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The eye lens crystallins: Ambiguity as evolutionary strategy

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Summary

Comparative studies of the different families of lens-specific proteins of the vertebrates, the crystallins, and their genes reveal several interesting evolutionary features. The origin of α-crystallin can be traced back to the small heat shock proteins, while the superfamily of βγ-crystallins shows structural similarities with a bacterial spore coat protein. The crystallins display a great diversity within and between species, as well as during development. Ambiguous transcription, mRNA-processing, and translation contribute to this diversity of the crystallins and their expression. These mechanisms include the occurrence of atypical poly-A addition signals, alternative splicing, and the use of two initiation codons on a single mRNA.

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References

  • Bloemendal H (ed) (1981) Molecular and cellular biology of the eye lens. John Wiley and Sons, New York

    Google Scholar 

  • Blundell T, Lindley P, Miller L, Moss D, Slingsby C, Tickle I, Turnell B, Wistow G (1981) The molecular structure and stability of the eye lens: X-ray analysis of γ-crystallin II. Nature 289:771–777

    PubMed  Google Scholar 

  • Breitbart RE, Nadal-Ginard B (1986) Complete nucleotide sequence of the fast skeletal troponin T gene. Alternatively spliced exons exhibit unusual interspecies divergence. J Mol Biol 188:313–324

    Article  PubMed  Google Scholar 

  • Breitman ML, Lok S, Wistow G, Piatigorsky J, Treton JA, Gold RJM, Tsui L-C (1984) γ-Crystallin family of the mouse lens: structural and evolutionary relationships. Proc Natl Acad Sci USA 81:7762–7766

    PubMed  Google Scholar 

  • Chepelinksy AB, Piatigorsky J (1986) Activator sequences of the murine αA-crystallin gene. Invest Ophthalmol Vis Sci 27 (suppl) p 214

    PubMed  Google Scholar 

  • Chiou S-H (1984) Physicochemical characterization of a crystallin from the souid lens and its comparison with vertebrate lens crystallins. J Biochem 95:75–82

    PubMed  Google Scholar 

  • Chiou S-H, Chang W-C, Kuo J, Pan F-M, Lo T-B (1986) Biochemical comparison of ε-crytallins from duck and frog eye lenses. FEBS Letters 196:219–222

    Article  PubMed  Google Scholar 

  • Clayton RM, Jennyy JC, Bower DJ, Errington LH (1986) The presence of extralenticular crystallins and its relationship with transdifferentiation to lens. In: Okada TS (ed) Current topics in developmental biology. vol 20, Commitment and instability in cell differentiation. Academic Press, Orlando, pp 137–152

    Google Scholar 

  • de Jong WW (1981) Evolution of lens and crystallins. In: Bloemendal H (ed) Molecular and cellular biology of the eye lens. John Wiley and Sons, New York, pp 221–278

    Google Scholar 

  • de Jong WW, Cohen LH, Leunissen JAM, Zweers A (1980) Internally elongated rodent α-crystallin A chain: resulting from incomplete RNA splicing. Biochem Biophys Res Commun 96:648–655

    Article  PubMed  Google Scholar 

  • Delaye M, Tardieu A (1983) Shor-range order of cystallin protein accounts for eye lens transparency. Nature 302:415–417

    Article  PubMed  Google Scholar 

  • den Dunnen JT, Jongbloed RJE, Geurts van Kessel AHM, Schoenmakers JGG (1985) Human lens γ-crystallin sequences are located in the p12-qter region of chromosome 2. Hum Genet 70:217–221

    Article  PubMed  Google Scholar 

  • den Dunnen JT, Moormann RJM, Lubsen NH, Schoenmakers JGG (1986a) Intron insertions and deletions in the βγ-crystallin gene family: the rat βB1 gene. Proc Natl Acad Sci USA 83:2855–2859

    PubMed  Google Scholar 

  • den Dunnen JT, Moormann RJM, Lubsen NH, Schoenmakers JGG (1986b) Concerted and divergent evolution within the rat γ-crystallin gene family. J Mol Biol 189:37–46

