Trans-sulfuration pathway seleno-amino acids are mediators of selenomethionine toxicity in Saccharomyces cerevisiae

Journal of Biological Chemistry

Volumn 290, Issue 17, 2015, Pages 10741-10750

  Lazard, Myriam ^a   Dauplais, Marc ^a   Blanquet, Sylvain ^a   Plateau, Pierre ^a  

^a LABORATOIRE DE BIOCHIMIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYME ACTIVITY; OXYGEN; SELENIUM; SELENIUM COMPOUNDS; TOXICITY; YEAST;

COMPLETE OXIDATION; EXTRACELLULAR CONCENTRATION; ORGANIC DERIVATIVES; S-ADENOSYLMETHIONINE; SULFUR AMINO ACIDS; SUPEROXIDE PRODUCTION; SUPEROXIDE RADICAL; SUPEROXIDE SCAVENGERS;

PLANTS (BOTANY);

SELENIUM; SELENOCYSTEINE; SELENOHOMOCYSTEINE; SELENOMETHIONINE; UNCLASSIFIED DRUG; METHIONINE; S ADENOSYLMETHIONINE; SELENIOUS ACID; SELENIUM DERIVATIVE; SELENOL; SELENOMETHYLSELENOCYSTEINE; SULFUR AMINO ACID;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ASSAY; ENZYME SYNTHESIS; FUNGAL STRAIN; FUNGUS CULTURE; FUNGUS GROWTH; GENE DELETION; GROWTH INHIBITION; HYDROLYSIS; IMMUNOBLOTTING; MOLECULAR WEIGHT; NONHUMAN; OXIDATION; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SULFATION; TRANSSULFURATION; ANALOGS AND DERIVATIVES; DIET SUPPLEMENTATION; DNA REPAIR; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MUTATION; OXIDATIVE STRESS; TOXICITY;

SACCHAROMYCES CEREVISIAE;

AMINO ACIDS, SULFUR; DIETARY SUPPLEMENTS; DNA REPAIR; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METHIONINE; MUTATION; OXIDATIVE STRESS; S-ADENOSYLMETHIONINE; SACCHAROMYCES CEREVISIAE; SELENIOUS ACID; SELENIUM COMPOUNDS; SELENOCYSTEINE; SELENOMETHIONINE;

EID: 84928388565     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.640375     Document Type: Article

References (61)

1. Papp, L. V., Holmgren, A., and Khanna, K. K. (2010) Selenium and selenoproteins in health and disease. Antioxid. Redox Signal. 12, 793-795
2. Brozmanová, J., Mániková, D., Vlcková, V., and Chovanec, M. (2010) Selenium: a double-edged sword for defense and offence in cancer. Arch. Toxicol. 84, 919-938
3. Wallenberg, M., Misra, S., and Björnstedt, M. (2014) Selenium cytotoxicity in cancer. Basic Clin. Pharmacol. Toxicol. 114, 377-386
4. Valdiglesias, V., Pásaro, E., Méndez, J., and Laffon, B. (2010) In vitro evaluation of selenium genotoxic, cytotoxic, and protective effects: a review. Arch. Toxicol. 84, 337-351
5. Weekley, C. M., and Harris, H. H. (2013) Which form is that?: The importance of selenium speciation and metabolism in the prevention and treatment of disease. Chem. Soc. Rev. 42, 8870-8894
6. Letavayová, L., Vlcková, V., and Brozmanová, J. (2006) Selenium: from cancer prevention to DNA damage. Toxicology 227, 1-14
7. Letavayová, L., Vlasáková, D., Spallholz, J. E., Brozmanová, J., and Chovanec, M. (2008) Toxicity and mutagenicity of selenium compounds in Saccharomyces cerevisiae. Mutat. Res. 638, 1-10
8. Seko, Y., and Imura, N. (1997) Active oxygen generation as a possible mechanism of selenium toxicity. Biomed. Environ. Sci. 10, 333-339
9. Spallholz, J. E. (1994) On the nature of selenium toxicity and carcinostatic activity. Free Radic. Biol. Med. 17, 45-64
10. Tarze, A., Dauplais, M., Grigoras, I., Lazard, M., Ha-Duong, N. T., Barbier, F., Blanquet, S., and Plateau, P. (2007) Extracellular production of hydrogen selenide accounts for thiol-assisted toxicity of selenite against Saccharomyces cerevisiae. J. Biol. Chem. 282, 8759-8767
11. Seko, Y., Saito, Y., Kitahara, J., and Imura, N. (1989) Active oxygen generation by the reaction of selenite with reduced glutathione in vitro. In Fourth International Symposium on Selenium in Biology and Medicine (Wendel, A., ed) pp. 70-73, Springer-Verlag, Heidelberg, Germany
12. Spallholz, J. E. (1997) Free radical generation by selenium compounds and their prooxidant toxicity. Biomed. Environ. Sci. 10, 260-270
13. Peyroche, G., Saveanu, C., Dauplais, M., Lazard, M., Beuneu, F., Decourty, L., Malabat, C., Jacquier, A., Blanquet, S., and Plateau, P. (2012) Sodium selenide toxicity is mediated by O2-dependent DNA breaks. PLoS One 7, e36343
14. Letavayová, L., Marková, E., Hermanská, K., Vlcková, V., Vlasáková, D., Chovanec, M., and Brozmanová, J. (2006) Relative contribution of homologous recombination and non-homologous end-joining to DNA doublestrand break repair after oxidative stress in Saccharomyces cerevisiae. DNA Repair 5, 602-610
15. Letavayová, L., Vlasáková, D., Vlcková, V., Brozmanová, J., and Chovanec, M. (2008) Rad52 has a role in the repair of sodium selenite-induced DNA damage in Saccharomyces cerevisiae. Mutat. Res. 652, 198-203
16. Pinson, B., Sagot, I., and Daignan-Fornier, B. (2000) Identification of genes affecting selenite toxicity and resistance in Saccharomyces cerevisiae. Mol. Microbiol. 36, 679-687
17. Seitomer, E., Balar, B., He, D., Copeland, P. R., and Kinzy, T. G. (2008) Analysis of Saccharomyces cerevisiae null allele strains identifies a larger role for DNA damage versus oxidative stress pathways in growth inhibition by selenium. Mol. Nutr. Food Res. 52, 1305-1315
18. Mániková, D., Vlasáková, D., Letavayová, L., Klobucniková, V., Griac, P., and Chovanec, M. (2012) Selenium toxicity toward yeast as assessed by microarray analysis and deletion mutant library screen: a role for DNA repair. Chem. Res. Toxicol. 25, 1598-1608
19. Izquierdo, A., Casas, C., and Herrero, E. (2010) Selenite-induced cell death in Saccharomyces cerevisiae: protective role of glutaredoxins. Microbiology 156, 2608-2620
20. Lazard, M., Ha-Duong, N. T., Mounié, S., Perrin, R., Plateau, P., and Blanquet, S. (2011) Selenodiglutathione uptake by the Saccharomyces cerevisiae vacuolar ATP-binding cassette transporter Ycf1p. FEBS J. 278, 4112-4121
21. Lewinska, A., and Bartosz, G. (2008) A role for yeast glutaredoxin genes in selenite-mediated oxidative stress. Fungal Genet. Biol. 45, 1182-1187
