Evolution of mollusc lens crystalline: Glutathione S-transferase/S- crystallins and aldehyde dehydrogenase/Ω-crystallins

American Malacological Bulletin

Volumn 26, Issue 1-2, 2008, Pages 73-81

  Piatigorsky, Joram ^a  

^a NATIONAL EYE INSTITUTE   (United States)

Author keywords

Cephalopods; Enzymes; Eye; Gene expression; Lens proteins; Scallops

Indexed keywords

CEPHALOPODA; MOLLUSCA; PECTINIDAE;

EID: 58149393227     PISSN: 07402783     EISSN: None     Source Type: Journal    
DOI: 10.4003/006.026.0208     Document Type: Conference Paper

References (65)

1. Abedinia, M., T. Pain, E. M. Algar, and R. S. Holmes. 1990. Bovine corneal aldehyde dehydrogenase: The major soluble corneal protein with a possible dual protective role for the eye. Experimental Eye Research 51: 419-426.
2. Bateman, O. A., A. G. Purkiss, R. van Montfort, C. Slingsby, C. Graham, and G. Wistow. 2003. Crystal structure of eta-crystallin: Adaptation of a class 1 aldehyde dehydrogenase for a new role in the eye lens. Biochemistry 42: 4349-4356.
3. Benedek, G. B. 1971. Theory of transparency of the eye. Applied Optics 10: 459-473.
4. Bettelheim, F. A. and E. L. Siew. 1983. Effect of change in concentration upon lens turbidity as predicted by the random fluctuation theory. Biophysical Journal 41: 29-33.
5. Bloemendal, H. and W. W. de Jong. 1991. Lens proteins and their genes. Progress in Nucleic Acid Research and Molecular Biology 41: 259-281.
6. Carosa, E., Z. Kozmik, J. E. Rall, and J. Piatigorsky. 2002. Structure and expression of the scallop Omega-crystallin gene. Evidence for convergent evolution of promoter sequences. Journal of Biological Chemistry 277: 656-664.
7. Chiou, S. H. 1988. A novel crystallin from octopus lens. Federation of European Biochemical Societies Letters 241: 261-264.
8. Chiou, S. H., C. W. Yu, C. W. Lin, F. M. Pan, S. F. Lu, H. J. Lee, and G. G. Chang. 1995. Octopus S-crystallins with endogenous glutathione S-transferase (GST) activity: Sequence comparison and evolutionary relationships with authentic GST enzymes. Biochemical Journal 309 (Pt 3): 793-800.
9. Cuthbertson, R. A., S. I. Tomarev, and J. Piatigorsky. 1992. Taxon-specific recruitment of enzymes as major soluble proteins in the corneal epithelium of three mammals, chicken, and squid. Proceedings of the National Academy of Sciences of the United States of America 89: 4004-4008.
10. Cvekl, A. and J. Piatigorsky. 1996. Lens development and crystallin gene expression: Many roles for Pax-6. Bioessays 18: 621-630.
11. de Jong, W. W., W. Hendriks, J. W. Mulders, and H. Bloemendal. 1989. Evolution of eye lens crystalline: The stress connection. Trends in Biochemical Sciences 14: 365-368.
12. de Jong, W. W., N. H. Lubsen, and H. J. Kraft. 1994. Molecular evolution of the eye lens. Progress in Retinal and Eye Research 13: 391-442.
13. Delaye, M. and A. Tardieu. 1983. Short-range order of crystallin proteins accounts for eye lens transparency. Nature 302: 415-417.
14. Duncan, M. K., A. Cvekl, M. Kantorow, and J. Piatigorsky. 2004. Lens crystalline. In: M. L. Robinson and F. J. Lovicu, eds., Development of the Ocular Lens. Cambridge University Press, New York. Pp. 119-150
15. Estey, T., J. Piatigorsky, N. Lassen, and V. Vasiliou. 2007. ALDH3A1: A corneal crystallin with diverse functions. Experimental Eye Research 84: 3-12.
16. Gehring, W. J. 2004. Historical perspective on the development and evolution of eyes and photoreceptors. International Journal of Developmental Biology 48: 707-717.
