Solution properties of γ-crystallins: Compact structure and low frictional ratio are conserved properties of diverse γ-crystallins

Protein Science

Volumn 23, Issue 1, 2014, Pages 76-87

  Chen, Yingwei ^a   Zhao, Huaying ^b   Schuck, Peter ^b   Wistow, Graeme ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

Author keywords

Crystallin; Protein evolution; Protein stability; Solution behavior

Indexed keywords

BETA CRYSTALLIN; CYSTEINE; GAMMA CRYSTALLIN; METHIONINE; TRYPTOPHAN;

AMINO ACID COMPOSITION; ARTICLE; BETA SHEET; CRYSTAL STRUCTURE; HUMAN; HYDRODYNAMICS; MAMMAL; MOLECULAR CROWDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DENATURATION; SEDIMENTATION RATE; STRUCTURE ANALYSIS; ZEBRA FISH;

CRYSTALLIN; PROTEIN EVOLUTION; PROTEIN STABILITY; SOLUTION BEHAVIOR;

ALPHA-CRYSTALLIN B CHAIN; AMINO ACID SEQUENCE; ANIMALS; CIRCULAR DICHROISM; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; EYE PROTEINS; GAMMA-CRYSTALLINS; HUMANS; HYDRODYNAMICS; MICE; MODELS, MOLECULAR; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SOLUBILITY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84900408112     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2395     Document Type: Article

References (51)

