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Vertebrate Crystallins--from Proteins to Genes

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Abstract

A review of literature on tissue-specific proteins of the vertebrate eye lens and genes coding for these proteins is presented. Particular attention is paid to the most heterogeneous family of crystallins: β- and γ-crystallins, their nomenclature, and the structure of their genes. It is pointed out that mutations in gene coding for ubiquitous crystallins may be related to some forms of cataracts.

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REFERENCES

  • Aarts, H.J.M., den Dunnen, J.T., Lubsen, N.H., and Schoenmakers, J.G.G., Linkage between the β3B2 and βB3 Crystallin Genes in Man and Rat: A Remnant of an Ancient β-Crystallin Gene Cluster, Gene, 1987, vol. 59, no. 1, pp.127–135.

    PubMed  Google Scholar 

  • Andley, U.P., Mathur, S., Griest, T.A., and Petrash, J.M., Cloning, Expression, and Chaperon-Like Activity of Human αA-Crystallin, J. Biol. Chem., 1996, vol. 271, no. 50, pp. 31 973–31 980.

    Google Scholar 

  • Augusteyn, R.C. and Koretz, J.F., Hypothesis: A Possible Structure for α-Crystallin, FEBS Lett., 1987, vol. 222, no. 1, pp. 1–5.

    PubMed  Google Scholar 

  • Bagchi, M., Alcala, J.R., and Maisel, H., Delta Crystallin Synthesis by the Adult Chicken Lens, Exp. Eye Res., 1981, vol. 32, no. 3, pp. 251–254.

    PubMed  Google Scholar 

  • Berbers, G.A.M., Boerman, O.C., Bloemendal, H., and de Jong, W.W., Primary Gene Products of Bovine α-Crystallin and Reassociation Behavior of Its Aggregates, Eur. J. Biochem., 1982, vol. 128, nos. 2–3, pp. 495–502.

    PubMed  Google Scholar 

  • Berbers, G.A.M., Hoekman, W.A., Bloemendal, H., et al., Proline-and Alanine-Rich N-Terminal Extension of the Basic Bovine α-Crystallin B1 Chains, FEBS Lett., 1983, vol. 161, no. 2, pp. 225–229.

    PubMed  Google Scholar 

  • Berbers, G.A.M., Hoekman, W.A., Bloemendal, H., et al., Homology between the Primary Structures of the Major Bovine α-Crystallin Chains, Eur. J. Biochem., 1984, vol.139, no. 3, pp. 467–479.

    PubMed  Google Scholar 

  • Bhat, S.P. and Piatigorsky, J., Molecular Cloning and Partial Characterization of γ-Crystallin cDNA Sequences in a Bacterial Plasmid, Proc. Natl. Acad. Sci. USA, 1979, vol.76, no. 7, pp. 3299–3303.

    PubMed  Google Scholar 

  • Bhat, S.P. and Nagineni, N., αB Subunit of Lens-Specific γ-Crystallin Is Present in Other Ocular and Nonocular Tissues, Biochem. Biophys. Res. Commun., 1989, vol. 158, no. 1, pp. 319–325.

    PubMed  Google Scholar 

  • Bindels, J.G., Siezen, R.J., and Hoenders, H.J., A Model for the Architecture of α-Crystallin, Opthalmic Res., 1979, vol. 11, nos. 7–8, pp. 441–447.

    Google Scholar 

  • Bindels, J.G., Koopers, A., and Hoenders, H.J., Structural Aspects for Bovine β-Crystallins: Physical Characterization Including Dissociation-Association Behavior, Exp. Eye Res., 1981, vol. 33, no. 3, pp. 333–343.

    PubMed  Google Scholar 

  • Bindels, J.G., Bessems, G.J.J., de Man, B.M., and Hoenders, H.J., Comparative and Age-Dependent Aspects of Crystallin Size and Distribution in Human, Rabbit, Bovine, Rat, Chicken, Duck, Frog, and Dogish Lenses, Comp. Biochem. Physiol., 1983, vol. 76B, no. 1, pp. 47–55.

    Google Scholar 

  • Bjork, I., Studies on α-Crystallin from Calf Lens. I. Isolation by Gel Filtration, Exp. Eye Res., 1961, vol. 1, no. 3, pp.145–154.

    PubMed  Google Scholar 

  • Bjork, I., Studies on γ-Crystallin from Calf Lens. I. Purification and Some Properties of the Main Protein Components, Exp. Eye Res., 1964, vol. 3, no. 4, pp. 254–261.

    Google Scholar 

  • Bloemendal, H., Report on the Symposium on the Biochemistry of the Lens, Exp. Eye Res., 1969, vol. 8, no. 3, pp.227–240.

    PubMed  Google Scholar 

  • Bloemendal, H., The Lens Proteins, in Molecular and Cellular Biology of the Eye Lens, Bloemendal, H., Ed., New York: John Wiley & Sons, 1981, pp. 1–47.

    Google Scholar 

  • Bloemendal, H., Lens Proteins, Critical Rev. Biochem., 1982, vol. 12, no. 2, pp. 1–38.

    Google Scholar 

  • Bloemendal, H., Zweers, A., Vermorken, F., et al., The Plasma Membranes of Eye Lens Fibers: Biochemical and Structural Characterization, Cell Differ., 1972a, vol.1, no. 2, pp. 91–106.

    PubMed  Google Scholar 

  • Bloemendal, H., Berns, T., Zweers, A., et al., The State of Aggregation of α-Crystallin Detected after Large-Scale Preparation by Zonal Centrifugation, Eur. J. Biochem., 1972b, vol. 24, no. 3, pp. 401–406.

    PubMed  Google Scholar 

  • Bloemendal, H., Vermorken, A.J.M., Kibbelaar, M., et al., Nomenclature for the Polypeptides of the Lens Membranes, Exp. Eye Res., 1977, vol. 24, no. 3, pp. 413–415.

    PubMed  Google Scholar 

  • Bloemendal, H. and Groenewoud, G., One-Step Separation of the Subunits of α-Crystallin by Chromatofocusing in 6 M Urea, Analyt. Biochem., 1981, vol. 117, no. 2, pp.327–329.

    PubMed  Google Scholar 

  • Bloemendal, H., Voorter, C.E.M., and de Jong, W.W., Rational Nomenclature of Alpha Crystallin Subunits, Ophthalmic Res., 1988, vol. 20, no. 6, pp. 380–382.

