Solution properties of γ-crystallins: Hydration of fish and mammal γ-crystallins

Protein Science

Volumn 23, Issue 1, 2014, Pages 88-99

  Zhao, Huaying ^a   Chen, Yingwei ^b   Rezabkova, Lenka ^a   Wu, Zhengrong ^c   Wistow, Graeme ^b   Schuck, Peter ^a  

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

^b NATIONAL EYE INSTITUTE   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Crystallin; Hydrodynamic modeling; Protein hydration; Protein hydrodynamics; Protein interactions

Indexed keywords

GAMMA CRYSTALLIN; METHIONINE; SUCROSE;

ARTICLE; CHEMICAL BINDING; HUMAN; HYDRODYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; THERMODYNAMICS; ZEBRA FISH;

CRYSTALLIN; HYDRODYNAMIC MODELING; PROTEIN HYDRATION; PROTEIN HYDRODYNAMICS; PROTEIN INTERACTIONS;

ANIMALS; EYE PROTEINS; GAMMA-CRYSTALLINS; HUMANS; HYDRODYNAMICS; LENS, CRYSTALLINE; METHIONINE; MICE; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; SOLUBILITY; SOLUTIONS; THERMODYNAMICS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84900439499     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2394     Document Type: Article

References (74)

1. Land MF, Nilsson D-E (2002) Animal Eyes. Oxford: Oxford University Press
2. Wistow GJ (1995) Molecular biology and evolution of crystallins: Gene recruitment and multifunctional proteins in the eye lens. Georgetown, TX: R.G. Landes Company
3. Slingsby C, Wistow GJ, Clark AR (2013) Evolution of crystallins for a role in the vertebrate eye lens. Protein Sci 22:367-380
4. Bloemendal, de Jong W, Jaenicke R, Lubsen NH, Slingsby C, Tardieu A (2004) Ageing and vision: Structure, stability and function of lens crystallins. Progr Biophys Mol Biol 86:407-485
5. Wistow GJ, 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 1.9A resolution. J Mol Biol 170:175-202
6. Zhao H, Brown PH, Magone MT, Schuck P (2011) The molecular refractive function of lens g-crystallins. J Mol Biol 411:680-699
7. 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
8. Zhao H, Brown PH, Schuck P (2011) On the distribution of protein refractive index increments. Biophys J 100:2309-2317
9. Jaenicke R, Slingsby C (2001) Lens crystallins and their microbial homologs: Structure, stability, and function. Crit Rev Biochem Mol 36:435-499
10. Kröger 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. Vis Res 34:1815-1822
11. Purkiss AG, Bateman OA, Wyatt K, Wilmarth PA, David LL, Wistow GJ, Slingsby C (2007) Biophysical properties of gammaC-crystallin in human and mouse eye lens: The role of molecular dipoles. J Mol Biol 372: 205-222
12. Tardieu A, Veretout F, Krop B, Slingsby C, Vérétout F( 1992) Protein interactions in the calf eye lens: Interactions between beta-crystallins are repulsive whereas in gamma-crystallins they are attractive. Eur Biophys J 21:1-12
13. Benedek GB (1971) Theory of transparency of the eye. Appl Opt 10:459-473
14. Tardieu A (1988) Eye lens proteins and transparency: From light transmission theory to solution X-ray structural analysis. Annu Rev Biophys Bio 17:47-70
15. Delaye M, Tardieu A (1983) Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302:415-417
16. Wistow GJ, Piatigorsky J (1988) Lens crystallins: The evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479-504
17. Pande A, Annunziata O, Asherie N, Ogun O, Benedek GB, Pande J (2005) Decrease in protein solubility and cataract formation caused by the Pro23 to Thr mutation in human gamma D-crystallin. Biochemistry 44:2491-2500
18. Basak A, Bateman OA, Slingsby C, Pande A, Asherie N, Ogun O, Benedek GB, Pande J (2003) High-resolution X-ray crystal structures of human gammaD crystallin( 1.25 A) and the R58H mutant (1.15 A) associated with aculeiform cataract. J Mol Biol 328:1137-1147
19. McManus JJ, Lomakin A, Ogun O, Pande A, Basan M, Pande J, Benedek GB (2007) Altered phase diagram due to a single point mutation in human gamma-D crystallin. Proc Natl Acad Sci USA 104:16856-16861
20. Brubaker WD, Freites JA, Golchert KJ, Shapiro RA, Morikis V, Tobias DJ, Martin RW (2011) Separating instability from aggregation propensity in gS-crystallin variants. Biophys J 100:498-506
21. Stradner A, Sedgwick H, Cardinaux F, Poon WCK, Egelhaaf SU, Schurtenberger P (2004) Equilibrium cluster formation in concentrated protein solutions and colloids. Nature 432:492-495
