The structured core domain of αB-crystallin can prevent amyloid fibrillation and associated toxicity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages

  Hochberg, Georg K A ^a   Ecroyd, Heath ^b   Liu, Cong ^c,d,f   Cox, Dezerae ^b   Cascio, Duilio ^c,d   Sawaya, Michael R ^c,d   Collier, Miranda P ^a   Stroud, James ^c,d   Carver, John A ^e   Baldwin, Andrew J ^a   Robinson, Carol V ^a   Eisenberg, David S ^c,d   Benesch, Justin L P ^a   Laganowsky, Arthur ^a,c,d  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF WOLLONGONG   (Australia)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^f SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

Author keywords

Ion mobility mass spectrometry; Nuclear magnetic resonance spectroscopy; X ray crystallography

Indexed keywords

ALPHA CRYSTALLIN; AMYLOID; AMYLOID BETA PROTEIN[1-42]; DIMER; DISULFIDE; HEAT SHOCK PROTEIN 27; MONOMER;

AMINO TERMINAL SEQUENCE; AMYLOIDOGENESIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CELL VIABILITY; CONTROLLED STUDY; CORE DOMAIN; CYTOTOXICITY; DIMERIZATION; DISSOCIATION; DISULFIDE BOND; EMBRYO; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PC12 CELL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; X RAY CRYSTALLOGRAPHY;

ION MOBILITY MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; X-RAY CRYSTALLOGRAPHY;

ALPHA-CRYSTALLIN B CHAIN; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; ANIMALS; CRYSTALLIZATION; CYSTEINE; HEK293 CELLS; HELA CELLS; HSP27 HEAT-SHOCK PROTEINS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MAMMALS; MOLECULAR SEQUENCE DATA; PC12 CELLS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RATS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84899118154     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1322673111     Document Type: Article

References (75)

