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Crystallins and Their Complexes

  • Kalyan Sundar GhoshEmail author
  • Priyanka Chauhan
Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 93)

Abstract

The crystallins (α, β and γ), major constituent proteins of eye lens fiber cells play their critical role in maintaining the transparency and refractive index of the lens. Under different stress factors and with aging, β- and γ-crystallins start to unfold partially leading to their aggregation. Protein aggregation in lens basically enhances light scattering and causes the vision problem, commonly known as cataract. α-crystallin as a molecular chaperone forms complexes with its substrates (β- and γ-crystallins) to prevent such aggregation. In this chapter, the structural features of β- and γ-crystallins have been discussed. Detailed structural information linked with the high stability of γC-, γD- and γS-crystallins have been incorporated. The nature of homologous and heterologous interactions among crystallins has been deciphered, which are involved in their molecular association and complex formation.

Keywords

α-crystallin β-crystallin γ-crystallin Crystallin complexes Aggregation of crystallins 

References

  1. Acosta-Sampson L, King J (2010) Partially folded aggregation intermediates of human γD-, γC-, and γS-crystallin are recognized and bound by human αB-crystallin chaperone. J Mol Biol 401:134–152CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahmad MF, Singh D, Taiyab A, Ramakrishna T, Raman B, Rao CM (2008) Selective Cu2+ binding, redox silencing, and cytoprotective effects of the small heat shock proteins αA and αB-crystallin. J Mol Biol 382:812–824CrossRefPubMedGoogle Scholar
  3. Asomugha CO, Gupta R, Srivastava OP (2011) Structural and functional properties of NH2-terminal domain, core domain, and COOH-terminal extension of αA- and αB-crystallins. Mol Vis 17:2356–2367PubMedPubMedCentralGoogle Scholar
  4. Aziz A, Santhoshkumar P, Sharma KK, Abraham EC (2007) Cleavage of the C-terminal serine of human alphaA-crystallin produces alphaA1-172 with increased chaperone activity and oligomeric size. Biochemistry 46:2510–2519CrossRefPubMedGoogle Scholar
  5. Bagby S, Go S, Inouye S, Ikura M, Chakrabartty A (1998) Equilibrium folding intermediates of a Greek key beta-barrel protein. J Mol Biol 276:669–681CrossRefPubMedGoogle Scholar
  6. Bagnéris C, Bateman OA, Naylor CE, Cronin N, Boelens WC, Keep NH, Slingsby C (2009) Crystal structures of α-crystallin domain dimers of αB-crystallin and Hsp20. J Mol Bio 392:1242–1252CrossRefGoogle Scholar
  7. Bakthisaran R, Tangirala R, Rao CM (2015) Small heat shock proteins: role in cellular functions and pathology. Biochim Biophys Acta 1854:291–319CrossRefPubMedGoogle Scholar
  8. Banerjee PR, Pande A, Patrosz J, Thurston GM, Pande J (2011) Cataract-associated mutant E107A of human γD-crystallin shows increased attraction to α-crystallin and enhanced light scattering. Proc Natl Acad Sci U S A 108:574–579CrossRefPubMedGoogle Scholar
  9. Barnwal RP, Jobby MK, Devi KM, Sharma Y, Chary KVR (2009) Solution structure and calcium binding properties of M-crystallin, a primordial βγ-crystallin from archaea. J Mol Biol 386:675–689CrossRefPubMedGoogle Scholar
  10. Basak AK, Bateman O, Slingsby C, Pande A, Asherie N, Ogun O, Benedek G, Pande J (2003) High-resolution X-ray crystal structures of human γD-crystallin (1.25A) and the R58H mutant (1.15A) associated with aculeiform cataract. J Mol Biol 328:1137–1147CrossRefPubMedGoogle Scholar
  11. Basha E, O’Neill H, Vierling E (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends Biochem Sci 37:106–117CrossRefPubMedGoogle Scholar
  12. Bateman OA, Slingsby C (1992) Structural studies on βH-crystallin from bovine eye lens. Exp Eye Res 55:127–133CrossRefPubMedGoogle Scholar
  13. Bateman OA, Sarra A, Van Genesan ST, Kappe G, Lubsen NH, Slingsby C (2003) The stability of human acidic beta-crystallin oligomers and hetero-oligomers. Exp Eye Res 77:409–422CrossRefPubMedGoogle Scholar