    Article  PubMed  Google Scholar 

  • Dodemont H, Groenen M, Jansen L, Schoenmakers J, Bloemendal H (1985) Comparison of the crystallin mRNA populations from rat, calf and duck lens. Evidence for a longer αA2-mRNA and two distinct αB2-mRNAs in the birds. Biochim Biophys Acta 824:284–294

    PubMed  Google Scholar 

  • Driessen HPC, Herbrink P, Bloemendal H, de Jong WW (1981) Primary structure of the bovine β-crystallin Bp chain. Internal duplication and homology with γ-crystallin. Eur J Biochem 12:83–91

    Google Scholar 

  • Gause GG Jr, Tomarev SI, Zinovieva RD, Arutyunyan KG, Dolgilevich SM (1986) Crystallin gene sequences of the frogRana temporaria. In: Duncan G (ed) The lens: transparancy and cataract. Topics in aging research in Europe, vol 6, EUR-AGE, Rijswijk, pp 171–179

    Google Scholar 

  • Goodman M (1981) Decoding the pattern of protein evolution. Prog Biophys Molec Biol 37:105–164

    Article  Google Scholar 

  • Gorin MB, Horwitz J (1984) Cloning and characterization of a cow beta crystallin cDNA. Curr Eye Res 3:939–948

    PubMed  Google Scholar 

  • Harding JJ, Crabbe MJC (1984) The lens: development, proteins, metabolism and cataract. In: Davson H (ed) The eye, 3rd ed. Academic Press, London, New York, pp 207–492

    Google Scholar 

  • Hayashi S, Kondoh H, Yasuda K, Soma G-I, Ikawa Y, Okada TS (1985) Tissue-specific regulation of a chicken δ-crystallin gene in mouse cells: involvement of the 5′ end region. EMBO J 4:2201–2207

    PubMed  Google Scholar 

  • Heitmancik JF, Thompson MA, Wistow G, Piatigorsky J (1986) cDNA and deduced protein sequence for the βB1-crystallin polypeptide of the chicken lens. Conservation of the PAPA sequence. J Biol Chem 261:982–987

    PubMed  Google Scholar 

  • Hickey E, Brandon SE, Potter R, Stein G, Weber LA (1986) Sequence and organization of genes encoding the human 27 kDa heat shock protein. Nucl Acids Res 14:4127–4145

    PubMed  Google Scholar 

  • Hogg D, Tsui L-C, Gorin M, Breitman ML (1986) Characterization of the human β-crystallin gene HuβA3/A1 reveals ancestral relationships among the βγ-crystallin superfamily. J Biol Chem 261:12410–12427

    Google Scholar 

  • Ingolia TD, Craig EA (1982) Four smallDrosophila heat shock proteins are related to each other and to mammalian α-crystallin. Proc Natl Acad Sci USA 79:2360–2364

    PubMed  Google Scholar 

  • King CR, Piatigorsky J (1983) Alternative RNA splicing of the murine αA-crystallin gene: protein-coding information within an intron. Cell 32:707–712

    Article  PubMed  Google Scholar 

  • King CR, Shinohara T, Piatigorsky J (1982) αA-crystallin messenger RNA of the mouse lens: More non-coding than coding sequences. Science 215:985–987

    PubMed  Google Scholar 

  • Kondoh H, Yasuda K, Okada TS (1983) Tissue-specific expression of a cloned chicken δ-crystallin gene in mouse cells. Nature 301:440–442

    Article  PubMed  Google Scholar 

  • Kozak M (1986) Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283–292

    Article  PubMed  Google Scholar 

  • Lok S, Breitman ML, Chepelinsky AB, Piatigorsky J, Gold RJM, Tsui L-C (1985) Lens-specific promoter activity of a mouse γ-crystallin gene. Mol Cell Biol 5:2221–2230

    PubMed  Google Scholar 

  • Maisel H (ed) (1985) The ocular lens. Marcel Dekker, New York

    Google Scholar 

  • Meakin SO, Breitman ML, Tsui T-C (1985) Structural and evolutionary relationships among five members of the human γ-crystallin gene family. Mol Cell Biol 5:1408–1414

    PubMed  Google Scholar 

  • Nei M (1975) Molecular population genetics and evolution. North-Holland, Amsterdam

