DOI QR코드

DOI QR Code

Cloning and Characterization of a Glyoxalase I Gene from the Osmotolerant Yeast Candida magnoliae

  • Park, Eun-Hee (School of Biotechnology and Bioengineering, Kangwon National University) ;
  • Lee, Dae-Hee (Industrial Biotechnology and Bioenergy Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Seo, Jin-Ho (Industrial Biotechnology and Bioenergy Research Center, Korea Research Institute of Bioscience and Biotechnology) ;
  • Kim, Myoung-Dong (Department of Agricultural Biotechnology, Seoul National University)
  • Received : 2010.08.23
  • Accepted : 2010.12.13
  • Published : 2011.03.28

Abstract

Glyoxalase I catalyzes the conversion of methylglyoxal to S-D-lactoylglutathione in the presence of glutathione. The structural gene of glyoxalase I (GLO1) was cloned from an osmotolerant yeast, Candida magnoliae, which produces a functional sweetener, erythritol, from sucrose. DNA sequence analysis revealed that the uninterrupted open reading frame (ORF) of C. magnoliae GLO1 (CmGLO1) spans 945 bp, corresponding to 315 amino acid residues, and shares 45.2% amino acid sequence identity to Saccharomyces cerevisiae Glo1. The cloned ORF in a multicopy constitutive expression plasmid complemented the glo1 mutation of S. cerevisiae, confirming that it encodes Glo1 in C. magnoliae. The responses of CmGLO1 to environmental stresses were different from those of S. cerevisiae, which only responds to osmotic stress. An enzyme activity assay and reverse transcription polymerase chain reaction revealed that the expression of CmGLO1 is induced by stress inducers such as methylglyoxal, $H_2O_2$, KCl, and NaCl. The GenBank Accession No. for CmGLO1 is HM000001.