    PubMed  Google Scholar 

  • Blow, A.M.J., van Heyningen, R., and Barrett, A.J., Metal-Dependent Proteinase of the Lens. Assay Purification and Properties of the Bovine Enzyme, Biochem. J., 1975, vol. 145, no. 3, pp. 591–599.

    PubMed  Google Scholar 

  • Blundell, T., Lindley, P.F., Moss, D.S., et al., The Low-Reolution Structure Analysis of the Lens Protein γ-Crystallin, Acta Crystallographica, 1978, vol. B34, Pt. 12, pp. 3653–3657.

    Google Scholar 

  • Blundell, T., Lindley, P., Miller, L., et al., The Molecular Structure and Stability of the Eye Lens: X-Ray Analysis of γ-Crystallin II, Nature, 1981, vol. 289, no. 5800, pp.771–777.

    PubMed  Google Scholar 

  • Bossier, P., Fitsch, I.T., and Tuite, M.F., Structure and Expression of a Yeast Gene Encoding the Small Heat-Shock Protein Hsp 26, Gene, 1989, vol. 78, no. 2, pp.323–330.

    PubMed  Google Scholar 

  • Bours, J., Free Isoelectric Focusing of Bovine Lens γ-Crystallin, Exp. Eye Res., 1973, vol. 16, no. 6, pp. 501–515.

    PubMed  Google Scholar 

  • Bours, J., Isoelectric Focusing and Immunochemistry of Lens Crystallins, Docum. Ophthalmologica, 1974, vol.37, no. 1, pp. 1–46.

    Google Scholar 

  • Bours, J. and Delmotte, P., Age-Dependent Variations in the Composition of the Crystallins and Albuminoid of the Mouse Lens Studied by Isolelectric Focusing and Isotachophoresis, Sol. Tools, 1979, vol. 26, no. 4, pp. 58–64.

    Google Scholar 

  • Brahma, S.K. and Bours, J., Thin Layer Isoelectric Focusing of the Soluble Lens Extracts from Larval Stages and Adult Xenopus laevis, Exp. Eye Res., 1972, vol. 13, no. 4, pp. 309–314.

    Google Scholar 

  • Brahma, S.K., Rabaey, M., and van Doorenmaalen, W.J., Ontogeny and Localization of γ-Crystallin Antigen in the Developing Pigeon (Columbia livia) Lens, Exp. Eye Res., 1972, vol. 14, no. 2, pp. 130–134.

    PubMed  Google Scholar 

  • Brahma, S.K. and McDevitt, D.S., Ontogeny and Localization of γ-Crystallins in Rana temporaria, Ambystoma mexicanum, and Pleurodeles waltlii Normal Lens Development, Exp. Eye Res., 1974, vol. 19, no. 4, pp. 379–387.

    PubMed  Google Scholar 

  • Brahma, S.K. and van der Starre, H., Studies on Biosynthesis of Soluble Lens Crystallin Antigens in the Cnick by Isoelectric Focusing in Thin-Layer Polyacrylamide Gel., Exp. Cell Res., 1976, vol. 97, no. 1, pp. 175–183.

    PubMed  Google Scholar 

  • Brahma, S.K. and van Doorenmaalen, W.J., Preparation of Specific Antiserum Against Rana esculenta Pre-αLens Crystallin, Experientia, 1976, vol. 32, no. 7, pp. 930–931.

    PubMed  Google Scholar 

  • Brahma, S.K., Ontogeny and Localization of Pre-αCrystallin Antigen in Rana temporaria Lens Development, Exp. Eye Res., 1977, vol. 25, no. 3, pp. 311–315.

    Google Scholar 

  • Brakenhoff, R.H., Aarts, H.J.M., Reek, F.H., et al., Human α-Crystallin Genes. A Gene Family on Its Way to Extinction, J. Mol. Biol., 1990, vol. 216, no. 3, pp. 519–532.

    PubMed  Google Scholar 

  • Campbell, J.C., Clayton, R.M., and Truman, D.E.S., Antigens of the Lens of Xenopus laevis, Exp. Eye Res., 1968, vol. 7, no. 1, pp. 4–10.

    PubMed  Google Scholar 

  • Carper, D., Nishimura, C., Shinohara, T., et al., Aldose Reductase and α-Crystallin Belong to the Same Protein Superfamily As Aldehyde Reductase, FEBS Lett., 1987, vol. 220, no. 1, pp. 209–213.

    PubMed  Google Scholar 

  • Carver, J.A., Aquilina, J.A., and Truscott, R.J., A Possible Chaperone-Like Quaternary Structure for α-Crystallin, Exp. Eye Res., 1994, vol. 59, no. 2, pp. 231–234.

    PubMed  Google Scholar 

  • Chiou, S.-H., Biochemical Characterization of Crystallins from Frog Lenses, Int. J. Peptide Prot. Res., 1987, vol.30, no. 1, pp. 108–116.

    Google Scholar 

  • Chiou, S.-H., Chang, W.-P., Kuo, J., et al., Biochemical Comparison of γ-Crystallins from Duck and Frog Eye Lenses, FEBS Lett., 1986, vol. 196, no. 2, pp. 219–222.

    PubMed  Google Scholar 

  • Chiou, S.-H., Chang, W.-P., Lo, C.-H., and Chen, S.-W., Sequence Comparison of α-Crystallins from the Reptilian and Other Vertebrate Species, FEBS Lett., 1987, vol.221, no. 1, pp. 134–138.

  • Chiou, S.-H., Pan, F.-M., Peng, H.-S., et al., Characterization of γ-S-Crystallin Isoforms from a Catfish: Evolutionary Comparison of Various γ-, γS-, and β-Crystallins, Biochem. Biophys. Res. Commun., 1998, vol. 252, no. 2, pp.412–419.

    PubMed  Google Scholar 

  • Chirgadze, Yu.N., Nikonov, S.V., Garber, M.B., and Reshetnikova, L.S., Crystallographic Study of γ-Crystallins from Calf Lens, J. Mol. Biol., 1977, vol. 110, no. 3, pp.619–624.

    PubMed  Google Scholar 

  • Clayton, R.M., Cambell, J.C., and Truman, D.E.S., A Re-Examination of the Organ Specificity of Lens Antigens, Exp. Eye Res., 1968, vol. 7, no. 1, pp. 11–29.

