Probing the structure and interactions of crystallin proteins by NMR spectroscopy

Progress in Retinal and Eye Research

Volumn 18, Issue 4, 1999, Pages 431-462

  Carver, John A ^a  

^a UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CRYSTALLIN; BETA CRYSTALLIN; CHAPERONE; CORE PROTEIN; CRYSTALLIN; GAMMA CRYSTALLIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 25; PROTEIN SUBUNIT; SOLUBILIZER;

CARBOXY TERMINAL SEQUENCE; CATARACTOGENESIS; CRYSTAL STRUCTURE; DIMERIZATION; EXTENSION GENE; HOMOGENATE; HUMAN; LENS; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPHTHALMOLOGY; PRECIPITATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; STRESS; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; ANIMALS; CRYSTALLINS; DIMERIZATION; HEAT-SHOCK PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT;

EID: 0032983631     PISSN: 13509462     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1350-9462(98)00027-5     Document Type: Review

References (89)

1. Antuch W., Güntert P., Wüthrich K. Ancestral β,γ-crystallin precursor structure in a yeast killer toxin. Nat. Struct. Biol. 3:1996;662-665.
2. Augusteyn R. C., Koretz J. F. A possible structure for α-crystallin. FEBS Lett. 222:1987;1-5.
3. Bagby S., Harvey T. S., Eagle S. G., Inouye S., Ikura M. NMR-derived three-dimensional solution structure of protein S complexed with calcium. Structure. 2:1994;107-122.
4. Balbach J., Forge V., van Nuland N. A. J., Winder S. L., Hore P. J., Dobson C. M. Nat. Struct. Biol. 2:1995;865-870.
5. Bax B., Lapatto V., Driessen H., Lindley P. F., Mahadevan D., Blundell T. L., Slingsby C. X-ray analysis of βB2-crystallin and evolution of oligomeric lens proteins. Nature. 347:1990;776-780.
6. Benndorf R., Bielka H. Cellular stress response: stress proteins - physiology and implications for cancer. Rec. Results Cancer Res. 143:1997;129-144.
7. Berbers G. A. M., Hoekman W. A., Bloemendal H., de Jong W. W., Kleinschmidt T., Braunitzer G. Homology between the primary structures of the major β-crystallin chains. Eur. J. Biochem. 139:1984;467-479.
8. Blakytny R., Carver J. A., Harding J. J., Kilby G. W., Sheil M. M. A spectroscopic study of glycated bovine α-crystallin: investigation of flexibility of the C-terminal extension, chaperone activity and evidence for diglycation. Biochim. Biophys. Acta. 1343:1997;299-315.
9. Bloemendal H., Piatigorsky J., Spector A. Recommendations for crystallin nomenclature. Exp. Eye Res. 48:1989;465-466.
10. Blundell T., Lindley P., Miller L., Moss D., Slingsby C., Tickle I., Turnell B., Wistow G. The molecular structure and stability of the eye lens: X-ray analysis of γ-crystallin II. Nature. 289:1981;771-777.
11. Boelens W. C., de Jong W. W. α-Crystallins, versatile stress proteins. Mol. Biol. Rep. 21:1995;75-80.
12. Branden, C. and Tooze, J. (1991) In Introduction to Protein Structure, pp. 67-70. Garland, New York.
13. Buchner J. Supervising the fold: functional principles of molecular chaperones. FASEB J. 10:1996;10-19.
14. Caines G. H., Schleich T., Morgan C. F., Farnsworth P. N. Off-resonance rotating frame spin-lattice NMR relaxation studies of phosphorus metabolite rotational diffusion in bovine lens homogenates. Biochemistry. 29:1990;7547-7557.
15. Carver J. A., Lindner R. A. NMR spectroscopy of α-crystallin. Insights into the structure, interactions and chaperone action of small-heat shock proteins. Int. J. Biol. Macromol. 22:1998;197-209.
16. 1H NMR spectroscopy of flexible C-terminal extensions in bovine α-crystallin. FEBS Lett. 311:1992;143-149.
17. Carver J. A., Aquilina J. A., Cooper P. G., Williams G. A., Truscott R. J. W. α-Crystallin: molecular chaperone and protein surfactant. Biochim Biophys. Acta. 1204:1993;195-206.
18. 1H-NMR spectroscopy of βB2-crystallin from bovine lens. Conformation of the N- and C-terminal extensions. Eur. J. Biochem. 213:1993;313-320.
