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. 1995 Aug 1;309(Pt 3):793–800. doi: 10.1042/bj3090793

Octopus S-crystallins with endogenous glutathione S-transferase (GST) activity: sequence comparison and evolutionary relationships with authentic GST enzymes.

S H Chiou 1, C W Yu 1, C W Lin 1, F M Pan 1, S F Lu 1, H J Lee 1, G G Chang 1
PMCID: PMC1135702  PMID: 7639695

Abstract

S-Crystallin is a major protein present in the lenses of cephalopods (octopus and squid). To facilitate the cloning of this crystallin gene, cDNA was constructed from the poly(A)+ mRNA of octopus lenses, and amplified by PCR for nucleotide sequencing. Sequencing of 10 of 15 positive clones coding for this crystallin revealed three distinct S-crystallin isoforms with 61-64% identity in nucleotide sequences and 42-58% similarity in amino acid sequences when compared with homologous crystallins in squid lenses. These charge-isomeric crystallins also show between 26 and 33% amino acid sequence identity to four major classes of glutathione S-transferase (GST), a major detoxification enzyme present in most mammalian tissues. For further analysis, expression of one of the S-crystallin cDNAs was carried out in the bacterial expression system pQE-30, and the S-crystallin protein produced in Escherichia coli was purified to homogeneity to determine the enzymic properties. We found that the expressed octopus S-crystallin possessed much lower GST activity than the authentic GSTs from other tissues. Sequence comparison and construction of phylogenetic trees for S-crystallins from squid and octopus lenses and various classes of GSTs revealed that S-crystallins represent a multigene family which is structurally related to Alpha-class GSTs and probably derived from the ancestral GST by gene duplication and subsequent multiple mutational substitutions.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abramovitz M., Listowsky I. Selective expression of a unique glutathione S-transferase Yb3 gene in rat brain. J Biol Chem. 1987 Jun 5;262(16):7770–7773. [PubMed] [Google Scholar]
  2. Armstrong R. N. Glutathione S-transferases: reaction mechanism, structure, and function. Chem Res Toxicol. 1991 Mar-Apr;4(2):131–140. doi: 10.1021/tx00020a001. [DOI] [PubMed] [Google Scholar]
  3. Bloemendal H. Lens proteins. CRC Crit Rev Biochem. 1982;12(1):1–38. doi: 10.3109/10409238209105849. [DOI] [PubMed] [Google Scholar]
  4. Bloemendal H., de Jong W. W. Lens proteins and their genes. Prog Nucleic Acid Res Mol Biol. 1991;41:259–281. doi: 10.1016/s0079-6603(08)60012-4. [DOI] [PubMed] [Google Scholar]
  5. Chiou S. H. A novel crystallin from octopus lens. FEBS Lett. 1988 Dec 5;241(1-2):261–264. doi: 10.1016/0014-5793(88)81073-1. [DOI] [PubMed] [Google Scholar]
  6. Chiou S. H., Chang W. C., Pan F. M., Chang T., Lo T. B. Physicochemical characterization of lens crystallins from the carp and biochemical comparison with other vertebrate and invertebrate crystallins. J Biochem. 1987 Mar;101(3):751–759. doi: 10.1093/jb/101.3.751. [DOI] [PubMed] [Google Scholar]
  7. Chiou S. H., Lee H. J., Chang G. G. Kinetic analysis of duck epsilon-crystallin, a lens structural protein with lactate dehydrogenase activity. Biochem J. 1990 Apr 1;267(1):51–58. doi: 10.1042/bj2670051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chiou S. H. Phylogenetic comparison of lens crystallins from the vertebrate and invertebrate--convergent or divergent evolution? FEBS Lett. 1986 May 26;201(1):69–73. doi: 10.1016/0014-5793(86)80572-5. [DOI] [PubMed] [Google Scholar]
  9. Chiou S. H., Wang K. T. Simplified protein hydrolysis with methanesulphonic acid at elevated temperature for the complete amino acid analysis of proteins. J Chromatogr. 1988 Sep 16;448(3):404–410. doi: 10.1016/s0021-9673(01)84603-3. [DOI] [PubMed] [Google Scholar]
  10. Dirr H., Reinemer P., Huber R. X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition and catalytic function. Eur J Biochem. 1994 Mar 15;220(3):645–661. doi: 10.1111/j.1432-1033.1994.tb18666.x. [DOI] [PubMed] [Google Scholar]
  11. Habig W. H., Jakoby W. B. Assays for differentiation of glutathione S-transferases. Methods Enzymol. 1981;77:398–405. doi: 10.1016/s0076-6879(81)77053-8. [DOI] [PubMed] [Google Scholar]
  12. Harding J. J., Dilley K. J. Structural proteins of the mammalian lens: a review with emphasis on changes in development, aging and cataract. Exp Eye Res. 1976 Jan;22(1):1–73. doi: 10.1016/0014-4835(76)90033-6. [DOI] [PubMed] [Google Scholar]
  13. Hein J. Unified approach to alignment and phylogenies. Methods Enzymol. 1990;183:626–645. doi: 10.1016/0076-6879(90)83041-7. [DOI] [PubMed] [Google Scholar]
