Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1992 Nov 1;287(Pt 3):957–963. doi: 10.1042/bj2870957

An evolutionary perspective on glutathione transferases inferred from class-theta glutathione transferase cDNA sequences.

S E Pemble 1, J B Taylor 1
PMCID: PMC1133100  PMID: 1445253

Abstract

We report the cDNA sequence for rat glutathione transferase (GST) subunit 5, which is one of at least three class Theta subunits in this species. This sequence, when compared with that of subunit 12 recently published by Ogura, Nishiyama, Okada, Kajita, Narihata, Watabe, Hiratsuka & Watabe [(1991) Biochem. Biophys. Res. Commun. 181, 1294-1300] proves that Theta is a separate multigene class of GST with little amino acid sequence identity with Mu-, Alpha- or Pi-class enzymes. The amino acid sequence identity of class-Theta subunits is highly conserved in rat, the fruitfly Drosophila, maize (Zea mays) and Methylobacterium, which suggests that this family is representative of the ancient progenitor GST gene and originates from the endosymbioses of a purple bacterium leading to the mitochondrion. The high conservation of class Theta brings into prominence that Alpha-, Mu- and Pi-class enzymes, which are not present in plants, derive from a Theta-class gene duplication before the divergence of fungi and animals and, given the binding properties of the Alpha-, Mu- and Pi-classes, suggests a role for these in the evolution of fungi and animals.