19. Carver J. A., Aquilina J. A., Truscott R. J. W. An investigation into the stability of α-crystallin by NMR spectroscopy; evidence for a two-domain structure. Biochim. Biophys. Acta. 1164:1993;22-28.
20. Carver J. A., Aquilina J. A., Truscott R. J. W. A possible chaperone-like quaternary structure for α-crystallin. Exp. Eye Res. 59:1994;231-234.
21. Carver J. A., Guerreiro N., Nicholls K. A., Truscott R. J. W. On the interaction of α-crystallin with unfolded proteins. Biochim. Biophys. Acta. 1252:1995;251-260.
22. 1H NMR spectroscopy reveals that mouse Hsp25 has a flexible C-terminal extension of 18 amino acids. FEBS Lett. 369:1995;305-310.
23. Carver J. A., Nicholls K. A., Aquilina J. A., Truscott R. J. W. Age-related changes in bovine α-crystallin and high-molecular-weight protein. Exp. Eye Res. 63:1996;639-647.
24. Chiesa R., Gawinowicz-Kolks M. A., Kleiman N. J., Spector A. Definition and comparison of the phosphorylation sites of the A and B chains of bovine α-crystallin. Exp. Eye Res. 46:1988;199-208.
25. 1H-NMR spectroscopy of bovine lens β-crystallin. The role of the βB2-crystallin C-terminal extension in aggregation. Eur. J. Biochem. 213:1993;321-328.
26. 1H NMR spectroscopic comparison of γS- and γB-crystallins. Exp. Eye Res. 59:1994;211-220.
27. 1H NMR spectroscopic evidence for specific crystallin-crystallin interactions. Exp. Eye Res. 59:1994;607-616.
28. Das B. K., Liang J. J.-N., Chakrabarti B. Heat-induced conformational change and increased chaperone activity of lens α-crystallin. Curr. Eye Res. 16:1997;303-309.
29. Delaye M., Tardieu A. Short-range order of crystallin proteins accounts for lens transparency. Nature. 302:1983;415-417.
30. de Jong W. W., Leunissen J. A. M., Voorter C. E. M. Evolution of the α-crystallin/small heat-shock protein family. Mol. Biol. Evol. 10:1993;103-126.
31. Ehrnsperger, M., Buchner, J. and Gaestel., M. (1997a) In Molecular Chaperones in the Life Cycle of Proteins, Structure, Function and Mode of Action (ed. A. L. Fink and Y. Goto), pp. 533-575. Marcel Dekker, New York.
32. Ehrnsperger M., Gräber S., Gaestel M., Buchner J. Binding of nonnative protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J. 16:1997;221-229.
33. Esposito G., Viglino P., Fogolari F., Gaestel M., Carver J. A. Selective NMR experiments on macromolecules: implementation and analysis of QUIET-NOESY. J. Magn. Reson. 132:1998;204-213.
34. Evans, J. N. S. (1995) Biomolecular NMR Spectroscopy. Oxford University Press, Oxford.
35. Farahbakhsh Z. T., Huang Q.-L., Ding L.-L., Altenbach C., Steinhoff H.-J., Horwitz J., Hubbell W. L. Interaction of α-crystallin with spin-labeled peptides. Biochemistry. 34:1995;509-516.
36. Garner W. H., Spector A., Schleich T., Kaptein R. Determination of the solvent accessibility of specific aromatic residues in gamma-crystallin by photo-CIDNP NMR measurements. Curr. Eye Res. 3:1984;127-135.
37. Garner W. H., Balaji V. N. Structural analysis of bovine lens calf gamma-II crystallin: residue assignments of the five histidine CE1 resonances observed by proton-nuclear magnetic resonance spectroscopy. Curr. Eye Res. 7:1988;777-788.
38. Graw J. The crystallins: genes, proteins and diseases. Biol. Chem. 378:1997;1331-1348.
39. Groenen P. J. T. A., Merck K. B., de Jong W. W., Bloemendal H. Structure and modifications of the junior chaperone α-crystallin. From lens transparency to molecular pathology. Eur J. Biochem. 225:1994;1-19.
40. Haley D. A., Horwitz J., Stewart P. L. The small heat-shock protein, αB-crystallin, has a variable quaternary structure. J. Mol. Biol. 277:1998;27-35.
41. Harding, J. J. (1991) Cataract. Biochemistry, Epidemiology and Pharmacology. Chapman and Hall, London.
42. Hartl F. U. Molecular chaperones in cellular protein folding. Nature. 381:1996;571-580.
43. Hayer-Hartl M. K., Ewbank J. J., Creighton T. E., Hartl F. U. Conformational specificity of the chaperonin GroEL for the compact folding intermediates of α-lactalbumin. EMBO J. 13:1994;3192-3202.
44. Horwitz J. α-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA. 89:1992;10449-10453.