22. Stradner A, Foffi G, Dorsaz N, Thurston G, Schurtenberger P (2007) New insight into cataract formation: Enhanced stability through mutual attraction. Phys Rev Lett 99:198103
23. Slingsby C, Norledge B, Simpson A, Bateman OA, Wright G, Driessen HP, Lindley PF, Moss DS, Bax B( 1997) X-ray diffraction and structure of crystallins. Prog Retin Eye Res 16:4-25
24. Kiss AJ, Cheng C-HC (2008) Molecular diversity and genomic organisation of the alpha, beta and gamma eye lens crystallins from the Antarctic toothfish Dissostichus mawsoni. Comp Biochem Physiol Part D Genomics Proteomics 3:155-171
25. Pan FM, Chang WCC, Chao YKK, Chiou SHH (1994) Characterization of gamma-crystallins from a hybrid teleostean fish: Multiplicity of isoforms as revealed by cDNA sequence analysis. Biochem Biophys Res Commun 202:527-534
26. 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
27. Srikanthan D, Bateman OA, Purkiss AGG, Slingsby C( 2004) Sulfur in human crystallins. Exp Eye Res 79: 823-831
28. Mahler B, Chen Y, Ford J, Thiel C, Wistow G, Wu Z( 2013) Structure and dynamics of the fish eye lens protein, gM7-crystallin. Biochemistry 50:3579-3587
29. Israelachvili JN, Wennerström H (1996) Role of hydration and water structure in biological and colloidal interactions. Nature 379:219-225
30. Bettelheim FA, Reid MB, Garland D (1994) Hydration of gamma-crystallins. Exp Eye Res 58:219-223
31. Bettelheim FA, Popdimitrova N (1990) Hydration properties of lens crystallins. Exp Eye Res 50:715-718
32. Petitt P, Edwards ME, Forciniti D (1997) A small-angle neutron scattering study of gamma-crystallins near their isoelectric point. Eur J Biochem 243:415-421
33. Aragon SR, Hahn DK (2006) Precise boundary element computation of protein transport properties: Diffusion tensors, specific volume, and hydration. Biophys J 91: 1591-1603
34. Virtanen JJ, Makowski L, Sosnick TR, Freed KF( 2010) Modeling the hydration layer around proteins: HyPred. Biophys J 99:1611-1619
35. Ebel C, Eisenberg H, Ghirlando R (2000) Probing protein-sugar interactions. Biophys J 78:385-393
36. Edelstein SJ, Schachman HK (1967) The simultaneous determination of partial specific volumes and molecular weights with microgram quantities. J Biol Chem 242: 306-311
37. Durchschlag H, Specific volumes of biological macromolecules and some other molecules of biological interest. In: Hinz H-J, Ed. (1986) Thermodynamic data for biochemistry and biotechnology. Berlin: Springer, pp 45- 128
38. Halle B, Davidovic M (2003) Biomolecular hydration: From water dynamics to hydrodynamics. Proc Natl Acad Sci USA 100:12135-12140
39. Ghirlando R, Balbo A, Piszczek G, Brown PH, Lewis MS, Brautigam CA, Schuck P, Zhao H (2013) Improving the thermal, radial, and temporal accuracy of the analytical ultracentrifuge through external references. Anal Biochem 440:81-95
40. Errington N, Rowe AJ (2003) Probing conformation and conformational change in proteins is optimally undertaken in relative mode. Eur Biophys J 32:511-517
41. Wu Z, Delaglio F, Wyatt K, Wistow GJ, Bax A (2005) Solution structure of (gamma)S-crystallin by molecular fragment replacement NMR. Protein Sci 14:3101-3114
42. Wang J, Zuo X, Yu P, Byeon I-JL, Jung J, Wang X, Dyba M, Seifert S, Schwieters CD, Qin J, Gronenborn AM, Wang Y-X (2009) Determination of multicomponent protein structures in solution using global orientation and shape restraints. J Am Chem Soc 131: 10507-10515
43. Pettitt BM, Makarov VA, Andrews BK (1998) Protein hydration density: Theory, simulations and crystallography. Curr Opin Struct Biol 8:218-221
44. Makarov VA, Andrews BK, Pettitt BM (1998) Reconstructing the protein-water interface. Biopolymers 45: 469-478
45. Batchelor GK (1972) Sedimentation in a dilute dispersion of spheres. J Fluid Mech 52:245-268
46. Patel TR, Harding SE, Ebringerova A, Deszczynski M, Hromadkova Z, Togola A, Paulsen BS, Morris GA, Rowe AJ (2007) Weak self-association in a carbohydrate system. Biophys J 93:741-749
47. Cantor CR, Schimmel PR (1980) Biophysical Chemistry. II. Techniques for the study of biological structure and function. New York: W.H. Freeman
