Journal of Comparative Physiology B

, Volume 180, Issue 7, pp 1019–1032 | Cite as

Comparative analysis of crystallins and lipids from the lens of Antarctic toothfish and cow

  • Andor J. Kiss
  • Arthur L. Devries
  • Rachael M. Morgan-Kiss
Original Paper

Abstract

Animal model systems of senile cataract and lens crystallin stability are essential to understand the complex nature of lens transparency. Our aim in this study was to assess the long-lived Antarctic toothfish Dissostichus mawsoni (Norman) as a model system to understand long-term lens clarity in terms of solubility changes that occur to crystallins. We compared the toothfish with the mammalian model cow lens, dissecting each species’ lens into a cortex and nuclear region. In addition to crystallin distribution, we also assayed fatty acid (FA) composition by negative ion electrospray ionization mass spectrometry (ESI-MS). The majority of toothfish lens crystallins from cortex (90.4%) were soluble, whereas only a third (31.8%) from the nucleus was soluble. Crystallin solubility analysis by SDS-PAGE and immunoblots revealed that relative proportions of crystallins in both soluble and urea-soluble fractions were similar within each species examined and in agreement with previous reports for bovine lens. From our data, we found that both toothfish and cow crystallins follow patterns of insolubility that mirror each animals lens composition with more γ crystallin aggregation seen in the toothfish lens nucleus than in cow. Toothfish lens lipids had a large amount of polyunsaturated fatty acids that were absent in cow resulting in an unsaturation index (IU) four-fold higher than that of cow. We identified a novel FA with a molecular mass of 267 mass units in the lens epithelial layer of the toothfish that accounted for well over 50% of the FA abundance. The unidentified lipid in the toothfish lens epithelia corresponds to either an odd-chain (17 carbons) FA or a furanoid. We conclude that long-lived fishes are likely good animal models of lens crystallin solubility and may model post-translational modifications and solubility changes better than short-lived animal models.

Keywords

Lens Crystallins Antarctic toothfish Alpha crystallin Beta crystallin Gamma crystallin Lipid MALDI Albuminoid Fatty acid trophic marker (FATM) 