17. Gehring, W. J. 2005. New perspectives on eye development and the evolution of eyes and photoreceptors. Journal of Heredity 96: 171-184.
18. Gehring, W. J. and K. Ikeo. 1999. Pax 6: Mastering eye morphogenesis and eye evolution. Trends in Genetics 15: 371-377.
19. Graham, C., J. Hodin, and G. Wistow. 1996. A retinaldehyde dehydrogenase as a structural protein in a mammalian eye lens: Gene recruitment of eta-crystallin. Journal of Bioligical Chemistry 271: 15623-15628.
20. Groger, H., P. Callaerts, W. J. Gehring, and V. Schmid. 2000. Characterization and expression analysis of an ancestor-type Pax gene in the hydrozoan jellyfish Podocoryne carnea. Mechanisms of Development 94: 157-169.
21. Harris, J., B. Coles, D. J. Meyer, and B. Ketterer. 1991. The isolation and characterization of the major glutathione S-transferase from the squid Loligo vulgaris. Comparative Biochemistry and Physiology (B) 98: 511-515.
22. Horwitz, J. 1992. Alpha-crystallin can function as a molecular chaperone. Proceedings of the National Academy of Sciences of the United States of America 89: 10449-10453.
23. Horwitz, J., L. Ding, V. Vasiliou, M. Cantore, and J. Piatigorsky. 2006. Scallop lens Omega-crystallin (ALDH1A9): A novel tetrameric aldehyde dehydrogenase. Biochemical Biophysical Research Communications 348: 1302-1309.
24. Hoshiyama, D., H. Suga, N. Iwabe, M. Koyanagi, N. Nikoh, K. Kuma, F. Matsuda, T. Honjo, and T. Miyata. 1998. Sponge Pax cDNA related to Pax-2/5/8 and ancient gene duplications in the Pax family. Journal of Molecular Evolution 47: 640-648.
25. Jester, J. V., T. Moller-Pedersen, J. Huang, C. M. Sax, W. T. Kays, H. D. Cavangh, W. M. Petroll, and J. Piatigorsky. 1999. The cellular basis of corneal transparency: Evidence for 'corneal crystallins'. Journal of Cell Science 112 (Pt 5): 613-622.
26. Jester, J. V., A. Budge, S. Fisher, and J. Huang. 2005. Corneal keratocytes: Phenotypic and species differences in abundant protein expression and in vitro light-scattering. Investigative Ophthalmology and Visual Sciences 46: 2369-2378.
27. Ji, X., E. C. von Rosenvinge, W. W. Johnson, S. I. Tomarev, J. Piatigorsky, R. N. Armstrong, and G. L. Gilliland. 1995. Three-dimensional structure, catalytic properties, and evolution of a sigma class glutathione transferase from squid, a progenitor of the lens S-crystallins of cephalopods. Biochemistry 34: 5317-5328.
28. Kozmik, Z., M. Daube, E. Frei, B. Norman, L. Kos, L. J. Dishaw, M. Noll, and J. Piatigorsky. 2003. Role of Pax Genes in Eye Evolution: A Cnidarian PaxB Gene Uniting Pax2 and Pax6 Functions. Developmental Cell 5: 773-785.
29. Miller, D. J., D. C. Hayward, J. S. Reece-Hoyes, I. Scholten, J. Catmull, W. J. Gehring, P. Callaerts, J. E. Larsen, and E. E. Ball. 2000. Pax gene diversity in the basal cnidarian Acropora millepora (Cnidaria, Anthozoa): Implications for the evolution of the Pax gene family. Proceedings of the National Academy of Sciences of the United States of America 97: 4475-4480.
30. Montgomery, M. K. and M. J. McFall-Ngai. 1992. The muscle-derived lens of a squid bioluminescent organ is biochemically convergent with the ocular lens: Evidence for recruitment of aldehyde dehydrogenase as a predominant structural protein. Journal of Biological Chemistry 267: 20999-21003.
31. Nees, D. W., E. F. Wawrousek, W. G. Robison, Jr., and J. Piatigorsky. 2002. Structurally normal corneas in aldehyde dehydrogenase 3a1-deficient mice. Molecular and Cellular Biology 22: 849-855.