  14. Bax B, Lapatto R, Nalini V, Driessen H, Lindley PF, Mahadevan D, Blundell TL, Slingsby C (1990) X-ray analysis of beta-B2-crystallin and evolution of oligomeric lens proteins. Nature 347:776–780CrossRefPubMedGoogle Scholar
  15. Beaulieu CF, Clark JI, Brown RD III et al (1988) Relaxometry of calf lens homogenates, including cross-relaxation by crystallin NH groups. Magn Reson Med 8:45–57CrossRefPubMedGoogle Scholar
  16. Benedek GB (1971) Theory of transparency of the eye. Appl Opt 10:459–473CrossRefPubMedGoogle Scholar
  17. Bettelheim FA (1985) The ocular lens: structure, function, and pathology. In: Maisel H (ed) Marcel Dekker, Inc., New York, pp 265–300Google Scholar
  18. Bettelheim FA, Chen A (1998) Thermodynamic stability of bovine alpha-crystallin in its interactions with other bovine crystallins. Int J Biol Macromol 22:247–252CrossRefPubMedGoogle Scholar
  19. Biswas A, Das KP (2004) Role of ATP on the interaction of alpha-crystallin with its substrates and its implications for the molecular chaperone function. J Biol Chem 279:42648–42657CrossRefPubMedGoogle Scholar
  20. Biswas A, Das KP (2008) Zn2+ enhances the molecular chaperone function and stability of alpha-crystallin. Biochemistry 47:804–816CrossRefPubMedGoogle Scholar
  21. Bloemendal H (1981) The lens proteins. In: Bloemendal H (ed) Molecular and cellular biology of the eye lens. Willey, New York, NY, pp 1–49Google Scholar
  22. Bloemendal H, de Jong WW (1991) Lens proteins and their genes. Prog Nucleic Acid Res Mol Biol 41:259–281CrossRefPubMedGoogle Scholar
  23. 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 Biophy Mol Biol 86:407–485CrossRefGoogle Scholar
  24. Brakenhoff RH, Aarts HJ, Reek FH, Lubsen NH, Schoenmakers JG (1990) Human γ-crystallin genes: a gene family on its way to extinction. J Mol Biol 216:519–532CrossRefPubMedGoogle Scholar
  25. Breitman ML, Lok S, Wistow G, Piatigorsky J, Treton JA, Gold RJ, Tsui LC (1984) Gamma-crystallin family of the mouse lens: structural and evolutionary relationships. Proc Natl Acad Sci U S A 81:7762–7766CrossRefPubMedPubMedCentralGoogle Scholar
  26. Carver JA (1999) Probing the structure and interactions of crystallin proteins by NMR spectroscopy. Prog Retin Eye Res 18:431–462CrossRefPubMedGoogle Scholar
  27. Carver JA, Lindner RA (1998) NMR spectroscopy of α-crystallin, Insights into the structure, interactions and chaperone action of small heat-shock proteins. Int J Biol Macromol 22:197–209CrossRefPubMedGoogle Scholar
  28. Carver JA, Aquilina JA, Truscott RJW, Ralston GB (1992) Identification by 1H NMR spectroscopy of flexible C-terminal extensions in bovine lens α-crystallin. FEBS Lett 311:143–149CrossRefPubMedGoogle Scholar
  29. Carver JA, Aquilina JA, Cooper PG, Williams GA, Truscott RJ (1994) Alpha crystallin: molecular chaperone and protein surfactant. Biochim Biophys Acta 1205:195–206CrossRefGoogle Scholar
  30. Caspers GJ, Leunissen JA, de Jong WW (1995) The expanding small heat-shock protein family, and structure predictions of the conserved α-crystallin domain. J Mol Evol 40:238–248CrossRefGoogle Scholar
  31. Chauhan P, Muralidharan SB, Velappan AB, Datta D, Pratihar S, Debnath J, Ghosh KS (2017a) Inhibition of copper-mediated aggregation of human γD-crsytallin by Schiff bases. J Biol Inorg Chem 22:505–517CrossRefGoogle Scholar
  32. Chauhan P, Velappan AB, Sahoo BK, Debnath J, Ghosh KS (2017b) Studies on molecular interactions between Schiff bases and eye lens chaperone human αA-crystallin. J Lumin 192:148–155CrossRefGoogle Scholar
  33. Chaves JM, Srivastava K, Gupta R, Srivastava OP (2008) Structural and functional roles of deamidation and/or truncation of N- or C-termini in human alpha A-crystallin. Biochemistry 47:10069–10083CrossRefGoogle Scholar
  34. Chen Y, Zhao H, Schuck P, Wistow G (2014) Solution properties of γ-crystallins: compact structure and low frictional ratio are conserved properties of diverse γ-crystallins. Protein Sci 23:76–87CrossRefGoogle Scholar