    PubMed  Google Scholar 

  • Cohen, L.H., Westerhuis, L.W., de Jong, W.W., and Bloemendal, H., Rat γ-Crystallin A Chain with an Insertion of 22 Residues, Eur. J. Biochem., 1978, vol. 89, no. 1, pp.259–266.

    PubMed  Google Scholar 

  • Crable, J.C., Partial Sequence Homology of Human myc Oncogene Protein to Beta and Gamma Crystallins, FEBS Lett., 1985, vol. 181, no. 1, pp. 157–159.

    PubMed  Google Scholar 

  • Croft, L.R., The Amino Acid Sequence of γ-Crystallin (Fraction II) from Calf Lens, Biochem. J., 1972, vol. 128, no.4, pp. 961–970.

    PubMed  Google Scholar 

  • Cuypers, H.Th., van Loon-Klaassen, L.A.H., Vree Egberts,W.T.M., et al., The Primary Structure of Leucine Aminopeptidase from Bovine Eye Lens, J. Biol. Chem., 1982, vol. 257, no. 12, pp. 7077–7085.

    PubMed  Google Scholar 

  • van Dam, A.F., Purification and Composition Studies of α2S-Crystallin, Exp. Eye Res., 1966, vol. 5, no. 4, pp. 255–266.

    PubMed  Google Scholar 

  • van Dam, A.F. and ten Cate, G., Isolation and Some Properties of Bovine β-Crystallin, Biochim. Biophys. Acta, 1966, vol. 121, no. 1, pp. 183–186.

    PubMed  Google Scholar 

  • Delcour, J. and Papaconstantinou, J., A Change in the Stoichiometry of Assembly of Bovine Lens α-Crystallin Subunits in Relation to Cellular Differentiation, Biochim. Biophys. Res. Commun., 1974, vol. 57, no. 1, pp.134–141.

    Google Scholar 

  • Delcour, J. and Bouchet, H., Evidence for a Post-Translational Origin of Subunit αB1 in the Bovine Lens α-Crystallin, Exp. Eye Res., 1978, vol. 26, no. 2, pp. 191–195.

    PubMed  Google Scholar 

  • Dodemont, H.J., Andreoli, P.M., Moormann, R.J.M., et al., Molecular Cloning of mRNA Sequences Encoding Rat Lens Crystallins, Proc. Natl. Acad. Sci. USA, 1981, vol.78, no. 9, pp. 5320–5324.

    PubMed  Google Scholar 

  • Driessen, H.P.C., Herbrink, P., Bloemendal, H., and de Jong,W.W., Primary Structure of the Bovine β-Crystallin Bp Chain, Eur. J. Biochem., 1981, vol. 121, no. 1, pp.83–91.

    PubMed  Google Scholar 

  • Duguid, J.R., Rohwer, R.G., and Seed, B., Isolation of cDNAs of Scrapie-Modulated RNAs by Subtractive Hybridization of a cDNA Library, Proc. Natl. Acad. Sci. USA, 1988, vol. 85, no. 15, pp. 5738–5742.

    PubMed  Google Scholar 

  • Duncan, M.K., Roth, H.J., Thompson, M., et al., Chicken βB1 Crystallin: Gene Sequences and Evidence for Functional Conservation of Promoter Activity between Chicken and Mouse, Biochim. Biophys. Acta, 1995, vol.1261, no. 1, pp. 68–76.

    PubMed  Google Scholar 

  • Francis, P.J., Berry, V., Moore, A.T., and Bhattacharya, S., Lens Biology: Development and Human Cataractogenesis, Trends Genet., 1999, vol. 15, no. 5, pp. 191–196.

    PubMed  Google Scholar 

  • Gorgolyuk, N.A., Mikhailov, A.T., and Barabanov, V.M., Immunochemical Markers of Differentiation of Rana temporaria Lens in Embryonic Development. II. Immunochemical Analysis of the Appearance and Localization of Individual Classes of Lens Proteins, Ontogenez, 1978, vol. 9, no. 5, pp. 449–457.

    PubMed  Google Scholar 

  • Graham, C., Hodin, J., and Wistow, G., A Retinaldehyde Dehydrogenase As a Structural Protein in a Mammalian Eye Lens. Gene Recruitment of ŋ-Crystallin, J. Biol. Chem., 1996, vol. 271, no. 26, pp. 15 623-15 628.

    Google Scholar 

  • Green, P., Lipman, B., Hiller, L., et al., Ancient Conserved Regions in New Gene Sequences and the Protein Databases, Science, 1993, vol. 259, no. 5102, pp. 1711–1723.

    PubMed  Google Scholar 

  • Groenen, P.J.T.A., Merck, K.B., de Jong, W.W., and Bloemendal, H., Structure and Modification of the Junior Chaperon γ-Crystallin from Lens Transparency to Molecular Pathology, Eur. J. Biochem., 1994, vol. 225, no. 1, pp. 1–19.

    PubMed  Google Scholar 

  • Groth-Vasselli, B., Kumosinski, T.F., and Farnsworth, P.N., Computer-Generated Model of the Quartenary Structure of η-Crystallin in the Lens, Exp. Eye Res., 1995, vol. 61, no. 2, pp. 249–253.

    PubMed  Google Scholar 

  • Hanson, H., Glasser, D., and Kirschke, H., Leucinaminopeptidase aus Rinderaugenlinsen. Kristallisation, Eigensehaften und optimale Wirkungsweise, Hoppe-Seil. Zeit Physiol. Chem., 1965, vol. 340, no. 1, pp. 107–125.

    Google Scholar 

  • Harding, J.J. and Dilley, J., Structural Proteins of the Mammalian Lens: A Review with Emphasis on Changes in Development, Aging and Cataract, Exp. Eye Res., 1976, vol. 22, no. 1, pp. 1–73.

    PubMed  Google Scholar 

  • Hejtmancik, J.F., The Genetics of Cataract: Our Vision Becomes Clearer, Amer. J. Hum. Genet., 1998, vol. 62, no. 3, pp. 520–525.

    PubMed  Google Scholar 

  • Hendriks, W., Mulders, J.W.M., Bibby, M.A., et al., Duck Lens α-Crystallin and Lactate Dehydrogenase B4 Are Identical: A Single-Copy Gene Product with Two Distinct Functions, Proc. Natl. Acad. Sci. USA, 1988, vol.85, no. 19, pp. 7114–7118.