Full text

PDF
961

Images in this article

Selected References

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

  1. Aceto A., Di Ilio C., Bucciarelli T., Pantani C., Dell'Agata M., Pannunzio G., Federici G. Characterization of glutathione transferase from Gammarus italicus. Comp Biochem Physiol B. 1991;99(3):523–527. doi: 10.1016/0305-0491(91)90332-8. [DOI] [PubMed] [Google Scholar]
  2. Brophy P. M., Barrett J. Strategies for detoxification of aldehydic products of lipid peroxidation in helminths. Mol Biochem Parasitol. 1990 Sep-Oct;42(2):205–211. doi: 10.1016/0166-6851(90)90163-g. [DOI] [PubMed] [Google Scholar]
  3. Buetler T. M., Eaton D. L. Complementary DNA cloning, messenger RNA expression, and induction of alpha-class glutathione S-transferases in mouse tissues. Cancer Res. 1992 Jan 15;52(2):314–318. [PubMed] [Google Scholar]
  4. Casey J., Shalloe F., Sheehan D. Subunit structure of fungal glutathione-S-transferases. Biochem Soc Trans. 1991 Feb;19(1):17S–17S. doi: 10.1042/bst019017s. [DOI] [PubMed] [Google Scholar]
  5. Chang L. H., Chuang L. F., Tsai C. P., Tu C. P., Tam M. F. Characterization of glutathione S-transferases from day-old chick livers. Biochemistry. 1990 Jan 23;29(3):744–750. doi: 10.1021/bi00455a022. [DOI] [PubMed] [Google Scholar]
  6. Coschigano P. W., Magasanik B. The URE2 gene product of Saccharomyces cerevisiae plays an important role in the cellular response to the nitrogen source and has homology to glutathione s-transferases. Mol Cell Biol. 1991 Feb;11(2):822–832. doi: 10.1128/mcb.11.2.822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Di Ilio C., Aceto A., Piccolomini R., Allocati N., Caccuri A. M., Barra D., Federici G. N-terminal region of Proteus mirabilis glutathione transferase is not homologous to mammalian and plant glutathione transferases. FEBS Lett. 1989 Jun 19;250(1):57–59. doi: 10.1016/0014-5793(89)80684-2. [DOI] [PubMed] [Google Scholar]
  8. Dominey R. J., Nimmo I. A., Cronshaw A. D., Hayes J. D. The major glutathione S-transferase in salmonid fish livers is homologous to the mammalian pi-class GST. Comp Biochem Physiol B. 1991;100(1):93–98. doi: 10.1016/0305-0491(91)90090-z. [DOI] [PubMed] [Google Scholar]
  9. Doolittle R. F. Lens proteins. More molecular opportunism. Nature. 1988 Nov 3;336(6194):18–18. doi: 10.1038/336018a0. [DOI] [PubMed] [Google Scholar]
  10. Fahey R. C., Sundquist A. R. Evolution of glutathione metabolism. Adv Enzymol Relat Areas Mol Biol. 1991;64:1–53. doi: 10.1002/9780470123102.ch1. [DOI] [PubMed] [Google Scholar]
  11. Grove G., Zarlengo R. P., Timmerman K. P., Li N. Q., Tam M. F., Tu C. P. Characterization and heterospecific expression of cDNA clones of genes in the maize GSH S-transferase multigene family. Nucleic Acids Res. 1988 Jan 25;16(2):425–438. doi: 10.1093/nar/16.2.425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Habig W. H., Pabst M. J., Fleischner G., Gatmaitan Z., Arias I. M., Jakoby W. B. The identity of glutathione S-transferase B with ligandin, a major binding protein of liver. Proc Natl Acad Sci U S A. 1974 Oct;71(10):3879–3882. doi: 10.1073/pnas.71.10.3879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harris J. M., Meyer D. J., Coles B., Ketterer B. A novel glutathione transferase (13-13) isolated from the matrix of rat liver mitochondria having structural similarity to class theta enzymes. Biochem J. 1991 Aug 15;278(Pt 1):137–141. doi: 10.1042/bj2780137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harris J., Coles B., Meyer D. J., Ketterer B. The isolation and characterization of the major glutathione S-transferase from the squid Loligo vulgaris. Comp Biochem Physiol B. 1991;98(4):511–515. doi: 10.1016/0305-0491(91)90245-9. [DOI] [PubMed] [Google Scholar]
  15. Hiratsuka A., Sebata N., Kawashima K., Okuda H., Ogura K., Watabe T., Satoh K., Hatayama I., Tsuchida S., Ishikawa T. A new class of rat glutathione S-transferase Yrs-Yrs inactivating reactive sulfate esters as metabolites of carcinogenic arylmethanols. J Biol Chem. 1990 Jul 15;265(20):11973–11981. [PubMed] [Google Scholar]
  16. Howie A. F., Hayes P. C., Bouchier I. A., Hayes J. D., Beckett G. J. Glutathione S-transferase in human bile. Clin Chim Acta. 1989 Oct 16;184(3):269–278. doi: 10.1016/0009-8981(89)90060-0. [DOI] [PubMed] [Google Scholar]
  17. Igarashi T., Kohara A., Shikata Y., Sagami F., Sonoda J., Horie T., Satoh T. The unique feature of dog liver cytosolic glutathione S-transferases. An isozyme not retained on the affinity column has the highest activity toward 1,2-dichloro-4-nitrobenzene. J Biol Chem. 1991 Nov 15;266(32):21709–21717. [PubMed] [Google Scholar]
  18. La Roche S. D., Leisinger T. Identification of dcmR, the regulatory gene governing expression of dichloromethane dehalogenase in Methylobacterium sp. strain DM4. J Bacteriol. 1991 Nov;173(21):6714–6721. doi: 10.1128/jb.173.21.6714-6721.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. La Roche S. D., Leisinger T. Sequence analysis and expression of the bacterial dichloromethane dehalogenase structural gene, a member of the glutathione S-transferase supergene family. J Bacteriol. 1990 Jan;172(1):164–171. doi: 10.1128/jb.172.1.164-171.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lanar D. E., Pearce E. J., James S. L., Sher A. Identification of paramyosin as schistosome antigen recognized by intradermally vaccinated mice. Science. 1986 Oct 31;234(4776):593–596. doi: 10.1126/science.3094144. [DOI] [PubMed] [Google Scholar]
  21. Listowsky I., Abramovitz M., Homma H., Niitsu Y. Intracellular binding and transport of hormones and xenobiotics by glutathione-S-transferases. Drug Metab Rev. 1988;19(3-4):305–318. doi: 10.3109/03602538808994138. [DOI] [PubMed] [Google Scholar]