References

  1. Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A Mol Integr Physiol 138:405–415CrossRefPubMedGoogle Scholar
  2. Ahmed H, Du S, Vasta GR (2009) Knockdown of a galectin-1-like protein in zebrafish (Danio rerio) causes defects in skeletal muscle development. Glycoconj J 26:277–283CrossRefPubMedGoogle Scholar
  3. Asherie N, Pande J, Lomakin A, Ogun O, Hanson SR, Smith JB, Benedek GB (1998) Oligomerization and phase separation in globular protein solutions. Biophys Chem 75:213–227CrossRefPubMedGoogle Scholar
  4. Berbers GAM, Hoekman WA, Bloemendal H, de Jong WW, Kleinschmidt T, Braunitzer G (1983) Proline- and alanine-rich N-terminal extension of the basic bovine b-crystallin B1 chains. FEBS Lett 161:225–229CrossRefPubMedGoogle Scholar
  5. Bindels JG, Bours J, Hoenders HJ (1983) Age-dependent variations in the distribution of rat lens water-soluble crystallins. Size fractionation and molecular weight determination. Mech Ageing Dev 21:1–13CrossRefPubMedGoogle Scholar
  6. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedGoogle Scholar
  7. Bloemendal H, Berbers GA, De Jong WW, Ramaekers FC, Vermorken AJ, Dunia I, Benedetti EL (1984) Interaction of crystallins with the cytoskeletal-plasma membrane complex of the bovine lens. Ciba Found Symp 106:177–190PubMedGoogle Scholar
  8. Bloemendal H, De Jong W, Jaenicke R, Lubsen NH, Slingsby C, Tardieu A (2004) Ageing and vision: structure, stability and function of lens crystallins. Prog Biophys Mol Biol 86:407–485CrossRefPubMedGoogle Scholar
  9. Borchman D, Yappert MC, Afzal M (2004) Lens lipids and maximum lifespan. Exp Eye Res 79:761–768CrossRefPubMedGoogle Scholar
  10. Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an antarctic fish: on ice for winter. PLoS One 3:e1743CrossRefPubMedGoogle Scholar
  11. Chen J, Chang B, Chen Y, Lin CJ, Wu J, Kuo C (2001) Molecular cloning, developmental expression, and hormonal regulation of Zebrafish (Danio rerio) [beta] crystallin B1, a member of the superfamily of [beta] crystallin proteins. Biochem Biophys Res Commun 285:105–110CrossRefPubMedGoogle Scholar
  12. Chiou SH, Chang WP, Chen SW, Lo CH (1988) N-terminal sequences of gamma-crystallins from the amphibian lens and their homology with gamma-crystallins of other major classes of vertebrates. Int J Pept Protein Res 31:335–338CrossRefPubMedGoogle Scholar
  13. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905CrossRefGoogle Scholar
  14. Clayton JD, Cripps RM, Sparrow JC, Bullard B (1998) Interaction of troponin-H and glutathione S-transferase-2 in the indirect flight muscles of Drosophila melanogaster. J Muscle Res Cell Motil 19:117–127CrossRefPubMedGoogle Scholar
  15. Coop A, Goode D, Sumner I, Crabbe MJ (1998) Effects of controlled mutations on the N- and C-terminal extensions of chick lens beta B1 crystallin. Graefes Arch Clin Exp Ophthalmol 236:146–150CrossRefPubMedGoogle Scholar
  16. Cvekl A, Piatigorsky J (1996) Lens development and crystallin gene expression: many roles for Pax-6. Bioessays 18:621–630CrossRefPubMedGoogle Scholar
  17. Dahm R, Schonthaler HB, Soehn AS, van Marle J, Vrensen GFJM (2007) Development and adult morphology of the eye lens in the zebrafish. Exp Eye Res 85:74–89CrossRefPubMedGoogle Scholar
  18. Dalsgaard J, St John M, Kattner G, Muller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefPubMedGoogle Scholar
  19. Danysh BP, Duncan MK (2009) The lens capsule. Exp Eye Res 88:151–164CrossRefPubMedGoogle Scholar
  20. Davson H (1990). In: Davson H (ed) Physiology of the eye. Pergamon Press, Inc, New YorkGoogle Scholar
  21. Day KR, Jagadeeswaran P (2009) Microarray analysis of prothrombin knockdown in zebrafish. Blood Cell Mol Dis doi:http://dx.doi.org/10.1016/j.bcmd.2009.04.001
  22. Delaye M, Tardieu A (1983) Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302:415–417CrossRefPubMedGoogle Scholar
  23. Dische Z (1965) The glycoproteins and glycolipoproteins of the bovine lens and their relation to albuminoid. Invest Ophthalmol 4:759–778PubMedGoogle Scholar
  24. Fulhorst HW, Young RW (1966) Conversion of soluble lens protein to albuminoid. Invest Ophthalmol 5:298–303PubMedGoogle Scholar
  25. Greiling TMS, Houck SA, Clark JI (2009) The zebrafish lens proteome during development and aging. Mol Vis 15:2313–2325PubMedGoogle Scholar