    PubMed  Google Scholar 

  • Herbrink, P. and Bloemendal, H., Studies on β-Crystallin. I. Isolation and Partial Characterization of the Principal Polypeptide Chain, Biochim. Biophys. Acta, 1974, vol.336, no. 3, pp. 370–382.

    Google Scholar 

  • Herbrink, P., van Westreenen, H., and Bloemendal, H., Further Studies on the Polypeptide Chains of β-Crystallin, Exp. Eye Res., 1975, vol. 20, no. 6, pp. 541–548.

    PubMed  Google Scholar 

  • Hill, R.E., Favor, J., Hogan, B.L., et al., Mouse Small Eye Results from Mutants in a Paired-Like Homeobox-Containing Genes, Nature, 1991, vol. 354, no. 6354, pp.522–525.

    PubMed  Google Scholar 

  • Hockwin, O. and Ohrloff, C., Enzymes in Normal, Aging and Cataractous Lenses, Molecular and Cellular Biology of the Eye Lens, Bloemendal, H., Ed., New York: Jon Wiley and Sons, 1981, pp. 367–414.

    Google Scholar 

  • Huang, Q.L., Russel, P., Stone, S.H., and Zigler, J.S.,, Zeta-Crystallin, a Novel Lens Protein from the Guinea Pig, Current Eye Res., 1987, vol. 6, no. 5, pp. 725–732.

    Google Scholar 

  • Inana, G., Shinohara, T., Maisel, J.V., Jr., and Piatigorsky, J., Evolution and Diversity of the Crystallins. Nucleotide Sequence of a β-Crystallin mRNA from the Mouse Lens, J. Biol. Chem., 1982, vol. 257, no. 15, pp. 9064–9071.

    PubMed  Google Scholar 

  • Inana, G., Piatigorsky, J., Normal, B., et al., Gene and Protein Structure of a α-Crystallin Polypeptide in Murine Lens: Relationship of Exons and Structural Motifs, Nature, 1983, vol. 302, no. 5906, pp. 310–315.

    PubMed  Google Scholar 

  • Ingolia, T.D. and Craig, E.A., Four Small Drosophila Heat Shock Proteins Are Related to Each Other and to Mammalian β-Crystallin, Proc. Natl. Acad. Sci. USA, 1982, vol. 79, no. 7, pp. 2360–2364.

    PubMed  Google Scholar 

  • Jimenez-Asensio, J., Gonzalez, P., Zigler, J.S., Jr., and Garland, D.L., Glyceraldehyde 3-Phosphate Dehydrogenase Is an Enzyme-Crystallin in Diurnal Geskos of the Genus Phelsuma, Biochem. Biophys. Res. Commun., 1995, vol.209, no. 3, pp. 796–802.

    PubMed  Google Scholar 

  • De Jong, W.W., van der Ouderaa, F.J., Versteeg, M., et al., Primary Structures of the α-Crystallin A Chains of Seven Mammalian Species, Eur. J. Biochem., 1975, vol. 53, no. 1, pp. 237–242.

    Google Scholar 

  • De Jong, W.W., Nuy-Terwindt, E.C., and Versteeg, M., Primary Structures of α-Crystallin A Chains of Elephant, Whale, Hyrax and Rhinoceros, Biochim. Biophys. Acta, 1977, no. 2, pp. 573–580.

  • De Jong, W.W., Stapel, S.O., and Zweers, A., A Comparison of Avian and Reptilian α-Crystallins, Comp. Biochem. Physiol., 1981, vol. 69B, no. 3, pp. 593–598.

    Google Scholar 

  • De Jong, W.W., Leunissen, J.A.M., Leenen, P.J.M., et al., Dogfish α-Crystallin Sequences. Comparison with Small Heat Shock Proteins and Shistosoma Egg Antigen, J.αBiol. Chem., 1988, vol. 263, no. 11, pp. 5141–5149.

    PubMed  Google Scholar 

  • De Jong, W.W., Hendriks, W., Mulders, J.W.M., and Bloemendal, H., Evolution of Eye Lens Crystallins: the Stress Connection, Trends Biochem. Sci., 1989, vol. 14, no. 9, pp. 365–386.

    Google Scholar 

  • van Kamp, G.J. and Hoenders, H.J., The Distribution of the Soluble Proteins in the Calf Lens, Exp. Eye Res., 1973, vol.17, no. 4, pp. 417–426.

  • van Kamp, G.J., Kleef, F.S.M., and Hoenders, H.J., Reaggregation Studies on the Polypeptide Chains of Calf Lens α-Crystallin, Biochim. Biophys. Acta, 1974, vol. 342, no. 1, pp. 89–96.

    PubMed  Google Scholar 

  • Kibbelaar, M. and Bloemendal, H., The topography of lens Proteins Based on Chromatography and Two-Dimensional Gel Electrophoresis, Exp. Eye Res., 1975, vol. 21, no. 1, pp. 25–36.

    PubMed  Google Scholar 

  • Kibbelaar, M.A., Selten-Versteegen, A.M.E., Dunia, I., et al., Actin in Mammalian Lens, Eur. J. Biochem., 1979, vol.95, no. 3, pp. 543–549.

    PubMed  Google Scholar 

  • King, C.R. and Piatigorsky, J., Alternative RNA Splicing of the Murine αA-Crystallin Gene: Protein-Coding Information within an Intron, Cell, 1983, vol. 32, no. 3, pp.707–712.

    PubMed  Google Scholar 

  • Kodama, R. and Eguchi, G., Characterization of an Antiserum Against feather Keratins of the Chick: Its Crossreaction with Lens Protein, α-Crystallin, Devel. Growth Differ., 1983, vol. 25, no. 3, pp. 261–270.

    Google Scholar 

  • Konyukhov, B.V., Genetika razvitya pozvonochnykh (Genetics of Development of Vertebrates), Moscow: Nauka, 1980.

    Google Scholar 

  • Kozlov, K.A., Tomarev, S.I., Dzhumagaliev, E.B., et al., Preparation of the Clone Bank of Recombinant DNA Containing Nucleotide Sequences of Rana temporaria Lens mRNA, Dokl. Akad. Nauk SSSR, 1980, vol. 255, no. 6, pp. 1503–1506.