  14. Ji X., Zhang P., Armstrong R. N., Gilliland G. L. The three-dimensional structure of a glutathione S-transferase from the mu gene class. Structural analysis of the binary complex of isoenzyme 3-3 and glutathione at 2.2-A resolution. Biochemistry. 1992 Oct 27;31(42):10169–10184. doi: 10.1021/bi00157a004. [DOI] [PubMed] [Google Scholar]
  15. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  16. Lee H. J., Chiou S. H., Chang G. G. Biochemical characterization and kinetic analysis of duck delta-crystallin with endogenous argininosuccinate lyase activity. Biochem J. 1992 Apr 15;283(Pt 2):597–603. doi: 10.1042/bj2830597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lin C. W., Chiou S. H. Facile cloning and sequencing of S-crystallin genes from octopus lenses based on polymerase chain reaction. Biochem Int. 1992 Jun;27(1):173–178. [PubMed] [Google Scholar]
  18. Mannervik B., Danielson U. H. Glutathione transferases--structure and catalytic activity. CRC Crit Rev Biochem. 1988;23(3):283–337. doi: 10.3109/10409238809088226. [DOI] [PubMed] [Google Scholar]
  19. Mannervik B., Jensson H. Binary combinations of four protein subunits with different catalytic specificities explain the relationship between six basic glutathione S-transferases in rat liver cytosol. J Biol Chem. 1982 Sep 10;257(17):9909–9912. [PubMed] [Google Scholar]
  20. Mannervik B. The isoenzymes of glutathione transferase. Adv Enzymol Relat Areas Mol Biol. 1985;57:357–417. doi: 10.1002/9780470123034.ch5. [DOI] [PubMed] [Google Scholar]
  21. Piatigorsky J. Lens crystallins. Innovation associated with changes in gene regulation. J Biol Chem. 1992 Mar 5;267(7):4277–4280. [PubMed] [Google Scholar]
  22. Piatigorsky J., Wistow G. The recruitment of crystallins: new functions precede gene duplication. Science. 1991 May 24;252(5009):1078–1079. doi: 10.1126/science.252.5009.1078. [DOI] [PubMed] [Google Scholar]
  23. Pickett C. B., Lu A. Y. Glutathione S-transferases: gene structure, regulation, and biological function. Annu Rev Biochem. 1989;58:743–764. doi: 10.1146/annurev.bi.58.070189.003523. [DOI] [PubMed] [Google Scholar]
  24. Rushmore T. H., Pickett C. B. Glutathione S-transferases, structure, regulation, and therapeutic implications. J Biol Chem. 1993 Jun 5;268(16):11475–11478. [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Siezen R. J., Shaw D. C. Physicochemical characterization of lens proteins of the squid Nototodarus gouldi and comparison with vertebrate crystallins. Biochim Biophys Acta. 1982 Jun 4;704(2):304–320. doi: 10.1016/0167-4838(82)90160-1. [DOI] [PubMed] [Google Scholar]
  27. Sinning I., Kleywegt G. J., Cowan S. W., Reinemer P., Dirr H. W., Huber R., Gilliland G. L., Armstrong R. N., Ji X., Board P. G. Structure determination and refinement of human alpha class glutathione transferase A1-1, and a comparison with the Mu and Pi class enzymes. J Mol Biol. 1993 Jul 5;232(1):192–212. doi: 10.1006/jmbi.1993.1376. [DOI] [PubMed] [Google Scholar]
  28. Tomarev S. I., Zinovieva R. D., Piatigorsky J. Characterization of squid crystallin genes. Comparison with mammalian glutathione S-transferase genes. J Biol Chem. 1992 Apr 25;267(12):8604–8612. [PubMed] [Google Scholar]
  29. Tomarev S. I., Zinovieva R. D., Piatigorsky J. Crystallins of the octopus lens. Recruitment from detoxification enzymes. J Biol Chem. 1991 Dec 15;266(35):24226–24231. [PubMed] [Google Scholar]
  30. Tomarev S. I., Zinovieva R. D. Squid major lens polypeptides are homologous to glutathione S-transferases subunits. Nature. 1988 Nov 3;336(6194):86–88. doi: 10.1038/336086a0. [DOI] [PubMed] [Google Scholar]
  31. Tsuchida S., Sato K. Glutathione transferases and cancer. Crit Rev Biochem Mol Biol. 1992;27(4-5):337–384. doi: 10.3109/10409239209082566. [DOI] [PubMed] [Google Scholar]
  32. Waxman D. J. Glutathione S-transferases: role in alkylating agent resistance and possible target for modulation chemotherapy--a review. Cancer Res. 1990 Oct 15;50(20):6449–6454. [PubMed] [Google Scholar]
  33. Wilce M. C., Parker M. W. Structure and function of glutathione S-transferases. Biochim Biophys Acta. 1994 Mar 16;1205(1):1–18. doi: 10.1016/0167-4838(94)90086-8. [DOI] [PubMed] [Google Scholar]
  34. Wistow G. J., Mulders J. W., de Jong W. W. The enzyme lactate dehydrogenase as a structural protein in avian and crocodilian lenses. Nature. 1987 Apr 9;326(6113):622–624. doi: 10.1038/326622a0. [DOI] [PubMed] [Google Scholar]
  35. Wistow G. J., Piatigorsky J. Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem. 1988;57:479–504. doi: 10.1146/annurev.bi.57.070188.002403. [DOI] [PubMed] [Google Scholar]
  36. Zinovieva R. D., Tomarev S. I., Piatigorsky J. Aldehyde dehydrogenase-derived omega-crystallins of squid and octopus. Specialization for lens expression. J Biol Chem. 1993 May 25;268(15):11449–11455. [PubMed] [Google Scholar]

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