1. Wistow G (1993) Lens crystallins: Gene recruitment and evolutionary dynamism. Trends Biochem Sci 18: 301-306
2. Wistow GJ, Piatigorsky J (1988) Lens crystallins: The evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479-504
3. Bloemendal H, De Jong W, Jaenicke R, Lubsen NH, Slingsby C, Tardieu A (2004) Ageing and vision: Structure, stability and function of lens crystallins. Prog Biophys Mol Biol 86:407-485
4. Slingsby C, Clout NJ (1999) Structure of the crystallins. Eye 13:395-402
5. Hemmingsen JM, Gernert KM, Richardson JS, Richardson DC (1994) The tyrosine corner: A feature of most Greek keyá-barrel proteins. Protein Sci 3:1927- 1937
6. Kosinski-Collins MS, Flaugh SL, King J (2004) Probing folding and fluorescence quenching in human gammaD crystallin Greek key domains using triple tryptophan mutant proteins. Protein Sci 13:2223-2235
7. Chen J, Callis PR, King J (2009) Mechanism of the efficient quenching of tryptophan fluorescence in human gamma D- and gamma S-crystallins: The gammacrystallin fold may have evolved to protect tryptophan residues from ultraviolet photodamage. Biochemistry 48:3708-3716
8. Wistow G, Turnell B, Summers L, Slingsby C, Moss D, Miller L, Lindley P, Blundell T (1983) X-ray analysis of the eye lens protein gamma-II crystallin at 1.9 A resolution. J Mol Biol 170:175-202
9. Harding JJ, Dilley KJ (1976) Structural proteins of the mammalian lens: A review with emphasis on changes in development, aging and cataract. Exp Eye Res 22: 1-73
10. Truscott RJ (2005) Age-related nuclear cataractoxidation is the key. Exp Eye Res 80:709-725
11. Moreau KL, King JA (2012) Protein misfolding and aggregation in cataract disease and prospects for prevention. Trends Mol Med 18:273-282
12. Chang T, Jiang YJ, Chiou SH, Chang WC (1988) Carp gamma-crystallins with high methionine content: Cloning and sequencing of the complementary DNA. Biochim Biophys Acta 951:226-229
13. Wistow G, Wyatt K, David L, Gao C, Bateman O, Bernstein S, Tomarev S, Segovia L, Slingsby C, Vihtelic T (2005) Gamman-crystallin and the evolution of the betagamma-crystallin superfamily in vertebrates. FEBS J 272:2276-2291
14. Greiling TM, Houck SA, Clark JI (2009) The zebrafish lens proteome during development and aging. Mol Vis 15:2313-2325
15. Zhao H, Brown PH, Magone MT, Schuck P (2011) The molecular refractive function of lens gamma-crystallins. J Mol Biol 411:680-699
16. Zhao H, Brown PH, Schuck P (2011) On the distribution of protein refractive index increments. Biophys J 100:2309-2317
17. Zhao H, Magone MT, Schuck P (2011) The role of macromolecular crowding in the evolution of lens crystallins with high molecular refractive index. Phys Biol 8: 046004
18. Uhlhorn SR, Borja D, Manns F, Parel JM (2008) Refractive index measurement of the isolated crystalline lens using optical coherence tomography. Vision Res 48:2732-2738
19. Rao KD, Verma Y, Patel HS, Gupta PK (2006) Noninvasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography. Curr Sci 90:1506-1510
20. Hoshino M, Uesugi K, Yagi N, Mohri S, Regini J, Pierscionek B (2011) Optical properties of in situ eye lenses measured with X-ray Talbot interferometry: A novel measure of growth processes. PLoS One 6:e25140
21. Kroger RH, Campbell MC, Munger R, Fernald RD( 1994) Refractive index distribution and spherical aberration in the crystalline lens of the African cichlid fish Haplochromis burtoni. Vision Res 34:1815-1822
22. Delaye M, Tardieu A (1983) Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302:415-417
23. Benedek GB, Pande J, Thurston GM, Clark JI (1999) Theoretical and experimental basis for the inhibition of cataract. Prog Retin Eye Res 18:391-402
24. Clark JI, Clark JM (2000) Lens cytoplasmic phase separation. Int Rev Cytol 192:171-187
25. Fan J, Dong L, Mishra S, Chen Y, Fitzgerald P, Wistow G (2012) A role for gammaS-crystallin in the organization of actin and fiber cell maturation in the mouse lens. FEBS J 279:2892-2904
26. Sinha D, Wyatt MK, Sarra R, Jaworski C, Slingsby C, Thaung C, Pannell L, Robison WG, Favor J, Lyon M, Wistow G (2001) A temperature-sensitive mutation of Crygs in the murine Opj cataract. J Biol Chem 276: 9308-9315
27. Lee S, Mahler B, Toward J, Jones B, Wyatt K, Dong L, Wistow G, Wu Z (2010) A single destabilizing mutation( F9S) promotes concerted unfolding of an entire globular domain in gammaS-crystallin. J Mol Biol 399:320-330
28. Mahler B, Doddapaneni K, Kleckner I, Yuan C, Wistow G, Wu Z (2011) Characterization of a transient unfolding intermediate in a core mutant of gammaS-crystallin. J Mol Biol 405:840-850
29. Mahler B, Chen Y, Ford J, Thiel C, Wistow G, Wu Z( 2013) Structure and dynamics of the fish eye lens protein, gammaM7-crystallin. Biochemistry 50:3579-3587
30. Bagneris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, Keep NH, Slingsby C (2009) Crystal structures of alpha-crystallin domain dimers of alphaβ-crystallin and Hsp20. J Mol Biol 392:1242-1252
31. Clark AR, Lubsen NH, Slingsby C (2012) sHSP in the eye lens: Crystallin mutations, cataract and proteostasis. Int J Biochem Cell Biol 44:1687-1697
32. Brown PH, Balbo A, Zhao H, Ebel C, Schuck P (2011) Density contrast sedimentation velocity for the determination of protein partial-specific volumes. PLoS One 6:e26221
33. Cantor CR, Schimmel PR (1980) Biophysical chemistry. II. Techniques for the study of biological structure and function. New York: W.H. Freeman
34. Serdyuk IN, Zaccai NR, Zaccai J (2007) Methods in molecular biophysics: Structure, dynamics, function. Cambridge: Cambridge University Press
35. Bassnett S, Shi Y, Vrensen GF (2011) Biological glass: Structural determinants of eye lens transparency. Philos Trans Roy Soc B 366:1250-1264
36. Wistow G, Slingsby C, Structure and evolution of crystallins. In: Dartt DA, Besharse JC, Dana R, Eds.( 2010) The encyclopedia of the eye. Elsevier, pp 229- 238
37. Aravind P, Wistow G, Sharma Y, Sankaranarayanan R( 2008) Exploring the limits of sequence and structure in a variant betagamma-crystallin domain of the protein absent in Melanoma-1 (AIM1). J Mol Biol 381: 509-518
38. Shimeld SM, Purkiss AG, Dirks RP, Bateman OA, Slingsby C, Lubsen NH (2005) Urochordate betagamma-crystallin and the evolutionary origin of the vertebrate eye lens. Curr Biol 15:1684-1689
39. Kappe G, Purkiss AG, van Genesen ST, Slingsby C, Lubsen NH (2010) Explosive expansion of betagammacrystallin genes in the ancestral vertebrate. J Mol Evol 71:219-230
40. Evans P, Wyatt K, Wistow GJ, Bateman OA, Wallace BA, Slingsby C (2004) The P23T cataract mutation causes loss of solubility of folded gammaD-crystallin. J Mol Biol 343:435-444
41. Wu Z, Delaglio F, Wyatt K, Wistow G, Bax A (2005) Solution structure of (gamma)S-crystallin by molecular fragment replacement NMR. Protein Sci 14:3101-3114
42. Zhou HX (2008) Protein folding in confined and crowded environments. Arch Biochem Biophys 469:76-82
43. Tsao D, Minton AP, Dokholyan NV (2010) A didactic model of macromolecular crowding effects on protein folding. PLoS One 5:e11936
44. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids S 41:95-98
45. Wistow G, Bernstein SL, Wyatt MK, Behal A, Touchman JW, Bouffard G, Smith D, Peterson K (2002) Expressed sequence tag analysis of adult human lens for the NEIBank Project: Over 2000 non-redundant transcripts, novel genes and splice variants. Mol Vis 8:171-184
46. Vihtelic TS, Fadool JM, Gao J, Thornton KA, Hyde DR, Wistow G (2005) Expressed sequence tag analysis of zebrafish eye tissues for NEIBank. Mol Vis 11:1083-1100
47. Wistow G, Peterson K, Gao J, Buchoff P, Jaworski C, Bowes-Rickman C, Ebright JN, Hauser MA, Hoover D( 2008) NEIBank: Genomics and bioinformatics resources for vision research. Mol Vis 14:1327-1337
48. Zhao H, Ghirlando R, Piszczek G, Curth U, Brautigam CA, Schuck P (2013) Recorded scan times can limit the accuracy of sedimentation coefficients in analytical ultracentrifugation. Anal Biochem 437:104-108
49. Cohn EJ, Edsall JT, Density and apparent specific volume of proteins. In: Cohn EJ, Edsall JT, Eds. (1943) Proteins, amino acids and peptides. New Jersey: Van Nostrand-Reinhold, Princeton, pp 370-381
50. McMeekin TL, Groves ML, Hipp NJ, Refractive indices of amino acids, proteins and related substances. In: Stekol J, Ed. (1964) Amino acids and serum proteins. Washington DC: American Chemical Society
51. Zhao H, Chen Y, Rezabkova L, Wu Z, Wistow G, Schuck P (2013) Solution properties of gamma-crystallins: Hydration of fish and mammal gamma-crystallins. Prot. Sci 23:88-99