  22. Litwack G., Ketterer B., Arias I. M. Ligandin: a hepatic protein which binds steroids, bilirubin, carcinogens and a number of exogenous organic anions. Nature. 1971 Dec 24;234(5330):466–467. doi: 10.1038/234466a0. [DOI] [PubMed] [Google Scholar]
  23. Liu L. F., Tam M. F. Nucleotide sequence of a class mu glutathione S-transferase from chicken liver. Biochim Biophys Acta. 1991 Nov 11;1090(3):343–344. doi: 10.1016/0167-4781(91)90199-v. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Meyer D. J., Coles B., Pemble S. E., Gilmore K. S., Fraser G. M., Ketterer B. Theta, a new class of glutathione transferases purified from rat and man. Biochem J. 1991 Mar 1;274(Pt 2):409–414. doi: 10.1042/bj2740409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moore R. E., Davies M. S., O'Connell K. M., Harding E. I., Wiegand R. C., Tiemeier D. C. Cloning and expression of a cDNA encoding a maize glutathione-S-transferase in E. coli. Nucleic Acids Res. 1986 Sep 25;14(18):7227–7235. doi: 10.1093/nar/14.18.7227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nebert D. W., Gonzalez F. J. P450 genes: structure, evolution, and regulation. Annu Rev Biochem. 1987;56:945–993. doi: 10.1146/annurev.bi.56.070187.004501. [DOI] [PubMed] [Google Scholar]
  28. Norris J. S., Schwartz D. A., MacLeod S. L., Fan W. M., O'Brien T. J., Harris S. E., Trifiletti R., Cornett L. E., Cooper T. M., Levi W. M. Cloning of a mu-class glutathione S-transferase complementary DNA and characterization of its glucocorticoid inducibility in a smooth muscle tumor cell line. Mol Endocrinol. 1991 Jul;5(7):979–986. doi: 10.1210/mend-5-7-979. [DOI] [PubMed] [Google Scholar]
  29. Ogura K., Nishiyama T., Okada T., Kajital J., Narihata H., Watabe T., Hiratsuka A., Watabe T. Molecular cloning and amino acid sequencing of rat liver class theta glutathione S-transferase Yrs-Yrs inactivating reactive sulfate esters of carcinogenic arylmethanols. Biochem Biophys Res Commun. 1991 Dec 31;181(3):1294–1300. doi: 10.1016/0006-291x(91)92079-y. [DOI] [PubMed] [Google Scholar]
  30. Pemble S. E., Taylor J. B., Ketterer B. Tissue distribution of rat glutathione transferase subunit 7, a hepatoma marker. Biochem J. 1986 Dec 15;240(3):885–889. doi: 10.1042/bj2400885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Reinemer P., Dirr H. W., Ladenstein R., Schäffer J., Gallay O., Huber R. The three-dimensional structure of class pi glutathione S-transferase in complex with glutathione sulfonate at 2.3 A resolution. EMBO J. 1991 Aug;10(8):1997–2005. doi: 10.1002/j.1460-2075.1991.tb07729.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sato K. Glutathione transferases as markers of preneoplasia and neoplasia. Adv Cancer Res. 1989;52:205–255. doi: 10.1016/s0065-230x(08)60214-6. [DOI] [PubMed] [Google Scholar]
  33. Smith D. B., Davern K. M., Board P. G., Tiu W. U., Garcia E. G., Mitchell G. F. Mr 26,000 antigen of Schistosoma japonicum recognized by resistant WEHI 129/J mice is a parasite glutathione S-transferase. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8703–8707. doi: 10.1073/pnas.83.22.8703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stenersen J., Kobro S., Bjerke M., Arend U. Glutathione transferases in aquatic and terrestrial animals from nine phyla. Comp Biochem Physiol C. 1987;86(1):73–82. doi: 10.1016/0742-8413(87)90147-2. [DOI] [PubMed] [Google Scholar]
  35. Takahashi Y., Nagata T. parB: an auxin-regulated gene encoding glutathione S-transferase. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):56–59. doi: 10.1073/pnas.89.1.56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tamaki H., Kumagai H., Tochikura T. Nucleotide sequence of the yeast glutathione S-transferase cDNA. Biochim Biophys Acta. 1991 Jun 13;1089(2):276–279. doi: 10.1016/0167-4781(91)90025-h. [DOI] [PubMed] [Google Scholar]
  37. Taylor J. B., Pemble S. E., Cowell I. G., Dixon K. H., Ketterer B. Molecular biology of glutathione transferases. Biochem Soc Trans. 1987 Aug;15(4):578–581. doi: 10.1042/bst0150578. [DOI] [PubMed] [Google Scholar]
  38. Taylor J. B., Vidal A., Torpier G., Meyer D. J., Roitsch C., Balloul J. M., Southan C., Sondermeyer P., Pemble S., Lecocq J. P. The glutathione transferase activity and tissue distribution of a cloned Mr28K protective antigen of Schistosoma mansoni. EMBO J. 1988 Feb;7(2):465–472. doi: 10.1002/j.1460-2075.1988.tb02834.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tipping E., Ketterer B. The influence of soluble binding proteins on lipophile transport and metabolism in hepatocytes. Biochem J. 1981 May 1;195(2):441–452. doi: 10.1042/bj1950441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Toung Y. P., Hsieh T. S., Tu C. P. Drosophila glutathione S-transferase 1-1 shares a region of sequence homology with the maize glutathione S-transferase III. Proc Natl Acad Sci U S A. 1990 Jan;87(1):31–35. doi: 10.1073/pnas.87.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Vorachek W. R., Pearson W. R., Rule G. S. Cloning, expression, and characterization of a class-mu glutathione transferase from human muscle, the product of the GST4 locus. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4443–4447. doi: 10.1073/pnas.88.10.4443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Weston K., Yochem J., Greenwald I. A Caenorhabditis elegans cDNA that encodes a product resembling the rat glutathione S-transferase P subunit. Nucleic Acids Res. 1989 Mar 11;17(5):2138–2138. doi: 10.1093/nar/17.5.2138. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES