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

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 180, Issue 7, 2010, Pages 1019-1032

  Kiss, Andor J ^a,b   Devries, Arthur L ^a   Morgan Kiss, Rachael M ^b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b MIAMI UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

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

Indexed keywords

ALPHA CRYSTALLIN; BETA CRYSTALLIN; CRYSTALLIN; FATTY ACID; GAMMA CRYSTALLIN; PHOSPHOLIPID; UNSATURATED FATTY ACID;

ANIMAL; ARTICLE; CATARACT; CATTLE; CHEMISTRY; COMPARATIVE STUDY; DISEASE MODEL; ELECTROSPRAY MASS SPECTROMETRY; EPITHELIUM; ISOLATION AND PURIFICATION; LENS; LENS NUCLEUS; LONGEVITY; METABOLISM; PERCIFORMES; PROTEIN STABILITY; SOLUBILITY;

ALPHA-CRYSTALLINS; ANIMALS; BETA-CRYSTALLINS; CATARACT; CATTLE; CRYSTALLINS; DISEASE MODELS, ANIMAL; EPITHELIUM; FATTY ACIDS; FATTY ACIDS, UNSATURATED; GAMMA-CRYSTALLINS; LENS CORTEX, CRYSTALLINE; LENS NUCLEUS, CRYSTALLINE; LENS, CRYSTALLINE; LONGEVITY; PERCIFORMES; PHOSPHOLIPIDS; PROTEIN STABILITY; SOLUBILITY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

ANIMALIA; BOVINAE; DISSOSTICHUS MAWSONI; MAMMALIA; PISCES;

EID: 77956772127     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-010-0475-9     Document Type: Article

References (86)

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: 405-415.
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: 277-283.
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: 213-227.
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: 225-229.
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: 1-13.
6. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
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: 177-190.
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: 407-485.
9. Borchman D, Yappert MC, Afzal M (2004) Lens lipids and maximum lifespan. Exp Eye Res 79: 761-768.
10. Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an antarctic fish: on ice for winter. PLoS One 3: e1743.
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: 105-110.
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: 335-338.
13. Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68: 893-905.
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: 117-127.
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: 146-150.
16. Cvekl A, Piatigorsky J (1996) Lens development and crystallin gene expression: many roles for Pax-6. Bioessays 18: 621-630.
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: 74-89.
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: 225-340.
19. Danysh BP, Duncan MK (2009) The lens capsule. Exp Eye Res 88: 151-164.
20. Davson H (1990). In: Davson H (ed) Physiology of the eye. Pergamon Press, Inc, New York.
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: 415-417.
23. Dische Z (1965) The glycoproteins and glycolipoproteins of the bovine lens and their relation to albuminoid. Invest Ophthalmol 4: 759-778.
24. Fulhorst HW, Young RW (1966) Conversion of soluble lens protein to albuminoid. Invest Ophthalmol 5: 298-303.
25. Greiling TMS, Houck SA, Clark JI (2009) The zebrafish lens proteome during development and aging. Mol Vis 15: 2313-2325.
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: 53-63.
27. Hains PG, Truscott RJW (2007) Post-translational modifications in the nuclear region of young, aged, and cataract human lenses. J Proteome Res 6: 3935-3943.
28. Han X, Gross RW (1994) Electrospray ionization mass spectroscopic analysis of human erythrocyte plasma membrane phospholipids. Proc Natl Acad Sci USA 91: 10635-10639.
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: 1-73.
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: 476-489.
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: 982-987.
32. Hochachka PW, Somero G (2002) Biochemical adaptation. In: Hochachka PW, Somero G (eds) Mechanism and process in physiological evolution. Oxford University Press, New York.
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: 275-287.
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: 125-138.
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: 2623-2639.
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: 946-957.
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-Champaign.
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: 155-171.
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: 4633-4649.
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: 1815-1822.
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: 31-43.
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: 9274-9279.
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: 379-385.
44. Loewenstein MA, Bettelheim FA (1979) Cold cataract formation in fish lenses. Exp Eye Res 28: 651-663.
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: 2105-2115.
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 3-26.
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.
48. Mörner C (1864) Untersuchung der Proteïnsubstanzen in den leichtbrechenden Medien des Auges I. Zeitscrift für physiologische Chemie 18: 61-106.
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: 725-732.
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: 51-56.
51. Paolisso G, Barbieri M, Bonafè M, Franceschi C (2000) Metabolic age modelling: the lesson from centenarians. Eur J Clin Invest 30: 888-894.
52. Paterson CA, Delamere NA (1992). In: Mosby-Year Book (ed) Physiology of the Eye. Mosby-Year Book, New York.
53. Patwardhan V, Modak SP (1992) Physicochemical characterization and phylogenetic comparison of fish lens proteins. Indian J Biochem Biophys 29: 498-507.
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: 11-23.
55. Pierscionek BK, Augusteyn RC (1991) Structure/function relationship between optics and biochemistry of the lens. Lens Eye Toxic Res 8: 229-243.
56. Pierscionek BK, Augusteyn RC (1995) The refractive index and protein distribution in the blue eye trevally lens. J Am Optom Assoc 66: 739-743.
57. Posner M (2003) A comparative view of alpha crystallins: the contribution of comparative studies to understanding function. Integr Comp Biol 43: 481-491.
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: 806-814.
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: 569-579.
60. Rezanka T, Sigler K (2009) Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdoms. Prog Lipid Res 48: 206-238.
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: 2875-2883.
62. Rujoi M, Estrada R, Yappert MC (2004) In situ MALDI-TOF MS regional analysis of neutral phospholipids in lens tissue. Anal Chem 76: 1657-1663.
63. Sand D, Glass R, Olson D, Pike H, Schlenk H (1984) Metabolism of furan fatty acids in fish. Biochim Biophys Acta 793: 429-434.
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: 8477-8485.
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.
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: 81-93.
67. Sinclair A, Murphy K, Li D (2000) Marine lipids: overview "news insights and lipid composition of Lyprinol". Allergy Immunol 32: 261-271.
68. Sivak JG (1985) The Glenn A. fry award lecture: optics of the crystalline lens. Am J Optom Physiol Opt 62: 299-308.
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 63-80.
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: 551-559.
71. Smith AC (1969b) Protein variation in the eye lens nucleus of the mackerel scad (Decapterus pinnulatus). Comp Biochem Physiol 28: 1161-1168.
72. Smith AC (1988) Indirect tissue electrophoresis: a new method for analyzing solid tissue protein. Comp Biochem Physiol B 90: 791-794.
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: 601-608.
74. Spector A (1984a) Oxidation and cataract. Ciba Found Symp 106: 48-64.
75. Spector A (1984b) The search for a solution to senile cataracts. Proctor lecture. Invest Ophthalmol Vis Sci 25: 130-146.
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: 3177-3181.
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: 233-238.
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: 863-869.
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: 19-21.
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: 49-56.
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: 205-215.
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: 1819-1825.
83. Wistow G (1993) Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem Sci 18: 301-306.
84. Wistow G (1995) Peptide sequences for beta-crystallins of a teleost fish. Mol Vis 1: 1.
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: 2276-2291.
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: 249-261.