Small heat shock proteins and α-crystallins: Dynamic proteins with flexible functions

Trends in Biochemical Sciences

Volumn 37, Issue 3, 2012, Pages 106-117

  Basha, Eman ^a   O'Neill, Heather ^b   Vierling, Elizabeth ^b  

^a University of Arizona   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; CHAPERONE; HEAT SHOCK PROTEIN B1; HEAT SHOCK PROTEIN B10; HEAT SHOCK PROTEIN B3; HEAT SHOCK PROTEIN B4; HEAT SHOCK PROTEIN B5; HEAT SHOCK PROTEIN B8; SMALL HEAT SHOCK PROTEIN; UNCLASSIFIED DRUG;

BINDING AFFINITY; CELL PROTECTION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PHYSICAL DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; STRESS;

ALPHA-CRYSTALLINS; AMINO ACID SEQUENCE; EVOLUTION, MOLECULAR; GENETIC DISEASES, INBORN; HEAT-SHOCK PROTEINS, SMALL; HUMANS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; STRESS, PHYSIOLOGICAL; SUBSTRATE SPECIFICITY;

EID: 84858003372     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2011.11.005     Document Type: Review

References (88)

1. Gidalevitz T., et al. A cellular perspective on conformational disease: the role of genetic background and proteostasis networks. Curr. Opin. Struct. Biol. 2010, 20:23-32.
2. Tyedmers J., et al. Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 2010, 11:777-788.
3. Hartl F.U., et al. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
4. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:10449-10453.
5. Jakob U., et al. Small heat shock proteins are molecular chaperones. J. Biol. Chem. 1993, 268:1517-1520.
6. van Montfort R., et al. Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. Adv. Protein Chem. 2002, 59:105-156.
7. McHaourab H.S., et al. Structure and mechanism of protein stability sensors: chaperone activity of small heat shock proteins. Biochemistry 2009, 48:3828-3837.
8. Mymrikov E.V., et al. Large potentials of small heat shock proteins. Physiol. Rev. 2011, 91:1123-1159.
9. Haslbeck M., et al. Some like it hot: the structure and function of small heat-shock proteins. Nat. Struct. Mol. Biol. 2005, 12:842-846.
10. Poulain P., et al. Detection and architecture of small heat shock protein monomers. PLoS ONE 2010, 5:e9990.
11. Kriehuber T., et al. Independent evolution of the core domain and its flanking sequences in small heat shock proteins. FASEB J. 2010, 24:3633-3642.
12. Waters E.R., et al. Comparative analysis of the small heat shock proteins in three angiosperm genomes identifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperones 2008, 13:127-142.
13. Vos M.J., et al. Structural and functional diversities between members of the human HSPB, HSPH, HSPA, and DNAJ chaperone families. Biochemistry 2008, 47:7001-7011.
14. Kampinga H.H., et al. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 2009, 14:105-111.
15. Siddique M., et al. The plant sHSP superfamily: five new members in Arabidopsis thaliana with unexpected properties. Cell Stress Chaperones 2008, 13:183-197.
16. Wadhwa R., et al. Proproliferative functions of Drosophila small mitochondrial heat shock protein 22 in human cells. J. Biol. Chem. 2010, 285:3833-3839.
17. Kim K.K., et al. Crystal structure of a small heat-shock protein. Nature 1998, 394:595-599.
18. van Montfort R.L., et al. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct. Biol. 2001, 8:1025-1030.
19. Horwitz J. Alpha crystallin: the quest for a homogeneous quaternary structure. Exp. Eye Res. 2009, 88:190-194.
20. Baldwin A.J., et al. αB-crystallin polydispersity is a consequence of unbiased quaternary dynamics. J. Mol. Biol. 2011, 413:297-309.
21. Jehle S., et al. Solid-state NMR and SAXS studies provide a structural basis for the activation of alphaB-crystallin oligomers. Nat. Struct. Mol. Biol. 2010, 17:1037-1042.
22. Jehle S., et al. N-terminal domain of αB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:6409-6414.
23. Peschek J., et al. The eye lens chaperone alpha-crystallin forms defined globular assemblies. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13272-13277.
24. Baldwin, A.J. et al. (2011) The polydispersity of αB-crystallin is rationalised by an inter-converting polyhedral architecture. Structure (in press).
25. Bagneris C., et al. Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20. J. Mol. Biol. 2009, 392:1242-1252.
26. Jehle S., et al. alphaB-crystallin: a hybrid solid-state/solution-state NMR investigation reveals structural aspects of the heterogeneous oligomer. J. Mol. Biol. 2009, 385:1481-1497.
27. Laganowsky A., et al. Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci. 2010, 19:1031-1043.