48. Serdyuk IN, Zaccai NR, Zaccai J (2007) Methods In Molecular Biophysics: Structure, Dynamics, Function. Cambridge. U.K.: Cambridge University Press
49. Chen S-H, Bendedouch D (1986) Structure and interactions of proteins in solution studied by small-angle neutron scattering. Methods Enzym 130:79-116
50. Lopez MM, Makhatadze GI (1998) Solvent isotope effect on thermodynamics of hydration. Biophys Chem 74:117-125
51. Jasnin M, Tehei M, Moulin M, Haertlein M, Zaccai G( 2008) Solvent isotope effect on macromolecular dynamics in E. coli. Eur Biophys J 37:613-617
52. Chiou SH, Azari P, Himmel ME (1988) Physicochemical characterization of gamma-crystallins from bovine lens-hydrodynamic and biochemical properties. J Prot Chem 7:67-80
53. Barlow DJ, Thornton JM (1983) Ion-pairs in proteins. J Mol Biol 168:867-885
54. Blundell T, Lindley P, Miller L, Moss D, Slingsby C, Tickle I, Turnell B, Wistow GJ (1981) The molecular structure and stability of the eye lens: X-ray analysis of g-crystallin II. Nature 289:771-777
55. Merzel F, Smith JC (2002) Is the first hydration shell of lysozyme of higher density than bulk water? Proc Natl Acad Sci USA 99:5378-5383
56. Yaminsky VV, Vogler EA (2001) Hydrophobic hydration. Curr Opin Colloid Interface Sci 6:342-349
57. Zhou HX (2008) Protein folding in confined and crowded environments. Arch Biochem Biophys 469:76-82
58. Young MA, Tunstall MJ, Kistler J, Donaldson PJ( 2000) Blocking chloride channels in the rat lens: Localized changes in tissue hydration support the existence of a circulating chloride flux. Invest Ophthalmol Vis Sci 41:3049-3055
59. Rao PV, Garrow TA, John F, Garland D, Millian NS, Zigler JS (1998) Betaine-homocysteine methyltransferase is a developmentally regulated enzyme crystallin in rhesus monkey lens. J Biol Chem 273:30669-30674
60. Ando T, Skolnick J (2010) Crowding and hydrodynamic interactions likely dominate in vivo macromolecular motion. Proc Natl Acad Sci USA 107:18457-18462
61. Annunziata O, Ogun O, Benedek GB (2003) Observation of liquid-liquid phase separation for eye lens gammaS- crystallin. Proc Natl Acad Sci USA 100:970-974
62. Norledge BV, Hay RE, Bateman OA, Slingsby C, Driessen HP (1997) Towards a molecular understanding of phase separation in the lens: A comparison of the X-ray structures of two high Tc gamma-crystallins, gammaE and gammaF, with two low Tc gammacrystallins, gammaB and gammaD. Exp Eye Res 65: 609-630
63. Broide ML, Berland CR, Pande J, Ogun OO, Benedek GB (1991) Binary-liquid phase separation of lens protein solutions. Proc Natl Acad Sci USA 88:5660-5664
64. Fenimore PW, Frauenfelder H, McMahon BH, Young RD (2004) Bulk-solvent and hydration-shell fluctuations, similar to alpha- and beta-fluctuations in glasses, control protein motions and functions. Proc Natl Acad Sci USA 101:14408-14413
65. Sinha D, Wyatt MK, Sarra R, Jaworski C, Slingsby C, Thaung C, Pannell L, Robison WG, Favor J, Lyon M, Wistow GJ (2001) A temperature-sensitive mutation of Crygs in the murine Opj cataract. J Biol Chem 276: 9308-9315
66. Balbo A, Brown PH, Braswell EH, Schuck P (2007) Measuring protein-protein interactions by equilibrium sedimentation. Curr Protoc Immunol Chapter 18:Unit 18 8
67. Vistica J, Dam J, Balbo A, Yikilmaz E, Mariuzza RA, Rouault TA, Schuck P (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal Biochem 326:234-256.
68. Zhao H, Brautigam CA, Ghirlando R, Schuck P (2013) Current methods in sedimentation velocity and sedimentation equilibrium analytical ultracentrifugation. Curr Protoc Prot Sci 7:20.12.1
69. Brown PH, Balbo A, Schuck P (2008) Characterizing protein-protein interactions by sedimentation velocity analytical ultracentrifugation. Curr Protoc Immunol 18:Unit 18 15
70. 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
71. Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78:1606-1619
72. Aragon SR (2011) Recent advances in macromolecular hydrodynamic modeling. Methods 54:101-114
73. Connolly ML (1993) The molecular surface package. J Mol Graph 11:139-141
74. Chen Y, Zhao H, Schuck P, Wistow GJ (2013) Solution properties of gamma crystallins: Compact structure and low frictional ratio are conserved properties of diverse gamma crystallins. Prot. Sci. 23:76-87