22. Malkowski, M. G., Quartley, E., Friedman, A. E., Babulski, J., Kon, Y., Wolfley, J., Said, M., Luft, J. R., Phizicky, E. M., DeTitta, G. T., and Grayhack, E. J. (2007) Blocking S-adenosylmethionine synthesis in yeast allows selenomethionine incorporation and multiwavelength anomalous dispersion phasing. Proc. Natl. Acad. Sci. U.S.A. 104, 6678-6683
23. Bockhorn, J., Balar, B., He, D., Seitomer, E., Copeland, P. R., and Kinzy, T. G. (2008) Genome-wide screen of Saccharomyces cerevisiae null allele strains identifies genes involved in selenomethionine resistance. Proc. Natl. Acad. Sci. U.S.A. 105, 17682-17687
24. Kitajima, T., Chiba, Y., and Jigami, Y. (2010) Mutation of high-affinity methionine permease contributes to selenomethionyl protein production in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 76, 6351-6359
25. Okuno, T., Kubota, T., Kuroda, T., Ueno, H., and Nakamuro, K. (2001) Contribution of enzymic alpha, gamma-elimination reaction in detoxification pathway of selenomethionine in mouse liver. Toxicol. Appl. Pharmacol. 176, 18-23
26. Palace, V. P., Spallholz, J. E., Holm, J., Wautier, K., Evans, R. E., and Baron, C. L. (2004) Metabolism of selenomethionine by rainbow trout (Oncorhynchus mykiss) embryos can generate oxidative stress. Ecotoxicol. Environ. Saf. 58, 17-21
27. Spallholz, J. E., Palace, V. P., and Reid, T. W. (2004) Methioninase and selenomethionine but not Se-methylselenocysteine generate methylselenol and superoxide in an in vitro chemiluminescent assay: implications for the nutritional carcinostatic activity of selenoamino acids. Biochem. Pharmacol. 67, 547-554
28. Misra, S., Peak, D., and Niyogi, S. (2010) Application of XANES spectroscopy in understanding the metabolism of selenium in isolated rainbow trout hepatocytes: insights into selenium toxicity. Metallomics 2, 710-717
29. Kajander, E. O., Harvima, R. J., Kauppinen, L., Akerman, K. K., Martikainen, H., Pajula, R. L., and Kärenlampi, S. O. (1990) Effects of selenomethionine on cell growth and on S-adenosylmethionine metabolism in cultured malignant cells. Biochem. J. 267, 767-774
30. Kitajima, T., Jigami, Y., and Chiba, Y. (2012) Cytotoxic mechanism of selenomethionine in yeast. J. Biol. Chem. 287, 10032-10038
31. Dardel, F. (1994) MC-Fit: using Monte-Carlo methods to get accurate confidence limits on enzyme parameters. Comput. Appl. Biosci. 10, 273-275
32. Zhou, Z. S., Smith, A. E., and Matthews, R. G. (2000) L-Selenohomocysteine: one-step synthesis from L-selenomethionine and kinetic analysis as substrate for methionine synthases. Bioorg. Med. Chem. Lett. 10, 2471-2475
33. Soda, K. (1967) A spectrophotometric microdetermination of keto acids with 3-methyl-2-benzothiazolone hydrazone. Agr. Biol. Chem. 31, 1054-1060
34. Dickson, R. C., and Tappel, A. L. (1969) Reduction of selenocystine by cysteine or glutathione. Arch. Biochem. Biophys. 130, 547-550
35. Gardner, P. R., Raineri, I., Epstein, L. B., and White, C. W. (1995) Superoxide radical and iron modulate aconitase activity in mammalian cells. J. Biol. Chem. 270, 13399-13405
36. Pirkov, I., Norbeck, J., Gustafsson, L., and Albers, E. (2008) A complete inventory of all enzymes in the eukaryotic methionine salvage pathway. FEBS J. 275, 4111-4120
37. Tehlivets, O., Malanovic, N., Visram, M., Pavkov-Keller, T., and Keller, W. (2013) S-Adenosyl-L-homocysteine hydrolase and methylation disorders: yeast as a model system. Biochim. Biophys. Acta 1832, 204-215
38. Kanai, M., Masuda, M., Takaoka, Y., Ikeda, H., Masaki, K., Fujii, T., and Iefuji, H. (2013) Adenosine kinase-deficient mutant of Saccharomyces cerevisiae accumulates S-adenosylmethionine because of an enhanced methionine biosynthesis pathway. Appl. Microbiol. Biotechnol. 97, 1183-1190
39. Singh, S., and Banerjee, R. (2011) PLP-dependent H2S biogenesis. Biochim. Biophys. Acta 1814, 1518-1527
40. Yamagata, S., D'Andrea, R. J., Fujisaki, S., Isaji, M., and Nakamura, K. (1993) Cloning and bacterial expression of the CYS3 gene encoding cystathionine γ-lyase of Saccharomyces cerevisiae and the physicochemical and enzymatic properties of the protein. J. Bacteriol. 175, 4800-4808
41. Huber, R. E., and Criddle, R. S. (1967) Comparison of the chemical properties of selenocysteine and selenocystine with their sulfur analogs. Arch. Biochem. Biophys. 122, 164-173
42. Hiraishi, H., Miyake, T., and Ono, B. (2008) Transcriptional regulation of Saccharomyces cerevisiae CYS3 encoding cystathionine γ-lyase. Curr. Genet. 53, 225-234