  35. Chiou SH, Huang CH, Lee IL, Wang YT, Liu NY, Tsay YG, Chen YJ (2010) Identification of in vivo phosphorylation sites of lens proteins from porcine eye lenses by a gel-free phosphoproteomics approach. Mol Vis 16:294–302PubMedPubMedCentralGoogle Scholar
  36. 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 408:118–134CrossRefPubMedPubMedCentralGoogle Scholar
  37. Cooper PG, Aquilina JA, Truscott RJW, Carver JA (1994) Supramolecular order within the lenses: 1HNMR spectroscopic evidence for specific crystallin-crystallin interactions. Exp Eye Res 59:607–616CrossRefGoogle Scholar
  38. Cvekl A, Duncan MK (2007) Genetic and epigenetic mechanisms of gene regulation during lens development. Prog Retin Eye Res 26:555–597CrossRefPubMedPubMedCentralGoogle Scholar
  39. D’Alessio G (2002) The evolution of monomeric and oligomeric betagamma-type crystallins. Facts and hypotheses. Eur J Biochem 269:3122–3130CrossRefGoogle Scholar
  40. Das P, King JA, Zhou R (2010) Beta-strand interactions at the domain interface critical for the stability of human lens gammaD-crystallin. Protein Sci 19:131–140CrossRefPubMedPubMedCentralGoogle Scholar
  41. de Jong WW, Leunissen JA, Voorter CE (1993) Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol 10:103–126Google Scholar
  42. de Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the α-crystallin-small heat shock protein superfamily. Int J Biol Macromol 22:151–162CrossRefPubMedPubMedCentralGoogle Scholar
  43. Delaye M, Tardieu A (1983) Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302:415–417CrossRefPubMedPubMedCentralGoogle Scholar
  44. Delbecq SP, Klevit RE (2013) One size does not fit all: the oligomeric states of alpha-B crystallin. FEBS Lett 587:1073–1080CrossRefPubMedPubMedCentralGoogle Scholar
  45. Dixit K, Pande A, Pande J, Sarma SP (2016) Nuclear magnetic resonance structure of a major lens protein, human gamma γC-crystallin: role of the dipole moment in protein solubility. Biochemistry 55:3136–3149CrossRefPubMedPubMedCentralGoogle Scholar
  46. Farnsworth PN, Groth-Vasselli B, Greenfield NJ, Singh K (1997) Effects of temperature and concentration on bovine lens alpha-crystallin secondary structure: a circular dichroism spectroscopic study. Int J of Biol Macromol 20:283–291CrossRefGoogle Scholar
  47. Flaugh SL, Kosinski-Collins MS, King J (2005a) Interdomain side-chain interactions in human gammaD-crystallin influencing folding and stability. Protein Sci 14:2030–2043CrossRefPubMedPubMedCentralGoogle Scholar
  48. Flaugh SL, Kosinski-Collins MS, King JA (2005b) Contributions of hydrophobic domain interface interactions to the folding and stability of human gammaD-crystallin. Protein Sci 14:569–581CrossRefPubMedPubMedCentralGoogle Scholar
  49. Fu L, Liang JJ (2002) Unfolding of human lens recombinant betaB2 and gammaC-crystallins. J Struct Biol 139:191–198CrossRefPubMedPubMedCentralGoogle Scholar
  50. Fu L, Liang JJ (2003) Alteration of protein-protein interactions of congenital cataract crystallin mutants. Invest Ophthalmol Vis Sci 44:1155–1159CrossRefGoogle Scholar
  51. Ganadu ML, Aru M, Mura GM, Coi A, Mlynarz P, Kozlowski H (2004) Effects of divalent metal ions on the alphaB-crystallin chaperone-like activity: spectroscopic evidence for a complex between copper (II) and protein. J Inorg Biochem 98:1103–1109 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Garrido C, Paul C, Seigneuric R, Kampinga HH (2012) The small heat shock proteins family: the long forgotten. Int J Biochem Cell Biol 44:1588–1592CrossRefPubMedPubMedCentralGoogle Scholar
  53. Ghosh JG, Shenoy AK, Clark JI (2006) N- and C-terminal motifs in human αB crystalline play an important role in the recognition, selection, and solubilization of subtrates. Biochemistry 45:13847–13854CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ghosh KS, Pande A, Pande J (2011) Binding of γ-crystallin substrate prevents the binding of copper and zinc ions to the molecular chaperone α-crystallin. Biochemistry 50:3279–3281CrossRefPubMedPubMedCentralGoogle Scholar