  26. Grove TJ, Sidell BD (2004) Fatty acyl CoA synthetase from Antarctic notothenioid fishes may influence substrate specificity of fat oxidation. Comp Biochem Physiol B Biochem Mol Biol 139:53–63CrossRefPubMedGoogle Scholar
  27. Hains PG, Truscott RJW (2007) Post-translational modifications in the nuclear region of young, aged, and cataract human lenses. J Proteome Res 6:3935–3943CrossRefPubMedGoogle Scholar
  28. Han X, Gross RW (1994) Electrospray ionization mass spectroscopic analysis of human erythrocyte plasma membrane phospholipids. Proc Natl Acad Sci USA 91:10635–10639CrossRefPubMedGoogle Scholar
  29. Harding JJ, Dilley KJ (1976) Structural proteins of the mammalian lens: a review with emphasis on changes in development, aging and cataract. Exp Eye Res 22:1–73CrossRefPubMedGoogle Scholar
  30. Harrington V, McCall S, Huynh S, Srivastava K, Srivastava OP (2004) Crystallins in water soluble-high molecular weight protein fractions and water insoluble protein fractions in aging and cataractous human lenses. Mol Vis 10:476–489PubMedGoogle Scholar
  31. Hejtmancik JF, Thompson MA, Wistow G, Piatigorsky J (1986) cDNA and deduced protein sequence for the beta B1-crystallin polypeptide of the chicken lens. Conservation of the PAPA sequence. J Biol Chem 261:982–987PubMedGoogle Scholar
  32. Hochachka PW, Somero G (2002) Biochemical adaptation. In: Hochachka PW, Somero G (eds) Mechanism and process in physiological evolution. Oxford University Press, New YorkGoogle Scholar
  33. Horn PL (2002) Age and growth of Patagonian toothfish (Dissostichus eleginoides) and Antarctic toothfish (D. mawsoni) in waters from the New Zealand subantarctic to the Ross Sea, Antarctica. Fish Res 56:275–287CrossRefGoogle Scholar
  34. Horn P, Sutton C, DeVries AL (2003) Evidence to support the annual formation of growth zones in otoliths of Antarctic toothfish (Dissostichus mawsoni). CCAMLR Sci 10:125–138Google Scholar
  35. Jagger WS, Sands PJ (1996) A wide-angle gradient index optical model of the crystalline lens and eye of the rainbow trout. Vision Res 36:2623–2639CrossRefPubMedGoogle Scholar
  36. Jaillon O, Aury J, Brunet F, Petit J, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, Nicaud S, Jaffe D, Fisher S, Lutfalla G, Dossat C, Segurens B, Dasilva C, Salanoubat M, Levy M, Boudet N, Castellano S, Anthouard V, Jubin C, Castelli V, Katinka M, Vacherie B, Biemont C, Skalli Z, Cattolico L, Poulain J, de Berardinis V, Cruaud C, Duprat S, Brottier P, Coutanceau J, Gouzy J, Parra G, Lardier G, Chapple C, McKernan KJ, McEwan P, Bosak S, Kellis M, Volff J, Guigo R, Zody MC, Mesirov J, Lindblad-Toh K, Birren B, Nusbaum C, Kahn D, Robinson-Rechavi M, Laudet V, Schachter V, Quetier F, Saurin W, Scarpelli C, Wincker P, Lander ES, Weissenbach J, Roest Crollius H (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957CrossRefPubMedGoogle Scholar
  37. Kiss AJ (2005) Functional, biochemical and molecular analyses of the cold stable eye lens crystallins from the Antarctic toothfish Dissostichus mawsoni. Dissertation, University of Illinois at Urbana-ChampaignGoogle Scholar
  38. Kiss A, Cheng C (2008) Molecular diversity and genomic organisation of the alpha, beta and gamma eye lens crystallins from the Antarctic toothfish Dissostichus mawsoni. Comp Biochem Physiol Pt D 3:155–171Google Scholar
  39. Kiss AJ, Mirarefi AY, Ramakrishnan S, Zukoski CF, Devries AL, Cheng CH (2004) Cold-stable eye lens crystallins of the Antarctic nototheniid toothfish Dissostichus mawsoni Norman. J Exp Biol 207:4633–4649CrossRefPubMedGoogle Scholar
  40. Kroger RHH, Campbell MCW, Munger R, Fernald RD (1994) Refractive index distribution and spherical aberration in the crystalline lens of the African cichlid fish Haplochromis burtoni. Vision Res 34:1815–1822CrossRefPubMedGoogle Scholar
  41. 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
  42. Lee Sohn R, Huang P, Kawahara G, Mitchell M, Guyon J, Kalluri R, Kunkel LM, Gussoni E (2009) A role for nephrin, a renal protein, in vertebrate skeletal muscle cell fusion. Proc Natl Acad Sci USA 106:9274–9279CrossRefGoogle Scholar
  43. Lin Y, Dobbs G III, DeVries AL (1974) Oxygen consumption and lipid content in red and white muscles of antarctic fishes. J Exp Zool 189:379–385CrossRefPubMedGoogle Scholar
