Skip to main content
SpringerLink
Log in

Molecular characterization of glyoxalase II from Arabidopsis thaliana

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Glyoxalase II is part of the glutathione-dependent glyoxalase detoxification system. In addition to its role in the detoxification of cytotoxic 2-oxo-aldehydes, specifically methylglyoxal, it has been suggested that the glyoxalase system may also play a role in controlling cell differentiation and proliferation. During the analysis of a T-DNA-tagged mutant of Arabidopsis we identified the gene for a glyoxalase II isozyme (GLY1) that appears to be mitochondrially localized. The cDNA encoding a glyoxalase II cytoplasmic isozyme (GLY2) was also isolated and characterized. Southern blot and sequence analyses indicate that glyoxalase II proteins are encoded by at least two multigene families in Arabidopsis. Escherichia coli cells expressing either GLY1 or GLY2 exhibit increased glyoxalase II activity, confirming that they do, in fact, encode glyoxalase II proteins. Northern analysis shows that the two genes are differentially expressed. Transcripts for the mitochondrial isozyme are most abundant in roots, while those for the cytoplasmic isozyme are highest in flower buds. The identification of glyoxalase II isozymes that are differentially expressed suggests that they may play different roles in the cell.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Allen R, Lo T, Thornalley PJ: Inhibitors of glyoxalase I: design, synthesis, inhibitory characteristics and biological evaluation. Biochem Soc Trans 21: 535-540 (1993).

    PubMed  Google Scholar 

  2. Allen R, Lo T, Thornalley P: Purification and characterization of glyoxalase II from human red blood cells. Eur J Biochem 213: 1261-1267 (1993).

    PubMed  Google Scholar 

  3. Ball J, Vander Jagt D: S-2-hydroxyacylgluthathione hydrolase (glyoxalase II): active sitemapping of a nonserine thiolesterase. Biochemistry 20: 899-905 (1981).

    PubMed  Google Scholar 

  4. Concha N, Rasmussen B, Bush K, Herzberg O: Crystal structure of the wide-spectrum binuclear zinc B-lactamase from Bacteroides fragilis. Structure 4: 823-836 (1996).

    PubMed  Google Scholar 

  5. Deswal R, Chakaravarty T, Sopory S: The glyoxalase system of higher plants: regulation in growth and differientation. Biochem Soc Trans 21: 527-530 (1993).

    PubMed  Google Scholar 

  6. Doyle J, Doyle J: Isolation of plant DNA from fresh tissue. BRL Focus 12: 13-15 (1990).

    Google Scholar 

  7. Espartero J, Sanchez-Aguayo I, Pardo J: Molecular characterization of glyoxalase-I from a higher plant; upregulation by stress. Plant Mol Biol 29: 1223-1233 (1995).

    PubMed  Google Scholar 

  8. Feldmann KA: T-DNA Insertion Mutagenesis in Arabidopsis: Mutational Spectrum. Plant J 1: 71-82 (1991).

    Google Scholar 

  9. Henikoff S: Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351-359 (1984).

    PubMed  Google Scholar 

  10. Laemmli EK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685 (1970).

    PubMed  Google Scholar 

  11. Lo T, Westwood M, McLellan A, Selwood T, Thornalley P: Binding and modification of proteins by methylglyoxal under physiological conditions: a kinetic and mechanistic study with N-acetylarginine, N-acetylcysteine, and N-acetyl-lysine and bovine serum albumin. J Biol Chem 269: 32299-32305 (1994).

    PubMed  Google Scholar 

  12. Lyles G, Chalmers J: The metabolism of aminoacetone to methylglyoxal by semicarbazide-sensitive amino oxidase in human umbilical artery. Biochem Pharmacol 43: 1409-1414 (1992).

    PubMed  Google Scholar 

  13. Makaroff CA, Palmer JD: Extensive mitochondrial specific transcription of the Brassica campestris mitochondrial genome. Nucl Acids Res 15: 5141-5156 (1987).

    PubMed  Google Scholar 

  14. Nakai K, Kanehisa M: Aknowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14: 897-911 (1992).

    PubMed  Google Scholar 

  15. Norton S, Elia A, Chyan M, Gillis G, Frenzel C, Principato G: Inhibitors and inhibition studies of mammalian glyoxalase II activity. Biochem Soc Trans 21: 545-549 (1990).

    Google Scholar 

  16. Nortron SJ, Talesa V, Yuan W-J, Principato GB: Glyoxalase I and glyoxalase II from Aloe vera: purification, characterization and comparison with animal glyoxalases. Biochem Int 22: 411-418 (1990).

    PubMed  Google Scholar 

  17. Novagen: pET System Manual. Novagen, Madison WI (1995).

    Google Scholar 

  18. Papoulis A, Al-Abed Y, Bucala R: Identification of N2-(1-carboxyethyl)guanine (CEG) as a guanine advanced glycosylation endproduct. Biochemistry 34: 648-655 (1995).