  55. Graw J (2009) Genetics of crystallins: cataract and beyond. Exp Eye Res 88:173–178CrossRefPubMedPubMedCentralGoogle Scholar
  56. Graw J, Löster J, Soewarto D, Fuchs H, Reis A, Wolf E, Balling R, Angelis MH (2002) V76D mutation in a conserved γD-crystallin region leads to dominant cataracts in mice. Mamm Genome 13:452–455CrossRefPubMedPubMedCentralGoogle Scholar
  57. Graw J, Neuhäuser-Klaus A, Klopp N, Selby PB, Löster J, Favor J (2004) Genetic and allelic heterogeneity of Cryg mutations in eight distinct forms of dominant cataract in the mouse. Invest Ophthalmol Vis Sci 45:1202–1213CrossRefPubMedPubMedCentralGoogle Scholar
  58. Gupta R, Srivastava OP (2004a) Deamidation affects structural and functional properties of human alphaA-crystallin and its oligomerization with alphaB-crystallin. J Biol Chem 279:44258–44269CrossRefPubMedPubMedCentralGoogle Scholar
  59. Gupta R, Srivastava OP (2004b) Effect of deamidation of asparagine 146 on functional and structural properties of human lens alphaB-crystallin. Invest Ophthalmol Vis Sci 45:206–214CrossRefPubMedPubMedCentralGoogle Scholar
  60. Hains PG, Truscott RJW (2007) Post-translational modifications in the nuclear region of young, aged, and cataract human lenses. J Proteome Res 6:3935–3943CrossRefPubMedPubMedCentralGoogle Scholar
  61. Haley DA, Horwitz J, Stewart PL (1998) The small heat-shock protein, alpha B-crystallin, has a variable quaternary structure, J Mol. Biol. 277:27–35Google Scholar
  62. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846CrossRefPubMedGoogle Scholar
  63. Hejtmancik JF, Wingfield PT, Chambers C, Russell P, Chen HC, Sergeev YV, Hope JN (1997) Association properties of beta B2- and beta A3-crystallin: ability to form dimmers. Protein Eng 10:1347–1352CrossRefPubMedGoogle Scholar
  64. Hejtmancik JF, Wingfield PT, Sergeev YV (2004) Beta-crystallin association. Exp Eye Res 79:377–383CrossRefPubMedGoogle Scholar
  65. Hochberg GK, Ecroyd H, Liu C, Cox D, Cascio D, Sawaya MR, Collier MP, Stroud J, Carver JA, Baldwin AJ, Robinson CV, Eisenberg DS, Benesch JL, Laganowsky A (2014) The structured core domain of αB-crystallin can prevent amyloid fibrillation and associated toxicity. Proc Natl Acad Sci U S A 111:1562–1570Google Scholar
  66. Horwitz J (1992) α-Crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A 89:10449–10453CrossRefPubMedPubMedCentralGoogle Scholar
  67. Horwitz J, Bova MP, Ding L, Haley DA, Stewart PL (1999) Lens α-crystallin: function and structure. Eye 13:403–408CrossRefPubMedGoogle Scholar
  68. Jaenicke R, Slingsby C (2001) Lens crystallins and their microbial homologs: structure, stability, and function. Crit Rev Biochem Mol Biol 36:435–499CrossRefPubMedGoogle Scholar
  69. Jehle S, van Rossum B, Stout JR, Noguchi SM, Falber K, Rehbein K, Oschkinat H, Klevit RE, Rajagopal P (2009) αB-crystallin: a hybrid solid-state/solution-state NMR investigation reveals structural aspects of the heterogeneous oligomer. J Mol Biol 385:1481–1497CrossRefPubMedGoogle Scholar
  70. Jehle S, Rajagopal P, Bardiaux B, Markovic S, Kühne R, Stout JR, Higman VA, Klevit RE, van Rossum BJ, Oschkinat H (2010) Solid-state NMR and SAXS studies provide a structural basis for the activation of αB-crystallin oligomers. Nat Struct Mol Bio 1371:1037–1042CrossRefGoogle Scholar
  71. Jehle S, Vollmar BS, Bardiaux B, Dove KK, Rajagopal P, Gonen T, Oschkinat H, Klevit RE (2011) N-terminal domain of αB-crystallin provides a conformational switch for multimerization and structural heterogeneity. Proc Natl Acad Sci U S A 108:6409–6414CrossRefPubMedPubMedCentralGoogle Scholar
  72. Ji F, Jung J, Koharudin LMI, Gronenborn AM (2013) The human W42R gamma D-crystallin mutant structure provides a link between congenital and age related cataracts. J Biolog Chem 288:99–109CrossRefGoogle Scholar
  73. Kappé G, Boelens WC, de Jong WW (2010) Why proteins without an α-crystallin domain should not be included in the human small heat shock protein family HSPB. Cell Stress Chaperones 15:457–461CrossRefPubMedGoogle Scholar