32. Nilsson, D. E., L. Gislen, M. M. Coates, C. Skogh, and A. Garm. 2005. Advanced optics in a jellyfish eye. Nature 435: 201-205.
33. Packard, A. 1972. Cephalopods and fish: The limits of convergence. Biological Reviews 47: 241-307.
34. Perozich, J., H. Nicholas, B. C. Wang, R. Lindahl, and J. Hempel. 1999. Relationships within the aldehyde dehydrogenase extended family. Protein Science 8: 137-146.
35. Piatigorsky, J. 1998. Gene sharing in lens and cornea: Facts and implications. Progress in Retina and Eye Research 17: 145-174.
36. Piatigorsky, J. 2001. Enigma of the abundant water-soluble cytoplasmic proteins of the cornea: The "refracton" hypothesis. Cornea 20: 853-858.
37. Piatigorsky, J. 2006. Evolutionary genetics: Seeing the light: The role of inherited developmental cascades in the origins of vertebrate lenses and their crystalline. Heredity 96: 275-7.
38. Piatigorsky, J. 2007. Gene Sharing and Evolution: The Diversity of Protein Functions. Harvard University Press, Cambridge, Massachusetts.
39. Piatigorsky, J. and Z. Kozmik. 2004. Cubozoan jellyfish: An Evo/Devo model for eyes and other sensory systems. International Journal of Developmental Biology 48: 719-729.
40. Piatigorsky, J. and G. J. Wistow. 1989. Enzyme/crystallins: Gene sharing as an evolutionary strategy. Cell 57: 197-199.
41. Piatigorsky, J. and P. S. Zelenka. 1992. Transcriptional regulation of crystallin genes: cis-elements, trans-factors, and signal transduction systems in the lens. Advances in Developmental Biochemistry 1: 211-256.
42. Piatigorsky, J., J. Horwitz, and B. L. Norman. 1993. J1-crystallins of the cubomedusan jellyfish lens constitute a novel family encoded in at least three intronless genes. Journal of Biological Chemistry 268: 11894-11901.
43. Piatigorsky, J., J. Horwitz, T. Kuwabara, and C. E. Cutress. 1989. The cellular eye lens and crystalline of cubomedusan jellyfish. Journal of Comparative Physiology (A) 164: 577-587.
44. Piatigorsky, J., W. E. O'Brien, B. L. Norman, K. Kalumuck, G. J. Wistow, T. Borras, J. M. Nickerson, and E. F. Wawrousek. 1988. Gene sharing by delta-crystallin and argininosuccinate lyase. Proceedings of the National Academy of Sciences of the United States of America 85: 3479-3483.
45. Piatigorsky, J., Z. Kozmik, J. Horwitz, L. Ding, E. Carosa, W. G. Robison, Jr., P. J. Steinbach, and E. R. Tamm. 2000. Omega-crystallin of the scallop lens. A dimeric aldehyde dehydrogenase class 1/2 enzyme-crystallin. Journal of Biological Chemistry 275: 41064-41073.
46. Roth, H. J., G. C. Das, and J. Piatigorsky. 1991. Chicken beta B1-crystallin gene expression: Presence of conserved functional polyomavirus enhancer-like and octamer binding-like promoter elements found in non-lens genes. Molecular and Cellular Biology 11: 1488-1499.
47. Shimeld, S. M., A. G. Purkiss, R. P. Dirks, O. A. Bateman, C. Slingsby, and N. H. Lubsen. 2005. Urochordate betagamma-crystallin and the evolutionary origin of the vertebrate eye lens. Current Biology 15: 1684-1689.
48. Siezen, R. J. and D. C. Shaw. 1982. Physicochemical characterization of lens proteins of the squid Nototodarus gouldi and comparison with vertebrate crystallins. Biochimica Biophysica Acta 704: 304-320.
49. Sophos, N. A. and V. Vasiliou. 2003. Aldehyde dehydrogenase gene superfamily: The 2002 update. Chemico-Biological Interaction 143-144: 5-22.