28. Clark A.R., et al. Crystal structure of R120G Disease mutant of human alphaB-crystallin domain dimer shows closure of a groove. J. Mol. Biol. 2011, 408:118-134.
29. Takeda K., et al. Dimer structure and conformational variability in the N-terminal region of an archaeal small heat shock protein, StHsp14.0. J. Struct. Biol. 2011, 174:92-99.
30. Baldwin A.J., et al. Quaternary dynamics of αB-crystallin as a direct consequence of localised tertiary fluctuations in the C-terminus. J. Mol. Biol. 2011, 413:310-320.
31. White H.E., et al. Multiple distinct assemblies reveal conformational flexibility in the small heat shock protein Hsp26. Structure 2006, 14:1197-1204.
32. Stamler R., et al. Wrapping the [alpha]-crystallin domain fold in a chaperone assembly. J. Mol. Biol. 2005, 353:68-79.
33. Marchler-Bauer A., et al. CDD: a conserved domain database for the functional annotation of proteins. Nucl. Acids Res. 2011, 39:D225-D229.
34. Painter A.J., et al. Real-time monitoring of protein complexes reveals their quaternary organization and dynamics. Chem. Biol. 2008, 15:246-253.
35. Stengel F., et al. Quaternary dynamics and plasticity underlie small heat shock protein chaperone function. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:2007-2012.
36. Schneider F., et al. Transthyretin slowly exchanges subunits under physiological conditions: A convenient chromatographic method to study subunit exchange in oligomeric proteins. Protein Sci. 2001, 10:1606-1613.
37. Uetrecht C., et al. Subunit exchange rates in hepatitis B virus capsids are geometry- and temperature-dependent. Phys. Chem. Chem. Phys. 2010, 12:13368-13371.
38. Cheng G., et al. Insights into small heat shock protein and substrate structure during chaperone action derived from hydrogen/deuterium exchange and mass spectrometry. J. Biol. Chem. 2008, 283:26634-26642.
39. Doyle S.M., Wickner S. Hsp104 and ClpB: protein disaggregating machines. Trends Biochem. Sci. 2009, 34:40-48.
40. Saibil H.R. Chaperone machines in action. Curr. Opin. Struct. Biol. 2008, 18:35-42.
41. Basha E., et al. Mechanistic differences between two conserved classes of small heat shock proteins found in the plant cytosol. J. Biol. Chem. 2010, 285:11489-11497.
42. Bukach O.V., et al. Some properties of human small heat shock protein Hsp20 (HspB6). Eur. J. Biochem. 2004, 271:291-302.
43. Franzmann T.M., et al. Activation of the chaperone hsp26 is controlled by the rearrangement of its thermosensor domain. Mol. Cell 2008, 29:207-216.
44. Ecroyd H., et al. Mimicking phosphorylation of alphaB-crystallin affects its chaperone activity. Biochem. J. 2007, 401:129-141.
45. Shashidharamurthy R., et al. 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. 2005, 280:5281-5289.
46. Ahrman E., et al. Chemical cross-linking of the chloroplast localized small heat-shock protein, Hsp21, and the model substrate citrate synthase. Protein Sci. 2007, 16:1464-1478.
47. Ghosh J.G., et al. Interactions between important regulatory proteins and human alphaB crystallin. Biochemistry 2007, 46:6308-6317.
48. Jaya N., et al. Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:15604-15609.
49. Ratajczak E., et al. Distinct activities of Escherichia coli small heat shock proteins IbpA and IbpB promote efficient protein disaggregation. J. Mol. Biol. 2009, 386:178-189.
50. Basha E., et al. The N-terminal arm of small heat shock proteins is important for both chaperone activity and substrate specificity. J. Biol. Chem. 2006, 281:39943-39952.
51. Haslbeck M., et al. Hsp42 is the general small heat shock protein in the cytosol of Saccharomyces cerevisiae. EMBO J. 2004, 23:638-649.
52. Basha E., et al. 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. 2004, 279:7566-7575.
53. Carra S., et al. Identification of the Drosophila ortholog of HSPB8: implication of HSPB8 loss of function in protein folding diseases. J. Biol. Chem. 2010, 285:37811-37822.
54. Carra S., et al. HspB8 participates in protein quality control by a non-chaperone-like mechanism that requires eIF2{alpha} phosphorylation. J. Biol. Chem. 2009, 284:5523-5532.
55. Carra S., et al. HspB8 and Bag3: a new chaperone complex targeting misfolded proteins to macroautophagy. Autophagy 2008, 4:237-239.
56. Goldfarb L.G., et al. Intermediate filament diseases: desminopathy. Adv. Exp. Med. Biol. 2008, 642:131-164.
57. Clark J.I., Muchowski P.J. Small heat-shock proteins and their potential role in human disease. Curr. Opin. Struct. Biol. 2000, 10:52-59.
58. Graw J. Genetics of crystallins: cataract and beyond. Exp. Eye Res. 2009, 88:173-189.
59. Rajasekaran N.S., et al. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardiomyopathy in mice. Cell 2007, 130:427-439.
60. Goldfarb L.G., Dalakas M.C. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J. Clin. Invest. 2009, 119:1806-1813.
61. Willis M.S., et al. Build it up-tear it down: protein quality control in the cardiac sarcomere. Cardiovasc. Res. 2009, 81:439-448.
62. Simon S., et al. Myopathy-associated αB-crystallin mutants: abnormal phosphorylation, intracellular location and interactions with other small heat shock proteins. J. Biol. Chem. 2007, 282:34276-34287.
63. Tannous P., et al. Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:9745-9750.
64. Dierick I., et al. Small heat shock proteins in inherited peripheral neuropathies. Ann. Med. 2005, 37:413-422.
65. Sun X., et al. Abnormal interaction of motor neuropathy-associated mutant HspB8 (Hsp22) forms with the RNA helicase Ddx20 (gemin3). Cell Stress Chaperones 2010, 15:567-582.
66. Xi J.H., et al. Mechanism of small heat shock protein function in vivo: a knock-in mouse model demonstrates that the R49C mutation in alpha A-crystallin enhances protein insolubility and cell death. J. Biol. Chem. 2008, 283:5801-5814.
67. Kamada M., et al. Hsp27 knockdown using nucleotide-based therapies inhibit tumor growth and enhance chemotherapy in human bladder cancer cells. Mol. Cancer Ther. 2007, 6:299-308.
68. Deng M., et al. The small heat shock protein alphaA-crystallin is expressed in pancreas and acts as a negative regulator of carcinogenesis. Biochim. Biophys. Acta 2010, 1802:621-631.
69. Ecroyd H., Carver J.A. Crystallin proteins and amyloid fibrils. Cell. Mol. Life Sci. 2009, 66:62-81.
70. van Noort J.M., et al. Alphab-crystallin is a target for adaptive immune responses and a trigger of innate responses in preactive multiple sclerosis lesions. J. Neuropath. Exp. Neurol. 2010, 69:694-703.
71. Laskowska E., et al. Small heat shock proteins and protein-misfolding diseases. Curr. Pharm. Biotech. 2010, 11:146-157.
72. Kumarapeli A.R., et al. Protein quality control in protection against systolic overload cardiomyopathy: the long term role of small heat shock proteins. Am. J. Transl. Res. 2010, 2:390-401.
73. Morrow G., et al. Protection from aging by small chaperones: a trade-off with cancer?. Ann. N. Y. Acad. Sci. 2010, 1197:67-75.
74. Ousman S.S., et al. Protective and therapeutic role for alphaB-crystallin in autoimmune demyelination. Nature 2007, 448:474-479.
75. Toth M.E., et al. Neuroprotective effect of small heat shock protein, Hsp27, after acute and chronic alcohol administration. Cell Stress Chaperones 2010, 15:807-817.
76. Robertson A.L., et al. Small heat-shock proteins interact with a flanking domain to suppress polyglutamine aggregation. Proc. Natl.Acad. Sci. U.S.A. 2010, 107:10424-10429.
77. Vos M.J., et al. HSPB7 is the most potent polyQ aggregation suppressor within the HSPB family of molecular chaperones. Hum. Mol. Genet. 2010, 19:4677-4693.
78. Waudby C.A., et al. The interaction of alphaB-crystallin with mature alpha-synuclein amyloid fibrils inhibits their elongation. Biophys. J. 2010, 98:843-851.
79. Shammas S.L., et al. Binding of the molecular chaperone alphaB-crystallin to Abeta amyloid fibrils inhibits fibril elongation. Biophys. J. 2011, 101:1681-1689.
80. Balch W.E., et al. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
81. Mymrikov E.V., et al. Heterooligomeric complexes of human small heat shock proteins. Cell Stress Chaperones 2011, 10.1007/s12192-011-0296-0.
82. Pei J., et al. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucl. Acids Res. 2008, 36:2295-2300.
83. Tamura K., et al. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
84. Hilario E., et al. Crystallization and preliminary X-ray diffraction analysis of XAC1151, a small heat-shock protein from Xanthomonas axonopodis pv. citri belonging to the alpha-crystallin family. Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 2006, 62:446-448.
85. Hilario E., et al. Crystal structures of xanthomonas small heat shock protein provide a structural basis for an active molecular chaperone oligomer. J. Mol. Biol. 2011, 408:74-86.
86. Laganowsky A., Eisenberg D. Non-3D domain swapped crystal structure of truncated zebrafish alphaA crystallin. Protein Sci. 2010, 19:1978-1984.
87. Kennaway C.K., et al. Dodecameric structure of the small heat shock protein Acr1 from Mycobacterium tuberculosis. J. Biol. Chem. 2005, 280:33419-33425.
88. Baranova E.V., et al. Three dimensional structure of α-crystallin domain dimers of human heat shock proteins HSPB1 and HSPB6. J. Mol. Biol. 2011, 411:110-122.