  74. Kingsley CN, Brubaker WD, Markovic S, Diehl A, Brindley AJ, Oschkinat H, Martin RW (2013) Preferential and specific binding of human alpha B-crystallin to a cataract-related variant of gamma S-crystallin. Structure 21:2221–2227CrossRefPubMedPubMedCentralGoogle Scholar
  75. Klemenz R, Fröhli E, Steiger RH, Schäferand R, Aoyama A (1991) αB-crystallin is a small heat shock protein. Proc Natl Acad Sci U S A 88:3652–3656CrossRefPubMedPubMedCentralGoogle Scholar
  76. Koenig SH, Brown RD III, Spiller M et al (1992) Intermolecular protein interactions in solutions of calf lens-crystallin: results from 1/T1 nuclear magnetic relaxation dispersion profiles. Biophys J 61:776–785CrossRefPubMedPubMedCentralGoogle Scholar
  77. Kong F, King J (2011) Contributions of aromatic pairs to the folding and stability of long-lived human γD-crystallin. Protein Sci 20:513–528CrossRefPubMedPubMedCentralGoogle Scholar
  78. Kosinski-Collins MS, King J (2003) In vitro unfolding, refolding, and polymerization of human gammaD crystallin, a protein involved in cataract formation. Protein Sci 12:480–490CrossRefPubMedPubMedCentralGoogle Scholar
  79. Kosinski-Collins MS, Flaugh SL, King JA (2004) Probing folding and fluorescence quenching in human gammaD crystallin Greek key domains using triple tryptophan mutant proteins. Protein Sci 13:2223–2235CrossRefPubMedPubMedCentralGoogle Scholar
  80. Kriehuber T, Rattei T, Weinmaier T, Bepperling A, Haslbeck M, Buchner J (2010) Independent evolution of the core domain and its flanking sequences in small heatshock proteins. FASEB J. 24:3633–3642CrossRefPubMedGoogle Scholar
  81. Kundu M, Sen PC, Das KP (2007) Structure, stability, and chaperone function of αAcrystallin: role of N-terminal region. Biopolymers 86:177–192CrossRefPubMedGoogle Scholar
  82. Laganowsky A, Eisenberg D (2010) Non-3D domain swapped crystal structure of truncated zebrafish alpha-crystallin. Protein Sci 19:1978–1984CrossRefPubMedPubMedCentralGoogle Scholar
  83. Laganowsky A, Benesch JLP, Landau M, Ding L, Sawaya MR, Cascio D, Huang Q, Robinson C, Horwitz J, Eisenberg D (2010) Crystal structures of truncated alphaA and alphaB-crystallins reveal structural mechanisms of polydispersity important for eye lens function. Protein Sci 19:1031–1043CrossRefPubMedPubMedCentralGoogle Scholar
  84. Lampi KJ, Ma Z, Shih M, Shearer TR, Smith JB, Smith DL, David LL (1997) Sequence analysis of βA3, βB3, and βA4 crystallins completes the identification of the major proteins in young human lens. J Biol Chem 272:2268–2275CrossRefPubMedGoogle Scholar
  85. Lampi KJ, Ma Z, Hanson SR, Azuma M, Shih M, Shearer TR, Smith DL, Smith JB, David LL (1998) Age-related changes in human lens crystallins identified by two dimensional electrophoresis and mass spectrometry. Exp Eye Res 67:31–43CrossRefPubMedGoogle Scholar
  86. Lampi KJ, Kim YH, Bachinger HP, Boswell BA, Linder RA, Carver JA, Shearer TR, David LL, Kapfer DM (2002) Decreased heat stability and increased chaperone requirement of modified human betaB1-crystallins. Mol. Vis. 8:359–366PubMedGoogle Scholar
  87. Lampi KJ, Wilmarth PA, Murray MR, David LL (2014) Lens β-crystallins: the role of deamidation and related modifications in aging and cataract. Prog Biophys Mol Biol 115:21–31CrossRefPubMedPubMedCentralGoogle Scholar
  88. Liang JJN, Chakrabarti B (1998) Intermolecular interaction of lens crystallins: from rotationally mobile to immobile states at high protein concentrations. Biochem Biophys Res Commun 246:441–445CrossRefPubMedGoogle Scholar
  89. Liang JN, Li XY (1991) Interaction and aggregation of lens crystallins. Exp Eye Res 53:61–66CrossRefPubMedGoogle Scholar
  90. Lubsen NH, Aarts HJ, Schoenmakers JG (1988) The evolution of lenticular proteins: the beta- and gamma-crystallin super gene family. Prog Biophys Mol Biol 51:47–76CrossRefPubMedGoogle Scholar
  91. MacDonald JT, Purkiss AG, Smith MA, Evans P, Goodfellow JM, Slingsby C (2005) Unfolding crystallins: the destabilizing role of a beta-hairpin cysteine in betaB2-crystallin by simulation and experiment. Protein Sci 14:1282–1292CrossRefPubMedPubMedCentralGoogle Scholar