    Google Scholar 

  • Nickerson JM, Wawrousek EF, Hawkins JW, Wakil AS, Wistow GJ, Thomas G, Norman BL, Piatigorsky J (1985) The complete sequence of the chicken δ1 crystallin gene and its 5′ flanking region. J Biol Chem 260:9100–9105

    PubMed  Google Scholar 

  • Nickerson JM, Wawrousek EF, Borras T, Hawskins JW, Norman BL, Filpula DR, Nagle JW, Ally AH, Piatigorsky J (1986) Sequence of the chicken δ2 crystallin gene and its intergenic spacer. Extreme homology with the δ1 crystallin gene. J Biol Chem 261:552–557

    PubMed  Google Scholar 

  • Okazaki K, Yasuda K, Kondoh H, Okada TS (1985) DNA sequences responsible for tissue-specific expression of a chicken α-crystallin gene in mouse lens cells. EMBO J 4:2589–2595

    PubMed  Google Scholar 

  • Overbeek PA, Chepelinsky AB, Khillan JS, Piatigorsky J, Westphal H (1985) Lens-specific expression and developmental regulation of the bacterial chloramphenicol acetyltransferase gene driven by the murine αA-crystallin promoter in transgenic mice. Proc Natl Acad Sci USA 82:7815–7819

    PubMed  Google Scholar 

  • Peterson CA, Piatigorsky J (1986) Preferential conservation of the globular domains of the βA3/A1-crystallin polypetide of the chicken eye lens. Gene 45:139–147

    Article  PubMed  Google Scholar 

  • Piatigorsky J (1981) Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation. 19:134–153

    PubMed  Google Scholar 

  • Piatigorsky J (1984) Delta crystallins and their nucleic acids. Mol Cell Biochem 59:33–56

    Article  PubMed  Google Scholar 

  • Piatigorsky J (1987) Gene expression and genetic engineering in the lens. Invest Ophthalmol Vis Sci 28:9–28

    PubMed  Google Scholar 

  • Quax-Jeuken Y, Janssen C, Quax W, van den Heuvel R, Bloemendal H (1984) Bovine β-crystallin complementary DNA clones: alternating proline/alanine sequence of βB1 subunit originates from a repetitive DNA sequence. J Mol Biol 180:457–472

    Article  PubMed  Google Scholar 

  • Quax-Jeuken Y, Driessen H, Leunissen J, Quax W, de Jong WW, Bloemendal H (1985a) βs-Crystallin: structure and evolution of a distinct member of the βγ-superfamily. EMBO J 4:2597–2602

    PubMed  Google Scholar 

  • Quax-Jeuken Y, Quax W, van Rens G, Khan PM, Bloemendal H (1985b) Complete structure of the αB-crystallin gene: conservation of the exon-intron distribution in the two nonlineked α-crystallin genes. Proc Natl Acad Sci USA 82:5819–5823

    PubMed  Google Scholar 

  • Russnak RH, Jones D, Candido EPM (1983) Cloning and analysis of cDNA sequences coding for two 16 kilodalton heat shock proteins (hsps) inCaenorhabditis elegans: homology with the small hsps ofDrosophila. Nucl Acids Res 11:3187–3205

    PubMed  Google Scholar 

  • Schoenmakers JGG, Aarts HJM, van Leen RJ, den Dunnen JT, Lubsen NH (1986) Structure and expression of rat and human crystallin genes. In: Iwata S (ed) Proc Internat Soc Eye Res, vol. IV, Nagoya, pp44

  • Shiloh Y, Donion T, Bruns G, Breitman ML, Tsui L-C (1986) Assignment of the human γ-crystallin gene cluster (CRYG) to the long arm of chromosome 2, region q33-36. Human Genet 73:17–19

    Article  Google Scholar 

  • Siezen RJ, Shaw DC (1982) Physiocochemical characterization of lens proteins of the squidNototodarus gouldi and comparison with vertebrate crystallins. Biochim Biophys Acta 704:304–320

    PubMed  Google Scholar 

  • Siezen RJ, Fisch MR, Slingsby C, Benedek GB (1985) Opacification of γ-crystallin solutions from calf lens in relation to cold cataract formation. Proc Natl Acad Sci USA 82:1701–1705