    PubMed  Google Scholar 

  • Kramps, H.A., Stols, A.L.H., Hoenders, H.J., and de Groot, K., On the Quarternary Structure of High-Molecular-Weight Proteins from the Bovine Eye Lens, Eur. J. Biochim., 1975, vol. 50, no. 3, pp. 503–509.

    Google Scholar 

  • Lampi, K.J., Ma, Z., Shih, M., et al., Sequence Analysis of βA3, βB3, and βA4 Crystallins Completes the Identification of the Major Proteins in Young Human Lens, J.αBiol. Chem., 1997, vol. 272, no. 4, pp. 2268–2275.

    PubMed  Google Scholar 

  • Lopashov, G.V. and Stroeva, O.G., Razvitie glaza v svete eksperimental'nykh issledovanii (Eye Development in the Light of Experimental Studies), Moscow: Nauka, 1963.

    Google Scholar 

  • Lu, S.-F., Pan, F.-M., and Chiou, S.-H., Characterization of γ-Crystallin from Eye Lens of Bullfrog: Complexity of γ-Crystallin Multigene Family As Revealed by Sequence Comparison Among Different Amphibian Species,J.Prot. Chem., 1996, vol. 15, no. 1, pp. 103–113.

    Google Scholar 

  • Lubsen, N.H., Aarts, H.J.M., and Schoenmakers, J.G.G., The Evolution of Lenticular Proteins: the β-and γ-Crystallin Super Gene Family, Progr. Biphys. Molec. Biol., 1988, vol. 51, no. 1, pp. 47–76.

    Google Scholar 

  • Maisel, H. and Langman, J., An Immuno-Embryological Study on the Chick Lens, J. Embryol. Exp. Morphol., 1961, vol. 9, part 1, pp. 191–201.

    PubMed  Google Scholar 

  • McAvoy, J.W., Cell Division, Cell Elongation, and Distribution of α-, β-, and γ-Crystallins in the Rat Lens, J.Embryol. Exp. Morphol., 1978, vol. 44, pp. 149–165.

    PubMed  Google Scholar 

  • McDermott, J.B., Cvekl, A., and Piatigorsky, J., A Complex Enhancer of the Chicken βA3/A1-Crystallin Gene Depends on an AP-1-CRE Element for Activity, Invest. Ophthalm. Vis. Sci., 1997, vol. 38, no. 5, pp. 951–959.

    Google Scholar 

  • McDevitt, D.S., The Crystallins of Normal and Regenerated Newt Eye Lenses, Stability and Switching in Cellular Differentiation, Clayton, R.M. and Truman, D.E.S., Eds., New York: Plenum Press, 1982, pp. 177–186.

    Google Scholar 

  • McDevitt, D.S., Meza, I., and Yamada, T., Immunofluorescence Localization of the Crystallins in Amphibian Lens Development with Special Reference to the γ-Crystallins, Devel. Biol., 1969, vol. 19, no. 6, pp. 581–607.

    Google Scholar 

  • McDevitt, D.S. and Brahma, S.K., Ontogeny and Localization of the Crystallins during Embryonic Lens Development in Xenopus laevis, J. Exp. Zool., 1973, vol. 186, no.2, pp. 127–140.

    PubMed  Google Scholar 

  • McDevitt, D.S. and Collier, C.R., The Lens Proteins of Eastern North American Salamanders and Their Application to Urodelian Systematics, Exp. Eye Res., 1975, vol. 21, no. 1, pp. 1–8.

    PubMed  Google Scholar 

  • McDevitt, D.S. and Croft, L.R., On the Existence of γ-Crystallin in the Bird Lens, Exp. Eye Res., 1977, vol. 25, no.5, pp. 473–481.

    PubMed  Google Scholar 

  • McDevitt, D.S. and Brahma, S.K., Ontogeny and Localization of the α, β, and γ-Crystallins in Newt Eye Lens Development, Devel. Biol., 1981, vol. 84, no. 2, pp. 449–454.

    Google Scholar 

  • Mikhailov, A.T., Immunochemical Markers of Differentiation of Rana temporaria Lens during Embryonic Development. I. Composition and Properties of Water-Soluble Lens Antigens, Ontogenez, 1978, vol. 9, no. 5, pp. 439–448.

    PubMed  Google Scholar 

  • Mikhailov, A.T. and Takenov, Zh.A., Changes in Cell Localization of γ-Crystallins in the Process of Differentiation of the Amphibian Lens, Ontogenez, 1983, vol. 14, no. 4, pp. 374–381.

    PubMed  Google Scholar 

  • Mikhailov, A.T., Gorgolyuk, N.A., and Takenov, Zh.A., Specific Proteins of the Amphibian Lens: Immunochemical Identification during Normal Development and Under Experimental Conditions, in Immunological Aspects of Developmental Biology, Moscow: Nauka, 1984, pp.201–216.

    Google Scholar 

  • Mikhailov, A.T., Simirskii, V.N., and Takenov, Zh.A., Crystallins in the Processes of Differentiation and Regeneration of the Amphibian Eye Lens, Ontogenez, 1988, vol.19, no. 4, pp. 341–357.

    PubMed  Google Scholar 

  • Mörner, C.T., Untersuchungen der Protein-substanzen in den lichtbrechenden Medien des Auges, Hoppe-Seyl. Zeit Physiol. Chem., 1894, vol. 18, no. 1, pp. 61–106.

    Google Scholar 

  • Mulders, J.W.M., Hendriks, W., Blankesteijn, W.M., et al., λ-Crystallin, a Major Rabbit Lens Protein, Is Related to Hydroxyacyl-Coenzyme A Dehydrogenases, J. Biol. Chem., 1988, vol. 263, no. 30, pp. 15 462-15 466.

    Google Scholar 

  • Nene, V., Dunne, D.W., Johnson, K.S., et al., Sequence and Expression of a Major Egg Antigen from Schistosoma mansoni. Homologies to Heat Shock Proteins and α-Crystallins, Mol. Biochem. Parasitol., 1986, vol. 21, no.2, pp. 179–188.

    PubMed  Google Scholar 

  • Nerland, A.H., Mustafa, A.S., Sweetser, D., et al., A Protein Antigen of Mycobacterium leprae Is Related to a Family of Small Heat Shock Proteins, J. Bacteriol., 1988, vol.170, no. 12, pp. 5919–5921.