  92. Mach H, Trautman PA, Thomson JA, Lewis RV, Middaugh CR (1990) Inhibition of alpha-crystallin aggregation by gamma-crystallin. J Biol Chem 265:4844–4848PubMedGoogle Scholar
  93. Mainz A, Bardiaux B, Kuppler F, Multhaup G, Felli IC, Pierattelli R, Reif B (2012) Structural and mechanistic implications of metal binding in the small heat-shock protein αB-crystallin. J Biol Chem 287:1128–1138CrossRefPubMedGoogle Scholar
  94. Manski W, Naliitowski K, Boxitsis G (1979) Immunochemical studies on lens protein-protein complexes I. the heterogeneity and structure of complexed α-crystallin. Exp Eye Res 29:625–635CrossRefPubMedGoogle Scholar
  95. Merck KB, de Haard-Hoekman WA, Oude Essink BB, Bloemendal H, de Jong WW (1992) Expression and aggregation of recombinant αA-crystallin and its two domains. Biochim Biophys Acta 1130:267–276CrossRefPubMedGoogle Scholar
  96. Merck KB, Horwitz J, Kersten M, Overkamp P, Gaestel M, Bloemendal H, de Jong WW (1993) Comparison of the homologous carboxy-terminal domain and tail of α-crystallin and small heat shock protein. Mol Biol Rep 18:209–215CrossRefPubMedGoogle Scholar
  97. Mills IA, Flaugh SL, Kosinski-Collins MS, King JA (2007) Folding and stability of the isolated Greek key domains of the long-lived human lens proteins γD-crystallin and γS-crystallin. Protein Sci 16:2427–2444CrossRefPubMedPubMedCentralGoogle Scholar
  98. Mills-Henry IAR (2007) Stability, unfolding, and aggregation of the gamma D and gamma S human eye lens crystallins. Ph.D. thesis from Department of Biology, MIT, Cambridge, USAGoogle Scholar
  99. Mishra A, Krishnan B, Swaroop SS, Sharma Y (2014) Microbial βγ-crystallins. Prog Biophys Mol Biol 115:42–51CrossRefPubMedGoogle Scholar
  100. Moreau KL, King J (2009) Hydrophobic core mutations associated with cataract development in mice destabilize human gamma D-crystallin. J Biol Chem 284:33285–33295CrossRefPubMedPubMedCentralGoogle Scholar
  101. Moreau KL, King JA (2012) Cataract-causing defect of a mutant gamma crystallin proceeds through an aggregation pathway which bypasses recognition by the alpha-crystallin chaperone. PLoS ONE 7:e37256CrossRefPubMedPubMedCentralGoogle Scholar
  102. Morgan CF, Schleich T, Caines GH, Farnsworth PN (1989) Elucidation of intermediate (mobile) and slow (solid like) protein motions in bovine lens homogenates by carbon-13 NMR spectroscopy. Biochemistry 28:5065–5074CrossRefPubMedGoogle Scholar
  103. Peschek J, Braun N, Rohrberg J, Back KC, Kriehuber T, Kastenmüller A, Weinkauf S, Buchner J (2013) Regulated structural transitions unleash the chaperone activity of αB-crystallin. Proc Natl Acad Sci U S A 110:3780–3789CrossRefGoogle Scholar
  104. Ponce A, Takemoto L (2005) Screening of crystallin-crystallin interactions using microequilibrium dialysis. Mol Vis 11:752–757PubMedPubMedCentralGoogle Scholar
  105. Purkiss AG, Bateman OA, Goodfellow JM, Lubsen NH, Slingsby C (2002) The X-ray crystal structure of human gamma S-crystallin C-terminal domain. J Biol Chem 277:4199–4205CrossRefPubMedGoogle Scholar
  106. Purkiss AG, Bateman OA, Wyatt K, Wilmarth PA, David LL, Wistow GJ, Slingsby C (2007) Biophysical properties of γC-crystallin in human and mouse eye lens: the role of molecular dipoles. J Mol Biol 372:205–222CrossRefPubMedPubMedCentralGoogle Scholar
  107. Ray NJ (2015) Biophysical chemistry of the ageing eye lens. Biophys Rev 7:353–368CrossRefPubMedPubMedCentralGoogle Scholar
  108. Reddy GB, Kumar PA, Kumar MS (2006) Chaperone-like activity and hydrophobicity of alpha-crystallin. IUBMB Life 58:632–641CrossRefPubMedGoogle Scholar
  109. Richardson JS (1977) Beta-sheet topology and the relatedness of proteins. Nature 268:495–500CrossRefPubMedGoogle Scholar
  110. Robinson NE, Lampi KJ, Speir JP, Kruppa G, Easterling M, Robinson AB (2006) Quantitative measurement of young human eye lens crystallins by direct injection Fourier transform ion cyclotron resonance mass spectrometry. Mol Vis 12:704–711PubMedGoogle Scholar
  111. Schafheimer N, King J (2013) Tryptophan cluster protects human γD-crystallin from ultraviolet radiation-induced photoaggregation in vitro. Photochem Photobiol 89:1106–1115CrossRefPubMedPubMedCentralGoogle Scholar
  112. Serebryany E, King JA (2014) The βγ-crystallins: native state stability and pathways to aggregation. Prog Biophys Mol Biol 115:32–41CrossRefPubMedPubMedCentralGoogle Scholar
  113. Sharma V, Ghosh KS (2017) Inhibition of amyloid fibrillation and destabilization of fibrils of human γD-crystallin by direct red 80 and orange G. Intl J Biol Macromol 105:956–964CrossRefGoogle Scholar
  114. Sharma V, Ghosh KS (2019) Inhibition of amyloid fibrillation by small molecules and nanomaterials: strategic development of pharmaceuticals against amyloidosis. Prot Pept Lett (accepted)Google Scholar
  115. Sharma KK, Santhoshkumar P (2009) Lens aging: effects of crystallins. Biochim Biophys Acta 1790:1095–1108CrossRefPubMedPubMedCentralGoogle Scholar
  116. Siezen RI, Hoenders HJ (1979) The quaternary structure of bovine α-crystallin. Surface probing by limited proteolysis in vitro. Eur J Biochem 96:431–440CrossRefPubMedGoogle Scholar
  117. Siezen RJ, Owen EA (1983) Interactions of lens proteins: self-association and mixed-association studies of bovine α -crystallin and γ-crystallin. Biophys Chem 18:181–194CrossRefPubMedGoogle Scholar
  118. Siezen RJ, Thomson JA, Kaplan ED, Benedek GB (1987) Human lens gamma crystallins: isolation, identification, and characterization of the expressed gene products. Proc Natl Acad Sci U S A 84:6088–6092CrossRefPubMedPubMedCentralGoogle Scholar
  119. 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 276:9308–9315CrossRefPubMedGoogle Scholar
  120. Slingsby C, Bateman OA (1990) Quaternary interactions in eye lens beta-crystallins: basic and acidic subunits of beta-crystallins favor heterologous association. Biochemistry 29:6592–6599CrossRefPubMedGoogle Scholar
  121. Slingsby C, Clout NJ (1999) Structure of the crystallins. Eye (Lond) 13:395–402CrossRefGoogle Scholar
  122. Slingsby C, Norledge B, Simpson A, Bateman OA, Wright G, Driessen HPC, Lindley PF, Moss DS, Bax B (1997) X-ray diffraction and structure of crystallins. Prog Ret Eye Res 16:3–29CrossRefGoogle Scholar
  123. Smith MA, Bateman OA, Jaenicke R, Slingsby C (2007) Mutation of interfaces in domain-swapped human βB2-crystallin. Protein Sci 16:615–625CrossRefPubMedPubMedCentralGoogle Scholar
  124. Spector A (1964) Methods of isolation of alpha, beta, and gamma crystallins and their subgroups. Invest Ophthalmol 3:182–193PubMedGoogle Scholar
  125. Srivastava K, Chaves JM, Srivastava OP, Kirk M (2008) Multi-crystallin complexes exist in the water-soluble high molecular weight protein fractions of aging normal and cataractous human lenses. Exp Eye Res 87:356–366CrossRefPubMedGoogle Scholar
  126. Stevens A, Wang SX, Caines GH, Schleich T (1995) 13C-NMR off-resonance rotating frame spin-lattice relaxation studies of bovine lens gamma-crystallin self association: effect of macromolecular crowding. Biochim Biophys Acta 1246:82–90CrossRefPubMedGoogle Scholar
  127. Stradner A, Foffi G, Dorsaz N, Thurston G, Schurtenberger R (2007) New insight into cataract formation: enhanced stability through mutual attraction. Phys Rev Lett 99:198103-1–198103-4CrossRefGoogle Scholar
  128. Sun TX, Akhtar NJ, Liang JJ (1999) Thermodynamic stability of human lens recombinant alphaA- and alphaB-crystallins. J Biol Chem 274:34067–34071CrossRefPubMedGoogle Scholar
  129. Takemoto LJ, Ponce A (2006) Decreased association of aged alpha-crystallins with gamma crystallins. Exp Eye Res 83:793–797CrossRefPubMedGoogle Scholar
  130. Takemoto L, Sorensen CM (2008) Protein-protein interactions and lens transparency. Exp Eye Res 87:496–501CrossRefPubMedPubMedCentralGoogle Scholar
  131. Takemoto L, Ponce A, Sorensen CM (2008) Age-dependent association of gamma crystallins with aged alpha crystallins from old bovine lens. Mol. Vis. 14:970–974PubMedPubMedCentralGoogle Scholar
  132. Tardieu A, Veretout F, Krop B, Slingsby C (1992) Protein interactions in the calf eye lens: interactions between alpha-crystallins are repulsive whereas in gamma-crystallins they are attractive. Eur Biophys J 21:1–12CrossRefPubMedGoogle Scholar
  133. Thurston GM, Pande J, Ogun O, Benedek GB (1999) Static and quasielastic light scattering and phase separation of concentrated ternary mixtures of bovine alpha and gammaB crystallins. Invest Ophthalmol Vis Sci 40:S299Google Scholar
  134. Treweek TM, Rekas A, Walker MJ, Carver JA (2010) A quantitative NMR spectroscopic examination of the flexibility of the C-terminal extensions of the molecular chaperones, αA- and αB-crystallin. Exp Eye Res 91:691–699Google Scholar
  135. Treweek TM, Meehan S, Ecroyd H, Carver JA (2015) Small heat-shock proteins: important players in regulating cellular proteostasis. Cell Mol Life Sci 72:429–451CrossRefPubMedPubMedCentralGoogle Scholar
  136. Vendra VPR, Khan I, Chandani S, Muniyandi A, Balasubramanian D (2016) Gamma crystallins of the human eye lens. Biochim Biophys Acta 1860:333–343CrossRefPubMedGoogle Scholar
  137. Veretout F, Delaye M, Tardieu A (1989) Molecular basis of eye lens transparency: osmotic pressure and X-ray analysis of α-crystallin solutions. J Mol Biol 205:713–728CrossRefPubMedPubMedCentralGoogle Scholar
  138. Voorter CEM, Mulders JW, Bloemendal H, de Jong WW (1986) Some aspects of the phosphorylation of α-crystallin A. Eur J Biochem 160:203–210CrossRefPubMedPubMedCentralGoogle Scholar
  139. Wang Y, Petty SA, Trojanowski AT, Knee KM, Goulet DR, Mukerji I, King JA (2010) Formation of amyloid fibrils in vitro from partially unfolded intermediates of human gamma C-crystallin. Invest Ophthalmol Vis Sci 51:672–678CrossRefPubMedPubMedCentralGoogle Scholar
  140. Wenk M, Herbst R, Hoeger D, Kretschmar M, Lubsen NH, Jaenicke R (2000) Gamma S crystallin of bovine and human eye lens: solution structure, stability and folding of the intact two-domain protein and its separate domains. Biophys Chem 86:95–108CrossRefPubMedPubMedCentralGoogle Scholar
  141. West SK, Duncan DD, Munoz B, Rubin GS, Fried LP, Bandeen-Roche K, Schein OD (1998) Sunlight exposure and risk of lens opacities in a population-based study: the Salisbury Eye Evaluation project. J Am Med Assoc 280:714–718CrossRefGoogle Scholar
  142. Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504CrossRefPubMedPubMedCentralGoogle Scholar
  143. Wu Z, Delaglio F, Wyatt K, Wistow G, Bax A (2005) Solution structure of gamma-S-crystallin by molecular fragment replacement NMR. Protein Sci 14:3101–3114CrossRefPubMedPubMedCentralGoogle Scholar
  144. Wu JW, Chen ME, Wen WS, Chen WA, Li CT, Chang CK, Lo CH, Liu HS, Wang SS (2014) Comparative analysis of human γD-crystallin aggregation under physiological and low pH conditions. PLoS ONE 9(11):e112309.  https://doi.org/10.1371/journal.pone.0112309CrossRefPubMedPubMedCentralGoogle Scholar
  145. Xia Z, Yang ZX, Huynh T, King JA, Zhou RH (2013) UV-radiation induced disruption of dry-cavities in human γD-crystallin results in decreased stability and faster unfolding. Sci Rep 3:1560CrossRefPubMedPubMedCentralGoogle Scholar
  146. Yang Z, Xia Z, Huynh T, King JA, Zhou R (2014) Dissecting the contributions of β-hairpin tyrosine pairs to the folding and stability of long-lived human γD-crystallins. Nanoscale 6:1797–1807CrossRefPubMedPubMedCentralGoogle Scholar
  147. Yoshida H, Yumoto N, Tsukahara I, Murachi T (1986) The degradation of α-crystallin at its carboxyl-terminal portion by calpain in bovine lens. Invest Ophthalmol Vis Sci 27:1269–1273PubMedGoogle Scholar
  148. Zhao H, Chen Y, Rezabkova L, Wu Z, Wistow G, Schuck P (2014) Solution properties of γ-crystallins: hydration of fish and mammal γ-crystallins. Protein Sci 23:88–99CrossRefPubMedGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of ChemistryNational Institute of Technology HamirpurHamirpurIndia

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