    PubMed  Google Scholar 

  • Skow LC, Donner ME (1985) The locus encoding αA-crystallin is closely linked to H-2K on mouse chromosome 17. Genetics 110:723–732

    PubMed  Google Scholar 

  • Skow LC, Kunz HW, Gill TJ III (1985) Linkage of the locus encoding the A chain of α-crystallin (Acry-l) to the major histocompatibility complex in the rat. Immunogenetics 22:291–294

    Article  PubMed  Google Scholar 

  • Slingsby C (1985) Structural variation in lens crystallins. Trends Biochem Sci 10:281–284

    Article  Google Scholar 

  • Sparkes RS, Mohandes T, Heinzmann C, Gorin MB, Zollman S, Horwitz J (1986) Assignment of a human beta crystallin gene to 17 cen-q23*. Hum Genet 74:133–136

    Article  PubMed  Google Scholar 

  • Spector A, Chiesa R, Sredy J, Garner W (1985) cAMP-dependent phosphorylation of bovine lens α-crystallin. Proc Natl Acad Sci USA 82:4712–4716

    PubMed  Google Scholar 

  • Stapel SO, de Jong WW (1983) Lamprey 48-kDa lens protein represents a novel class of crystallins. FEBS Letters 162:305–309

    Article  PubMed  Google Scholar 

  • Stapel SO, Zweers A, Dodemont HJ, de Jong WW (1985) ε-Crystallin, a novel avian and reptilian eye lens protein Eur J Biochem 147:129–136

    Article  PubMed  Google Scholar 

  • Summers L, Slingsby C, White H, Narebor M, Moss D, Miller L, Mahadevan D, Lindley P, Driessen H, Blundell T (1984) The molecular structures and interactions of bovine and human γ-crystallins. In: Nugent J, Whelan J (eds) Human cataract formation, CIBA Foundation Symposium 106, Pitman, London, pp 219–236

    Google Scholar 

  • Tomarev SI, Zinovieva RD, Dolgilevich SM, Krayev AS, Skryabin KG, Gause Jr, GG (1983) The absence of the long 3′-non-translated region in mRNA coding for eye lens αA2-crystallin of the frog (Rana temporaria). FEBS Letters 162:47–51

    Article  PubMed  Google Scholar 

  • van den Heuvel R, Hendriks W, Quax W, Bloemendal H (1985) Complete structure of the hamster αA crystallin gene. Reflection of an evolutionary history by means of exon shuffling. J Mol Biol 185:273–284

    Article  PubMed  Google Scholar 

  • van Leen RW, Kastrop PMM, van Roozendaal KEP and Schoenmakers JGG (1986) Sequence divergence and selection of cap sites in the rat γ-crystallin gene family. Eur J Biochem 157:203–208

    Article  PubMed  Google Scholar 

  • Voorter CEM, Mulders JWM, Bloemendal H, de Jong WW (1986) Some aspects of the phosphorylation of α-crystallin. Eur J Biochem 160:203–210

    Article  PubMed  Google Scholar 

  • Williams LA, Ding L, Horwitz J, Piatigorsky J (1985) τ-Crystallin from the turtle lens: purification and partial characterization. Exp Eye Res 40:741–749

    Article  PubMed  Google Scholar 

  • Wistow G (1985) Domain structure and evolution in α-crystallins and small heat shock proteins. FEBS Letters 181:1–6

    Article  PubMed  Google Scholar 

  • Wistow G, Summers L, Blundell T (1985)Myxococcus xanthus spore coat protein S may have a similar structure to vertebrate lens βγ-crystallins. Nature 316:771–773

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, University of Nijmegen, P.O. Box 9101, 6500 HB, Nijmegen, The Netherland

    Wilfried W. de Jong & Wiljan Hendriks

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  1. Wilfried W. de Jong
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  2. Wiljan Hendriks
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de Jong, W.W., Hendriks, W. The eye lens crystallins: Ambiguity as evolutionary strategy. J Mol Evol 24, 121–129 (1986). https://doi.org/10.1007/BF02099960

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