DOI QR코드

DOI QR Code

Inhibition of methionine sulfoxide reduction by dimethyl sulfoxide

  • Kwak, Geun-Hee (Department of Biochemistry and Molecular Biology, Aging-associated Vascular Disease Research Center, Yeungnam University College of Medicine) ;
  • Choi, Seung-Hee (Department of Biochemistry and Molecular Biology, Aging-associated Vascular Disease Research Center, Yeungnam University College of Medicine) ;
  • Kim, Jae-Ryong (Department of Biochemistry and Molecular Biology, Aging-associated Vascular Disease Research Center, Yeungnam University College of Medicine) ;
  • Kim, Hwa-Young (Department of Biochemistry and Molecular Biology, Aging-associated Vascular Disease Research Center, Yeungnam University College of Medicine)
  • Published : 2009.09.30

Abstract

Dimethyl sulfoxide (DMSO) is widely used in chemistry and biology as a solvent and as a cryoprotectant. It is also used as a pharmaceutical agent for the treatment of interstitial cystitis and rheumatoid arthritis. Previous reports described DMSO as being reduced by methionine-S-sulfoxide reductase (MsrA). However, little is known about the DMSO reduction capability of methionine-R-sulfoxide reductase (MsrB) or its effect on the catalysis of methionine sulfoxide reduction. We show that mammalian MsrB2 and MsrB3 were unable to reduce DMSO. This compound inhibited MsrB2 activity but did not inhibit MsrB3 activity. We further determined that DMSO functions as an inhibitor of MsrA and MsrB2 in the reduction of methionine sulfoxides via different inhibition mechanisms. DMSO competitively inhibited MsrA activity but acted as a non-competitive inhibitor of MsrB2 activity. Our study also demonstrated that DMSO inhibits in vivo methionine sulfoxide reduction in yeast and mammalian cells.

Keywords

References

  1. Weissbach, H., Resnick, L. and Brot, N. (2005) Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage. Biochim. Biophys. Acta 1703, 203-212 https://doi.org/10.1016/j.bbapap.2004.10.004
  2. Kim, H. Y. and Gladyshev, V. N. (2007) Methionine sulfoxide reductases: selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem. J. 407, 321-329 https://doi.org/10.1042/BJ20070929
  3. Kwak, G. H., Kim, J. R. and Kim, H. Y. (2009) Expression, subcellular localization, and antioxidant role of mammalian methionine sulfoxide reductases in Saccharomyces cerevisiae. BMB Rep. 42, 113-118
  4. Gabbita, S. P., Aksenov, M. Y., Lovell, M. A. and Markesbery, W. R. (1999) Decrease in peptide methionine sulfoxide reductase in Alzheimer's disease brain. J. Neurochem. 73, 1660-1666 https://doi.org/10.1046/j.1471-4159.1999.0731660.x
  5. Glaser, C. B., Yamin, G., Uversky, V. N. and Fink, A. L. (2005) Methionine oxidation, alpha-synuclein and Parkinson's disease. Biochim. Biophys. Acta. 1703, 157-169 https://doi.org/10.1016/j.bbapap.2004.10.008
  6. Moskovitz, J., Bar-Noy, S., Williams, W. M., Requena, J., Berlett, B. S. and Stadtman, E. R. (2001) Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc. Natl. Acad. Sci. U.S.A. 98, 12920-12925 https://doi.org/10.1073/pnas.231472998
  7. Ruan, H., Tang, X. D., Chen, M. L., Joiner, M. L., Sun, G., Brot, N., Weissbach, H., Heinemann, S. H., Iverson, L., Wu, C. F. and Hoshi, T. (2002) High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proc. Natl. Acad. Sci. U.S.A. 99, 2748-2753 https://doi.org/10.1073/pnas.032671199
  8. Schoneich, C. (2005) Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer's disease. Biochim. Biophys. Acta 1703, 111-119 https://doi.org/10.1016/j.bbapap.2004.09.009
  9. Hansen, J. (1999) Inactivation of MXR1 abolishes formation of dimethyl sulfide from dimethyl sulfoxide in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 65, 3915-3919
  10. Moskovitz, J., Weissbach, H. and Brot, N. (1996) Cloning and expression of a mammalian gene involved in the reduction of methionine sulfoxide residues in proteins. Proc. Natl. Acad. Sci. U.S.A. 93, 2095-2099 https://doi.org/10.1073/pnas.93.5.2095
  11. Lee, B. C., Le, D. T. and Gladyshev, V. N. (2008) Mammals reduce methionine-S-sulfoxide with MsrA and are unable to reduce methionine-R-sulfoxide, and this function can be restored with a yeast reductase. J. Biol. Chem. 283, 28361-28369 https://doi.org/10.1074/jbc.M805059200
  12. Lin, Z., Johnson, L. C., Weissbach, H., Brot, N., Lively, M. O. and Lowther, W. T. (2007) Free methionine-(R)-sulfoxide reductase from Escherichia coli reveals a new GAF domain function. Proc. Natl. Acad. Sci. U.S.A. 104, 9597-9602 https://doi.org/10.1073/pnas.0703774104
  13. Le, D. T., Lee, B. C., Marino, S. M., Zhang, Y., Fomenko, D. E., Kaya, A., Hacioglu, E., Kwak, G. H., Koc, A., Kim, H. Y. and Gladyshev, V. N. (2009) Functional analysis of free methionine-R-sulfoxide reductase from Saccharomyces cerevisiae. J. Biol. Chem. 284, 4354-4364 https://doi.org/10.1074/jbc.M805891200
  14. Kim, H. Y. and Gladyshev, V. N. (2004) Methionine sulfoxide reduction in mammals: characterization of methionine-R-sulfoxide reductases. Mol. Biol. Cell 15, 1055-1064 https://doi.org/10.1091/mbc.E03-08-0629
  15. Hansel, A., Heinemann, S. H. and Hoshi, T. (2005) Heterogeneity and function of mammalian MSRs: enzymes for repair, protection and regulation. Biochim. Biophys. Acta 1703, 239-247 https://doi.org/10.1016/j.bbapap.2004.09.010
  16. Santos, N. C., Figueira-Coelho, J., Martins-Silva, J. and Saldanha, C. (2003) Multidisciplinary utilization of dimethyl sulfoxide: pharmacological, cellular, and molecular aspects. Biochem. Pharmacol. 65, 1035-1041 https://doi.org/10.1016/S0006-2952(03)00002-9
  17. Schindelin, H., Kisker, C., Hilton, J., Rajagopalan, K. V. and Rees, D. C. (1996) Crystal structure of DMSO reductase: redox-linked changes in molybdopterin coordination. Science 272, 1615-1621 https://doi.org/10.1126/science.272.5268.1615
  18. Adams, B., Smith, A. T., Bailey, S., McEwan, A. G. and Bray, R. C. (1999) Reactions of dimethylsulfoxide reductase from Rhodobacter capsulatus with dimethyl sulfide and with dimethyl sulfoxide: complexities revealed by conventional and stopped-flow spectrophotometry. Biochemistry 38, 8501-8511 https://doi.org/10.1021/bi9902034
  19. Boschi-Muller, S., Azza, S., Sanglier-Cianferani, S., Talfournier, F., Van Dorsselear, A. and Branlant, G. (2000) A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J. Biol. Chem. 275, 35908-35913 https://doi.org/10.1074/jbc.M006137200
  20. Lowther, W. T., Weissbach, H., Etienne, F., Brot, N. and Matthews, B. W. (2002) The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat. Struct. Biol. 9, 348-352
  21. Murata, Y., Watanabe, T., Sato, M., Momose, Y., Nakahara, T., Oka, S. and Iwahashi, H. (2003) Dimethyl sulfoxide exposure facilitates phospholipid biosynthesis and cellular membrane proliferation in yeast cells. J. Biol. Chem. 278, 33185-33193 https://doi.org/10.1074/jbc.M300450200
  22. Wassef, R., Haenold, R., Hansel, A., Brot, N., Heinemann, S. H. and Hoshi, T. (2007) Methionine sulfoxide reductase A and a dietary supplement S-methyl-L-cysteine prevent Parkinson's-like symptoms. J. Neurosci. 27, 12808-12816 https://doi.org/10.1523/JNEUROSCI.0322-07.2007
  23. Liu, S. X., Athar, M., Lippai, I., Waldren, C. and Hei, T. K. (2001) Induction of oxyradicals by arsenic: implication for mechanism of genotoxicity. Proc. Natl. Acad. Sci. U. S. A. 98, 1643-1648 https://doi.org/10.1073/pnas.031482998
  24. Perez-Pasten, R., Martinez-Galero, E., Garduno-Siciliano, L., Lara, I. C. and Cevallos, G. C. (2006) Effects of dimethylsulphoxide on mice arsenite-induced dysmorphogenesis in embryo culture and cytotoxicity in embryo cells. Toxicol. Lett. 161, 167-173 https://doi.org/10.1016/j.toxlet.2005.09.001
  25. Cao, X. G., Li, X. X., Bao, Y. Z., Xing, N. Z. and Chen, Y. (2007) Responses of human lens epithelial cells to quercetin and DMSO. Invest. Ophthalmol. Vis. Sci. 48, 3714-3718 https://doi.org/10.1167/iovs.06-1304
  26. Kim, H. Y. and Gladyshev, V. N. (2005) Role of structural and functional elements of mouse methionine-S-sulfoxide reductase in its subcellular distribution. Biochemistry 44, 8059-8067 https://doi.org/10.1021/bi0501131
  27. Koc, A., Gasch, A. P., Rutherford, J. C., Kim, H. Y. and Gladyshev, V. N. (2004) Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species- dependent and -independent components of aging. Proc. Natl. Acad. Sci. U. S. A. 101, 7999-8004 https://doi.org/10.1073/pnas.0307929101
  28. Kumar, R. A., Koc, A., Cerny, R. L. and Gladyshev, V. N. (2002) Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J. Biol. Chem. 277, 37527-37535 https://doi.org/10.1074/jbc.M203496200

Cited by

  1. Determination of protein-bound methionine oxidationin the hippocampus of adult and old rats by LC-ESI-ITMS method after microwave-assisted proteolysis vol.399, pp.6, 2011, https://doi.org/10.1007/s00216-010-4604-9
  2. Metabolic Fingerprint of Dimethyl Sulfone (DMSO2) in Microbial–Mammalian Co-metabolism vol.13, pp.12, 2014, https://doi.org/10.1021/pr500629t
  3. Dimethylsulfoxide reduction activity is linked to nutrient stress in Thalassiosira pseudonana NCMA 1335 vol.507, 2014, https://doi.org/10.3354/meps10842
  4. Protection of l-methionine against H2O2-induced oxidative damage in mitochondria vol.50, pp.8, 2012, https://doi.org/10.1016/j.fct.2012.04.047
  5. Analyses of methionine sulfoxide reductase activities towards free and peptidyl methionine sulfoxides vol.527, pp.1, 2012, https://doi.org/10.1016/j.abb.2012.07.009
  6. Intracellular repair of oxidation-damaged α-synuclein fails to target C-terminal modification sites vol.7, 2016, https://doi.org/10.1038/ncomms10251
  7. Resveratrol preconditioning increases methionine sulfoxide reductases A expression and enhances resistance of human neuroblastoma cells to neurotoxins vol.24, pp.6, 2013, https://doi.org/10.1016/j.jnutbio.2012.08.005
  8. Cepharanthine alleviates liver injury in a rodent model of limb ischemia–reperfusion vol.54, pp.1, 2016, https://doi.org/10.1016/j.aat.2015.11.004
  9. Probing the emitter site of Renilla luciferase using small organic molecules; an attempt to understand the molecular architecture of the emitter site vol.93, 2016, https://doi.org/10.1016/j.ijbiomac.2016.09.060
  10. The discovery of methionine sulfoxide reductase enzymes: An historical account and future perspectives vol.41, pp.3, 2015, https://doi.org/10.1002/biof.1214
  11. A study of enzymatic activity in cell cultures via the analysis of volatile biomarkers vol.137, pp.20, 2012, https://doi.org/10.1039/c2an35815h
  12. A specific and rapid colorimetric method to monitor the activity of methionine sulfoxide reductase A vol.53, pp.6-7, 2013, https://doi.org/10.1016/j.enzmictec.2013.08.005
  13. Characterization of dimethyl sulphoxide reductase from brewing yeast vol.123, pp.3, 2017, https://doi.org/10.1002/jib.435
  14. vol.8, pp.5, 2017, https://doi.org/10.1128/mBio.01169-17
  15. Methionine Sulfoxide Reductases of Archaea vol.7, pp.10, 2018, https://doi.org/10.3390/antiox7100124