45. Horwitz J. The function of alpha-crystallin. Invest. Ophthal. Vis. Sci. 34:1993;10-22.
46. Ingolia T. D., Craig E. A. Four Drosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc. Natl. Acad. Sci. USA. 79:1982;2360-2364.
47. Kim, K. K., Kim, R. and Kim, S.-H. (1998a) Crystal structure of a small heat-shock protein. Nature 394, 595-599.
48. Kim K. K., Yokota H., Santoso S., Lerner D., Kim R., Kim S.-H. Purification, crystallization and preliminary X-ray crystallographic data analysis of small heat shock protein homolog from Methanococcus jannaschii, a hyperthermophile. J. Struct. Biol. 121:1998;76-80.
49. 1 nuclear magnetic relaxation dispersion profiles. Biophys. J. 57:1990;461-469.
50. Kuwajima K. The molten globule state of α-lactalbumin. FASEB J. 10:1996;102-109.
51. Kuwajima K., Ikeguchi M., Sugawara T., Hiraoka Y., Sugai S. Kinetics of disulfide bond reduction in α-lactalbumin by dithiothreitol and molecular basis of superreactivity of the Cys6-Cys120 disulfide bond. Biochemistry. 29:1990;8240-8249.
52. Lapatto R., Nalini V., Driessen H., Lindley P. F., Blundell T. L., Slingsby C. High resolution structure of an oligomeric eye lens β-crystallin. Loops, arches, linkers and interfaces in βB2 dimer compared to a monomeric γ-crystallin. J. Mol. Biol. 222:1991;1067-1083.
53. Le Breton E. R., Carver J. A. Solution conformation of bovine lens α- and βB2-crystallin terminal extensions. Int. J. Pep. Prot. Res. 47:1996;9-19.
54. Leroux M. R., Ma B. J., Batelier G., Melki R., Candido E. P. M. Unique features of a novel class of small heat shock protein. J. Biol. Chem. 272:1997;12847-12853.
55. Li L.-K. Effects of temperature, concentration and carboxymethylation on interactions of calf lens crystallins. Exp. Eye Res. 28:1979;717-731.
56. Liang J. N., Li X.-Y. Interaction and aggregation of lens crystallins. Exp. Eye Res. 53:1991;61-66.
57. Lindley P., Najmudin S., Bateman O., Slingsby C., Myles D., Kumaraswamy V. S., Glover I. Structure of bovine γB-crystallin at 150K. J. Chem. Soc. Faraday Trans. 89:1993;2677-2682.
58. Lindner R. A., Kapur A., Carver J. A. The interaction of the molecular chaperone, α-crystallin, with molten globule states of bovine α-lactalbumin. J. Biol. Chem. 272:1997;27722-27729.
59. Lindner, R. A., Kapur, A., Mariani, M., Titmuss, S. J. and Carver, J. A. (1998) Structural alterations of α-crystallin during its chaperone action. Eur. J. Biochem. (in press).
60. Morgan C. F., Schleich T., Caines G. H., Farnsworth P. N. Elucidation of intermediate (mobile) and slow (solidlike) protein motions in bovine lens homogenates by carbon-13 NMR spectroscopy. Biochemistry. 28:1989;5065-5074.
61. Norledge B. V., Mayr E.-M., Glockshuber R., Bateman O. A., Slingsby C., Jaenicke R., Driessen H. P. C. The X-ray structures of two mutant crystallin domains shed light on the evolution of multi-domain proteins. Nat. Struct. Biol. 3:1996;267-274.
62. Okazaki A., Ikura T., Nikaido K., Kuwajima K. The chaperonin GroEL does not recognize apo-α-lactalbumin in the molten globule state. Struct. Biol. 1:1994;439-446.
63. Palleros D. R., Welch W. J., Fink A. L. Interaction of hsp70 with unfolded proteins: effects of temperature and nucleotides on the kinetics of binding. Proc. Natl. Acad. Sci. USA. 88:1991;5719-5723.
64. Piatigorsky J., Wistow G. J. Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell. 57:1989;197-199.
65. Raman B., Rao Ch. M. Chaperone-like activity and temperature-induced structural changes of α-crystallin. J. Biol. Chem. 272:1997;23559-23564.
66. Sergeev Y. V., Chirgadze Y. N., Mylvaganam S. E., Driessen H., Slingsby C., Blundell T. L. Surface interactions of γ-crystallins in the crystal medium in relation to their association in the eye lens. Prot. Struct. Funct. Genet. 4:1988;137-147.
67. Shearer T. R., Shih M., Azuma M., David L. L. Precipitation of crystallins from young rat lens by endogenous calpain. Exp. Eye Res. 61:1995;141-150.