1. Baldwin AJ, et al. (2011) Metastability of native proteins and the phenomenon of amyloid formation. J Am Chem Soc 133(36):14160-14163.
2. Olzscha H, et al. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144(1):67-78.
3. Powers ET, Balch WE (2013) Diversity in the origins of proteostasis networks-a driver for protein function in evolution. Nat Rev Mol Cell Biol 14(4):237-248.
4. Balch WE, Morimoto RI, Dillin A, Kelly JW (2008) Adapting proteostasis for disease intervention. Science 319(5865):916-919. (Pubitemid 351263754)
5. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475(7356):324-332.
6. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: Life on the verge of death. Mol Cell 40(2):253-266.
7. Basha E, O'Neill H, Vierling E (2012) Small heat shock proteins and α-crystallins: Dynamic proteins with flexible functions. Trends Biochem Sci 37(3):106-117.
8. Hilton GR, Lioe H, Stengel F, Baldwin AJ, Benesch JLP (2013) Small heat-shock proteins: Paramedics of the cell. Top Curr Chem 328:69-98.
9. McHaourab HS, Godar JA, Stewart PL (2009) Structure and mechanism of protein stability sensors: Chaperone activity of small heat shock proteins. Biochemistry 48(18):3828-3837.
10. Carra S, et al. (2013) Different anti-aggregation and pro-degradative functions of the members of the mammalian sHSP family in neurological disorders. Philos Trans R Soc Lond B Biol Sci 368(1617):20110409.
11. Garrido C, Paul C, Seigneuric R, Kampinga HH (2012) The small heat shock proteins family: The long forgotten chaperones. Int J Biochem Cell Biol 44(10):1588-1592.
12. Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89(21):10449-10453.
13. Boncoraglio A, Minoia M, Carra S (2012) The family of mammalian small heat shock proteins (HSPBs): Implications in protein deposit diseases and motor neuropathies. Int J Biochem Cell Biol 44(10):1657-1669.
14. Ecroyd H, Carver JA (2009) Crystallin proteins and amyloid fibrils. Cell Mol Life Sci 66(1):62-81.
15. Kampinga HH, Garrido C (2012) HSPBs: Small proteins with big implications in human disease. Int J Biochem Cell Biol 44(10):1706-1710.
16. Chiti F, Dobson CM (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366. (Pubitemid 44118036)
17. Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148(6):1188-1203.
18. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8(2):101-112. (Pubitemid 46432529)
19. Wilhelmus MM, et al. (2006) Small heat shock proteins inhibit amyloid-beta protein aggregation and cerebrovascular amyloid-beta protein toxicity. Brain Res 1089(1):67-78. (Pubitemid 43786300)
20. Mannini B, et al. (2012) Molecular mechanisms used by chaperones to reduce the toxicity of aberrant protein oligomers. Proc Natl Acad Sci USA 109(31):12479-12484.
21. Knowles TP, et al. (2007) Kinetics and thermodynamics of amyloid formation from direct measurements of fluctuations in fibril mass. Proc Natl Acad Sci USA 104(24):10016-10021. (Pubitemid 47175255)
22. Raman B, et al. (2005) AlphaB-crystallin, a small heat-shock protein, prevents the amyloid fibril growth of an amyloid beta-peptide and beta2-microglobulin. Biochem J 392(Pt 3):573-581. (Pubitemid 43022737)
23. Rekas A, et al. (2004) Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: Effects on amyloid fibril formation and chaperone activity. J Mol Biol 340(5):1167-1183. (Pubitemid 38968709)
24. Shammas SL, et al. (2011) Binding of the molecular chaperone αB-crystallin to Aβ amyloid fibrils inhibits fibril elongation. Biophys J 101(7):1681-1689.
25. Waudby CA, et al. (2010) The interaction of alphaB-crystallin with mature alpha-synuclein amyloid fibrils inhibits their elongation. Biophys J 98(5):843-851.
26. Binger KJ, et al. (2013) Avoiding the oligomeric state: αB-crystallin inhibits fragmentation and induces dissociation of apolipoprotein C-II amyloid fibrils. FASEB J 27(3):1214-1222.
27. Baldwin AJ, Lioe H, Robinson CV, Kay LE, Benesch JLP (2011) αB-crystallin polydispersity is a consequence of unbiased quaternary dynamics. J Mol Biol 413(2):297-309.
28. Aquilina JA, Shrestha S, Morris AM, Ecroyd H (2013) Structural and functional aspects of hetero-oligomers formed by the small heat shock proteins αB-crystallin and HSP27. J Biol Chem 288(19):13602-13609.
29. Delbecq SP, Klevit RE (2013) One size does not fit all: The oligomeric states of αB crystallin. FEBS Lett 587(8):1073-1080.
30. Aquilina JA, Watt SJ (2007) The N-terminal domain of alphaB-crystallin is protected from proteolysis by bound substrate. Biochem Biophys Res Commun 353(4):1115-1120. (Pubitemid 46080413)
31. Bhattacharyya J, Padmanabha Udupa EG, Wang J, Sharma KK (2006) Mini-alphaB-crystallin: A functional element of alphaB-crystallin with chaperone-like activity. Biochemistry 45(9):3069-3076. (Pubitemid 43334555)
32. Ghosh JG, Estrada MR, Clark JI (2005) Interactive domains for chaperone activity in the small heat shock protein, human alphaB crystallin. Biochemistry 44(45):14854-14869. (Pubitemid 41612265)
33. Narayanan S, Kamps B, Boelens WC, Reif B (2006) alphaB-crystallin competes with Alzheimer's disease beta-amyloid peptide for peptide-peptide interactions and induces oxidation of Abeta-Met35. FEBS Lett 580(25):5941-5946. (Pubitemid 44584297)
34. Sharma KK, Kaur H, Kester K (1997) Functional elements in molecular chaperone alpha-crystallin: Identification of binding sites in alpha B-crystallin. Biochem Biophys Res Commun 239(1):217-222. (Pubitemid 27480344)
35. Bova MP, Ding LL, Horwitz J, Fung BKK (1997) Subunit exchange of alphaA-crystallin. J Biol Chem 272(47):29511-29517.
36. Augusteyn RC (2004) Dissociation is not required for alpha-crystallin's chaperone function. Exp Eye Res 79(6):781-784.