43. Saez, G., Thornalley, P. J., Hill, H. A., Hems, R., and Bannister, J. V. (1982) The production of free radicals during the autoxidation of cysteine and their effect on isolated rat hepatocytes. Biochim. Biophys. Acta 719, 24-31
44. Misra, H. P. (1974) Generation of superoxide free radical during the autoxidation of thiols. J. Biol. Chem. 249, 2151-2155
45. Chaudiere, J., Courtin, O., and Leclaire, J. (1992) Glutathione oxidase activity of selenocystamine: a mechanistic study. Arch. Biochem. Biophys. 296, 328-336
46. Wallace, M. A., Bailey, S., Fukuto, J. M., Valentine, J. S., and Gralla, E. B. (2005) Induction of phenotypes resembling CuZn-superoxide dismutase deletion in wild-type yeast cells: an in vivo assay for the role of superoxide in the toxicity of redox-cycling compounds. Chem. Res. Toxicol. 18, 1279-1286
47. Sanchez, R. J., Srinivasan, C., Munroe, W. H., Wallace, M. A., Martins, J., Kao, T. Y., Le, K., Gralla, E. B., and Valentine, J. S. (2005) Exogenous manganous ion at millimolar levels rescues all known dioxygen-sensitive phenotypes of yeast lacking CuZnSOD. J. Biol. Inorg. Chem. 10, 913-923
48. Iwig, D. F., and Booker, S. J. (2004) Insight into the polar reactivity of the onium chalcogen analogues of S-adenosyl-L-methionine. Biochemistry 43, 13496-13509
49. Singh, S., Padovani, D., Leslie, R. A., Chiku, T., and Banerjee, R. (2009) Relative contributions of cystathionine β-synthase and γ-cystathionase to H2S biogenesis via alternative trans-sulfuration reactions. J. Biol. Chem. 284, 22457-22466
50. Chiku, T., Padovani, D., Zhu, W., Singh, S., Vitvitsky, V., and Banerjee, R. (2009) H2S biogenesis by human cystathionine γ-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J. Biol. Chem. 284, 11601-11612
51. Arnaudguilhem, C., Bierla, K., Ouerdane, L., Preud'homme, H., Yiannikouris, A., and Lobinski, R. (2012) Selenium metabolomics in yeast using complementary reversed-phase/hydrophilic ion interaction (HILIC) liquid chromatography-electrospray hybrid quadrupole trap/Orbitrap mass spectrometry. Anal. Chim. Acta 757, 26-38
52. Rahmanto, A. S., and Davies, M. J. (2012) Selenium-containing amino acids as direct and indirect antioxidants. IUBMB Life 64, 863-871
53. Larabee, J. L., Hocker, J. R., and Hanas, J. S. (2009) Mechanisms of inhibition of zinc-finger transcription factors by selenium compounds ebselen and selenite. J. Inorg. Biochem. 103, 419-426
54. Park, H. S., Park, E., Kim, M. S., Ahn, K., Kim, I. Y., and Choi, E. J. (2000) Selenite inhibits the c-Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) through a thiol redox mechanism. J. Biol. Chem. 275, 2527-2531
55. Gopalakrishna, R., and Gundimeda, U. (2001) Protein kinase C as a molecular target for cancer prevention by selenocompounds. Nutr. Cancer 40, 55-63
56. Kade, I. J., Paixão, M. W., Rodrigues, O. E., Barbosa, N. B., Braga, A. L., Avila, D. S., Nogueira, C. W., and Rocha, J. B. (2008) Comparative studies on dicholesteroyl diselenide and diphenyl diselenide as antioxidant agents and their effect on the activities of Na+/K+ ATPase and δ-aminolevulinic acid dehydratase in the rat brain. Neurochem. Res. 33, 167-178
57. Chan, G., Hardej, D., Santoro, M., Lau-Cam, C., and Billack, B. (2007) Evaluation of the antimicrobial activity of ebselen: role of the yeast plasma membrane H+-ATPase. J. Biochem. Mol. Toxicol. 21, 252-264
58. Azad, G. K., Singh, V., Mandal, P., Singh, P., Golla, U., Baranwal, S., Chauhan, S., and Tomar, R. S. (2014) Ebselen induces reactive oxygen species (ROS)-mediated cytotoxicity in Saccharomyces cerevisiae with inhibition of glutamate dehydrogenase being a target. FEBS Open Bio. 4, 77-89
59. Bierla, K., Bianga, J., Ouerdane, L., Szpunar, J., Yiannikouris, A., and Lobinski, R. (2013) A comparative study of the Se/S substitution in methionine and cysteine in Se-enriched yeast using an inductively coupled plasma mass spectrometry (ICP MS)-assisted proteomics approach. J. Proteomics 87, 26-39
60. Van Hoewyk, D. (2013) A tale of two toxicities: malformed selenoproteins and oxidative stress both contribute to selenium stress in plants. Ann. Bot. 112, 965-972
61. Thomas, D., and Surdin-Kerjan, Y. (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 61, 503-532