  44. Loewenstein MA, Bettelheim FA (1979) Cold cataract formation in fish lenses. Exp Eye Res 28:651–663CrossRefPubMedGoogle Scholar
  45. Logue JA, de Vries AL, Fodor E, Cossins AR (2000) Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. J Exp Biol 203:2105–2115PubMedGoogle Scholar
  46. Lovicu FJ, Robinson ML (2004) The lens: historical and comparative perspectives. In: Lovicu FJ, Robinson ML (eds) Development of the ocular lens. Cambridge University Press, pp 3–26Google Scholar
  47. Mirarefi AY, Boutet S, Ramakrishnan S, Kiss AJ, Cheng CC, DeVries AL, Robinson IK, Zukoski CF (2010) Small-angle X-ray scattering studies of the intact eye lens: effect of crystallin composition and concentration on microstructure. Biochimica et Biophysica Acta (BBA)—General Subjects 1800:556–564. doi:10.1016/j.bbagen.2010.02.004 Google Scholar
  48. Mörner C (1864) Untersuchung der Proteïnsubstanzen in den leichtbrechenden Medien des Auges I. Zeitscrift für physiologische Chemie 18:61–106Google Scholar
  49. Pan FM, Chang WC, Lin CH, Hsu AL, Chiou SH (1995) Characterization of gamma-crystallin from a catfish: structural characterization of one major isoform with high methionine by cDNA sequencing. Biochem Mol Biol Int 35:725–732PubMedGoogle Scholar
  50. Pan FM, Chuang MH, Chiou SH (1997) Characterization of gamma S-crystallin isoforms from lip shark (Chiloscyllium colax): evolutionary comparison between gamma S and beta/gamma crystallins. Biochem Biophys Res Commun 240:51–56CrossRefPubMedGoogle Scholar
  51. Paolisso G, Barbieri M, Bonafè M, Franceschi C (2000) Metabolic age modelling: the lesson from centenarians. Eur J Clin Invest 30:888–894CrossRefPubMedGoogle Scholar
  52. Paterson CA, Delamere NA (1992). In: Mosby-Year Book (ed) Physiology of the Eye. Mosby-Year Book, New YorkGoogle Scholar
  53. Patwardhan V, Modak SP (1992) Physicochemical characterization and phylogenetic comparison of fish lens proteins. Indian J Biochem Biophys 29:498–507PubMedGoogle Scholar
  54. Pierscionek B, Augusteyn RC (1988) Protein distribution patterns in concentric layers from single bovine lenses: changes with development and ageing. Curr Eye Res 7:11–23CrossRefPubMedGoogle Scholar
  55. Pierscionek BK, Augusteyn RC (1991) Structure/function relationship between optics and biochemistry of the lens. Lens Eye Toxic Res 8:229–243PubMedGoogle Scholar
  56. Pierscionek BK, Augusteyn RC (1995) The refractive index and protein distribution in the blue eye trevally lens. J Am Optom Assoc 66:739–743PubMedGoogle Scholar
  57. Posner M (2003) A comparative view of alpha crystallins: the contribution of comparative studies to understanding function. Integr Comp Biol 43:481–491CrossRefGoogle Scholar
  58. Posner M, Hawke M, Lacava C, Prince CJ, Bellanco NR, Corbin RW (2008) A proteome map of the zebrafish (Danio rerio) lens reveals similarities between zebrafish and mammalian crystallin expression. Mol Vis 14:806–814PubMedGoogle Scholar
  59. Rafferty NS, Scholz DL (1989) Comparative study of actin filament patterns in lens epithelial cells. Are these determined by the mechanisms of lens accommodation? Curr Eye Res 8:569–579CrossRefPubMedGoogle Scholar
  60. Rezanka T, Sigler K (2009) Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdoms. Prog Lipid Res 48:206–238CrossRefPubMedGoogle Scholar
  61. Römisch K, Collie N, Soto N, Logue J, Lindsay M, Scheper W, Cheng CH (2003) Protein translocation across the endoplasmic reticulum membrane in cold-adapted organisms. J Cell Sci 116:2875–2883CrossRefPubMedGoogle Scholar
  62. Rujoi M, Estrada R, Yappert MC (2004) In situ MALDI-TOF MS regional analysis of neutral phospholipids in lens tissue. Anal Chem 76:1657–1663CrossRefPubMedGoogle Scholar
  63. Sand D, Glass R, Olson D, Pike H, Schlenk H (1984) Metabolism of furan fatty acids in fish. Biochim Biophys Acta 793:429–434PubMedGoogle Scholar
  64. Santhoshkumar P, Udupa P, Murugesan R, Sharma KK (2008) Significance of interactions of low molecular weight crystallin fragments in lens aging and cataract formation. J Biol Chem 283:8477–8485CrossRefPubMedGoogle Scholar
  65. Sharma KK, Santhoshkumar P (2009) Lens aging: effects of crystallins. Biochimica et Biophysica Acta (BBA)—General Subjects 1790:1095–1108. doi:10.1016/j.bbagen.2009.05.008 Google Scholar
