Cold-stable eye lens crystallins of the Antarctic nototheniid toothfish Dissostichus mawsoni Norman

Journal of Experimental Biology

Volumn 207, Issue 26, 2004, Pages 4633-4649

  Kiss, Andor J ^a   Mirarefi, Amir Y ^a   Ramakrishnan, Subramanian ^a   Zukoski, Charles F ^a   DeVries, Arthur L ^a   Cheng, Chi Hing C ^a  

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

Author keywords

Alpha crystallin; Antarctic toothfish; Bigeye tuna; Chaperone; Cold adaptation; Cold cataract; Dissostichus mawsoni; Dynamic light scattering; Gamma crystallin; Lens crystallins

Indexed keywords

ALPHA CRYSTALLIN; CHAPERONE; HEAT SHOCK PROTEIN;

ACCLIMATIZATION; ANIMAL; ANTARCTICA; ARTICLE; CATTLE; CHEMISTRY; COLD; COMPARATIVE STUDY; GEL CHROMATOGRAPHY; IMMUNOBLOTTING; LENS; METABOLISM; PERCIFORMES; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SPECIES DIFFERENCE;

ACCLIMATIZATION; ALPHA-CRYSTALLINS; ANIMALS; ANTARCTIC REGIONS; CATTLE; CHROMATOGRAPHY, GEL; COLD; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEAT-SHOCK PROTEINS; IMMUNOBLOTTING; LENS, CRYSTALLINE; MOLECULAR CHAPERONES; PERCIFORMES; SPECIES SPECIFICITY;

BOS; BOS TAURUS; DISSOSTICHUS; DISSOSTICHUS MAWSONI; MAMMALIA; PISCES; SCOMBRIDAE GEN. SP.; THUNNUS; THUNNUS OBESUS;

EID: 13144261777     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01312     Document Type: Article

References (81)

1. Abgar, S., Yevlampieva, N., Aerts, T., Vanhoudt, J. and Clauwaert, J. (2000). Chaperone-like activity of bovine lens alpha-crystallin in the presence of dithiothreitol-destabilized proteins: characterization of the formed complexes. Biochem. Biophys. Res. Commun. 276, 619-625.
2. Abgar, S., Vanhoudt, J., Aerts, T. and Clauwaert, J. (2001). Study of the chaperoning mechanism of bovine lens alpha-crystallin, a member of the alpha-small heat shock superfamily. Biophys. J. 80, 1986-1995.
3. Annunziata, O., Ogun, O. and Benedek, G. B. (2003). Observation of liquid-liquid phase separation for eye lens {gamma}S-crystallin. Proc. Natl. Acad. Sci. USA 15, 15.
4. Augusteyn, R. C., Parkhill, E. M. and Stevens, A. (1992). The effects of isolation buffers on the properties of α-crystallin. Exp. Eye Res. 54, 219-228.
5. Augusteyn, R. C., Murnane, L., Nicola, A. and Stevens, A. (2002). Chaperone activity in the lens. Clin. Exp. Optom. 85, 83-90.
6. Banh, A. and Sivak, J. G. (2004). Laser scanning analysis of cold-cataract in young and old bovine lenses. Mol. Vis. 10, 144-147.
7. Björk, I. (1961). Studies on γ-crystallin from calf lens: I isolation by gel filtration. Exp. Eye Res. 1, 145-154.
8. Bloemendal, H. (1986). The lens proteins. In Molecular and Cellular Biology of the Eye Lens (ed. H. Bloemendal), pp. 1-47. New York: Wiley and Sons.
9. Broide, M. L., Borland, C. R., Pande, J., Ogun, O. O. and Benedek, G. B. (1991). Binary-liquid phase separation of lens protein solutions. Proc. Natl. Acad. Sci. USA 88, 5660-5664.
10. Chen, L., DeVries, A. L. and Cheng, C. H. (1997a). Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc. Natl. Acad. Sci. USA 94, 3817-3822.
11. Chen, L., DeVries, A. L. and Cheng, C. H. (1997b). Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc. Natl. Acad. Sci. USA 94, 3811-3816.
12. Cheng, C. H. and Chen, L. (1999). Evolution of an antifreeze glycoprotein. Nature 401, 443-444.
13. Chiou, S. H., Chang, T., Chang, W. C., Kuo, J. and Lo, T. B. (1986). Characterization of lens crystallins and their mRNA from the carp lenses. Biochim. Biophys. Acta 871, 324-328.
14. Chiou, S. H., Chang, W. C., Pan, F. M., Chang, T. and Lo, T. B. (1987). Physicochemical characterization of lens crystallins from the carp and biochemical comparison with other vertebrate and invertebrate crystallins. J. Biochem. (Tokyo) 101, 751-759.
15. Clark, J. I. and Benedek, G. B. (1980a). The effects of glycols, aldehydes, and acrylamide on phase separation and opacification in the calf lens. Invest. Ophthalmol. Vis. Sci. 19, 771-776.
16. Clark, J. I. and Benedek, G. B. (1980b). Phase diagram for cell cytoplasm from the calf lens. Biochem. Biophys. Res. Commun. 95, 482-489.
17. Cossins, A. R., Murray, P. A., Gracey, A. Y., Logue, J., Polley, S., Caddick, M., Brooks, S., Postle, T. and Maclean, N. (2002). The role of desaturases in cold-induced lipid restructuring. Biochem. Soc. Trans. 30, 1082-1086.
18. Davson, H. (1990). Physiology of the Eye. New York, NY: Pergamon Press, Inc.
19. de Jong, W. W., Leunissen, J. A. and Voorter, C. E. (1993). Evolution of the alpha-crystallin/small heat-shock protein family. Mol. Biol. Evol. 10, 103-126.
20. Delaye, M., Clark, J. I. and Benedek, G. B. (1982). Identification of the scattering elements responsible for lens opacification in cold-cataracts. Biophys. J. 37, 647-656.
21. Derham, B. K., van Boekel, M. A., Muchowski, P. J., Clark, J. I., Horwitz, J., Hepburne-Scott, H. W., de Jong, W. W., Crabbe, M. J. and Harding, J. J. (2001). Chaperone function of mutant versions of alpha A- and alpha B-crystallin prepared to pinpoint chaperone binding sites. Eur. J. Biochem. 268, 713-721.
22. Detrich, H. W., 3rd, Parker, S. K., Williams, R. C., Jr, Nogales, E. and Downing, K. H. (2000). Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes present in the alpha- and beta-tubulins of Antarctic fishes. J. Biol. Chem. 275, 37038-37047.
23. DeVries, A. L. (1971). Glycoproteins as biological antifreeze agents in antarctic fishes. Science 172, 1152-1155.
24. Eastman, J. T. (1993). Antarctic Fish Biology: Evolution in a Unique Environment. New York: Academic Press, Inc.
25. Eastman, J. T. and Lannoo, M. J. (2001). Anatomy and histology of the brain and sense organs of the Antarctic eel cod Muraenolepis microps (Gadiformes; Muraenolepididae). J. Morphol. 250, 34-50.
26. Eastman, J. T. and Lannoo, M. J. (2003). Anatomy and histology of the brain and sense organs of the Antarctic plunderfish Dolloidraco longedorsalis (Perciformes: Notothenioidei: Artedidraconidae), with comments on the brain morphology of other artedidraconids and closely related harpagiferids. J. Morphol. 255, 358-377.
27. Eastman, J. T. and McCune, A. R. (2000). Fishes on the Antarctic continental shelf: evolution of a marine species flock? J. Fish Biol. 57 Suppl. A, 84-102.
28. Ferguson, W. E., Calhoun, W. B., 3rd and Koenig, V. L. (1971). Studies on the cold insoluble proteins from the lens of the striped mullet (Mugil cephalus). Comp. Biochem. Physiol. 40B, 959-972.
29. Fields, P. A. and Somero, G. N. (1998). Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes. Proc. Natl. Acad. Sci. USA 95, 11476-11481.
30. Gomori, G. (1955). Preparation for use in enzyme studies. Meth. Enzymol. 1, 138-146.
31. Gulik-Krzywicki, T., Tardieu, A. and Delaye, M. (1984). Spatial reorganization of low molecular weight proteins during cold-cataract opacification. Biochim. Biophys. Acta 800, 28-32.
32. 2+-free medium. Exp. Eye Res. 41, 179-182.
33. Hikida, M. and Iwata, S. (1986). Studies of eye lens in poikilothermal animals. III. Long-term incubation of rainbow trout lenses. Jpn. J. Ophthalmol. 30, 43-50.
34. Hochachka, P. W. and Somero, G. (2002). Biochemical Adaptation: Mechanism and Process in Physiological Evolution. New York: Oxford University Press.
35. Holland, K. N., Brill, R. W., Chang, R. K. C., Sibert, J. R. and Fournier, D. A. (1992). Physiological and behavioral thermoregulation in bigeye tuna (Thunnus obesus). Nature 358, 410-412.
36. Horwitz, J. (1992). Alpha-crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. USA 89, 10449-10453.
37. Horwitz, J. (2003). Alpha-crystallin. Exp. Eye Res. 76, 145-153.
38. Horwitz, J., Huang, Q. L., Ding, L. and Bova, M. P. (1998). Lens alpha-crystallin: chaperone-like properties. Meth. Enzymol. 290, 365-383.
39. Hunt, B. M., Hoefling, K. and Cheng, C.-H. C. (2003). Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fish. Antarctic Sci. 15, 333-338.
40. Ingolia, T. D. and Craig, E. A. (1982). Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc. Natl. Acad. Sci. USA 79, 2360-2364.
41. Jaenicke, R. and Seckler, R. (1997). Protein misassembly in vitro. Adv. Protein Chem. 50, 1-59.
42. Jagger, W. S. and Sands, P. J. (1996). A wide-angle gradient index optical model of the crystallin lens and eye of the rainbow trout. Vision Res. 36, 2623-2639.
43. Jagger, W. S. and Sands, P. J. (1999). A wide-angle gradient index optical model of the crystallin lens and eye of the octopus. Vision Res. 39, 2841-2852.
44. Johnston, I. A., Walesby, N. J., Davison, W. and Goldspink, G. (1975). Temperature adaptation in myosin of Antarctic fish. Nature 254, 74-75.
45. Kokke, B. P., Boelens, W. C. and de Jong, W. W. (2001). The lack of chaperonelike activity of Caenorhabditis elegans Hsp12.2 cannot be restored by domain swapping with human alphaB-crystallin. Cell Stress Chaperones 6, 360-367.
46. Krivandin, A. V., Muranov, K. O. and Ostrovsky, M. A. (2004). Heat-induced complex formation in solutions of alpha- and beta L-crystallins: a small-angle X-ray scattering study. Dokl. Biochem. Biophys. 394, 1-4.
47. Liao, J. H., Lee, J. S. and Chiou, S. H. (2002). Distinct roles of alphaA- and aiphaB-crystallins under thermal and UV stresses. Biochem. Biophys. Res. Commun. 295, 854-861.
48. Liaw, Y. C., Chiou, S. H., Chang, T. and Chang, W. C. (1992). Predicted secondary and tertiary structures of carp gamma-crystallins with high methionine content: role of methionine residues in the protein stability. J. Biochem. (Tokyo) 112, 341-345.
49. Loewenstein, M. A. and Bettelheim, F. A. (1979). Cold-cataract formation in fish lenses. Exp. Eye Res. 28, 651-663.
50. McFall-Ngai, M. J. and Horwitz, J. (1990). A comparative study of the thermal stability of the vertebrate eye lens: Antarctic ice fish to the desert iguana. Exp. Eye Res. 50, 703-709.
51. Mörner, C. T. (1864), Untersuchung der Proteïnsubstanzen in den leichtbrechenden Medien des Auges I. Zeit. Physiol. Chemie 18, 61-106.
52. Narberhaus, F. (2002). Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol. Mol. Biol. Rev. 66, 64-93.
53. Norledge, B. V., Hay, R. E., Bateman, O. A., Slingsby, C. and Driessen, H. P. C. (1997). Towards a molecular understanding of phase separation in the lens - a comparison of the X-ray structures of two high T-C Gamma-crystallins, Gamma-E and Gamma-F, with two low T-C Gamma-crystallins, Gamma-B and Gamma-D. Exp. Eye Res. 65, 609-630.
54. Pasta, S. Y., Raman, B., Ramakrishna, T. and Rao, C. M. (2002). Role of the C-terminal extensions of alpha-crystallins. Swapping the C-terminal extension of alpha A-crystallin to alpha B-crystallin results in enhanced chaperone activity. J. Biol. Chem. 277, 45821-45828.
55. Pasta, S. Y., Raman, B., Ramakrishna, T. and Rao, C. M. (2003). Role of the conserved SRLFDQFFG region of alpha-crystallin, a small heat shock protein. Effect on oligomeric size, subunit exchange, and chaperone-like activity. J Biol. Chem. 278, 51159-51166.
56. Piccione, G., Caola, G. and Refinetti, R. (2003). Daily and estrous rhythmicity of body temperature in domestic cattle. BMC Physiol. 3, 7.
57. Pierscionek, B. K. and Augusteyn, R. C. (1995). The refractive index and protein distribution in the blue eye trevally lens. J. Am. Optom. Assn. 66, 739-743.
58. Posner, M. (2003). A comparative view of alpha crystallins: The contribution of comparative studies to understanding function. Int. Comp. Biol. 43, 481-491.
59. Posner, M., Kantorow, M. and Horwitz, J. (1999). Cloning, sequencing and differential expression of alphaB-crystallin in the zebrafish, Danio rerio. Biochim. Biophys. Acta 1447, 271-277.
60. Privalov, P. L. (1990). Cold denaturation of proteins. Crit. Rev. Biochem. Mol. Biol. 25, 281-305.
61. Putilina, T., Skouri-Panet, F., Prat, K., Lubsen, N. H. and Tardieu, A. (2003). Subunit exchange demonstrates a differential chaperone activity of calf alpha-crystallin toward beta low- and individual gamma-crystallins. J. Biol. Chem. 278, 13747-13756.
62. Raman, B. and Rao, C. M. (1997). Chaperone-like activity and temperature-induced structural changes of alpha-crystallin. J. Biol. Chem. 272, 23559-23564.
63. Romisch, K., Collie, N., Soto, N., Logue, J., Lindsay, M., Scheper, W. and Cheng, C. H. (2003). Protein translocation across the endoplasmic reticulum membrane in cold-adapted organisms. J. Cell Sci. 116, 2875-2883.
64. Runkle, S., Hill, J., Kantorow, M., Horwitz, J. and Posner, M. (2002). Sequence and spatial expression of zebrafish (Danio rerio) alphaA-crystallin. Mol. Vis. 8, 45-50.
65. Siezen, R. J., Fisch, M. R., Slingsby, C. and Benedek, G. B. (1985). Opacification of gamma-crystallin solutions from calf lens in relation to cold-cataract formation. Proc. Natl. Acad. Sci. USA 82, 1701-1705.
66. Siezen, R. J., Anello, R. D. and Thomson, J. A. (1986). Interactions of lens proteins. Concentration dependence of beta-crystallin ageregation. Exp. Eye Res. 43, 293-303.
67. Slingsby, C. and Clout, N. J. (1999). Structure of the crystallins. Eye 13, 395-402.
68. Smith, A. C. (1972). Lens iso-precipitin in yellowfin tuna (Thunnus albacares). Comp. Biochem. Physiol. 42B, 497-499.
69. Summers, L. J., Slingsby, C., Blundell, T. L., den Dunnen, J. T., Moormann, R. J. and Schoenmakers, J. G. (1986). Structural variation in mammalian gamma-crystallins based on computer graphics analyses of human, rat and calf sequences. 1. Core packing and surface properties. Exp. Eye Res. 43, 77-92.
70. Thomson, J. A., Schurtenberger, P., Thurston, G. M. and Benedek, G. B. (1987). Binary liquid phase separation and critical phenomena in a protein/water solution. Proc. Natl. Acad. Sci. USA 84, 7079-7083.
71. Tsai, C. J., Maizel, J. V., Jr and Nussinov, R. (2002). The hydrophobic effect: a new insight from cold denaturation and a two-state water structure. Crit. Rev. Biochem. Mol. Biol. 37, 55-69.
72. van Dam, A. F. (1966). Purification and composition studies of βs-crystallin. Exp. Eye Res. 5, 255-266.
73. Vanhoudt, J., Abgar, S., Aerts, T. and Clauwaert, J. (2000). Native quaternary structure of bovine alpha-crystallin. Biochemistry 39, 4483-4492.
74. Williams, R. C., Jr, Correia, J. J. and DeVries, A. L. (1985). Formation of microtubules at low temperature by tubulin from Antarctic fish. Biochemistry 24, 2790-2798.
75. Wistow, G. (1993). Lens crystallins: gene recruitment and evolutionary dynamism. Trends Biochem Sci 18, 301-306.
76. Wistow, G. (1995). Peptide sequences for beta-crystallins of a teleost fish. Mol. Vis 1, 1. http://www.molvis.org/molvis/vl/al/〉.
77. Wolken, J. J. (1995). Bird and fish eyes. In Light Detectors, Photoreceptors and Imaging Systems in Nature, vol. 1 (ed. J. J. Wolken), pp. 259. New York: Oxford University Press.
78. Yu, C. M., Chang, G. G., Chang, H. C. and Chiou, S. H. (2004). Cloning and characterization of a thermostable catfish alphaB-crystallin with chaperone-like activity at high temperatures. Exp. Eye Res. 79, 249-261.
79. Zigler, J. S., Jr and Sidbury, J. B., Jr (1976). A comparative study of the beta-crystallins of four sub-mammalian species. Comp. Biochem. Physiol. 55B, 19-24.
80. Zigman, S. and Lerman, S. (1964). A cold precipitable protein in the lens. Nature 203, 662-663.
81. Zigman, S. and Lerman, S. (1965). Properties of a cold-precipitable protein fraction in the lens. Exp. Eye Res. 159, 24-30.