    PubMed  Google Scholar 

  • Nguen Ngok Kyong, Tomarev, S.I., Arutyunyan, K.G., and Gause, G.G., Isolation and Characterization of Human Recombinant DNA Clones Homologous to the Gene Coding for a 35-kDa Polypeptide of the Frog Eye Lens, Dokl. Akad. Nauk SSSR, 1983, vol. 268, no. 6, pp. 1260–1263.

    PubMed  Google Scholar 

  • Nickerson, J.M., Wawrousek, E.P., Borras, T., et al., Sequence of the Chicken δ2-Crystallin Gene and Its Intergenic Spacer: Extreme Homology with the δ1 Crystallin Gene, J. Biol. Chem., 1986, vol. 261, no. 1, pp.552–557.

    PubMed  Google Scholar 

  • Nothiger, R., McDevitt, D.S., and Yamada, T., Comparison of γ-Crystallins from Frog and Newt, Exp. Eye Res., 1971, vol. 12, no. 1, pp. 94–98.

    PubMed  Google Scholar 

  • O'Farrell, P.H., High Resolution Two-Dimensional Electrophoresis of Proteins, J. Biol. Chem., 1975, vol. 250, no.10, pp. 4007–4021.

    PubMed  Google Scholar 

  • Orwerth, B.J. and Byrnes, R.J., Properties of a Ribonuclease Inhibitor from Bovine Lens, Exp. Eye Res., 1971, vol.12, no. 2, pp. 120–127.

    PubMed  Google Scholar 

  • Orwerth, B.J. and Byrnes, R.J., Further Studies on the Puri-fication and Properties of a Ribonuclease Inhibitor from Lens Cortex, Exp. Eye Res., 1972, vol. 14, no. 2, pp.114–122.

    PubMed  Google Scholar 

  • Ostrer, H., and Piatigorsky, J., β-Crystallins of the Adult Chicken Lens: Relatedness of the Polypeptides and Their Aggregates, Exp. Eye Res., 1980, vol. 30, no. 6, pp.679–689.

    PubMed  Google Scholar 

  • Ostrer, H., Beebe, D.C., and Piatigorsky, J., β-Crystallin mRNAs: Differential Distribution in the Developing Chicken Lens, Devel. Biol., 1981, vol. 86, no. 2, pp.403–408.

    Google Scholar 

  • van der Ouderaa, F.J., de Jong, W.W., and Bloemendal, H., The Amino Acid Sequence of the αA2 Chain of Bovine α-Crystallin, Eur. J. Biochem., 1973, vol. 39, no. 2, pp. 207–222.

    PubMed  Google Scholar 

  • van der Ouderaa, F.J., de Jong, W.W., Hilderink, A., and Bloemendal,H., The Amino Acid Sequence of the αB2 Chain of Bovine α-Crystallin, Eur. J. Biochem., 1974, vol. 49, no.1, pp. 157–168.

    PubMed  Google Scholar 

  • Papaconstantinou, J., Biochemistry of Bovine Lens Proteins. II. The γ-Crystallin of Adult Bovine, Calf and Embryonic Lenses, Biochim. Biophys. Acta, 1965, vol. 107, no.1, pp. 81–90.

    PubMed  Google Scholar 

  • Persson, B., Zigier, J.S., Jr., and Jornvall, H., A Super-Family of Medium-Chain Dehydrogenases/Reductases (MDR).Sub-Lines Including ζ-Crystallin, Alcohol and Polyol Dehydrogenases, Quinone Oxireductases, Enoyl Reductases, VAT-1 and Other Proteins, Eur. J. Biochem., 1994, vol. 226, no. 1, pp. 15–22.

    PubMed  Google Scholar 

  • Piatigorsky, J., Gene Expression and Genetic Engineering in the Lens. Fridenwald Lecture, Invest. Ophthalmol. Vis. Sci., 1987, vol. 28, no. 1, pp. 9–28.

    PubMed  Google Scholar 

  • Piatigorsky, J., Lens Crystallins and Their Genes: Diversity and Tissue-specific Expression, FASEB J., 1989, vol. 3, no. 8, pp. 1933–1940.

    PubMed  Google Scholar 

  • Piatigorsky, J. and Wistow, G., Enzyme/Crystallins: Gene Sharing As an Evolutionary Strategy, Cell, 1989, vol. 57, no. 2, pp. 197–199.

    PubMed  Google Scholar 

  • Piatigorsky, J. and Zelenka, P., Molecular Weight and Subunit Structure of Delta-Crystallin from Embryonic Chick Lens Fibers, Exp. Eye Res., 1974, vol. 18, no. 5, pp. 435–446.

    PubMed  Google Scholar 

  • Piatigorsky, J. and Wistow, G., The recruiment of Crystallins: New Functions Precede Gene Duplication, Science, 1991, vol. 252, no. 5009, pp. 1078–1079.

    PubMed  Google Scholar 

  • de Pomerai, D.I., Ellis, D.K., and Carr, A., A Lamprey Lens Protein Related to Avian and Reptilian δ-Crystallin, Curr. Eye Res., 1984, vol. 3, no. 5, pp. 729–735.

    PubMed  Google Scholar 

  • Quiring, R., Walldorf, U., Kloter, U., and Gehring, W.J., Homology of the Eyeless Gene of Drosophila to the Small Eye Gene in Mice and Aniridia in Humans, Science, 1994, vol. 265, no. 5173, pp. 785–789.

    PubMed  Google Scholar 

  • Rabaey, M., Electrophoretic and Immunoelectrophoretic Studies on the Soluble Proteins in the Developing Lens of Birds, Exp. Eye Res., 1962, vol. 1, no. 5, pp. 310–316.

    PubMed  Google Scholar 

  • Ramaekers, F.C.S., Kan, P.L.E., and Bloemendal, H., A Comparative Study of β-Crystallins from Ungulates, Whale and Dog, Ophthalmic. Res., 1979, vol. 11, nos. 3–4, pp. 143–153.

    Google Scholar 

  • Ramaekers, F.C.S., Selten-Versteegen, A.M.E., Benedetti, E.L., et al., In vitro Synthesis of the Major Lens Membrane Protein, Proc. Natl. Acad. Sci. USA, 1980, vol. 77, no. 2, pp. 725–729.