50. Sun, H., A. Rodin, Y. Zhou, D. P. Dickinson, D. E. Harper, D. Hewett-Emmett, and W. H. Li. 1997. Evolution of paired domains: Isolation and sequencing of jellyfish and hydra Pax genes related to Pax-5 and Pax-6. Proceedings of the National Academy of Sciences of the United States of America 94: 5156-5161.
51. Sun, H., D. P. Dickinson, J. Costello, and W. H. Li. 2001. Isolation of Cladonema Pax-B genes and studies of the DNA-binding properties of cnidarian Pax paired domains. Molecular Biology Evolution 18: 1905-1918.
52. Sweeney, A. M., D. L. Des Marais, Y. E. Ban, and S. Johnsen. 2007. Evolution of graded refractive index in squid lenses. Journal of the Royal Society Interface 4: 685-698.
53. Tang, S. S., C. C. Lin, and G. G. Chang. 1994. Isolation and characterization of octopus hepatopancreatic glutathione S-transferase: Comparison of digestive gland enzyme with lens S-crystallin. Journal of Protein Chemistry 13: 609-618.
54. Tomarev, S. I. and R. D. Zinovieva. 1988. Squid major lens polypeptides are homologous to glutathione S-transferases subunits. Nature 336: 86-88.
55. Tomarev, S. I., R. D. Zinovieva, and J. Piatigorsky. 1991. Crystallins of the octopus lens. Recruitment from detoxification enzymes. Journal of Biological Chemistry 266: 24226-24231.
56. Tomarev, S. I., R. D. Zinovieva, and J. Piatigorsky. 1992. Characterization of squid crystallin genes. Comparison with mammalian glutathione S-transferase genes. Journal of Biological Chemistry 267: 8604-8612.
57. Tomarev, S. I., R. D. Zinovieva, K. Guo, and J. Piatigorsky. 1993. Squid glutathione S-transferase. Relationships with other glutathione S-transferases and S-crystallins of cephalopods. Journal of Biological Chemistry 268: 4534-4542.
58. Tomarev, S. I., M. K. Duncan, H. J. Roth, A. Cvekl, and J. Piatigorsky. 1994. Convergent evolution of crystallin gene regulation in squid and chicken: The AP-1/ARE connection. Journal of Molecular Evolution 39: 134-143.
59. Tomarev, S. I., S. Chung, and J. Piatigorsky. 1995. Glutathione S-transferase and S-crystallins of cephalopods: Evolution from active enzyme to lens-refractive proteins. Journal of Molecular Evolution 41: 1048-1056.
60. Tomarev, S. I. and J. Piatigorsky. 1996. Lens crystalline of invertebrates - diversity and recruitment from detoxification enzymes and novel proteins. European Journal of Biochemistry 235: 449-465.
61. Tomarev, S. I., P. Callaerts, L. Kos, R. Zinovieva, G. Halder, W. Gehring, and J. Piatigorsky. 1997. Squid Pax-6 and eye development. Proceedings of the National Academy of Sciences of the United States of America 94: 2421-2426.
62. Vasiliou, V., A. Bairoch, K. F. Tipton, and D. W. Nebert. 1999. Eukaryotic aldehyde dehydrogenase (ALDH) genes: Human polymorphisms, and recommended nomenclature based on divergent evolution and chromosomal mapping. Pharmacogenetics 9: 421-434.
63. West, J. A., J. G. Sivak, J. Pasternak, and J. Piatigorsky. 1994. Immunolocalization of S-crystallins in the developing squid (Loligo opalescens) lens. Developmental Dynamics 199: 85-92.
64. Wistow, G. J. and J. Piatigorsky. 1988. Lens crystallins: The evolution and expression of proteins for a highly specialized tissue. Annual Reviews of Biochemistry 57: 479-504.
65. Zinovieva, R. D., S. I. Tomarev, and J. Piatigorsky. 1993. Aldehyde dehydrogenase-derived omega-crystallins of squid and octopus. Specialization for lens expression. Journal of Biological Chemistry 268: 11449-11455.