    PubMed  Google Scholar 

  19. Paulus C, Knollner B, Jacobsen H: Physiological and biochemical characterization of glyoxalase I, a general marker for cell proliferation, from a soybean cell suspension. Planta 189: 561-566 (1993).

    PubMed  Google Scholar 

  20. Peirson BN, Owen HA, Feldmann KA, Makaroff CA: Characterization of three male-sterile mutants of Arabidopsis thaliana exhibiting alterations in meiosis. Sex Plant Reprod 9: 1-16 (1996).

    Google Scholar 

  21. Phillips S, Thornalley P: The formation of methyl glyoxal from triose phosphates. Investigation using a specific assay for methyl glyoxal. Eur J Biochem 212: 101-105 (1993).

    PubMed  Google Scholar 

  22. Pompliano D, Peyman A, Knowles J: Stabilization of a reaction intermediate as a catalytic device: definition of the functional role of the flexable loop in triosephosphate isomerase. Biochemistry 29: 3186-3194 (1990).

    PubMed  Google Scholar 

  23. Rahman A, Shahabuddin A, Hadi S: Formation of strand breaks and interstrand crosslinks in DNA by methylglyoxal. J Biochem Toxicol 5: 161-166 (1990).

    PubMed  Google Scholar 

  24. Ray S, Ray M: Isolation of methyl glyoxal synthase from goat liver. J Biol Chem 256: 6230-6234 (1981).

    PubMed  Google Scholar 

  25. Ridderstrom M, Saccucci F, Hellman U, Bergman T, Principato G, Mannervik B: Molecular cloning, heterologous expression, and characterization of human glyoxalase II. J Biol Chem 271: 319-323 (1996).

    PubMed  Google Scholar 

  26. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  27. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chainterminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467 (1977).

    PubMed  Google Scholar 

  28. Sieburth LE, Meyerowitz EM: Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9: 355-365 (1997).

    PubMed  Google Scholar 

  29. Studier F, Rosenberg A, Dunn J, Dubendorff J: Use of T7 RNA polymerase to direct expression of cloned genes. Meth Enzymol 185: 60-89 (1990).

    PubMed  Google Scholar 

  30. Sutton B, Artymiuk P, Cordero-Borboa A, Little C, Phillips D, Waley S: An X-ray-crystallographic study of β-lactamase II from Bacillus cereus at 0.35 nm resolution. Biochem J 248: 181-188 (1987).

    PubMed  Google Scholar 

  31. Talesa V, Rosi G, Contenti S, Mangiabene C, Lupattelli M, Norton SJ, Giovannini E, Principato GB: Presence of glyoxalase II in mitochondria from spinach leaves: comparison with the enzyme from cytosol. Biochem Int 22: 1115-1120 (1990).

    PubMed  Google Scholar 

  32. Talesa V, Uotila L, Koivusalo M, Principato GB, Giovannini E, Rosi G: Isolation of glyoxalase II from two different compartments of rat liver mitochondria. Kinetic and immunochemical characterization of the enzymes. Biochim Biophys Acta 993: 7-11 (1989).

    PubMed  Google Scholar 

  33. Thornalley P: The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 269: 1-11 (1990).

    PubMed  Google Scholar 

  34. Thornalley P: The glyoxalase system in health and disease. Mol Asp Med 14: 287-371 (1993).

    Google Scholar 

  35. Thornalley PJ: Pharmacology of methylglyoxal: formation, modification of proteins and nucleic acids, and enzymatic detoxification: a role in pathogenesis and antiproliferative chemotherapy. Gen Pharmacol 27: 565-573 (1996).

    PubMed  Google Scholar 

  36. Uotila L: Purification and characterization of S-2-hydroxyacylglutathione hydrolase (glyoxalase II) from human liver. Biochemistry 12: 3944-3951 (1973).

    PubMed  Google Scholar 

  37. Vallee B, Auld D: Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29: 5647-5659 (1990).

    PubMed  Google Scholar 

  38. Vander Jagt DL: Glyoxalase II: Molecular characteristics, kinetics and mechanism Trans Biochem Soc Gr Brit 21: 522-527 (1993).

    Google Scholar 

  39. Verwoerd T, Dekker B, Hoekema A: A small-scale procedure for the rapid isolation of plant RNAs. Nucl Acids Res 17: 2362 (1989).

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Subbiah Krishnasamy

    Present address: Department of Biology, Loyola University, Maywood, IL, 60153, USA

  2. Heather A. Owen

    Present address: Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, 53211, USA

Authors and Affiliations

  1. Department of Chemistry, Miami University, Hughes Hall, Oxford, OH, 45056, USA

    Mrinal K. Maiti & Christopher A. Makaroff*

Authors
  1. Mrinal K. Maiti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Subbiah Krishnasamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heather A. Owen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher A. Makaroff*
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maiti, M.K., Krishnasamy, S., Owen, H.A. et al. Molecular characterization of glyoxalase II from Arabidopsis thaliana. Plant Mol Biol 35, 471–481 (1997). https://doi.org/10.1023/A:1005891123344

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005891123344

Search

Navigation