    PubMed  Google Scholar 

  • Ramaekers, F., Dodemont, H., Vorstenbosch, P., and Bloemendal, H., Classification of Rat Lens Crystallins and Identification of Proteins Encoded by Rat Lens mRNA, Eur. J. Biochem., 1982, vol. 128, no. 2, pp. 503–508.

    PubMed  Google Scholar 

  • Rao, P.V., Gonzalez, P., Persson, B., et al., Guinea Pig and Bovine α-Crystallins Have Distinct Functional Characteristics Highlighting Replacements in Otherwise Similar Structures, Biochemistry, 1997, vol. 36, no. 18, pp.5353–5362.

    PubMed  Google Scholar 

  • van Rens, G.L.M., Raats, J.M.H., Driessen, H.P.C., et al., Structure of the Bovine Eye Lens Gamma Crystallin Gene Formely Beta S, Gene, 1989, vol. 78, no. 2, pp. 225–234.

    PubMed  Google Scholar 

  • van Rens, G.L.M., de Jong, W.W., and Bloemendal, H., A Superfamily in the Mammalian Eye Lens: the β/γ-Crystallins, Mol. Biol. Reports, 1992, vol. 16, no. 1, pp. 1–10.

    Google Scholar 

  • Reszelbach, R., Shinohara, T., and Piatigorsky, J., Resolution of Two Distinct Embryonic Chick δ-Crystallin Bands by Polyacrylamide Gel Electrophoresis in the Presence of Sodium Dodecyl Sulfate and Urea, Exp. Eye Res., 1977, vol. 25, no. 6, pp. 583–593.

    PubMed  Google Scholar 

  • Richardson, J., Cvekl, A., and Wistow, G., Pax-6 Is Essential for Lens-Specific Expression of ϰ-Crystallin, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, no. 10, pp. 4676–4680.

    PubMed  Google Scholar 

  • Robinson, M.L., Ohtakamaruyama, C., Chan, C.C., et al., Disregulation of Ocular Morphogenesis by lens-Specific Expression of FGF-3/Int-2 in Transgenic Mice, Devel. Biol., 1998, vol. 198, no. 1, pp. 13–31.

    Google Scholar 

  • Rodokanaki, A., Holmes, R.K., and Borra's, T., Zeta-Crystallin, a Novel Protein from the Guinea Pig Lens, Is Related to Alcohol Dehydrogenases, Gene, 1989, vol. 78, no. 2, pp. 215–224.

    PubMed  Google Scholar 

  • Roll, B. and Schwemer, J., Iota-Crystallin and Vitamin A (2) Isomers in Lenses of Diurnal Geckos, J. Comp. Physiol. Sensory Neur. Behaivior. Physiol., 1999, vol. 185, no. 1, pp. 51–58.

    Google Scholar 

  • Russnak, R.H., Jones, D., and Candido, E.P.M., Cloning and Analysis of cDNA Sequences Coding for Two 16 Kilodalton Heat Shock Proteins (hsps) in Caenorhabditis elegans: Homology with the Small hsps of Drosophila, Nucl. Acids Res., 1983, vol. 11, no. 10, pp. 3187–3205.

    PubMed  Google Scholar 

  • Sen, P.C. and Pfeiffer, D.R., Characterization of Partially Purified (Na+ K+)-ATPase from Porcine Lens, Biochim. Biophys. Acta, 1982, vol. 693, no. 1, pp. 34–44.

    PubMed  Google Scholar 

  • Shinohara, T., Reszelbach, R., and Piatigorsky, J., Two Tryptic Peptide Differences Among the Subunits of δ-Crystallin of the Embryonic Chick Lens, Exp. Eye Res., 1980, vol. 30, no. 4, pp. 361–370.

    PubMed  Google Scholar 

  • Siezen, R.J., Reflections on the Internal Primary, Secondary and Tertiary Structure Homology of the Eye Lens Proteins α-, β-and γ-Crystallin, FEBS Lett., 1981, vol. 133, no. 1, pp. 1–8.

    PubMed  Google Scholar 

  • Siezen, R.J., Bindels, J.C., and Hoenders, H.J., The Interrelationships between Monomeric, Oligomeric and Polymeric γ-Crystallin in the Calf Lens Nucleus, Exp. Eye Res., 1979, vol. 28, no. 5, pp. 551–567.

    PubMed  Google Scholar 

  • Siezen, R.J., Wu, E., Kaplan, E.D., et al., Rat Lens γ-Crystallins. Characterization of Six Gene Products and Their Spatial and Temporal Distribution Resulting from Differential Synthesis, J. Mol. Biol., 1988, vol. 199, no. 3, pp. 475–490.

    PubMed  Google Scholar 

  • Slingsby, C. and Croft, L.R., Structural Studies on Calf Lens γ-Crystallin Fraction IV: A Comparison of the Cystein-Containing Tryptic Peptides with the Corresponding Amino Acid Sequence of γ-Crystallin Fraction II, Exp. Eye Res., 1978, vol. 26, no. 3, pp. 291–304.

    PubMed  Google Scholar 

  • Spector, A., The Soluble Proteins of the Lens, Invest. Ophthalmol., 1965, vol. 4, no. 4, pp. 579–591.

    Google Scholar 

  • Spector, A., Physiological Chemistry of the Eye, Arch. Ophthalmol., 1969, vol. 81, no. 1, pp. 127–143.

    PubMed  Google Scholar 

  • Stapel, S.O. and de Jong, W.W., Lamprey 48-kDa Lens Protein Represents a Novel Class of Crystallins, FEBS Lett., 1983, vol. 162, no. 2, pp. 305–309.

    PubMed  Google Scholar 

  • Stapel, S.O., Zweers, A., Dodemont, H.J., et al., ε-Crystallin, a Novel Avian and Reptilian Eye Lens Protein, Eur. J.Biochem., 1985, vol. 147, no. 1, pp. 129–136.

    PubMed  Google Scholar 

  • Stöger, T., Augusteyn, R.C., and Graw, J., The Cryner Element in the Murine γ-Crystallin Promoters Interacts with lens Proteins, Ophthalmic Res., 1997, vol. 29, no. 3, pp.161–171.

    PubMed  Google Scholar 

  • Stone, E.M., Fingert, J.H., Alward, W.L.M., et al., Identification of a Gene That Causes Primary Open Angle Glaucoma, Science, 1997, vol. 275, no. 5300, pp. 668–670.