Keywords

References

  1. Ahmed, N., U. Ahmed, P. J. Thornalley, K. Hager, G. Fleischer, and G. Munch. 2005. Protein glycation, oxidation and nitration adduct residues and free adducts of cerebrospinal fluid in Alzheimer's disease and link to cognitive impairment. J. Neurochem. 92: 255-263. https://doi.org/10.1111/j.1471-4159.2004.02864.x
  2. Albertyn, J., S. Hohmann, J. M. Thevelein, and B. A. Prior. 1994. GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol. Cell Biol. 14: 4135-4144. https://doi.org/10.1128/MCB.14.6.4135
  3. Ayoub, F., M. Zaman, P. Thornalley, and J. Masters. 1993. Glyoxalase activities in human tumour cell lines in vitro. Anticancer Res. 13: 151-155.
  4. Blomberg, A. and L. Adler. 1989. Roles of glycerol and glycerol-3-phosphate dehydrogenase ($NAD^{+}$) in acquired osmotolerance of Saccharomyces cerevisiae. J. Bacteriol. 171: 1087-1092. https://doi.org/10.1128/jb.171.2.1087-1092.1989
  5. Burg, M. B., E. D. Kwon, and D. Kultz. 1996. Osmotic regulation of gene expression. FASEB J. 10: 1598-1606. https://doi.org/10.1096/fasebj.10.14.9002551
  6. Chenna, R., H. Sugawara, T. Koike, R. Lopez, T. J. Gibson, D. G. Higgins, and J. D. Thompson. 2003. Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res. 31: 3497-3500. https://doi.org/10.1093/nar/gkg500
  7. Clugston, S. L., E. Daub, R. Kinach, D. Miedema, J. F. Barnard, and J. F. Honek. 1997. Isolation and sequencing of a gene coding for glyoxalase I activity from Salmonella typhimurium and comparison with other glyoxalase I sequences. Gene 186: 103-111. https://doi.org/10.1016/S0378-1119(96)00691-9
  8. Du, J., H. Suzuki, F. Nagase, A. A. Akhand, T. Yokoyama, T. Miyata, K. Kurokawa, and I. Nakashima. 2000. Methylglyoxal induces apoptosis in Jurkat leukemia T cells by activating c-Jun N-terminal kinase. J. Cell Biochem. 77: 333-344. https://doi.org/10.1002/(SICI)1097-4644(20000501)77:2<333::AID-JCB15>3.0.CO;2-Q
  9. Felsenstein, J. 2001. Taking variation of evolutionary rates between sites into account in inferring phylogenies. J. Mol. Evol. 53: 447-455. https://doi.org/10.1007/s002390010234
  10. Ferguson, G. P., A. D. Chacko, C. H. Lee, and I. R. Booth. 1996. The activity of the high-affinity $K^{+}$ uptake system Kdp sensitizes cells of Escherichia coli to methylglyoxal. J. Bacteriol. 178: 3957-3961. https://doi.org/10.1128/jb.178.13.3957-3961.1996
  11. Gietz, R. D. and R. A. Woods. 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350: 87-96.
  12. Hohmann, S. 2002. Osmotic adaptation in yeast - control of the yeast osmolyte system. Int. Rev. Cytol. 215: 149-187.
  13. Hohmann, S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol. Rev. 66: 300-372. https://doi.org/10.1128/MMBR.66.2.300-372.2002
  14. Hohmann, S., M. Krantz, and B. Nordlander. 2007. Yeast osmoregulation. Methods Enzymol. 428: 29-45.
  15. Inoue, Y. and A. Kimura. 1995. Methylglyoxal and regulation of its metabolism in microorganisms. Adv. Microb. Physiol. 37: 177-227.
  16. Inoue, Y. and A. Kimura. 1996. Identification of the structural gene for glyoxalase I from Saccharomyces cerevisiae. J. Biol. Chem. 271: 25958-25965. https://doi.org/10.1074/jbc.271.42.25958
  17. Inoue, Y., Y. Tsujimoto, and A. Kimura. 1998. Expression of the glyoxalase I gene of Saccharomyces cerevisiae is regulated by high osmolarity glycerol mitogen-activated protein kinase pathway in osmotic stress response. J. Biol. Chem. 273: 2977-2983. https://doi.org/10.1074/jbc.273.5.2977
  18. Junaid, M. A., D. Kowal, M. Barua, P. S. Pullarkat, S. Sklower Brooks, and R. K. Pullarkat. 2004. Proteomic studies identified a single nucleotide polymorphism in glyoxalase I as autism susceptibility factor. Am. J. Med. Genet. A 131: 11-17.
  19. Kalapos, M. P. 1999. Methylglyoxal in living organisms: Chemistry, biochemistry, toxicology and biological implications. Toxicol. Lett. 110: 145-175. https://doi.org/10.1016/S0378-4274(99)00160-5
  20. Kang, Y., L. G. Edwards, and P. J. Thornalley. 1996. Effect of methylglyoxal on human leukaemia 60 cell growth: Modification of DNA G1 growth arrest and induction of apoptosis. Leuk. Res. 20: 397-405. https://doi.org/10.1016/0145-2126(95)00162-X
  21. Kim, N. S., Y. Umezawa, S. Ohmura, and S. Kato. 1993. Human glyoxalase I. cDNA cloning, expression, and sequence similarity to glyoxalase I from Pseudomonas putida. J. Biol. Chem. 268: 11217-11221.
  22. Kim, S. Y., Y. J. Jeon, and J. H. Seo. 1996. Analysis of fermentation characteristics for production of erythritol by Candida sp. Kor. J. Food Sci. Technol. 28: 935-939.
