fiber cell-specific intermediate filament protein filensin. Invest. Ophthalmol. Vis. Sci. 44: 5252-5258.
3. _. 2004. Characterization of a mutation in the lens-specific CP49 in the 129 strain of mouse. Invest. Ophthalmol. Vis. Sci. 45: 884-891.
4. Aquilina, J.A., Benesch, J.L., Ding, L.L., Yaron, O., Horwitz, J., and Robinson, C.V. 2004. Phosphorylation of αB-crystallin alters chaperone function through loss of dimeric substructure. J. Biol. Chem. 279: 28675-28680.
5. Bernard, J., Harb, C., Mortier, E., Quemener, A., Meloen, R.H., Vermot-Desroches, C., Wijdeness, J., van Dijken, P., Grotzinger, J., Slootstra, J.W., et al. 2004. Identification of an interleukin-15α receptor-binding site on human interleukin-15. J. Biol. Chem. 279: 24313-24322.
6. Bova, M.P., McHaourab, H.S., Han, Y., and Fung, B.K. 2000. Subunit exchange of small heat shock proteins. Analysis of oligomer formation of αA-crystallin and Hsp27 by fluorescence resonance energy transfer and site-directed truncations. J. Biol. Chem. 275: 1035-1042.
7. Caspers, G.J., Leunissen, J.A., and de Jong, W.W. 1995. The expanding small heat-shock protein family, and structure predictions of the conserved "α-crystallin domain". J. Mol. Evol. 40: 238-248.
8. Cherian, M. and Abraham, E.C. 1995. Decreased molecular chaperone property of α-crystallins due to posttranslational modifications. Biochem. Biophys. Res. Commun. 208: 675-679.
9. Chin, J., Fell, B., Shapiro, M.J., Tomesch, J., Wareing, J.R., and Bray, A.M. 1997. Magic angle spinning NMR for reaction monitoring and structure determination of molecules attached to multipin crowns. J. Org. Chem. 62: 538-539.
10. Clark, J.I. and Muchowski, P.J. 2000. Small heat-shock proteins and their potential role in human disease. Curr. Opin. Struct. Biol. 10: 52-59.
11. de Jong, W.W., Hendriks, W., Mulders, J.W., and Bloemendal, H. 1989. Evolution of eye lens crystallins: The stress connection. Trends Biochem Sci. 14: 365-368.
12. Derham, B.K. and Harding, J.J. 1999. α-crystallin as a molecular chaperone. Prog. Retin. Eye Res. 18: 463-509.
13. Derham, B.K., van Boekel, M.A., Muchowski, P.J., Clark, J.I., Horwitz, J., Hepburne-Scott, H.W., de Jong, W.W., Crabbe, M.J., and Harding, J.J. 2001. Chaperone function of mutant versions of α A- and α B-crystallin prepared to pinpoint chaperone binding sites. Eur. J. Biochem. 268: 713-721.
14. Fechteler, T., Dengler, U., and Schomburg, D. 1995. Prediction of protein three-dimensional structures in insertion and deletion regions: A procedure for searching data bases of representative protein fragments using geometric scoring criteria. J. Mol. Biol. 253: 114-131.
15. Feil, I.K., Malfois, M., Hendle, J., van Der Zandt, H., and Svergun, D.I. 2001. A novel quaternary structure of the dimeric α-crystallin domain with chaperone-like activity. J. Biol. Chem. 276: 12024-12029.
16. Geysen, H.M. 1990. Molecular technology: Peptide epitope mapping and the pin technology. Southeast Asian J. Trop. Med. Public Health 21: 523-533.
17. Gupta, R. and Srivastava, O.P. 2004. Effect of deamidation of asparagine 146 on functional and structural properties of human lens αB-crystallin. Invest. Ophthalmol. Vis. Sci. 45: 206-214.
18. Guruprasad, K. and 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.
19. Haley, D.A., Bova, M.P., Huang, Q.L., McHaourab, H.S., and Stewart, P.L. 2000. Small heat-shock protein structures reveal a continuum from symmetric to variable assemblies. J. Mol. Biol. 298: 261-272.
20. Haslbeck, M. and Buchner, J. 2002. Chaperone function of sHsps. Prog. Mol. Subcell. Biol. 28: 37-59.
21. Hepburne-Scott, H.W. and Crabbe, M.J. 1999. Maintenance of chaperone-like activity despite mutations in a conserved region of murine lens αB crystallin. Mol. Vis. 5: 15.
22. Horwitz, J. 1992. α-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. 89: 10449-10453.
23. _. 2003. α-crystallin. Exp. Eye Res. 76: 145-153.
24. Horwitz, J., Emmons, T., and Takemoto, L. 1992. The ability of lens α crystallin to protect against heat-induced aggregation is age-dependent. Curr. Eye Res. 11: 817-822.
25. Iwaki, T., Kume-Iwaki, A., Liem, R.K., and Goldman, J.E. 1989. α B-crystallin is expressed in non-lenticular tissues and accumulates in Alexander's disease brain. Cell 57: 71-78.
26. Iwaki, T., Iwaki, A., Tateishi, J., Sakaki, Y., and Goldman, J.E. 1993. α B-crystallin and 27-kd heat shock protein are regulated by stress conditions in the central nervous system and accumulate in Rosenthal fibers. Am. J. Pathol. 143: 487-495.
27. Jacob, J., Robertson, N.J., and Hilton, D.A. 2003. The clinicopathological spectrum of Rosenthal fibre encephalopathy and Alexander's disease: A case report and review of the literature. J. Neurol. Neurosurg. Psychiatry 74: 807-810.
28. Jeanmougin, F., Thompson, J.D., Gouy, M., Higgins, D.G., and Gibson, T.J. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403-405.
29. Kim, K.K., Kim, R., and Kim, S.H. 1998. Crystal structure of a small heat-shock protein. Nature 394: 595-599.
30. Kokke, B.P., Leroux, M.R., Candido, E.P., Boelens, W.C., and de Jong, W.W. 1998. Caenorhabditis elegans small heat-shock proteins Hsp12.2 and Hsp12.3 form tetramers and have no chaperone-like activity. FEBS Lett. 433: 228-232.
31. Kokke, B.P., Boelens, W.C., and de Jong, W.W. 2001. The lack of chaperone-like activity of Caenorhabditis elegans Hsp12.2 cannot be restored by domain swapping with human αB-crystallin. Cell Stress Chaperones 6: 360-367.
32. Koteiche, H.A. and McHaourab, H.S. 1999. Folding pattern of the α-crystallin domain in αA-crystallin determined by site-directed spin labeling. J. Mol. Biol. 294: 561-577.
33. _. 2002. The determinants of the oligomeric structure in Hsp16.5 are encoded in the α-crystallin domain. FEBS Lett. 519: 16-22.
34. Koteiche, H.A., Berengian, A.R., and McHaourab, H.S. 1998. Identification of protein folding patterns using site-directed spin labeling. Structural characterization of a β-sheet and putative substrate binding regions in the conserved domain of α A-crystallin. Biochemistry 37: 12681-12688.
35. Laksanalamai, P. and Robb, F.T. 2004. Small heat shock proteins from extremophiles: A review. Extremophiles 8: 1-11.
36. Lentze, N. and Narberhaus, F. 2004. Detection of oligomerisation and substrate recognition sites of small heat shock proteins by peptide arrays. Biochem. Biophys. Res. Commun. 325: 401-407.
37. Lentze, N., Studer, S., and 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.
38. Leroux, M.R., Melki, R., Gordon, B., Batelier, G., and Candido, E.P. 1997. Structure-function studies on small heat shock protein oligomeric assembly and interaction with unfolded polypeptides. J. Biol. Chem. 272: 24646-24656.
39. Levitt, M. 1992. Accurate modeling of protein conformation by automatic segment matching. J. Mol. Biol. 226: 507-533.
40. MacCoss, M.J., McDonald, W.H., Saraf, A., Sadygov, R., Clark, J.M., Tasto, J.J., Gould, K.L., Wolters, D., Washburn, M., Weiss, A., et al. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl. Acad. Sci. 99: 7900-7905.
41. McHaourab, H.S., Berengian, A.R., and Koteiche, H.A. 1997. Site-directed spin-labeling study of the structure and subunit interactions along a conserved sequence in the α-crystallin domain of heat-shock protein 27. Evidence of a conserved subunit interface. Biochemistry 36: 14627-14634.
42. McLean, P.J., Kawamata, H., Shariff, S., Hewett, J., Sharma, N., Ueda, K., Breakefield, X.O., and Hyman, B.T. 2002. TorsinA and heat shock proteins act as molecular chaperones: Suppression of α-synuclein aggregation. J. Neurochem. 83: 846-854.
43. Meloen, R.H., Puijk, W.C., and Slootstra, J.W. 2000. Mimotopes: Realization of an unlikely concept. J. Mol. Recognit. 13: 352-359.
44. Meloen, R.H., Langeveld, J.P., Schaaper, W.M., and Slootstra, J.W. 2001. Synthetic peptide vaccines: Unexpected fulfillment of discarded hope? Biologicals 29: 233-236.
45. Morris, A.L., MacArthur, M.W., Hutchinson, E.G., and Thornton, J.M. 1992. Stereochemical quality of protein structure coordinates. Proteins 12: 345-364.
46. Muchowski, P.J., Bassuk, J.A., Lubsen, N.H., and Clark, J.I. 1997. Human αB-crystallin. Small heat shock protein and molecular chaperone. J. Biol. Chem. 272: 2578-2582.
47. Muchowski, P.J., Hays, L.G., Yates 3rd, J.R., and Clark, J.I. 1999a. ATP and the core "α-Crystallin" domain of the small heat-shock protein αB-crystallin. J. Biol. Chem. 274: 30190-30195.
48. Muchowski, P.J., Wu, G.J., Liang, J.J., Adman, E.T., and Clark, J.I. 1999b. Site-directed mutations within the core "α-crystallin" domain of the small heat-shock protein, human αB-crystallin, decrease molecular chaperone functions. J. Mol. Biol. 289: 397-411.
49. 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
50. Nicholl, I.D. and Quinlan, R.A. 1994. Chaperone activity of α-crystallins modulates intermediate filament assembly. EMBO J. 13: 945-953.
51. Pasta, S.Y., Raman, B., Ramakrishna, T., and Rao Ch, M. 2003. Role of the conserved SRLFDQFFG region of α-crystallin, a small heat shock protein. Effect on oligomeric size, subunit exchange, and chaperone-like activity. J. Biol. Chem. 278: 51159-51166.
52. Piatigorsky, J. 1989. Lens crystalline and their genes: Diversity and tissue-specific expression. FASEB J. 3: 1933-1940.
53. Plater, M.L., Goode, D., and Crabbe, M.J. 1996. Effects of site-directed mutations on the chaperone-like activity of αB-crystallin. J. Biol. Chem. 271: 28558-28566.
54. Plesofsky, N. and Brambl, R. 2002. Analysis of interactions between domains of a small heat shock protein, Hsp30 of Neurospora crassa. Cell Stress Chaperones 7: 374-386.
55. Putilina, T., Skouri-Panet, F., Prat, K., Lubsen, N.H., and Tardieu, A. 2003. Subunit exchange demonstrates a differential chaperone activity of calf α-crystallin toward β LOW- and individual γ-crystallins. J. Biol. Chem. 278: 13747-13756.
56. Quinlan, R. and Van Den Ijssel, P. 1999. Fatal attraction: When chaperone turns harlot. Nat. Med. 5: 25-26.
57. Sharma, K.K., Kumar, R.S., Kumar, G.S., and Quinn, P.T. 2000. Synthesis and characterization of a peptide identified as a functional element in αA-crystallin. J. Biol. Chem. 275: 3767-3771.
58. Slootstra, J.W., Puijk, W.C., Ligtvoet, G.J., Langeveld, J.P., and Meloen, R.H. 1996. Structural aspects of antibody-antigen interaction revealed through small random peptide libraries. Mol. Divers. 1: 87-96.
59. Slootstra, J.W., Puijk, W.C., Ligtvoet, G.J., Kuperus, D., Schaaper, W.M., and Meloen, R.H. 1997. Screening of a small set of random peptides: A new strategy to identify synthetic peptides that mimic epitopes. J. Mol. Recognit. 10: 217-224.
60. Stege, G.J., Renkawek, K., Overkamp, P.S., Verschuure, P., van Rijk, A.F., Reijnen-Aalbers, A., Boelens, W.C., Bosman, G.J., and de Jong, W.W. 1999. The molecular chaperone αB-crystallin enhances amyloid β neurotoxicity. Biochem. Biophys. Res. Commun. 262: 152-156.
61. Studer, S., Obrist, M., Lentze, N., and Narberhaus, F. 2002. A critical motif for oligomerization and chaperone activity of bacterial α-heat shock proteins. Eur. J. Biochem. 269: 3578-3586.
62. Swaim, C.L., Smith, D.L., and Smith, J.B. 2004. The reaction of α-crystallin with the cross-linker 3, 3′-dithiobis (sulfosuccinimidyl propionate) demonstrates close proximity of the C termini of αA and αB in the native assembly. Protein Sci. 13: 2832-2835.
63. Tardieu, A. 1998. α-Crystallin quaternary structure and interactive properties control eye lens transparency. Int. J. Biol. Macromol. 22: 211-217.
64. Thampi, P. and Abraham, E.C. 2003. Influence of the C-terminal residues on oligomerization of α A-crystallin. Biochemistry 42: 11857-11863.
65. Thampi, P., Hassan, A., Smith, J.B., and Abraham, E.C. 2002. Enhanced C-terminal truncation of αA- and αB-crystalline in diabetic lenses. Invest. Ophthalmol. Vis. Sci. 43: 3265-3272.
66. Timmerman, P., Van Dijk, E., Puijk, W., Schaaper, W., Slootstra, J., Carlisle, S.J., Coley, J., Eida, S., Gani, M., Hunt, T., et al. 2004. Mapping of a discontinuous and highly conformational binding site on follicle stimulating hormone subunit-β(FSH-β) using domain Scan and Matrix Scan technology. Mol. Divers. 8: 61-77.
67. van Boekel, M.A., de Lange, F., de Grip, W.J., and de Jong, W.W. 1999. Eye lens αA- and αB-crystallin: Complex stability versus chaperone-like activity. Biochim. Biophys. Acta. 1434: 114-123.
68. van Montfort, R.L., Basha, E., Friedrich, K.L., Slingsby, C., and Vierling, E. 2001. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct Biol. 8: 1025-1030.
69. Wistow, G. 1985. Domain structure and evolution in α-crystallins and small heat-shock proteins. FEBS Lett. 181: 1-6.
70. Wyttenbach, A. 2004. Role of heat shock proteins during polyglutamine neurodegeneration: Mechanisms and hypothesis. J. Mol. Neurosci. 23: 69-96.