37. Aquilina JA, et al. (2005) Subunit exchange of polydisperse proteins: Mass spectrometry reveals consequences of alphaA-crystallin truncation. J Biol Chem 280(15):14485-14491. (Pubitemid 40562789)
38. Bagnéris C, et al. (2009) Crystal structures of alpha-crystallin domain dimers of alphaB-crystallin and Hsp20. J Mol Biol 392(5):1242-1252.
39. Clark AR, Naylor CE, Bagnéris C, Keep NH, Slingsby C (2011) Crystal structure of R120G disease mutant of human αB-crystallin domain dimer shows closure of a groove. J Mol Biol 408(1):118-134.
40. Jehle S, et al. (2010) Solid-state NMR and SAXS studies provide a structural basis for the activation of alphaB-crystallin oligomers. Nat Struct Mol Biol 17(9):1037-1042.
41. Laganowsky A, et al. (2010) Crystal structures of truncated alphaA and alphaB crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci 19(5):1031-1043.
42. Laganowsky A, Eisenberg D (2010) Non-3D domain swapped crystal structure of truncated zebrafish alphaA crystallin. Protein Sci 19(10):1978-1984.
43. Delbecq SP, Jehle S, Klevit R (2012) Binding determinants of the small heat shock protein, αB-crystallin: Recognition of the 'IxI' motif. EMBO J 31(24):4587-4594.
44. Mymrikov EV, Bukach OV, Seit-Nebi AS, Gusev NB (2010) The pivotal role of the beta 7 strand in the intersubunit contacts of different human small heat shock proteins. Cell Stress Chaperones 15(4):365-377.
45. Baranova EV, et al. (2011) Three-dimensional structure of α-crystallin domain dimers of human small heat shock proteins HSPB1 and HSPB6. J Mol Biol 411(1):110-122.
46. Arrigo AP (2001) Hsp27: Novel regulator of intracellular redox state. IUBMB Life 52(6):303-307.
47. Indu S, Kochat V, Thakurela S, Ramakrishnan C, Varadarajan R (2011) Conformational analysis and design of cross-strand disulfides in antiparallel β-sheets. Proteins 79(1):244-260.
48. Jehle S, et al. (2009) alphaB-crystallin: A hybrid solid-state/solution- state NMR investigation reveals structural aspects of the heterogeneous oligomer. J Mol Biol 385(5):1481-1497.
49. Ruotolo BT, Benesch JLP, Sandercock AM, Hyung SJ, Robinson CV (2008) Ion mobility-mass spectrometry analysis of large protein complexes. Nat Protoc 3(7):1139-1152.
50. Benesch JLP, Ruotolo BT (2011) Mass spectrometry: Come of age for structural and dynamical biology. Curr Opin Struct Biol 21(5):641-649.
51. Hilton GR, et al. (2013) C-terminal interactions mediate the quaternary dynamics of αB-crystallin. Philos Trans R Soc Lond B Biol Sci 368(1617):20110405.
52. Carver JA, et al. (2002) The interaction of the molecular chaperone α-crystallin with unfolding α-lactalbumin: A structural and kinetic spectroscopic study. J Mol Biol 318(3):815-827. (Pubitemid 34729371)
53. Feil IK, Malfois M, Hendle J, van Der Zandt H, Svergun DI (2001) A novel quaternary structure of the dimeric alpha-crystallin domain with chaperone-like activity. J Biol Chem 276(15):12024-12029.
54. Härd T, Lendel C (2012) Inhibition of amyloid formation. J Mol Biol 421(4-5):441-465.
55. Liberek K, Lewandowska A, Zietkiewicz S (2008) Chaperones in control of protein disaggregation. EMBO J 27(2):328-335. (Pubitemid 351161659)
56. Piatigorsky J, Wistow G (1991) The recruitment of crystallins: New functions precede gene duplication. Science 252(5009):1078-1079.
57. Bepperling A, et al. (2012) Alternative bacterial two-component small heat shock protein systems. Proc Natl Acad Sci USA 109(50):20407-20412.
58. Basha E, et al. (2013) An unusual dimeric small heat shock protein provides insight into the mechanism of this class of chaperones. J Mol Biol 425(10):1683-1696.
59. Bukach OV, Seit-Nebi AS, Marston SB, Gusev NB (2004) Some properties of human small heat shock protein Hsp20 (HspB6). Eur J Biochem 271(2):291-302. (Pubitemid 38130457)
60. Kulig M, Ecroyd H (2012) The small heat-shock protein αB-crystallin uses different mechanisms of chaperone action to prevent the amorphous versus fibrillar aggregation of α-lactalbumin. Biochem J 448(3):343-352.
61. Ecroyd H, et al. (2008) Dissociation from the oligomeric state is the rate-limiting step in fibril formation by kappa-casein. J Biol Chem 283(14):9012-9022.
62. Laganowsky A, et al. (2012) Atomic view of a toxic amyloid small oligomer. Science 335(6073):1228-1231.
63. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26(6):795-800.
64. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674. (Pubitemid 47080256)
65. Adams PD, et al. (2002) PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58(Pt 11):1948-1954. (Pubitemid 35337293)
66. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
67. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53(Pt 3):240-255. (Pubitemid 27235885)
68. Smart OS, et al. (2012) Exploiting structure similarity in refinement: Automated NCS and target-structure restraints in BUSTER. Acta Crystallogr D Biol Crystallogr 68(Pt 4):368-380.
69. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774-797. (Pubitemid 47321791)
70. Larkin MA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947-2948. (Pubitemid 350162903)
71. Pettersen EF, et al. (2004) UCSF Chimera- a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.
72. Bush MF, et al. (2010) Collision cross sections of proteins and their complexes: A calibration framework and database for gas-phase structural biology. Anal Chem 82(22):9557-9565.
73. Delaglio F, et al. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6(3):277-293.
74. Ecroyd H, Carver JA (2008) The effect of small molecules in modulating the chaperone activity of alphaB-crystallin against ordered and disordered protein aggregation. FEBS J 275(5):935-947. (Pubitemid 351230209)
75. Slob W (2002) Dose-response modeling of continuous endpoints. Toxicol Sci 66(2):298-312.