  23. Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5: 150-163. https://doi.org/10.1093/bib/5.2.150
  24. Lee, D. H., M. D. Kim, Y. W. Ryu, and J. H. Seo. 2008. Cloning and characterization of CmGPD1, the Candida magnoliae homologue of glycerol-3-phosphate dehydrogenase. FEMS Yeast Res. 8: 1324-1333. https://doi.org/10.1111/j.1567-1364.2008.00446.x
  25. Lu, T., D. J. Creighton, M. Antoine, C. Fenselau, and P. S. Lovett. 1994. The gene encoding glyoxalase I from Pseudomonas putida: Cloning, overexpression, and sequence comparisons with human glyoxalase I. Gene 150: 93-96. https://doi.org/10.1016/0378-1119(94)90864-8
  26. Maeta, K., K. Mori, Y. Takatsume, S. Izawa, and Y. Inoue. 2005. Diagnosis of cell death induced by methylglyoxal, a metabolite derived from glycolysis, in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 243: 87-92. https://doi.org/10.1016/j.femsle.2004.11.046
  27. Norbeck, J., A. K. Pahlman, N. Akhtar, A. Blomberg, and L. Adler. 1996. Purification and characterization of two isoenzymes of DL-glycerol-3-phosphatase from Saccharomyces cerevisiae. Identification of the corresponding GPP1 and GPP2 genes and evidence for osmotic regulation of Gpp2p expression by the osmosensing mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 271: 13875-13881. https://doi.org/10.1074/jbc.271.23.13875
  28. Ranganathan, S., E. S. Walsh, A. K. Godwin, and K. D. Tew. 1993. Cloning and characterization of human colon glyoxalase-I. J. Biol. Chem. 268: 5661-5667.
  29. Ratliff, D. M., D. J. Vander Jagt, R. P. Eaton, and D. L. Vander Jagt. 1996. Increased levels of methylglyoxal-metabolizing enzymes in mononuclear and polymorphonuclear cells from insulindependent diabetic patients with diabetic complications: Aldose reductase, glyoxalase I, and glyoxalase II-a clinical research center study. J. Clin. Endocrinol. Metab. 81: 488-492. https://doi.org/10.1210/jc.81.2.488
  30. Saito, H. and K. Tatebayashi. 2004. Regulation of the osmoregulatory HOG MAPK cascade in yeast. J. Biochem. 136: 267-272. https://doi.org/10.1093/jb/mvh135
  31. Sambrook, J. and D. W. Russell. 2001. Molecular Cloning, pp. 1.119-1.122, 3rd Ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  32. Schuller, C., J. L. Brewster, M. R. Alexander, M. C. Gustin, and H. Ruis. 1994. The HOG pathway controls osmotic regulation of transcription via the stress response element (STRE) of the Saccharomyces cerevisiae CTT1 gene. EMBO J. 13: 4382-4389.
  33. Takatsume, Y., S. Izawa, and Y. Inoue. 2004. Identification of thermostable glyoxalase I in the fission yeast Schizosaccharomyces pombe. Arch. Microbiol. 181: 371-377. https://doi.org/10.1007/s00203-004-0666-4
  34. Takatsume, Y., S. Izawa, and Y. Inoue. 2005. Unique regulation of glyoxalase I activity during osmotic stress response in the fission yeast Schizosaccharomyces pombe: Neither the mRNA nor the protein level of glyoxalase I increase under conditions that enhance its activity. Arch. Microbiol. 183: 224-227. https://doi.org/10.1007/s00203-005-0762-0
  35. Thornalley, P. J. 1990. The glyoxalase system: New developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem. J. 269: 1-11. https://doi.org/10.1042/bj2690001
  36. Thornalley, P. J. 1993. The glyoxalase system in health and disease. Mol. Aspects Med. 14: 287-371. https://doi.org/10.1016/0098-2997(93)90002-U
  37. Yu, J. H., D. H. Lee, Y. J. Oh, K. C. Han, Y. W. Ryu, and J. H. Seo. 2006. Selective utilization of fructose to glucose by Candida magnoliae, an erythritol producer. Appl. Biochem. Biotechnol. 131: 870-879. https://doi.org/10.1385/ABAB:131:1:870

Cited by

  1. Cloning of Orotidine-5'-phosphate Decarboxylase (URA3) Gene from Sourdough Yeast Candida milleri CBS 8195 vol.21, pp.5, 2012, https://doi.org/10.1007/s10068-012-0164-4
  2. Cloning and Functional Verification of the Candida milleri HIS3 Gene Encoding Imidazoleglycerol Phosphate Dehydratase vol.22, pp.10, 2012, https://doi.org/10.4014/jmb.1207.07064
  3. Cloning of the Transketolase Gene from Erythritol-Producing Yeast Candida magnoliae vol.24, pp.10, 2014, https://doi.org/10.4014/jmb.1407.07032
  4. Isolation of the Inositol Phosphoceramide Synthase Gene (AUR1) from Stress-Tolerant Yeast Pichia kudriavzevii vol.25, pp.11, 2011, https://doi.org/10.4014/jmb.1508.08019
  5. 김치에서 분리된 Lactobacillus buchneri의 젖산 생산 특성 vol.43, pp.3, 2015, https://doi.org/10.4014/mbl.1506.06006
  6. 막걸리로부터 분리된 Bacillus amyloliquefaciens 균주의 항균 활성 vol.44, pp.1, 2016, https://doi.org/10.4014/mbl.1511.11005