68. Siezen R. J., Anello R. D., Thomson J. A. Interactions of lens proteins. Concentration dependence of β-crystallin aggregation. Exp. Eye Res. 43:1986;293-303.
69. Siezen R. J., Wu E., Kaplan E. D., Thomson J. A., Benedek G. B. Rat lens γ-crystallins. Characterization of the six gene products and their spatial distribution resulting from differential synthesis. J. Mol. Biol. 199:1988;475-490.
70. Simpson A., Bateman O., Driessen H., Lindley P., Moss D., Mylvaganam S., Narebor E., Slingsby C. The structure of avian eye lens δ-crystallin reveals a new fold for a superfamily of oligomeric enzymes. Nat. Struct. Biol. 1:1994;724-734.
71. Simpson A., Moss D., Slingsby C. The avian eye lens protein δ-crystallin shows a novel packing arrangement of tetramers in a supramolecular helix. Structure. 3:1995;403-412.
72. Slingsby C., Norledge B., Simpson A., Bateman O. A., Wright G., Driessen H. P. C., Lindley P. F., Moss D. S., Bax B. X-ray diffraction and structure of crystallins. Prog. Ret. Eye Res. 16:1997;3-29.
73. Smulders R. H. P. H., Carver J. A., Lindner R. A., van Boekel M. A. M., Bloemendal H., de Jong W. W. Immobilization of the C-terminal extension of bovine αA-crystallin reduces chaperone-like activity. J. Biol. Chem. 271:1996;29060-29066.
74. Stevens A., Augusteyn R. C. Isolation of α-crystallin subunits by gel filtration. Curr. Eye Res. 6:1987;739-740.
75. Sun T. X., Das B. K., Liang J. J.-N. Conformational and functional differences between recombinant human lens αA and αB-crystallin. J. Biol. Chem. 272:1997;6220-6225.
76. Surewicz W. K., Olesen P. R. On the thermal stability of α-crystallin: a new insight from infrared spectroscopy. Biochemistry. 34:1995;9655-9660.
77. Tardieu A., Vérétout F., Krop B., Slingsby C. Protein interactions in the calf lens: interactions between β-crystallins are repulsive whereas in γ-crystallins they are attractive. Eur. Biophys. J. 21:1992;1-12.
78. Thomas P. J., Qu B.-H., Pedersen P. L. Defective protein folding as a basis of human disease. Trends Biochem. Sci. 20:1995;456-459.
79. Thomson J. A., Siezen R. J., Kaplan E. D., Messmer M., Chakrabarti B. Comparative studies of βS-crystallins from human, bovine, rat and rabbit lenses. Curr. Eye Res. 8:1989;139-149.
80. van de Klundert, F. A. J. M., Smulders, R. H. P. H., Gijsen, M. L. J., Carver, J. A., Lindner, R. A. and de Jong, W. W. (1998) The mammalian small heat shock protein Hsp20 forms dimers and is a poor chaperone. Eur. J. Biochem. (in press).
81. van den Oetelaar P. J. M., Hoenders H. J. Folding-unfolding and aggregation-dissociation of bovine α-crystallin subunits; evidence for unfolding intermediates of the αA subunits. Biochim. Biophys. Acta. 995:1989;91-96.
82. Vlaanderen I., van Grondelle R., Bloemendal M. The use of fast protein liquid (size exclusion) chromatography for the fractionation of crystallins and the study of β-crystallin aggregation. J. Liq. Chromat. 16:1993;367-382.
83. Welch W. J., Brown C. R. Influence of molecular and chemical chaperones on protein folding. Cell Stress Chap. 1:1996;109-115.
84. Werten P. J. L., Carver J. A., Jaenicke R., de Jong W. W. The elusive role of the N-terminal extension of βA3- and βA1-crystallin. Prot. Engin. 9:1996;1021-1028.
85. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR. 5:1995;67-81.
86. Wistow G. Domain structure and evolution in α-crystallins and small heat-shock proteins. FEBS Lett. 181:1985;1-6.
87. Wistow G., Turnell B., Summers L., Slingsby C., Moss D., Miller L., Lindley P., Blundell T. X-ray analysis of the eye lens protein γ-II crystallin at 1.9Å resolution. J. Mol. Biol. 170:1983;175-202.
88. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids. John Wiley, New York.
89. Zarina S., Slingsby C., Jaenicke R., Zaidi Z. H., Driessen H., Srinivasan N. Three-dimensional model and quaternary structure of the human eye lens protein γS-crystallin based on β- and γ-crystallin X-ray coordinates and ultracentrifugation. Prot. Sci. 3:1994;1840-1846.