    PubMed  Google Scholar 

  • Tatusov, R.L., Koonin, E.V., and Lipman, D.J., A Genomic Perspective on Protein Families, Science, 1997, vol. 278, no. 5338, pp. 631–637.

    PubMed  Google Scholar 

  • Tomarev, S.I., Zinovieva, R.D., Dolgilevich, S.M., et al., A Novel Type of Crystallin in the Frog Eye Lens, FEBS Lett., 1984, vol. 171, no. 1, pp. 34–45.

    Google Scholar 

  • Vermorken, A.J.M., Herbrink, P., and Bloemendal, H., Synthesis of Lens Protein in vitro: Formation of γ-Crystallin, Eur. J. Biochim., 1977, vol. 78, no. 2, pp. 617–622.

    Google Scholar 

  • Vermorken, A.J.M. and Bloemendal, H., β-Crystallin Polypeptides As Markers of Lens Cell Differentiation, Nature, 1978, vol. 271, no. 5647, pp. 779–781.

    PubMed  Google Scholar 

  • Vermorken, A.J.M., Hilderink, J.M.H.C., van de Ven, W.J.M., and Bloemendal, H., Lens Differentiation. Crystallin Synthesis in isolated Epithelia from Calf Lenses, J. Cell Biol., 1978, vol. 16, no. 1, pp. 175–183.

    Google Scholar 

  • Waley, S.G., Nomenclature for the Polypeptide Chains of γ-Crystallin, Exp. Eye Res., 1969, vol. 8, no. 5, pp. 477–478.

    PubMed  Google Scholar 

  • Watanabe, K., Fujii, Y., Nakayama, K., et al., Structural Similarity of Bovine Lung Prostaglandin F Synthase to Lens ε-Crystallin of the European Common Frog, Proc. Natl. Acad. Sci. USA, 1988, vol. 85, no. 1, pp. 11–15.

    PubMed  Google Scholar 

  • Williams, L.A. and Piatigorsky, J., Comparative and Evolutionary Aspects of δ-Crystallin in the Vertebrate Lens, Eur. J. Biochem., 1979a, vol. 100, no. 2, pp. 349–357.

    PubMed  Google Scholar 

  • Williams, L.A. and Piatigorsky, J., Heterogeneity of δ-Crystallins of the Embryonic Mallard Lens. Correlation between Subunit Compositions and Isoelectric Points, Biochemistry, 1979b, vol. 18, no. 8, pp. 1438–1442.

    PubMed  Google Scholar 

  • Williams, L.A., Ding, L., Horwitz, J., and Piatigorsky, J., δ-Crystallin from the Turtle Lens: Purification and Partial Characterization, Exp. Eye Res., 1985, vol. 40, no. 5, pp.741–749.

    PubMed  Google Scholar 

  • Wistow, G., Domain Structure and Evolution in τ-Crystallins and Small Heat-Shock Proteins. Hypothesis, FEBS Lett., 1985, vol. 181, no. 1, pp. 1–6.

    PubMed  Google Scholar 

  • Wistow, G., Summers, L., and Blundell, T., Myxococcus xanthus Spore Coat Proteins S May Have a Similar Structure to Vertebrate Lens β/γ-Crystallins, Nature, 1985, vol.315, no. 6022, pp. 771–773.

    PubMed  Google Scholar 

  • Wistow, G.J., Lietman, T., Williams, L.A., et al., τ-Crystallin/ α-Enolase: One Gene Encodes Both an Enzyme and a Lens Structural Protein, J. Cell Biol., 1988, vol. 107, no. 6, part 2, pp. 2729–2736.

    PubMed  Google Scholar 

  • Wistow, G.J. and Piatigorsky, J., Lens Crystallins: the Evolution and Expression of Proteins for a Highly Specialized Tissue, Ann. Rev. Biochem., 1988, vol. 57, pp. 479–504.

    PubMed  Google Scholar 

  • Wistow, G.J., Anderson, A., and Piatigorsky, J., Evidence for Neutral and Selective Processes in the Recruitment of Enzyme-Crystallins in Avian Lenses, Proc. Natl. Acad. Sci. USA, 1990, vol. 87, no. 16, pp. 6277–6280.

    PubMed  Google Scholar 

  • Wistow, G. and Kim, H., Lens Protein Expression in Mammals: Taxon-Specificity and the Recruitment of Crystallins, J. Mol. Evol., 1991, vol. 32, no. 2, pp. 262–269.

    PubMed  Google Scholar 

  • Yeh, L.-S.L., Elzanowski, A., Hunt, L.T., and Barker, W.C., Homology of Delta Crystallin and Argininosuccintae Lyase, Comp. Biochem. Physiol., 1988, vol. 889, no. 2, pp. 433–437.

    Google Scholar 

  • Zaraiskii, A.G., Homeobox Genes ANF-Regulators of Early Development of the Anterior Head Region in Vertebrates, Doctorate (Biol.) Dissertation, Moscow: Institute of Developmental Biology, Russian Academy of Sciences, 2000.

    Google Scholar 

  • Zigler, J.S., Jr. and Sidbury, J.B., Jr., A Comparative Study of β-Crystallin from Six Mammals, Comp. Biochem. Physiol., 1976a, vol. B53, no. 3, pp. 349–355.

    Google Scholar 

  • Zigler, J.S., Jr. and Sidbury, J.B., Jr., A Comparative Study of the β-Crystallins of Four Sub-Mammalian Species, Comp. Biochem. Physiol., 1976b, vol. B55, no. 1, pp.19–24.

    Google Scholar 

  • Zigler, J.S., Jr. and Goosey, J., Aging of Protein Molecules: Lens Crystallins As a Model System, Trends Biochem. Sci., 1981, vol. 6, pp. 133–136.

    Google Scholar 

  • Zwaan, J. and Ikeda, A., An Immunochemical Study on the β-Crystallins of the Chicken Lens: Ontogenetic and Phylogenetic Aspects, The Structure of the Eye, Rohen, J.W., Ed., Stuttgart: Schatlauer-Verlag, 1965, pp. 419–429.

    Google Scholar 

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Kozlov, K.A. Vertebrate Crystallins--from Proteins to Genes. Russian Journal of Developmental Biology 32, 265–282 (2001). https://doi.org/10.1023/A:1012389831820

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