  66. Siezen RJ, Hom C, Kaplan ED, Thomson JA, Benedek GB (1988) Heterogeneity of gamma-crystallins from spiny dogfish (Squalus acanthias) eye lens. Exp Eye Res 46:81–93CrossRefPubMedGoogle Scholar
  67. Sinclair A, Murphy K, Li D (2000) Marine lipids: overview “news insights and lipid composition of Lyprinol”. Allergy Immunol 32:261–271Google Scholar
  68. Sivak JG (1985) The Glenn A. fry award lecture: optics of the crystalline lens. Am J Optom Physiol Opt 62:299–308PubMedGoogle Scholar
  69. Sivak JG (1990) Optical variability of the fish lens. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall Ltd, London pp 63–80Google Scholar
  70. Smith AC (1969a) An electrophoretic study of protein extracted in distilled water and in saline solution from the eye lens nucleus of the squid, Nototodarus hawaiiensis (Berry). Comp Biochem Physiol 30:551–559CrossRefPubMedGoogle Scholar
  71. Smith AC (1969b) Protein variation in the eye lens nucleus of the mackerel scad (Decapterus pinnulatus). Comp Biochem Physiol 28:1161–1168CrossRefPubMedGoogle Scholar
  72. Smith AC (1988) Indirect tissue electrophoresis: a new method for analyzing solid tissue protein. Comp Biochem Physiol B 90:791–794CrossRefPubMedGoogle Scholar
  73. Smith JB, Sun YP, Smith DL, Green B (1992) Identification of the posttranslational modifications of bovine lens alpha-b-crystallins by mass-spectrometry. Protein Sci 1:601–608CrossRefPubMedGoogle Scholar
  74. Spector A (1984a) Oxidation and cataract. Ciba Found Symp 106:48–64PubMedGoogle Scholar
  75. Spector A (1984b) The search for a solution to senile cataracts. Proctor lecture. Invest Ophthalmol Vis Sci 25:130–146PubMedGoogle Scholar
  76. Stark GR, Stein WH, Moore S (1960) Reactions of the cyanate present in aqueous urea with amino acids and proteins. J Biol Chem 235:3177–3181Google Scholar
  77. Sweetman G, Trinei M, Modha J, Kusel J, Freestone P, Fishov I, Joseleau-Petit D, Redman C, Farmer P, Norris V (1996) Electrospray ionization mass spectrometric analysis of phospholipids of Escherichia coli. Mol Microbiol 20:233–238CrossRefPubMedGoogle Scholar
  78. Terrados J, Lopez-Jimenez JA (1996) Fatty acid composition and chilling resistance in the green alga Cauterpa prolifera (Forrskal) lamouroux (Chlorophyta, Caulerpales). Biochem Mol Biol Int 39:863–869PubMedGoogle Scholar
  79. Toivonen LV, Sidorov VS, Nefedova ZA, Yurovitskii YG (2003) Age-related features of cataractogenesis in salmon fry. I. Lipid composition of lens during normal development. Russian J Dev Biol 34:19–21CrossRefGoogle Scholar
  80. Toivonen LV, Nefedova ZA, Sidorov VS, Yurovitskii YG (2004) Age-related features of cataractogenesis in salmon fry. II. Biochemical features of lens during cataractogenesis. Russian J Dev Biol 35:49–56CrossRefGoogle Scholar
  81. Ueda Y, Duncan MK, David LL (2002) Lens proteomics: the accumulation of crystallin modifications in the mouse lens with age. Invest Ophthalmol Vis Sci 43:205–215PubMedGoogle Scholar
  82. Von Sallmann L, Halver JE, Collins E, Grimes P (1966) Thioacetamide-induced cataract with invasive proliferation of the lens epithelium in rainbow trout. Cancer Res 26:1819–1825Google Scholar
  83. Wistow G (1993) Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem Sci 18:301–306CrossRefPubMedGoogle Scholar
  84. Wistow G (1995) Peptide sequences for beta-crystallins of a teleost fish. Mol Vis 1:1PubMedGoogle Scholar
  85. Wistow G, Wyatt K, David L, Gao C, Bateman O, Bernstein S, Tomarev S, Segovia L, Slingsby C, Vihtelic T (2005) γN-crystallin and the evolution of the βγ-crystallin superfamily in vertebrates. FEBS J 272:2276–2291CrossRefPubMedGoogle Scholar
  86. Yu CM, Chang GG, Chang HC, Chiou SH (2004) Cloning and characterization of a thermostable catfish alphaB-crystallin with chaperone-like activity at high temperatures. Exp Eye Res 79:249–261CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Andor J. Kiss
    • 1
    • 2
  • Arthur L. Devries
    • 1
  • Rachael M. Morgan-Kiss
    • 3
    • 4
  1. 1.Department of Animal BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Laboratory for Ecophysiological Cryobiology, Department of ZoologyMiami UniversityOxfordUSA
  3. 3.Department of MicrobiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  4. 4.Department of MicrobiologyMiami UniversityOxfordUSA

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